Nederlands tijdschrift voor Kinder

Nederlands tijdschrift voor

Kinderfysiotherapie december 2010 jaargang 22

Special

25 JAARK N V F Het vak kindergeneeskunde Scientific progress in pediatric physical therapy Changing theories, changing practices, changing challenges

Nieuws Colofon

Inhoud

Nederlands Tijdschrift voor Kinderfysiotherapie Een uitgave van de NVFK, de Nederlandse Vereniging voor Fysiotherapie in de Kinderen Jeugdgezondheidszorg Verschijnt medio maart, juni, september en december 20e jaargang, oplage 1320 ex.

3 Editorial

Redactie Ines Dragt Annette van der Putten Eugène Rameckers Marian Schouwaert-Schiesser Winy Verdegaal (eindredactie) Alke Wijn Redactiemedewerkers Dirk-Wouter Smits Olaf Verschuren Ron van Empelen Redactieadres e-mail: [email protected] Bestuur NVFK [email protected] www. NVFK.nl of www. Kinderfysiotherapie.nl Ledensecretariaat NVFK Bureau KNGF Afd. ledenservice Tel 033-4672929 e-mail: [email protected] Prijs los abonnement E 60,-. Opgave via ledensecretariaat Advertenties Vraag- en aanbod advertenties van leden gratis. Opgave bij redactieadres o.v.v. lidmaatschapsnummer Commerciële advertenties: Tarieven schriftelijk op te vragen bij redactieadres of op www.NVFK.nl. Het overnemen van artikelen is uitsluitend in overleg met de redactie toegestaan. De NVFK stelt zich niet verantwoordelijk voor de tekst en inhoud van de artikelen en de advertenties in dit blad.

Druk Zodiak, Groningen Ontwerp Tom Venema, Winsum De NVFK is een erkende specialistenvereniging van het Koninklijk Nederlands Genootschap voor Fysiotherapie

Afbeelding achterzijde: ‘Klapps kruipen’. Met dank aan: Stichting Geschiedenis Fysiotherapie.

4 Het vak kindergeneeskunde

J.F. Swart en J.J. Roord

8 Ontwikkelingen in de ontwikkelingsneurologie: de betekenis van variatie en variabiliteit

M. Hadders-Algra

16 Recent and past developments in neonatal neurology

L.S. de Vries

24 Developmental psychology, pediatric psychology and pediatric physical therapy:

Joining forces in supporting children to develop ‘mens sana in corpore sano’ M.J. Jongmans

29 Scientific progress in pediatric physical therapy: 1985-2010

S.R. Harris

36 Changing theories, changing practices, changing challenges

J. Darrah

41 Developmental pediatrics: perspectives on 25 years of development and scientific progress

P. Rosenbaum and A. Harvey

Editorial 25 jaar Nederlandse Vereniging voor Kinderfysiotherapie Dit jaar bestaat de Nederlandse Vereniging voor Kinderfysiotherapie (NVFK) 25 jaar. Terugkijkend kan met trots en tevredenheid worden gesteld dat zowel de NVFK als vereniging en de kinderfysiotherapie als vakgebied het in die afgelopen 25 jaar voorbeeldig hebben gedaan. Er is uit de verschillende werkgroepen een krachtige vereniging ontstaan met een duidelijke visie, terwijl het vakgebied zelf zich wetenschappelijk onmiskenbaar heeft gemanifesteerd. Geen enkele andere specialistische vereniging van het Koninklijk Nederlands Genootschap voor Fysiotherapie (KNGF) heeft zo veel van zijn leden zien promoveren, terwijl het opleidingscurriculum Kinderfysiotherapie als voorbeeld kan dienen voor de ontwikkeling en groei naar een beroepsopleiding op masterniveau. De gezondheidszorg voor het kind is complex en daarom multidisciplinair. Kinderfysiotherapeuten werken met vele andere specialisten samen, terwijl kennis

en bevindingen uit het wetenschappelijk onderzoek van aanpalende vakgebieden niet zelden consequenties hebben voor hun diagnostisch en/of therapeutisch redeneren en handelen. De redactie heeft daarom aan een aantal internationaal bekende hoogleraren uit de kindergeneeskunde, ontwikkelingsneurologie, neonatologie en neonatale neurologie, kinderen jeugdpsychologie, developmental pediatrics/kinderrevalidatie en uit de kinderfysiotherapie zelf, gevraagd hun visie te geven op de ontwikkelingen in hun eigen vakgebied in de afgelopen 25 jaar. Aan hen is ook gevraagd welke ontwikkelingen in hun optiek van belang zijn of zijn geweest voor de kinderfysiotherapie. Deze speciale uitgave van ons tijdschrift is daarmee een gedenkwaardige bundeling geworden van 25 jaar ontwikkeling van de gezondheidszorg voor het kind. Prof. dr. Paul Helders, gastredacteur Dr. Eugène Rameckers, hoofdredacteur

Het vak kindergeneeskunde J.F. Swart en J.J. Roord

J.F. Swart VU Universitair medisch centrum, afdeling Kindergeneeskunde; Reade, Centrum voor revalidatie en reumatologie, Amsterdam

Van observatie naar ziektepreventie De kindergeneeskunde is een relatief jong vakgebied dat gestalte begon te krijgen in de zeventiende eeuw. Het was de Engelse dokter Thomas Sydenham (1624-1689) die door jarenlange nauwkeurige observatie en casusvergelijkingen de kinderziekten roodvonk, mazelen, pokken, epilepsie, rachitis (ook wel Engelse ziekte genaamd), scheurbuik en chorea van Sydenham beschreef.1 In de daaropvolgende eeuw vond een zeer belangwekkend en overtuigend experiment plaats door dokter Edward Jenner (1749-1823). Hij entte 23 personen in met koeienpokken en bewees vervolgens dat deze lieden immuun waren tegen de veel ernstiger gewone pokken. Verder bewees hij dat deze inenting van persoon tot persoon werkte en niet slechts via het vee.2 Aangezien het epidemische pokkenvirus leidde tot sterfte bij 1 op de 3 besmette personen en vaak forse vervormingen gaf bij de overlevenden was dit een enorme doorbraak die er na succesvolle mondiale pokkenvaccinaties toe heeft geleid dat de wereld nu geheel pokkenvrij is. Er ontstond gaandeweg meer aandacht voor de zorg, ontwikkeling en ziekten van kinderen die tot op dat moment vaak waren ondergebracht bij moeders en vroedvrouwen. Het eerste ziekenhuis (‘The Hospital for Sick Children’) dat exclusief gewijd was aan de behandeling van kinderen werd in 1852 opgericht in Londen. In Nederland werd het eerste kinderziekenhuis in 1863 in Rotterdam geopend op de bovenetage van een pand in een drukke winkelstraat in het stadshart van Rotterdam. Twee jaar later volgde Amsterdam en vervolgens Arnhem, Den Haag, Utrecht, Dordrecht en Groningen. De artsen die daar werkten, hadden bijzondere interesse in de kindergeneeskunde, maar er bestond nog geen opleiding tot kinderarts. Tussen 1863 en 1891 werden in totaal zeven kinderziekenhuizen gesticht waar kinderen ‘curatieve zorg op maat’ kregen van algemene artsen en internisten die zich speciaal op de zorg voor zieke kinderen toelegden.3 In 1892, slechts 9 jaar na de vorming van ’s werelds eerste nationale kinderartsenorganisatie in Duitsland (1883) en 38 jaar voorafgaand aan de Amerikaanse tegenhanger (‘The American Academy of Pediatrics’ in 1930), werd de Nederlandsche Vereeniging voor Paediatrie opgericht, met 23 kinderartsen. Ten tijde van de oprichting van de vereniging was er in de maatschappij sprake van zeer slechte woon- en leefomstandigheden. Als gevolg van armoede en onkunde leden talloze kinderen onder slechte hygiëne, verwaarlozing en honger. Vitaminetekort (met name vitamine C en D), voedingsstoornissen, maag-darmziekten met uitdroging, chronische ondervoeding en infectieziekten als tetanus, difterie, roodvonk, kinderverlamming, kinkhoest, syfilis, tuberculose, pokken en cholera waren verantwoordelijk voor de hoge kindersterfte.4 Niet minder dan 17% van de kinderen overleed in het eerste levensjaar en vanwege de lage levensverwachting bestond de bevolking voor 44% uit 0-19-jarigen.5 De inspanningen van de kinderartsen in die jaren richtten zich dan ook met name op verbetering van de voedingstoestand en de verzorging van zuigelingen en peuters. De kinderziekenhuizen waren toen nog vrijwel volledig afhankelijk van liefdadigheid. Medicijnen waren er nauwelijks en dus werd de nadruk vooral gelegd op goede voorlichting over hygiëne en voeding. Rond dezelfde tijd, in

4 • Nederlands Tijdschrift voor Kinderfysiotherapie • Special • december 2010

Prof. dr. J.J. Roord VU Universitair medisch centrum, afdeling Kindergeneeskunde, Amsterdam Correspondentie E-mail: [email protected]

1880, begon Aletta Jacobs in Amsterdam, boven een kroeg in de Spuistraat te Amsterdam, met een avondcursus voor vrouwen en meisjes over algemene hygiëne en verzorging van zuigelingen en richtte zich daarmee op preventie van ziekte.6 In 1901 opende kinderarts Plantenga als eerste in Nederland een consultatiebureau voor zuigelingen om de gezondheid van (sociaal) zwakkere kinderen te verbeteren, wat snel navolging vond in andere steden.6

De eerste (buitengewoon) hoogleraar kindergeneeskunde in Nederland In 1909 werd in Groningen dokter Scheltema, die zich na een assistentschap interne geneeskunde in het buitenland had gespecialiseerd in de kindergeneeskunde, benoemd tot eerste (buitengewoon) hoogleraar kindergeneeskunde in Nederland.7 Mede dankzij hem werd het vak kindergeneeskunde toegevoegd aan het medisch curriculum in Nederland. Door de ontwikkeling van de medische wetenschap, verbetering van socio-economische omstandigheden en hygiëne door de aanleg van riolering en waterleiding, alsmede door de invoering van de arbeids- en kinderwetten kon de voorzitter van de Nederlandsche Vereeniging voor Paediatrie (later NVK) in 1917 met enige trots melden dat de zuigelingensterfte tot 9% was gedaald.5 Zowel professor Scheltema in Groningen als professor Gorter in Leiden zagen een grote rol weggelegd voor de preventieve geneeskunde in Nederland. In 1929 riep laatstgenoemde een stichting in het leven, het Instituut voor Praeventieve Geneeskunde (later NIPG).8 De levensvoorwaarden verbeterden verder en in 1935 stierf ‘nog maar’ 4% van de kinderen in het eerste levensjaar.5 In die periode werd de kindergeneeskunde een vak van klinisch werkzame specialisten, waarbij de extramuraal werkende kinderartsen nog slechts als provinciaal of districtsarts voor de consultatiebureaus optraden.9 Door de vorming van een landelijk netwerk van consultatiebureaus, het propageren van borstvoeding en het gebruik van schoon water bij de bereiding van flesvoeding kwamen talrijke ‘oude’ ziektebeelden minder vaak voor,10 maar difterie, kinkhoest, tetanus, polio, roodvonk en mazelen speelden nog steeds een hoofdrol: de complicaties waren ernstig en de sterfte was nog hoog.11 In 1942 telde Nederland ongeveer 150 kinderartsen. Zij werkten als huisarts voor kinderen met een praktijk aan huis en daarnaast een deelaanstelling in een algemeen ziekenhuis. De kennis over de pathofysiologie van allerlei ziekten en aandoeningen nam wel exponentieel toe, maar door het ontbreken van adequate therapie, met name bij deze infectieziekten, bleef de kindersterfte hoog tot na de Tweede Wereldoorlog.

De scheiding tussen preventieve en curatieve zorg De medische wetenschap maakt in de naoorlogse jaren een enorme ontwikkeling door. De kinderarts gaat meer en meer op zoek naar specifieke oorzaken en steeds meer aandoeningen kunnen worden behandeld. De ontwikkeling op het gebied van nieuwe behandelmethoden had vooral te maken met het beschikbaar komen van nieuwe medicijnen. Vrijwel alle 200 ziekenhuizen in Nederland hadden begin jaren 50 een kinderafdeling. De gemiddelde opnameduur was toen nog ruim 21 dagen. In 1951 werd door een commissie (Geneeskundig Hoofdinspectie, Rijksinstituut voor Volksgezondheid en kinderartsen) een gedragslijn voor de huisarts gepubliceerd om kinderen middels vaccinatie te beschermen tegen pokken, difterie, kinkhoest, tetanus, tuberculose en roodvonk.12 In 1953 werd het Rijksvaccinatieprogramma als nieuwe taak toegevoegd aan de taken van het consultatiebureau.13 De sterfte in het eerste levensjaar bedroeg, mede vanwege de vaccinaties en het gebruik van antibiotica, in de jaren 50 nog ‘slechts’ 1,7%.5 De ruim 200 kinderartsen besloten zich te beperken tot de uitoefening van de kindergeneeskunde in het ziekenhuis, mede in het kader van de erkenning van medische specialismen.14 De opleiding kindergeneeskunde bevond zich in de academische ziekenhuizen en de opleiding jeugdgezondheidszorg in het Nederlands Instituut voor Pediatrische Geneeskunde (NIPG) (sinds 1962 ook als erkende tak van de sociale geneeskunde). Hiermee was de scheiding tussen preventie en curatie een feit. De preventieve gezondheidszorg voor kinderen wordt in Nederland nog altijd geleverd door de jeugdgezondheidszorg, de curatieve zorg in de eerste lijn door huisartsen (extramuraal) en in de tweede lijn door (intramuraal werkende) kinderartsen en andere specialisten.8 In tegenstelling tot in de meeste andere Europese landen, waar de kinderarts ook werkzaam is in de preventie en eerstelijnszorg voor het kind. Door de toenemende kennis ontwikkelt zich in de jaren vijftig binnen de kindergeneeskunde de kindercardiologie als eerste subspecialisme.

Subspecialisaties binnen de kindergeneeskunde In de daaropvolgende decennia kwam meer aandacht voor het vakgebied tijdens de medische studie en sinds de jaren 70 is de kindergeneeskunde in alle faculteiten een doctoraalexamenvak.15 Er volgde een verschuiving van werkplek, waarbij in 1960 slechts 22% van de 300 kinderartsen werkzaam was binnen een academisch ziekenhuis, terwijl anno 2010 48% van de 1200 kinderartsen werkt in een universitair medisch centrum.15 Ook ontstonden er vanaf die tijd meer subspecialismen, die waren gericht op afzonderlijke organen, orgaansystemen of leeftijdscategorieën, zowel binnen de kindergeneeskunde (bijvoorbeeld kindernefrologie, kinderendocrinologie, neonatologie) als binnen andere specialismen (bijvoorbeeld kinderchirurgie, kinderneurologie en kinderorthopedie).8 Momenteel zijn er 15 door de NVK erkende subspecialismen, is bijna 50% van de kinderartsen geregistreerd als subspecialist en werkt driekwart van hen vrijwel geheel binnen hun deelgebied in een academisch centrum.15 In algemene ziekenhuizen heeft een deel van de kinderartsen een aandachtsgebied, dat in deeltijd wordt beoefend naast de algemene kindergeneeskunde. De kwaliteit van de zorg kan verbeteren wanneer er meer tijd is voor een deelspecialisme, zoals dit mogelijk is bij een grotere praktijkomvang. Door de subspecialisering bezitten kinderartsen nu vrijwel alle voor het kind specifieke kennis en behandelmogelijkheden, zodat vrijwel geen gebruik meer hoeft

te worden gemaakt van die van specialisten voor volwassenen. Deze verregaande specialisatie heeft een verviervoudiging van het aantal kinderartsen tot gevolg gehad, ondanks dat het aantal 0-20-jarigen circa 10% is gedaald ten opzichte van de jaren 60 en 70.15 Wel dient hierbij te worden vermeld dat het aantal fulltime werkende kinderartsen het afgelopen decennium flink is gedaald. Deels wordt dit verklaard door de toenemende feminisering van de kindergeneeskunde, waarin nu 75% van de assistenten in opleiding tot kinderarts vrouw is.15 Anderzijds is de balans tussen werk en de tijd die men overhoudt voor gezin en/of het sociale leven voor veel basisartsen zo belangrijk geworden dat controleerbare leefstijl en aantal werkuren medebepalende factoren zijn voor het kiezen van de medische vervolgopleiding.16

Van overleven naar kwaliteit van leven Er heeft een belangrijke ontwikkeling plaatsgevonden op het gebied van de intensieve zorg voor kinderen en pasgeborenen. Kinderen bij wie de vitale functies bedreigd zijn door trauma of ziekte kunnen terecht op 1 van de 8 academische pediatrische intensive care units (PICU’s). Pasgeborenen van wie de vitale functies bedreigd zijn, kunnen terecht op 1 van de 10 neonatologische intensive care units (NICU’s). Ongeveer de helft van hen betreft kinderen geboren na een zwangerschapsduur korter dan 30 weken.15 Ethische kwesties dringen zich regelmatig op, zoals: ‘wat is de grens van de levensvatbare leeftijd waarop verwijzing naar een NICU zinvol is’ en ‘hoe om te gaan met uitzichtloos en ondraaglijk lijden bij een pasgeborene of ouder kind’. Als gevolg van de verbeterde behandelingen en het hogere kennisniveau binnen de gehele kindergeneeskunde is het accent in de zorg verschoven van overleven naar kwaliteit van leven.17 In de jaren 70 was de kans op overleven nadat de diagnose kanker was gesteld ongeveer 5%, terwijl momenteel ruim 70% van de kinderen met kanker overleeft. In 1970 bereikte minder 30% van de kinderen met spina bifida de volwassenheid, terwijl dit momenteel meer dan 80% is.17 Het aantal kinderen met een chronische ziekte is door de enorme medisch-technische vooruitgang sterk toegenomen. In Nederland hebben momenteel een half miljoen kinderen een chronische aandoening.18 Van alle adolescenten heeft 14% een chronische aandoening; bij 1 op de 6 van deze groep wordt het levenspatroon aanzienlijk beperkt door hun aandoening.19,20 Bij vele kinderen met chronische somatische aandoeningen doen zich eveneens opvoedingsproblemen voor.21 De jeugdzorg, het derde zorgsysteem voor kinderen, geeft ondersteuning bij opvoedingsvraagstukken van geestelijke, sociale of pedagogische aard die de ontwikkeling naar volwassenheid belemmeren. Ondanks het bestaan van multidisciplinaire teams in (academische) ziekenhuizen hebben veel gezinnen behoefte aan intensievere psychosociale begeleiding dichtbij huis.22 Hiervoor is een nauwe samenwerking vereist tussen de kindergeneeskunde, jeugdgezondheidszorg en jeugdzorg. Van de kinderen met een chronische aandoening bereikt momenteel 90% de volwassen leeftijd, waar dit in de jaren 60 nog 30% was.23 Deze ontwikkeling stelt niet alleen nieuwe eisen aan de kindergeneeskunde, maar ook aan de volwassenengeneeskunde. Het doel ‘transitie’ is tweevoudig: a) voorbereiden van de patiënt op de overdracht naar de volwassenengeneeskunde door het verwerven van inzicht in het ziektebeeld en in het doel en de mogelijkheden van de behandeling, en het verwerven van eigen verantwoordelijkheid voor medicijnen en dieet en b) het op elkaar afstemmen van zorg die wordt verleend door de kindergeneeskunde en de zorg die wordt geboden door de voor volwassenengeneeskunde.24

Nederlands Tijdschrift voor Kinderfysiotherapie • Special • december 2010 • 5

Van zwaaien achter het glas naar ‘rooming-in’ Door de vele ziekenhuisfusies in de afgelopen jaren vindt de kindergeneeskundige intramurale zorg momenteel plaats in nog slechts circa 100 ziekenhuizen. Deze ziekenhuizen bestaan uit circa 60 kleinere ziekenhuizen, circa 30 grote topklinische ziekenhuizen (veelal door fusies uitgegroeid) en 8 academische kinderafdelingen.15 De inrichting van de ziekenhuizen is ook veranderd. Infectieziekten waren vroeger geregeld de reden voor opname, zodat kinderen vaak alleen op een kamertje werden verzorgd. Hierdoor kregen de kinderen dagen en soms wekenlang geen troostende hand, omarming of zoen van hun ouders en familie tijdens hun ziekte. Zwaaiend aan de andere kant van het glas was vaak de meest nabije vorm van contact. Tegenwoordig heeft een ziekenhuisopname vaak een andere reden en is slechts in zeldzame gevallen geïsoleerde verpleging noodzakelijk. In de meeste ziekenhuizen bestaat er tegenwoordig dan ook de mogelijkheid om een van de ouders samen met het zieke kind op te nemen, waardoor de opname voor kind en ouders minder traumatisch is.

Geneesmiddel en onderzoek bij kinderen Weliswaar is de zorg rond het kind de afgelopen decennia sterk verbeterd en zijn er vele geneesmiddelen beschikbaar die we in de kindergeneeskunde gebruiken, op een NICU was 48% van de voorgeschreven medicatie niet geregistreerd (‘unlicensed’) en in 18% van de gevallen waren er geen doseringsvoorschriften (‘off-label’-gebruik).25 Poliklinische medicatie die aan kinderen werd gegeven was ook in 16% van de gevallen ongeregistreerd, in 21% van de gevallen was het niet bekend of de medicatie bij kinderen gebruikt kon worden en in nog eens 20% van de gevallen bestonden er geen leeftijdsgerelateerde doseringsvoorschriften.26 In navolging van de Verenigde Staten is sinds 1 juli 2007 in de Europese Unie de Paediatric Regulation van kracht. Daarmee zijn de regels voor het registreren van medicatie veranderd, zodat nieuwe geneesmiddelen veilig bij kinderen kunnen worden toegepast en bewaakt. Onderzoek naar effectiviteit en veiligheid van medicatie bij kinderen wordt gestimuleerd met subsidies en alleenverkooprecht voor fabrikanten. Ook voor bestaande middelen geldt dat als een firma onderzoek doet naar een leeftijdsadequate doseervorm voor kinderen er een 10 jaar durende bescherming voor het voeren van het product gegeven wordt. Door de beperkingen van de in 1999 in werking getreden Wet medisch-wetenschappelijk onderzoek met mensen (WMO) is het in Nederland meermalen onmogelijk gebleken om nieuwe middelen te testen bij zieke kinderen.27 De WMO stelt in het geval van niet-therapeutisch onderzoek bij wilsonbekwamen (waaronder kinderen) een ‘nee, tenzij’, met als beperkingen verwaarloosbaar risico, minimale belasting en groepsgebondenheid (oftewel: alleen deze groep of categorie proefpersonen kan de benodigde gegevens leveren). De term verwaarloosbaar in dit verband is uniek in de wereld. Ook voor geneesmiddelenonderzoek bij kinderen geldt volgens de WMO dat de risico’s verwaarloosbaar en de bezwaren minimaal moeten zijn, indien het onderzoek het deelnemende kind zelf niet ten goede kan komen.27 De Europese regelgeving (Clinical Trials Directive 2001) daarentegen staat het geneesmiddelenonderzoek bij kinderen toe als het onderzoek enig direct voordeel heeft voor de groep patiënten waartoe de proefpersoon behoort. Andere voorwaarden zijn dat het onderzoek groepsgebonden is en dat pijn, ongemak en risico tot een minimum beperkt worden. Een advies van de Commissie Doek om de regels van de WMO iets te verruimen, is recent gesteund


door de Raad voor Gezondheidsonderzoek (RGO).28 Ondanks de strenge nationale regels voor onderzoek bij kinderen is er de laatste twee decennia door een aantal subspecialistische groepen een substantiële bijdrage geleverd aan het (inter)nationaal kindergeneeskundig onderzoek. De kwaliteit en kwantiteit van dit onderzoek is aanzienlijk versterkt. Tegelijkertijd is dit toponderzoek veelal afkomstig uit een beperkt aantal academische centra met grote verschillen in wetenschappelijke output van de diverse academische subspecialismen.29 Patiëntgebonden onderzoek, zoals geneesmiddelenonderzoek en onderzoek op het gebied van diagnostiek en preventie is het domein van artsen en andere zorgverleners. Ziektegebonden (oftewel translationeel) onderzoek waarbij de kennis de zorg op een te overziene termijn kan verbeteren, vereist interactie met de preklinische basisvakken van het medisch curriculum. Basaal onderzoek daarentegen is ondertussen vrijwel exclusief het terrein waarop fundamentele onderzoekers zich bewegen.29 Het recent geïnitieerde Medicines for Children Research Network (MCRN) heeft als doel onderzoekers te helpen bij het opzetten van multicenter geneesmiddelenonderzoek bij kinderen en onderzoekers te ondersteunen in de processen van regelgeving. De verwachting is dat geneesmiddelenonderzoek bij kinderen in de nabije toekomst een hoge vlucht zal nemen.

De nieuwste ontwikkelingen en de toekomstvisie Door vakinhoudelijke, beleidsmatige, organisatorische en financiële ontwikkelingen in Nederland wordt een duidelijke toekomstvisie van de organisatie van de kindergeneeskunde gevraagd.15 Wat betreft de toekomst van de kindergeneeskundige zorg lijkt concentratie van zorg ook binnen de algemene ziekenhuizen binnen niet al te lange tijd onafwendbaar. Als voorbeeld geldt de discussie rond de relatief hoge perinatale sterfte in Nederland. Volgens het recent verschenen rapport ‘Een goed begin, veilige zorg rond zwangerschap en geboorte’ dienen de perinatale hulpverleners binnen 15 minuten aanwezig te zijn en behandeling aan te vangen. Het zal ertoe leiden dat in ziekenhuizen waar tweede- en derdelijnsbevallingen plaatsvinden permanente aanwezigheid van de perinatale hulpverleners wordt vereist. De verloskundige praktijkvoering zal dan geconcentreerd worden in een aantal ziekenhuizen. Dit zal waarschijnlijk betekenen dat in een aantal ziekenhuizen kindergeneeskundige verpleegafdelingen zullen verdwijnen. Overdag wordt dan de zorg geleverd in poliklinieken; tijdens de avond- en nachtelijke uren zullen ouders met hun kind naar het regionale ziekenhuis moeten komen. Een vrij recente ontwikkeling is het ontstaan van extramurale zelfstandige behandelcentra (ZBC) of expertisecentra. Er zijn ZBC’s die een binding houden met een ziekenhuis, als ook ZBC’s die zich volledig onafhankelijk profileren.29 Voorbeelden van de eerste categorie zijn twee kinderastmacentra, Kinderhaven in Rotterdam en RAAcK in Nijmegen, en het kinderdiabetescentrum in Nijmegen. Voorbeelden van de tweede categorie zijn Diabeter, een ZBC voor kinderen met diabetes mellitus en AllesKits, een ZBC voor kinderen met ADHD en aanverwante leer- en gedragsstoornissen, beide in Rotterdam. Indien de beroepsgroep verantwoordelijkheid blijft dragen voor het borgen van de kwaliteit van 24-uurs integraal kindergeneeskundige zorg en ervoor zorgt dat de ZBC aan alle NVK-eisen voldoet, wordt dit ondernemerschap door de NVK ondersteund.29 De nieuwste ontwikkeling op het gebied van extramurale kindergeneeskundige zorg is de opening van de eerste allochtonenkliniek in Nederland te Amsterdam. In deze kliniek (VATAN Kliniek) zijn zieke kinderen en hun ouders welkom voor een second opinion bij een Nederlands-Turkse kinderarts.

In de academische klinieken ligt het zwaartepunt bij de subspecialistische zorg met op sommige gebieden topklinische zorg (vergunning Wet op bijzondere medische verrichtingen) en topreferente zorg (zeer specialistische zorg met bijzondere diagnostiek en behandeling waarbij gespecialiseerde en kostbare infrastructuur nodig zijn). Deze laatste vorm van zorg is ook gekoppeld aan fundamenteel en patiëntgericht onderzoek. Het betrekkelijk kleine aantal kinderen met aandoeningen waarvoor zeer gespecialiseerde, dure diagnostiek en behandeling is vereist, leidt tot concentratie van die zorg in een beperkt aantal academische centra. Recent werden door het Ministerie van Volksgezondheid Welzijn en Sport 4 kindercardiologische interventiecentra aangewezen. De Nederlands Federatie van Universitaire Medische Centra (NFU) lanceerde een plan om te komen tot concentratie van expertisecentra, dat zijn bestaansrecht vindt in de zeldzaamheid van de ziekte en de ervaring ermee binnen dat centrum, danwel doordat in dat centrum topreferente zorg geleverd kan worden op basis van internationaal erkende topkwaliteit, mede gebaseerd op wetenschappelijk onderzoek. In aansluiting op deze expertisecentra kunnen er dan ondersteunende shared care centra worden gevormd, waarbij de coördinatie van de zorg bij het expertisecentrum ligt. Iedere academische kinderkliniek dient volgens dit plan te beschikken over een rompstructuur met een afdeling Algemene pediatrie, een NICU, een PICU en een aantal vastgestelde vormen van subspecialistische zorg. De discussie over de concentratie van kindergeneeskundige zorg zal ongetwijfeld navolging krijgen binnen andere disciplines. Referenties 1 Luecke PE jr. The history of pediatrics at Baylor University Medical Center. BUMC Proceedings. 2004;17:56-60.

