Background Since the mid-1980s, increasing numbers of childrenwith birth weights under 750 g have survived to school age.
Methods We matched a regional cohort of 68 surviving childrenborn from 1982 through 1986 with birth weights under 750 g (mean,670 g; gestational age, 25.7 weeks) with 65 children weighing750 to 1499 g at birth and 61 children born at term. Growth,neurosensory status, and functioning at school age in the threegroups were compared. Associations of biologic and social riskfactors with major developmental outcomes were examined by meansof logistic-regression analyses.
Results Children with birth weights under 750 g were inferiorto both comparison groups in cognitive ability, psychomotorskills, and academic achievement. They had poorer social skillsand adaptive behavior and more behavioral and attention problems.The mean (±SD) Mental Processing Composite score forthe cohort was 87 ±15, as compared with 93 ±14for children with birth weights of 750 to 1499 g and 100 ±13for children born at term (P<0.001). The rates of mentalretardation (IQ <70) in the three groups were 21, 8, and2 percent, respectively; the rates of cerebral palsy were 9,6, and 0 percent; and the rates of severe visual disabilitywere 25, 5, and 2 percent. Major cerebral ultrasonographic abnormalitieswere associated with mental retardation (odds ratio, 5.4; 95percent confidence interval, 1.8 to 15.8) and cerebral palsy(odds ratio, 15.2; 95 percent confidence interval, 3.0 to 77.4).Oxygen dependence at 36 weeks of corrected age was associatedwith mental retardation (odds ratio, 4.5; 95 percent confidenceinterval, 1.2 to 10.7) and severe visual disability (odds ratio,4.3; 95 percent confidence interval, 1.3 to 14.2). Social disadvantage,though associated with several neuropsychological outcomes,was not associated with major developmental impairment.
Conclusions Children with birth weights under 750 g who surviverepresent a subgroup of very-low-birth-weight children who areat high risk for neurobehavioral dysfunction and poor schoolperformance.
During the past decade, advances in perinatal care have resultedin increases in the survival of extremely small and immatureinfants1,2. Whereas few infants with birth weights below 750g were actively treated before the 1980s, treatment is now acceptedpractice for most infants born in North America with birth weightsof at least 500 g, those born at 24 or more weeks' gestation,or both. The high rates of neonatal morbidity among extremely-low-birth-weightinfants who survive have been well documented, as has a 20 to50 percent rate of neurodevelopmental impairment during earlychildhood1,2. However, few reports have discussed outcomes atearly school age, which are critical indicators of how thesechildren will ultimately function in society3,4,5,6.
We studied the health and developmental outcomes at early schoolage of children with birth weights below 750 g who were bornfrom 1982 through 1986, the period when increasing numbers ofsurvivors were first reported1. We hypothesized that such childrenwould function at lower levels at school age than either childrenwith birth weights of 750 to 1499 g or classmates born at term.
Methods
Study Group
The study subjects included the survivors of the cohort of 243children with birth weights below 750 g who were born from 1982through 1986 in a six-county region of Ohio including the greaterCleveland area and who were admitted to the three tertiary-levelneonatal intensive care units in the region. During this period,the region had 147,732 live births; 408 (0.3 percent) of theseinfants weighed 500 to 749 g. One hundred seventy-seven wereborn in the three perinatal centers and the remainder in communityhospitals; 66 of these infants were deemed viable and were transferredto two of the centers. Seventy-three (30 percent) of the 243children born weighing less than 750 g who were admitted tothe three neonatal intensive care units survived to discharge.At school age, 68 of the 73 survivors (93 percent) were availablefor study. We were unable to recruit the remaining 5 children,but with respect to mean birth weight (684 g), gestational age(26 weeks), and the occurrence of early sequelae, they weresimilar to the 68 children who were followed. We had informationthat one was blind and that two functioned in the low-normalrange.
Comparison Groups
Two comparison groups were recruited, a group of children bornweighing 750 to 1499 g and a group born at full term. For eachchild weighing below 750 g, we selected the next survivor whowas born weighing 750 to 1499 g, was treated at the same perinatalcenter, and was of the same race and sex. Of the 68 matches,28 children born weighing 750 to 1499 g could not be scheduledfor assessment, and 1 child had esophageal atresia with multiplesequelae related to the malformation rather than to prematurity.The next child born weighing 750 to 1499 g and appropriatelymatched was then selected to replace the originally matchedchild. Three children were not assessed because of multiplemissed appointments. Thus, the comparison group of childrenwith birth weights of 750 to 1499 g included 65 children ofschool age.
