Pediatric Neurology 51 (2014) 681e687
Contents lists available at ScienceDirect
Pediatric Neurology journal homepage: www.elsevier.com/locate/pnu
Original Article
Relationship Between Neurological Assessments of Preterm Infants in the First 2 Years and Cognitive Outcome at School Age Jana Kodric PhD a, Breda Sustersic MD b, Darja Paro-Panjan MD, PhD c, * a
Division of Paediatrics, Department of Neurology, University Medical Centre Ljubljana, Ljubljana, Slovenia Developmental Department, Health Centre, Domzale, Slovenia c Division of Paediatrics, Department of Neonatology, University Medical Centre Ljubljana, Ljubljana, Slovenia b
abstract BACKGROUND: The risk of cognitive disability in preterm infants is higher than in general population. The Amiel-
Tison neurological assessment could be a useful tool for early identification of preterm children at risk of cognitive disability in school age. This study investigated the value of categorization of neurological signs assessed by the Amiel-Tison neurological assessment in the first 2 years of life in relation to cognitive performance at school age in a group of preterm children. METHODS: Preterm children with gestational age from 23 to 36 weeks were included in the prospective study. From the initial group of 45 children, in whom the Amiel-Tison neurological assessment was performed at term age, at 3 months corrected age, and at 2 years, the Wechsler Intelligence Scale for Childrenethird edition was performed in 39 children after school entry. RESULTS: Full scale IQ, Verbal IQ, and Performance IQ of the whole group of preterm children were not significantly different from the normative data; most of the children had IQ scores in the normal range (85). The mean cognitive results of children decreased as the number of neurological signs increased. There was a significant correlation between the categories of neurological signs at 2 years and later cognitive results. CONCLUSIONS: The grade of severity of neurological signs at 2 years was associated with the cognitive results at school age. The categorization of neurological signs according to the Amiel-Tison neurological assessment in preterm children might have prognostic value for cognitive outcome at school age. Keywords: Amiel-Tison neurological assessment, preterm, cognitive, outcome
Pediatr Neurol 2014; 51: 681-687 Ó 2014 Elsevier Inc. All rights reserved.
Introduction
Medical and technological advances have improved the survival of preterm infants, but neurodevelopmental disabilities remain the most important consequence of preterm birth. Many preterm infants require additional medical and educational resources throughout childhood into adolescence, so it is important to identify these children early. In recent years, the research focus in developmental outcome of preterm infants has shifted from the study of major handicaps, such as intellectual disability,
Article History: Received June 9, 2014; Accepted in final form July 17, 2014 * Communications should be addressed to: Dr. Paro-Panjan; Division of Paediatrics; Department of Neonatology; University Medical Centre Ljubljana; Bohoriceva 20; Ljubljana 1000, Slovenia. E-mail address: [email protected] 0887-8994/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.pediatrneurol.2014.07.024
sensorineural hearing loss or blindness, cerebral palsy (CP), and epilepsy, to less severe and more frequent dysfunctions such as learning disabilities, borderline intelligence, neuropsychologic deficits, attention deficit hyperactivity disorder, and other behavioral problems.1,2 Although new measures of brain structure and function have improved the ability to identify preterm infants at risk of developmental disabilities, neurological assessment remains an important tool in daily clinical practice. The structural, standardized, and age-dependent AmielTison neurological assessment (ATNA) covers growth parameters and cranial morphology, neurosensory aspects, passive and active muscle tone, spontaneous motor activity, and primary reflexes. It considers signs that depend on the integrity of the upper structures (cranial signs, alertness, and axial tone) and enables a clinician to recognize minor neurological signs from the neonatal period to the age of 6 years.3,4 Minor neurological signs, which reflect minor brain
682
J. Kodric et al. / Pediatric Neurology 51 (2014) 681e687