2 Levinson A. Pioneers of Pediatrics. New York: Froben Press; 1927. 3 Dooren LJ. Voordracht ter gelegenheid van de viering van het Eeuwfeest van de Nederlandse Vereniging voor Kindergeneeskunde in de Domkerk te Utrecht op 12 juni 1992. Tijdschr Kindergen. 1992;60:86- 90. 4 Hoogendoorn D. De zuigelingensterfte in Nederland. Assen: Van Gorcum; 1959. 5 Centraal Bureau voor de Statistiek. Historie bevolking, huishoudens en bevolkingsontwikkeling. 2009. http://statline.cbs.nl/statweb/. 6 Knapper N. Een kwart eeuw zuigelingenzorg in Nederland. Uitgegeven ter gelegenheid van het zilveren jubileum van den Nederlandschen Bond tot bescherming van zuigelingen en kleuters en ter bevordering der praenatale zorg. Amsterdam: Scheltema & Holkema; 1935. 7 Henssen EWA. Langs zelf gekozen paden: het leven van H.J. Scheltema, N.E.M. Pareau en mr. J. Jer. van Nes. Amsterdam: Querido; 1992. 8 Verloove-VanHorick SP. Preventieve en curatieve gezondheidszorg voor kinderen: een wisselwerking. Ned Tijdschr Geneesk. 1995;139(13):677-81. 9 De Pree-Geerlings B, De Pree IMN, Bulk-Bunschoten AMW. 1901-2001: 100 jaar artsen op het consultatiebureau voor zuigelingen en peuters. Ned Tijdschr Geneesk. 2001;145:2461-5. 10 Gorter E. Kinderziekten die in de laatste 50 jaar ontdekt zijn. In: De ontwik-

keling van de kindergeneeskunde in de afgeloopen 50 jaar. Amsterdam: Nederlandsche Vereeniging voor Kindergeneeskunde; 1942. 11 Gelderen HH van. Pre-school child mortality in theNetherlands. Leiden: Stenfert Kroese; 1955. 12 Geneeskundige Hoofdinspectie van de Volksgezondheid (GHI). Immunisatie tegen infectieziekten bij kinderen (het ‘Blauwe boekje’). Den Haag, GHI; 1951. 13 Loghem JJ, van. De taak der consultatiebureau’s voorzuigelingen in de strijd tegen de besmettelijke ziekten. Ned Tijdschr Geneesk. 1951;95:3452-1. 14 Jonge GA de, Plomp HRN, Stoelinga GBA. Pediatrie in de toekomst. Utrecht: Nederlandse Vereniging voor Kindergeneeskunde; 1973. 15 Bestuur Nederlandse Vereniging voor Kindergeneeskunde. Discussienota als aanzet tot Toekomstvisie Kindergeneeskunde in Nederland. Deel I: De tweede en derdelijns Kindergeneeskundige zorg. Utrecht: Nederlandse Vereniging voor Kindergeneeskunde; 2010. 16 Dorsey RE, Jarjoura D, Rutecki GW. Influence of controllable life-style on recent trends in specialty choice by US medical students. JAMA. 2003;290:1173-8. 17 Sengers RCA. Kindergeneeskunde in beweging. Afscheidsrede Hoogleraar Kindergeneeskunde Nijmegen: UMC St Radboud. 2004. 18 Büller HA. Kindergeneeskunde in de 21e eeuw - een visie. Chronisch Ziek dat kan beter! Post academisch onderwijs. Rotterdam: Sophia Ziekenhuis; 2000. 19 Betz, CL. Adolescent transitions: a nursing concern. Pediatr Nurs. 1998;24(1):23-8. 20 Blum RW, Garell D, Hodgman CH, Jorissen TW, Okinow NA, Orr DP, Slap GB. Transition from child-centered to adult health-care systems for adolescents with chronic conditions. A position paper of the Society for Adolescent Medicine. J Adolesc Health. 1993;14(7):570-6. 21 Van Zeben-Van der Aa DMCB, Donckerwolcke R. Tussen wal en schip. Jeugdzorg en gezondheidszorg moeten meer samenwerken. Medisch Contact. 2003;58:354-5. 22 Donckerwolcke RAMG. Kindergeneeskunde: De grenzen verlegd. Afscheidscollege Hoogleraar Kindergeneeskunde Universiteit Maastricht. 2005. 23 Reiss J, Gibson R. Health care transition: destinations unknown. Pediatrics. 2002;110(6 Pt 2):1307-14. 24 Donckerwolcke RAMG, Zeben-Van der Aa DMCB, van. Overdracht van de zorg voor adolescenten met chronische ziekten: van kindergeneeskunde naar specialismen voor volwassenen. Ned Tijdschr Geneesk. 2002;146(14):675-8. 25 ’t Jong GW, Vulto AG, De Hoog M, Schimmel KJ, Tibboel D, Anker JN van den. A survey of the use of off-label and unlicensed drugs in a Dutch children’s hospital. Pediatrics. 2001;108(5):1089-93. 26 Schirm E, Tobi H, Jong-van den Berg LT de. Unlicensed and off label drug use by children in the community: cross sectional study. BMJ. 2002;324(7349): 1312-3. 27 Visser HKA. Wetenschappelijk onderzoek met kinderen. Afweging voor- en nadelen bij ruimere wettelijke grenzen. Ned Tijdschr Geneesk. 2010;154:A2395. 28 Raad voor Gezondheidsonderzoek (RGO). Kind en ziekte: onderzoek voor gezondheid. RGO advies nr. 62. Den Haag: Gezondheidsraad; 2010. 29 Groot R de, Hoekstra JH, Scheewe JH, Visser HKA, Brackel-Welten MAEA. Kindergeneeskunde in Nederland: Tijd voor verandering. Een notitie ter bijdrage aan de discussie en besluitvorming met betrekking tot de NVK-notitie ‘Toekomstvisie Kindergeneeskunde Nederland’. Aangeboden aan de NVVK d.d. 7-9-2010. Uitgegeven in eigen beheer.


Ontwikkelingen in de ontwikkelingsneurologie: de betekenis van variatie en variabiliteit M. Hadders-Algra

Prof. dr. Mijna Hadders-Algra Beatrix Kinderziekenhuis – Instituut voor Ontwikkelingsneurologie, Universitair Medisch Centrum Groningen, Groningen

Inleiding Menselijk gedrag wordt gekenmerkt door variatie. Met andere woorden, de mens heeft een omvangrijk gedragsrepertoire. Het repertoire verschaft de mens de mogelijkheid om zich aan een grote diversiteit aan omstandigheden aan te passen.1 Dit weerspiegelt zich in de motoriek van de mens. Het uitermate rijk gevarieerde en flexibele gedrag van de mens wordt toegeschreven aan de specifieke kenmerken van de menselijke neocortex. De neocortex is het deel van het brein dat gedurende de evolutie verhoudingsgewijs het sterkst in omvang toenam. De cerebrale schors werd niet zozeer dikker, vooral het oppervlak ervan werd groter. Daardoor was er plaats voor nieuwe gebieden, zoals de taalgebieden, belangrijke delen van de frontale schors en de associatiegebieden. Niet alleen de grijze stof nam in omvang toe, ook de witte stof. Deze laatste nam in verhouding zelfs meer toe, vooral vanwege een toename van de cortico-corticale verbindingen.2 De ontwikkeling van het zenuwstelsel is een langdurig en ingewikkeld proces.3 Dit laat zich goed aflezen aan de ontwikkeling van gedrag. Vergelijk bijvoorbeeld het niet-doelgerichte gedrag van de foetus met het gedrag van de peuter die een blokkentoren bouwt, en dat weer met het gedrag van de volwassene die een brief schrijft. Dit artikel beoogt een overzicht te geven van de huidige kennis over het zich ontwikkelende brein, de motorische ontwikkeling en de gevolgen van een hersenbeschadiging op jonge leeftijd voor de ontwikkeling van motorisch gedrag. Het artikel besluit met praktische toepassingsmogelijkheden van deze kennis in de kinderfysiotherapeutische diagnostiek. Het accent van de beschouwingen ligt op de vroege fasen van de ontwikkeling.

De ontwikkeling van het zenuwstelsel De ontwikkeling van het zenuwstelsel, met name die van de neocorticale netwerken, duurt ongeveer 40 jaar.3 Ze begint vroegfoetaal met de productie van neuronen. Het merendeel van de corticale neuronen ontstaat in de kiemlagen vlakbij de ventrikels. Na hun ontstaan migreren zenuwcellen van hun diepgelegen geboorteplaats naar hun uiteindelijke bestemming, de vrij oppervlakkig gelegen corticale plaat.4 De tocht naar de corticale plaat wordt tijdelijk onderbroken in de zogeheten subplaat. Deze tijdelijke pleisterplaats voor zenuwcellen ligt tussen de corticale plaat en de toekomstige witte stof.5 De subplaat ontstaat vroegfoetaal, bereikt haar maximale dikte rond de 29e zwangerschapsweek en verdwijnt daarna geleidelijk. Zes maanden na de à terme leeftijd is de subplaat helemaal verdwenen. Het merendeel van de afferente en efferente verbindingen van de subplaat loopt door de periventriculaire witte stof. De subplaat kan worden beschouwd als de kernstructuur van de foetale hersenschors. Zij speelt dan ook een belangrijke rol in foetaal gedrag.5 Zenuwcellen zijn ten tijde van hun ontstaan eenvoudige structuren. De differentiatie tot volgroeide neuronen omvat de vorming van


Correspondentie E-mail: [email protected]

axonen, dendrieten, synapsen, neurotransmitters, complexe neurale membranen en intracellulaire signaalketens. Deze differentiatie start al tijdens de neurale migratie en het verblijf in de subplaat en is bijzonder actief in de periode vlak voor de à terme leeftijd. De volledige differentiatie neemt echter vele jaren in beslag.3 Naast zenuwcellen bevat het zenuwstelsel ook veel gliacellen. De meeste gliacellen worden aangelegd in de tweede helft van de zwangerschap. Een deel van deze cellen verzorgt de myelinisatie. Die begint vroeg foetaal en vertoont een productiespurt tussen de tweede helft van de zwangerschap en de leeftijd van 1 jaar. Daarna zet de myelinisatie zich voort in een langzamer tempo. Pas rond de leeftijd van 40 jaar is de myelinisatie voltooid; het duurt met name lang voordat de intracorticale myelinisatie is afgerond.3,6 De ontwikkeling van het zenuwstelsel is niet alleen een kwestie van aanmaak. Hersenontwikkeling gaat ook gepaard met grootschalige afbraak. Ongeveer de helft van de aangelegde neuronen is maar een kort leven beschoren en gaat te gronde in een proces van neuronale celdood. Dat proces speelt zich vooral af halverwege de zwangerschap.7 Op soortgelijke wijze worden ook axonen en synapsen verwijderd. Vooral in de jaren tussen de puberteit en de jongvolwassen leeftijd worden er op grote schaal synapsen geëlimineerd. Dit betekent dat de cortex pas op jongvolwassen leeftijd de synaptische dichtheid heeft die kenmerkend is voor het volwassen brein.3,8 De teloorgang van cellen en verbindingen wordt veroorzaakt door een ingenieuze interactie tussen genetische informatie en chemische en elektrische signalen die voortkomen uit ervaring. Dit brengt ons bij de vraag of de ontwikkeling van het brein (en van de motoriek) een kwestie is van aanleg en/of ervaring. Geleidelijk aan is het duidelijk geworden dat zowel genetische informatie (‘nature’) als ervaring (‘nurture’) hierbij een belangrijke rol spelen.9,10 In het begin van de ontwikkeling domineren de invloeden van het erfelijk materiaal, in latere fasen zijn omgeving en ervaring van cruciaal belang. Belangrijk is echter te beseffen dat er altijd sprake is van interactie tussen genetische informatie en ervaring. Men spreekt van epigenetische cascaden, wat wil zeggen dat genetische informatie en omgeving elkaar stapsgewijs beïnvloeden. Dit houdt in dat de activiteit van bepaalde genen maakt dat bepaald gedrag tot expressie komt. Dat gedrag geeft aanleiding tot een specifieke interactie met de omgeving, die op haar beurt resulteert in specifieke ervaringen. Die ervaringen kunnen er vervolgens toe bijdragen dat bepaalde genen aan- of uitgeschakeld worden.

Theorieën over motorische ontwikkeling Hoewel we geleidelijk aan steeds meer te weten zijn gekomen over ontwikkelingsprocessen in het brein, is de kennis over de samenhang tussen hersenontwikkeling en de ontwikkeling van motoriek nog steeds beperkt. Door de kennisleemten konden er verschillende theoretische modellen ter verklaring van de ontwikkeling van motoriek ontstaan. Zo werd in de vorige eeuw ontwikkeling aanvankelijk beschouwd als een endogeen rijpingsproces, maar in de laatste twee decennia van die eeuw brak het inzicht door dat de ontwikkeling van motoriek ook sterk wordt beïnvloed door ervaring. Tegenwoordig worden vooral de dynamische systeemtheorie11 en de Neuronale Group Selectie Theorie (NGST) gebruikt als theoretisch model voor de motorische ontwikkeling.12,13 Beide modellen zijn het erover eens dat de motorische ontwikkeling wordt gekenmerkt door een niet-lineair verloop, dat wil zeggen door een sprongsgewijze ontwikkeling met transities. Ook is het inherent aan beide modellen dat de ontwikkeling wordt beïnvloed door veel factoren. Deze factoren variëren van aspecten van het kind zelf, zoals lichaamslengte of de aanwezigheid van een hartgebrek, tot allerlei omgevingsfactoren, zoals de woonsituatie, de aanwezigheid van stimulerende opvoeders en het speelgoed dat voorhanden is. Dit impliceert dat beide modellen het belang onderschrijven van ervaring en context. Er bestaan echter ook principiële verschillen tussen de uitgangspunten van beide modellen. In de dynamische systeemtheorie spelen genetische factoren voor hersenaanleg slechts een beperkte rol, terwijl in de NGST aan genetische aanleg, epigenetische cascades en ervaring een gelijkwaardige rol wordt toegekend. In de volgende paragrafen zal ik het model van de NGST gebruiken om principes van de normale en afwijkende motorische ontwikkeling te bespreken.

van het kind. Het brein gebruikt bij de selectie functiespecifieke referentiewaarden. Zo fungeert de stabiliteit van het hoofd in de ruimte vaak als referentiemaat voor de bepaling van de adaptieve kwaliteit van houdingsaanpassingen.17 De transitie van primaire naar secundaire variabiliteit vindt plaats op functiespecifieke leeftijden. Zo vindt deze overgang in de ontwikkeling van zuigen waarschijnlijk al voor de à terme leeftijd plaats, en die in de ontwikkeling van het afrollen van de voet tijdens lopen in de leeftijdsperiode van 12 tot 18 maanden.13,18 Het feit dat de overgang van primaire naar secundaire variabiliteit in de ontwikkeling van het zuigen al voor de à terme leeftijd plaatsvindt, maakt dat de op tijd geboren baby zich wat betreft de zuigmotoriek al in de fase van secundaire variabiliteit bevindt. Dit betekent dat de pasgeborene in staat is om het zuiggedrag aan te passen aan de hoeveelheid melk die in de mond vloeit. Rond de leeftijd van 18 maanden hebben alle motorische basisfuncties, zoals zuigen, reiken, grijpen, houdingsregulatie en lopen, de eerste stadia van de secundaire variabiliteit bereikt. Het duurt echter tot de adolescentie dat de volwassen configuratie van de secundaire variabiliteit wordt bereikt. Dat deze ontwikkeling zoveel tijd in beslag neemt, wordt veroorzaakt door de continue ingenieuze interactie tussen zelfgeproduceerde motoriek die gepaard gaat met leren op basis van trial-anderror, en de voortdurende ontwikkelingsprocessen in het brein. Die ontwikkelingsprocessen, zoals dendrietenontwikkeling, myelinisatie en de uitgebreide synaptische reorganisatie, doen nieuwe neuromotore mogelijkheden ontstaan die weer uitgeprobeerd kunnen worden. Kenmerkend voor de fase van secundaire variabiliteit is de aanwezigheid van een gevarieerd repertoire, waaruit voor iedere situatie de beste strategie geselecteerd kan worden. In de secundaire variabiliteit is er dus sprake van variabiliteit, dat wil zeggen variatie met adaptatie.13

NGST en de normale motorische ontwikkeling De NGST is ontwikkeld door de neurobioloog Gerald Edelman.12 Hij beschreef dat de motorische ontwikkeling wordt gekenmerkt door twee fasen van variabiliteit: de primaire en de secundaire variabiliteit. De grenzen van de variabiliteit worden bepaald door genetische instructies. In de fase van primaire variabiliteit is de motoriek erg gevarieerd; deze variatie wordt teweeggebracht door uitprobeeractiviteit van het zenuwstelsel. Alle mogelijkheden die de anatomie toestaan, worden geëxploreerd. De uitprobeermotoriek levert een schat aan sensorische, afferente informatie, die op haar beurt de ontwikkeling van het zenuwstelsel beïnvloedt. Op deze wijze wordt gestalte gegeven aan de continue interactie tussen genetische informatie en ervaring, inclusief de ervaring met veranderende lichaamsmaten. In de fase van primaire variabiliteit kan de afferente informatie echter niet worden gebruikt om de motoriek aan te passen aan de situatie. Met andere woorden, de fase van primaire variabiliteit wordt gekenmerkt door variatie zonder adaptatie. Op een gegeven moment begint het zenuwstelsel de afferente informatie die verbonden is met het eigen gedrag te gebruiken om uit het variabele repertoire die strategie te kiezen die het beste past bij de situatie. De fase van secundaire variabiliteit begint. Dit onbewuste kiezen, dit proces van selectie, is gebaseerd op eigen uitprobeerervaringen, dat wil zeggen op ‘trial-and-error’. In de literatuur komen inderdaad steeds meer bewijzen dat sensorimotorische ervaring door zelfgeproduceerde activiteit een sleutelrol speelt in de motorische ontwikkeling.14-16 Door voortdurend zelf te doen, leert het zenuwstelsel de strategie te selecteren die het best past bij de situatie, inclusief de leeftijd

NGST en de afwijkende motorische ontwikkeling Een beschadiging van de hersenen tijdens de vroege fasen van de ontwikkeling kan leiden tot motorische ontwikkelingsstoornissen, zoals cerebrale parese (CP) of onhandigheid,A maar het is ook mogelijk dat het kind zich helemaal normaal ontwikkelt. Als een kind door een beschadiging van de hersenen op jonge leeftijd motorische stoornissen ontwikkelt, zijn de gevolgen, in termen van de NGST, in de eerste plaats een functionele verkleining van de neuronale repertoires.13,19 Dit betekent dat er binnen het repertoire minder varianten beschikbaar zijn, wat weer leidt tot minder gevarieerd of, anders gezegd, meer stereotiep motorisch gedrag. Het probleem van het beperkte repertoire doet zich zowel voor in de fase van de primaire als in die van de secundaire variabiliteit. De meeste kinderen met motorische stoornissen ten gevolge van een beschadiging van het brein tijdens de vroege fasen van de ontwikkeling bereiken de fase van secundaire variabiliteit, zij het meestal met wat vertraging. Alleen kinderen met ernstige vormen van CP bereiken deze fase niet. Zij blijven stereotype bewegingen vertonen die niet aangepast kunnen worden aan de vereisten van de omstandigheden. In de fase van secundaire variabiliteit zijn de gevolgen van een hersenbeschadiging op jonge leeftijd tweeërlei. In de eerste plaats heeft het kind met een vroege hersenbeschadiging de beschikking over een beperkt repertoire aan bewegingsstrategieën. Dat A Het is belangrijk te beseffen dat bij het merendeel van de kinderen met een onhandige motoriek er géén sprake is van een vroege beschadiging van het brein.


maakt ook dat het kind met een hersenbeschadiging dikwijls andere motorische strategieën gebruikt dan het zich normaal ontwikkelende kind, omdat de gebruikelijke strategieën uit het repertoire zijn verdwenen. De motoriek ziet er anders uit dan gewoonlijk het geval is, maar het is goed te bedenken dat dit meestal voor het kind in kwestie de zelf gekozen, beste oplossing is. Ten tweede heeft het kind problemen met de selectie van de best passende strategie uit het repertoire. Dit selectieprobleem heeft een tweeledige oorzaak. Ten eerste moet het kind vaak een keuze maken uit niet-optimale strategieën, omdat de beste oplossingen, die aanwezig zijn in het onbeschadigde repertoire, verdwenen zijn. Ten tweede hebben dergelijke kinderen niet alleen stoornissen in de centrale organisatie van motoriek, maar ook in de centrale verwerking van sensorische informatie, zoals de proprioceptieve informatie, de informatie over aanraking of de informatie die afkomstig is uit het visuele systeem.20-22 De stoornissen in het verwerken van sensorische informatie interfereren met het selectieproces, dat immers plaatsvindt op geleide van afferente informatie afkomstig uit zelfgeproduceerde trial-and-error. De combinatie van het moeten kiezen uit niet-optimale strategieën en de slechte sensorische terugkoppeling van het effect van eigen bewegingen, maakt dat het selectieproces bij kinderen met een hersenbeschadiging aanzienlijk meer actieve trial-and-error vergt dan bij kinderen met een onbeschadigd brein. De stoornissen in de selectie hebben een paradoxaal effect als kinderen met CP of ernstige onhandigheid een motorische test ondergaan: het testresultaat van het kind met het motorische probleem is variabeler dan dat van het gezonde kind. Dit komt doordat het gezonde kind uit zijn grote repertoire aan strategieën na een keer of drie proberen onbewust precies weet welke motorische oplossing in de gegeven situatie de beste is (het testresultaat is daardoor weinig variabel), terwijl het kind met vroege hersenbeschadiging door de problemen met de selectie veel meer oefening nodig heeft voordat het in de gaten heeft wat de beste motorische oplossing is. Het testresultaat van het kind met hersenbeschadiging is om die reden variabeler, ondanks het feit dat het kind over een beperkt repertoire beschikt.23,24 Een en ander impliceert dat het kind met vroege hersenbeschadiging moeite heeft met het aanpassen van de motoriek aan wisselende omstandigheden, met andere woorden, het kind heeft een verminderde adaptieve variabiliteit.

De normale motorische ontwikkeling van foetus en zuigeling Niet-doelgerichte motoriek De foetus begint te bewegen op de leeftijd van 7 weken en 2 dagen postmenstruele leeftijd (PML).25 De eerste bewegingen bestaan uit kleine zijwaartse beweginkjes van het hoofd en/of de romp. Een paar dagen later worden daar kleine, langzame en enkelvoudige bewegingen van armen en benen aan toegevoegd. Op de leeftijd van 9-10 weken PML ontstaan gegeneraliseerde bewegingen (‘general movements’, GM’s), dat wil zeggen complexe en gevarieerde bewegingen waaraan alle onderdelen van het lichaam meedoen.25 Het GM-begrip ‘complexiteit’ betekent dat alle mogelijke combinaties van bewegingen die in de verschillende gewrichten mogelijk zijn, worden uitgeprobeerd; het GM-begrip ‘variatie’ betekent dat het kind door de tijd heen voortgaat met het uitproberen van alle mogelijke bewegingscombinaties.26,27 Het verschijnen van complexe en gevarieerde GMs op de leeftijd van 9-10 weken PML valt samen met het ontstaan van synaptische activiteit in de corticale subplaat. Niet alleen verschijnen de specifieke GM-kenmerken gelijktijdig met subplaatactiviteit,


de GM’s en de subplaat veranderen ook gelijktijdig van vorm en verdwijnen gelijktijdig. Deze opvallende gelijktijdigheid vormde de basis voor de hypothese dat de variatie en complexiteit van GM’s teweeggebracht wordt door subplaatactiviteit.28 Na het ontstaan van de GM’s breidt het foetale bewegingsrepertoire zich snel uit.29 Er ontstaan geïsoleerde armen beenbewegingen, verschillende soorten hoofdbewegingen (rotatie, ante- en retroflexie), uitrekbewegingen, adem-, zuigen slikbewegingen en hand-mondcontact. De leeftijd waarop een foetus een bepaalde beweging gaat vertonen vertoont een grote interindividuele variatie. Desalniettemin heeft het merendeel van de foetussen rond 16 weken PML het hele foetale bewegingsrepertoire tot zijn beschikking. Het repertoire blijft gedurende de hele zwangerschap in gebruik, met de GM als het meest gebruikte bewegingspatroon. De overgang van het intra-uteriene naar het extra-uteriene leven – op de à terme of op de preterme leeftijd – gaat gepaard met slechts minimale veranderingen in de motoriek. De adembewegingen worden continue (en houden niet meer periodiek op, zoals de foetus zich permitteert), de moro-reactie kan worden uitgelokt, en anteflexie van het hoofd in rugligging is niet langer mogelijk door de tegenwerking van de zwaartekracht. De GM’s blijven het meest gebruikte bewegingspatroon. In de periode van 2-4 maanden (na de à terme leeftijd) doen zich opvallende gedragsveranderingen voor: de baby leert lachjes en geluidjes in te zetten in de sociale interactie, de ogen kunnen goed fixeren, snelle visuele oriëntatie raakt mogelijk en de hoofdbalans wordt stabiel.30 Tegelijkertijd zijn de GM’s in hun laatste fase gekomen en verschijnen voorlopers van reikbewegingen, zoals handjes-speelgedrag in de middellijn. In hun laatste fase krijgen GM’s een specifiek kenmerk, ze worden ‘fidgety’. Dat wil zeggen dat de GMs bestaan uit een continue stroom van kleine en elegante bewegingen die onregelmatig verspreid over het hele lichaam voorkomen.26-28 Dat de leeftijd van 2-4 maanden voor het brein een belangrijke overgangsfase is, valt ook af te leiden uit onderzoek met beeldvormende technieken. Deze onderzoeken toonden aan dat er op de leeftijd van 2-4 maanden duidelijke veranderingen optreden in de activiteit van grote delen van het brein, zoals basale ganglia, cerebellum, pariëtale, temporale en occipitale schors.31

Doelgerichte motoriek De ontwikkeling van doelgerichte motoriek bij zuigelingen wordt gekenmerkt door intra- en interindividuele variatie. Zo bestaat er grote variatie in het ontstaan van een functie, in de manier waarop een functie wordt uitgevoerd, in de duur van verschillende ontwikkelingsfasen en in de leeftijd waarop infantiele reacties, zoals de mororeactie, verdwijnen.18,32 Andere varianten van ontwikkeling zijn het overlappen van verschillende ontwikkelingsfasen – een kind kan op een bepaalde leeftijd zowel tijgeren als kruipen op handen en knieën – en een tijdelijke terugval in de ontwikkeling van één specifieke functie. Zolang een tijdelijke terugval inderdaad beperkt is tot één enkele functie is dit te beschouwen als een variant van normaal. Dit alles betekent dat kinderen een grote variatie vertonen in het bereiken van motorische mijlpalen. Door deze variatie heeft het laat bereiken van een enkele mijlpaal meestal geen klinische betekenis. Pas het vertraagd bereiken van meerdere mijlpalen is van diagnostisch belang.32 In de zuigelingenperiode vindt de transitie plaats van primaire naar secundaire variabiliteit, dat wil zeggen de overgang van motoriek die niet aan de situatie kan worden aangepast naar motoriek die wel adaptief is. Die overgang vindt plaats op functiespecifieke leeftijden. Een recent onderzoek toonde aan dat de transitie van

Figuur 1 Variatie in zitgedrag van een kind van 11 maanden. De figuur bestaat uit frames die gekozen zijn uit een video-opname van ongeveer 3 minuten (gepubliceerd met toestemming van de ouders).


primaire naar secundaire variabiliteit bij de ontwikkeling van het zitgedrag plaatsvindt op de leeftijd van 6-10 maanden, die van het kruipen op de leeftijd van 8 -15 maanden, die van het reiken op de leeftijd van 6 -12 maanden en die van het grijpen op de leeftijd van 15-18 maanden.33 Kinderen kunnen hun motoriek na deze overgangsleeftijden dus duidelijk waarneembaar aanpassen. In de zuigelingenperiode neemt ook het vermogen tot houdingsregulatie spectaculair toe.34 De toegenomen houdingsregulatie maakt dat het kind in de periode van 9 maanden tot 1,5 jaar leert staan en lopen. Houdingsregulatie is een ingewikkeld proces dat zich met name richt op het handhaven van een verticale houding van hoofd en romp. De verticale oriëntatie van de proximale delen van het lichaam is van belang, aangezien deze oriëntatie de optimale uitgangspositie vormt voor het visuele systeem en voor doelgerichte bewegingen. In de houdingsregulatie kunnen twee functionele niveaus worden onderscheiden. Het basisniveau bestaat uit zogeheten richtingsspecifieke houdingsaanpassingen.34 Dit betekent dat het zenuwstelsel bijvoorbeeld bij een dreigende val naar voren onmiddellijk een commando voor het activeren van de spieren aan de dorsale zijde van het lichaam genereert, en bij een dreigende val naar achteren een signaal genereert voor activiteit in de ventrale houdingsspieren. Het onderzoek van Hedberg et al. liet zien dat baby’s van 1 maand al beschikken over richtingsspecifieke houdingsaanpassingen.35 Dit zou erop kunnen duiden dat richtingsspecificiteit een aangeboren eigenschap is. De mens beschikt niet over slechts 1 richtingsspecifieke houdingsaanpassing, maar over een heel repertoire van dergelijke aanpassingen. Jonge zuigelingen gebruiken het repertoire op variabele en niet-adaptieve wijze. Maar al vanaf de leeftijd van 4 maanden ontwikkelt het kind geleidelijk het vermogen om uit het repertoire de aanpassing te kiezen die het best bij de situatie past (figuur 1). Tijdens het leren selecteren van de beste strategieën leert het kind zelfstandig te zitten. Hoe ouder de baby, des te preciezer kan de houding worden aangepast. Rond de leeftijd van 12-14 maanden wordt ook anticipatoire houdingsregulatie mogelijk; dit regulatiemechanisme is van groot belang is bij het (leren) lopen.34 Doelgerichte reikbewegingen worden voorafgegaan door ‘prereik’bewegingen. Zo toonde Von Hofsten aan dat pasgeboren baby’s hun hand dichterbij een voorwerpje brengen als ze ernaar kijken, dan wanneer ze geen visuele aandacht aan het voorwerpje schenken.36 Reiken resulteert vanaf de leeftijd van 4-5 maanden in succesvol grijpen. Aanvankelijk hebben reikbewegingen een zeer variabel verloop. De reikende hand verandert voortdurend van bewegingsrichting. Dat maakt dat de reikbeweging eigenlijk bestaat uit een hele reeks kleine beweginkjes (bewegingssegmenten, ‘movement units’), waarbij de overgang naar elk volgend bewegingssegment de mogelijkheid biedt tot bijsturing van de beweging. Met andere woorden, op jonge leeftijd is het reiktraject nog niet voorgeprogrammeerd. Het kind moet door eindeloze trial-and-error leren wat de meest efficiënte manier van reiken is. Met het ouder worden, wordt de reikbeweging steeds rechter en vloeiender. Het aantal bewegingssegmenten neemt af, het afgelegde reiktraject wordt korter en kost steeds minder tijd. Tegelijkertijd raakt ook de hand van de reikende arm steeds beter aangepast en voorbereid op het te grijpen voorwerp.18 Vanaf de leeftijd van 1 jaar gebruikt het kind in toenemende mate de pincetgreep om kleine voorwerpjes te pakken. Dit duidt op een toename van corticospinale invloeden.37 Een pasgeboren baby kan, net als de foetus, loopbewegingen


maken. Deze bewegingen worden waarschijnlijk gegenereerd door een centrale patroongenerator in het ruggenmerg.38 Het neonatale lopen verdwijnt rond de leeftijd van 2-3 maanden. De beenmotoriek ontwikkelt zich daarna vooral door activiteiten zoals rollen en kruipen. Staan en lopen beginnen in de laatste maanden van het eerste levenslaar tot ontplooiing te komen. Ook hier is het een kwestie van uitproberen, variëren en geleidelijk leren selecteren van de beste strategieën.18 Zoals eerder gesteld, de ontwikkeling van lopen is sterk afhankelijk van de ontwikkeling van houdingsregulatie. Ontwikkelingen na de zuigelingenleeftijd maken de motoriek steeds flexibeler en adaptiever. Het vermogen om ingewikkelde bewegingssequenties uit te voeren groeit, wat bijvoorbeeld veters strikken en pianospelen mogelijk maakt. Het kind bevindt zich in de fase van de secundaire variabiliteit, waarin de secundaire neurale repertoires ontstaan. Deze zeer adaptieve neurale netwerken komen tot stand door een voortdurende interactie tussen de ontwikkelingsprocessen in het brein enerzijds, en veranderende lichaamsmaten en een veelheid aan gedragservaringen anderzijds. Het ontstaan van de secundaire repertoires gaat gepaard met uitgebreide synaptische herverkaveling, dat wil zeggen synapsaanleg en -eliminatie, en met een steeds snellere signaalverwerking op grond van voortschrijdende myelinisatie.3

De afwijkende motorische ontwikkeling van foetus en zuigeling De ontwikkeling van het zenuwstelsel heeft grote gevolgen voor de wijze waarop een afwijkende motorische ontwikkeling tot uitdrukking wordt gebracht. Het is bijvoorbeeld mogelijk dat een hersenlaesie zich op jonge babyleeftijd uit als neurologische disfunctie, maar dat er in de verdere ontwikkeling normalisatie optreedt, zodat het kind later volledig normaal functioneert. Het omgekeerde kan echter ook het geval zijn. Dat betekent dat verschijnselen van disfunctie geleidelijk tevoorschijn komen, na een periode waarin er aanvankelijk niet tot nauwelijks disfunctie waarneembaar was.27 Op de zuigelingenleeftijd kan een afwijkende motorische ontwikkeling zich manifesteren als een vertraagde ontwikkeling – de mijlpalen worden langzamer bereikt door een minder goed functionerende selectie –, als een tonusregulatiestoornis, een blijven bestaan van infantiele reacties en een beperkte variatie in de motoriek. Waarschijnlijk is dat laatste verschijnsel het meest specifiek voor een vroege hersenbeschadiging. De andere verschijnselen kunnen ook het gevolg zijn van een hersenbeschadiging, maar zij zijn vaker een uiting van minder ernstige ontwikkelingsproblematiek, zoals een niet-optimale ontwikkeling na vroeggeboorte.13 De beperkte variatie in motoriek is goed af te lezen aan de kwaliteit van de GM’s. Afwijkende GM’s worden gekenmerkt door een beperkte variatie en een beperkte complexiteit.26-28 Recent onderzoek toonde aan dat duidelijk afwijkende GM’s vooral samenhangen met beschadigingen van de (diepe) witte stof en niet met afwijkingen van de grijze stof van het brein.28 Ook nadat de GM’s zijn verdwenen, ongeveer vanaf de leeftijd van 4 maanden, wordt afwijkende motoriek gekenmerkt door een gebrek aan variatie, dat wil zeggen door stereotypie (figuur 2). Bekende voorbeelden van stereotypieën zijn vuistjes, extensie van de benen, klauwen van de tenen, een dominerend patroon van de asymmetrische tonisch nekreactie (ATNR), hyperextensie van romp en nek, of een stereotype asymmetrie. Mogelijk weerspiegelt de mate waarin de motorische variatie is afgenomen de mate van disfunctie van de corticale connectiviteit.

