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Cognitive Development, Temperament and. Behavior at 2 Years as Indicative of Language. Development at 4 Years in Pre-Term Infants. Nina Sajaniemi ...
Cognitive Development, Temperament and Behavior at 2 Years as Indicative of Language Development at 4 Years in Pre-Term Infants Nina Sajaniemi, LicA(Psych) Helsinki University Hospital for Children and Adolescents

Liisa Hakamies-Blomqvist, PhD University of Helsinki

Jukka Ma¨kela¨, MD Child Psychiatry, Helsinki

Anne Avellan, MA Helsinki University Hospital for Children and Adolescents

Hannu Rita, MSc University of Helsinki

Lennart von Wendt, PhD Helsinki University Hospital for Children and Adolescents

ABSTRACT: This study focuses on the early temperamental (TTQ = toddler temperament questionnaire), behavioral (IBR = infant behavior record), and cognitive precursors of impaired language functioning in preschool-age pre-terms infants. The study group consisted of 63 pre-term infants with a mean birth weight of 1246 ± 437 g born in 1989–1991 in the University Central Hospital of Helsinki. Children with major disabilities (CP or mental retardation) were excluded. At the age of 4 years, 22% showed impaired language function. Logistic regression analysis showed that the Bayley MDI score was the best predictor in identifying an increased risk for language impairment. Behavioral characteristics were more strongly associated with subsequent language impairment than temperament. KEY WORDS: Pre-Term Infants; Cognitive Performance; Behavior; Temperament; Language Impairments.

This study was financially suppoted by the Arvo and Lea Ylppo¨ Foundation and the Rinnekoti Foundation. We thank Dr. Teija Salokorpi for neurological consultation. Address correspondence to Nina Sajaniemi, Helsinki University Hospital for Children and Adolescent Neurology, Lastenlinnantie 2, 00250 Helsinki, Finland; e-mail: nina. [email protected]. Child Psychiatry and Human Development, Vol. 31(4), Summer 2001  2001 Human Sciences Press, Inc.

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Introduction Early language delay in pre-term children has been documented in very few studies. Byrne1 reported that at 12 months, 8.3% of pre-term children in his study had delayed expressive language (Early Language Milestone Scale, ELM).2 At 24 months of age, 28% of the infants had delayed expressive language and 5.7% had delayed receptive language. In addition, only 32% of those with age-appropriate expressive language had a mean length of response within the normal range.1 In the study by Grunau et al.,3 ELBW children were significantly behind controls in both receptive and expressive language development at the age of 3 years. Recently, Luoma et al.4 found significant differences in 5-year old low-risk pre-terms compared to full-terms on language comprehension and production tests. Pre-term children without major handicap and with normal IQ scored significantly lower than full-term controls in Rapid Automatic Naming Test (RAN; Colors and Objects)5 and in Naming Tokens test (NEPSY).6 In addition, pre-term children scored lower than full-terms in Relative Concepts test (NEPSY), which measures comprehension of verbal-logical concepts and relations between words.4 Several studies have stressed the importance of early language development for other areas of development. Carson et al.7 found that delayed expressive language predicted behavioral, social and cognitive disorders. Whitfield8 concluded that subtle impairments in language development apparent in the early years may contribute to later academic difficulties. A connection between behavioral problems and language was implicated by Cohen et al.9 who showed that 34.4% of 288 four to twelve-year old children referred to treatment for psychiatric disorders had a language impairment not suspected previously. These findings were further confirmed in a study of Beitchman10 in which children with speech/language problems at age 5 had significantly more psychiatric problems at the age of 12.5 years than normal controls, even if their speech/language abilities improved. Cognitive impairments are common even in pre-term infants who do not have major neurological deficits such as CP and mental retardation.11–26 These impairments have mainly been attributed to mild neurological symptoms described as attention deficits, hyperactivity, motor clumsiness, and visual-spatial and visual-motor deficits.27,28,24,25 Less attention has been paid to the role of cognitive factors in the subsequent language development. Language has a significant mediating role in both cognitive, social and behavioral development. To prevent the cumulative disadvan-

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tages of unfavorable language development, it would probably be useful to identify at-risk children as early as possible. This is especially important in children with known biological risk factors such as preterm children with very low birth weight. In addition to cognitive factors, the developmental importance of behavioral and temperamental characteristics has been demonstrated in both pre-term and full-term children.29–31 Several studies have shown that optimal behavioral functioning during cognitive evaluation is associated with higher cognitive performance.32–34,30 In an early study using behavioral assessment, Matheny found that children with optimal cognitive functioning tended to be responsive to and cooperative with the examiner, positive in emotional tone, object oriented, task persistent, reactive to test stimuli, vocal, and generally well gocoordinated for their age.35 It has been shown that the child’s temperament is related to cognitive performance: scores of high adaptability and high persistence especially have been associated with higher scores in cognitive tests.36–38 Temperament is a multi-dimensional construct that includes both state and affect and it refers to the infant’s typical behavior across time and across situations.39 The child’s temperament may decrease or increase her or his ability to adapt to the learning environment40 and it may also affect the probability of successfully concluding a testing session. However, the predictive role of behavioral or temperamental factors in the development of language has so far received limited attention. The present study focuses on early cognitive performance in addition to temperamental and behavioral factors as precursor of later language impairment. The following questions were asked: 1. Are the results of a cognitive assessment at 2 years of age associated with impaired language functioning at 4 years of age in preterm children without major neurological disabilities? 2. Are individual temperamental characteristics and behavioral characteristics at 2 years of age associated with impaired language functioning at 4 years of age in pre-term children without major neurological disabilities? Methods Study Group The initial study group consisted of 80 infants born at gestational ages varying from 23 to 34 weeks whose mothers were referred to the University

