pediatrics 2012 munck 503 8

DOI: 10.1542/peds.2011-1566; originally published online February 27, 2012; 2012;129;503Pediatrics

the PIPARI Study GroupPetriina Munck, Pekka Niemi, Helena Lapinleimu, Liisa Lehtonen, Leena Haataja and

Weight ChildrenStability of Cognitive Outcome From 2 to 5 Years of Age in Very Low Birth

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located on the World Wide Web at: The online version of this article, along with updated information and services, is

of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2012 by the American Academy published, and trademarked by the American Academy of Pediatrics, 141 Northwest Pointpublication, it has been published continuously since 1948. PEDIATRICS is owned, PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

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Stability of Cognitive Outcome From 2 to 5 Years of Agein Very Low Birth Weight Children

WHATS KNOWN ON THIS SUBJECT: Very preterm children are atrisk for developmental problems and, therefore, a systematicfollow-up is important. However, the relevance of early follow-upof cognitive development has been questioned because of thedivergent data on the prognostic value of early measures.

WHAT THIS STUDY ADDS: Good stability of cognitive developmentwas found between the ages of 2 and 5 years. Well-conductedassessment of cognitive development in infancy is both reliable toanticipate later development and clinically valuable to identifythose children who need developmental support.

abstractOBJECTIVE: This study assessed the stability of cognitive outcomes ofpremature, very low birth weight (VLBW; #1500 g) children.

METHODS: A regional cohort of 120 VLBW children born between 2001and 2004 was followed up by using the Bayley Scales of Infant Devel-opment, Second Edition, at 2 years of corrected age and the WechslerPreschool and Primary Scale of IntelligenceRevised at the age of 5years. The Mental Development Index (MDI) and the full-scale IQ (FSIQ)were measured, respectively. A total of 168 randomly selected healthyterm control children born in the same hospital were assessed forMDI and FSIQ.

RESULTS: In the VLBW group, mean6 SD MDI was 101.26 16.3 (range:50128), mean FSIQ was 99.3 6 17.7 (range: 39132), and the corre-lation between MDI and FSIQ was 0.563 (P, .0001). In the term group,mean MDI was 109.8 6 11.7 (range: 54128), mean FSIQ was 111.7 614.5 (range: 73150), and the correlation between MDI and FSIQ was0.400 (P , .0001). Overall, 83% of those VLBW children who hadsignificant delay (2 SD or less) according to MDI had it also in FSIQ.Similarly, 87% of those children who were in the average range in MDIwere within the average range in FSIQ as well.

CONCLUSIONS: Good stability of cognitive development over time wasfound in VLBW children and in term children between the ages of 2and 5 years. This conclusion stresses the value and clinical signifi-cance of early assessment at 2 years of corrected age. However, wealso emphasize the importance of a long-term follow-up covering adetailed neuropsychological profile of these at-risk children. Pediatrics2012;129:503508

AUTHORS: Petriina Munck, MA,a,b Pekka Niemi, PhD,b

Helena Lapinleimu, MD, PhD,a,c Liisa Lehtonen, MD, PhD,a,c

Leena Haataja, MD, PhD,c,d and the PIPARI Study Group

Departments of aPediatrics and dPediatric Neurology, TurkuUniversity Hospital, Turku, Finland; and Departments ofbPsychology and cMedicine, University of Turku, Turku, Finland

KEY WORDSintelligent quotient, Mental Development Index, very preterm

ABBREVIATIONSBSID-IIBayley Scales of Infant Development, Second EditionFSIQfull-scale IQMDIMental Development IndexVLBWvery low birth weightWPPSI-RWechsler Preschool and Primary Scale of IntelligenceRevised

Ms Munck contributed substantially in designing the study,acquisition of data, data analysis, drafting the article, and in thefinal approval of the version to be submitted; and Drs Niemi,Lapinleimu, Lehtonen, and Haataja contributed substantially indesigning the study, revising the content of the draft critically,and in the final approval of the version to be submitted.

www.pediatrics.org/cgi/doi/10.1542/peds.2011-1566

doi:10.1542/peds.2011-1566

Accepted for publication Nov 11, 2011

Address correspondence to Petriina Munck, MA, Department ofPediatrics, Turku University Hospital, Kiinamyllynkatu 4-8, 20520Turku, Finland. E-mail: [email protected]

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright 2012 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors have indicated they haveno financial relationships relevant to this article to disclose.