damage occurring before, during, or after birth, present a window into central nervous system disruption, which may present as intellectual, academic, and behavioral problems.2 Amiel-Tison et al. studied three minor neurological and cranial signs, two of which refer to passive tone (imbalance in axial tone with excessive dorsal extension and a phasic stretch reflex in one or both gastrocnemius muscles), and a palpable ridge on the squamous suturesdthe Amiel-Tison triad (ATT). They demonstrated that these signs were important in documenting the relationship between mild brain damage and possible future learning disabilities.4 Significant correlations between the categories of neurological signs and the Bayley-II Mental Developmental Index have been found at age 2 years.5,6 At age 2 to 5 years, significant differences in the coordination, language, and practical reasoning according to categories of ATNA were present.4 Parents of children with abnormal neurological signs on ATNA reported significantly more problems in motor and/or praxis skills, language development, and attention at age 3 to 5 years in comparison with parents of children with optimal neurological status.7 In the longitudinal study, in which preterm children were classified into three groups (normal, impaired without disability, and with associated disability) at age 1 year, the results of ATNA were predictive of the cognitive performance on Griffiths Developmental Test at age 4, 8, and 14-15 years.8-10 The aim of the study was to evaluate the usefulness of ATNA for predicting developmental disabilities and to analyze the correlation between neurological signs assessed at three periods (newborn, infant, and toddler age) and cognitive performance at school age in a heterogeneous group of preterm children. The study is a part of a longitudinal follow-up of preterm children in which ATNA proved to be a useful clinical tool for predicting cognitive outcome at 2 years.5 Materials and Methods Participants In a single-centre longitudinal cohort study, we monitored a group of 45 preterm infants (23 boys and 22 girls) born in the period 2001-2004. All except three children were born at the Ljubljana Maternity Hospital. The inclusion criteria were (1) gestational age of 36 weeks or less; (2) one or more neonatal complications; and (3) first neurological examination at the corrected age of 40 weeks (5 days). Children with dysmorphic syndromes and chromosomal abnormalities were excluded from the study.
one ATT sign, intermediate with two ATT signs, ATT, minimal CP, and CP). The detailed procedures, scoring, and categorization of neurological signs are described elsewhere.3,11,12 Cognitive abilities at school age were assessed using the Wechsler Intelligence Scale for Childrenethird edition.13 Three composite scores were calculated: Full Scale IQ (FIQ), Verbal IQ (VIQ), and Performance IQ (PIQ). The results of IQ scores were considered as severely abnormal when the S.D. values were below 2, as mildly abnormal when between 1 and 2, and normal when 1 below the mean or higher. After the cognitive assessment at school age, parents were asked if their child was recognized as having special education needs according to the Slovenian Special Education Act.
Procedure After discharge from the maternity hospital, children were routinely referred to their regional outpatient Developmental Centre. Infants whose parents agreed to participate and signed an informed consent form were consequently enrolled in the study. ATNA was performed by an experienced pediatrician at term age and repeated every 3 months up to the age of 2 years when the final categorization was made. When children started school, they were invited for cognitive assessment; if there was no response, another postal and then telephone contact were attempted; and if there was still no response, a final invitation letter was sent a few months later. An experienced psychologist performed the cognitive assessment individually. The National Medical Ethics Committee in Slovenia approved the study.
Statistical analysis The mean and the S.D. of FIQ, VIQ, and PIQ were used in analysis. The measures of skewness and kurtosis were calculated for the distribution of the IQ scores. The z scores for skewness and kurtosis were 0.30 and 0.51, respectively, for the FIQ; 0.55 and 0.32, respectively, for the VIQ; and 0.21 and 0.53, respectively, for the PIQ. Both measures were below the limit of z score of 2.58, the level at which the distribution is considered to be significantly skewed or kurtic.14 A one-group t test was used to compare the results of the studied group with the reference population. P values 1 wk Sepsis CNS infection Seizures Hyperbilirubinemia exchange transfusion Surgical intervention CNS hemorrhage
23/22 (51/49) 8 (18) 15 (33) 22 (49) 7 10 28 12 28 18 3 6 4 2 6
683
She had a severe degree of neurological signs at term age and at 3 months corrected age, and CP was diagnosed at 2 years. Her Mental Developmental Index on the Bayley Scales of Infant Developmentesecond edition was below 50, and she was attending a special education program at the time of the follow-up. Cognitive outcome at school age
(16) (22) (62) (27) (62) (40) (7) (13) (9) (4) (13)
Abbreviation: CNS ¼ Central nervous system
successively preformed from term age to 2 years. The numbers of children in different categories of the classification according to neurological signs are presented in Table 2. From the initial group, 39 children participated in the cognitive assessment between 6 years 10 months and 9 years 8 months (mean age, 7.9 years; S.D., 0.8 years). The parents of four children refused to participate, one child was uncontactable, and one child was unable to cooperate with the assessment because of moderate intellectual disability.