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Central Hospital of Helsinki in 1989–1991 for threatened pre-term delivery. The enrolled women delivered 138 live-born pre-term infants of whom 104 were born before 34 weeks of gestation and had no life-threatening malformations. Of these 104 pre-term infants, 12 died during the initial hospitalization. The 92 surviving infants were recruited into this follow-up study during the nursery stay following birth. Twelve infants were lost from follow-up: one infant died, four infants were lost for parental refusal, two infants were living abroad, and five infants were in other regions of the country. All 11 surviving infants lost from the follow-up were born at 29–33 weeks of gestation. Children with major neurological disabilities (CP or mental retardation) were excluded. Cerebral palsy (CP) was diagnosed at the adjusted age of 24 months if pathological muscle tonus, persisting primitive reflexes, and delay in motor development were found.41 There were 12 children with CP diagnosis and five children without CP were diagnosed as having mild mental retardation (Bayley’s MDI < 70). The pre-term children in the exclusion group were slightly but not significantly smaller than the pre-term children in the study group. Not surprisingly, the level of cognitive performance at the age of 24 months was significantly lower in the exclusion group than in the study group. The final study group thus consisted of 63 infants without major neurological disabilities and with MDI > 70. The mean birth weight was 1246 ± 472 grams, mean gestational age 29.4 ± 3 weeks, and days of mechanical ventilation 12.3 ± 26 (this high SD value is due to one outlier case having 182 ventilator days). Seven children (11%) had cranial ultrasound changes indicating PVL (periventricular leucomalacia) or IVH (intraventricular hemorrhage) gradus I-II.

Measures and Procedures Background clinical data on pregnancy, birth and the perinatal period were obtained from hospital records. The psychological investigation was carried out by a clinical neuropsychologist (NS, first author of this paper) at the Hospital for Children and Adolescents, Helsinki University Central Hospital, in 1991–1993 at the corrected age of 2 years (24 months ± 2 weeks) and in 1993– 1995 at the age of 4 years (48 weeks ± 2 weeks) as a part of the follow-up program for premature infants. The neurological examination was conducted by a child neurologist (TS) according to a method standardized for Finnish healthy full-term children.42 The method includes screening tasks for gross motor, fine motor, verbal and visual-spatial abilities, and attention. The result is considered subnormal when the child does not reach normal scores in one ore more of these five groups. In this test battery, the scores in each item group are subnormal when they are more than 15 percentiles below the mean scores of healthy term children. In the present study, the children were considered to have minor neurological symptoms at the age of 18 months if they (1) had slight motor delay and motor clumsiness in their general neurological status and (2) did not reach normal test scores as defined above.

Assessment at 2 Years of Age The Mental Development Index (MDI) from the Bayley Scales of Infant Development43 was used as a measure of a child’s cognitive level at 24 months

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of corrected age. The MDI is based on a child’s performance on items that measure sensory-perceptual accuracy and discrimination, object constancy, memory, learning and problem-solving abilities, psycholinguistic ability, and generalization and classification abilities. In the original Bayley scales standardization sample,43 the mean MDI was 100 and the standard deviation 16. The behavioral characteristics were assessed with the Infant Behavior Record (IBR) of the Bayley Scales. The IBR consists of 30 rating items that permit an aggregated evaluation of social responsiveness, fearfulness, emotional tone, activity, attention span, and goal directness during the test. Behavior is rated on a 9-grade Likert scale, low scores indicating more problematic behavior. A number of investigations have examined the relationship of IBR ratings to other indices of infant behavior. Plomin and deFries44 reported significant correlations in the expected direction between IBR results and videotaped ratings of infant behavior in several naturalistic situations. IBR ratings have also been shown to correlate with parental ratings of their infant’s general temperament and reactions to daily events.44,45 The Toddler Temperament Questionnaire (TTQ)46 was used to assess children’s temperament at 2 years of age. It contains 97 items that measure nine dimensions of temperament: activity, rhythmicity, approach, adaptability, intensity, mood, persistence, distractibility, and sensory threshold. The evaluations are made by parents on a 6-grade Likert scale. TTQ yields scores for each of the nine dimensions of temperament and four diagnostic groups: easy, intermediate, difficult, and slow to warm up. Children with easy temperament are rhythmical, approaching, adaptable, mild, and positive. Children with difficult temperament are arrhythmic, withdrawing, low in adaptability, intense, and negative in mood. Slow-to-warm up temperament resembles the difficult temperament, but the children are more approaching and less intense.