The comparison group of children born at term was formed byrandomly selecting a full-term child from the same classroomas the child born weighing less than 750 g who was of the samesex, race, and birth date, within three months. Matches werenot selected for seven children (five were in schools out ofthe city, one was not at school, and the parent of one refusedpermission to contact the school). For the 61 children bornat term who were selected, 10 parents of the children originallymatched declined to participate, and a second match with a full-termchild was thus selected.
School-Age Assessments
The children with birth weights below 750 g were examined ata mean (±SD) age of 6.7 ±0.9 years, those bornweighing 750 to 1499 g at 6.9 ±0.9 years, and the childrenborn at term at 7.0 ±0.9 years. A complete physical andneurologic examination was performed. Hearing was measured withpure-tone audiometric screening, and visual acuity was testedwith Snellen's letters. The children were classified neurologicallyas normal or abnormal (i.e., having a major neurologic or sensoryabnormality). The psychometric testing of the children includedassessments of neuropsychological abilities and academic achievementas described in Table 17,8,9,10,11,12,13,14,15,16,17,18,19.All tests were scored on the basis of the child's postnatalage. IQ-equivalent scores were assigned to all children on thebasis of the Kaufman Assessment Battery for Children MentalProcessing Composite Short Form or, in three cases of childrenwho could not be tested with these procedures, with alternativetests. An IQ equivalent of 55 was assigned to five childrenwho could not be tested by any procedures because of severeneurosensory disability.
Table 1. Measures of Neuropsychological Achievement.
A parent, usually the mother, was interviewed to obtain backgrounddemographic, health, and developmental data, and both the parentand the teacher completed questionnaires on the child's behaviorand performance at school (Table 1)20,21,22,23,24.
A composite score for social risk, which we have used previously,25included maternal race (with scores of 0 for white and 1 forblack), maternal education (0 for high school or above and 1for less than a high-school education), and marital status (0for married and 1 for unmarried). The composite scale rangedfrom 0, for lowest social risk, to 3, for highest social risk.In this study the composite scale had a higher correlation withthe Kaufman Assessment Battery in the comparison group bornat term (-0.58) than did any of the components analyzed separately.
Study Design and Statistical Analysis
We compared the three groups of children with regard to outcomesat early school age. The outcome measures were standardizedfor age before analysis26. Overall differences between groupson continuous measures of outcome were examined by an analysisof variance or a multivariate analysis of variance. The alphalevel was set at 0.05 for each domain, and Bonferroni adjustmentsin the alpha level were used in making univariate comparisonswithin multiple-measure domains. Two-tailed tests were usedto examine differences between each pairing of the three groups.
Logistic regression was used to assess associations of socialand neonatal risk factors with major developmental outcomesamong children in the two very-low-birth-weight (<1500-g)groups27. The outcomes considered in these analyses includedmental retardation (IQ equivalent, <70), cerebral palsy,and visual disability (i.e., unilateral or bilateral blindnessor vision 20/200 without glasses, in at least one eye). Theindex of social disadvantage was first entered into these analysesas a covariate. Five neonatal risk factors were then enteredin a stepwise fashion to identify the factors that best predictedeach outcome, independently of social status. These includedsepticemia, necrotizing enterocolitis, maximal serum bilirubinconcentration greater than 10 mg per deciliter (171 µmolper liter), apnea of prematurity, and severe cerebral ultrasonographicabnormality (grade 3 or 4 periventricular bleeding,28 persistentventricular dilatation, or both). Interaction terms (the effectof each neonatal complication according to birth-weight group)were entered into the logistic-regression equations after thegroup and all neonatal-complication factors had been entered.Chronic lung disease (defined as dependence on oxygen for atleast 36 weeks of corrected age [i.e., postmenstrual plus postnatalage] vs. dependence on oxygen for less than 36 weeks of correctedage29) was then entered in the regression equations, with controlfor social disadvantage and those neonatal-complication factorsthat were found to be associated with outcome. We separatedthe early neonatal correlates of outcome from the later measuresof chronic lung disease in order to identify early prognosticindicators that might be relevant to critical therapeutic decisionsin the neonatal period. Interactions of oxygen dependence withgroup were entered in the final stage of the analyses.