Figuur 2 Beperkte variatie in zitgedrag van een kind van 10 maanden. De figuur bestaat uit frames die gekozen zijn uit een video-opname van ongeveer 3 minuten (gepubliceerd met toestemming van de ouders).


Een afwijkende motorische ontwikkeling gaat vrijwel altijd gepaard met stoornissen in de houdingsregulatie.17 Kinderen die door ernstige hersenbeschadiging een ernstige vorm van bilaterale spastische of dyskinetische CP hebben (Gross Motor Function Classification System niveau V) missen hoogstwaarschijnlijk het basale niveau van de houdingsregulatie, de richtingsspecificiteit. Bij kinderen met minder ernstige vormen van CP is het basale niveau van houdingsregulatie min of meer intact. Wel verloopt de houdingsontwikkeling bij deze kinderen moeizamer, en daardoor ook trager, door beperkingen in het repertoire van houdingsaanpassingen en door het beperkte vermogen om de houding aan te passen aan de specifieke eigenschappen van de situatie.17

Variatie en variabiliteit in de kinderfysiotherapeutische diagnostiek Geleidelijk aan wordt steeds meer duidelijk dat de concepten ‘variatie’ (de grootte van het repertoire) en ‘variabiliteit’ (het vermogen om in iedere situatie de meest geschikte motorische gedragsvariant te kunnen kiezen) van belang zijn in de (vroeg) diagnostiek van motorische ontwikkelingsstoornissen. Vroegdiagnostiek heeft twee oogmerken. Het eerste doel van vroegdiagnostiek is de bepaling van de huidige conditie van het kind. Aan de hand van het oordeel over de huidige conditie wordt besloten of het kind interventie behoeft of niet. Het tweede doel van vroegdiagnostiek is de voorspelling van de verdere ontwikkeling. Echter, zoals eerder opgemerkt, het ontwikkelende brein maakt precieze predictie op jonge leeftijd onmogelijk. Voorspellen van de ontwikkeling blijft dus lastig, maar gaat beter als men een combinatie van instrumenten gebruikt, zoals anamnese, beeldvormend onderzoek, neurofysiologisch onderzoek, en neurologisch en motorisch onderzoek. Voorspelling lukt het best, maar is nog steeds niet perfect, op basis van een longitudinale reeks van onderzoekingen.39 Inmiddels zijn twee methoden ontwikkeld om de motoriek van zuigelingen te beoordelen, gebaseerd op de principes van variatie en/of variabiliteit. Voor jonge baby’s gaat het om het beoordelen van de kwaliteit van GM’s,26-28,40 voor kinderen van 3-18 maanden om de Infant Motor Profile (IMP).41,42 De beoordeling van de kwaliteit van GM’s is een betrouwbare methode, die is gebaseerd op de evaluatie van de variatie in motoriek. Bij GM’s wordt niet de variabiliteit beoordeeld, omdat GM’s – als uitzondering op de regel – geen fase van secundaire variabiliteit hebben. Bij de GM-beoordeling worden twee vormen van variatie geëvalueerd: GM-complexiteit, waarbij het gaat om de ruimtelijke aspecten van variatie, en GM-variatie, waarbij het gaat om de temporele aspecten van variatie.27,28 Duidelijk afwijkende GM’s worden gekenmerkt door een sterke afname van bewegingscomplexiteit en variatie; licht afwijkende GM’s hebben wel enige complexiteit en variatie, maar in onvoldoende mate.27,28 Kinderen die in de eerste postnatale maanden voortdurend duidelijk afwijkende GM’s vertonen, hebben een zeer hoog risico op de ontwikkeling van CP.40 De predictieve waarde van een enkel GMonderzoek is minder sterk. Deze predictieve waarde neemt toe met de leeftijd en is het best in de fidgetyfase, dat wil zeggen rond de gecorrigeerde leeftijd van 3 maanden.26-28,40 Bij risicozuigelingen duiden duidelijk afwijkende GM’s op de leeftijd van 3 maanden op een hoog risico op CP (percentages in de literatuur variëren van 25-80%); licht afwijkende GM’s zijn geassocieerd met een verhoogd risico op lichte neurologische disfunctie en psychiatrische morbiditeit op de schoolleeftijd.27,28 Het verband tussen licht afwijkende GM’s en latere ontwikkelingsstoornissen is echter zo


zwak dat licht afwijkende GM’s klinisch geen betekenis hebben. Recent is aangetoond dat de voorspellende waarde van GMkwaliteit bij risicozuigelingen veel groter is dan bij baby’s uit de algemene populatie.43 Deze bevinding past bij de gedachte dat de kwaliteit van GM’s met name de integriteit van de corticale connectiviteit weerspiegelt, dat wil zeggen de integriteit van de witte stof in de hersenen.28 De witte stof bevindt zich immers voor een belangrijk deel in de buurt van de ventrikels, en juist dit periventriculaire gebied is gevoelig voor beschadiging in de preterme periode.44 De IMP is een recent ontwikkeld instrument waarin vijf domeinen van babymotoriek worden geëvalueerd.41,42 Twee domeinen zijn gebaseerd op de NGST: variatie (de grootte van het repertoire) en variabiliteit (het vermogen van het kind tot selectie). In de 3 overige domeinen worden meer traditionele aspecten van motoriek beoordeeld: symmetrie, vloeiend bewegingsverloop en prestatie. De betrouwbaarheid en de constructvaliditeit van de IMP zijn goed en de eerste gegevens over de predictieve waarde van de IMP lijken gunstig.

Tot besluit Waarschijnlijk is de rijke cerebrale connectiviteit bij de mens de neurale basis van gedragsvariabiliteit, dat wil zeggen van het vermogen om uit een groot repertoire aan gedragsmogelijkheden dat gedrag te kiezen dat het beste past bij de situatie. Bevindingen uit de ontwikkelingsneurologie sluiten hierbij aan: de normale motorische ontwikkeling wordt gekenmerkt door variatie en de ontwikkeling van adaptieve variabiliteit, terwijl de afwijkende motorische ontwikkeling wordt gekenmerkt door beperkingen in variatie en variabiliteit. Een evident beperkte variatie duidt op een hersenlaesie, met name op afwijkende cerebrale connectiviteit. Beperkte variabiliteit kan een gevolg zijn van een hersenlaesie, maar komt veel vaker voor zonder een duidelijke hersenbeschadiging.13 Het kan bijvoorbeeld een gevolg zijn van vroeggeboorte. Bij kinderen met beperkte variatie is een doel van vroege interventie het vergroten van het motorische repertoire. Echter, dierexperimenteel onderzoek geeft aan dat de mogelijkheden voor repertoirevergroting klein zijn.45 Dit betekent dan ook dat kinderen met een beperkt repertoire, ondanks interventie, dikwijls een beperkt repertoire blijven houden. Met andere woorden, er zitten grenzen aan de behandelmogelijkheden op het niveau van beperkingen. Aangezien met name participatie in het dagelijks leven centraal staat, is het van groot belang om bij kinderen met beperkingen in het motorische repertoire niet te lang te wachten met het gebruik van hulpmiddelen. Bij de beperkingen in de variabiliteit speelt gebrekkige sensorische terugkoppeling van (het resultaat van) eigen bewegingen een duidelijke rol. Kinderen met beperkte variabiliteit zullen dan ook baat hebben bij veel en variabele, zelf uitgevoerde trial-anderroractiviteit. Referenties 1 Krubitzer L, Kaas J. The evolution of the neocortex in mammals: how is phenotypic diversity generated? Curr Opin Neurobiol. 2005;15:444-53. 2 Zhang K, SejnowskiTJ. A universal scaling law between gray matter and white matter of cerebral cortex. Proc Natl Acad Sci USA. 2000;97:5621-6. 3 Graaf-Peters VB de, Hadders-Algra M. Ontogeny of the human central nervous system: what is happening when? Early Hum Dev. 2006;82:257-66. 4 Bystron I, Blakemore C, Rakic P. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci. 2008;9:110-22.

5 Kostovic I, Judas M. Transient patterns of cortical lamination during prenatal life: do they have implications for treatment? Neurosci Biobehav Rev. 2007;31:1157-68. 6 Sowell ER, Trauner DA, Gamst A, Jernigan TL. Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev Med Child Neurol. 2002;44:4-16. 7 Buss RR, Sun W, Oppenheim RW. Adaptive roles of programmed cell death during nervous system development. Annu Rev Neurosci. 2006;29:1-35. 8 Martin JH, Friel KM, Salimi I, Chakrabarty S. Activity- and use-dependent plasticity of the developing corticospinal system. Neurosci Biobehav Rev. 2007;31:1125-35. 9 Krubitzer L, Kahn DM. Nature versus nurture revisited: an old idea with a new twist. Prog Neurobiol. 2003;70:33-52. 10 Diamond A. The interplay of biology and the environment broadly defined. Dev Psychol. 2009;45:1-8. 11 Smith LB, Thelen E. Development as a dynamic system. Trends Cogn Sci. 2003;7:343-8. 12 Edelman GM. Neural Darwinism. The theory of neuronal group selection. Oxford: Oxford University Press; 1989. 13 Hadders-Algra M. Variation and variability: keywords in human motor development. Phys Ther. In press 2010. 14 Hadders-Algra M, Brogren E, Forssberg H. Training affects the development of postural adjustments in sitting infants. J Physiol. 1996;493:289-98. 15 Higgins CI, Campos JJ, Kermoian R. Effect of self-produced locomotion on infant postural compensation to optic flow. Dev Psychol. 1996;32:836-41. 16 Adolph KE. Learning in the development of infant locomotion. Monogr Soc Res Child Dev. 1997;62:1-158. 17 Hadders-Algra M, Brogren Carlberg E, editors. Postural control: a key issue in developmental disorders. Clin Dev Med. 2008;179:22-73. 18 Hadders-Algra M, Dirks T. De motorische ontwikkeling van de zuigeling: variëren, selecteren en leren adapteren. Houten: Bohn, Stafleu van Loghum; 2000. 19 Hadders-Algra M. The Neuronal Group Selection Theory: promising principles for understanding and treating developmental motor disorders. Dev Med Child Neurol. 2000;42:707-15. 20 Yekutiel M, Jariwalda M, Stretch P. Sensory deficit in the hands of children with cerebral palsy: a new look at assessment and prevalence. Dev Med Child Neurol. 1994;36:619-24. 21 Guzetta A, Mercuri E, Cioni G. Visual disorders in children with brain lesions: 2. Visual impairment associated with cerebral palsy. Eur J Paediatr Neurol. 2001;5:115-9. 22 McLaughlin J, Felix SD, Nowbar S, Ferrel A, Bjornson K, Hays RM. Lower extremity sensory function in children with cerebral palsy. Pediatr Rehab. 2005;8:45-52. 23 Eliasson AC, Gordon AM, Forssberg H. Impaired anticipatory control of isometric forces during grasping by children with cerebral palsy. Dev Med Child Neurol. 1992;34:216-25. 24 Smits-Engelsman BC, Rameckers EA, Duysens J. Muscle force generation and force control of finger movements in children with spastic hemiplegia during isometric tasks. Dev Med Child Neurol. 2005;47:337-42. 25 Lüchinger AB, Hadders-Algra M, Kan CM van, Vries JIP de. Fetal onset of general movements. Pediatr Res. 2008;63:191-5. 26 Prechtl HFR. General movement assessment as a method of developmental neurology: new paradigms and their consequences. Dev Med Child Neurol. 2001;43:836-42.

27 Hadders-Algra M. General movements: a window for early identification of children at high risk of developmental disorders. J Pediatr. 2004;145:S12-8. 28 Hadders-Algra M. Putative neural substrate of normal and abnormal general movements. Neurosci Biobehav Rev. 2007;31:1181-90. 29 Vries JIP de, Fong BF. Normal fetal motility. An overview. Ultrasound Obstet Gynecol. 2006;27:701-11. 30 Prechtl HFR. Continuity of neural functions form prenatal to postnatal life. Clin Dev Med 1984;94:179-92. 31 Rubinstein M, Denays R, Ham HR, Piepsz A, VanPachterbeke T, Haumont D, Noël P. Functional imaging of brain maturation in humans using Iodine-123 Idoamphetamine and SPECT. J Nucl Med. 1989;30:1982-5. 32 Touwen BCL. De neurologische ontwikkeling van de zuigeling. Utrecht, Antwerpen: Bohn, Scheltema & Holkema; 1984. 33 Heineman KR, Middelburg KJ, Hadders-Algra M. Development of adaptive motor behaviour in typically developing infants. Acta Paediatr. 2010;99:618-24. 34 Hadders-Algra M, Brogren Carlberg E. Postural control: a key issue in developmental disorders. Clin Dev Med. 2008;179:22-73. 35 Hedberg Å, Forssberg H, Hadders-Algra M. Early development of postural adjustments in sitting position: evidence for the innate origin of direction specificity. Exp Brain Res. 2004;157:10-7. 36 Von Hofsten C. Eye-hand coordination in the newborn. Dev Psychol. 1982;18:450-61. 37 Lemon RN, Kirkwood PA, Maier MA, Nakajima K, Nathan P. Direct and indirect pathways for corticospinal control of upper limb motoneurons in the primate. Prog Brain Res. 2004;143:263-79. 38 Yang JF, Gorassini M. Spinal and brain control of human walking: implications for retraining of walking. Neuroscientist. 2006;12:379-89. 39 Heineman KR, Hadders-Algra M. Evaluation of neuromotor function in infancy - a systematic review of available methods. J Dev Behav Pediatr. 2008;29:315-23. 40 Einspieler C, Prechtl HFR, Bos AF, Fererari F, Cioni G. Prechtl’s method on the qualitative assessment of General Movements in preterm, term and young infants. Clin Dev Med. No. 167. London: Mac Keith Press; 2005. 41 Heineman KR, Bos AF, Hadders-Algra M. The Infant Motor Profile – a standardized and qualitative method to assess motor behaviour in infancy. Dev Med Child Neurol. 2008:50:275-82. 42 Heineman KR, La Bastide-van Gemert S, Fidler V, Middelburg KJ, Bos AF, Hadders-Algra M. Construct validity of the Infant Motor Profile: relation with prenatal, perinatal and neonatal risk factors. Dev Med Child Neurol. 2010;52:e209-15. 43 Bouwstra H, Dijck-Stigter GR, Grooten HMJ, Janssen-Plas FEM, Koopmans AJ, Mulders CD, Belle A van, Hadders-Algra M. Predictive value of definitely abnormal GMs at three months in the general population. Dev Med Child Neurol. 2010;52:456-61. 44 Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009;8:110-24. 45 Kolb B, Gibb R. Brain plasticity and recovery from early cortical injury. Dev Psychobiol. 2007;49:107-18.


Recent and past developments in neonatal neurology L.S. de Vries Introduction It is difficult to imagine that it was only in the late seventies that we were for the first time able to assess the neonatal brain noninvasively using neuro-imaging techniques. Neonatal intensive care initially focused on support of respiratory function, aiming mainly for survival, without being able to obtain information about the brain. Since the introduction of neonatal intensive care, there has been a significant increase in survival during the neonatal period (first 4 weeks following delivery). While about 60% of all infants born in 1960 with a birthweight between 1000-1500 g died, this percentage came down to 23% in 1983 (Project Onderzoek [transl.: investigation] Praematuritas and Small-for gestational age [POPS]) and a further decrease was shown in the Netherlands in 1994 to 15% and in 2005 to 6%.1 We have recently shown that even in preterm infants with a birthweight ≤ 750 g, survival increased from 66% of infants born between 1996 and 2000 to 88% when born between 2001 and 2005.2 While the mortality rate of these preterm infants continues to decrease, they unfortunately remain at risk for neurological disabilities later in life.3 They are prone to develop both motor and cognitive impairments affecting their long-term intellectual, behavioural and social functioning.4,5 Most of these impairments have their origin in the immediate perinatal period and this applies especially to the extremely low birth weight infants, born with a weight below a 1000 g and/or a gestational age below 28 weeks. Recent publications have shown that the incidence of severe motor handicaps is no longer increasing and, in some centres, including our own, is now even decreasing.6,7,8 A severe form of cerebral palsy (CP) is however still reported in 5-7% of extremely low birth weight infants (ELBW), with yet another 8% developing a mild degree of spasticity. Another 25% will develop some degree of ‘disability’. The term disabilities is an umbrella term, covering impairments, activity limitations, and participation restrictions. An impairment is a problem in body function or structure; an activity limitation is a difficulty encountered by an individual in executing a task or action, whereas a participation restriction is a problem experienced by an individual involvement in life situations. Thus, disability is a complex phenomenon, reflecting an interaction between features of a person’s body and features of the society in which he or she lives. In the Epicure study, all infants born with a gestation of 23-25 weeks, who were born in the United Kingdom and Ireland, in 1995, were followed into childhood and results have now been reported till 11 years of age.9 The prevalence of serious functional disability was 46% at 6 years of age and 45% at 11 years of age. Serious cognitive impairment (score of less than -2 SD) was present in 40% of extremely preterm children and 1.3% of classmates (odds ratio [OR]: 50 [95% confidence interval (CI): 12-206]) at 11 years of age. Overall at 11 years of age, 38 (17%) extremely preterm children had CP; moderate or severe impairment of neuromotor function, vision, and hearing was present in 10%, 9%, and 2% of these children, respectively. Combining impairment across domains, 98 (45%)


Linda S. de Vries Professor in Neonatal Neurology, Department of Neonatology, Wilhelmina Kinderziekenhuis, University Medical Centre Utrecht, Utrecht, the Netherlands Correspondence E-mail : [email protected]

extremely preterm children had serious functional disability compared with 1% of the classmates (OR: 61 [95% CI = 15-253]); this was more common in boys than in girls (OR: 1.8 [95% CI: 1.0-3.1]) and in those born at 23 or 24 weeks’ gestation compared with those born at 25 weeks’ gestation (OR: 1.8 [95% CI: 1.0-3.1]).10,11 With improvement in neuro-imaging techniques, especially magnetic resonance imaging, we now better understand why these ELBW infants develop motor problems later in infancy and cognitive and behavioral problems later in childhood. In this review, the most commonly occurring brain lesions will be discussed with a focus on the preterm infant.

Brain injury in the preterm infant Since cranial ultrasound became part of routine clinical care in the late seventies, the ‘black box’ concept disappeared and we started to visualize intracranial lesions in this vulnerable population. Until then, haemorrhagic-ischemic lesions had only been diagnosed by the pathologist. The first neuro-imaging studies were performed using computed tomography, but because of radiation hazard, this rapidly changed to using ultrasonography. With early low resolution ultrasonography, performed through the temporal bone, haemorrhagic lesions, rather than ischaemic lesions could be diagnosed and it was of interest to see the onset and evolution of these lesions, which often appeared in the absence of any (obvious) clinical symptoms. Within a couple of years, ultrasonography techniques improved, using higher resolution transducers and making use of the anterior fontanelle as an excellent acoustic window. It soon became clear that a unilateral parenchymal haemorrhage often had less of an adverse effect on later outcome, than bilateral white matter injury, referred to as leukomalacia (Greek for softening of the white matter). In the eighties of the last century, cystic leukomalacia was not uncommon and bilateral cystic lesions in the periventricular white matter almost invariably led to bilateral spastic cerebral palsy (BSCP).12 In recent years, several centres also have used the mastoid sutures as an acoustic window, which has helped to better visualize the posterior fossa and the cerebellum. Cerebellar haemorrhages are now known to be not uncommon in the ELBW infants and are increasingly being reported as a strong predictor of poor cognitive and behavioral outcome.13,14 Performing sequential ultrasound within the first days to weeks following a preterm delivery has shed light on understanding timing of onset and evolution of the different patterns of injury, but in particular this made us recognize risk factors preceding these lesions. Recognition of risk factors helped to bring down the incidence of especially haemorrhagic lesions and more recently also of ischemic lesions, in particular cystic periventricular leukomalacia (PLV).15

With the introduction of magnetic resonance imaging (MRI), more detailed information could be obtained in these infants and it became clear that cranial ultrasound underestimated lesions occurring in the white matter. While small cysts could be clearly recognized with sequential cranial ultrasound, more diffuse injury to the white matter was less apparent and more difficult to assess objectively.16,17 This is especially important as cystic PVL is no longer a common problem in this population of infants, while with decreasing maturity of admitted infants, subtle but more diffuse white matter injury is now more common and is more often associated with cognitive and behavioral problems rather than severe motor problems.15,18 Recent advances in MRI include diffusion tensor imaging and sophisticated image analysis tools, such as functional connectivity, voxel-based morphometry, and mathematical morphology-based cortical folding strategies.19,20 Using these new sophisticated techniques there is insight in development of cortical folding and maturation of white matter tracts. Volumes of different tissue structures can be calculated and reduced grey and white matter volumes have been shown to be associated with later cognitive outcome.21,22 These changes in volumes are now known to persist till adolescence.23,24

also develop in the white matter, due to impaired venous drainage, associated with an IVH (referred to as grade IV or haemorrhagic parenchymal infarction, HPI). Grade I-II haemorrhages are considered small, while grade III and IV haemorrhages are considered severe with a higher risk for adverse neurological sequelae (figure 1). About 10-20% of all preterm infants admitted to a NICU, with a birth weight below 1500 g will develop a GMH-IVH, but a severe haemorrhage will occur in only 6-8% of the infants.6 Sequential imaging has shown that any haemorrhage tends to develop during the first 3 days after delivery and rarely beyond the first week. It was also clear that haemorrhages were more commonly seen in those infants with the lowest gestational age. These very immature infants were also more prone to develop a severe haemorrhage, which can be explained by the increased need for ventilation due to lung immaturity. Cardiovascular changes with fluctuations in blood pressure and cerebral blood flow are more likely to occur, while being on a ventilator. The increased use of antenatal corticosteroids and postnatal administration of surfactant has reduced the need for ventilatory support and this has led to a reduction of severe intracranial lesions.

White matter damage Germinal layer- and intraventricular haemorrhages The very preterm infant has an immature vascular network, existing of thin fragile vessels, most prominent underneath the lateral ventricles, a region referred to as the germinal matrix. This network of vessels is most prominent between 24 and 34 weeks of gestation and during periods of fluctuating blood pressure, in the absence of cerebral autoregulation, changes in cerebral blood flow may co-exist and lead to rupture of these fragile vessels. Haemorrhage in a preterm infant will almost invariably occur in the germinal matrix (GMH grade I) and often blood will rupture through the ependyma into the lateral ventricle, leading to an intraventricular haemorrhage (IVH grade II). When there is a lot of blood in the lateral ventricle, there tends to be acute ventricular dilatation (grade III) and this is often followed by development of posthaemorrhagic ventricular dilatation (PHVD). Haemorrhage can

Until the beginning of this millennium white matter damage was usually referred to as PLV. This condition, seen almost exclusively in the preterm infant, was initially considered to be due to underperfusion of so-called boundary zones. We have since become to realize that other underlying problems play a more important role, such as inflammation, associated with prolonged rupture of membranes and chorioamnionitis. Another important factor is the vulnerability of a specific population of brain cells, the oligodendroglia.25 Furthermore, there has been a change in the pattern of white matter damage, visualized with neuro-imaging techniques. While the incidence of cystic periventricular leukomalacia was noted to come down, more diffuse and more subtle white matter injury was recognized in a majority of preterm infants, when undergoing MRI, rather than only cranial ultrasound.15,18,22 While cystic PVL has now become a

Figure 1 Preterm infant, gestational age 25 weeks and 6 days. Ultrasound, coronal view, performed at 3 weeks of age, shows large right-sided IVH with parenchymal involvement. The MRI (T2 weighted spinecho sequence) performed at 30 weeks postmenstrual age shows a very similar pattern of injury.


Figure 2 Preterm infant, gestational age 31 weeks. Ultrasound, coronal view (a) and MRI, T2 weighted sequence (b). Areas of increased echogenicity on ultrasound correlate well with areas of decreased signal intensity on MRI. These punctate white matter lesions are suggestive of petechial haemorrhages. rare condition in most neonatal units (2-5%), it is known to almost invariably lead to CP.17 Sequelae of subtle white matter changes are less severe and more difficult to study, as they often co-exist with other types of injury, seen in this vulnerable population, such as a small GMH-IVH or mild ventriculomegaly, often considered a sequel of subtle white matter injury. Abnormalities in the white matter, have been reported to be common and when graded as moderate to severe, to be strongly associated with later motor and cognitive outcome.26 Some groups have described white matter injury on MRI as ‘DEHSI’, meaning diffuse excessive high signal intensity.27 This entity was subsequently reported to occur in 6070% of all their preterm infants, when assessed at term equivalent age.18 White matter injury, even when subtle, has now been shown by several groups to lead to volume loss of not only the white matter but also the cortex and central grey matter.28 In contrast to haemorrhages, white matter damage can develop at any time during the neonatal period. Diffuse white matter damage but also cystic PVL can occur following septicaemia or necrotizing enterocolitis, occurring weeks after a preterm delivery.17,29 See figure 2. Sequelae following a haemorrhage Infants who develop a severe haemorrhage (graad III and HPI) are most at risk (25%) to develop posthaemorrhagic ventricular dilatation, which may require intervention, either repeat lumbar punctures or insertion of a subcutaneous reservoir. In about 40% of those requiring insertion of a reservoir, there is an ongoing disbalance between production and reabsorption of cerebrospinal fluid, eventually requiring insertion of a ventriculo-peritoneal shunt.30 The size of the lateral ventricles can be sequentially measured in a reliable and noninvasive way, using cranial ultrasound. There is no agreement about timing of intervention. Observational and retrospective studies have suggested that early intervention, before clinical symptoms of raised intracranial pressure occur (full fontanelle, vomiting, apneas, sunsetting), may lead to a better outcome with a significantly smaller number of infants eventually requiring a ventriculoperitoneal shunt. This


is now being studied in a prospective randomized controlled trial (early versus late intervention study [ELVIS]). Several studies have shown a very poor outcome in preterm infants with a gestational age below 32 weeks and infantile hydrocephalus, i.e. those infants who required a ventriculo-peritoneal sunt.31 About 75% developed CP and about half also developed learning disabilities. Cerebral visual impairment and epilepsy were also common. Our own data are not so dismal, with a lower but still significant risk to develop CP (30-40%) or learning disabilities (30%).17,30 Maybe we can attribute the better outcome in our population to earlier intervention of PHVD, although motor outcome is unlikely to be affected in infants with associated parenchymal injury. Recent data have been able to show that some of the children with parenchymal injury have a better long term outcome than expected.32,33 This can be best explained by the fact that a parenchymal haemorrhage tends to be unilateral and as these children are still very young, they are apparently able to reorganize their sensorimotor cortex which is considered due to ‘brain plasticity’.34 Sequelae following white matter injury The initial follow-up studies focused on outcome in infants with GMH-IVH. This was mostly due to the fact that lesions in the white matter were often overlooked using low resolution cranial ultrasound. One can therefore wonder how valuable these early studies are, as it is likely that lesions in the white matter must have been present in infants with a poor outcome, in spite of a normal ultrasound scan. Some of these cohorts have subsequently been studied with MRI, allowing us to better understand the relation between long term outcome into adolescence and involvement of both brain structure and volume.35 Following these initial studies, cranial ultrasound technology has improved and with a wider angle of insonation and a higher resolution transducer, it became possible to see small cystic lesions in the white matter and it became clear that these lesions were of more importance with regard to an adverse motor outcome, compared to GMH-IVH. When considering outcome in relation to white matter injury, we

have to make a distinction between cystic white matter lesions, usually referred to as cystic PVL and more subtle white matter injury, which is best diagnosed using MRI. Extensive cystic PVL almost invariably leads to CP with a GMFCS level grade IV-V and is not uncommonly associated with development of epilepsy, learning disabilities and cerebral visual impairment.12,36 Cerebral visual impairment should be recognized early in infancy to allow early intervention. Impaired visual perception is more common in early childhood in children with PVL compared to those with GM-IVH.37 In infants with noncystic or more localized cystic PVL, there is still a considerable risk of developing CP, but 85% of these children, who did develop CP, had a level I-II on the GMFCS and were able to walk independently, compared to less than 10% in those with extensive cystic PVL. The most likely explanation for the difference in motor outcome between infants with a parenchymal haemorrhage and cystic PVL is unilateral versus bilateral involvement. Cystic PVL is a predominantly bilateral type of injury, not allowing any compensation from a nonaffected hemisphere. More recently one has been able to better evaluate the role of (subtle) white matter injury, best diagnosed with MRI, with regard to later outcome.26 The conclusion of this elegant study was that moderate to severe white matter injury was strongly associated with all aspects of later outcome. MRI does not only allow us to visually assess the white matter, but also makes it possible to quantitatively assess tissue characteristics, such as volumetric analysis and calculation of the progression of cortical folding (sulcation index).20,22 These sophisticated neuro-imaging techniques will allow us to study the neonatal brain in a way which is less subjective and will therefore allow comparison of data between different centres. Access to these new technologies is required as we are nowadays often looking at infants with subtle injury rather than large parenchymal lesions.