Assessment at 4 Years of Age The Finnish version of Wechsler Preschool-Primary Scale of Intelligence (WPPSI)47 was used to assess outcome at 4 years of age. The Finnish version of the revised WPPSI was published in 1995 and therefore not available during this assessments. The items in the WPPSI are divided into two scales and further grouped into 11 subtests. The Verbal Scale includes tests of knowledge, comprehension, verbal similarities, arithmetical ability, vocabulary, and memory span. The Performance Scale includes tests of visual learning, visual discrimination, visual-motor ability, and visual-spatial ability. A Verbal IQ and Performance IQ are derived from scores on the Verbal and Performance Scales. The neuropsychological assessment was carried out using a pre-standard version of the Finnish Neuropsychological Investigation for Children (NEPSY-r, extended version)48 confining the analysis to the subscales for visual attention, visuo-motor performance, naming, word fluency, phonological analysis of speech, recognition of incomplete pictures, and comprehension of sentences. This test battery has now been standardized for Finnish children between the ages of 3–12 years. The test items used in the present study were identical with those in the standardized version.

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Analysis of the Data A criterion variable defining impaired language functioning was defined as a simultaneous presence, in WPPSI, of a 1 SD difference between verbal and performance quotients (VQ < PQ), and in NEPSY, of a score < 1 SD in phonological analysis, naming, comprehension of sentences and word fluency. The NEPSY scores directly reflect language functioning. In WPPSI, the discrepancy of 1 SD has clinical significance.47 This discrepancy has been considered to indicate significant impairment of language functioning in other studies as well.4

Statistical Methods According to the criteria defined above, each pre-term child was determined either to have or not to have an impaired language function. Logistic regression analysis was used to assess the associations of the outcome variables at age 2 (cognitive, temperamental and behavioral) with the occurrence of impaired language functioning at age 4. Due to the large number of temperamental and behavioral dimensions as compared to the size of the study group, conclusions regarding the role of individual variables or dimensions are not possible. Because of this, cognitive, behavioral and temperamental variables were treated only as groups of variables, with nine dimensions in each. Statistical tests were applied only to the groups of variables as a whole. Analysis of variance (Anova) was used to examine differences between group means. Chisquare tests were used to study the relation between the Bayley scores and the outcome of language functions at 4 years of age. For all comparisons, the alpha level was set at 0.05.

Results Outcome at 2 Years The cognitive performance measured by Bayley Scales revealed, that the mean Bayley MDI was 104 ± 12 at the corrected age of 2 years. Eight children (12.7%) scored one standard deviation below test mean (MDI 85 or less, but more than 70) (Table 1). There were 17 children (10.7%) with minor neurological symptoms as defined above. According to temperament assessment (TTQ), the pre-term children in our study showed a tendency to be less active, more adaptive, less intense, and less persistent, and to have lower sensory threshold to respond than normal children according to published age norms (Table 2). Four children were rated as having difficult temperament, easy temperament was assessed in 32 children. There were no children with slow-to-warm-up temperament. Assessment of behavior with IBR showed that pre-term children

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Table 1 Cognitive Performances at 2 Years of Age (Bayley MDI) and at 4 Years of Age (WPPSI) in Pre-Term Children Without and With Impaired Language Functioning

Bayley MDI SD MDI < 86 (%) Full Scale IQ SD IQ < 86 (%) Verbal Quotient (VQ) SD VQ < 86 (%) Information Vocabulary Arithmetic Similarities Comprehension Memory Span Performance Quotient (PQ) SD PQ < 86 (%) Animals house Picture completion Mazes Geometrical figures Block design

Pre-Terms Without Impaired Language Functioning (n = 49)

Pre-Terms With Impaired Language Functioning (n = 14)

110 13 8 (13) 107 13 12 (19) 108 11 12 (19) 12,1 11 9,1 12,6 11,5 10,9 104 13 10 (15) 11,4 12,3 10,7 7,9 10,9

91,7** 13 6 (43) 84** 16 9 (64) 79** 13 10 (71) 8** 6,2** 5,3** 7,5** 6,7** 7,7* 95* 17 4 (28) 8* 10,7 9* 7,8 9,6*

**p < 0.001; *p < 0.05.

tended to be less oriented toward environmental stimuli, less goal directed, less reactive, less enduring, and less co-operating, and they tended to have a more negative emotional tone than an average child at two years of age43 (Table 2). Outcome at 4 Years The cognitive performance measured by WPPSI at the age of 4 years revealed that the mean Full Scale Quotient (FQ) was 102 ± 17, the mean Verbal Quotient (VQ) was 101 ± 16, and the mean Performance

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Table 2 The Means of the Nine Dimensions of Toddler Temperament Questionnaire (TTQ) and the Means of the Nine Dimensions in the Infant Behavior Rating Scale (IBR) in 63 Pre-Term Children at the Corrected Age of 2 Years Pre-Term Infants Mean

SD

Mean

SD

3,27 2,55 2,97 2,85 3,57 2,59 2,96 4,09 4,3

0,73 0,79 1,09 0,8 0,85 0,74 1,01 4,09 4,3

4,13 2,49 2,97 3,42 4,03 2,96 3,45 4,39 3,61

0,8 0,81 1,00 0,86 0,76 0,69 0,83 0,76 0,88

Pre-Term Infants

IBR Dimensions Social orientation Emotional tone Cooperation Object orientation Goal directedness Attention span Endurance Activity Reactivity

