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Environmental context of child development
Environmental context of child development A r n o l d J. Sameroff, Ph.D. From the Institute for Study of Developmental Disabilities, University of Illinois at Chicago
Pediatrics has been the discipline most concerned with the prevention of developmental disabilities. Among these disabilities are a variety of physical and behavioral disorders that require long-term intervention and treatment at great social cost. It has always been clear that disabilities affect the family and the community by the enormous drain on emotional and financial resources. It has been less obvious that the disabilities are in turn affected by parents and society. Prevention approaches that focus on the affected individual alone frequently have been found to be inadequate. The usual explanation for the ineffectiveness of such intervention programs is that the wrong treatment is being used. Another interpretation is that the treatment did not extend to a wide enough social context. In many cases, family and cultural factors may be more important than factors in the child for preventing developmental disabilities. This review is devoted to providing a balanced perspective on the factors that contribute to healthy psychologic outcomes in children. In this view, the biologic condition is only one ingredient in the developmental formula that will lead to intellectual and social-emotional competence. Whereas linkages have been found between some "germs" and specific biologic disorders, this has not been true for behavioral disorders. Attempts to prevent developmental disabilities in the sense of deterring a biologic factor will have meaning in a very small percentage of cases, although these cases may be the most severe and profound. On the other hand, the vast majority of identified handicaps are the result of factors more strongly associated with psychologic and social environment than of any intrinsic characteristics of the child. Between these two categories lie the high-risk graduates of neonatal intensive care units, whose risk for retardation is a complex function of the interplay between their biologic development and Reprint requests: Arnold J. Sameroff, Ph.D., Institute for the Study of Developmental Disabilities, University of Illinois, 840 S. Wood St., Chicago, IL 60612.
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experience. New approaches to biologic and behavioral development emphasize causal analyses based on probabilistic interactions of multiple factors) These approaches were required to explain paradoxes that occurred when explanations for a variety of disorders were restricted to linear causal models. Agent-disease models were most effective in understanding acute, primarily infectious diseases, in contrast to more chronic disorders: For chronic disorders, whether heart disease, cancer, or mental retardation, unfavorable outcomes are produced by a combination of biologic, psychologic, social, and environmental risks, usually involving complex interactions among these factors. The complexity of the relationships between germs, context, and disorder is illustrated by the study of cytomegalovirus.3 Congenital cytomegalovirus infections are HOME SES VLBW
Home Observation for Measurement of the Environment Socioeconomic status Very low birth weight
found in about 1% of babies born in the United States, with the highest rates in infants of teenage mothers of low socioeconomic status: Of those infected, fewer than 5% have symptoms. As a group, infants with subclinical infections had lower IQ scores than did noninfected comparison infants, and about 10% to 20% had later central nervous system deficits. However, these differences were found only between infected lower SES children and their peers. When similar comparisons were made between groups of infected and noninfected middle-class children, no IQ differences were found) For such disorders, at least two factors and probably more are involved in producing clinical symptoms. Because the combination of these factors varies in each individual, the probability that a disorder will result will vary. If we turn directly to the study of developmental disabilities, especially mental retardation, the necessity for
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the consideration of nonbiologic factors becomes even more apparent. Epidemiologic surveys in Sweden have found a prevalence of severe mental retardation in childhood of about 3:1000, compatible with rates of severe mental retardation in the United States. On the other hand, the prevalence of mild mental retardation in Sweden is about 4:1000, eight or ten times lower than rates recorded in the United States. Susser et al. 6 point out that these rates are related to the reduction in Sweden of cultural-familial retardation and evidence the powerful impact of the social environment on mental performance. Another indication of the role of environment in mild mental retardation is the percentage of such children with detectable clinical abnormalities. In Sweden, 40% of mildly retarded children have identifiable conditions, 7 whereas the comparable proportion in the United States is only 10%. In the Collaborative Perinatal Project of the National Institute of Neurological Diseases and Stroke, the proportion of cases with mild mental retardation and detectable abnormalities was 14% for white children and 6% for blacks, s Similarly, in an English study that compared rates of mild mental retardation in schools with high or low social standing, the rate for children with organic conditions was twice as high in the schools with low social standing, but the rate for mildly retarded children without clinical abnormalities was 15 times as high. 9 It can be argued that there are subtle biologic factors yet to be discovered that will explain mental retardation in all children, but there is a great deal of evidence to support an alternative hypothesis. This evidence is reviewed below. IDENTIFYING
TARGETS
FOR TREATMENT
To prevent developmental disabilities, a clear idea of the causes of the disorder is necessary. Because intellectual functioning requires cerebral activity, a biologic orientation would lead one to conclude that mental retardation must result from damage to the brain. Targets for treatment then become those factors that produce brain damage. The basis for the connection between developmental disabilities and perinatal factors was laid more than a century ago in the work of Little, l~ who first focused attention on asphyxia as a cause of brain damage in the child. The mechanism of such a connection remained elusive, but this did not prevent many investigators from proposing various cause-effect models. Gesell and Amatruda" popularized the concept of "minimal cerebral damage" as the causal link. The inability to document the linkage was attributed to the adjective "minimal," that is, undetectable. The empirical basis for such a connection was provided in the work of Pasamanick and Knobloch ~2 when they
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proposed the existence of a "continuum of reproductive casualty." In a series of retrospective studies in which they examined the delivery and birth histories of children with a variety of subsequent disorders, they were able to find a number of significant relationships. From these data they postulated a dimension running from gross neurologic disorders such as cerebral palsy and epilepsy at one extreme to a range of minor motor, perceptual, learning, and behavioral disabilities at the other. The more severe the disability (e.g., cerebral palsy in contrast to tics) the more severe the causal perinatal complication (e.g., maternal bleeding in contrast to cesarean section). TESTING
CAUSAL
HYPOTHESES
Retrospective studies, such as those of Pasamanick and Knobloch, are important for generating hypotheses; however, other approaches are necessary to test them. In a typical retrospective study, persons are identified who already have the disorder, and then the investigator looks into their early history to find some cause. Retrospective approaches, however, entail serious problems in subject selection, because only those subjects who have the later disorder are studied. By contrast, prospective research permits the selection of subjects with early characteristics thought to be implicated in the cause of the later disorder. If indeed asphyxia leads to brain damage and mental retardation, and if a group of infants who had asphyxia at birth were followed up, a significantly greater amount of retardation would be found in this group than in a control group of infants who did not have anoxia. Even if such a prospective connection were found, another explanation is possible. One of the ancillary findings of Pasamanick and Knobloch's epidemiologic work was that the absolute number of abnormalities of pregnancy was higher among poorer groups. Children from poorer families have poorer intellectual and social outcomes. ~3 Later lower intelligence scores could be a consequence of earlier medical problems, or they could be a consequence of the fact that poorer families have both more medical problems and children with intellectual problems. In one of the better of the longitudinal studies of the consequences of birth complications, Graham et al) 4 tried to overcome the inadequacies of previous studies that used either poor measures of anoxia at birth or poor measures of intelligence at follow-up. They argued that if a large variety of measures, including neurologic, personality adjustment, and perceptual-motor tasks, were utilized in a longitudinal study, the significant differences between the affected and control groups should be revealed. Several hundred infants from a St. Louis hospital were seen in the newborn period" and were followed up at 3 and 7 years of
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age.~6.17 As expected, when examined during the first days of life, anoxic infants were found to be impaired on a number of behavioral indices. ~4 When the performance on these measures was compared with a prognostic score based on the degree of anoxia experienced by the children, those infants with the poorest prognostic scores performed most poorly on the newborn assessments. At 3 years of age the children were tested with a battery of cognitive, perceptual-motor, personality, and neurologic tests, ~6 The group of anoxic infants scored lower than did controls on all tests of cognitive function, had more positive neurologic findings, and showed some personality differences, but there were no differences on tests of perceptualmotor functioning. At 7 years of age the children were again tested. ~7Surprisingly, significant IQ differences had disappeared between the anoxic group and the control population; of the 21 cognitive and perceptual measures, only two showed differences. The investigators were forced to conclude that anoxic newborn infants showed minimal impairment of functioning at 7 years and that efforts to predict current functioning on the basis of the severity of newborn medical status were highly unreliable. Many advances were made in diagnostic and assessment technology during the 1960s, but there was little change in the pattern of results among prospective studies of birth complications. Gottfried, ~s in a review of 20 investigations of the longitudinal effects of anoxia, came to conclusions similar to those of the St. Louis study, among which were that (1) intellectual consequences of perinatal anoxia are more prevalent in infants and preschoolers than in older children and adolescents; (2) anoxic subjects as a group are not mentally retarded; and (3) whether anoxic subjects are deficient in specific intellectual abilities is not known. The most compelling of the prospective longitudinal studies in neonates, if only for its magnitude, is the Collaborative Perinatal Project of the National Institute of Neurological Diseases and Stroke in the United States29 Between 1959 and 1965, more than 50,000 women and their infants were recruited at birth, primarily from clinic populations in 12 medical centers, to investigate the relationship between birth condition and later neurotogic or behavioral deficits. The first major report of developmental outcome was the analysis of the IQ scores of the sample when the children were 4 years of age. ~ The effects on intelligence of 169 prenatal, delivery, infant, and family variables were examined. The implicit causal hypotheses of the collaborative study were reflected in this set of measures: Only eight of the 169 variables examined were related to family characteristics; the remaining 161 were assessments of the medical and developmental condition of the mother and child through the first year of life. The surprising result of the 4-year analysis was that the