Cerebellar haemorrhages The extremely preterm infant is especially at risk to develop haemorrhages involving the cerebellum.13,14 Limperoupolos et al. were one of the first to study a large cohort of preterm infants,

using both the anterior fontanelle, as well as the mastoid suture as an acoustic window. Almost 8% of those with a birth weight below 750 gram were noted to develop a cerebellar haemorrhage, most often restricted to one cerebellar hemisphere (figure 3). These infants tend to have a large GMH-IVH or associated white matter lesions as well. The importance of recognizing these cerebellar haemorrhages became apparent, when outcome at 2-4 years of age of this very cohort was reported. When comparing their preterm infants with and without a cerebellar haemorrhage, it was obvious that outcome was significantly worse in those with a cerebellar haemorrhage and not only in motor performance, but especially in behavioral and cognitive skills. Severe atrophy tended to be present on a repeat MRI.38 When using MRI, rather than ultrasonography, smaller and punctate cerebellar haemorrhages can be recognized.14 The effect of these smaller haemorrhages on neurodevelopmental outcome is not yet known.

Intra-uterine growth retardation (IUGR) IUGR is present when fetal growth is restricted, most often in the presence of a raised blood pressure of the mother with an adverse effect on placental function. Due to these problems the pregnancy is often terminated prematurely and results in an infant who is small for gestational age. Although these infants are less often affected by respiratory problems, due to enhanced pulmonary maturation, or severe intracranial lesions, they are still at increased risk of an adverse neurodevelopmental outcome, especially with regard to their cognitive and behavioral skills.39,40 Recent MRIstudies have been able to show loss of hippocampal volume and altered cortical folding.41

The full-term newborn This review would not be complete without mentioning the full-term infant. In spite of improved obstetric care, neonatal encephalopathy is still common. Hypoxic-ischemic encephalopathy occurs in 3-9 per 1000 livebirths within hours to days after delivery, being moderate to severe in 3 per 1000 newborn infants. In the

Figure 3 Preterm infant, gestational age 25 weeks. Ultrasound, coronal view, performed at 3 days of age, shows large bilateral cerebellar haemorrhages as well as mild ventricular dilatation. The MRI (T2 weighted spinecho sequence) taken in a transverse plane at a lower level, shows the haemorrhagic lesions in more detail.


moderate to severe group, there is a 50% risk of either death or an adverse outcome. Hypothermia was recently shown to have a neuroprotective effect. Several randomized controlled trials have now shown that hypothermia is effective in reducing death and disability and significantly improves outcome without any disability.42,43 As there is no significant decrease over the last decades in the incidence of CP, in spite of improvement of obstetric care, it has been suggested that CP seen in children born at term is not often a result of ‘perinatal asphyxia’ but rather stems from problems already present before the onset of the delivery.44 Problems present before the onset of labor could make the infant more susceptible to any problem occurring during or around the time of delivery. It is also possible that an antenatal problem is not associated with symptoms at or soon after the delivery, but will only later develop symptoms, such as for instance CP and/or learning disabilities. Only developing cognitive deficits in the absence of CP is also possible following problems at or around delivery.45-47 When CP is noted to develop in the full-term infant with problems at or around the time of delivery, the type of CP is most likely BSCP or dyskinetic CP (DCP). MRI has played a crucial role in the understanding and recognition of different patterns of injury.48

Acute near total asphyxia Acute near total asphyxia is most often seen following an acute sentinel event, for instance a ruptured uterus, placental abruption or a prolapsed cord.49,50,51 Due to the high metabolic rate of the thalami and basal ganglia and perirolandic cortex at this stage of development, these areas will be a target for this pattern of injury.50 Using conventional MRI, it was first shown by Rutherford et al. that absence of a normal high-signal intensity of the posterior limb of the internal capsule (PLIC), indicative of normal early myelination is highly predictive of severe adverse sequelae.52 This change

in signal intensity of the PLIC is only seen from 48 to 72 hours onward. When MRI is performed early, another sequence, diffusion weighted imaging (DWI), will already show changes in the basal ganglia/thalami (BGT). Children with the BGT pattern of injury tend to be severely disabled due to DCP. Himmelmann et al. studied 48 children at a mean age of 9 years (range 4-13 years) with DCP mostly due to BGT injury and found that most children had Gross Motor Function Classification System levels of level IV (n = 10), and level V, (n = 28).53 The rate of learning disabilities (n = 35) and epilepsy (n = 30) increased with the severity of motor disability.

Watershed predominant pattern of injury (WS) This pattern of injury is the second most common pattern of injury which is also referred to as a pattern seen following ‘prolonged partial asphyxia’. The vascular watershed zones (anterior-middle cerebral artery and posterior-middle cerebral artery) are involved, affecting white matter and in more severely affected infants also the overlying cortex (figure 4). The lesions can be uni- or bilateral, posterior and/or anterior. Although loss of the cortical ribbon and therefore the grey-white matter differentiation can be seen on conventional MRI, DWI is able to highlight these abnormalities and is especially helpful in making an early diagnosis.54 A repeat MRI may show cystic evolution, but more often atrophy and gliotic changes will be recognized.55 It is not uncommon to find a history of decreased fetal movements and it is also more common to see this type of injury after hypotension, infection and hypoglycaemia, all of which may be associated with a more protracted course.56 Neurological manifestations at birth may be mild and do not always meet the strict criteria for perinatal asphyxia and the onset of neurological signs can be delayed.57 Severe motor impairment is uncommon in this group of infants, but mild BSCP can develop. They are often considered to have an early normal outcome, when seen at 12-18 months. However, when seen up till early childhood suboptimal head growth, behavioral problems and delay in

Figure 4 Full-term infant with seizures and neonatal encephalopathy. MRI performed during the first week, shows signal intensity changes in the corpus callosum and frontal white matter, which are easier to recognize on diffusion weighted image (right) than on the T2 weighted sequence (left).


Figure 5 Full-term infant presenting with hemiconvulsions. MRI performed within the first week (a, b) after seizure onset shows a large left-sided infarct in the territory of the middle cerebral artery. a Inversion recovery sequence. b Diffusion weighted image, both on the neonatal as well as on the 3 month MRI. c Inversion recovery sequence, performed at 3 months, shows a large area of cavitation. Note that there is no myelin at the level of the posterior limb of the internal capsule. language are common.58,59 Miller et al. were the first investigators who were able to recognize cognitive deficits associated with the watershed pattern of injury at 30 months, while the problems were largely overlooked when seen at 12 months.60 More recently, they also showed a correlation with verbal IQ at 4 years of age.59 In a recent study, children were assessed at 9-10 years of age following mild to moderate encephalopathy and were found to be at increased risk of learning disabilities with more than 20% of these children, who did not develop CP, requiring special education.46 Symptomatic parieto-occipital epilepsy may occur later in childhood, often associated with reduced intelligence quotients and visuospatial cognitive functions.61

Neonatal stroke Neonatal stroke, involving the territory of one of the main cerebral arteries, but usually the territory of the left middle cerebral artery. While it was recognized in about 1/4000 livebirths, more recent studies report an incidence of 1/2500 newborn infants, presenting with neonatal encephalopathy and/or seizures. The higher incidence is most likely due to a lower threshold to perform MRI in newborn infants with seizures. These infants tend to present on day 1-2 with hemiconvulsions and, although not often associated with severe perinatal asphyxia, a more complicated obstetric history is often present, with a history of abnormal cardiotocography, an instrumental delivery or an emergency caesarean section.62 MRI is by far superior in making an early and appropriate diagnosis, compared with cranial ultrasound (figure 5). DWI is even better and will be able to show the lesion within hours after it’s onset. This sequence has also been shown to be very helpful in the early prediction of later hemiplegia. When a change in signal intensity is seen within the descending corticospinal tracts (the PLIC and the cerebral peduncle), this is almost invariably associated with an abnormal motor development and is now referred to as ‘preWallerian degeneration’.63,64 True Wallerian degeneration will follow 6-12 weeks later and is then seen as delayed myelination at the level of the PLIC and atrophy of the affected cerebral peduncle.64 In about 30% of the infants who develop perinatal stroke subsequent development of a hemiplegia is seen. These infants are also at risk of developing behavioral problems, language delay and epilepsy.

Prevention and early intervention Preventing preterm birth would be the best way to reduce the number of newborn infants with haemorrhagic and ischaemic lesions, as these type of brain lesions tend to almost exclusively occur in this group of infants. Over the years there has been a significant increase in survival in very and extremely low birth weight infants, associated with a decrease in cystic PVL, one of the main determinants for later development of CP in the preterm infant. Improved antenatal care, with in utero referral and antenatal administration of corticosteroids to improve lung maturation has played an important role. Care of the extremely low birth weight infant is also very different compared with care given 20 years ago. Surfactant can be given to facilitate and shorten the period of ventilatory support; more effective methods, other than artificial ventilation, like continuous positive airway pressure, can help to maintain spontaneous ventilation and more routine insertion of arterial lines allows better blood pressure control as well as maintaining CO2 levels within the normal range. More attention is now also paid to providing individualized care when the preterm infant is nursed in the neonatal intensive care unit (Newborn Individualized Developmental Care and Assessment Program [NIDCAP]). The aim is to reduce stress in the infant and improving the infant’s development by improving the bond between mother and child at an early stage. There is now some proof that at least short term outcome can be improved by NIDCAP.65 Since neuro-imaging and especially sophisticated MRI techniques are used around term equivalent age, we are now better able to predict which infant may benefit from early intervention following discharge home.66,67 For the full-term infant, hypothermia (33.5 ºC, for 72 h) can be used to provide neuroprotection. There is however a therapeutic window of only 6 hours and it is still a challenge to refer the infants early enough, to start cooling within this time frame.

Discussion Improvement in visualizing the neonatal brain has had an enormous impact on neonatal intensive care. We have now become to realize that survival of a newborn infant, admitted to


a NICU, is only the beginning of success, while intact survival is the real aim. While the lower limit of viability has come down to 23 weeks gestation, survival rates are still increasing and major handicaps are coming down in some centres, which can be mainly attributed to a decrease in incidence of cystic PVL. Sophisticated MRI technologies will help us further in understanding how the brain of a very preterm infant will try to adjust and show a different development, with changes in volumes of certain regions and differences in connectivity. By improving our understanding, we may be able to intervene in a more specific way and ultimately further improve long term outcome.

history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics. 2006;118:536-48. 19 Ment LR, Hirtz D, Hüppi PS. Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol. 2009;8(11):1042-55. 20 Dubois J, Benders M, Cachia A, et al. Mapping the early cortical folding process in the preterm newborn brain. Cereb Cortex. 2008;18:144-54. 21 Soria-Pastor S, Padilla N, Zubiaurre-Elorza L, Ibarretxe-Bilbao N, Botet F, Costas-Moragas C, Falcon C, Bargallo N, Mercader JM, Junqué C. Decreased regional brain volume and cognitive impairment in preterm children at low risk. Pediatrics. 2009;124(6):e1161-70. 22 Inder TE, Warfield SK, Wang H, Hüppi PS, Volpe JJ. Abnormal cerebral structure is present at term in premature infants. Pediatrics. 2005;115:286-94. 23 Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung HY, Nosarti C, et al. Cerebellar growth and

References 1 Stichting perinatale registratie Nederland. Perinatale zorg in Nederland 2005. Utrecht: Stichting Perinatale Registratie Nederland; 2008. 2 Claas MJ, Bruinse HW, Heide-Jalving M van der, Termote JUM, Vries LS de. Changes in survival and neonatal morbidity in infants with a birth weight of 750 g or less. Neonatology. 2010; 98:278-88. 3 Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. 2008;371:261-9. 4 Larroque B, Ancel PY, Marret S, Marchand L, André M, Arnaud C, Pierrat V, Rozé JC, Messer J, Thiriez G, Burguet A, Picaud JC, Bréart G, Kaminski M; EPIPAGE Study group. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study. Lancet. 2008(8);371(9615):813-20. 5 Latal B. Prediction of neurodevelopmental outcome after preterm birth. Pediatr Neurol. 2009;40:413-9. 6 Groenendaal F, Termote JU, Heide-Jalving M van der, Haastert IC van, Vries LS de. Complications affecting preterm neonates from 1991 to 2006: what have we gained? Acta Paediatr. 2010;99:354-8. 7 Surman G, Hemming K, Platt MJ, Parkes J, Green A, Hutton J, et al. Children with cerebral palsy: severity and trends over time. Paediatr Perinat Epidemiol. 2009;23:513-21. 8 Robertson CM, Watt MJ, Yasui Y. Changes in the prevalence of cerebral palsy for children born very prematurely within a population-based program over 30 years. JAMA. 2007;297:2733-40. 9 Marlow N, Wolke D, Bracewell MA, Samara M; EPICure Study Group. Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med. 2005;352:9-19. 10 Johnson S, Fawke J, Hennessy E, Rowell V, Thomas S, Wolke D, Marlow N. Neurodevelopmental disability through 11 years of age in children born before 26 weeks of gestation. Pediatrics. 2009 Aug;124(2):e249-57. 11 Johnson S, Hennessy E, Smith R, Trikic R, Wolke D, Marlow N. Academic attainment and special educational needs in extremely preterm children at 11 years of age: the EPICure study. Arch Dis Child Fetal Neonatal Ed. 2009 Jul;94(4):F283-9. 12 Haastert IC van, Vries LS de, Helders PJM, Jongmans MJ, Gorter JW. Gross motor functional abilities in preterm children with cerebral palsy due to periventricular leukomalacia. DMCN. 2008;50:684-9. 13 Limperopoulos C, Benson CB, Bassan H, Disalvo DN, Kinnamon DD, Moore M, Ringer SA, Volpe JJ, du Plessis AJ. Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors. Pediatrics. 2005;116:717-24. 14 Steggerda SJ, Leijser LM, Wiggers-de Bruïne FT, Grond J van der, Walther FJ, Wezel-Meijler G van. Cerebellar injury in preterm infants: incidence and findings on US and MR images. Radiology. 2009 Jul;252(1):190-9. 15 Hamrick SE, Miller SP, Leonard C, Glidden DV, Goldstein R, Ramaswamy V, et al. Trends in severe brain injury and neurodevelopmental outcome in premature newborn infants: the role of cystic periventricular leukomalacia. J Pediatr. 2004;145:593-9. 16 Miller SP, Ferriero DM, Leonard C, Piecuch R, Glidden DV, Partridge JC, et al. Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr. 2005;147:609-16. 17 Vries LS de, Haastert IC van, Rademaker KJ, Koopman C, Groenendaal F. Ultrasound abnormalities preceding cerebral palsy in high-risk preterm infants. J Pediatr. 2004;144:815-20. 18 Dyet LE, Kennea N, Counsell SJ, Maalouf EF, Ajayi-Obe M, Duggan PJ, Harrison M, Allsop JM, Hajnal J, Herlihy AH, Edwards B, Laroche S, Cowan FM, Rutherford MA, Edwards AD. Natural


behavioural & neuropsychological outcome in preterm adolescents. Brain. 2008;131:1344-51. 24 Nosarti C, Giouroukou E, Healy E, et al. Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain. 2008;181:205-117. 25 Back S. Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment Retard Dev Disabil Res Rev. 2006;12(2):129-40. 26 Woodward LJ, Anderson PJ, Austin NC, Howard K, Inder TE. Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med. 2006;355:685-94. 27 Counsell SJ, Allsop JM, Harrison MC, Larkman DJ, Kennea NL, Kapellou O, Cowan FM, Hajnal JV, Edwards AD, Rutherford MA. Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics. 2003 Jul;112(1 Pt 1):1-7. 28 Boardman JP, Counsell SJ, Rueckert D, Kapellou O, Bhatia KK, Aljabar P, Hajnal J, Allsop JM, Rutherford MA, Edwards AD. Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. Neuroimage. 2006(1);32:70-8. 29 Shah DK, Doyle LW, Anderson PJ, Bear M, Daley AJ, Hunt RW, Inder TE. Adverse neurodevelopment in preterm infants with postnatal sepsis or necrotizing enterocolitis is mediated by white matter abnormalities on magnetic resonance imaging at term. J Pediatr. 2008;153:170-5. 30 Brouwer A, Groenendaal F, Haastert IL van, Rademaker K, Hanlo P, Vries L de. Neurodevelopmental outcome of preterm infants with severe intraventricular hemorrhage and therapy for post-hemorrhagic ventricular dilatation. J Pediatr. 2008;152:648-54. 31 Persson EK, Hagberg G, Uvebrant P. Hydrocephalus prevalence and outcome in a populationbased cohort of children born in 1989-1998. Acta Paediatr. 2005;94:726-32. 32 Roze E, Braeckel KN van, Veere CN van der, Maathuis CG, Martijn A, Bos AF. Functional outcome at school age of preterm infants with periventricular hemorrhagic infarction. Pediatrics. 2009 Jun;123(6):1493-500. 33 Sherlock RL, Synnes AR, Grunau RE, Holsti L, Hubber-Richard P, Johannesen D, Whitfield MF. Long-term outcome after neonatal intraparenchymal echodensities with porencephaly. Arch Dis Child Fetal Neonatal Ed. 2008;93:F127-131. 34 Staudt M, Grodd W, Gerloff C, Erb M, Stitz J, Krägeloh-Mann I. Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study. Brain. 2002;125(Pt 10):2222-37. 35 Northam G, Liegeois F, Chong K, Wyatt J, Baldweg T. Total brain white matter is a major determinant of IQ in preterm adolescents. In press Annals Neurol. 2010. 36 Eken P, Vries LS de, Graaf Y van der, Meiners LC, Nieuwenhuizen O van. Haemorrhagic ischaemic lesions of the neonatal brain: correlation between cerebral visual impairment, neurodevelopmental outcome and MRI in infancy. Dev Med Child Neurol. 1995;37:41-55. 37 Hout BM van den, Stiers P, Haers M, Schouw YT van der, Eken P, Vandenbussche E, Van Nieuwenhuizen O, Vries LS de. Visual perceptual impairment in 5.5 year old children with haemorrhagic/ischaemic lesions of perinatal origin. Dev Med Child Neurol. 2000:42:376-86. 38 Limperopoulos C, Bassan H, Gauvreau K, Robertson RL, Jr., Sullivan NR, Benson CB, et al. Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics. 2007;120:584-93. 39 Walker DM, Marlow N. Neurocognitive outcome following fetal growth restriction. Arch Dis Child Fetal Neonatal Ed. 2008;93:F322-5. 40 Claas MJ, Bruinse HW, Koopman C, Haastert IC van, Peelen LM, Vries LS de. 2-year neurodevelopmental outcome of preterm born children £ 750 g at birth. Arch Dis Child Fetal Neon Ed. June 7, Epub ahead of print. 41 Lodygensky GA, Seghier ML, Warfield SK, Tolsa CB, Sizonenko S, Lazeyras F, Hüppi PS. Intrauterine growth restriction affects the preterm infant’s hippocampus. Pediatr Res. 2008;63:438-43.

42 Gluckman P,Wyatt J, Azzopardi D, Ballard R, Edwards D, Ferriero D, et al. Selective head cooling with mild systemic hypothermia after neonatal encephalopathy: multicentre randomised trial. Lancet. 2005;365:663-70. 43 Edwards AD, Brocklehurst P, Gunn AJ, et al. Neurological outcome at 18 months of age after moderate hypothermia for perinatal hypoxic-ischaemic encephalaopthy: synthesis and metaanalysis of trial data. BMJ. 2010;340:c363. 44 Cowan F, Rutherford M, Groenendaal F, Eken P, Mercuri E, Bydder GM, Meiners LC, Dubowitz LMS, Vries LS de. Orgin and timing of brain lesions in tern infants with neonatal encephalopathy. Lancet. 2003;361:763-42. 45 Gonzalez FF, Miller SP. Does perinatal asphyxia impair cognitive function without cerebral palsy? Review. Arch Dis Child Fetal Neonatal Ed. 2006 Nov;91(6):F454-9. 46 Kooij BJM van, Handel M van, Nievelstein RAJ, Groenendaal F, Jongmans MJ, Vries LS de. Serial MRI and neurodevelopmental outcome in 9-10 year old children with neonatal encephalopathy. J Pediatr. 2010;157(2):221-7. 47 Miller SP, Ramaswamy V, Michelson D, Barkovich AJ, Holshouser B, Wycliffe N, et al. Patterns of brain injury in term neonatal encephalopathy. J Pediatr. 2005;146:453-60. 48 Vries LS de, Groenendaal F. Patterns of neonatal hypoxic-ischaemic brain injury. Neuroradiology. 2010;52(6):555-66. 49 Okereafor A, Allsop J, Counsell SJ, Fitzpatrick J, Azzopardi D, Rutherford MA, Cowan FM. Patterns of brain injury in neonates exposed to perinatal sentinel events. Pediatrics. 2008;121:906-14. 50 Pasternak JF, Gorey MT. The syndrome of acute near-total intrauterine asphyxia in the term infant. Pediatr Neurol. 1998;18:391-8. 51 Perlman JM. Intrapartum asphyxia and cerebral palsy: is there a link? Clin Perinatol. 2003;33:335-53. 52 Rutherford MA, Pennock JM, Counsell SJ, Mercuri E, Cowan FM, Dubowitz LM, et al. Abnormal magnetic resonance signal in the internal capsule predicts poor neurodevelopmental outcome in infants with hypoxic-ischemic encephalopathy. Pediatrics. 1998;102:323-8. 53 Himmelmann K, Hagberg G, Wiklund LM, Eek MN, Uvebrant P. Dyskinetic cerebral palsy: a population-based study of children born between 1991 and 1998. Dev Med Child Neurol. 2007;49:246-51. 54 Chau V, Poskitt KJ, Sargent MA, Lupton BA, Hill A, Roland E, Miller SP. Comparison of computer tomography and magnetic resonance imaging scans on the third day of life in term newborns with neonatal encephalopathy. Pediatrics. 2009;123:319-26. 55 Rutherford M, Pennock J, Schwieso J, Cowan F, Dubowitz L Hypoxic-ischaemic encephalopathy:

56 Burns C, Boardman J, Rutherford M, et al. Patterns of cerebral injury and neurodevelopmental outcome following symptomatic neonatal hypoglycaemia. Pediatrics. 2008;122:65-74. 57 Sato Y, Hayakawa M, Iwata O, Okumura A, Kato T, Hayakawa F, et al. Delayed neurological signs following isolated parasagittal injury in asphyxia at term. Eur J Paediatr Neurol. 2008;12:359-65. 58 Mercuri E, Ricci D, Cowan FM, Lessing D, Frisone MF, Haataja L, et al. Head growth in infants with hypoxic-ischemic encephalopathy: correlation with neonatal magnetic resonance imaging. Pediatrics. 2000;106:235-43. 59 Steinman KJ, Gorno-Tempini ML, Glidden DV, Kramer JH, Miller SP, Barkovich AJ, Ferriero DM. Neonatal watershed brain injury on magnetic resonance imaging correlates with verbal IQ at 4 years. Pediatrics. 2009;123:1025-30. 60 Miller SP, Ferriero NN, DM PJC, Glidden DV, Barnwell A, et al. Predictors of 30-month outcome after perinatal depression: role of proton MRS and socioeconomic factors. Pediatr Res. 2002;52:71-7. 61 Oguni H, Sugama M, Osawa M. Symptomatic parietooccipital epilepsy as sequela of perinatal asphyxia. Pediatr Neurol. 2008;38:345-52. 62 Cheong JL, Cowan FM. Neonatal arterial ischaemic stroke: obstetric issues. Semin Fetal Neonatal Med. 2009;14:267-71. 63 Vries LS de, Grond J van der, Haastert IC van, Groenendaal F. Prediction of outcome in newborn infants with arterial ischaemic stroke using diffusion-weighted magnetic resonance imaging. Neuropediatrics. 2005;36:12-20. 64 Kirton A, Shroff M, Visvanathan T, deVeber G. Quantified corticospinal tract diffusion restriction predicts neonatal stroke outcome. Stroke. 2007;38:974-80. 65 Als H, Duffy FH, McAnulty GB, Rivkin MJ, Vajapeyam S, Mulkern RV, Warfield SK, Huppi PS, Butler SC, Conneman N, Fischer C, Eichenwald EC. Early experience alters brain function and structure. Pediatrics. 2004;113:846-57. 66 Als H, Duffy FH, McAnulty GB, Rivkin MJ, Vajapeyam S, Mulkern RV, Warfield SK, Huppi PS, Butler SC, Conneman N, Fischer C, Eichenwald EC. Early experience alters brain function and structure. Pediatrics. 2004;113:846-57. 67 Blauw-Hospers CH, Graaf-Peters VB de, Dirks T, Bos AF, Hadders-Algra M. Does early intervention in infants at high risk for a developmental motor disorder improve motor and cognitive development? Neurosci Biobehav Rev. 2007;31(8):1201-12. 68 Koldewijn K, Wassenaer A van, Wolf MJ, Meijssen D, Houtzager B, Beelen A, Kok J, Nollet F.

early and late magnetic resonance imaging findings in relation to outcome. Arch Dis Child

A neurobehavioral intervention and assessment program in very low birth weight infants:

Fetal Neonatal Ed. 1996;75:F145-51.

outcome at 24 months. J Pediatr. 2010;156:359-65.


Developmental psychology, pediatric psychology and pediatric physical therapy: Joining forces in supporting children to develop ‘mens sana in corpore sano’ M.J. Jongmans Introduction We all know the Latin quotation ‘mens sana in corpore sano’. In fact, the whole line included in one of the satirical poems written by the Roman poet Juvenal is ‘orandum est ut sit mens sana in corpore sano’ and translates as ‘it is to be prayed that the mind be sound in a sound body’.A In context, the phrase is part of the poet’s answer to the question of what people should desire in life. Although the original connotation is that health of mind and body is good in itself and to be rightly desired (as opposed to beauty, wealth and power), its most general usage nowadays is to express the concept of a healthy balance in a person’s way of life. This quotation has survived for many centuries: why? While one could spend many hours debating its ‘true’ meaning (in the eye of the beholder, be it a poet, psychologist, doctor, philosopher, pediatric physical therapist or a lay person), the quotation apparently triggers something very recognizable to us all: human well-being and development depends on a healthy interplay between ‘mind and body’. When children are referred to a pediatric physical therapist, often the expectation is that the therapist focuses on the child’s ‘body’ in order to support an increase in motor functioning in every day life. However, as all therapists will recognize from their own experience, motor behavior is not a separate entity in a child’s life. Rather, all behavioral patterns of the child can best be understood, both in research and practice, by a systems-approach. In the most broad sense, a systems-oriented perspective assumes a reciprocal influence between the individual’s behavior and the behavior of other individuals within the system and the ecological environment in which it lives. Perhaps one of the most recognizable and broad conceptual models that illustrates a systems-oriented approach to child development is the social-ecological model of human development as proposed by Bronfenbrenner since the 1970s.1 The model conceives the ecological environment as a topologically nested arrangement of structures, each contained within the next (like Russian dolls). It is obvious that in order to assess movement restrictions in children and subsequently design and implement appropriate intervention strategies, the therapist therefore needs to draw from, and incorporate, knowledge from several other disciplines. In this paper, a personal selection of emerging trends within the past 25 years from two fields within psychology, each thought to have particular relevance for the field of pediatric physical therapy namely developmental psychology and pediatric psychology, will be highlighted. First, within the realm of developmental A D. Iunius Iuvenalis, Satura X, 365; http://www.thelatinlibrary.com/juvenal/10.shtml.


Marian J. Jongmans Human movement scientist, Health psychologist at the Department of Pediatric Psychology, University Medical Center Utrecht and Department of Special Education, Utrecht University, the Netherlands Correspondence E-mail: [email protected]

psychology probably one of the most influential theories is the dynamic systems theory. Several central concepts of this theory are presented, illustrated and its relevance for pediatric physical therapy practice outlined. Secondly, more practical, clinical issues and trends within the relative ‘young’ field of pediatric psychology focusing on a fruitful collaboration between physical therapists and psychologists in pediatric populations (i.e., children with a chronic illness) will be presented. The aim of this paper is to provoke and encourage ever more dialogue and collaboration among professionals in developmental psychology, pediatric psychology and pediatric physical therapy.