Mean

SD

Age Mode (24 months)

5,74 5,60 2,30 5,60 3,90 4,60 4,60 5,20 5,00

1,34 1,60 1,80 1,20 1,30 1,50 1,30 1,10 1,30

5 7 3 7 5 5 7 5 7

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TTQ Dimensions Activity Rhytmicity Approach/Withdrawal Adaptability Intensity Mood Persistence Distractibility Threshold

Published Standards

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Quotient (PQ) was 102 ± 14. There were 12 children (19%) with subnormal FQ (85 or less), 12 children (19%) with subnormal VQ (85 or less), and 10 children (15%) with subnormal PQ (85 or less). The test profile is presented in Table 1. Boys scored significantly lower in FQ, VQ and PQ (p < 0.001) than girls. Neuropsychological assessment showed that the pre-term children in our study displayed difficulties in most of NEPSY tasks. Besides the NEPSY language tasks, mean scores in NEPSY were one standard deviation below age norms in visual attention and in visuo-motor accuracy (Table 3). At the age of 4 years, 22% of the pre-term children (14; 9 boys, 5 girls) met the criteria of impaired language functioning as defined above. The children with impaired language functioning did not differ significantly from the other children on birth weight, gestational age, or on days of mechanical ventilation. Of the 17 children classified as having minor neurological symptoms at the age of 18 months, 11 children had impaired language functioning. In all the children with impaired language functioning, the Full Scale Quotient (FQ) was 1 SD below the mean. Non-verbal performance (PQ) in the language impairment group was within the normal range, yet significantly lower than in children without impaired language functioning (94/102, respec-

Table 3 NEPSY Test Profiles at the Age of 4 Years in Pre-Term Children Without and With Impaired Language Functioning

NEPSY subtests Visual attention Visuomotor accuracy Phonological analysis Naming Word fluency Comprehension Picture recognition *p < 0.001.

Pre-Terms Without Language Impairment (n = 49)

Pre-Terms With Language Impairment (n = 14)

Mean

SD

Mean

SD

5,4 8 8,6 8,3 8,8 6,9 9,8

2,4 2,8 3,4 2,4 2,4 2,0 3,1

6,2 7,1 3,92* 5* 5,64 3,28* 8,7

2,7 2,6 2,4 2,4 1,2 2,1 4,0

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tively). The difference was due to low scores in the WPPSI subtests of animals’ houses, mazes, and block designs in the children with impaired language functioning. There was no significant difference between the groups in non-verbal NEPSY tasks (Table 3). In children with impaired language functioning, there was a decline in cognitive level between the ages of 2 and 4 years. At the age of two, the Bayley MDI score (92) had been at a normal level, as opposed to the slightly subnormal WPPSI FQ score (84) (Table 1). Factors Associated with Increased Risk for Impaired Language Functions All except for two children with normal language functioning at the age of four years had normal Bayley Scales score (> mean - 1SD). In the logistic regression analysis, the Bayley MDI score was significant in identifying increased risk for impaired language functioning, and it remained significant even in models including the other explanatory variables assessed at 2 years of age (chi-square tests, both with p < 0.05, df = 1). Based on the logistic regression model, a child scoring 72 in Bayley MDI had a 90 percent risk for impaired language functioning. The corresponding Bayley MDI scores for risk levels of 75, 50, 25 and 10% were 82, 92, 100, and 106, respectively. The group of the nine temperamental dimensions (TTQ) as a whole was statistically significant in identifying increased risk for an impaired language functioning when alone in the logistic model (chisquare, p < 0.05, df = 9). The analysis of individual temperamental dimensions pinpointed low persistence and high distractibility as the potentially important dimensions (smallest p-values) in indicating an increased risk of impaired language functioning, although they did not reach statistical significance. Since temperamental factors are important in forming behavioral patterns, the significance of the nine behavioral dimensions in the Bayley scales (IBR), as a group, was tested in a model which also included the nine temperamental variables. In this analysis none of the temperament dimensions emerged as a significant indicator of impaired language functioning. Low IBR-ratings as a whole were related to impaired language functioning (p < 0.01, df = 9). Among the single IBR dimensions, low endurance and poor co-operativeness seemed to be the best indicators (smallest p-values) of increased risk, although they did not reach statistical significance.