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intellectual outcome for children was far better explained by the small set of family factors than any combination of the multitude of biomedical variables. In the second major report on the intellectual development of the children from the collaborative study the focus moved from the general case of mental retardation to examine the cause of more specific learning disabilities?~ It is not surprising that children with low IQs do poorly in school. But what about children with normal intelligence who do poorly? The analysis of the development of these children was expected to offer new hope for the identification of specific biomedical causes of these school-age disorders. Whereas the cause of general mental retardation did not seem to be illuminated by analysis of the early medical condition of the child, perhaps more specific entities, such as learning disabilities, dyslexia, minimal brain dysfunction, hyperkinetic syndrome, or attention deficit disorder, might be better targets for biologic causal models. From a sample of 35,000 children tested at 7 years of age in the collaborative study, about a thousand were identified as having normal intelligence but poor school performance. This cohort was compared with a demographically matched sample of more than 6000 children with normal school performance to evaluate the contribution of perinatal conditions, behavior during the preschool period, and the child's social environment to problems of learning, reading, and hyperactivityl The most compelling result of the 7-year follow-up analysis was that even when specific conditions are studied, the primary causal factors reside not in the child's biomedical history but in the environment, that is, the social context of development. The authors concluded that their major findings support and augment the conclusions of others that "lower socioeconomic status, less maternal education, higher birth order, and larger family size are related to higher rates of academic failure" (Broman et al., 2~ p 92). The report of the school behavior of the large sample in the collaborative project supported the findings of many other studies that followed the development of smaller groups of children who had experienced perinatal complications. If social variables are ignored, there seems to be a correlation causal connection between birth complications and later lower IQ. When social status is included in the analysis, children from poorer SES groups are found to have the most perinatal difficulties and the lowest IQ scores. In fact, an adverse medical condition and an adverse social condition frequently act synergistically to worsen the fate of these children compared with children who experience only one of these detrimental conditions? j A new generation of advances in neonatology has
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produced a new breed of intensive care nursery graduates. Not only are these infants of far lower birth weight than in previous samples, but diagnostic procedures have moved from inferred relations between birth complications and brain development to actual examinations of the brain through a variety of imaging techniques. New questions can be asked about the relation of birth condition to developmental disabilities. One such question is whether biologic factors play a greater role in the behavioral outcome of these VLBW infants than in heavier groups of infants. Another question is whether more sophisticated assessments of neurologic conditions can provide clearer causal links to later disabilities, In regard to the questio n of whether VLBW infants have worse outcomes than LBW infants, the data are not completely clear. Because of the recency of many medical innovations, there is a necessary lag before extensive longitudinal data will be available. Furthermore, the introduction of some changes in high-risk infant care practices may have produced increases in morbidity while the appropriate applications were being tested. In a survey of the world literature on follow-up of VLBW babies, Stewart et al? 2 concluded that the chances of healthy survival have increased steadily, whereas the prevalence of handicap has remained stable. It would not be unreasonable to assume from these data that the role of social factors in the development of VLBW infants will be similar to their role in previous studies of high-risk infants. The studies reviewed give clear evidence that there is no deterministic relationship between perinatal medical status and later outcome. Further data from the Collaborative Perinatal Project indicate that the biologic condition of the child even a year after birth is not strongly related to later disability. Of 229 children in whom cerebral palsy was diagnosed at one year of age, more than half were free of motor handicap at age 7 years. 23 In most of the children who were judged to be nonhandicapped at follow-up, mild cerebral palsy had been diagnosed, but the group included more than one fourth of those with moderate or severe cerebral palsy. The second question was whether more sophisticated diagnostic techniques can more accurately identify those children who will have later disabilities. Neonatal neurologic examinations continue to produce many false positive results in the light of follow-up studies, indicating a high degree of transient neonatal morbidity?4 Brain lesions have been hypothesized to have a strong connection with developmental disabilities. A common method of determining cerebral intraventricular hemorrhage has been use of computed tomographic brain scans. In a 24-month followup of VLBW infants with varying degrees of hemorrhage, Papile et al? 5 found more major handicaps to be associated
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with higher grades of hemorrhage. However, the majority of infants with hemorrhage grades 1 through 3 had no major handicap, and not a few infants with the most extensive grade 4 hemorrhage were found to have no evidence o? handicap. In a similar study, 26 a large proportion of infants with moderate ventriculomegaly showed spontaneous regression or stabilization, with normal development in a high percentage of cases. Despite the lack of linear connections between birth status and measures of later general cognitive functioning, such as IQ scores, there is evidence from a number of studies that differentiated cognitive assessments may reveal subtle specific deficits in behavior at later ages. For example, deficits have been found in visual recognition memory?7.2s In these cases, however, it is not clear that such deficits are maintained in development independent of environmental conditions. Sigman 28 reported that for full-term infants there were relationships between caretaking patterns and visual attentiveness. For preterm infants the relationship was only evident in a female subsample; visual attention performance was correlated to the amount of verbal and social interaction with caretakers. Rose 29 found that preterm infants performed more poorly at differentiating novel from familiar stimuli in an attention task at 6 months of age. However, if the preterm infants received extrasensory stimulation during the first weeks of life, their later performance was indistinguishable from that of full-term infants. Rose suggested that visual recognition memory is negatively affected by prematurity and that performance can be improved by altering early environmental conditions. In a study that compared preterm infants' performance on a complex perceptual processing task at 1 year with that of lower and middle-class full-term infants, Rose et al. 3~found that the preterm and lower SES full-term infants performed similarly, with neither doing as well as the middle SES full-term babies. These studies indicate that environment is able to facilitate or inhibit even specific aspects of cognitive functioning throughout the first year of life. The need to study the developmental course of specific functions is evidenced by the differential impact of perinatal events on separate aspects of behavior. SiegeP ~ examined the relation between child language and intellectual competence at 3 years and reproductive, perinatal, and demographic risk factors. A measure of the home environment in terms of cognitive and social-emotional stimulation, the H O M E scale, ~2 also was made at 3 years. Children who were classified as being at risk at 12 months but who had scores in the normal range at 3 years came from families with significantly higher scores on the H O M E scale. Children not detected as being at risk in infancy, but whose development was delayed at 3 years,
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came from families with lower scores on the H O M E scale. In a further follow-up of this sample at 5 years, Siegel33 added specific tests of perceptual-motor functioning to the earlier measures of language and general intelligence. She found that environmental and demographic variables continued to contribute more to the prediction of language functioning and delay, but that perinatal and reproductive variables contributed more to the prediction of perceptualmotor functioning. In the absence of frank disorder, major questions remain as to the nature of the developmental risk to which LBW and VLBW infants are subject. In those who show no later deficits, a case can be made for biologic resiliency or recovery. In those that do have later difficulties, it is not altogether clear that there was a direct connection with the biologic risk. An explanation is needed for the discrepancy between the retrospective and prospective studies of perinatal risk factors reported above. CASUALTY
AND CONTEXT
How do we explain the later disappearance of the effects of severe trauma to the early physiologic functioning of the brain? Moreover, how do we explain the retrospective data that tends to show that children with a variety of deficits do have more perinatal complications in their histories than children without these disorders? The answers to these questions require the study of children in their environmental context. This context is invisible in most follow-up studies of pefinatal complications because it is rarely assessed. Luckily, some studies have examined both sets of factors: the developmental progress of high-risk infants, and the family and social context. An excellent example of such research is the Kauai study of child development. Werner et al.34 reported on the growth of all 670 children born in 1955 on Kauai in the Hawaiian Islands. The multiracial nature of Hawaii and the total sampling of social class involved in the Kauai sample permitted the investigators to provide ample controls for both racial and social class variables. During the newborn period, each infant was scored on a 4-point scale for severity of perinatal complications. At 20 months and again at 10 years of age these scores were related to assessments of physical health, psychologic status, and such environmental variables as socioeconomic status, family stability, and mother's education. As in the St. Louis study, during early childhood, Kauai infants who had had severe perinatal stress were found to have lower scores. In addition, however, a clear interaction was found between the impairing effect of perinatal complications and environmental variables, especially socioeconomic status. For infants living in a high SES environment with a stable family structure or with a