The study protocol was reviewed and approved by the institutionalreview board at each center. Informed consent was obtained fromthe parents of the study children.
Results
Comparison of Demographic and Birth Data
The three groups of infants were similar with regard to theirmothers' age, marital status, and racial background (Table 2).There were no differences between groups in the composite indexof social disadvantage. Sixty-six percent of the sample wasfemale because of the greater survival of girls in the groupborn weighing less than 750 g.
Table 2. Maternal Demographic Risk Factors and Perinatal Data.
Perinatal and Neonatal Risk Factors in the Very-Low-Birth-Weight Groups
There were no material differences between the two very-low-birth-weightgroups with regard to the rate of maternal complications ofpregnancy, the mode of delivery, or the rate of infant transfersfrom community hospitals (Table 3). All children were born beforethe use of surfactant. Infants weighing less than 750 g at birthhad significantly higher rates of intrauterine growth failure,respiratory distress requiring assisted ventilation, patentductus arteriosus, apnea of prematurity, and septicemia. Significantlyfewer infants in this group had normal cerebral ultrasonogramsthan did infants weighing 750 to 1499 g at birth. Shunt-dependenthydrocephalus developed in two children in each group. The groupweighing less than 750 g at birth had significantly longer dependenceon oxygen and mechanical ventilation and longer hospital stays.Forty-three percent of these infants required oxygen at 36 weeksof corrected age, as compared with 11 percent of the infantswith birth weights of 750 to 1499 g.
Table 3. Perinatal and Neonatal Descriptors of the Very-Low-Birth-Weight Children.
Neurosensory and Physical Outcomes
Ten children weighing less than 750 g at birth (15 percent)had major neurosensory impairment, including cerebral palsy,blindness, and deafness, as compared with five of those weighing750 to 1499 g (8 percent) and none of those born at term. Twochildren in each of the very-low-birth-weight groups could notwalk. Table 4 summarizes the abnormal neurosensory and growthoutcomes. Selected results are shown in Figure 1.
Figure 1. Percentage of Children in Each Study Group with Each of Four Major Impairments.
Cerebral palsy was defined to include hemiplegia, diplegia, or quadriplegia; visual impairment to include unilateral or bilateral blindness or visual acuity 20/200 without glasses in at least one eye; and subnormal head size and height as less than 2 SD below the mean for the child's age.31,32.
Developmental Outcomes
The mean (±SD) Mental Processing Composite score forthe children weighing less than 750 g at birth who were testedwas 87 ±15, as compared with 93 ±14 for the childrenweighing 750 to 1499 g and 100 ±13 for the children bornat term. As compared with the children born at term, the groupborn weighing less than 750 g had significantly poorer scoreson all the measures listed in Table 1, except for one test ofverbal memory. Those born weighing less than 750 g had significantlypoorer outcomes than those weighing 750 to 1499 g with regardto cognitive ability, language-processing skills, gross motorand visual motor function, attention skills, academic achievement,ratings of school performance by a parent or a teacher, behaviorand social skills, and adaptive behavior.
The fact that the groups also differed in the frequency of severedeficits in test performance or elevated ratings of behavioralproblems (Table 5) suggests that the differences between groupsare clinically meaningful. Representative results are shownin Figure 2. Differences in measures of cognition, psychomotorfunction, attention, and academic achievement remained significantwhen the comparisons were further restricted to children whowere both neurologically intact and of normal intelligence (MentalProcessing Composite score 85).
Figure 2. Percentage of Children in Each Study Group with Subnormal Functioning.
Subnormal functioning was defined as a standard score of less than 70 for cognitive function,7 academic skills,19 visual motor function,14 and adaptive function24 and a score of less than 30 for gross motor function.13.
Relation of Social Risk and Gestational Age to Outcome
The index of social disadvantage was significantly correlatedwith many of the outcome measures, including the IQ equivalent(r = -0.34, P<0.001), the Vineland Adaptive Behavior Compositescore (r = -0.21, P<0.01), the Woodcock-Johnson Skills Cluster(r = -0.17), and the Expressive One-Word Picture VocabularyTest (r = -0.42, P<0.001). Correlations with measures ofmotor performance and behavioral-problem ratings were not significant.Gestational age was significantly related to the IQ equivalentin the two very-low-birth-weight groups combined (r = 0.19,P<0.03), but not when each group was considered separately.