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Discussion The main finding of the present study is that it was possible, in an assessment made at the age of 2 years, to identify factors associated with increased risk for impaired language functioning at age 4 in preterm children without major disabilities. Predictive of subsequent language impairments were (1) low Bayley MDI scores, (2) temperamental factors emphasizing high distractibility and low persistence and (3) low scores in the IBR (especially endurance and co-operativeness). Cognitive Level A number of pediatric follow-up studies have reported that many very low birth-weight premature neonates attain normal developmental quotients when assessed during infancy. The usual conclusion has been that such findings reflect the effectiveness of neonatal intensive care.49,50 However, most interpretations of the cognitive status of pre-term infants are based upon the norms of standardized tests published in test manuals and generally obtained years ago, rather than on appropriate control group comparisons.51 Recent evidence also indicates a consistent and widespread rise in IQ and DQ scores both in children and adults over the last generation.52,53 Thus, conclusions based on norm referred age-appropriate developmental status may lead to an underestimation of the true incidence of cognitive delay in pre-term children.26 This is illustrated by the present study in which 22% of those children with normal cognitive level at age 2, in fact, had an impaired language functioning at age 4. The usefulness of early infant test performance for predicting later cognitive test performance has been questioned in a number of studies.54,55 Weisglas-Kuperus56 found that only 35% of the VLBW children with a mental delay at 2 years of age assessed with the Bayley Scales had a mental handicap at 3.6 years of age. However, it has also been shown that the predictive accuracy of the Bayley test increases with age.57 In addition, Siegel58 found that the predictive and classificatory accuracy of early infant test scores for subsequent cognitive development improved for pre-term children, if perinatal risk measures were included in the model. This may not be equally true for all samples. In the present study of a low-risk group of pre-term children the perinatal risk factors were not associated with the occurrence of impaired language functioning.

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Our findings are in accordance with those reported by Ross.59 He found that despite a normal overall MDI at the age of one year, preterm infants had deficits in the areas of eye-hand coordination, imitation, comprehension, and vocalization, as compared to full-term infants. The follow-up of these children showed that low scores on the Bayley Scales and delay in visuo-motor integration, speech articulation, and receptive language at preschool age indicated an increased risk for learning disabilities at the ages of 7 to 8 years.60 Ross et al.60 also reported that 7 to 8 years old pre-term children with learning disabilities had significantly lower Full Scale and Verbal IQ scores, but they did not differ from the pre-term children without learning disabilities on the Performance IQ. In general, this finding was partly confirmed in our study. The only significant differences we found in non-verbal performance (PQ, NEPSY) between children with and without impaired language functioning were in the tasks requiring a capacity for visual memorizing, conceptualizing, and planning. Since these are complex tasks producing high momentary working load, the poor performance of children with impaired language functioning may reflect an underdevelopment of meta-cognitive skills which are of great importance in developing subsequent academic skills. Ross et al.60 interpreted their findings to imply a continuing neuromotor basis for academic difficulties among pre-term children. This interpretation is in harmony with the maturational lag theory proposed by Saltz.61 According to this theory, there may be an underlying maturational delay in one major area of development that occurs earlier (e.g., motor ability) which then becomes evident through a delay in a different area developing at a later age (e.g., language). In accordance with this, the majority of children with impaired language functioning in the present study had minor neurological symptoms at the age of 18 months. Other studies have shown that early neurological symptoms may decrease over time, whereas difficulties in other areas such as verbal ability and behavior, may became apparent only later.62–68,22 Temperamental and Behavioral Factors The pre-term children in the present study were temperamentally less active, less intensive, and less persistent than normal children according to published age norms (TTQ). These characteristics, predisposing the child to a passive attitude towards environmental influ-

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ences, are likely to affect the child’s intentional, goal-oriented behavior. According to Tomasello,69 a child needs to develop its skills of intentionality both in order to organize its own behavior and to understand others behavior in terms of outcomes they intend to achieve. Such understanding is known to influence the way infants communicate with other people.69 Early intentional communication also has been shown to predict language abilities at 24 months of age.70 The temperamental profile of pre-term children thus may contribute to a risk of difficulties in the development of verbal and communication skills. Based on the findings of the present study, especially the dimensions of low persistence and high distractibility (TTQ) might be interesting as objects of further investigation. The importance of persistence in developing verbal and cognitive skills has also been emphasized in other studies.30,37,38 Analogous conclusions may be drawn on the basis of the present findings regarding behavioral variables. As a group, these pre-term children were at the age of 2 years less oriented toward environmental stimuli, less goal directed, less reactive, less enduring, and less cooperating than average children, and they also had a more negative emotional tone. Behavior was more strongly associated with language impairment than temperament. This is logical, since the child’s behavior is a molar variable combining the effects of a multitude of innate and acquired dispositions, such as temperament and social style. Based on the present findings, the behavioral characteristics of cooperation and endurance might be interesting objects for future research. Because of the small sample size of the present study, the conclusions regarding the basis of impaired language development must be considered tentative. However, albeit small, the sample should be reasonably representative, since it includes all pre-term children born at the University Central Hospital in Helsinki, with the exception of those who migrated out of Helsinki and those who were excluded on the basis of major disability. During the period of inclusion, all cases of threatening pre-term delivery in Helsinki area were treated at this hospital, irrespective of their socio-economic status. The importance of behavioral observations as early as at the age of two years as a complement to other measures should be underlined. The Bayley Scales (IBR) seems to be useful also in this respect, and specific temperament assessment may not yield additional information. It is important to highlight the possibility that even pre-term children without serious impairment, but who show some signs of be-