The Journal of Pediatrics July 1986
mother who was well educated, the IQ score differences between children with and without complication was only 5 to 7 points. For infants living in a low SES environment, with low family stability or with a mother of poor educational background, the difference in mean IQ scores between infants with and without perinatai complications ranged from 19 to 37 points. The results of the Kauai study seem to indicate that perinatal complications taken alone are not consistently related to later physical and psychologic development, but only when combined with and supported by persistently poor environmental circumstances. In the infants of the Kauai sample there was no correlation between the perinatal stress score and the measures at 10 years. 35 Some correlation was found, however, between the 20-month and 10-year data, especially when SES and parents' educational level were taken into consideration. The stability of intellectual functioning was much higher for those children who had IQ scores <80 at the 10-year testing period. All of these children had 20-month scores of ~100, with almost half <80, and the majority had parents with little education and low SES. The Kauai study seems to suggest that risk factors operative during the perinatal period disappear during childhood as more potent familial and social factors exert their influence, Werner et al. 34 extrapolated their findings to predict that of every 1000 live births in Kauai, by age 10 years only 66% of children would be functioning adequately without a recognized physical, intellectual, or behavioral problem in school. In the 34% who had problems at the age of 10 years, only a minor proportion could be attributed to the effects of serious perinatal stress. The authors concluded that "ten times more children had problems related to the effects of poor early environment than to the effects of perinatal stress." How are we to understand a situation where perinatal complications have a greater impact on later development in children raised in poor environmental conditions? These data imply that the biologic outcome of pregnancy is worse for those in poorer environments. The level of later disability is clearly not the result of the delivery complications alone; children with identical complications raised in good environmental situations show fewer consequences of such problems. The few studies of infant development that have examined environmental factors typically have used global variables, for example, family SES or mother's education. When a more differentiated view of the developmental context is examined, we can appreciate the multiplicity of factors that have an impact on the child's progress. Social status is only a summary variable that incorporates a variety of risk factors that exert both independent and interactive influences on outcome. These variables include enduring characteristics of the family
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(e.g., number of children; marital and minority status), psychologic characteristics of the parents (e.g., mental health, education, child-rearing attitudes, beliefs and coping skills), and stressful life events that interfere with the family's ability to provide a nurturant context for the child. Sameroff and Seifer 36 have shown that the developmental outcome for young children is determined by these multiple variables. The greater the number of these factors that are in the risk category, the poorer the outcome for the child. No single factor is always present or always absent when high levels of social-emotional and intellectual incompetency are found. If the child also is at risk by virtue of biologic condition, this must be added to the existing list of risk factors in the family. To understand how these risk factors operate, we can turn to specific studies of the interaction between biologic risk and caregiver behavior. Several investigations have been directed at identifying specific factors that may differentiate caregiver interactions with normal infants from those with infants who had medically complicated newborn periods? 7 In a review of this work, Goldberg et al? ~ found consistent group differences in the developing parent-infant relationship. At discharge preterm infants were less alert and responsive and their motor coordination and state control were less organized. Their parents appeared to be less actively involved, made less body contact, and smiled, talked to, and touched them less. Goldberg concluded that the parent-preterm infant relationship may follow a different course of development than do full-term dyads. The continuation of these differences in interaction patterns through 2 years of age was confirmed in a study by Barnard et al. 39 They found that by 8 months of age preterm infants had caught up to full-term babies in their ability to participate in the mother-infant interaction, but the mothers continued to treat them differently. The mothers of preterm infants were less positive in teaching interactions and described themselves as less involved with the child. One cause of these differences is the separation of high-risk infants from their parents? ~ The separation effects are somewhat confounded by the effects of the illness that cause the separation. In an innovative study, Field et al. 4~ compared interactions of mothers with preterm, full-term, and post-term infants. If the preterm infants behaved differently from both full-term and postterm infants, the explanation would be based on their relative biologic immaturity or in the fact that they were the only group separated from the mother during the lying-in period. The results were that both post-term and preterm infants differed from the full-term control group in attentive behavior and mother caregiving behavior. The hypothesized common factor was that both groups of
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infants had physical problems, albeit different ones. To explore directly the effects of illness, Minde et al. 42 compared relatively sick with relatively well VLBW infants. Not surprising, the sick infants were less interactive than the well ones. Somewhat more surprising was the finding that mothers visited the sicker infants less than the well ones, and were still interacting less with them several months after discharge. In a study of twins with birth weights <1500 gm, Minde et al. 43 found that mothers developed preferences within the first month for the healthier twin that were expressed in more positive behavior for at least 6 months afterward. Illness affects the behavior of newborn infants and their parents. Would these behavioral differences be consistently related to later developmental problems? Cohen et a144 compared the development of sick and well preterm infants in their UCLA longitudinal study. They found that a postnatal illness rating alone did not relate to outcome at 5 years of age, but that children who were doing poorly all had had a number of such hazardous events. They explained this paradox by hypothesizing two paths from illness to outcome. One path reflected the negative consequences of illness for development; the other reflected the ameliorating and fostering effects of good caregiving. Better parental caregiving interactions were related to better outcome. None of the sick infants who received good caregiving had below average intelligence scores at 5 years. INTERVENTION
EFFECTS
The relations that have been described between child development and environmental effects are primarily based on correlational analyses of risk factors and longitudinal outcomes. To test these interactive causal models, experiments that manipulated environmental factors would be necessary. Such studies can be found in attempts at early intervention with infants at high biologic risk, primarily preterm infants. This rich literature 37 cannot be extensively reviewed in this context, but several examples give an indication of the results of intervention efforts. To the extent that environmental risks are found in demographic variables such as SES or minority status, effective intervention strategies lie primarily in the political rather than the health domain. However, developmental risks associated with parental lack of knowledge or cognitively and emotionally impoverished parent-child interaction patterns can be suitable targets for behavioral interventions. One group of mothers generally defined as high-risk are lower SES, single teenagers. Field45 reviewed several approaches for working with this population. In one study the mothers were given demonstrations of the Brazelton Neonatal Behavioral Assessment Scale 46 during their pre-
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term baby's first month of life and were asked to administer a version of the examination independentlyY The treated mothers had better interactions with their infants, and by the end of a year their infants were attaining higher developmental scores than a control group of infants. Another group of low SES teenage mothers were visited at home every 2 weeks and were trained to do a variety of age-appropriate baby exercises and simple developmental assessments. At the end of a year, infants in the intervention group were heavier and longer than control infants, did better on developmental assessment mental scales, and were rated by their mothers as having a less difficult temperament; their mother-child interactions were more playful and verbally stimulating. In a third study, an attempt was made at a more substantial impact on the teen-age mother's life. A new group of such mothers brought their infants to a center-based infant nursery, where they carried out the exercise program from the previous home intervention and were employed as parttime teacher aide trainees for 20 hours a week. Thus the teenage mothers received free day care for their infants, a paid job, training, and an incentive to continue schooling. At the end of a year the infants of those mothers were heavier and taller than the home intervention group of infants, and they performed significantly better on both mental and motor scales of developmental assessments. Of possibly more important long-term value to their infants, the mothers in the center-based program had a much higher rate of return to school and a lower rate of repeat pregnancy. Such extensive interventions would not be necessary or appropriate for many groups of mothers with better personal or social resources. On the other hand, the extent of the intervention needs to be determined more by the deficits in the caregiving context than by the biologic condition of the child. Field4s concludes her review by noting that the reported effects are suggestive of a transactional phenomenon whereby teaching parents other ways of caregiving, or altering their perceptions, attitudes, and behaviors, appears to mediate developmental strides in their infants, which in turn reinforce and elicit more of the parenting skills necessary for fostering development.