Association between Social Risk and Medical Factors and Very-Low-Birth-Weight Outcomes
According to logistic-regression analysis, the index of socialdisadvantage was not associated with any of the three majordevelopmental outcomes. Neonatal complications, however, wereassociated with all three outcomes. The stepwise entry intothe analysis of the five neonatal complications under considerationrevealed that higher risks of both mental retardation and cerebralpalsy were associated with severe ultrasonographic abnormality.Even after we controlled for social disadvantage, the odds ratiosfor a child's having mental retardation or cerebral palsy, givena severely abnormal ultrasonogram, were 5.4 (95 percent confidenceinterval, 1.8 to 15.8) and 15.2 (95 percent confidence interval,3.0 to 77.4), respectively. After the entry of social disadvantageand cerebral-ultrasonogram status into the equation, dependenceon oxygen at 36 weeks' corrected age was also associated withmental retardation and visual disability. The adjusted oddsratios for mental retardation and visual disability, given dependenceon oxygen at 36 weeks' corrected age, were 4.5 (95 percent confidenceinterval, 1.2 to 10.7) and 4.3 (95 percent confidence interval,1.3 to 14.2), respectively. The associations of severe ultrasonographicabnormalities and oxygen dependence with adverse outcomes didnot vary with birth-weight group. Furthermore, the entry ofthe very-low-birth-weight group (<750 g vs. 750 to 1499 g)into the equation after ultrasonographic status and oxygen dependencehad already been added did not significantly improve the predictionof any of the three outcomes. This last finding suggests thatthe effects of birth weight were mediated by neonatal complications.Two measures available at discharge, the modified Hobel neonatalrisk score, which we have used previously,25 and the lengthof the hospital stay, also predicted mental retardation, cerebralpalsy, and severe visual disability.
Discussion
The results of this study of very-low-birth-weight childrenat early school age confirm our hypothesis that these childrenare at serious disadvantage in every skill required for adequateperformance in school. Twenty-one percent of our sample hadsubnormal mental abilities, and 45 percent required some specialeducation in school. A substantial percentage also had visualdisability and subnormal growth. This study presents regionaloutcomes, avoiding the selection bias inherent in hospital-basedstudies.
Previous reports of the school-age outcomes of very-low-birth-weightchildren included very few children weighing less than 750 gat birth, because few survived before the 1980s. Our resultsare consistent with those of two small, hospital-based studies3,5.The only other regional outcome study reported a mean IQ of89 among 48 children born from 1977 to 1984 weighing less than800 g at birth4. We and other investigators have not correctedthe children's ages for preterm birth, since performance relativeto uncorrected age is the standard by which they are judgedat school.
Because of concern over the reliability of using gestationalages, most reports, including our own, examine outcome accordingto birth weight. The estimation of gestational age based onobstetrical information is problematic when the mothers havenot received prenatal care, whereas the postnatal assessmentof gestational age results in overestimates2. However, Johnsonet al. recently reported that 22 of 42 children born at lessthan 27 weeks' gestation had moderate-to-severe disability atfour years of age6.
The results of our study also confirm the hypothesis that althoughoutcomes at early school age are related to both social andbiologic risks, major developmental outcomes were more closelyassociated with neonatal complications than with social disadvantage.Of the biologic risk factors we considered, major cerebral abnormalityon ultrasonographic examination and dependence on oxygen at36 weeks' corrected age were associated with mental retardation.Major ultrasonographic abnormality was also associated withcerebral palsy, and prolonged oxygen dependence predicted severevisual impairment.