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havioral or cognitive difficulties as early as at the age of two years, might be at risk for unfavorable language development. Summary The role of temperamental and behavioral factors in predicting language impairments in pre-term children has received less attention than that of cognitive factors. The present study focused on the early temperamental (TTQ = toddler temperament questionnaire), behavioral (IBR = infant behavior record), and cognitive precursors of impaired language functioning in pre-school age pre-terms infants. The study group consisted of 63 pre-term infants with a mean birth weight of 1246 ± 437 g born in 1989–1991 in the University Central Hospital of Helsinki. Children with major disabilities (CP or mental retardation) were excluded. The assessments were made at the ages of 2 (Bayley MDI and IBR, TTQ) and 4 (WPPSI, NEPSY). At the age of 4 years, 22% showed impaired language function. Logistic regression analysis showed that the Bayley MDI score was the best predictor in identifying an increased risk for language impairment. Based on the logistic regression model, a child scoring 72 in Bayley MDI had a 90% risk for impaired language functioning. The corresponding Bayley MDI scores for risk levels of 75, 50, 25 and 10% were 82, 92, 100, and 106, respectively. Both temperamental and behavioral factors were associated with impaired language functioning. However, behavioral characteristics were more strongly associated with subsequent language impairment than temperament. In conclusion, the present findings show that it is possible to identify, in an assessment made at the age of 2 years, factors associated with impaired language functioning at the age of 4 in pre-term children without major disabilities. The findings also suggest that behavioral factors merit more consideration in the context of language development than has been traditionally attributed to them. It is important to highlight the possibility that even pre-term children without serious impairment, but who show some signs of behavioral or cognitive difficulties as early as at the age of two years, may be at risk for unfavorable language development. References 1. Byrne J, Elsworth C, Bowering E, Vincer M: Language development in low birth weight infants: the first two years of life. J Dev Behav Pediatr 14: 208–9, 1993.

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2. Coplan J, Gleason JR: Quantifying language development from birth to 3 years using the Early Language Milestone Scale. Pediatrics 86: 963–71, 1990. 3. Grunau RV, Kearney S, Whitfield MF: Language development at 3 years in preterm children of birth weight below 1000 g. Br J Disord Commun 25: 173–182, 1990. 4. Luoma L, Herrga˚ ard E, Martikainen A, Ahonen T: Speech and language development of children born at < or = 32 weeks gestation; a 5-year prospective follow-up study. Dev Med Child Neurol 40: 380–387, 1998. 5. Denckla MB, Rudel R: Rapid automatized naming of pictured objects, colors, letters and numbers by normal children. Cortex 10: 186–202, 1974. 6. Korkman M: NEPSY-a proposed neuropsychological test battery for young developmentally disabled children. Theory and evaluation. Helsinki, Finland: Helsinki University Press (Thesis), 1988a. 7. Carson DK, Klee T, Perry CK, Muskina G, Donaghy T: Comparison of children with delayed and normal language at 24 months of age on measures of behavioral difficulties, social and cognitive development. Inf Mental Hlth J 19: 59–75, 1998. 8. Whitfield MF, Grunau R, Holsti L: Extremely premature (< or = to 800 g) schoolchildren: multiple areas of hidden disability. Arch Dis Child Fetal Neonatal Ed 77: 857–907, 1997. 9. Cohen NJ, Davine M, Horodezky N, Lipsett L, Isaacson L: Unsuspected language impairment in psychiatrically disturbed children: prevalence and language and behavioral characteristics. J Am Acad Child Adolesc Psychiatry 32: 595–603, 1993. 10. Beichman JH, Brownlie FB, Ingis A, Wild J, Ferfuson B, Schachter D, Lancee W, Wilson B, Mathews R: Seven-year follow-up of speech/language impaired and control children: psychiatric outcome. J Child Psychol Psychiatry 37: 961–70, 1996. 11. Allen M: An overwiew of long-term outcome. In: Prematurity: Antecedents, Treatment and Outcome, eds. Witter, FR. and Keith, L. Boston: Little, Brown and Co., 1993. 12. Aylward GP, Pfeiffer SI, Wright A, Verhulst SJ: Outcome studies of low birth weight infants published in the last decade: A meta-analysis. J Pediatr 115–515, 1989. 13. Fazzi E, Orcesi S, Telesca S, Ometto A, Rondini G: Neurodevelopmental outcome in very low birth weight infants at 24 months and 5 to 7 years of age. Pediatr Neurol 17: 240–248, 1997. 14. Fawer CL, Besnier S, Forcada M, Buclin T, Calame A: Influence of perinatal, developmental and environmental factors on cognitive abilities of preterm children without major impairments at 5 years. Early Hum Dev 43:151–164, 1995. 15. Hall A, McLeod A, Counsell C, Thomson L, Mutch L: School attainment, cognitive ability and motor function in a total scottish very-low-birthweight population at eight years: a controlled study. Dev Med Child Neurol 37: 1037–1050, 1995. 16. Herrga˚ rd E, Luoma L, Tuppurainen K, Karjalainen S, Martikainen A: Neurodevelopmental profile at five years of children born at < 32 weeks gestation. Dev Med Child Neurol 35: 1083–1096, 1993. 17. Jongmans M, Mercuri E, deVries L, Dubowitz L, Henderson SE: Minor neurological signs and perceptual-motor difficulties in prematurely born children. Arch Dis Child Fetal Neonatal Ed 76: 9–14, 1997. 18. Korkman M, Liikanen A, Fellman V: Neuropsychological concequences of very low birth weight and asphyxia at term: follow-up until school-age. J Clin Exp Neuropsychol 18: 220–233, 1996. 19. Marlow N, Roberts L, Cooke R: Outcome at 8 years for children with birth weights of 1250 g or less. Arch Dis Child 68: 286–290, 1993. 20. Monset-Couchard M, deBethmann O, Kastler B: Mid- and long-term outcome of 89 premature infants weighing less than 1000 g at birth, all appropriate for gestational age. Biol Neonate 70: 328–338, 1996. 21. Roussounis SH, Hubley PA, Dear PR: Five-year-follow-up of very low birthweight

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38. 39. 40. 41.