Results of intelligence test (FIQ, VIQ, and PIQ) of all children were in the normal or mildly abnormal range, whereas none had results in the severely abnormal range (Figure). The FIQ scores ranged from 72 to 132, VIQ ranged from 72 to 140, and PIQ ranged from 71 to 133. The mean IQ scores of the whole group of preterm children at 7 years were in the normal range (Table 2). They were not significantly different from the normative data (FIQ: t(38) ¼ 0.51, P ¼ 0.62; VIQ: t(38) ¼ 0.49, P ¼ 0.63; PIQ: t(38) ¼ 0.36, P ¼ 0.72). The percentage of children with IQ 85 or higher was 79.49, 87.18, and 76.92 for FIQ, VIQ, and PIQ, respectively. The FIQ, VIQ, and PIQ scores were the highest in the groups of children with normal neurological status at term age, at 3 months corrected age, and at 2 years. The IQ scores decreased according to the number of neurological signs (Table 2). Children with a severely abnormal neurological status achieved the lowest IQ scores. The average IQ scores for three children with severe neurological signs at term age and at 3 months corrected age (two of them had CP and one had MCP at 2 years) were significantly lower than the normative mean. The children in whom the ATT was diagnosed at age 2 years achieved the lowest scores on FIQ and
TABLE 2. Results of WISC-III in Different Categories of ATNA at Three Different Assessment Periods and the Effect Size Compared With Normative Data
ATNA
n
WISC-III FIQ
At term age Normal Mild/moderate Severe At 3 mo corrected age Normal Mild Moderate Severe At 2 yr Normal Intermediate one sign Intermediate two signs Amiel-Tison triad MCP CP TOTAL
VIQ
PIQ
Mean
S.D.
d
Mean
S.D.
d
Mean
S.D.
d
10 26 3
103.30 98.27 87.33
13.42 17.08 0.58
0.22 0.11 0.84
102.30 98.46 90.67
12.11 16.27 2.52
0.15 0.10 0.62
104.10 98.65 86.00
15.79 16.08 4.00
0.27 0.09 0.93
13 11 12 3
104.54 100.18 93.92 87.33
13.43 18.16 16.30 0.57
0.30 0.01 0.40 0.84
103.77 100.00 94.50 90.67
14.87 16.28 14.14 2.52
0.25 0.00 0.37 0.62
104.46 100.73 95.00 86.00
13.19 17.47 17.11 4.00
0.30 0.05 0.34 0.93
16 6 9 3 2 3 39
106.81 102.83 96.78 79.67 81.00 84.00 98.72
12.51 15.20 16.00 11.59 8.48 6.08 15.82
0.45 0.19 0.21 1.35 1.27 1.07 0.08
105.88 102.83 97.67 76.67 84.50 88.67 98.85
14.06 10.76 13.42 4.51 12.02 2.08 14.75
0.39 0.19 0.15 1.56 1.03 0.75 0.08
106.88 101.67 96.67 88.33 80.00 83.00 99.08
12.31 17.59 15.29 19.30 2.83 8.89 15.82
0.46 0.11 0.22 0.78 1.33 1.13 0.06
Abbreviations: ATNA ¼ Amiel-Tison neurological assessment CP ¼ Cerebral palsy FIQ ¼ Full Scale IQ MCP ¼ Minimal cerebral palsy PIQ ¼ Performance IQ VIQ ¼ Verbal IQ WISC-III ¼ Wechsler Intelligence Scale for Childrenethird edition
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J. Kodric et al. / Pediatric Neurology 51 (2014) 681e687
FIGURE. Distribution of FIQ scores at different ages according to categories of neurological signs assessed by ATNA. ATNA, Amiel-Tison neurological assessment; ATT1, intermediate with one sign; ATT2, intermediate with two signs; ATT3, Amiel-Tison triad; CP, cerebral palsy; FIQ, Full Scale IQ; MCP, minimal cerebral palsy; PIQ, Performance IQ; VIQ, Verbal IQ.