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afflicted children. Our indepth review of available information shows that while each of these insults, either alone or together, can cause brain damage, they are not alone frequent causes of mental retardation... In the area of mental retardation, we despair of disentangling the individual environmental factors that interact with the individual child's biologic potential to produce a given level of function. Yet we continue to believe that optimizing environment and minimizing risk factors will result in better function and adaptability for the individual" (pp 13q5). The despair felt by the authors of the report is in part a consequence of the disproportionate lack of attention that has been paid to the study of the environment's role in enhancing or hindering child development. Much of the research reviewed above has pointed to fruitful directions for further research efforts in the analysis of environmental influences. Many factors, including family social context, parental child-rearing attitudes and practices, the school system, and the availability of medical and educational services to the disabled, have been identified as playing a role in the child's outcome. For many years the theory of a continuum of reproductive casualty played a major role in filling the gap between early medical risk and later developmental disabilities by hypothesizing as yet unmeasurable biologic insults. As our understanding of the developmental process has advanced, a new continuum has been hypothesized to fill the gap. Sameroff and ChandleP 9 proposed a "continuum of caretaking casualty" to describe the range of developmental disorders that could be attributed to poor parenting, that is, to the socioeconomic and familial factors that tend to overshadow the effects of early perinatal difficulties in producing emotional and intellectual problems in children. Prevention has become a much more complex enterprise because, as in the analysis of biomedical factors thought to lead to mental retardation, no single environmental factor alone determines outcome. On the other hand, this conclusion has been interpreted optimistically because it permits a variety of possibilities for either prevention or treatment.
SUMMARY REFERENCES
In the summary of a recent report to the National Institute of Neurologic and Communicative Disorders and Stroke, and the National Institute of Child Health and Human Development on current knowledge about prenatal and perinatal cause of neurologic dysfunction, Freeman 48 states, "It once seemed simple to say that a specific insult, such as birth trauma, asphyxia or obstetric maneuvers, were each the cause of brain disorders, and that prevention of these insults would substantially decrease the number of
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4. Hanshaw J. Cytomegalovirus infections. Pediatr Rev 1981; 2(8):245-251. 5. Hanshaw J, Scheiner A, Moxley A, et al. School failure and deafness after "silent" congenital eytomegalovirus infection. N Engl J Med 1976;295:468-470. 6. Susser M, Hauser WA, Kiely JL, et al. Quantitative estimates of prenatal and perinatal risk factors for perinatal mortality, cerebral palsy, mental retardation and epilepsy. In: Freeman JM, ed. Prenatal and perinatal factors associated with brain disorders. Washington D.C.: National Institutes of Health, 1985, Publ. No. 85-1149. 7. Hagberg B, Hagberg G, Lewerth A, et al: Mild mental retardation in Swedish school children. I. Prevalence. Acta Paediatr Scand 1981;70:445-452. 8. Broman SH. Perinatal anoxia and cognitive development in early childhood. In Field TM, ed. Infants born at risk. New York: Spectrum Publications, 1979. 9. Stein ZA, Susser M. The social distribution of mental retardation. Am J Mental Defic 1963;67:811-821. 10. Little WJ. On the influence of abnormal partuition, difficult labor, premature birth, and asphyxia neonatorum on the mental and physical condition of the child especially in relation to deformities. Lancet 1861;2:378-380. 1 I. Gesell A, Amatruda C. Developmental diagnosis. New York, Hoeber, 1941. 12. Pasamanick B, Knobloch H. Epidemiologic studies on the complications of pregnancy and the birth process. In: Caplan G, ed. Prevention of mental disorders in children. New York: Basic Books, 1961. 13. Broman SH, Nichols PL, Kennedy WA. Preschool IQ: prenatal and early developmental correlates. Hillsdale, N.J., Lawrence Erlbaum Associates, 1975. 14. Graham FK, Pennoyer MM, Caldwell BM, et al. Anoxia as a significant perinatal experience: a critique. J PEDIATR 1957; 50:556-569. 15. Graham FK, Matarazzo RG, Caldwell BM. Behavioral differences between normal and traumatized newborns. II. Standardization, reliability, and validity. Psychol Monogr 1956;70:21 (428). 16. Graham FK, Ernhart CB, Thurston DL, et al. Development three years after perinatal anoxia and other potentially damaging newborn experiences. Psychol Monogr 1962; 73:3(522). 17. Corah NL, Anthony E J, Painter P, et al. Effects of perinatal anoxia after seven years. Psychol Monogr 1965;79:3(596). 18. Gottfried AW. Intellectual consequenes of perinatal anoxia. Psychol Bull 1973;80:231-242. 19. Broman S. The Collaborative Perinatal Project: an overview. In: Mednick SA, Harway M, Finello KM, eds+ Handbook of longitudinal research, vol 1. New York: Praeger, 1984. 20. Broman S, Bien E, Shaughnessy P. Low achieving children: the first seven years. Hillsdale, N.J.: Lawrence Erlbaum Associates, 1985. 21. Escalona SK. Babies at double hazard: early development of infants at biologic and social risk. Pediatrics 1982;70:670768. 22. Stewart AL, Reynolds EOR, Lipscomb AP. Outcome for infants of very low birthweight: survey of world literature. Lancet 1981;1:1038-1041. 23. Nelson KB, Ellenberg JH. Children who "outgrew" cerebral palsy. Pediatrics 1982;69:529-536. 24. Bierman-van Eendenburg MEC, Jurgens-van der Zee AD,