Child Psychiatry and Human Development

infants: neurological and psychological outcome. Child Care Health Dev 19: 45–59, 1993. Roth SC, Baudin J, Pezzani-Goldsmith M, Townsend J, Reynolds EO, Stewart AL: Relation between neurodevelopmental status of very preterm infants at one and eight years. Dev Med Child Neurol 36: 1049–1062, 1993. Saigal SP, Szatmari P, Rosenbaum P, Cambell D, King S: Cognitive Abilities and Scool Performance of Extremely Low Birth Weight Children and Matched Term Control Children at Age 8 Years: A Regional Study. J Pediatr 118: 751–760, 1991. Siegel L: The long-term prognosis of pre-term infants. Hum Nature 5: 103–126, 1992. Waber DP, McCormic MC: Late neuropsychological outcomes in preterm infants of normal IQ: selective vulnerability of the visual system. J Pediatr Psychol 20: 721– 735, 1995. Wolke D, Ratschinski G, Ohrt B, Riegel K: The cognitive outcome of very preterm infants may be poorer than often reported: an empirical investigation of how methological issues make a big difference. Eur J Pediatr 153: 906–915, 1994. Hunt JV, Cooper AB, Tooley VH: Very low birth weight infants at 8 and 11 years of age: Role of neonatal illness and family status. Pediatrics 82: 596–603, 1988. Klein NK, Hack M, Breslan H: Children who were very low birthweight: developmental and academic achievement at nine years of age. J Dev Behav Pediatr 10: 32–37, 1989. Daniels D, Plomin R, Greenhalg J: Correlates of difficult temperament in infancy. Child Dev 55: 1184–1194, 1984. Roth K, Eisenberg N, Sell ER: The relation of preterm and full-term infants temperament to test-taking behavior and developmental status. Infant Behav Dev 7: 495– 505, 1984. Sajaniemi N, Salokorpi T, von Wendt L: Temperament profiles and their role in neurodevelopmenal assessed preterm children at two years of age. Eur Child Adolesc Psychiatry 7: 145–152, 1998. DiLalla LF, Thompson LA, Plomin R, Phillips K, Fagan JF, Haith MM, Cyphers LH, Fulker DW: Infant pedictors of preschool and adult IQ: A study of twins and their parents. Dev Psychol 26: 759–769, 1990. Field T, Dempsey J, Shuman HH: Bayley behavioral ratings of normal and highrisk infants: The relationship to Bayley mental scores. J Pediatr Psychol 4: 277– 283, 1979. Stevenson MB, Lamb ME: Effects of infant sociability and the caretaking environment on infant cognitive performance. Child Dev 50: 340–349, 1979. Matheny AP, Dolan AB, Wilson RS: Bayley’s Infant Behavior Record: Relations between behaviors and mental test scores. Dev Psychol 10: 696–702, 1974. Carey WB: Temperament issues in the school-aged child. Pediatr Clin North Am 39, 1992. Matheny AP: Temperament and cognition: relations between temperament and mental test scores. In Temperament in Childhood, eds. Kohnstam, GA, Rothbart, MK. Chichester, New York, Brisbane, Toronto, Singapore: John Wiley & Sons, 1989. Ross G: Temperament of preterm infants: Its relationship to perinatal factors and one-year outcome. J Dev Behav Pediatr 8: 106–110, 1987. Garrison WT: Assessment of temperament and behavioral style. In Developmental assessment in clinical child psychology: A handbook, eds. Johnson, J, Goldman, J. New York: Pergamon Press, 1990. Lerner RM, Lerner JV: Temperament-intelligence reciprocities in early childhood. In Origins of Intelligence: Infancy and Early Childhood: A contextual model, 2nd ed., 419–493, ed. Lewis, JD. New York: Plenum Press, 1983. Hagberg B, Hagberg G, Zetterstroˆ m R: Decreasing perinatal mortality—increase in cerebral palsy morbidity? Acta Pediatr Scand 78: 664–70, 1989.

Nina Sajaniemi et al.