VIQ. Children with the ATT, MCP, and CP had significantly lower results compared with the normative mean. The mean score for verbal abilities (VIQ) was higher than the mean score for nonverbal abilities (PIQ) in the group of children with MCP and CP, whereas the profile was reversed in the group of children with the ATT. The categories of neurological signs assessed by ATNA at 2 years were significantly correlated with the FIQ, VIQ, and PIQ at school age (Table 3). The correlation between the category of neurological signs at 3 months and cognitive outcome at school age was significant for FIQ and PIQ and approaching significance for VIQ, whereas the correlation between neurological signs at term age and cognitive outcome was not significant. The sensitivity of neurological signs assessed by ATNA to identify children with mildly abnormal cognitive outcomes and the negative predictive value were high at term age, 3 months, and 2 years, whereas the specificity and positive predictive value were low at all three ages (Table 4). Eight children needed special education assistance in mainstream schools; none of whom had a normal
neurological status at 3 months corrected age and at 2 years. Two of them had two neurological signs; three had the ATT, one MCP, and two had CP. Parents of two other children (one in the intermediate group with two signs and one from the group with CP at 2 years) reported significant learning problems, although the children had not yet been recognized as children with special education needs at school. Discussion
The risk of cognitive disability in preterm infants is higher than in term controls, although it is reported that most of the children born prematurely have IQs within the normal range.15 The results of the cognitive outcome measures in our group (FIQ, VIQ, and PIQ) are consistent with this observation because they were not significantly different from the normative data, and the variability was in the expected range. Results of all children on the Full Scale, Verbal Scale, and Performance Scale were in the normal or mildly abnormal range (>70), with most of the children achieving scores of 85 or higher. Aylward described a
J. Kodric et al. / Pediatric Neurology 51 (2014) 681e687 TABLE 3. The Correlations Between ATNA at Three Different Assessment Periods and Full Scale, Verbal, and Nonverbal IQ of WISC-III
ATNA
WISC-III FIQ
VIQ
r 0.261 95% CI 0.01 to 0.49 P 0.11 At 3 mo corrected age r 0.355 95% CI 0.07-0.56 P 0.03 At 2 yr r 0.608 95% CI 0.35-0.77 P
Contents lists available at ScienceDirect
Pediatric Neurology journal homepage: www.elsevier.com/locate/pnu
Original Article
Relationship Between Neurological Assessments of Preterm Infants in the First 2 Years and Cognitive Outcome at School Age Jana Kodric PhD a, Breda Sustersic MD b, Darja Paro-Panjan MD, PhD c, * a
Division of Paediatrics, Department of Neurology, University Medical Centre Ljubljana, Ljubljana, Slovenia Developmental Department, Health Centre, Domzale, Slovenia c Division of Paediatrics, Department of Neonatology, University Medical Centre Ljubljana, Ljubljana, Slovenia b
abstract BACKGROUND: The risk of cognitive disability in preterm infants is higher than in general population. The Amiel-
Tison neurological assessment could be a useful tool for early identification of preterm children at risk of cognitive disability in school age. This study investigated the value of categorization of neurological signs assessed by the Amiel-Tison neurological assessment in the first 2 years of life in relation to cognitive performance at school age in a group of preterm children. METHODS: Preterm children with gestational age from 23 to 36 weeks were included in the prospective study. From the initial group of 45 children, in whom the Amiel-Tison neurological assessment was performed at term age, at 3 months corrected age, and at 2 years, the Wechsler Intelligence Scale for Childrenethird edition was performed in 39 children after school entry. RESULTS: Full scale IQ, Verbal IQ, and Performance IQ of the whole group of preterm children were not significantly different from the normative data; most of the children had IQ scores in the normal range (85). The mean cognitive results of children decreased as the number of neurological signs increased. There was a significant correlation between the categories of neurological signs at 2 years and later cognitive results. CONCLUSIONS: The grade of severity of neurological signs at 2 years was associated with the cognitive results at school age. The categorization of neurological signs according to the Amiel-Tison neurological assessment in preterm children might have prognostic value for cognitive outcome at school age. Keywords: Amiel-Tison neurological assessment, preterm, cognitive, outcome
Pediatr Neurol 2014; 51: 681-687 Ó 2014 Elsevier Inc. All rights reserved.