Olinga AA, et al. Predictive value of neonatal neurological examination: a follow-up study at 18 months. Dev Med Child Neurol 1981;23:296-305. Papile L-A, Munsick-Bruno G, Schaefer A. Relationship of cerebral intraventricular hemorrhage and early childhood neurologic handicaps. Pediatric 1983;103:273-277. Liechty EA, Gilmo RL, Bryson CQ, Bull MJ. Outcome of high-risk neonates with ventrieulomegaly. Dev Med Child Neurol 1983;25:162-168. Rose SA, Gottfried AW, Bridger WH. Effects of haptic cues on visual recognition memory in full-term and preterm infants. Infant Behav Dev 1979;2:55-67. Sigman M. Individual differences in infant attention: relations to birth status and intelligence at five years. In Field T, Sostek A, eds. Infants born at risk: physiological, perceptual, and cognitive processes. New York: Grune & Stratton, 1983. Rose S. Enhancing visual recognition memory in preterm infants. Dev Psychol 1980;16:85-92. Rose SA, Gottfried AW, Bridger W. Cross-modal transfer in infants: relationship to prematurity and socioeconomic background. Dev Psychol 1979;14:643-652. Sigel LS. Reproductive, perinatal, and environmental factors as predictors of the cognitive and language development of preterm and full-term infants. Child Dev 1982;53:963-973. Bradley RH, Caldwell BM. The relation of home environment, cognitive competence, and IQ among males and females. Child Dev 1980;51:1140-1148. Siegel LS. The prediction of possible learning disabilities in preterm and full-term children. In: Field T, Sostek A, eds. Infants born at risk: physiological, perceptual, and cognitive processes. New York: Grune & Stratton, 1983. Werner EE, Bierman JM, French FE. The Children of Kauai. Honolulu: University of Hawaii, 1971. Werner EE, Honzik M, Smith R. Prediction of intelligence and achievement at ten years from twenty months pediatric and psychologic examinations. Child Dev 1968;39:10361075. Sameroff A J, Seifer R. Familial risk and child competence. Child Dev 1983;54:1254-1268. Sameroff AJ. The psychological needs of the parent in infant development. In: Avery G, ed. Neonatology, 3rd ed. New York: Lippincott, 1986. Goldberg S, Brachfield S, DiVitto B. Feeding, fussing and play: parent-infant interaction in the first year as a function of prematurity and perinatal medical problems. In: Field TM, Goldberg S, Stern D, eds. High-risk infants and children: adult and peer interactions. New York: Academic Press, 1980:133-153. Barnard KE, Bee HL, Hammond MA. Developmental changes in maternal interactions with term and preterm infants. Infant Behav Dev 1984;7:101-113. Klaus MH, Kennell JH. Parent-infant bonding. St. Louis: Mosby, 1982. Field T, Dempsey J, Sehuman HH. Developmental follow-up of pre- and post-term infants. In: Friedman S, Sigman M, eds. Preterm birth and psychological development. New York: Academic Press, 1981. Minde K, Whitelaw A, Brown J, Fitzhardinge P. Effect of neonatal complications in premature infants on early parentinfant interactions. Dev Med Child Neurol 1983;25:763. Minde K, Perrotta M, Corter C. The effect of neonatal
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complications in same-sexed premature twins on their mothers' preferences. J Am Acad Child Psychiatry 1982;21:446. Cohen SE, Sigman M, Parmelee AH, Beckwith L. Perinatal risk and developmental outcome in preterm infants. Semin Perinatol 1982;6:334-339. Field TM. Infants born at risk: early compensatory experiences. In: Bond LA, Joffe JM, eds. Facilitating infant and early childhood development. Hanover, N.H.: University Press of New England, 1982:251-283. Brazelton TB. Neonatal Behavioral Assessment Scale. London: Spastics International Medical Publications, 1973. Widmayer S, Field T. Effects of Brazelton demonstrations on
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early interactions of preterm infants and their mothers. Infant Behav Dev 1980;3:79-89. 48. Freeman JM. Summary. In Freeman JM, ed. Prenatal and perinatal factors associated with brain disorders. Washington D.C.: National Institutes of Health, 1985, Publ. No. 851149. 49. Sameroff A, Chandler M. Reproductive risk and the continuum of caretaking casualty. In: Horowitz FD, Hetherington M, Scarr-Salapatek S, Siegel G. Review of Child Development Research, vol 4. Chicago: University of Chicago Press, 1975.
Pediatrics has been the discipline most concerned with the prevention of developmental disabilities. Among these disabilities are a variety of physical and behavioral disorders that require long-term intervention and treatment at great social cost. It has always been clear that disabilities affect the family and the community by the enormous drain on emotional and financial resources. It has been less obvious that the disabilities are in turn affected by parents and society. Prevention approaches that focus on the affected individual alone frequently have been found to be inadequate. The usual explanation for the ineffectiveness of such intervention programs is that the wrong treatment is being used. Another interpretation is that the treatment did not extend to a wide enough social context. In many cases, family and cultural factors may be more important than factors in the child for preventing developmental disabilities. This review is devoted to providing a balanced perspective on the factors that contribute to healthy psychologic outcomes in children. In this view, the biologic condition is only one ingredient in the developmental formula that will lead to intellectual and social-emotional competence. Whereas linkages have been found between some "germs" and specific biologic disorders, this has not been true for behavioral disorders. Attempts to prevent developmental disabilities in the sense of deterring a biologic factor will have meaning in a very small percentage of cases, although these cases may be the most severe and profound. On the other hand, the vast majority of identified handicaps are the result of factors more strongly associated with psychologic and social environment than of any intrinsic characteristics of the child. Between these two categories lie the high-risk graduates of neonatal intensive care units, whose risk for retardation is a complex function of the interplay between their biologic development and Reprint requests: Arnold J. Sameroff, Ph.D., Institute for the Study of Developmental Disabilities, University of Illinois, 840 S. Wood St., Chicago, IL 60612.