345

42. Autti-Ra¨ mo¨ I, Granstro¨ m, M.-L: The effect of intrauterine alcohol exposition in various durations on early cognitive developmant. Neuropediatric 22: 203–210, 1991. 43. Bayley N: Bayley Scales of Infant Development. Manual. New York: The Psychological Corporation, 1969. 44. Plomin R, DeFries JC: Origins of individual differences in infancy: The Colorado Adoption Project. Orlando, FL: Academic Press, 1985. 45. Matheny AP: Twin similarity in the developmental transformations of infant temperament as measured in a multi-method, longitudinal study. Acta Genet Med Gemellol: Twin Research 33: 181–189, 1984. 46. Fullard W, McDevitt SC, Carey WB: Assessing temperament in one- to three-yearold children. J Pediatr Psychol 9: 205–217, 1984. 47. Wechsler D: Wechsler Preschool and Primary Scale of Intelligence. Finish Edition. Helsinki, Finland: Psykologien kustannus, 1971. 48. Korkman M, Kirk U, Kemp S: Neuropsychological investigation for children (NEPSY). Helsinki: The Psychological Corporation, 1997. 49. Driscoll JM, Driscoll VT, Steir ME, Stark RI, Dangman BC, Perez A, Wang J, Kritz P: Mortality and morbidity in infants less than 1000 grams birth weight. Pediatrics 69: 21–26, 1982. 50. Shennan AT, Milligan JE: The growth and development of infants weighing 1000 to 2000 grams at birth and delivered in a perinatal unit. Am J Obstetr Gynegol 136: 273–275, 1980. 51. Veen S, Ens-Dokkum MH, Schreuder AM, Verloove-Vanhornick SP, Brandt R, Ruys, JH: Impairments, disabilities, and handicap of very preterm and very-lowbirthweight infants at 5 years. Lancet 338: 33–36, 1991. 52. Flynn JR: Massive IQ gains in 14 nations: what IQ tests really measure. Psychol Bull 101: 171–191, 1987. 53. Fuggle PW, Tokar S, Grant DB, Smith I: Rising IQ scores in British children: recent evidence. J Child Psychol Psychiatry 33: 1241–1247, 1992. 54. Bee H, Bamars K, Eyres S, Grat C, Hammond K, Spiez A, Snyder C, Clark B: Prediction of IQ and language skill from perinatal status, child performance, family characteristics and mother-infant interaction. Child Dev 53: 1134–1156, 1982. 55. Rose S: Visual Recognition memory: A predictor of later cognitive functioning in preterm children. Child Dev 56: 544–553, 1985. 56. Weisglas-Kuperus N, Baerts W, Sauer PJ: Early assessment and neurodevelopmental outcome in very low-birth-weight infants: implications for pediatric practice. Acta Paediatr 82: 449–53, 1993. 57. Molfese VJ, Acheson S: Infant and preschool mental and verbal abilities. How are infant scores related to preschool scores? Int J Behav Dev 20: 595–607, 1997. 58. Siegel L: Infant tests as predictors of cognitive and language development at two years. Child Dev 52: 545–557, 1981. 59. Ross G: Use of the Bayley Scales to characterize abilities of premature infants. Child Dev 56: 835–842, 1985. 60. Ross G, Lipper E, Auld P: Cognitive abilities and early precursors of learning disabilities in very-low-birth-weight children with normal intelligence and normal neurological status. Int J Behav Dev 19: 563–580, 1996. 61. Salz P, Friel J: Some predictive antecedents of specific learning disability: a preliminary one year follow-up. In: The disabled learner: Early detection and intervention, eds. Friel, J and Saltz, P. Rotterdam: Rotterdam University Press, 1973. 62. Als H: (1985). Patterns of infant behavior: Analogues of later organizational difficulties. In: Dyslexia: A neuroscientific approach to clinical evaluation, pp. 67–92, eds. Duffy, FH and Geschwind, N, Boston: Little, Brown and Co., 1985. 63. DeGangi GA, Greenspan S: The development of sensory function in infants. Occup Ther Pediatr 8: 21–33, 1988. 64. Godbole K, Barve S, Chaudhari S: Early predictors of neurodevelopmental outcome in high risk infants. Indian Pediatr 34: 491–495, 1997.

346

Child Psychiatry and Human Development

65. Greenspan SJ: The development of ego: Insights from clinical work with infants and young children. In: The course of life: Infancy, pp. 85–164, eds. Greenspan, SI and Pollock, GH. Madison, WI: International Universities Press, 1989. 66. Nelson KB, Ellenberg J: Children who outgrew cerebral palsy. Pediatrics 69: 529– 536, 1982. 67. Prechtl HFR, Einspieler C, Cioni G, Bos AF, Ferrari F, Sontheimer D: An early marker for neurological deficits after perinatal brain lesions. Lancet 349: 1361– 1363, 1997. 68. Silva PA, McGee R, Williams S: A prospective study of the association between delayed motor development at ages three and five and low intelligence and reading difficulties at age seven: A report from Dunedin multidiciplinary child development study. J Hum Mov Stud 8: 187–193, 1982. 69. Tomasello M: Joint attention as social cognition. In: Joint attention: Its origins and role in development, pp. 103–129, eds. Dunham, P, Moore, C. Hillsdale, NJ: Lawrence Erlbaum, 1995. 70. Laakso M-L: Prelinguistic Skills and early Interactional Context as Predictors of Childrens’ Language Development. Jyva¨ skyla¨ , Finland: Jyva¨ skyla¨ University Press (Thesis), 1999.