Developmental psychology - dynamic systems theory Unlike other theories of development, which try to explain changes in behavior by focusing on a single cause, dynamic systems theory emphasizes multicausality as the core of developmental change by considering the many, often nonobvious factors across all systems of life that influence development.2 As eloquently summarized by Spencer et al., looking back at the work of Thelen in her quest to develop a holistic dynamic systems theory of development, four central concepts can be distinguished.3 First, a new emphasis was placed on time: behavior emerges in the moment (‘on the spot’), but the effects of each behavioral decision accumulate over longer time scales, as each change sets the stage for future changes. Second, it is proposed that behavior is multidetermined from the nonlinear interactions of multiple subsystems. Thirdly, perception, action, and cognition form an integrated system that cannot be partitioned, called embodiment. Finally, a new respect for individuality emerged: development happens in individual children solving individual problems in their own unique ways.

Emerging behavior - time Following several longitudinal studies using frequent observations and experimental manipulations of infant stepping, kicking and reaching Thelen et al. drew the conclusion that behavior emerges in the moment from the self-organization of multiple components (often coined ‘soft-assembly’). The sophisticated stepping studies they conducted, which show how posture, strength of muscles, and the pull from the environment all combine in a moment in

time to create or hinder leg movements in infants illustrated this point beautifully. Further studies provided evidence that progress in early motor development is often characterized by nonlinearity, increasingly less stable behavior during periods of change and a tendency to shift to increasing organization. Throughout her career, Thelen was aware that translating the principles of dynamic systems theory in to clinical practice was important. With her research investments in building a conceptual model of development she wanted to inspire therapists to think differently about child development and the ways in which young children with motor disabilities could be supported to overcome barriers in their own unique pathway of motor development. In particular, Thelen’s early work on kicking, stepping, and walking sparked great interest among those studying and working with young children with motor disabilities including pediatric physical therapists. Examples of these are studies in infants with cerebral palsy, Down’s syndrome, and spina bifida.4,5,6 These translational efforts have been quite promising. By carefully controlling and manipulating the subsystems involved in, for instance, stepping behaviors, it was shown that the system can be pushed into new forms of organization and uncover control parameters – intrinsic or extrinsic – that give leverage to elicit behavioral change.

Developmental pathways and individual variation Moving on to studying goal-directed motor behavior, Thelen et al. conducted detailed studies of four infants in their attempts to learn to reach for and grasp objects in the first year of life. This revealed that different developmental pathways can lead to similar outcomes.7 However, and probably more important, the microgenetic approach applied in these studies proved to be invaluable in studying changes in development. Reasoning along the same lines, Adolph et al. have argued that in order to understand development, efforts should be geared towards understanding developmental change rather than describing children’s behavior and abilities at different ages.8 However, an accurate description of developmental pathways depends on the time scale the events are measured. Measurements in real time (e.g., milliseconds, seconds) converge to patterns that might be quite different from those that are based on measurements at macro time scales (e.g., days, months, years). Accurate, micro-genetic studies of developmental trajectories are therefore needed. The micro-genetic method refers to a sampling method at small time intervals during which researchers collect observations of important target behavior that span the entire period of change from one stable state to another. These sampling intervals should be small enough to detect the shape of the underlying pathways. Using statistical simulations from a set of 32 infant motor skills observed daily during the first 18 months the findings suggested that sampling rates typically used in developmental studies may be inadequate to accurately depict patterns of variability and the shape of developmental change. An important issue emerging from this work, which can be applied to the pediatric physical therapy setting, is that the emphasis should be on close, repeated observation of how children discover their own, individual, intrinsic movement characteristics to improve their functional motor skills over time. Moreover, this line of thinking seems an important catharsis in opening a new avenue in practice in which comparison of motor pathways of children with and without health conditions becomes less of a central issue. Instead, investigating differences between pathways of individual children with a similar health condition seems a more fruitful approach. However, large, prospective, longitudinal studies in this

area are not available yet. Examples of large cross-sectional studies on gross motor developmental status of children with Down syndrome and children born preterm show provisional evidence of the benefits of creating ‘intra-group’ growth curves in order to distinguish between children with expected or unexpected delays in motor development.9,10

Multidetermined behavior - embodied cognition Another result of the infant reaching studies by Thelen et al. was that when infants learn to reach they do so via exploring a range of possibilities and selecting viable solutions to meet the demands of the task. ‘In this achievement, body and mind come together as infants assemble the many components that make a reach: the biomechanics of the body, the details of the specific environment including the perceived location of the toy, the speed and force needed to extend the arms away from the body, the ongoing movement and postural context, and so on. This integration of body and mind is a fundamental characteristic of all goal-directed actions and creates a bridge to an embodied view of cognition and behavior...’.3 Indeed, as it was Thelen’s belief that there must be a ‘grand theory of development’ encompassing general principles of development irrespective of the content domain, she turned her attention to cognitive development of infants. One of the most natural starting points for this was Piaget’s question on how children move from the sensorimotor origins of thought to cognition. Point of departure to study this was the role of motor skill in the classic Piagetian A-not-B task. In this task infants watch while a toy is repeatedly hidden in one location (‘A’). Then, after a brief delay, infants are encouraged to retrieve the object from this hidden location. After several trials to this first location, infants watch while the toy is hidden in a different, nearby location (‘B’). Interestingly, almost without fail, 8- to 10-months-old infants will reach back to the original location ‘A’ after a short delay, that is they reach to ‘A’ and not to ‘B’. Thelen et al. looked for an explanation of this (from an adult perspective surprising) behavior taking the child’s motor actions as the starting point of their enquiries. They demonstrated, amongst many other things, that infant’s decision to reach to location ‘A’ or ‘B’ is influenced by the feel of the arms of the infants by putting weights on their arms throughout the entire task or parts of the task. In other words, what infants know (‘where is the hidden object?’) is always assembled, in the moment, with contributions from memory, attention and action.11 Moreover, Thelen (and her contemporaries) propagated the idea that cognition is embodied. The idea that action is a foundation for cognitive development, has been studied in parallel to Thelen’s efforts and since been elaborated and refined on by other developmental psychologists including Claus von Hofsten et al.12 In his words, actions reflects the motives of the child, the problems to be solved, the goals to be attained, and the constraints and possibilities of the child’s body and sensory-motor system. They are directed into the future and their control is based on knowledge of what is going to happen next. Indeed, the child’s sensory-motor system is especially designed to facilitate the extraction of this knowledge and the infant is endowed with motives that ensure that these innate predispositions are transformed into a system of knowledge for guiding actions. An exciting strand of research has shown that specific areas in the brain (mirror neuron systems) encode our own and other people’s actions in a similar fashion, and that this forms a base for the understanding of how the actions of others are


carried out as well as the goals and motives that drive them. The concept of embodied cognition might not, at a first superficial glance, seem of huge relevance to pediatric physical practice. How would the idea that children’s (perceptions of ) body movements relate to their ‘thinking’ (i.e., cognitive processes) help in supporting children with motor disabilities overcome their movement difficulties? However, when combined with the dynamic systems idea that effects of each behavioral decision accumulate over longer time scales, as each change sets the stage for future changes, the relevance becomes more clear. Early intertwined experiences in motor and cognitive demands in the environment of the child shape it’s future pathway. Pediatric psychology - childhood chronic illness practice ‘Pediatric psychology is a multifaceted and integrated field of both scientific research and clinical practice that focuses on addressing a wide range of physical and psychological issues related to promoting the health and development of children, adolescents, and their families, with an emphasis on evidence-based methods.’13 Although founded in the United States of America nearly 40 years ago, pediatric psychology is regarded as a relative ‘young’ field in psychology in general. Pediatric psychologists are mainly employed in hospital settings. Generally their role is to contribute to the alleviation of suffering, distress and disease management challenges in childhood illness. They provide a range of interventions such as, for example, addressing physical symptoms, helping to manage physical pain, teaching coping skills and serving as a liaison among the patient, the family and the medical team.14 Theoretical underpinnings of pediatric psychology are interdisciplinary and draw from clinical, developmental, social, cognitive, behavioral, counseling, community and school psychology. Services provided by the pediatric psychologist vary widely according to local circumstances. Whereas some psychologists provide assessment and guidance to a pediatrician colleague on a ‘case-by-case’ basis in the management of a circumscribed clinical problem with a specific patient, others take on a multifaceted role including educational and managerial tasks as part of a multidisciplinary team, or anything in between these two roles. A survey has shown that common referral questions to pediatric psychologists include requests for assisting a child in coping with physical illness/injury, improving treatment adherence, assessing and treating depression and anxiety, teaching pain management techniques, assistance with parent coping, helping with adjustment to a new medical diagnosis, and resolving family conflict.15 Research over the past 25 years in the field of pediatric psychology has grown fast with expansion in terms of illnesses studied and collaboration with other professionals in pediatric health care.B The current, 4th edition of the handbook of Pediatric Psychology contains psychological issues related to medical, developmental, behavioral and cognitive-affective conditions such as prematurity, asthma, cystic fibrosis, diabetes mellitus, oncology, central nervous system disorders (e.g., epilepsy and spina bifida), juvenile rheumatoid arthritis, cardiovascular disease, abdominal pain, obesity etcetera.16 Moreover, in keeping with the ‘rise’ of the social-ecological model in developmental science in general, also within the pediatric psychology community a clear shift has taking place from an individual approach toward health-related issues in B Readers interested in research conducted in this field are referred to the Journal of Pediatric Psychology.


children to a systems-approach including ways in which illness of the child affects all family members (i.e., parents and siblings).

Treatment adherence - the case of Cystic Fibrosis One area in which a joint professional effort from pediatric psychologists and pediatric physical therapists seems particularly relevant is that of treatment adherence: the extent to which a person’s behavior is consistent with healthcare recommendations. This is the case in those childhood chronic illnesses which require the child to adhere to physical therapy recommendations (e.g., exercising) in order to successfully participate in age-appropriate daily life activities such as going to school and engaging in social activities. Take, for example, the case of children and adolescents with cystic fibrosis (CF). Although it is unrealistic to expect patients with CF to comply with all subscribed treatments absolutely there is evidence that adherence is treatment specific. A recent study reports 38% daily compliance for physical therapy while 21% never practice physical therapy.17 Trajectories of adherence to airway clearance therapy (ACT) are reported as low (14%), medium (49%) or high (37%), with type of ACT as the only predictor.18 In young children (< 5 years) problems with physical therapy adherence are common. Moreover, their caregivers report symptoms of depression and harsh parenting is associated with internalizing problems of the child.19 Good convergence exists between parents and schoolaged children (6-13 years) regarding overall adherence.20 Barriers to support treatment adherence in their child for parents are related to time-consuming treatments (i.e., ACT), taking enzymes, forgetting, oppositional behaviors of the child, time management, side effects, nonoptimal patient-professional communication and treatment effectiveness perceptions. Adolescents often report forgetting/losing medications and being too busy to adhere to all recommended therapies. Attitudinal patterns in this age group include unintentional forgetting, feeling that following CF treatments results in less freedom, and believing it is acceptable to miss a treatment every few days or to miss treatments when busy.21 Nonadherence increases from 10 years onwards, peaking at around 16 years despite that, by age 15, youth complete almost 90% of treatments independently. Discrepancies exist in the literature regarding the presence of psychopathology in children/youths with CF, with some reporting no increase of adjustment difficulties or psychiatric co-morbity, while others report elevated rates of psychopathology, especially depression which negative effects adherence.22,23 Using a clinical interview, White showed anxiety disorders to be the most common in children/youths with CF.24 Although no difference in adherence was found between those with/without a psychiatric disorder, the presence of an anxiety disorder is related to greater reported adherence. In sum, as many pediatric physical therapists working with children with CF will recognize, psychosocial factors of the child and support-systems in its immediate environment influence adherence and vice versa. Although in general it is known that optimistic beliefs facilitate adherence while avoidance behaviors (which are amenable to change by means of behavioral therapy) are associated with nonadherence, little empirical evidence for this phenomena yet exists for improvements in adherence specific to ACT and exercise in CF.25 From the above it is needless to say that close collaboration between pediatric psychologists and pediatric physical therapists in setting (realistic) goals for treatment and motivating children and adolescents with CF (and their families) to adhere to physical therapy recommendations is needed both in research and practice.

Managing pain - the case of juvenile idiopathic arthritis Another area particularly worth highlighting here is that of managing pain in children and adolescents within pediatric health care.26 Pain is considered to be ‘chronic’ and/or ‘recurrent’ when it persists for 3-6 months, either continuously (chronic pain) or intermittently (recurrent pain). Despite major advances in medical treatments, one major pediatric population affected by chronic or recurrent pain conditions are children and adolescents with juvenile idiopathic arthritis (JIA). Pain has been shown to be a primary determinant of the physical, emotional, and social functioning in these children.27 Pediatric physical therapists often play an important role in managing JIA by offering treatment programs designed to increase mobility and physical fitness. The latter seems necessary, since research has shown that adolescents with JIA spend more time in bed and less time on moderate to rigorous physical activity compared to their healthy peers. Interestingly, low levels of physical activity seem not related to disease activity, and control over the disease does not restore previous physical activity levels. One possible explanation is that experienced levels of pain and discomfort when physically active in a period in which the disease is also active, results in patterns of (too much) inactivity even in periods when the disease itself is not active. Another psychological barrier related to reduced physical activity might involve anxiety toward a possible damaging effect of physical activity.28 Fortunately, an internet-based program for children with JIA (aged 8-12 years) directed at promoting physical activity in daily life (including addressing the issue of pain in one of the 17 weekly sessions) has shown good results in patients with low levels of physical activity.29 The pathogenesis of pain in children with rheumatic diseases is multifactorial, and disease treatment alone by means of medication or exercise is often not enough to alleviate it. Indeed, a growing body of research in JIA highlights the importance of environmental and cognitive behavioral influences in the pain experience of children in addition to the contribution of disease activity. These influences include factors innate in the child, such as emotional distress, daily stress, coping, and mood, and familial factors, such as parental psychological health, parental pain history, and the nature of family interactions.30 One of the specialists tools available to pediatric psychologists to assist in pain treatment is cognitive behavioral therapy (CBT). This is an umbrella term to include approaches to pain management that are designed to teach children and adolescents coping skills for controlling behavioral, cognitive, and physiologic responses to pain. CBT involves educating children about mechanisms by which pain messages are transmitted and perceived as well as the own role of the child in these processes. Children then are taught various pain-coping skills with guidance in applying the skills in difficult situations. Skills taught include decreasing cognitive responses to pain and relaxation strategies such as progressive muscle relaxation, distraction, and guided imagery. Finally, children are encouraged to anticipate situations in which they are likely to experience increased pain or difficulty managing pain and to plan strategies for handling these challenges. Two published studies have demonstrated (modest to large) improvements in selfreported pain ratings of children with chronic arthritis following CBT immediately after treatment and at 6-month follow-up.31,32 However, both studies have methodological shortcomings and therefore future studies are necessary to fully understand the role of CBT in the treatment of JIA. Nevertheless, research in many other disease populations supports its applicability.

Furthermore, parental responses to their child’s pain seem related to daily adjustment of children with JIA.33 The use of ‘protective’ pain responses by parents, i.e., responses characterized by high levels of attention or vigilance to pain, as well as responses that convey permission to avoid daily responsibilities because of pain, significantly predicted decreases in child activity and positive mood. Alarmingly, there was an even stronger inverse relationship between protective pain response and positive mood observed in children with higher than average disease severity. The use of ‘distracting’ responses by parents, i.e., responses that promote active coping efforts and refocus the child’s attention away from pain sensations, significantly predicted less child activity restrictions but only in children having higher disease severity. There also was an unexpected trend in which parental use of more distracting pain responses tended to be associated with lower child positive mood. These findings suggest the importance of incorporating parents into comprehensive pain management approaches.

The future - joining forces in multi-system approaches toward pediatric health care Much of the emphasis throughout this paper has been on ‘systems’ of one kind or another incorporated in both theory and practice of developmental and pediatric psychology from such diverse disciplines as natural sciences, social sciences and behavioral sciences itself. Undoubtedly, the main progress which has been made in the past 25 years relevant to pediatric physical therapy is the notion that a multi-systems approach is first and foremost needed in order to explain developmental change in (a)typical pathways of motor functioning at a theoretical level. Subsequently, a multi-systems approach is needed at a practical, clinical level to improve motor functioning in children with a motor disability or those experiencing physical limitations as a result of chronic illness. Given this multi-systems approach, what will the future bring in terms of progress made in the field of pediatric physical therapy? In analogy to a trend in which physical therapists increasingly incorporate psychological intervention techniques in their work with injured adult athletes,34 one such future scenario may be that pediatric physical therapists, given proper formal education and training, are increasing their capabilities in incorporating and providing psychological intervention techniques in their treatment programs (for an example see the earlier discussed internet-based treatment to increase physical activity in children with JIA.29 A maybe less extreme crossing of boundaries of disciplines (and therefore less threatening in the eyes of some and therefore more plausible, future scenario) lies in the nature of collaborations between professionals. Whereas the past 25 years have witnessed an increase in multidisciplinary and/or interdisciplinary collaboration in pediatric health care, the next (logical) step might be moving toward transdisciplinary collaboration in order to improve the quality of service to children and their families even further. Transdisciplinary implies a level of integration and synergy that blurs the lines between discipline-specific knowledge and methods in such a way that the resulting outcome is unique and not discernable from a single discipline’s perspective.35 For example, in a pediatric clinical setting, psychologists and physical therapists determine and agree upon the best treatment approach in re-activating an adolescent with JIA given the psychological and physical make-up of the child and the environmental system (i.e., family and other sources of social support) surrounding it.


Although establishing ‘real’ links between professionals from different disciplines in providing such care remains quite a challenge, plenty of initiatives have emerged over the past years either at an individual (professional-to-professional contact in the clinical setting) or organizational level (e.g., psychologists and pediatric physical therapists exchanging information and inspiring each other at conferences). As such, collaboration between individuals involved in clinical, research or educational activities, or among large organizations with different perspectives and memberships create exciting opportunities. Likewise, the development of theories and conceptual models incorporating contributions from a developmental psychology, pediatric psychology and pediatric physical therapy perspective are likely to lead not only to new insights but, ultimately, also to better service provision. Therefore, how else to end this plea than to call for joining forces in order to support children to develop ‘mens sana in corpore sano’.

15 Carter BD, Kronenberger WG, Baker J, Grimes LM, Crabtree VM, Smith C, et al. Inpatient pediatric consultation-liaison: A case-controlled study. J Pediatr Psychol. 2003;28(6):423-32. 16 Handbook of pediatric psychology. New York: The Guilford Press; 2009. 17 Arias Llorente RP, Bousono Garcia C, Diaz Martin JJ. Treatment compliance in children and adults with cystic fibrosis. J Cyst Fibros. 2008 Sep;7(5):359-67. 18 Modi AC, Cassedy AE, Quittner AL, Accurso F, Sontag M, Koenig JM, et al. Trajectories of adherence to airway clearance therapy for patients with cystic fibrosis. J Pediatr Psychol. 2010 Mar 18. Epub ahead of print. 19 Ward C, Massie J, Glazner J, Sheehan J, Canterford L, Armstrong D, et al. Problem behaviours and parenting in preschool children with cystic fibrosis. Arch Dis Child. 2009 May;94(5):341-7. 20 Modi AC, Lim CS, Yu N, Geller D, Wagner MH, Quittner AL. A multi-method assessment of treatment adherence for children with cystic fibrosis. J Cyst Fibros. 2006 Aug;5(3):177-85. 21 Dziuban EJ, Saab-Abazeed L, Chaudhry SR, Streetman DS, Nasr SZ. Identifying barriers to treatment adherence and related attitudinal patterns in adolescents with cystic fibrosis. Pediatr Pulmonol. 2010 May;45(5):450-8. 22 Quittner AL, Barker DH, Snell C, Grimley ME, Marciel K, Cruz I. Prevalence and impact of

References 1 Bronfenbrenner U. Toward an experimental ecology of human development. Am Psychol. 1977;32(7):513-31. 2 Thelen E, Smith LB. A dynamic systems approach to the development of cognition and action. Cambridge: The MIT Press; 1994. 3 Spencer JP, Clearfield M, Corbetta D, Ulrich B, Buchanan P, Schöner G. Moving toward a grand theory of development: in memory of Esther Thelen. Child Dev. 2006;77(6):1521-38. 4 Angulo-Barroso RM, Tiernan CW, Chen L-, Ulrich D, Neary H. Treadmill responses and physical activity levels of infants at risk for neuromotor delay. Pediatric Physical Therapy. 2010;22(1):61-8. 5 Ulrich DA, Lloyd MC, Tiernan CW, Looper JE, Angulo-Barroso RM. Effects of intensity of treadmill training on developmental outcomes and stepping in infants with Down syndrome: A randomized trial. Phys Ther. 2008;88(1):114-22. 6 Teulier C, Smith BA, Kubo M, Chang C-, Moerchen V, Murazko K, et al. Stepping responses of infants with myelomeningocele when supported on a motorized treadmill. Phys Ther. 2009;89(1):60-72. 7 Thelen E, Corbetta D, Spencer JP. Development of reaching during the first year: Role of movement speed. J Exp Psychol Hum Percept Perform. 1996;22(5):1059-76. 8 Adolph KE, Robinson SR, Young JW, Gill-Alvarez F. What is the shape of developmental change? Psychol Rev. 2008;115(3):527-43. 9 Palisano RJ, Walter SD, Russell DJ, Rosenbaum PL, Gémus M, Galuppi BE, et al. Gross motor function of children with Down syndrome: Creation of motor growth curves. Arch Phys Med Rehabil. 2001;82(4):494-500. 10 Haastert IC van, Vries LS de, Helders PJM, Jongmans MJ. Early gross motor development of preterm infants according to the Alberta Infant Motor Scale. J Pediatr. 2006;149(5):617-22. 11 Thelen E. Motor development as foundation and future of developmental psychology. Int J Behav Dev. 2000;24(4):385-97. 12 Von Hofsten C. Action, the foundation for cognitive development. Scand J Psychol. 2009 Dec;50(6):617-23. 13 Aylward BS, Bender JA, Graves MM, Roberts MC. Historical developments and trends in pediatric psychology. In: Roberts MC, Steele RG, editors. Handbook of pediatric psychology. 4th ed. New York: The Guilford Press; 2009. p. 3-18. 14 Carter BD, Kronenberger WG, Scott E, Ernst MM. Inpatient pediatric consultation-liaison. In: Roberts MC, Steele RG, editors. Issues in Clinical Child Psychology, 4th ed. New York: The Guilford Press; 2009. p. 114-129.


depression in cystic fibrosis. Curr Opin Pulm Med. 2008 Nov;14(6):582-8. 23 Cruz I, Marciel KK, Quittner AL, Schechter MS. Anxiety and depression in cystic fibrosis. Semin Respir Crit Care Med. 2009 Oct;30(5):569-78. 24 White T, Miller J, Smith GL, McMahon WM. Adherence and psychopathology in children and adolescents with cystic fibrosis. Eur Child Adolesc Psychiatry. 2009 Feb;18(2):96-104. 25 Duff AJ, Latchford GJ. Motivational interviewing for adherence problems in cystic fibrosis. Pediatr Pulmonol. 2010 Mar;45(3):211-20. 26 Dahlquist LM, Nagel MS. Chronic and recurrent pain. In: Roberts MC, Steele RG, editors. Handbook of pediatric psychology. 4th ed. New York: The Guilford Press; 2009. p. 153-170. 27 Gutiérrez-Suárez R, Pistorio A, Cespedes Cruz A, Norambuena X, Flato B, Rumba I, et al. Health-related quality of life of patients with juvenile idiopathic arthritis coming from 3 different geographic areas. The PRINTO multinational quality of life cohort study. Rheumatology. 2007;46(2):314-20. 28 Lelieveld OTHM, Armbrust W, Leeuwen MA van, Duppen N, Geertzen JHB, Sauer PJJ, et al. Physical activity in adolescents with juvenile idiopathic arthritis. Arthritis Care Res. 2008;59(10):1379-84. 29 Lelieveld OTHM, Armbrust W, Geertzen JHB, Graaf I de, Leeuwen MA van, Sauer PJJ, et al. Promoting physical activity in children with juvenile idiopathic arthritis through an internet-based program: Results of a pilot randomized controlled trial. Arthritis Care Res. 2010;62(5):697-703. 30 Anthony KK, Schanberg LE. Pediatric pain syndromes and management of pain in children and adolescents with rheumatic disease. Pediatr Clin North Am. 2005;52(2):611-39. 31 Lavigne JV, Ross CK, Berry SL, Hayford JR, Pachman LM. Evaluation of a psychological treatment package for treating pain in juvenile rheumatoid arthritis. Arthritis Care Res. 1992;5(2):101-10. 32 Walco GA, Varni JW, Ilowite NT. Cognitive-behavioral pain management in children with juvenile rheumatoid arthritis. Pediatrics. 1992;89(6):1075-107. 33 Connelly M, Anthony KK, Sarniak R, Bromberg MH, Gil KM, Schanberg LE. Parent pain responses as predictors of daily activities and mood in children with juvenile idiopathic arthritis: the utility of electronic diaries. J Pain Symptom Manage. 2010 Mar;39(3):579-90. 34 Arvinen-Barrow M, Penny G, Hemmings B, Corr S. UK chartered physiotherapists’ personal experiences in using psychological interventions with injured athletes: An Interpretative Phenomenological Analysis. Psychol Sport Exerc. 2010;11(1):58-66. 35 Armstrong FD, Reaman GH. Psychological research in childhood cancer: The Children’s Oncology Group perspective. J Pediatr Psychol. 2005;30(1):89-97.

Scientific progress in pediatric physical therapy: 1985-2010 S.R. Harris

Susan R. Harris, PhD, PT, FAPTA, FCAHS Professor Emerita of Physical Therapy, Department of Physical Therapy, University of British Columbia, Wesbrook Mall, Vancouver, Canada

Introduction Pediatric physical therapists have much to celebrate based on the amazing scientific development of our specialty area and the many contributions made by our research colleagues over the past quarter-century. Tracing the history of scientific progress in pediatric physical therapy (PT) over the past 25 years is an exciting but formidable challenge! Where does one begin? How should such a paper be organized to be of maximal benefit to the entire pediatric physical therapists audience: clinicians, educators, and researchers? This paper will focus first on two international initiatives that have changed the face of health care practice, including pediatric PT, over the past 25 years: the World Health Organization’s International Classification of Functioning, Disability and Health1 and the move toward evidence-based practice (EBP), including the advent of systematic reviews that have synthesized the efficacy of various pediatric PT interventions. Systematic reviews involving pediatric therapy interventions will be highlighted including descriptions of two databases helpful in locating these invaluable resources for clinical decision making. Next, an important classification strategy for categorizing children with cerebral palsy (CP) based on functional performance will be described, followed by a summary of measurement tools developed by pediatric physical therapists and their colleagues. Finally, future directions in scientific development in pediatric PT will be highlighted.

International Classification of Functioning, Disability and Health Introduced in 2002, the World Health Organization’s (WHO) International Classification of Functioning, Disability and Health (ICF) has had a major impact on how disability is viewed worldwide – not only by clinicians but also by researchers, educators, health care policy makers, disability advocates, and consumers.1 The key terms in this document are functioning and disability, both overarching concepts with the former referring to body functions, activity and participation and the latter to impairments, activity limitations, and participation restrictions.1 (p 2) The ICF model of disability is referred to as a biopsychosocial model, viewing health from biological, individual, and social perspectives.1 (p 9) This model represents a marked departure from the medical model, in which so many of us were trained, and which called upon us as clinicians to ‘correct’ the individual’s disability through our own interventions. Instead of focusing on ‘fixing’ the child’s impairments with interventions aimed at normalizing the quality of their movement patterns2 or minimizing progression of joint contractures,3 for example, the ICF model encourages us to move away from therapy goals directed at impairments and turn our direction toward enhancing the child’s activity (execution of specific tasks or actions) and participation (involvement in real-life situations).1 (p 10) This shift in focus of therapy goals toward activity and participation was exemplified very nicely in a 2001 randomized controlled

Correspondence E-mail: [email protected]

trial by Ketelaar et al. in which the authors examined the relative effects of a functional PT approach, aimed at practicing and enhancing functional activities within natural environments, and an impairment-based approach, aimed at normalizing quality of movement.4 Study participants were 55 young Dutch children (ages 2 to 7 years) with mild or moderate spastic CP. The authors provided an example of a child who lives on a farm but who falls repeatedly when walking on uneven surfaces. Because the child likes to walk in the stables, which have uneven surfaces, the goal developed for him (as part of the functional PT approach) was ‘to walk in and around the stables without falling’.4 (p 1539) This goal represents a perfect example of enhancing the child’s participation in real-life situations, a focus encouraged within the ICF model.1 The Ketelaar et al. study will be highlighted several times within this article to exemplify different key points in our scientific development over the past 25 years. In 2007, WHO published a version of the ICF aimed specifically at children and adolescents: the ICF-Children and Youth (ICF-CY),5 with renewed emphasis on ‘participation in everyday life situations’.6 (p 670) In a recent mixed-methods study exploring how Swedish pediatric practitioners working on interdisciplinary teams perceived the implementation of the ICF-CY, Adolfsson et al. reported that the framework enhanced practitioners’ awareness of family viewpoints on child participation in everyday life and fostered a more equal partnership between professionals and families, by viewing parents as experts in decision making and goal-setting for their children.6 Publication of the ICF and the ICF-CY during the past decade has helped enormously to shift the focus of pediatric PT toward familyand child-centered goals aimed at fostering activity and participation rather than goals aimed solely at impairment-level outcomes. As Damiano commented: ‘functional-based training is likely to be far more relevant, and therefore more motivating, for patients and clients who rarely state their goals in terms of impairment… but are concerned instead with promoting activity or participation to enhance their daily lives.’7 (p 329)

Evidence-based practice In the mid-1990s, the Evidence-Based Working Group at McMaster University in Canada published a seminal series of articles in The Journal of the American Medical Association (JAMA) on how physicians could critically appraise research articles to guide their practice in caring for patients.8-12 As a result, evidence-based practice (EBP) has become the cornerstone on which all health care professionals are encouraged to base their diagnoses, prognoses, and therapeutic interventions. During that same time period, this article’s author


published a professional perspective in Physical Therapy on how therapy interventions should be critiqued for scientific merit.13 Included among the criteria for evaluating the scientific merit of an intervention was the need for peer-reviewed experimental studies of that therapy approach, studies that included standardized and welldefined intervention techniques and objective and reliable outcome measures.13 Although evidence-based medicine was defined in 1996 by Sackett et al. as ‘the conscientious, explicit, and judicious use of current best evidence in making decisions about the care of individual patients’,14 (p 71) thus focusing primarily on research evidence, this definition was expanded in 2000 to integrate clinical expertise and patient values along with the best research evidence.15 Turning again to the study by Ketelaar et al. as an example, patient values were nicely incorporated into the functional approach to PT by including parent/ child goals that were ‘meaningful in the child’s environment and perceived as problematic by either the child or the parents’.4 (p 1536) For readers who are interested in more comprehensive descriptions of EBP use in pediatrics and pediatric rehabilitation, please see review articles by Kersten et al.16 and O’Donnell and Roxborough.17 Concurrent with the move toward EBP was the introduction of methodologies for synthesizing the available research evidence related to a specific research question: the systematic review and the meta-analysis. The move toward critically evaluating and synthesizing available research evidence took a giant step forward in 1993 with the establishment of the Cochrane Collaboration. In the following sections, these advancements will be described in further detail with specific examples provided in pediatric rehabilitation.