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experience. New approaches to biologic and behavioral development emphasize causal analyses based on probabilistic interactions of multiple factors) These approaches were required to explain paradoxes that occurred when explanations for a variety of disorders were restricted to linear causal models. Agent-disease models were most effective in understanding acute, primarily infectious diseases, in contrast to more chronic disorders: For chronic disorders, whether heart disease, cancer, or mental retardation, unfavorable outcomes are produced by a combination of biologic, psychologic, social, and environmental risks, usually involving complex interactions among these factors. The complexity of the relationships between germs, context, and disorder is illustrated by the study of cytomegalovirus.3 Congenital cytomegalovirus infections are HOME SES VLBW
Home Observation for Measurement of the Environment Socioeconomic status Very low birth weight
found in about 1% of babies born in the United States, with the highest rates in infants of teenage mothers of low socioeconomic status: Of those infected, fewer than 5% have symptoms. As a group, infants with subclinical infections had lower IQ scores than did noninfected comparison infants, and about 10% to 20% had later central nervous system deficits. However, these differences were found only between infected lower SES children and their peers. When similar comparisons were made between groups of infected and noninfected middle-class children, no IQ differences were found) For such disorders, at least two factors and probably more are involved in producing clinical symptoms. Because the combination of these factors varies in each individual, the probability that a disorder will result will vary. If we turn directly to the study of developmental disabilities, especially mental retardation, the necessity for
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the consideration of nonbiologic factors becomes even more apparent. Epidemiologic surveys in Sweden have found a prevalence of severe mental retardation in childhood of about 3:1000, compatible with rates of severe mental retardation in the United States. On the other hand, the prevalence of mild mental retardation in Sweden is about 4:1000, eight or ten times lower than rates recorded in the United States. Susser et al. 6 point out that these rates are related to the reduction in Sweden of cultural-familial retardation and evidence the powerful impact of the social environment on mental performance. Another indication of the role of environment in mild mental retardation is the percentage of such children with detectable clinical abnormalities. In Sweden, 40% of mildly retarded children have identifiable conditions, 7 whereas the comparable proportion in the United States is only 10%. In the Collaborative Perinatal Project of the National Institute of Neurological Diseases and Stroke, the proportion of cases with mild mental retardation and detectable abnormalities was 14% for white children and 6% for blacks, s Similarly, in an English study that compared rates of mild mental retardation in schools with high or low social standing, the rate for children with organic conditions was twice as high in the schools with low social standing, but the rate for mildly retarded children without clinical abnormalities was 15 times as high. 9 It can be argued that there are subtle biologic factors yet to be discovered that will explain mental retardation in all children, but there is a great deal of evidence to support an alternative hypothesis. This evidence is reviewed below. IDENTIFYING
TARGETS
FOR TREATMENT
To prevent developmental disabilities, a clear idea of the causes of the disorder is necessary. Because intellectual functioning requires cerebral activity, a biologic orientation would lead one to conclude that mental retardation must result from damage to the brain. Targets for treatment then become those factors that produce brain damage. The basis for the connection between developmental disabilities and perinatal factors was laid more than a century ago in the work of Little, l~ who first focused attention on asphyxia as a cause of brain damage in the child. The mechanism of such a connection remained elusive, but this did not prevent many investigators from proposing various cause-effect models. Gesell and Amatruda" popularized the concept of "minimal cerebral damage" as the causal link. The inability to document the linkage was attributed to the adjective "minimal," that is, undetectable. The empirical basis for such a connection was provided in the work of Pasamanick and Knobloch ~2 when they
19 3
proposed the existence of a "continuum of reproductive casualty." In a series of retrospective studies in which they examined the delivery and birth histories of children with a variety of subsequent disorders, they were able to find a number of significant relationships. From these data they postulated a dimension running from gross neurologic disorders such as cerebral palsy and epilepsy at one extreme to a range of minor motor, perceptual, learning, and behavioral disabilities at the other. The more severe the disability (e.g., cerebral palsy in contrast to tics) the more severe the causal perinatal complication (e.g., maternal bleeding in contrast to cesarean section). TESTING
CAUSAL
HYPOTHESES
Retrospective studies, such as those of Pasamanick and Knobloch, are important for generating hypotheses; however, other approaches are necessary to test them. In a typical retrospective study, persons are identified who already have the disorder, and then the investigator looks into their early history to find some cause. Retrospective approaches, however, entail serious problems in subject selection, because only those subjects who have the later disorder are studied. By contrast, prospective research permits the selection of subjects with early characteristics thought to be implicated in the cause of the later disorder. If indeed asphyxia leads to brain damage and mental retardation, and if a group of infants who had asphyxia at birth were followed up, a significantly greater amount of retardation would be found in this group than in a control group of infants who did not have anoxia. Even if such a prospective connection were found, another explanation is possible. One of the ancillary findings of Pasamanick and Knobloch's epidemiologic work was that the absolute number of abnormalities of pregnancy was higher among poorer groups. Children from poorer families have poorer intellectual and social outcomes. ~3 Later lower intelligence scores could be a consequence of earlier medical problems, or they could be a consequence of the fact that poorer families have both more medical problems and children with intellectual problems. In one of the better of the longitudinal studies of the consequences of birth complications, Graham et al) 4 tried to overcome the inadequacies of previous studies that used either poor measures of anoxia at birth or poor measures of intelligence at follow-up. They argued that if a large variety of measures, including neurologic, personality adjustment, and perceptual-motor tasks, were utilized in a longitudinal study, the significant differences between the affected and control groups should be revealed. Several hundred infants from a St. Louis hospital were seen in the newborn period" and were followed up at 3 and 7 years of
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age.~6.17 As expected, when examined during the first days of life, anoxic infants were found to be impaired on a number of behavioral indices. ~4 When the performance on these measures was compared with a prognostic score based on the degree of anoxia experienced by the children, those infants with the poorest prognostic scores performed most poorly on the newborn assessments. At 3 years of age the children were tested with a battery of cognitive, perceptual-motor, personality, and neurologic tests, ~6 The group of anoxic infants scored lower than did controls on all tests of cognitive function, had more positive neurologic findings, and showed some personality differences, but there were no differences on tests of perceptualmotor functioning. At 7 years of age the children were again tested. ~7Surprisingly, significant IQ differences had disappeared between the anoxic group and the control population; of the 21 cognitive and perceptual measures, only two showed differences. The investigators were forced to conclude that anoxic newborn infants showed minimal impairment of functioning at 7 years and that efforts to predict current functioning on the basis of the severity of newborn medical status were highly unreliable. Many advances were made in diagnostic and assessment technology during the 1960s, but there was little change in the pattern of results among prospective studies of birth complications. Gottfried, ~s in a review of 20 investigations of the longitudinal effects of anoxia, came to conclusions similar to those of the St. Louis study, among which were that (1) intellectual consequences of perinatal anoxia are more prevalent in infants and preschoolers than in older children and adolescents; (2) anoxic subjects as a group are not mentally retarded; and (3) whether anoxic subjects are deficient in specific intellectual abilities is not known. The most compelling of the prospective longitudinal studies in neonates, if only for its magnitude, is the Collaborative Perinatal Project of the National Institute of Neurological Diseases and Stroke in the United States29 Between 1959 and 1965, more than 50,000 women and their infants were recruited at birth, primarily from clinic populations in 12 medical centers, to investigate the relationship between birth condition and later neurotogic or behavioral deficits. The first major report of developmental outcome was the analysis of the IQ scores of the sample when the children were 4 years of age. ~ The effects on intelligence of 169 prenatal, delivery, infant, and family variables were examined. The implicit causal hypotheses of the collaborative study were reflected in this set of measures: Only eight of the 169 variables examined were related to family characteristics; the remaining 161 were assessments of the medical and developmental condition of the mother and child through the first year of life. The surprising result of the 4-year analysis was that the
The Journal of Pediatrics July 1986