FUNDING: This work was supported by grants from SundellsStiftelse, The Finnish Cultural Foundation, The Eemil AaltonenFoundation, and the Foundation for Paediatric Research/South-Western Finnish Fund of Neonatal Research.

PEDIATRICS Volume 129, Number 3, March 2012 503

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Very preterm birth has been shown torelate strongly with cognitive impair-ments through childhood.18 However,a positive trend for improvement incognitive development has been repor-ted,911 but follow-up data of thesepromising findings are not yet available.

Because very preterm children are atrisk for developmental problems, manyhospitals have follow-up programs thatinclude assessment of cognitive abili-ties. However, timing of the follow-up,the length of the follow-up period, andthe applied methods vary betweencountries and centers, thus makinginternational comparisons difficult. Therelevance of early cognitive measures(usually at 2 years of corrected age)for prediction of long-term outcomehas been questioned because of di-vergent data on their prognostic value.Some longitudinal studies have shownthat early measures give too pessi-mistic a view of the long-term cognitiveoutcome, and it has been suggestedthat preterm children would graduallyclose the gap to their term peers, atleast to some degree.12,13 It has alsobeen suggested that the number ofpreterm children without any earlycognitive deficits would decrease overthe years and at the same time, thenumber of children having early moder-ate to severe disabilities would diminish,both of which would increase the num-ber of children with minor problems.14

Conversely, good stability of the scoresmeasuring cognitive development overtime has been reported.1518

In the current study population, a goodcognitive outcomewas found at the ageof 2 years.11 The aims of the currentstudy were: (1) to study the clinicalsignificance of the assessment con-ducted at the age of 2 years by studyingthe stability of cognitive development ina regional very low birth weight (VLBW)cohort between the ages of 2 and 5years; and (2) to compare the stabilitywith term controls. Our hypothesis was

that a well-conducted assessment ofcognitive development at the correctedage of 2 years would show good cor-relation with assessment at the age of5 years.

METHODS

Participants

This study is a part of a multidisciplin-ary follow-up study, PIPARI (Developm-ent and Functioning of Very Low BirthWeight Infants from Infancy to SchoolAge). All VLBW (#1500 g and preterm)infants born at Turku University Hos-pital in the period between 2001 and2006 and living in the catchment areawere eligible. The current study sampleconsisted of infants born to familiesspeaking either Finnish and/or Swedish(the official languages of Finland) be-tween 2001 and 2004. Infantswith severecongenital anomalies or a diagnosedsyndrome affecting their developmentwere excluded.

A total of 199 healthy term infants bornat the same hospital between 2001 and2003 were recruited to the controlgroup. Term infants were born at orabove 37 gestational weeks into Finnishand/or Swedish-speaking families andwerenotadmitted toaNICUduring theirfirst week of life. The exclusion criteriawerecongenitalanomaliesorsyndromes,mothers self-reported use of illicit drugsor alcohol during the pregnancy, andbirth weight 2.0 SD or less (small forgestational age) according to age andgender-specific Finnish growth charts.The research psychologist (Ms Munck)recruited the term group by asking theparents of the first boy and the first girlborn in each week to participate. At re-fusal, the parents of the next boy/girl ofthe week were approached.

The ethics review committee of theHospital District of the South-WestFinland approved the PIPARI study pro-tocol in December 2000. All parentswho agreed to participate gave written

informed consent after written and oralinformation was provided.

Assessment of CognitiveDevelopment

Bayley Scales of Infant Development,Second Edition

At 2 years of corrected age (from 1week to 1 month), cognitive develop-ment was assessed by using Finnishtranslation11 of the Mental DevelopmentIndex (MDI) of the Bayley Scales of InfantDevelopment, Second Edition (BSID-II).19

MDI was used both as a continuousvariable (mean6 SD: 1006 15) and asa categorized variable. A significant de-laywas defined as anMDI,70 (2 SD orless) and a mild delay as 70 to 84 (2 SD, MDI , 1 SD). MDI $85 (1 SD ormore) was considered average.

Wechsler Preschool and PrimaryScale of IntelligenceRevised

At the age of 5 years (from 1 week to 2months), cognitive development wasassessed with the short version ofWechsler Preschool and Primary Scaleof IntelligenceRevised (WPPSI-R), Finnishtranslation (1995).20 Three verbal (in-formation, sentences, and arithme-tic) and 3 performance (block design,geometric design, and picture comple-tion) subscales were selected based onthe strongest correlation with the full-scale IQ (FSIQ). FSIQ was used both asa continuous variable (mean: 1006 15)and as a categorized variable. A signifi-cant delay was defined as FSIQ,70 (2SD or less) and a mild delay as 70 to 84(2 SD, FSIQ, 1 SD). FSIQ$85 (1SD or more) was considered average.The psychologist who assessed thechildren at the age of 5 years was blin-ded to childrens perinatal history andto MDI status to avoid the bias of in-formation of the previous assessment.