Poor outcomes at early school age after severe periventricularhemorrhage and cerebral atrophy have been previously described33,34.This report documents poor outcomes associated with cerebralabnormalities detected ultrasonographically in children withbirth weights of less than 750 g. We suspect that in some casesthe smallest and least mature infants with severe brain hemorrhageare allowed to die. This would explain why the rates of severeultrasonographic abnormality did not differ significantly betweenthe two very-low-birth-weight groups, whereas the rates of theother neonatal complications and medical outcomes, includingchronic lung disease, visual disability, and subnormal growth,were higher in the group weighing less than 750 g at birth.The significant relation of prolonged dependence on oxygen tooutcomes is probably due to multiple factors, including hypoxicepisodes and the effects of prolonged hospitalization and poorgrowth35. We have previously reported on the relation of subnormalhead growth to poor later outcomes25. In the current study,36 percent of the children with birth weights under 750 g hadsubnormal head sizes at school age, as compared with 14 percentof children with birth weights of 750 to 1499 g. The high ratesof visual impairment in the children we studied are consistentwith recent reports of poor visual outcomes in early childhoodfor children weighing less than 750 g at birth. We did not performophthalmologic fundal examinations, but reports from the children'sophthalmologists suggested that retinopathy of prematurity wasprimarily responsible for the visual impairment.
The known variations among institutions in neonatal mortalityand morbidity2 and their effects on regional outcomes may limitthe generalizability of our results to other regions. Furthermore,one of the problems inherent in neonatal follow-up studies isthat many years pass before outcomes can be fully evaluated.The children in this study were born before many recent innovationsin care, including surfactant therapy, treatment of chroniclung disease with steroids, and cryotherapy to ameliorate severeretinopathy of prematurity. There is no evidence that treatmentwith surfactant or postnatal steroids has decreased the rateof chronic lung disease among recent survivors38. Cryotherapycan decrease the rate of blindness, but its effects on lesssevere disorders of vision are still unclear39. The rate ofsevere ventricular hemorrhage may, however, have decreased40.
In summary, the results of this study indicate that survivinginfants with birth weights less than 750 g represent a distinctsubgroup of children whose extreme immaturity, low birth weight,or both predispose them to excessive pulmonary and central nervoussystem injury. These children are the survivors of only 0.3percent of live births in the region and will not contributesubstantially to the overall rate of school-age handicap; thesefacts, however, do not detract from the enormous expenditurein neonatal resources for each child or from the ongoing educationalburden on the child, family, and school system. Although programsof early-childhood intervention may have some compensatory influenceson development,41 they have little influence on structural deficits.The prevention of extreme prematurity is thus critical.
Supported by a grant (R01 HD26554) from the National Institutesof Health and by a Mental Retardation Training Grant (HD07176)from the National Institute of Child Health and Human Development.
We are indebted to Dr. John Moore (MetroHealth Medical Center,Cleveland), Dr. Lawrence Lilien (Fairview General Hospital,Cleveland), Dr. David Francis, Sharon Cohen, Mary Ann Ricci,Harriet Friedman, and Kathy Winter for their assistance in compilingand analyzing the data; to Dr. A.A. Fanaroff and Dr. Saeid B.Amini for their critical comments; and to Joyce Nolan for assistancein the preparation of the manuscript.
Source Information
From the Department of Pediatrics, School of Medicine (M.H., H.G.T., R.E., N.M.-M.), and the Department of Psychology (C.S.), Case Western Reserve University; and the Department of Special Education (N.K.), Cleveland State University -- both in Cleveland.
Address reprint requests to Dr. Hack at Rainbow Babies and Children's Hospital, University Hospitals of Cleveland, 11100 Euclid Ave., Cleveland, OH 44106.
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20/200 without glasses, in at least one eye). The index of social disadvantage was first entered into these analyses as a covariate. Five neonatal risk factors were then entered in a stepwise fashion to identify the factors that best predicted each outcome, independently of social status. These included septicemia, necrotizing enterocolitis, maximal serum bilirubin concentration greater than 10 mg per deciliter (171 µmol per liter), apnea of prematurity, and severe cerebral ultrasonographic abnormality (grade 3 or 4 periventricular bleeding,28 persistent ventricular dilatation, or both). Interaction terms (the effect of each neonatal complication according to birth-weight group) were entered into the logistic-regression equations after the group and all neonatal-complication factors had been entered. Chronic lung disease (defined as dependence on oxygen for at least 36 weeks of corrected age [i.e., postmenstrual plus postnatal age] vs. dependence on oxygen for less than 36 weeks of corrected age29) was then entered in the regression equations, with control for social disadvantage and those neonatal-complication factors that were found to be associated with outcome. We separated the early neonatal correlates of outcome from the later measures of chronic lung disease in order to identify early prognostic indicators that might be relevant to critical therapeutic decisions in the neonatal period. Interactions of oxygen dependence with group were entered in the final stage of the analyses. 
85). 