intellectual outcome for children was far better explained by the small set of family factors than any combination of the multitude of biomedical variables. In the second major report on the intellectual development of the children from the collaborative study the focus moved from the general case of mental retardation to examine the cause of more specific learning disabilities?~ It is not surprising that children with low IQs do poorly in school. But what about children with normal intelligence who do poorly? The analysis of the development of these children was expected to offer new hope for the identification of specific biomedical causes of these school-age disorders. Whereas the cause of general mental retardation did not seem to be illuminated by analysis of the early medical condition of the child, perhaps more specific entities, such as learning disabilities, dyslexia, minimal brain dysfunction, hyperkinetic syndrome, or attention deficit disorder, might be better targets for biologic causal models. From a sample of 35,000 children tested at 7 years of age in the collaborative study, about a thousand were identified as having normal intelligence but poor school performance. This cohort was compared with a demographically matched sample of more than 6000 children with normal school performance to evaluate the contribution of perinatal conditions, behavior during the preschool period, and the child's social environment to problems of learning, reading, and hyperactivityl The most compelling result of the 7-year follow-up analysis was that even when specific conditions are studied, the primary causal factors reside not in the child's biomedical history but in the environment, that is, the social context of development. The authors concluded that their major findings support and augment the conclusions of others that "lower socioeconomic status, less maternal education, higher birth order, and larger family size are related to higher rates of academic failure" (Broman et al., 2~ p 92). The report of the school behavior of the large sample in the collaborative project supported the findings of many other studies that followed the development of smaller groups of children who had experienced perinatal complications. If social variables are ignored, there seems to be a correlation causal connection between birth complications and later lower IQ. When social status is included in the analysis, children from poorer SES groups are found to have the most perinatal difficulties and the lowest IQ scores. In fact, an adverse medical condition and an adverse social condition frequently act synergistically to worsen the fate of these children compared with children who experience only one of these detrimental conditions? j A new generation of advances in neonatology has
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produced a new breed of intensive care nursery graduates. Not only are these infants of far lower birth weight than in previous samples, but diagnostic procedures have moved from inferred relations between birth complications and brain development to actual examinations of the brain through a variety of imaging techniques. New questions can be asked about the relation of birth condition to developmental disabilities. One such question is whether biologic factors play a greater role in the behavioral outcome of these VLBW infants than in heavier groups of infants. Another question is whether more sophisticated assessments of neurologic conditions can provide clearer causal links to later disabilities, In regard to the questio n of whether VLBW infants have worse outcomes than LBW infants, the data are not completely clear. Because of the recency of many medical innovations, there is a necessary lag before extensive longitudinal data will be available. Furthermore, the introduction of some changes in high-risk infant care practices may have produced increases in morbidity while the appropriate applications were being tested. In a survey of the world literature on follow-up of VLBW babies, Stewart et al? 2 concluded that the chances of healthy survival have increased steadily, whereas the prevalence of handicap has remained stable. It would not be unreasonable to assume from these data that the role of social factors in the development of VLBW infants will be similar to their role in previous studies of high-risk infants. The studies reviewed give clear evidence that there is no deterministic relationship between perinatal medical status and later outcome. Further data from the Collaborative Perinatal Project indicate that the biologic condition of the child even a year after birth is not strongly related to later disability. Of 229 children in whom cerebral palsy was diagnosed at one year of age, more than half were free of motor handicap at age 7 years. 23 In most of the children who were judged to be nonhandicapped at follow-up, mild cerebral palsy had been diagnosed, but the group included more than one fourth of those with moderate or severe cerebral palsy. The second question was whether more sophisticated diagnostic techniques can more accurately identify those children who will have later disabilities. Neonatal neurologic examinations continue to produce many false positive results in the light of follow-up studies, indicating a high degree of transient neonatal morbidity?4 Brain lesions have been hypothesized to have a strong connection with developmental disabilities. A common method of determining cerebral intraventricular hemorrhage has been use of computed tomographic brain scans. In a 24-month followup of VLBW infants with varying degrees of hemorrhage, Papile et al? 5 found more major handicaps to be associated
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19 5
with higher grades of hemorrhage. However, the majority of infants with hemorrhage grades 1 through 3 had no major handicap, and not a few infants with the most extensive grade 4 hemorrhage were found to have no evidence o? handicap. In a similar study, 26 a large proportion of infants with moderate ventriculomegaly showed spontaneous regression or stabilization, with normal development in a high percentage of cases. Despite the lack of linear connections between birth status and measures of later general cognitive functioning, such as IQ scores, there is evidence from a number of studies that differentiated cognitive assessments may reveal subtle specific deficits in behavior at later ages. For example, deficits have been found in visual recognition memory?7.2s In these cases, however, it is not clear that such deficits are maintained in development independent of environmental conditions. Sigman 28 reported that for full-term infants there were relationships between caretaking patterns and visual attentiveness. For preterm infants the relationship was only evident in a female subsample; visual attention performance was correlated to the amount of verbal and social interaction with caretakers. Rose 29 found that preterm infants performed more poorly at differentiating novel from familiar stimuli in an attention task at 6 months of age. However, if the preterm infants received extrasensory stimulation during the first weeks of life, their later performance was indistinguishable from that of full-term infants. Rose suggested that visual recognition memory is negatively affected by prematurity and that performance can be improved by altering early environmental conditions. In a study that compared preterm infants' performance on a complex perceptual processing task at 1 year with that of lower and middle-class full-term infants, Rose et al. 3~found that the preterm and lower SES full-term infants performed similarly, with neither doing as well as the middle SES full-term babies. These studies indicate that environment is able to facilitate or inhibit even specific aspects of cognitive functioning throughout the first year of life. The need to study the developmental course of specific functions is evidenced by the differential impact of perinatal events on separate aspects of behavior. SiegeP ~ examined the relation between child language and intellectual competence at 3 years and reproductive, perinatal, and demographic risk factors. A measure of the home environment in terms of cognitive and social-emotional stimulation, the H O M E scale, ~2 also was made at 3 years. Children who were classified as being at risk at 12 months but who had scores in the normal range at 3 years came from families with significantly higher scores on the H O M E scale. Children not detected as being at risk in infancy, but whose development was delayed at 3 years,
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came from families with lower scores on the H O M E scale. In a further follow-up of this sample at 5 years, Siegel33 added specific tests of perceptual-motor functioning to the earlier measures of language and general intelligence. She found that environmental and demographic variables continued to contribute more to the prediction of language functioning and delay, but that perinatal and reproductive variables contributed more to the prediction of perceptualmotor functioning. In the absence of frank disorder, major questions remain as to the nature of the developmental risk to which LBW and VLBW infants are subject. In those who show no later deficits, a case can be made for biologic resiliency or recovery. In those that do have later difficulties, it is not altogether clear that there was a direct connection with the biologic risk. An explanation is needed for the discrepancy between the retrospective and prospective studies of perinatal risk factors reported above. CASUALTY
AND CONTEXT
How do we explain the later disappearance of the effects of severe trauma to the early physiologic functioning of the brain? Moreover, how do we explain the retrospective data that tends to show that children with a variety of deficits do have more perinatal complications in their histories than children without these disorders? The answers to these questions require the study of children in their environmental context. This context is invisible in most follow-up studies of pefinatal complications because it is rarely assessed. Luckily, some studies have examined both sets of factors: the developmental progress of high-risk infants, and the family and social context. An excellent example of such research is the Kauai study of child development. Werner et al.34 reported on the growth of all 670 children born in 1955 on Kauai in the Hawaiian Islands. The multiracial nature of Hawaii and the total sampling of social class involved in the Kauai sample permitted the investigators to provide ample controls for both racial and social class variables. During the newborn period, each infant was scored on a 4-point scale for severity of perinatal complications. At 20 months and again at 10 years of age these scores were related to assessments of physical health, psychologic status, and such environmental variables as socioeconomic status, family stability, and mother's education. As in the St. Louis study, during early childhood, Kauai infants who had had severe perinatal stress were found to have lower scores. In addition, however, a clear interaction was found between the impairing effect of perinatal complications and environmental variables, especially socioeconomic status. For infants living in a high SES environment with a stable family structure or with a
The Journal of Pediatrics July 1986
mother who was well educated, the IQ score differences between children with and without complication was only 5 to 7 points. For infants living in a low SES environment, with low family stability or with a mother of poor educational background, the difference in mean IQ scores between infants with and without perinatai complications ranged from 19 to 37 points. The results of the Kauai study seem to indicate that perinatal complications taken alone are not consistently related to later physical and psychologic development, but only when combined with and supported by persistently poor environmental circumstances. In the infants of the Kauai sample there was no correlation between the perinatal stress score and the measures at 10 years. 35 Some correlation was found, however, between the 20-month and 10-year data, especially when SES and parents' educational level were taken into consideration. The stability of intellectual functioning was much higher for those children who had IQ scores <80 at the 10-year testing period. All of these children had 20-month scores of ~100, with almost half <80, and the majority had parents with little education and low SES. The Kauai study seems to suggest that risk factors operative during the perinatal period disappear during childhood as more potent familial and social factors exert their influence, Werner et al. 34 extrapolated their findings to predict that of every 1000 live births in Kauai, by age 10 years only 66% of children would be functioning adequately without a recognized physical, intellectual, or behavioral problem in school. In the 34% who had problems at the age of 10 years, only a minor proportion could be attributed to the effects of serious perinatal stress. The authors concluded that "ten times more children had problems related to the effects of poor early environment than to the effects of perinatal stress." How are we to understand a situation where perinatal complications have a greater impact on later development in children raised in poor environmental conditions? These data imply that the biologic outcome of pregnancy is worse for those in poorer environments. The level of later disability is clearly not the result of the delivery complications alone; children with identical complications raised in good environmental situations show fewer consequences of such problems. The few studies of infant development that have examined environmental factors typically have used global variables, for example, family SES or mother's education. When a more differentiated view of the developmental context is examined, we can appreciate the multiplicity of factors that have an impact on the child's progress. Social status is only a summary variable that incorporates a variety of risk factors that exert both independent and interactive influences on outcome. These variables include enduring characteristics of the family