Statistical Analysis

Statistical analyses were conducted byusing SAS version 9.2 (SAS Institute, Inc,

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Cary, NC). The association between MDIandFSIQwasstudiedbyusingPearsonscorrelation. Independent sample t testswere used when continuous MDI andFSIQ values were compared betweenVLBW and term children. Cohensweighted k was calculated to estimatethe agreement between of categorizedMDI and categorized FSIQ. Receiver op-erating characteristic curve analysiswasperformed to study the sensitivity andspecificity of MDI on categorized FSIQ.MDI was used as a continuous vari-able and FSIQ as a categorized variable(significant delay and mild/significantdelay).

RESULTS

Characteristics

A total of 184 VLBW infants were born inthe period between 2001 and 2004. Ofthese, 28 (15%) died during the neo-natal period. Finnish and/or Swedishwere not the only languages of thefamilies of 15 infants (10%). One infantwas excluded because of multipleanomalies. The families of 4 of the 140eligible infants (3%) refused to partici-pate or were withdrawn from the study.A total of 136 VLBW infants wereassessed at the corrected age of 2years. Of these, 124 children (91%) werealso assessed at the age of 5 years. Fourof these children were too severelyhandicapped to be assessed. However,they were included in the analysis of thecategorized data and were classified ashaving a significant cognitive delay atthe age of 5 years. Families of 8 terminfants (4%) refused to participate inthe follow-up at the age of 2 years. Of theremaining 191 children, 168 (88%) werealso assessed at the age of 5 years. Thecharacteristics of the children andparents, along with the neonatal data ofVLBW infants, are shown in Table 1.

Cognitive Development

In the VLBW group, mean 6 SD MDIwas 101.26 16.3 (range: 50128), mean

FSIQ was 99.3 6 17.7 (range: 39132),and the correlation between MDI andFSIQ was 0.563 (P, .0001). In the termgroup, mean MDI was 109.8 6 11.7(range: 54128), mean FSIQ was 111.76 14.5 (range: 73150), and the cor-relation between MDI and FSIQ was0.400 (P , .0001). VLBW children hadlower mean MDI and FSIQ (both com-parisons: P , .001) compared withterm controls.

MDI and FSIQ were studied as catego-rized variables, and the stability of thedevelopmental categorywascalculatedbetween the 2 time-points. Four VLBWchildren who were too severely handi-capped to be assessed at the age of5 years were added to the significantdelay group. A total of 83%of the childrenwith significant delay in MDI (n = 6) alsohad significant delay in FSIQ. Similarly,

87% of the children in the average rangein MDI (n = 113) were within the averagerange also in FSIQ. Children with milddevelopmental delay at the age of 2years (n = 5) were distributed in allgroups at the age of 5 years. Cohens kwas 0.61, showing a substantial agree-ment of stability. Data are presented inTable 2. Receiver operating character-istic curve analysis reveals a sensitivityand specificity of MDI on significant de-lay (Fig 1) and mild delay (Fig 2).

There were no term children with sig-nificant developmental delay at eitherage point. Of the term children withinthe average range at the age of 2 years(n = 164), 97% were within the averagerange also at the age of 5 years. Ofthose 4 term children who had milddelay at the age of 2 years, 3 had im-proved in their development and only

TABLE 1 Infant Characteristics of VLBW and Term Children and the Length of Parental Education

Variable VLBW (n = 124) Term (n = 168)

Prenatal corticosteroids 117 (94) Multiple birth 38 (31) 1 (1)Birth weight (g)Mean (SD) [min, max] 1061 (260) [400, 1500] 3659 (454) [2570, 4980]

Gestational age (weeks)Mean (SD) [min, max] 28.7 (2.8) [23.3, 35.9] 40.1 (1.2) [37.1, 42.3]

Small for gestational agea 49 (40) 0Male 67 (54) 81 (48)Apgar ,6 at 5 min 28 (23)b 0Days on ventilatorMean 6 SD [min, max] 9.4 (12.7) [0, 50]