Introduction
Medical and technological advances have improved the survival of preterm infants, but neurodevelopmental disabilities remain the most important consequence of preterm birth. Many preterm infants require additional medical and educational resources throughout childhood into adolescence, so it is important to identify these children early. In recent years, the research focus in developmental outcome of preterm infants has shifted from the study of major handicaps, such as intellectual disability,
Article History: Received June 9, 2014; Accepted in final form July 17, 2014 * Communications should be addressed to: Dr. Paro-Panjan; Division of Paediatrics; Department of Neonatology; University Medical Centre Ljubljana; Bohoriceva 20; Ljubljana 1000, Slovenia. E-mail address: [email protected] 0887-8994/$ - see front matter Ó 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.pediatrneurol.2014.07.024
sensorineural hearing loss or blindness, cerebral palsy (CP), and epilepsy, to less severe and more frequent dysfunctions such as learning disabilities, borderline intelligence, neuropsychologic deficits, attention deficit hyperactivity disorder, and other behavioral problems.1,2 Although new measures of brain structure and function have improved the ability to identify preterm infants at risk of developmental disabilities, neurological assessment remains an important tool in daily clinical practice. The structural, standardized, and age-dependent AmielTison neurological assessment (ATNA) covers growth parameters and cranial morphology, neurosensory aspects, passive and active muscle tone, spontaneous motor activity, and primary reflexes. It considers signs that depend on the integrity of the upper structures (cranial signs, alertness, and axial tone) and enables a clinician to recognize minor neurological signs from the neonatal period to the age of 6 years.3,4 Minor neurological signs, which reflect minor brain
682
J. Kodric et al. / Pediatric Neurology 51 (2014) 681e687
damage occurring before, during, or after birth, present a window into central nervous system disruption, which may present as intellectual, academic, and behavioral problems.2 Amiel-Tison et al. studied three minor neurological and cranial signs, two of which refer to passive tone (imbalance in axial tone with excessive dorsal extension and a phasic stretch reflex in one or both gastrocnemius muscles), and a palpable ridge on the squamous suturesdthe Amiel-Tison triad (ATT). They demonstrated that these signs were important in documenting the relationship between mild brain damage and possible future learning disabilities.4 Significant correlations between the categories of neurological signs and the Bayley-II Mental Developmental Index have been found at age 2 years.5,6 At age 2 to 5 years, significant differences in the coordination, language, and practical reasoning according to categories of ATNA were present.4 Parents of children with abnormal neurological signs on ATNA reported significantly more problems in motor and/or praxis skills, language development, and attention at age 3 to 5 years in comparison with parents of children with optimal neurological status.7 In the longitudinal study, in which preterm children were classified into three groups (normal, impaired without disability, and with associated disability) at age 1 year, the results of ATNA were predictive of the cognitive performance on Griffiths Developmental Test at age 4, 8, and 14-15 years.8-10 The aim of the study was to evaluate the usefulness of ATNA for predicting developmental disabilities and to analyze the correlation between neurological signs assessed at three periods (newborn, infant, and toddler age) and cognitive performance at school age in a heterogeneous group of preterm children. The study is a part of a longitudinal follow-up of preterm children in which ATNA proved to be a useful clinical tool for predicting cognitive outcome at 2 years.5 Materials and Methods Participants In a single-centre longitudinal cohort study, we monitored a group of 45 preterm infants (23 boys and 22 girls) born in the period 2001-2004. All except three children were born at the Ljubljana Maternity Hospital. The inclusion criteria were (1) gestational age of 36 weeks or less; (2) one or more neonatal complications; and (3) first neurological examination at the corrected age of 40 weeks (5 days). Children with dysmorphic syndromes and chromosomal abnormalities were excluded from the study.
one ATT sign, intermediate with two ATT signs, ATT, minimal CP, and CP). The detailed procedures, scoring, and categorization of neurological signs are described elsewhere.3,11,12 Cognitive abilities at school age were assessed using the Wechsler Intelligence Scale for Childrenethird edition.13 Three composite scores were calculated: Full Scale IQ (FIQ), Verbal IQ (VIQ), and Performance IQ (PIQ). The results of IQ scores were considered as severely abnormal when the S.D. values were below 2, as mildly abnormal when between 1 and 2, and normal when 1 below the mean or higher. After the cognitive assessment at school age, parents were asked if their child was recognized as having special education needs according to the Slovenian Special Education Act.
Procedure After discharge from the maternity hospital, children were routinely referred to their regional outpatient Developmental Centre. Infants whose parents agreed to participate and signed an informed consent form were consequently enrolled in the study. ATNA was performed by an experienced pediatrician at term age and repeated every 3 months up to the age of 2 years when the final categorization was made. When children started school, they were invited for cognitive assessment; if there was no response, another postal and then telephone contact were attempted; and if there was still no response, a final invitation letter was sent a few months later. An experienced psychologist performed the cognitive assessment individually. The National Medical Ethics Committee in Slovenia approved the study.