Systematic reviews Greenhalgh defined a systematic review as ‘an overview of primary studies which contains an explicit statement of objectives, materials, and methods and has been conducted according to explicit and reproducible methodology’;18 (p 672) a meta-analysis or quantitative synthesis goes a step further by statistically pooling the effects across separate studies to examine combined effect sizes. The advent of using these procedures in pediatric therapy occurred in 1986 with the publication of a meta-analysis on the effectiveness of the neurodevelopmental treatment (NDT) approach for children with developmental disabilities.19 Nine previous studies met the inclusion criteria for that first systematic review. Since that seminal metaanalysis was published, at least a half-dozen other English-language systematic reviews examining the effects of NDT (and other therapies) for children with CP and other developmental disabilities have been published.20-26 One freely available resource for locating systematic reviews in PT is the Physiotherapy Evidence Database or PEDro, maintained by the Centre for Evidence-Based Physiotherapy at The University of Sydney in Australia.27 The PEDro website includes 23 additional systematic reviews related to pediatric therapy that have been published in the 25 years since the Ottenbacher et al. quantitative analysis was published.19 Topics for these reviews have included the effects of treadmill training for children involved in rehabilitation,28,29 the effects of adaptive seating on postural control30,31 and upper extremity function,32 and the effects of various types of strengthening interventions for children with CP33-35 and those with meningomyelocele.36 Other systematic reviews have been published on complementary therapy approaches, such as the effects of therapeutic horseback riding for children with CP37 and the therapeutic effects of yoga for typical children and children with asthma.38


Not surprisingly, the majority of these systematic reviews (approximately 60%) have appeared in the two peer-reviewed journals that focus on pediatric therapy: Pediatric Physical Therapy and Physical & Occupational Therapy in Pediatrics.

Cochrane Collaboration Established in 1993, the Cochrane Collaboration is an international network of health care researchers and others who work in an interdisciplinary fashion to develop systematic reviews based on the best available evidence.39 The goal of the Cochrane Collaboration is to assist health care providers, policy makers, clients and their families to make informed decisions about health care. Thus far, more than 4000 reviews have been published online in The Cochrane Library. Cochrane reviews enable clinicians to determine if an intervention is effective for certain types of clients within a specific clinical context. As well, clients and their families can assess the risks and benefits of prescribed interventions. Ideally, these reviews are updated every few years. As of July 2010, there were 45 reviews or protocols for reviews in progress on the Cochrane website that relate to . Intervention reviews that would be of interest specifically to pediatric physical therapists included the use of bolulinum toxin type A in the treatment of spasticity,40,41 constraint-induced movement therapy for children with hemiplegic CP,42 and the effects of early intervention programs for preterm infants.43 Protocols are in progress on muscle strengthening for children and adults with CP,44 and the use of baclofen in the management of spasticity.45,46 Although there is a protocol in progress for evaluating the effects of occupational therapy for children with CP,47 there is no comparable protocol for PT, unfortunately. In spite of the number of Cochrane reviews related to CP, there are no reviews or protocols in progress using the key words ‘spina bifida’ (or meningomyelocele) and only five related to ‘Duchenne muscular dystrophy’, two fairly prevalent disorders in pediatric PT. None of the intervention reviews for Duchenne muscular dystrophy relate to PT. Although there are 17 reviews or protocols in progress relating to Down syndrome, only 1 review focuses on exercise and that relates to adults with Down syndrome.48 Of 13 reviews or protocols in autism, there are none related to PT but 1 about parentmediated early intervention for young children with autism spectrum disorder.49 With regard to developmental coordination disorder (DCD), there are no completed Cochrane reviews but 1 intervention protocol in progress on occupational therapy and PT for children with DCD.50 As far as childhood musculoskeletal disorders, there is 1 intervention review on exercise in juvenile idiopathic arthritis51 and 1 on bracing for idiopathic scoliosis.52 All 4 reviews related to treatment of torticollis focused exclusively on botulinum toxins with none related to PT interventions. With regard to respiratory diseases for which pediatric physical therapists frequently provide intervention, none of the 13 reviews related to childhood asthma focused on PT, but primarily on drug therapies for asthma. Of the 109 Cochrane reviews or protocols on cystic fibrosis (CF), most were again related to drug interventions although there is 1 review on the effects of physical training for children and adults with CF,53 1 on inspiratory muscle training,54 and 3 on chest PT.55-57

Summary of systematic reviews It is disappointing that so few of the 4000 Cochrane reviews

Intervention

First author (year)

Number of studies meeting inclusion criteria

Participant characteristics

Outcomes

Authors’ conclusions

adaptive seating in CP

Chung31 (2008)

14

n = 176 (174 with CP); age range = 12 months to 20.8 years

sitting posture, postural control

significant improvements with seat inserts, external supports, and modular seating systems

botulinum toxin A (and OT) in spastic CP

Hoare41 (2010)

10 (all RCT)

n = 329 with spastic CP; age range = 22 months to 16 years

spasticity and function in upper extremities

high level evidence for botulinum toxin A as adjunct to managing UE spasticity; should be accompanied by planned OT

bracing for idiopathic scoliosis

Negrini52 (2010)

2 (1 RCT)

n = 329 adolescent girls

progression of scoliotic curve

low quality evidence in favor of using braces

chest physical therapy in CF

Main56 (2005)

15 (all RCT or quasi-RCT)

n = 475 with cystic fibrosis (mean ages: 9 to 25 years)

respiratory function

no advantage of conventional chest physical therapy over other airway clearance techniques

constraint-induced movement therapy in spastic CP

Hoare42 (2007)

3 (1 RCT)

n = 90 with hemiplegic CP; age range = 7 months to 8 years

spontaneous use of affected upper extremity

significant treatment effect in 1 trial; CIMT should be considered experimental in children with hemiplegic CP

early intervention for preterm infants

Spittle43 (2007)

16 (12 RCT)

n = 2379 preterm infants

motor and cognitive development at infancy, preschool, or school age

improved cognitive outcomes through preschool age

exercise therapy in JIA

Takken51 (2008)

3 (all RCT)

n = 212 with JIA; age range = 4-19 years

functional ability, QOL, aerobic capacity, pain

no clinically important or statistically significant evidence that exercise therapy improves functional ability, quality of life, aerobic capacity or pain

inspiratory muscle training for CF

Houston54 (2008)


n = 140 with CF; age range = 6-34 years

health-related QOL, pulmonary function, exercise tolerance

no evidence that treatment is or is not beneficial

physical training for CF

Bradley53 (2008)


n = 231 (adolescents and young adults)

exercise capacity, strength, lung function

limited evidence that aerobic or anaerobic physical training has positive effect on exercise capacity, strength and lung function (improvements not consistent across studies)

strengthening interventions (electrical stimulation, exercise training, motor skills training)

Dagenais36 (2009)

6

n = 29 children with MM; age range = 4-21 years

strength, cardiovascular endurance, independence in motor skills, timed functional tasks, wheelchair propulsion, self-concept; GM and FM function

strength improved across all 6 studies but most usen designs with low levels of evidence

therapeutic horseback riding in CP

Snider37 (2007)

9 (3 RCT)

n = 99 children with CP; age range = 2.3-12 years

posture / postural reactions, muscle symmetry, gross motor function, energy expenditure, socialization

short-term effects on muscle symmetry in trunk and hips; improved gross motor function

treadmill training with body weight support

Damiano28 (2009)

29 (1 RCT)

CP and other CNS disorders (n=114), DS infants (n = 45), children and young adults with SCI (n = 7)

gait improvement

demonstrated efficacy in DS infants; weak evidence in CP; insufficient information in SCI

Table 1 Examples of systematic reviews of intervention studies for children. CIMT: constraint-induced movement therapy; CF: cystic fibrosis; CNS: central nervous system; CP: cerebral palsy; DS: Down syndrome; FM: fine motor; GM: gross motor; JIA: juvenile idiopathic arthritis; MM: meningomyelocele; OT: occupational therapy; PT: physical therapy; RCT: randomized controlled trial; SCI: spinal cord injury. focus on interventions provided by pediatric physical therapists. However, the responsibility for being involved in the development and completion of such reviews belongs to all of us. Especially needed are systematic reviews of interventions for developmental disabilities other than CP, in that there are children with many other types of disabilities represented in our clinical caseloads. Table 1 summarizes some examples of systematic reviews of various pediatric therapy interventions. These examples were selected based on being recent and/or representative of a variety of different interventions, but not all systematic reviews cited

in this article have been included. Readers should be aware that systematic reviews on the same intervention can provide conflicting results depending upon how the intervention is operationally defined, what types of study designs are included, and how the data are analyzed, i.e., qualitative systematic review vs. metaanalysis. In 2 recent systematic reviews on muscle strengthening for children and adolescents with CP, for example, 1 review showed positive effects on gait, strength and function34 whereas the second suggests that strengthening interventions ‘are neither effective nor worthwhile’.35 (p 81) Pediatric PT clinicians should read these


papers themselves to determine similarities or differences between the samples studied, the specific interventions provided, and the characteristics (age range, diagnoses) of children within their own caseloads.

Classification and measurement tools developed by pediatric physical therapists During the past 25 years, we have seen a number of important advances in measurement by pediatric physical therapists, either as lead authors of tools or classification systems or as members of interdisciplinary teams of authors. Certainly, one of the most important classification systems that has been developed and is used wforldwide is the Gross Motor Function Classification System (GMFCS), developed by Palisano et al. to classify gross motor abilities and functional limitations of children with CP into five different levels.58 Since the system was first described in 1997, more than 250 articles have been published in which the GMFCS has been used in research involving children with CP or other developmental disabilities. Recently, the GMFCS was expanded and revised (GMFCS-E&R) to develop a 12- to 18-year age band and to revise the original 6- to 12-year age band.59 A further purpose of these revisions was to broaden the conceptual framework of the system to be more congruent with the ICF. These landmark contributions (GMFCS and GMFCS-E&R) by Palisano et al. have shifted the categorization of CP solely as a medical diagnosis to a far more meaningful classification system based on the child’s functional abilities. To set the stage for discussing specific measurement tools developed by pediatric physical therapists, either as primary authors or as members of interdisciplinary teams, the now classic paper on issues in measurement in CP provides a useful framework.60 Using the framework developed by Kirshner and Guyatt, Rosenbaum et al. applied this to measures related to CP.61 A discriminative index (or measure) is designed to differentiate between children who do or do not have a specific characteristic or behavior, e.g., motor delay, and usually includes normative data. As its name implies, a predictive index aims to predict a child’s (or a group’s) future behavior or classification, e.g. CP or no CP, and an evaluative index is designed to measure change over time as a result of development or a specific therapy intervention.

Discriminative Tests Beginning with the publication of the Movement Assessment of Infants (MAI) in 1980,62 we have witnessed the development of at least five other, predominantly infant-focused discriminative tests over the past three decades: the Alberta Infant Motor Scale (AIMS),63 the Harris Infant Neuromotor Test (HINT),64 the NeuroSensory Motor Development Assessment (NSMDA),65 the Structured Observation of Motor Performance (SOMP-1),66 and the Test of Infant Motor Performance (TIMP).67 For each of these six tests, the first author is a pediatric physical therapist. All but one of these tests focus exclusively on infants with the ages across the five tests ranging from 32 weeks’ gestation to 18 months.68,69 The NSMDA covers a much broader age range: 1 month to 6 years.65 Although discriminative tests are usually norm-referenced (or standardized), only 3 of the tests authored by pediatric physical therapists include normative data: the AIMS, the HINT, and the TIMP. For more comprehensive descriptions of infant neuromotor tests, including those developed by pediatric professionals other than physical therapists, see the 2008 systematic reviews by Heineman and Hadders-Algra68 and Spittle et al.69


Evaluative Tests Whereas most discriminative tests are norm-referenced, most evaluative tests are criterion-referenced.70 A number of the 6 predominantly discriminative tests developed by pediatric physical therapists have been identified also as being evaluative (secondary purpose), i.e., they can be used to measure change over time as a result of development or intervention:68,69 the AIMS, the MAI, the NSMDA and the TIMP. Two of the most widely-used evaluative tests in clinical research and practice are the Pediatric Evaluation of Disability Inventory (PEDI)71 and the Gross Motor Function Measure (GMFM).72 Both were developed by interdisciplinary groups of pediatric clinicians, either with a physical therapist as first author71 or included among the authors.72 The PEDI is both norm-referenced (discriminative) and criterionreferenced (evaluative), covering an age range of 6 months to 7.5 years, and includes 3 domains: mobility, self-care, and social function.70 The aims of the test are: 1) to measure functional capabilities and performance; 2) to monitor progress in rehabilitation; and 3) to serve as an outcome measure. Since its publication in 1992, the PEDI has been used in approximately 200 studies around the world, involving children with a wide range of disabilities including CP, spinal cord injury, and acquired brain injury, and has been translated into a dozen different languages.73 The normative data and content of the PEDI were expanded in 2006 to include an age range up to 15 years74; continued revision and updating of the PEDI is currently in progress.73 Published initially in 1989 as an 88-item tool to evaluate motor change in children with CP,72 there are now two versions of the GMFM: the GMFM-66 and the GMFM-88.75 In addition to measuring change in children with CP, the GMFM has been validated for use in measuring change in children with Down syndrome76 and those with traumatic brain injury.77 Most recently, item sets were developed and validated for the GMFM-66 to improve its efficiency of administration; this research resulted in the GMFM-66-IS as a potential alternative to the GMFM-66.78 Used as an outcome measure in hundreds of studies around the world, the GMFM, along with the GMFCS, represent two of the most important contributions made to measurement in children with developmental disabilities over the past quarter century. Not surprisingly, both the PEDI and the GMFM were used as outcome measures in Ketelaar et al.’s study of the effects of a functional therapy program for young children with CP.4

Predictive Tests The ability to predict later performance has been identified as a secondary purpose for the following infant tests developed by pediatric physical therapists: the AIMS, the MAI, and the TIMP.69 The comparative predictive validity of the AIMS and the HINT was examined recently in a sample of 144 low- and high-risk infants assessed initially on both measures at 4-6.5 months and 10-12.5 months; outcomes were assessed and 2 and 3 years on the Bayley Scales of Infant Development (BSID).79 The HINT, the newer of the two tests, had comparable or slightly better predictive capabilities than the AIMS. The most recent predictive validity study of the MAI involved a sample of 134 term-born infants at developmental risk due to both biological and social factors.80 Four-month MAI scores were compared to 2-year-old outcomes on the BSID Mental and Motor Scales. Infants with MAI total risk scores >13 were nearly three times as likely to show cognitive delays on the 2-year-old BSID. Although the TIMP covers the earliest age range (32 weeks’ gestation

to 4 months), it has shown the longest predictive validity – to the Bruininks-Oseretsky Test of Motor Performance at a mean age of 5.75 years with a very respectable correlation of r = 0.36.81 The study sample was comprised of 35 randomly selected children who had been assessed as infants on the TIMP. In addition to specific tests having predictive properties, the prognosis (or prediction for the course or outcome of a disease or disability) for attaining later motor abilities has been examined through the development of motor development curves using the GMFCS in children with Down syndrome82 and those with CP.83

Summary of Pediatric Measurement Tools The tests and measures included in this paper are examples only, representing those that have involved significant contributions by pediatric physical therapists. For additional information on the predictive capabilities of a number of infant neuromotor tests, readers are advised to review the two recent systematic reviews on methods for evaluating neuromotor function in infancy.68,69 For a review of preschool tests that assess motor development and function, see the paper by Tieman et al.70 And finally, for schoolaged children with CP, a systematic review by Sakzewski et al. described clinimetric properties of measures of participation.84

be purchased on line at http://www.unisa.edu.au/cahe/Textbook/ Default.asp.89 Pediatric physical therapist researchers must continue to be involved in the validation and refinement of existing measurement tools, as exemplified so well by the ongoing research of the interdisciplinary team from the CanChild Centre for Childhood Disability Research at McMaster University. And pediatric clinicians need to be conscientious in using these tools for their intended purpose and applying them to the type of children for whom they were developed and validated.60 With the ICF move toward enhancing activity and participation for persons with disabilities, therapists should be cognizant also of tools that specifically assess children in these areas.84 It is incumbent upon all of us to continue the scientific development of our specialty area throughout the next 25 years – not only for the benefit of the children and families with whom we collaborate in clinical decision making but also for the advancement of PT as a profession. References 1 World Health Organization. International classification of functioning, disability and health: ICF. Geneva: World Health Organization; 2001. 2 Bobath K, Bobath B. The neurodevelopmental treatment. In: Scrutton D, editor. Management

Future directions in pediatric PT research What a remarkable quarter-century of development and scientific progress this has been for pediatric PT and our wonderful interdisciplinary collaborators! Although it would be comfortable to rest on our laurels and reflect smugly about these amazing accomplishments, we should instead keep this momentum going as we look forward to the next 25 years. Using the themes developed in this article, let’s look into my crystal ball for ways in which we can all move ahead. With the introduction of the ICF and ICF-CY over the past decade, clinicians and researchers need to embrace the biopsychosocial model of disability by enhancing activity and participation for children within their natural environments, as so nicely exemplified by Ketelaar et al.4 One important movement in this direction has been the recent focus on enhancing physical fitness in children with developmental disabilities85 and those with chronic diseases.51,86 A wonderful example of promoting fitness in a natural environment, i.e., community gyms, was exemplified in a study by Darrah et al. involving adolescents with CP.87 Although there have been many studies related to enhancing fitness in children and adolescents with CP, as well as in adults with Down syndrome, there are notable gaps in finding studies of children with Down syndrome, spina bifida, and other developmental disabilities. For an overview of the benefits of physical activity for children and adolescents with disabilities, readers are referred to the recent systematic review by Johnson.88 Practicing in an evidence-based manner by integrating the best research evidence with clinical expertise and the child’s and family’s values is the responsibility of all practicing clinicians and should be embraced enthusiastically by pediatric physical therapists in the coming years. With the advent and proliferation of systematic reviews synthesizing evidence of treatment efficacy (and their enhanced availability through PubMed and PEDro), clinicians owe it to their clients and families to provide interventions based on the best available research evidence. A highly readable small text on practical tips for finding evidence that was developed at the Centre for Allied Health Evidence at the University of South Australia can

of the motor disorders of children with cerebral palsy. Clinics in Developmental Medicine (No. 90). Philadelphia: Lippincott; 1984. pp 6-18. 3 Smith LH, Harris SR. Upper extremity inhibitive casting for a child with cerebral palsy. Phys Occup Ther Pediatr. 1985;5(1):71-9. 4 Ketelaar M, Vermeer A, Hart H, van-Petegem-van Beek E, Helders PJM. Effects of a functional therapy program on motor abilities of children with cerebral palsy. Phys Ther. 2001;81:1534-45. 5 World Health Organization. International classification of disability, functioning and health for children and youth (ICF-CY). Geneva: World Health Organization; 2007. 6 Adolfsson M, Granlund M, Björck-Åkesson E, Ibragimova N, Pless M. Exploring changes over time in habilitation professionals’ perceptions and applications of the International Classification of Functioning, Disability and Health, version for Children and Youth (ICF-CY). J Rehabil Med. 2010;42:670-8. 7 Damiano DL. Is addressing impairments the shortest path to improving function? Phys Occup Ther Pediatr. 2008;28:327-30. 8 Oxman AD, Sackett DL, Guyatt GH. Users’ guide to the medical literature. I. How to get started. Evidence-Based Medicine Working Group. JAMA. 1993;270:2093-5. 9 Guyatt GH, Sackett DL, Cook DJ. Users’ guide to the medical literature. II. How to use an article about therapy or prevention. A. Are the results of the study valid? Evidence-Based Medicine Working Group. JAMA. 1993;270:2598-601. 10 Guyatt GH, Sackett DL, Cook DJ. Users’ guide to the medical literature. II. How to use an article about therapy or prevention. B. What were the results and will they help me in caring for my patients? Evidence-Based Medicine Working Group. JAMA. 1994;271:59-63. 11 Jaeschke R, Guyatt GH, Sackett DL. Users’ guide to the medical literature. III. How to use an article about a diagnostic test. A. Are the results of the study valid? Evidence-Based Medicine Working Group. JAMA. 1994;271:389-91. 12 Jaeschke R, Guyatt GH, Sackett DL. Users’ guide to the medical literature. III. How to use an article about a diagnostic test. B. What were the results and will they help me in caring for my patients? Evidence-Based Medicine Working Group. JAMA. 1994;271:703-7. 13 Harris SR. How should treatments be critiqued for scientific merit? Phys Ther. 1996;76:175-81. 14 Sackett DL, Rosenberg WMC, Gray JAM, Haynes RB, Richardson WS. Evidence-based medicine: what it is and what it isn’t. BMJ. 1996;312:71-2. 15 Sackett DL, Straus SE, Richardson WS, Rosenberg W, Haynes RB. Evidence-based medicine: how to practice and teach EBM. London: Churchill Livingstone; 2000. 16 Kersten HB, Thompson ED, Frohna JG. The use of evidence-based medicine in pediatrics: past, present and future. Curr Opin Pediatr. 2008;20:326-31. 17 O’Donnell ME, Roxborough L. Evidence-based practice in pediatric rehabilitation. Phys Med Rehabil Clin N Am. 2002;13:991-1005.


18 Greenhalgh T. Papers that summarize other papers (systematic reviews and meta-analyses). BMJ. 1997:315:672-5. 19 Ottenbacher KJ, Biocca Z, Cremer G de, Gevelinger M, Jedlovec KB, Johnson MB. Quantitative analysis of the effectiveness of pediatric therapy. Emphasis on the neurodevelopmental treatment approach. Phys Ther. 1986;66:1095-101. 20 Hur JJ. Review of research on therapeutic interventions for children with cerebral palsy. Acta Neurol Scand. 1995;91:423-32. 21 Boyd RN, Morris ME, Graham HK. Management of upper limb dysfunction in children with cerebral palsy: a systematic review. Eur J Neurol. 2001 Nov;8 Suppl 5:150-66. 22 Brown GT, Burns SA. The efficacy of neurodevelopmental treatment in paediatrics: a systematic review. Brit J Occup Ther. 2001;64:235-44. 23 Butler C, Darrah J. Effects of neurodevelopmental treatment (NDT) for cerebral palsy: an AACPDM evidence report. Dev Med Child Neurol. 2001;43:778-90. 24 Anttila H, Autti-Rämö I, Suoranta J, Mäkelä M, Malmivaara A. Effectiveness of physical therapy interventions for children with cerebral palsy: a systematic review. BMC Pediatr. 2008 Apr 24;8:14. 25 Effgen SK, McEwen IR. Review of selected physical therapy interventions for school age children with disabilities. Phys Ther Rev. 2008;13:297-312. 26 Sakzewski L, Ziviani J, Boyd R. Systematic review and meta-analysis of therapeutic management of upper-limb dysfunction in children with congenital hemiplegia. Pediatrics. 2009. Jun;123:e1111-22. Epub 2009 May 18. 27 Physiotherapy Evidence Data Base (PEDro). Centre of Evidence-Based Physiotherapy. The George Institute for Global Health. The University of Sydney. [Updated 5 July 2010; cited 18 July 2010.] Available from: http://www.pedro.org.au/. 28 Damiano DL, Jong SL de. A systematic review of the effectiveness of treadmill training and body weight support in pediatric rehabilitation. J Neurol Phys Ther. 2009;33:27-44. 29 Mattern-Baxter K. Effects of partial body weight supported treadmill training on children with cerebral palsy. Pediatr Phys Ther. 2009;21:12-22. 30 Harris SR, Roxborough L. Efficacy and effectiveness of physical therapy in enhancing postural control in children with cerebral palsy. Neural Plast. 2005;12:229-43. 31 Chung J, Evans J, Lee C, Lee J, Rabbani Y, Roxborough L, et al. Effectiveness of adaptive seating on sitting posture and postural control in children with cerebral palsy. Pediatr Phys Ther. 2008;20:303-17. 32 Stavness C. The effect of positioning for children with cerebral palsy on upper-extremity function: a review of the evidence. Phys Occup Ther Pediatr. 2006;26:39-53. 33 Darrah J, Fan JSW, Chen LC, Nunweiler J, Watkins B. Review of the effects of progressive resisted muscle strengthening in children with cerebral palsy: a clinical consensus exercise. Pediatr Phys Ther. 1997;9:12-7. 34 Mockford M, Caulton JM. Systematic review of progressive, strength training in children and adolescents with cerebral palsy who are ambulatory. Pediatr Phys Ther. 2008;20:318-33. 35 Scianni A, Butler JM, Ada L, Teixeira-Salmela LF. Muscle strengthening is not effective in children and adolescents with CP. Aust J Physiother. 2009;55:81-7. 36 Dagenais LM, Lahay ER, Stueck KA, White E, Williams L, Harris SR. Effects of electrical stimulation, exercise training and motor skills training on children with meningomyelocele: a systematic review. Phys Occup Ther Pediatr. 2009;29:445-63. 37 Snider L, Korner-Bitensky N, Kammann C, Warner S, Saleh M. Horseback riding as therapy for children with cerebral palsy: is there evidence of its effectiveness? Phys Occup Ther Pediatr. 2007;27:5-23. 38 Galantino ML, Galbavy R, Quinn L. Therapeutic effects of yoga for children: a systematic review of the literature. Pediatr Phys Ther. 2008;20:66-80. 39 The Cochrane Collaboration. About us [document on the Internet]. Accessed 2010 July 18. Available from: http://www.cochrane.org/about-us. 40 Ade-Hall R, Moore P. Botulinum toxin type A in the treatment of lower limb spasticity in cerebral palsy. Cochrane Database Syst Rev. 2000(1):CD001408. 41 Hoare BJ, Wallen MA, Imms C, Villanueva E, Rawicki HB, Carey L. Botulinum toxin A as an adjunct to treatment in the management of the upper limb in children with spastic cerebral palsy (UPDATE). Cochrane Database Syst Rev. 2010(1):CD003469. 42 Hoare BJ, Wasiak J, Imms C, Carey L. Constraint-induced movement therapy in the treatment of the upper limb in children with hemiplegic cerebral palsy. Cochrane Database Syst Rev. 2007(2):CD004149.


43 Spittle A, Orton J, Doyle LW, Boyd R. Early developmental intervention programs post hospital discharge to prevent motor and cognitive impairments in preterm infants. Cochrane Database Syst Rev. 2007(2):CD005495. 44 Jones L, Miert C van, Holmes G, Pearn L, Jariwala M, Winney A. Muscle strengthening for children and adults with cerebral palsy (Protocol). Cochrane Database Syst Rev. 2009(3):CD007971. 45 Andersen J, Hartling L, Tjosvold L. Oral baclofen for the management of spasticity in children with cerebral palsy (Protocol). Cochrane Database Syst Rev. 2005(3):CD005357. 46 Hasnat MJ, Rice JE, O’Donnell ME. Intrathecal baclofen for treating spasticity in children with cerebral palsy (Protocol). Cochrane Database Syst Rev. 2004(1):CD004552. 47 Steultjens EEMJ, Dekker JJ, Bouter LM, Lambregts BB, Ende ECHM van den, Nes J van de. Occupational therapy for children with cerebral palsy (Protocol). Cochrane Database Syst Rev. 2003(4):CD004490. 48 Andriolo RB, El Dib RP, Ramos L, Atallah ÁN, da Silva EMK. Aerobic exercise training programmes for improving physical and psychosocial health in adults with Down syndrome. Cochrane Database Syst Rev. 2010(5):CD005176. 49 Diggle TTJ, McConachie HHR. Parent-mediated early intervention for young children with autism spectrum disorder. Cochrane Database Syst Rev. 2002(2):CD003496. 50 Lipson A, Edwards PJ, Logan S. Occupational therapy and physiotherapy for developmental coordination disorder (Protocol). Cochrane Database Syst Rev. 2003(1):CD004256. 51 Takken T, Van Brussel M, Engelbert RH, Net J van der, Kuis W, Helders PJM. Exercise therapy in juvenile idiopathic arthritis. Cochrane Database Syst Rev. 2008(2):CD005954. 52 Negrini S, Minozzi S, Bettany-Saltikov J, Zaina F, Chockalingam N, Grivas TB, Kotwicki T, Maruyama T, Romano M, Vasiliadis ES. Braces for idiopathic scoliosis in adolescents. Cochrane Database Syst Rev. 2010(1):CD006850. 53 Bradley JM, Moran F. Physical training for cystic fibrosis. Cochrane Database Syst Rev. 2008(1):CD002768. 54 Houston BW, Mills N, Solis-Moya A. Inspiratory muscle training for cystic fibrosis. Cochrane Database Syst Rev. 2008(4):CD006112. 55 Schans CP van der, Prasad A, Main E. Chest physiotherapy compared to no chest physiotherapy for cystic fibrosis. Cochrane Database Syst Rev. 2000(2):CD001401. 56 Main E, Prasad A, Schans CP van der. Conventional chest physiotherapy compared to other airway clearance techniques for cystic fibrosis. Cochrane Database Syst Rev. 2005(1):CD002011. 57 Elkins M, Jones A, Schans CP van der. Positive expiratory pressure physiotherapy for airway clearance in people with cystic fibrosis. Cochrane Database Syst Rev. 2006(2):CD003147. 58 Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39:214-23. 59 Palisano RJ, Rosenbaum P, Bartlett D, Livingston MH. Content validity of the expanded and revised Gross Motor Classification System. Dev Med Child Neurol. 2008;50:744-50. 60 Rosenbaum PL, Russell DJ, Cadman DT, Gowland C, Jarvis S, Hardy S. Issues in measuring change in motor function in children with cerebral palsy: a special communication. Phys Ther. 1990;70:125-31. 61 Kirshner B, Guyatt GH. A methodologic framework for assessing health indices. J Chronic Dis. 1985;38:27-36. 62 Chandler LS, Andrews MS, Swanson MW, Larson AH. Movement Assessment of Infants: A Manual. Rolling Bay, WA: Infant Movement Research; 1980. 63 Piper MC, Darrah J. Motor assessment of the developing infant. Philadelphia: Saunders; 1994. 64 Harris SR, Megens AM, Daniels LE. Harris Infant Neuromotor Test (HINT). Test user’s manual version 1.0. Clinical edition (2009). Chicago, IL: Infant Motor Performance Scales, LLC; 2010. 65 Burns YR, Ensbey RM, Norrie MA. The Neuro-Sensory Motor Development Assessment part 1: development and administration of the test. Aust J Physiother. 1989;35:141-57. 66 Persson K, Strömberg B. A protocol for structured observation of motor performance in preterm and term infants. Ups J Med Sci. 1993;98:77-82. 67 Campbell SK. The Test of Infant Motor Performance. Test user’s manual version 2.0. Chicago, IL: Infant Motor Performance Scales, LLC; 2005. 68 Heineman KR, Hadders-Algra M. Evaluation of neuromotor function in infancy – a systematic review of available methods. J Dev Behav Pediatr. 2008;29:315-23.