Postnatal steroids 21 (17) Chronic lung diseasec 19 (15) Ductal ligation 17 (14) Sepsis or meningitis 30 (24) Intestinal perforation (NEC included) 7 (6) Retinopathy of prematurity $grade III 3 (2) Hydrocephalus with a shunt 4 (3) Days in hospital, mean 6 SD [min, max] 59.6 (32.8) [3, 183] Maternal educationd

9 y 14 (11) 6 (4).912 y 36 (29) 53 (36).12 y 123 (59) 89 (60)

Paternal educatione

9 y 12 (10) 15 (11).912 y 69 (56) 59 (41).12 y 42 (34) 69 (48)

Data are presented as frequency (percentage) if not otherwise indicated. min, minimum; max, maximum; NEC, necrotizingenterocolitis. , indicates that treatments, morbidities, and operations were valid only for the VLBW data.a Defined as a birth weight of 2.0 SD or less, according to the age- and gender-specific Finnish growth charts.b Missing, n = 2.c Defined as a need for supplemental oxygen at the age of 36 gestational weeks.d Missing 1 patient and 20 patients, respectively, from each group.e Missing 1 patient and 25 patients, respectively, from each group.

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1 child remained in the mild delaygroup. Cohens k was 0.18, showinga slight agreement of stability. Data arepresented in Table 2.

DISCUSSION

Opinions regarding the stability of earlymeasures of cognitive outcome havevaried largely, suggesting that there isa poor predictive validity to later as-sessments12,13 and that early measurescan predict the later cognitive outcomequite reliably.1518 In the current study,a strong correlation was found betweenMDI measured at 2 years of age andFSIQ measured at the age of 5 years,

suggesting that early assessment ofcognitive development is significantlyassociated with cognitive developmentat least up to the age of 5 years. Thestability of the classification of cogni-tive outcome was high in normally de-veloping and in significantly delayedgroups. This finding implies that earlyassessment of cognitive developmentis clinically important. Children with sig-nificant developmental problems shouldbe addressed to appropriate diagnos-tic, etiologic, and rehabilitation servicesas early as possible in their develop-ment. Conversely, parents of childrenwith milder problems should also be

provided with counseling to supporttheir childs possible specific needs.

Cognitive development of the currentstudy population has been shown to berelativelygood,as themeanvalueofMDIhas been at the level of BSID-II norms atthe age of 2 years.11 Our study con-firmed this developmental pattern be-cause VLBW children performed at thelevel of WPPSI-R norms. Despite thisfinding, the difference to control groupwas almost 1 SD also at the age of 5years. Our control group was, however,selected because it included onlyhealthy-born infants excluding all pre-term and small for gestational ageinfants, those requiring NICU admissionfor any reason, and those who wereexposed antenatally to alcohol or illicitdrugs. In addition, the average educa-tion level in Finnish society is high, freehealth care is provided to all, and thevariation in socioeconomic backgroundis smaller than inmany other countries.Therefore, these findings may not bedirectly generalized to other popula-tions. Importantly, however, the socio-economic background factors (level ofparental education, which correlatesstrongly with socioeconomic status)did not differ between VLBW and terminfants, which served to differentiatethe VLBW population in the currentstudy from those of many other coun-tries. This condition makes it possibleto study the impact of prematuritywithout the confounding effects of so-cioeconomic factors.

Children did not take part in anystructured intervention program in thisstudy. However, all of the infants whohad a significant motor delay receivedphysiotherapy. If there were any con-cerns about the development or thebehavior of the child either at the ageof 2 or 5 years, he or she was referredto appropriate local rehabilitation serv-ices. In Finland, most children enter thecommunal day care system. This sys-tem provides appropriate support for

TABLE 2 VLBW Children and Term Children With a Significant Delay (,70), Mild Delay (7084),and Cognitive Development Within the Average Range ($85) on the Basis of MDI Scores

Study Group FSIQ ,70 FSIQ 7084 FSIQ $85 Total

VLBWMDI ,70 5 (83) 1 (17) 0 6MDI 7084 2 (40) 1 (20) 2 (40) 5MDI $85 2 (2) 13 (11) 98 (87) 113Total 9 15 100 124

TermMDI ,70 0 0 0 0MDI 70-84 0 1 (25) 3 (75) 4MDI $85 0 5 (3) 159 (97) 164Total 0 15 100 168

Data are presented as number and (percentage). Four VLBW children who were too severely handicapped to be assessed atthe age of 5 years were added to the group of significant delay. Cohens k was 0.61 for the VLBW population, showinga substantial agreement of stability, and 0.18 for the term population, showing a slight agreement of stability.