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(e.g., number of children; marital and minority status), psychologic characteristics of the parents (e.g., mental health, education, child-rearing attitudes, beliefs and coping skills), and stressful life events that interfere with the family's ability to provide a nurturant context for the child. Sameroff and Seifer 36 have shown that the developmental outcome for young children is determined by these multiple variables. The greater the number of these factors that are in the risk category, the poorer the outcome for the child. No single factor is always present or always absent when high levels of social-emotional and intellectual incompetency are found. If the child also is at risk by virtue of biologic condition, this must be added to the existing list of risk factors in the family. To understand how these risk factors operate, we can turn to specific studies of the interaction between biologic risk and caregiver behavior. Several investigations have been directed at identifying specific factors that may differentiate caregiver interactions with normal infants from those with infants who had medically complicated newborn periods? 7 In a review of this work, Goldberg et al? ~ found consistent group differences in the developing parent-infant relationship. At discharge preterm infants were less alert and responsive and their motor coordination and state control were less organized. Their parents appeared to be less actively involved, made less body contact, and smiled, talked to, and touched them less. Goldberg concluded that the parent-preterm infant relationship may follow a different course of development than do full-term dyads. The continuation of these differences in interaction patterns through 2 years of age was confirmed in a study by Barnard et al. 39 They found that by 8 months of age preterm infants had caught up to full-term babies in their ability to participate in the mother-infant interaction, but the mothers continued to treat them differently. The mothers of preterm infants were less positive in teaching interactions and described themselves as less involved with the child. One cause of these differences is the separation of high-risk infants from their parents? ~ The separation effects are somewhat confounded by the effects of the illness that cause the separation. In an innovative study, Field et al. 4~ compared interactions of mothers with preterm, full-term, and post-term infants. If the preterm infants behaved differently from both full-term and postterm infants, the explanation would be based on their relative biologic immaturity or in the fact that they were the only group separated from the mother during the lying-in period. The results were that both post-term and preterm infants differed from the full-term control group in attentive behavior and mother caregiving behavior. The hypothesized common factor was that both groups of
Environmental context o f child development
19 7
infants had physical problems, albeit different ones. To explore directly the effects of illness, Minde et al. 42 compared relatively sick with relatively well VLBW infants. Not surprising, the sick infants were less interactive than the well ones. Somewhat more surprising was the finding that mothers visited the sicker infants less than the well ones, and were still interacting less with them several months after discharge. In a study of twins with birth weights <1500 gm, Minde et al. 43 found that mothers developed preferences within the first month for the healthier twin that were expressed in more positive behavior for at least 6 months afterward. Illness affects the behavior of newborn infants and their parents. Would these behavioral differences be consistently related to later developmental problems? Cohen et a144 compared the development of sick and well preterm infants in their UCLA longitudinal study. They found that a postnatal illness rating alone did not relate to outcome at 5 years of age, but that children who were doing poorly all had had a number of such hazardous events. They explained this paradox by hypothesizing two paths from illness to outcome. One path reflected the negative consequences of illness for development; the other reflected the ameliorating and fostering effects of good caregiving. Better parental caregiving interactions were related to better outcome. None of the sick infants who received good caregiving had below average intelligence scores at 5 years. INTERVENTION
EFFECTS
The relations that have been described between child development and environmental effects are primarily based on correlational analyses of risk factors and longitudinal outcomes. To test these interactive causal models, experiments that manipulated environmental factors would be necessary. Such studies can be found in attempts at early intervention with infants at high biologic risk, primarily preterm infants. This rich literature 37 cannot be extensively reviewed in this context, but several examples give an indication of the results of intervention efforts. To the extent that environmental risks are found in demographic variables such as SES or minority status, effective intervention strategies lie primarily in the political rather than the health domain. However, developmental risks associated with parental lack of knowledge or cognitively and emotionally impoverished parent-child interaction patterns can be suitable targets for behavioral interventions. One group of mothers generally defined as high-risk are lower SES, single teenagers. Field45 reviewed several approaches for working with this population. In one study the mothers were given demonstrations of the Brazelton Neonatal Behavioral Assessment Scale 46 during their pre-
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term baby's first month of life and were asked to administer a version of the examination independentlyY The treated mothers had better interactions with their infants, and by the end of a year their infants were attaining higher developmental scores than a control group of infants. Another group of low SES teenage mothers were visited at home every 2 weeks and were trained to do a variety of age-appropriate baby exercises and simple developmental assessments. At the end of a year, infants in the intervention group were heavier and longer than control infants, did better on developmental assessment mental scales, and were rated by their mothers as having a less difficult temperament; their mother-child interactions were more playful and verbally stimulating. In a third study, an attempt was made at a more substantial impact on the teen-age mother's life. A new group of such mothers brought their infants to a center-based infant nursery, where they carried out the exercise program from the previous home intervention and were employed as parttime teacher aide trainees for 20 hours a week. Thus the teenage mothers received free day care for their infants, a paid job, training, and an incentive to continue schooling. At the end of a year the infants of those mothers were heavier and taller than the home intervention group of infants, and they performed significantly better on both mental and motor scales of developmental assessments. Of possibly more important long-term value to their infants, the mothers in the center-based program had a much higher rate of return to school and a lower rate of repeat pregnancy. Such extensive interventions would not be necessary or appropriate for many groups of mothers with better personal or social resources. On the other hand, the extent of the intervention needs to be determined more by the deficits in the caregiving context than by the biologic condition of the child. Field4s concludes her review by noting that the reported effects are suggestive of a transactional phenomenon whereby teaching parents other ways of caregiving, or altering their perceptions, attitudes, and behaviors, appears to mediate developmental strides in their infants, which in turn reinforce and elicit more of the parenting skills necessary for fostering development.
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afflicted children. Our indepth review of available information shows that while each of these insults, either alone or together, can cause brain damage, they are not alone frequent causes of mental retardation... In the area of mental retardation, we despair of disentangling the individual environmental factors that interact with the individual child's biologic potential to produce a given level of function. Yet we continue to believe that optimizing environment and minimizing risk factors will result in better function and adaptability for the individual" (pp 13q5). The despair felt by the authors of the report is in part a consequence of the disproportionate lack of attention that has been paid to the study of the environment's role in enhancing or hindering child development. Much of the research reviewed above has pointed to fruitful directions for further research efforts in the analysis of environmental influences. Many factors, including family social context, parental child-rearing attitudes and practices, the school system, and the availability of medical and educational services to the disabled, have been identified as playing a role in the child's outcome. For many years the theory of a continuum of reproductive casualty played a major role in filling the gap between early medical risk and later developmental disabilities by hypothesizing as yet unmeasurable biologic insults. As our understanding of the developmental process has advanced, a new continuum has been hypothesized to fill the gap. Sameroff and ChandleP 9 proposed a "continuum of caretaking casualty" to describe the range of developmental disorders that could be attributed to poor parenting, that is, to the socioeconomic and familial factors that tend to overshadow the effects of early perinatal difficulties in producing emotional and intellectual problems in children. Prevention has become a much more complex enterprise because, as in the analysis of biomedical factors thought to lead to mental retardation, no single environmental factor alone determines outcome. On the other hand, this conclusion has been interpreted optimistically because it permits a variety of possibilities for either prevention or treatment.
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