69 Spittle AJ, Doyle LW, Boyn RN. A systematic review of the clinimetric properties of neuromotor assessments for preterm infants during the first year of life. Dev Med Child Neurol. 2008;50:254-66. 70 Tieman BL, Palisano RJ, Sutlive AC. Assessment of motor development and function in preschool children. Ment Retard Dev Disabil Res Rev. 2005;11:189-96. 71 Haley SM, Coster WJ, Ludlow LH, et al. Pediatric Evaluation of Disability inventory: development, standardization and administration manual. Boston, MA: Trustees of Boston University; 1992. 72 Russell DJ, Rosenbaum PL, Cadman DT, Gowland C, Hardy S, Jarvis S. The gross motor function measure: a means to evaluate the effects of physical therapy. Dev Med Child Neurol. 1989;31:341-52. 73 Haley SM, Coster WI, Kao YC, Dumas HM, Fragala-Pinkham MA, Kramer JM, Ludlow LH, Moed R. Lessons from use of the Pediatric Evaluation of Disability Inventory: where do we go from here? Pediatr Phys Ther. 2010;22:69-75. 74 Haley S, Ni P, Ludlow L, Fragala-Pinkham M. Measurement precision and efficiency of multidimensional computer adaptive testing of physical functioning using the Pediatric Evaluation of Disability Inventory. Arch Phys Med Rehabil. 2006;87:1223-9. 75 Russell DJ, Rosenbaum PL, Avery LM, Lane M. Gross Motor Function Measure (GMFM-66 & GMFM-88) user’s manual. London: Mac Keith Press; 2002. 76 Russell D, Palisano R, Walter S, Rosenbaum P, Gemus M, Gowland C, et al. Evaluating motor function in children with Down syndrome: validity of the GMFM. Dev Med Child Neurol. 1998;40:693-701. 77 Linder-Lucht M, Othmer V, Walther M, Vry J, Michaelis U, Stein S, Weissmayer H, Korinthenberg R, Mall V, Gross Motor Function Measure – Traumatic Brain Injury Study Group. Validation of the Gross Motor Function Measure in children and adolescents with traumatic brain injuries. Pediatrics. 2007 Oct; 120(4):e880-6. 78 Russell DJ, Avery LM, Walter SD, Hanna SE, Bartlett DJ, Rosenbaum PL, et al. Development and validation of item sets to improve efficiency of administration of the 66-item Gross Motor Function Measure in children with cerebral palsy. Dev Med Child Neurol. 2010;e48-54. Epub 2009 Oct 7.

79 Harris SR, Backman CL, Mayson TA. Comparative predictive validity of the Harris Infant Neuromotor Test and the Alberta Infant Motor Scale. Dev Med Child Neurol. 2010;52:462-7. Epub 2009 Oct 26. 80 Rose-Jacobs R, Cabral H, Beeghly M, Brown ER, Frank DA. The Movement Assessment of Infants (MAI) as a predictor of two year neurodevelopmental outcome for infants born at term who are at social risk. Pediat Phys Ther. 2004;16:212-21. 81 Flegel J, Kolobe TH. Predictive validity of the test of infant motor performance as measured by the Bruininks-Oseretsky test of motor performance at school age. Phys Ther. 2002;82:762-71. 82 Palisano RJ, Walter SD, Russell DJ, Rosenbaum PL, Gémus M, Galuppi BE, et al. Gross motor function of children with Down syndrome: creation of motor growth curves. Arch Phys Med Rehabil. 2001;82:494-500. 83 Rosenbaum PL, Walter SD, Hanna SE, Palisano RJ, Russell DJ, Raina P, et al. Prognosis for gross motor function in cerebral palsy: creation of motor development curves. JAMA. 2002;288:1357-63. 84 Sakzewski L, Boyd R, Ziviani J. Clinimetric properties of participation measures for 5- to 13-year-old children with cerebral palsy: a systematic review. Dev Med Child Neurol. 2007;49:232-40. 85 Fowler EG, Kolobe TH, Damiano DL, Thorpe DE, Morgan DW, Brunstrom JE, et al. Promotion of physical fitness and prevention of secondary conditions for children with cerebral palsy: Section on Pediatrics Research Summit proceedings. Phys Ther. 2007;87:495-510. 86 Morris PJ. Physical activity recommendations for children and adolescents with chronic disease. Curr Sports Med Rep. 2008;7:353-8. 87 Darrah J, Wessel J, Nearingburg P, O’Connor M. Evaluation of a community fitness program for adolescents with cerebral palsy. Pediatr Phys Ther. 1999;11:18-23. 88 Johnson CC. The benefits of physical activity for youth with developmental disabilities: a systematic review. Am J Health Promot. 2009;23:157-67. 89 Grimmer-Somers K, Kumar S, Worley A, Young A. Practical tips in finding the evidence: an allied health primer. Manila: UST Publishing House; 2009.


Changing theories, changing practices, changing challenges J. Darrah Theories allow us to describe observations and assumptions and to evaluate assumed relationships between phenomena. They represent a collection of statements that summarize and attempt to explain observations.1 Theories can predict the outcome of assumed relationships between variables.2 Ideally, theories guide and inform clinical practice.3 In paediatric rehabilitation, theories can act as a roadmap for assessment and intervention decisions. During the last quarter century, paediatric physical therapy has experienced the impact of changing theoretical frameworks in two fundamental cornerstones of practice – our relationship with the children and families we work with, and our explanation of motor development and the mechanisms influencing the maturation and change of motor skills. Changing theoretical frameworks provide therapists an opportunity to reflect on past practice and consider future practice from new perspectives. This paper explores the change from child-centered to family-centered practice, and the change from a hierarchical model to explain motor development to more distributed interactive models. The impact these theoretical frameworks have had on practices is reviewed and some future challenges arising from the change in frameworks are suggested.

Family-centered care (FCC), its origins and its impact on the care of children with special needs Many disciplines, including mental health, social work, education, and health have adopted the concept of FCC in paediatrics.4 The advent of FCC over a half century ago encouraged service providers to view the family as the focus of attention, not solely the child. Although the roots of FCC differ slightly across the disciplines and between North American and European histories, a common theme across disciplines and settings is that FCC honours the centrality of the family in a child’s care, recognizes and encourages a family’s strengths and capabilities, and encourages the family to participate in informed decision making regarding their child’s care.4 In health, the emergence of Neonatal Intensive Care Units (NICUs) in the 1960’s represented a pivotal change in approach to the role of parents with their critically ill infants and recognized that parents needed to be present and participate in their children’s healthcare.5 Johnson6 and Arango, Anderson and Wells7 provide excellent overviews of the development of FCC in the United States of America. At the same time as the development of NICUs, consumer led movements were demanding more active participation in their child’s care. The emergence of Head Start programs emphasized parent participation, and legislation culminating in the Individuals with Disabilities Education Act (IDEA) mandated that parents have an active role in health and educational decisions for their children. Surgeon General Koop spearheaded two national meetings, one concerning the care for children dependent on technology in 1982 and the other in 1987, creating a national agenda for children with special health care needs. These meetings were the stimulus for the appearance of the Association for the Care of Children’s Health


Johanna Darrah PhD Professor Dept Physical Therapy, Faculty of Rehabilitation Medicine, University of Alberta, Edmonton, AB, Canada Correspondence E-mail: johanna.darrah@ ualberta.ca

(ACCH) and its successor, the Institute for Family-centered Care (IFCC). The IFCC was formed in 1992 and extended the principles of FCC to individuals of all ages. Recently the IFCC changed its name to the Institute for Patient and Family-centered Care (IPFCC), acknowledging that persons of all ages have families and support networks that they can involve as advisors in their healthcare.8 The history of the development of FCC in Europe was less legislative and more developmentally focused, predicated by the social change towards parent-child relationships created by World War II, and concern about the effect of separation of parents and families during this time.9,10 Paediatric physical therapy values the eight key elements of FCC first published by the ACCH in 1987 (box).11 The present IPFCC advocates four core principles: 1) respect and dignity, 2) information sharing, 3) participation and 4) collaboration. Prior to the adoption of family-centered principles, paediatric physical therapists delivered service using a childfocused, expert driven model. The therapist was viewed as the expert, providing information to families and teaching parents therapy activities to do with their child. Information and discussion was uni-directional, from the therapist to the parents. Families were viewed as homogeneous, with little consideration of variability in family strengths, cultures and attitudes. Excellent reviews discuss the emergence of FCC in rehabilitation and the concepts of FCC are considered essential to paediatric physical therapy.12-14 Research suggests that it is an effective model of service delivery for children with cerebral palsy and their families, yielding positive outcomes for the child, family and service system.13 Other research studies report that parents value being involved with setting their children’s rehabilitation goals15 and that parents’ satisfaction with services is directly linked to FCC.16 Despite the enthusiastic embracement of FCC theory in principle by paediatric physical therapists, confusion and challenges continue, both in clinical practice and in research.

Changing challenges Clinically, the term family-centered has almost become jargon. No therapist would admit to not being family-centered, but therapists’ perceptions of what constitutes FCC may differ and they may not be aware of all concepts of the family-centered framework. In a recent study17 54 therapists were asked to identify three concepts of FCC. Forty-eight therapists (89%) identified collaboration between therapists and families as an important concept. Detailed evaluation of the interview transcripts suggested that the dominant

Key Elements of Family-Centered Care 1 Incorporating into policy and practice the recognition that the family is the constant in a child’s life, while the service systems and support personnel within those system fluctuate. 2 Facilitating family/professional collaboration at all levels of hospital, home and community care: • care of an individual child; • program development, implementation, evaluation, and evolution; and • policy information. 3 Exchanging complete and unbiased information 4 Incorporating into policy and practice the recognition and honoring of cultural diversity, strengths, and individuality within and across all families, including ethnic, racial, spiritual, social, economic, educational and geographic diversity. 5 Recognizing and respecting different methods of coping and implementing comprehensive policies and programs that provide developmental, educational, emotional, environmental and financial supports to meet the diverse needs of families. 6 Encouraging and facilitating family to family support and networking. 7 Ensuring that hospital, home, and community service and support systems for children needing specialized health and developmental care and their families are flexible, accessible, and comprehensive in responding to diverse family-identified needs. 8 Appreciating families as families and children as children, recognizing that they possess a wide range of strengths, concerns, emotions, and aspirations beyond their need for specialized health and developmental services and supports. Source: Shelton TL, Stepanek JS. Family-Centered Care for Children Needing Specialized Health and Developmental Services. Bethesda: Association for the Care of Children’s Health; 1994.

view of collaboration was actually information sharing, and that the sharing of information was most often in one direction, from therapist to family. The concept of facilitating parent to parent support was identified as a concept of FCC by only one therapist. In an excellent article discussing the complexities of FCC, Lawlor and Mattingly identify many barriers to successful implementation of family-centered services, including the present context of health service delivery systems, therapists’ perceptions of what constitutes ‘real’ therapy’ (i.e. ‘hands-on’ interaction with the child), interprofessional areas of expertise that parse rehabilitation of the child by disciplines despite the presence of interdisciplinary teams, and the subliminal power differential that professionals have in relationships with families.18 They suggest that true success in

FCC cannot be accomplished merely by supplementing present practice with FCC philosophy. Service delivery models may need to be revised to reflect the concept of FCC at all levels of health care services. It is not a question of ‘top down’ or ‘bottom up’ implementation, but rather an integrated distributed commitment to measurable family-centered indicators that are valued by policy makers, administration, service providers and families. Research regarding the effectiveness of FCC continues. As King’s review reports, not all premises of FCC have been evaluated.13 The most frequently studied outcomes are parent satisfaction and various child and family outcomes. The research literature lacks strong studies comparing the effectiveness of an FCC approach in physical therapy to other service delivery models such as professional expert. A Cochrane review of studies of effectiveness of FCC with children who are hospitalized reported no studies that met the inclusion criteria and concluded that more stringent research is needed.19 Such studies are challenging and difficult to design but are necessary to provide empirical evidence of the importance of FCC. Further development and clarification of FCC principles in paediatric rehabilitation need to occur in the arenas of professional education, clinical practice and research. Professional programs need to include FCC principles in their curricula and apply it to all areas of practice, not just paediatrics. Programs need to include more education on how to be family-centered; for example how to include families in goal setting and intervention decisions. These types of skills are not intuitive and tools such as the Canadian Occupational Performance Measure can be used to develop students’ skills in this area.20 Students need to appreciate that ‘soft skills’ such as listening to clients, providing information to clients in an unbiased manner, and encouraging families to participate in decision making are as important as specific therapeutic handling skills. Clinically, therapists need to discuss how FCC is apparent in their setting at all levels of service delivery. Development of measureable, visible indicators of FCC is needed. Some examples are a clear reference to family-centered values in an organization’s mission statement, parent representation on advisory boards, opportunities for parents to meet each other, and standardised procedures to ensure that all families are provided an opportunity to participate in the decisions made for their children. Research methodological challenges include designing measureable FCC intervention packages that can be evaluated. In addition to family satisfaction other outcomes need to be evaluated such as cost effectiveness, the impact of FCC on the child’s development and participation and family relationships. The challenge of articulating a testable theory of FCC needs examination. Is FCC a true theory, as suggested by Bamm and Rosenbaum, or does it represent a philosophy with different operational definitions across disciplines and settings?12 Development of a well articulated theory of FCC with common assumptions across different disciplines and levels of service would provide a common FCC language, encouraging more effective evaluation and implementation.21,22 Family-centered care has to move from an ambiguous ‘feel good’ philosophy to standards of practice that are expected at all levels of service delivery in an organization.

Changing theories of motor development For many years the dominant theory to explain motor development and motor interventions for children with motor disabilities was the neuromaturational theory (NMT), first articulated by early


developmentalists such as Arnold Gesell,23 Mary Shirley24 and Myrtle McGraw.25 The major tenet of NMT is that maturation of motor skills is dependent on the maturation of the central nervous system and inhibition of lower centers of the brain by higher centers. It assumes a common process and sequence of motor development across infants. Although Gesell acknowledged the reciprocal interweaving or fluctuation of components of motor skills (e.g. flexion and extension, right and left, ipsilateral and bilateral segments), he was primarily interested in charting the hierarchical common pathway of motor development across infants, with predictable sequences of development such as cephalo-caudal progression, proximal to distal development and reflex to voluntary motor control. He believed that neither environment nor experience influenced the process of motor skill maturation. The Bobaths incorporated these hierarchical concepts in the development of neurodevelopmental treatment and these assumptions dominated physical therapy practice for children with cerebral palsy for many years.26 Over the last two decades, this hierarchical explanation of motor development has been replaced by interactionist theories. Two such theories gaining increased attention are dynamic systems theory (DST) and neuronal group selection theory (NGST). Both of these theories followed a different trajectory into paediatric rehabilitation compared to FCC. Rather than emerging from consumers’ demand for change, or legislated policy changes, DST and NGST were extrapolated into the realm of motor development from theoretical origins developed to explain broader developmental phenomena. DST has its origins in the nonlinear dynamics of chaos theory that has been applied to diverse basic and applied sciences.27 Esther Thelen, a developmental biologist, applied the tenets of DST to motor development with her elegant work evaluating the kicking and primary stepping patterns of movement in young infants. She dared to suggest that primary stepping disappeared, not because of inhibition of lower neurological centers by higher centers, but rather because of a critical fat:muscle ratio in the thigh muscles of infants that made the leg too heavy for the infant to continue stepping in standing.28,29 From this work and other experiments with kicking and reaching patterns of infants, she espoused that motor development was not dependent solely on maturation of the central nervous system, but that motor skills result from the spontaneous task specific self-organization and interaction of many subsystems.30 These subsystems derive from three sources: the child, the task and the environment.31 Within the child, subsystems include not only the central nervous system, but also factors such as biomechanics, anthropometric measures (e.g. head size), temperament, and cognition. Examples of subsystems within the task are the shape of an object being grasped, or the height of a table that the child uses to pull to stand. In the environment, diverse factors such as the surface on which the child is moving, the effect of gravity and the child’s interaction with caregivers or therapists may contribute to the motor behavior that emerges. Thelen suggested that motor development is characterized by nonlinearity; a small change in a critical subsytem can result is a large change in a child’s motor behavior. Another tenet of DST is the concept of transitional phases, when motor patterns are more variable and perhaps more amenable to change. Motor behaviours are targeted toward a functional goal or task – infants move for a purpose. Esther Thelen’s work challenged traditional thinking regarding the typical development of many skills including


kicking, reaching, cognition, language and visual habituation. She truly encouraged therapists to ‘think outside the box’ and her contributions to changing paediatric rehabilitation have yet to be recognized fully. Neuronal group selection theory32,33 (NGST) has been described as a bridge between NMT and DST34 because it acknowledges the influence of both nature (genetics) and nurture (task and environment) on development. NGST suggest that human behaviors, including motor development, are first dominated by the ‘genetic script’ of individuals. In this phase of development, described as ‘primary variability’ neuronal networks are abundant and determined by genetic evolution. Movement is characterized by variability and nonspecificity. Environmental experiences, especially afferent stimulation and feedback, strengthen the connectivity between some neuronal networks, resulting in a ‘secondary variability’ repertoire that is dependent on situation specific experience and selection. The initial variability resulting from redundant neuronal networks is replaced by a selection of specific networks influenced by behaviour and experience.35 NGST provides an explanation of the genetic starting point from which context and experience modulates motor development. Theories such as DST and NGST challenged traditional approaches to intervention for children with motor disabilities. Influenced by the potential impact of environmental context, therapists questioned the functional significance of working on isolated movement components such as balance in generic clinical contexts such as on a physio ball or on a balance beam. They realized that movement choices emerge and are shaped by a functional goal and by environmental context. Context matters, and different movement solutions may emerge depending on the environmental demands. One movement strategy may not be the best option in all environments. NGST and DST provided therapists the opportunity to consider many different approaches to intervention. New treatment approaches, emphasizing activity based,36,37 functional therapy38,39 and a task-oriented approach 40 are appearing in the literature. A recent context approach 41 describes a therapy approach that emphasizes changing the task and environment rather than focusing on remediation of a child’s abilities. Hadders-Algra has applied elegantly the principles of NGST to typical motor development 42 and to children with motor disorders,42,43 contributing to the development of a new infant assessment tool based on the concept of primary and secondary variability.44,45 The changing theoretical frameworks to explain motor development provided a catalyst to encourage consideration of new approaches to motor development and to physical therapy practice. Changing challenges DST principles have exploded into paediatric rehabilitation, but most of Dr. Thelen’s work applying this theory was directed at children with typical development. Many years ago she cautioned the author that it was presumptuous to extrapolate the theory and assumptions to children with movement challenges before evaluating the validity of DST premises using typically developing behaviours. Rehabilitation researchers need to continue to evaluate rigorously the assumptions and implications of DST that we have extrapolated to services provided to children with motor disabilities. DST is an overarching theory that can be applied to many developmental domains. The advantage of such an expansive theoretical model is that it can produce a comprehensive, cohesive theory of child development. The danger of an overarching

theory is that it can be used to support opposing assumptions. For example, are the compensatory movement solutions such as ‘W-sitting’ and ‘bunny hopping’ that children with cerebral palsy spontaneously use potential ‘deep attractor wells’ that will prevent children’s exploration of other movement options,46 or do they represent the most efficient movement solution at the moment, given the constraints of all subsystems?47 Is it possible to identify clinical signs of transition periods in children with motor challenges?48 These types of questions arising from DST require systematic evaluation. A common challenge for both FCC and the new motor theories is that present educational curricula, therapy service delivery models and administration policies may constrain implementation of the therapy services and interventions suggested by the theories. Are therapists adequately trained to be empathetic to families’ needs and to assist them in identifying the goals most important to them? Do paediatric rehabilitation centers offer flexible hours of service to accommodate the busy schedules of most families? Do physical therapy training programs emphasize function or do they continue to concentrate on remediation of impairment? Does most therapy occur on site, or are there opportunities to observe children’s capabilities and challenges in their home, school and community environments? Are there opportunities to incorporate ‘therapy’ into community recreational activities led by experts from other professions such as fitness and recreation, exercise physiology and adapted physical education? As a profession we need to discuss these kinds of questions and be prepared to make changes. Our profession needs to be cautious not to make the same mistake that we made with our long acceptance of NMT, we viewed it as truth. Theories are not truth, but rather a collection of assumptions to explain observations. Our responsibility is to evaluate the assumptions and modify those assumptions that do not stand up to scrutiny. The challenge of the next generation of researchers is to evaluate systematically the ‘active ingredients’ of each theory. It is time to evaluate the individual assumptions of each theory and to determine what aspects of each theory work, under what conditions, and for whom.49 All three theories discussed in this paper appeared in paediatric literature at least 20 years ago. Change takes time. Change also requires a critical mass of people who collectively are questioning traditional assumptions and are willing to consider new options. The next 20 years of paediatric therapy hold promise to be innovative, effective and marvelous; truly a ‘changing panorama’, as described by Dr. Helders.50

10 Robertson J, Bowlby J. Responses of young children to separation from their mothers. Courrier

References

32 Edelman GM. Neural Darwinism: The theory of neuronal group selection. Oxford: Oxford

Centre International de l’Enfance. 1952;2:131-42. 11 Shelton TL, Stepanek JS. Family-centered care for children needing specialised health and developmental services. Bethesda: Association for the Care of Children’s Health; 1994. 12 Bamm EL, Rosenbaum P. Family-centered theory: Origins, development, barriers, and supports to implementation in rehabilitation medicine. Arch Phys Med Rehabil. 2008;89:1618-24. 13 King S, Teplicky R, King G, Rosenbaum P. Family-centered service for children with cerebral palsy and their families: a review of the literature. Seminars in Pediatr Neurol. 2004;11:78-86. 14 Rosenbaum P, King S, Law M, King G, Evans J. Family-centred service: a conceptual framework and research review. Phys Occup Ther Pediatr. 1998;18:1-20. 15 Siebes RC, Wijnroks L, Ketelaar M, Schie PE van, Gorter JW, Vermeer A. Parent participation in paediatric rehabilitation treatment centres in the Netherlands: a parents’ viewpoint. Child Care Health Dev. 2006;33:196-205. 16 Law M, Hanna S, King G, Hurley P, King S, Kertoy M, Rosenbaum P. Factors affecting familycentred service delivery for children with disabilities. Child Care Health Dev. 2003;29:357-66. 17 Darrah J, Wiart L, Magill-Evans J, Ray L, Anderson J. Are family-centred principles, functional goal setting and transition planning evident in therapy services for children with cerebral palsy? Child Care Health Dev. In press. 18 Lawlor MC, Mattingly CF. The complexities embedded in family-centered care. Am J Occup Ther. 1998;52:259-67. 19 Shields L, Pratt J, Davis LM, Hunter J. Family-centred care for children in hospital. Cochrane Database Syst Rev. 2007(1):CD004811. 20 Law M, Baptiste S, Carswell A, McColl MA, Polatajko HJ, Pollock N. Canadian Occupational Performance Measure. Ottawa, ON: CAOT Publications ACE; 2005. 21 Franck LS, Callery P. Re-thinking family-centred care across the continuum of children’s healthcare. Child Care Health Dev. 2004;30:265-77. 22 Hutchfield K. Family-centered care: a concept analysis. J Adv Nurs 1999;29:1178-87. 23 Gesell A. Infancy and human growth. New York: McMillan;1928. 24 Shirley MM. The first two years: a study of twenty-five babies. Postural and locomotor development (Vol. 1). Minneapolis: University of Minnesota Press; 1931. 25 McGraw MB. The neuromuscular maturation of the human infant. New York: Hafner Press; 1945. 26 Keshner EA. Reevaluating the theoretical model underlying the neurodevelopmental theory: A literature review. Phys Ther. 1981;61:1035-40. 27 Gleick J. Chaos making a new science. New York: Penguin; 1987. 28 Thelen E, Fisher DM, Ridley-Johnson R. The relationship between physical growth and a newborn reflex. Infant Behav Dev. 1984;7:479-93. 29 Thelen E, Cooke DW. Relationship between newborn stepping and later walking: A new interpretation. Dev Med Child Neurol. 1987;29:380-93. 30 Thelen E, Kelso JAS, Fogel A. Self-organizing systems and infant motor development. Dev Rev. 1987;7:39-65. 31 Newell KM. Constraints on the development of coordination. In: Wade MG, Whiting HTA, editors. Motor development in children: Aspects of co-ordination and control. Boston: Martinus Nijhoff Publishers; 1986. p 341-60.

1 Lefrancois GR. Psychological Theories and Human Learning. Monterey: Brookes/Cole; 1982. 2 Portney LG, Watkins MP. Foundations of Clinical Research: Applications to Practice. Upper Saddle River, NJ: Prentice Hall Health; 2000. 3 Tammivaara J, Shepard KF. Theory: The guide to clinical practice and research. Phys Ther. 1990;70:578-82. 4 Allen RI, Petr CG. Rethinking family-centered practice. Am J Orthopsychiatry. 1998;68:4-15. 5 Thomas LM. The changing role of parents in neonatal care: a historical review. Neonatal Net. 2008;27:91-100. 6 Johnson BH. Family-centered care: Four decades of progress. Fam Syst Health. 2000;18:137-56. 7 Arango P, Anderson B, Wells N. Families, clinicians, and children and youth with special healthcare needs: A bright future. Pediatr Ann. 2008;37:212. 8 Bethesda. Institute for Patient- and Family-Centered Care. IPFCC. Bethesda: Institute for Patient- and Family-Centered Care; c2002 [updated 2010 October 10; cited 2010 Oct 11]. Available from: http://www.ipfcc.org/index.html. 9 Jolley J, Shields L. The Evolution of Family-Centered Care. J Pediatr Nurs. 2009;24:164-70.

University Press; 1989. 33 Sporns O, Edelman GM. Solving Bernstein’s problem: a proposal for the development of coordinated movement by selection. Child Dev. 1993;64:960-81. 34 Hadders-Algra M. Variability in infant motor development: A hallmark of the healthy nervous system. Infant Behav Dev. 2002;25:433-51. 35 Jouen F, Molina M. Exploration of the newborn’s manual activity: A window onto early cognitive processes. Infant Behav Dev. 2005;28:227-39. 36 Lowing K, Bexelius A, Carlberg EB. Activity focused and goal directed therapy for children with cerebral palsy – do goals make a difference? Disabil Rehabil. 2009;31:1808-16. 37 Valvano J. Activity-focused motor interventions for children with neurological conditions. Phys Occup Ther Pediatr. 2004;24:79-107. 38 Ahl LE, Johansson E, Granat T, Carlberg EB. Functional therapy for children with cerebral palsy: An ecological approach. Dev Med Child Neurol. 2005;47:613-9. 39 Ketelaar M, Vermeer A, Hart H ’t, Petegem-van Beek E van, Helders PJM. Effects of a functional therapy program on motor abilities of children with cerebral palsy. Phys Ther. 2001;81:1534-45.


40 Salem Y, Godwin EM. Effects of task-oriented training on mobility function in children with cerebral palsy. Neuro Rehabilitation. 2009;24:307-13. 41 Law M, Darrah J, Pollock N, Rosenbaum P, Russell D, Walter SD, Petrenchik T, Wilson B, Wright V. Focus on Function – A randomized controlled trial comparing two rehabilitation interventions for young children with cerebral palsy. BMC Pediatrics. 2007;7:31. 42 Hadders-Algra M. The neuronal group selection theory: A framework to explain variation in normal motor development. Dev Med Child Neurol. 2000;42:566-72. 43 Hadders-Algra M. The Neuronal Group Selection Theory: A framework to explain variation in normal motor development. Dev Med Child Neurol. 2000;42:566-72. 44 Heineman KR, Bos AF, Hadders-Algra M. The infant motor profile: A standardized and qualitative method to assess motor behaviour in infancy. Dev Med Child Neurol. 2008;50:275-82. 45 Heineman KR, Middelburg KJ, Hadders-Algra M. Development of adaptive motor behaviour in


typically developing infants. Acta Paediatr. 2010;99:618-24. 46 Kamm K, Thelen E, Jensen JL. A dynamical systems approach to motor development. Phys Ther. 1990;70:17-29. 47 Darrah J, Barlett D. Dynamic systems theory and management of children with cerebral palsy: unresolved issues. Infants Young Child. 1995;8:52-9. 48 Law M, Darrah J, Pollock N, King G, Rosenbaum P, Russell D, Palisano R, Harris S, Armstrong R, Watt J. Family-centred functional therapy for children with cerebral palsy: an emerging practice model. Phys Occup Ther Pediatr. 1998;18:83-102. 49 Whyte J, Hart T. It’s more than a black box; it’s a Russian doll: Defining rehabilitation treatments. Am J Phys Med Rehabil. 2003;82:639-52. 50 Helders PJM, Engelbert RHH, Custers JWG, Takken T, Net J van der. Creating and being created: the changing panorama of paediatric rehabilitation. Ped Rehab. 2003;6:5-12.

Developmental pediatrics: perspectives on 25 years of development and scientific progress P. Rosenbaum and A. Harvey

Peter Rosenbaum, MD, FRCP(C) Professor of Pediatrics at McMaster University, Canada; Canada Research Chair in C hildhood Disability, Hamilton ON, Canada

Introduction The nature of developmental pediatrics has evolved in important ways over the past 25 years. In this chapter we describe what we believe are the signal developments in the field, discussing in particular the conceptual underpinnings of how we think about ‘childhood disability’. We emphasize the importance of thinking about child development, the functional status of children with ‘complicated lives’, the importance of ‘participation’ and the role and well-being of the family. These ideas are contextualized particularly in the language and concepts of the World Health Organization’s International Classification of Functioning, Disability and Health (ICF).1 This is not meant to be a comprehensive history but rather an essay that considers what we believe are significant advances in how we are thinking about, and counselling about, childhood disability. For this reason the majority of the references cited to illustrate the points being argued are taken from work with which the authors have a particular familiarity. We also address how the research agenda has developed to address basic clinical and health services questions that emerge from the clinical realities of children with disabilities and their families in the 21st century.