FIGURE 1Receiveroperatingcharacteristic curveanalysisof thesensitivityandspecificityofMDIonseveredelay inFSIQ.


all children with developmental orbehavioral concerns, and no IQ dis-crepancy is required for inclusion.Trained nursery school teachers sup-port their development in daily playsituations.

The strengths of this study include highcoverage of the VLBW children with along follow-up period. Standardizedmethods were used for follow-up, anda regional control group was used inaddition to the normative data of theBSID-II and WPPSI-R. Different psychol-ogists conducted the assessment in 2different time-points to avoid the bias ofthe previous assessment. Strong cor-relation was found despite the fact thatdifferent methods had to be used tomeasure cognitive development at dif-ferent age point, as bothmethods coveronly limited age-span. However, bothmethods provide information about theindividual development compared withage-appropriate normative data, andthey use the same scaling. An additionalstrength was that all children partici-pated in the assessment within a verystrict timelimit.Timingof theassessmentwas chosen to be both developmentallyand clinically relevant. From the deve-lopmental point of view, 2 years is an

interesting time window as motor de-velopment is less dominant and lan-guage development is in a very activephase. Clinically, it is important toidentify those children who have de-velopmental problems as early andas accurately as possible to providethem with appropriate services. Fiveyears is a more reliable age of assess-ment considering the later academicperformance at school age, but thereis still time for preventive interventionsif child is at risk for academic failure.

Study limitations include that theBSID-IIand WPPSI-R were used instead of thenew versions (the Bayley Scales of In-fant and Toddler Development, ThirdEdition, and the third edition of theWPPSI), as these tests were not avail-able in Finland at the time of the study.It is also important to stress that mea-sures of cognitive development, suchas used here, do not allow inferencesabout neuropsychological deficits thatcan be found with more specific meas-ures or that may become evident onlylater in the childs development. Lowcognitive capacity is usually accom-panied with neuropsychological dif-ficulties, but average cognition doesnot imply that one would be free from

more specific neuropsychological prob-lems. Therefore, other methods are alsoneeded to complement follow-up ofat-risk preterm children. Long-termfollow-up is needed to identify specificproblems that may become evident onlylater in the development. However, it isimportant to offer families with asaccurate information as it is possibleto gain at the childs different deve-lopmental stages.

CONCLUSIONS

The current study revealed that thecognitive outcome of a regional VLBWcohort measured at the age of 2 yearswas significantly associated with cog-nitive outcome at the age of 5 years. Wesuggest that a well-conducted assess-ment is relevantandvaluablealsoat theearly age, making it possible to supportthose children with developmentalproblems. However, at the same time,we stress the importance to follow-up these at-risk children longitudi-nally and with methods covering bothcognitive and neuropsychological de-velopment.

ACKNOWLEDGMENTSThe PIPARI Study Group includes: SatuEkblad, RN; Mikael Ekblad, medical stu-dent; Eeva Ekholm, MD, PhD; LeenaHaataja, MD, PhD; Mira Huhtala, MD;Pentti Kero, MD, PhD; Riikka Korja, PhD;Harry Kujari, MD; Helena LapinleimuMD, PhD; Liisa Lehtonen, MD, PhD; MarikaLeppnen, MD; Annika Lind, PhD; HannaManninen, MD; Jaakko Matomki, MSc;Jonna Maunu, MD, PhD; Petriina Munck,MA; Pekka Niemi, PhD; Pertti Palo, MD,PhD; Riitta Parkkola, MD, PhD; JormaPiha, MD, PhD; Liisi Rautava, MD, PhD;Pivi Rautava, MD, PhD; Milla Ylijoki,MD, PhD; Hellevi Rikalainen, MD, PhD;Katriina Saarinen, Physiotherapist; ElinaSavonlahti, MD; Matti Sillanp, MD, PhD;Suvi Stolt, PhD; Pivi Tuomikoski-Koiranen,RN; Anniina Vliaho, MA; and Tuularimaa, MD, PhD.

FIGURE 2Receiver operating characteristic curve analysis of the sensitivity and specificity of MDI on severe andmild delay in FSIQ.

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DOI: 10.1542/peds.2011-1566; originally published online February 27, 2012; 2012;129;503Pediatrics

the PIPARI Study GroupPetriina Munck, Pekka Niemi, Helena Lapinleimu, Liisa Lehtonen, Leena Haataja and

Weight ChildrenStability of Cognitive Outcome From 2 to 5 Years of Age in Very Low Birth

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