The past It is important to begin by looking back on some of the traditions of the field – where we have come from – as a basis for appreciating how much has changed both conceptually and in practice over time. Again, these are the authors’ personal views and are not based on a detailed or systematic review of the literature. Physicians, and indeed most health professionals, have been brought up in the traditions of biomedicine. This way of approaching clinical dilemmas is clearly an essential framework to address acute problems (for example, how to analyse, understand and manage the sudden onset of chest pain). The thinking inherent in such a model includes the importance of ‘ruling out’ less likely causes of the problem, identifying the specific nature of the disorder (the diagnosis) and finding the most appropriate treatment regimens to manage that diagnosis. There are, however, challenges associated with this approach that we believe limit its applicability and generalizability to chronic conditions. This is often the case because (a) there may be either no clear ‘diagnosis’, or (more often in chronic conditions) many factors interact together to contribute to the manifestations of the problem; and (b) there may be no obvious specific ‘treatment’ to be applied even when a clear diagnosis can be reached. One need only think of common diagnoses in our field, such as ‘cerebral palsy’ or ‘autism spectrum disorder’, to appreciate the lack of connection between diagnosis and intervention in the absence of a great deal more information. In developmental disorders like these the diagnosis simply doesn’t tell us enough!

Adrienne Harvey, PT, PhD Post-Doctoral Fellow, McMaster Child Health Research Institute in Hamilton ON, Canada Correspondence E-mail: [email protected]

Newer inclusionary thinking encourages professionals to ‘rule in’ relevant aspects of people’s predicaments. This idea is embedded in concepts inherent in the biopsychosocial framework of the World Health Organization’s International Classification of Functioning, Disability and Health (ICF)(elaborated below).1 As we will argue, the ICF represents an important advance for many fields of health, including developmental pediatrics. We believe that these ideas have contributed to a fundamental shift in how we think about children with ‘disabilities’. Another tradition to which the field of developmental pediatrics is heir is people’s long-held sense of futility and pessimism about children with chronic conditions, especially those associated with neurological impairments. In this field professionals have often been seen as ‘very dedicated’ and committed, but in the same breath the people who express these kind thoughts also wonder “But what can you do for them?”2 Many people have traditionally seen developmental pediatrics as a kind of ‘pastoral care’, implying that working with children with disabilities (and their families) was more like social work than medicine. Thus, people in our field have been challenged to gain acceptance as ‘real doctors’ and as health services researchers who can contribute to the academic discourse. A related concern is the ease with which people have traditionally judged the book by the cover, and perhaps failed to see ‘possibility’ behind ‘disability’. This is a form of prejudice (prejudging) which does a disservice to both the judge and the judged. Thus a child with a neurodevelomental disability in one sphere of function can too easily be assumed to be ‘damaged goods’ in other areas of life as well, and not be recognized as possibly having capacity that can be developed, or a good quality of life.3 We suspect that everyone who works in our field can call to mind current or former patients whose lives are rich with achievements ‘despite’ their disability. As a couple of examples, one of PR’s former child patients with Level IV CP is now a colleague at CanChild and a doctoral student. Another young adult of our acquaintance is an ex-premature infant with Level I CP and visual impairment who works as the foreign correspondent for a national newspaper in a country where he has lived for several years and has learned the complex language of that country. People who entered this field 25 years ago were often the inheritors of a great deal of ‘received wisdom’ (what we call the ‘Everybody


Health condition

Body functions and structures

Activities

Environmental factors

Participation

Personal factors

Figure 1 The domains represented in the International Classification of Functioning, Disability and Health (ICF). (Source: World Health Organization, 2001.1) knows…’ truisms that are often simply not true)! These perspectives were often biased by selected clinical experience and memories, and were also based on our assumptions about what life must be like for ‘these children and families’. One popular example – for which we know of no sound research evidence – is that families of children with disabilities have a higher rate of marital breakdown than other families. We often seemed too willing to accept these ‘truths’ without questioning their validity, because they fit with what we thought must be true (“If I hadn’t believed it I wouldn’t have seen it”). Another of the traditions 25 years ago was the community’s attitudes toward disability. These were, we believe, much less accepting than is often the case in 2010. Developmental paediatricians are part of their community, and are influenced by the conventional thinking of that broader community. Insofar as ‘disability’ was a category of ‘difference’, and difference could be frightening, working in this field could be considered as working at the margins of medicine rather than in the mainstream. It is sobering to recognize that 25 years ago people were not yet talking about ‘evidence-based medicine’. To many people in child health EBM referred to ‘expressed breast milk’ (or, to the cynics, ‘Eminence-based medicine’ [meaning “Because I said so”!]). The research base of the field was quite thin, and in fact there were few ‘professional’ clinical and health services researchers actively working to move the field forward. As a young emerging clinical service developmental pediatrics could easily be considered the poor country cousin of colleagues in areas of child health such as neonatology and childhood cancer with their rich traditions of collaborative research and of services provided on the basis of sound research evidence.

The present Twenty-five years later a great deal has changed for the better. In the rest of this paper we will offer specific examples of what we believe are illustrations of ‘modern’ thinking and developments in research that today guide the actions of developmental paediatricians. This is by no means an exhaustive catalogue,


but may provide insights into how the field has evolved over the past quarter century. It may also offer guideposts for future opportunities to continue and enhance the journey. Other authors writing for this series of essays will almost certainly elaborate more fully of many of these ideas.

The International Classification of Functioning, Disability and Health (ICF) A fundamental change in the way clinicians and researchers view health conditions such as cerebral palsy and other developmental disorders has been stimulated by the advent of the ICF.1 Evolving from the earlier International Classification of Impairments, Disabilities and Handicaps (WHO 1980) the ICF provides a framework and standard language with which to think about and describe health and health-related states.4 It is effectively a social model of disability insofar as it incorporates and gives equal weight to both the biological and social aspects of people’s lives to represent more accurately the impact of health conditions on an individual’s life, including their participation in society.5 The domains represented in the ICF apply to any ‘health condition’. They are described from the perspective of the body, the individual and society, and include body functions and structures, activities and participation.1 These components of a health condition are complemented by contextual factors (environmental and personal factors) that may impact a person’s health state. An individual’s functioning in a specific domain is seen as a complex and dynamic interaction among the health condition and the many contextual factors (see diagram). The ICF has enhanced communication among clinicians and has advanced the way we both describe conditions and the way we measure specific aspects of developmental disorders. An important change over the past quarter century has been the shift away from directing our attentions solely to the impairments of neurodevelopmental disorders like cerebral palsy (such as range of motion of limbs or degree of spasticity) toward focusing more broadly on the daily lives of the children and their families. We now think about how a condition impacts on the development, activities

and participation of a child with a disability, and how treatments or interventions might influence these aspects of people’s lives. For example, orthopaedic surgery to correct contractures and deformities might improve the length of muscles and range of joints; the ‘developmental’ perspective explores whether the intervention improves the child’s ability to mobilize, transfer and participate with their friends and family.6 This approach incorporates the traditions of biomedicine but represents a fundamental expansion of our purview beyond a preoccupation with the biological manifestations of the condition to consider its impact on development, function and well-being. The ICF can be used to guide the selection of outcome measures to ensure that we examine the effects of interventions from all aspects of the child, that is, at the level of body functions and structure as well as at the level of activity and participation. This allows us to emphasize function and what is relevant and meaningful to the child and family, rather than focusing – as has traditionally been done – on what the clinician wants to see. This approach encourages the use of a set of outcome measures relevant to the clinical or research question in mind, rather than assuming that one tool can cover all areas, or simply reverting to those with which we are most familiar (i.e., what everyone else uses!). In the past many outcome studies focused on the impairment rather than the changes in functional limitations that might result.7 The focus has now shifted to measure comprehensively all areas of the ICF and to take a broader perspective of well-being and level of community integration.8 The ICF also helps us to recommend treatments appropriately based on expected functional gains. Many treatments for children with developmental disabilities address issues at the body structure and function level.

For example, in cerebral palsy botulinum toxin is widely and effectively used to address spasticity, and muscle strengthening is prescribed to counter weakness. It is usually assumed that the expected beneficial effects of these impairment-directed interventions will lead to positive changes in activity and participation; evidence suggests that this is not necessarily the case.9

The importance of participation, or involvement in life situations, has emerged as a key component in child health. Participation levels of children with disabilities have been shown to be lower than those of typically developing children, with reduced involvement in formal (or planned) activities.10 Participation levels of children with cerebral palsy are influenced by the severity of motor impairment.5,11 Now that we have evidence that children with physical disabilities have reduced participation, we can implement interventions to improve their participation levels.

can influence the child’s interactions with both the physical and human environment.13 Outcomes assessment in children with developmental disabilities therefore needs to consider the environments that are relevant to the age of the child.

For example, participation of children with cerebral palsy can be influenced by where they live14,15 and by the socioeconomic status of the family.10 Many environmental factors are external to the individual and make up the physical, social and attitudinal contexts in which people conduct their lives.1 At the personal level, however, environmental setting has been shown to exert a powerful effect on the methods of usual mobility of children with CP.16,17

In addition, mobility in daily life is influenced by age as well as environmental factors.18 These developments have led to the creation of a number of clinical measures to capture the concepts that are part of contemporary thinking and practice. These developments are outlined below in a section of this paper.

Capacity, capability and performance Also emerging in recent years are the distinctions between the constructs of capacity, capability and performance.19 Until recently, capacity and capability were sometimes used interchangeably. More recently they have been thought of as subtly but importantly different constructs. Within the ICF ‘capacity’ describes an individual’s ability to execute a task or action and indicates highest probable level of functioning, while ‘performance’ describes what an individual usually does in his or her current environment.1 Further to this, capacity has been described as ‘what a person can do in a standardized, controlled environment’, capability as ‘what a person can do in his/her daily environment’ and performance as ‘what a person actually does do in his/her daily environment’.20 The difference between capacity and capability, therefore, is the physical environment, with capacity referring to actions unfettered by environmental constraints. The person-environment interaction is the discriminating element among the three constructs. These differences have implications not only for measuring function, but also for planning interventions and for counselling families. Treatments may improve capacity in the clinical setting, but if the improvements do not translate into improved functional performance in the environments important to people with disabilities then it is unlikely that they will have received meaningful benefit. This indicates a need for both to be measured, and when capacity is greater the factors that limit performance need to be identified and managed.

Clinical measures Impact of the environment The ICF has also focused our attention on the impact of the environment on children’s daily functioning. Awareness of the dynamic between the child and surroundings and how this affects performance is important when considering the range of interventions possible to increase participation in the home, school and community.12 Children’s environments are many and varied, and they change considerably across the stages of infancy, early childhood, middle childhood and adolescence. These changes

Reference has been made to the ways that the ICF has expanded our awareness of the areas of child and family well-being to which we must pay attention. A related achievement in the field has been the systematic development of clinical assessment and outcome measures that describe children’s function and participation, or capture changes in outcomes like these over time. In particular change-detecting (evaluative) measures have been developed to capture meaningful change in various aspects of function. These include the Gross


Motor Function Measure,21 the Pediatric Evaluation of Disability Inventory22 and the Functional Mobility Scale.23,24 The importance of these measures is that they have been purpose-built to measure change, and have been validated with that goal in mind. Unlike norm-referenced measures that have traditionally been (mis)used to assess change these measures provide a more realistic account of what, and how much, has changed when children are assessed with them over time.25 In addition, these newer tools have been developed using contemporary methods from measurement science, enabling users to have confidence that the tools are likely to be reliable and valid for the functions for which they are used. In this essay we simply highlight a few examples of these clinical assessment tools we know best to illustrate how the shifts in intervention focus have led to the development of sound instruments which capture relevant aspects of the field. For example, given the role of environmental influences on the performance of children, there has been a need for reliable and valid tools to describe and measure this impact over time and following treatments and interventions. The expanded and revised Gross Motor Function Classification System (GMFCS E&R) is a simple method for classifying children with CP based on functional abilities.26 Building in part on the concepts of the ICF, the GMFCS E&R includes perspectives about how environmental and personal factors influence usual performance of gross motor function. Other recent developments in outcome measurement include new tools that consider the environment, including the Functional Mobility Scale (FMS).23 The FMS rates the amount of assistance required for mobility in three key environmental settings of children: home, school and community. Changes over time or following interventions can be measured, with differential impacts of efficacious interventions seen in these settings dependent on the demands, distances and familiarity of that environment. Using the GMFCS (to describe) and FMS (to measure change) together provides a clear picture of the abilities of children and adolescents with respect to their mobility and functional abilities.27 A systematic review of measures that examine activity limitations in children with CP and other developmental disorders showed that many do consider the environment to some extent, with the exception of those that are administered in the clinical setting. The FMS was the only one that examines in detail the differences in function across these environments.28 Tools may focus on different aspects of capacity, capability and performance. Using cerebral palsy as an example, capacity is usually measured in the clinical setting with standardized tests such as the GMFM or evaluations of muscle strength.21 It has been shown that children’s capacity often differs from their actual performance,29,20 therefore it is important to measure more than just capacity to reflect their daily functioning. Measures of performance include the FMS23 and the WeeFIM.31 The Activities Scale for Kids (ASK) has both a capability and a performance version.32 The Pediatric Evaluation of Disability Inventory (PEDI) section on functional skills measures capability and the caregiver assistance section measures performance.22 These perspectives – consistent with the thinking behind the ICF – illustrate how a modern approach to childhood disability has moved beyond the biomedical focus toward a consideration of the real-world impacts of disability.


The GMFCS has had a signal impact on the field by emphasizing performance (function), providing consistent language across disciplines and countries, and enabling people to identify meaningful clinical strata within the umbrella concept of ‘cerebral palsy’. The systematic classification of the hallmark functional disorder in CP has made it possible, for example, to relate this aspect of function to other classical ways of describing CP, and in the process to illustrate how these systems differ from one another in what they reveal about the condition.33 As of mid-2010 the GMFCS has been translated into over two dozen languages and been cited in the scientific literature over 800 times, a testament to its impact on the field. Another evidence of the impact of the GMFCS is that at least two analogues have been developed to describe function in manual abilities (the Manual Abilities Classification System [MACS])34 and communication (the Communication Function Classification System [CFCS]).35 This indicates an acceptance of the importance of talking about actual day-to-day function, and of the value of creating systems that are widely used and acceptable to families.36,37

The role of the family First articulated in the 1960s, the concept of ‘Family-centred Service’ (FCS) began to take root in developmental pediatrics in the 1990s. “Family-centred service is made up of a set of values, attitudes, and approaches to services for children with special needs and their families. Family-centred service recognizes that each family is unique; that the family is the constant in the child’s life; and that they are the experts on the child’s abilities and needs. The family works with service providers to make informed decisions about the services and supports the child and family receive. In familycentred service, the strengths and needs of all family members are considered.”38,39 The shift towards family-centredness is significant for a number of reasons. First, it formally recognizes the primacy of parents’ roles. They are experts on their child; the people who identify their child’s needs and capacities; the ‘clients’ with whom professionals work; and the main ‘context’ in the lives of the children. An interest in the family as the central element of the work in developmental pediatrics contrasts with the traditional focus on the child as the ‘patient’ with the ‘problem’. Second, with the formal identification of the importance of the family, the corollary of these ideas is that family well-being becomes an essential consideration for the well-being of children. There is accumulating evidence that compared to other adults in the community the physical and mental well-being of parents raising children with chronic conditions is less robust.40,41 It is therefore important for service providers, when prescribing management interventions for the child with a disability, to be aware of the needs and capacity of parents and other family members. Third, there is an opportunity for service providers to work collaboratively with parents to identify goals for management and to evaluate the success of interventions according to family goals. Evidence from Ketelaar et al. indicates that when this is done effectively the children’s functional outcomes are better – with less ‘therapy’!42 The implications of these observations concern how developmental paediatric services should be provided. In addition to the role of the physician, a developmental disability team should include professionals capable of addressing family needs, including the psychosocial dimensions of childhood disability and the impact of

children’s behaviour on parent well-being.43 In this respect, as well as many others, a modern approach to developmental pediatrics encompasses a far broader canvas than was the case 25 years ago. In addition a number of measures have been created to assess parents’ experience of family-centredness of services.44,45

Research paradigms Finally, a major step forward in the recent history of developmental pediatrics is the application of increasingly sophisticated research designs to address the important questions in the field. Thus, in addition to a growing number of well designed randomized clinical trials (RCTs)42,46,47 we have seen the excellent use of single-subject studies.48,49 This latter design provides a very useful way to assess change in status over time against a systematically observed baseline. Although each individual study has limited generalizability to the population they can allow clinicians and researchers to assess specific people – and specific interventions – in a methodologically sound way, as has been done by Butler and Bower in the references cited above. In parallel with conceptual developments in the field described earlier in this paper, researchers are recognizing the need to apply new methods of design and analysis in their studies to accommodate the acknowledged complexity of the issues faced by children with chronic conditions and their families. Examples of studies that have used the analytic technique of structural equation modelling include the work of King et al.,43 Law et al. (2003)50 and Raina et al.51 This design is one of many multivariable approaches that allow people to take account simultaneously of several variables that are known or thought to influence an outcome of interest, and to address the “Yes, but what about…?” questions that inevitably arise when we explore complex multi-factorial issues using simpler linear analyses. Another research design that is being much more widely applied is the use of prospective longitudinal studies.23,52,53 This design is demanding insofar as it requires a prospectively assembled cohort and research efforts over ‘real’ time, but the advantages are considerable. This approach to within-person development provides a much more sensitive understanding of change and development than cross-sectional studies that link together observations about different people at different stages of the evolution of their conditions. It is our belief that this kind of study will contribute very important understanding to many of the questions about development and prognosis that are uppermost in the minds of parents and young people with developmental disorders. Lastly, over the past twenty years qualitative research methods – long used in nursing and elsewhere – have been increasingly applied to enable researchers to get ‘under the surface’ of the complex issues that are so much a part of contemporary child health, including the issues of concern to developmental pediatrics. The recognized complementarity between quantitative and qualitative traditions has led to far richer understanding of issues than has traditionally been the case. In the process it is almost certainly also true that a broader range of health services researchers have become engaged in the field and enriched the dialogue among all the players interested in health services research.

changed. There has been a fundamental evolution in the field, partly based on secular changes in the broader community, and partly based on the development and adoption of new ways of looking at old issues. We believe that the conceptual changes represent the biggest shift, as the field has expanded beyond a limited focus on the biomedical aspects of disability and embraced the biopsychosocial, developmental and family dimensions of ‘childhood disability’. With these shifts have come new ways of thinking about ‘disability’; new approaches to counselling families; and new research paradigms with which to explore whether these ideas have currency. The current challenges are to implement the best of current thinking, to continue to create new clinical and research models, and to evaluate the big ideas to be sure that they work as well as we expect them to do. It is our hope that when, in 25 years, people look back at reports like this one, they will be able to observe at least as much change and excitement about the field as we have found! References 1 World Health Organization. International Classification of Functioning, Disability and Health (ICF). Geneva: World Health Organization; 2001. 2 Rosenbaum P. Editorial. But what can you do for them? Dev Med Child Neurol. 1998;40:579. 3 Rosenbaum PL, Livingston MH, Palisano RJ, Galuppi BE, Russell DJ. Quality of life and healthrelated quality of life of adolescents with cerebral palsy. Dev Med Child Neurol. 2007;49:516-21. 4 World Health Organization. International Classification of Impairment, Activity and Participation (ICIDH-2). Geneva: World Health Organization; 1980. 5 Beckung E, Hagberg G. Neuroimpairments, activity limitations, and participation restrictions in children with cerebral palsy. Dev Med Child Neurol. 2002;44:309-16. 6 Rosenbaum P. Editorial. Putting child development back into developmental disabilities. Dev Med Child Neurol. 2009;51:251. 7 Rosenbaum PL, Stewart D. The WHO International Classification of Functioning, Disability and Health. A Model to Guide Clinical Thinking, Practice and Research in the Field of Cerebral Palsy. Sem Pediatr Neurol. 2004;11:5-10. 8 Majnemer A, Mazer B. New directions in the outcome evaluation of children with cerebral palsy. Sem Pediatr Neurol. 2004;11:11-7. 9 Wright FV, Rosenbaum PL, Fehlings D. How do changes in Impairment, Activity, and Participation relate to each other? Study of children with cerebral palsy (CP) who have received lower extremity Botulinum Toxin Type-A (Bt-A) injections. Dev Med Child Neurol. 2007;50:283-9. 10 Law M, King G, King S, Kertoy M, Hurley P, Rosenbaum P, Young N, Hanna S. Patterns of participation in recreational and leisure activities among children with complex physical disabilities. Dev Med Child Neurol. 2006;48:337-42. 11 Schenker R, Coster WJ, Parush S. Neuroimpairments, activity performance, and participation in children with cerebral palsy mainstreamed in elementary schools [see comment]. Dev Med Child Neurol. 2005;47:808-14. 12 Goldstein DN, Cohn E, Coster W. Enhancing participation for children with disabilities: application of the ICF enablement framework to pediatric physical therapist practice. Pediatr. 2004;16:114-20. 13 Simeonsson RJ, Leonardi M, Lollar D, Bjorck-Akesson E, Hollenweger J, Martinuzzi A. Applying the International Classification of Functioning, Disability and Health (ICF) to measure childhood disability. Disabil Rehabil. 2003;25:602-10. 14 Hammal D, Jarvis SN, Colver AF. Participation of children with cerebral palsy is influenced by where they live [see comment]. Dev Med Child Neurol. 2004;46:292-8. 15 Fauconnier J, Dickinson HO, Beckung E, Marcelli M, McManus V, Michelsen SI, et al. Participation in life situations of 8-12 year old children with cerebral palsy: cross sectional European study. BMJ. 2009;338:b1458. 16 Palisano RJ, Tieman BL, Walter SD, Bartlett DJ, Rosenbaum PL, Russell D, Hanna SE. Effect of environmental setting on mobility methods of children with cerebral palsy. Dev Med Child

Conclusion This essay has provided an opportunity to look back over a quarter of a century of thinking and work in ‘childhood disability’, and to consider how the landscape of developmental pediatrics has

Neurol. 2003;45:113-20. 17 Tieman B, Palisano RJ, Gracely EJ, Rosenbaum P, Chiarello LA, O’Neil M. Changes in mobility of children with cerebral palsy over time and across environmental settings. Phys Occup Ther Pediatr. 2004;24:109-28.


18 Palisano RJ, Hanna SE, Rosenbaum PL, Tieman B. Probability of walking, wheeled mobility, and assisted mobility in children and adolescents with cerebral palsy. Dev Med Child Neurol. 2010;52:66-71. 19 Morris C. Measuring participation in childhood disability: how does the capability approach improve our understanding? Dev Med Child Neurol. 2009;51:92-4. 20 Holsbeeke L, Ketelaar M, Schoemaker MM, Gorter JW. Capacity, capability, and performance: different constructs or three of a kind? Arch Phys Med Rehabil. 2009;90:849-55. 21 Russell D, Rosenbaum PL, Avery L Lane M. The Gross Motor Function Measure. GMFM-66 and GMFM-88 (Users’ Manual). Clinics in Developmental Medicine No. 159. London: Mac Keith Press; 2002. 22 Haley SM, Coster, WJ, Ludlow LH, Haltiwanger JT, Andrellos PJ. Pediatric Evaluation of Disability Inventory: Development, Standardization, and Administration Manual, Version 1.0 Boston: England Medical Center; 1992. 23 Graham HK, Harvey A, Rodda J, Nattrass GR, Pirpiris M. The Functional Mobility Scale (FMS). J Pediatr Orthop. 2004;24(5):514-20. 24 Harvey AR, Morris ME, Graham HK, Wolfe R, Baker R. Reliability of the functional mobility scale for children with cerebral palsy. Phys Occup Ther Pediatr. 2010; May 30(2):139-49. 25 Rosenbaum P, Cadman D, Russell D, Gowland C, Hardy S, Jarvis S. Issues in measuring change in motor function in children with cerebral palsy. A special communication. Phys Ther. 1990;70(2):125-31. 26 Palisano RJ, Rosenbaum P, Bartlett D, Livingston MH. Content validity of the Expanded and Revised Gross Motor Function Classification System. Dev Med Child Neurol. 2008;50:744-50. 27 Harvey A, Rosenbaum P, Hanna S, Yousefi-Nooraie R, Graham HK. Long-term changes in mobility following single event multilevel surgery in ambulatory children with cerebral palsy. Dev Med Child Neurol. 2010 (submitted). 28 Harvey A, Robin J, Morris ME, Graham HK, Baker R. A systematic review of measures of activity limitation for children with cerebral palsy. Dev Med Child Neurol. 2008;50:190-8. 29 Tieman BL, Palisano RJ, Gracely EJ, Rosenbaum PL. Gross motor capability and performance of mobility in children with cerebral palsy: a comparison across home, school, and outdoors/community settings. Phys Ther. 2004;84:419-29. 30 Young NL, Williams JI, Yoshida KK, Bombardier C, Wright JG. The context of measuring disability: does it matter whether capability or performance is measured? J Clin Epidem. 1996;49:1097-101. 31 Msall ME, DiGaudio K, Duffy LC, LaForest S, Braun S, Granger CV. WeeFIM. Normative sample of an instrument for tracking functional independence in children. Clin Pediatr. 1994;33:431-8. 32 Young NL, Williams JI, Yoshida KK, Wright JG. Measurement properties of the activities scale for kids. J Clin Epidem. 2000;53:125-37. 33 Gorter JW, Rosenbaum PL, Hanna SE, Palisano RJ, Bartlett DJ, Russell DJ, Walter SD, Raina P, Galuppi BE, Wood E. Limb distribution, motor impairment, and functional classification of cerebral palsy Dev Med Child Neurol. 2004;46:461-7. 34 Eliasson AC, Krumlinde Sundholm L, Rösblad B, Beckung E, Arner M, Öhrvall A-M, Rosenbaum P. The Manual Ability Classification System (MACS) for children with cerebral palsy: scale development and evidence of validity and reliability. Dev Med Child Neurol. 2006;48:549-54. 35 Hidecker MJC, Paneth N, Rosenbaum P, Kent RD, Lillie J, Johnson B. Development of the Com-

36 Morris C, Galuppi BE, Rosenbaum PL. Reliability of family report for the Gross Motor Function Classification System. Dev Med Child Neurol. 2004;46:455-60. 37 Morris C, Kurinczuk JJ, Fitzpatrick R, Rosenbaum PL. Who best to make the assessment? Professionals and families’ classifications of gross motor function are highly consistent. Arch Dis Child. 2006 Aug;91(8):675-9. 38 CanChild, 2010. http://canchild.icreate3.esolutionsgroup.ca/en/childrenfamilies/resources/ FCSSheet1.pdf [Accessed June 14, 2010.] 39 Rosenbaum P, King S, Law M, King G, Evans J. Family-centred services: A conceptual framework and research review. Phys Occup Ther Pediatr. 1998;18(1):1-20.

40 Brehaut J, Kohen D, Raina P, Walter S, Russell D, Swinton M, O’Donnell M, Rosenbaum P.

The health of parents of children with cerebral palsy: How does it compare to other Canadian adults? Pediatr. 2004;114(2):e182-91.

41 Lach LM, Kohen DE, Garner RE, Brehaut JC, Miller AR, Klassen AF, Rosenbaum PL. The health and psychosocial functioning of caregivers of children with neurodevelopmental disorders. Disabil Rehabil. 2009;31(9):741-52. 42 Ketelaar M, Vermeer A, Hart H, Petegem-van Beek E van, Helders PJ. Effects of a functional therapy program on motor abilities of children with cerebral palsy. Phys Ther. 2001;81(9):1534-45. 43 King G, King S, Rosenbaum P, Goffin R. Family-centred caregiving and well-being of parents of children with disabilities: Linking process with outcome. J Pediatr Psychol. 1999:24:41-52. 44 King S, Rosenbaum P, King G. Parents’ perceptions of care-giving: development and validation of a process measure. Dev Med Child Neurol.1996;38(9):757-72. 45 Woodside J, Rosenbaum P, King S, King G. A measure of processes of care for service providers: development and properties of a self-report measure. Childr Health Care. 2001;30(3):237-52. 46 Palmer FB, Shapiro BK, Wachtel RC, Allen MC, Hiller JE, Harryman SE, Mosher BS, Meinert CL, Capute AJ. The effects of physical therapy on cerebral palsy. A controlled trial in infants with spastic diplegia. N Engl J Med. 1988:31(318):803-8. 47 Law M, Russell D, Pollock N, Rosenbaum P, Walter S, King G. A comparison of intensive neurodevelopmental therapy plus casting and a regular occupational therapy program for children with cerebral palsy. Dev Med Child Neurol. 1997;39:664-70. 48 Butler C. Effects of powered mobility on self-initiated behaviours of very young children with locomotor disability. Dev Med Child Neurol. 1986;28:325-32. 49 Bower E, McLellan DL. Evaluating therapy in cerebral palsy. Child Care Health Dev. 1994;20(6):409-19. 50 Law M, Hanna S, King G, Hurley P, King S, Kertoy M, Rosenbaum P. Factors affecting familycentred service delivery for children with disabilities. Child: Care, Health Dev. 2003;29:357-66. 51 Raina P, O’Donnell M, Rosenbaum P, Brehaut J, Walter SD, Russell D, Swinton M, Zhu B, Wood E, King S, King G. The health and well-being of caregivers of children with cerebral palsy: What are the determinants? Pediatr. 2005;115:e626-36. 52 Rosenbaum PL, Walter SD, Hanna SE, Palisano RJ, Russell DJ, Raina R, Wood E, Bartlett D, Galuppi B. Prognosis for gross motor function in cerebral palsy: Creation of motor development curves. JAMA. 2002; 288:1357-63. 53 Hanna SE, Rosenbaum PL, Bartlett DJ, Palisano RJ, Walter SD, Avery L, Russell DJ. Stability

munication Function Classification System (CFCS) for individuals with cerebral palsy. Dev Med

and decline in gross motor function among children and youth with cerebral palsy aged 2 to 21

Child Neurol. 2009;51(Suppl 2):48.

years. Dev Med Child Neurol. 2009;51(4):295-302.



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