Statistical analysis The mean and the S.D. of FIQ, VIQ, and PIQ were used in analysis. The measures of skewness and kurtosis were calculated for the distribution of the IQ scores. The z scores for skewness and kurtosis were 0.30 and 0.51, respectively, for the FIQ; 0.55 and 0.32, respectively, for the VIQ; and 0.21 and 0.53, respectively, for the PIQ. Both measures were below the limit of z score of 2.58, the level at which the distribution is considered to be significantly skewed or kurtic.14 A one-group t test was used to compare the results of the studied group with the reference population. P values 1 wk Sepsis CNS infection Seizures Hyperbilirubinemia exchange transfusion Surgical intervention CNS hemorrhage
23/22 (51/49) 8 (18) 15 (33) 22 (49) 7 10 28 12 28 18 3 6 4 2 6
683
She had a severe degree of neurological signs at term age and at 3 months corrected age, and CP was diagnosed at 2 years. Her Mental Developmental Index on the Bayley Scales of Infant Developmentesecond edition was below 50, and she was attending a special education program at the time of the follow-up. Cognitive outcome at school age
(16) (22) (62) (27) (62) (40) (7) (13) (9) (4) (13)
Abbreviation: CNS ¼ Central nervous system
successively preformed from term age to 2 years. The numbers of children in different categories of the classification according to neurological signs are presented in Table 2. From the initial group, 39 children participated in the cognitive assessment between 6 years 10 months and 9 years 8 months (mean age, 7.9 years; S.D., 0.8 years). The parents of four children refused to participate, one child was uncontactable, and one child was unable to cooperate with the assessment because of moderate intellectual disability.
Results of intelligence test (FIQ, VIQ, and PIQ) of all children were in the normal or mildly abnormal range, whereas none had results in the severely abnormal range (Figure). The FIQ scores ranged from 72 to 132, VIQ ranged from 72 to 140, and PIQ ranged from 71 to 133. The mean IQ scores of the whole group of preterm children at 7 years were in the normal range (Table 2). They were not significantly different from the normative data (FIQ: t(38) ¼ 0.51, P ¼ 0.62; VIQ: t(38) ¼ 0.49, P ¼ 0.63; PIQ: t(38) ¼ 0.36, P ¼ 0.72). The percentage of children with IQ 85 or higher was 79.49, 87.18, and 76.92 for FIQ, VIQ, and PIQ, respectively. The FIQ, VIQ, and PIQ scores were the highest in the groups of children with normal neurological status at term age, at 3 months corrected age, and at 2 years. The IQ scores decreased according to the number of neurological signs (Table 2). Children with a severely abnormal neurological status achieved the lowest IQ scores. The average IQ scores for three children with severe neurological signs at term age and at 3 months corrected age (two of them had CP and one had MCP at 2 years) were significantly lower than the normative mean. The children in whom the ATT was diagnosed at age 2 years achieved the lowest scores on FIQ and
TABLE 2. Results of WISC-III in Different Categories of ATNA at Three Different Assessment Periods and the Effect Size Compared With Normative Data
ATNA
n
WISC-III FIQ
At term age Normal Mild/moderate Severe At 3 mo corrected age Normal Mild Moderate Severe At 2 yr Normal Intermediate one sign Intermediate two signs Amiel-Tison triad MCP CP TOTAL
VIQ
PIQ
Mean
S.D.
d
Mean
S.D.
d
Mean
S.D.
d
10 26 3
103.30 98.27 87.33
13.42 17.08 0.58
0.22 0.11 0.84
102.30 98.46 90.67
12.11 16.27 2.52
0.15 0.10 0.62
104.10 98.65 86.00
15.79 16.08 4.00
0.27 0.09 0.93
13 11 12 3
104.54 100.18 93.92 87.33
13.43 18.16 16.30 0.57
0.30 0.01 0.40 0.84
103.77 100.00 94.50 90.67
14.87 16.28 14.14 2.52
0.25 0.00 0.37 0.62
104.46 100.73 95.00 86.00
13.19 17.47 17.11 4.00
0.30 0.05 0.34 0.93
16 6 9 3 2 3 39
106.81 102.83 96.78 79.67 81.00 84.00 98.72
12.51 15.20 16.00 11.59 8.48 6.08 15.82
0.45 0.19 0.21 1.35 1.27 1.07 0.08
105.88 102.83 97.67 76.67 84.50 88.67 98.85
14.06 10.76 13.42 4.51 12.02 2.08 14.75
0.39 0.19 0.15 1.56 1.03 0.75 0.08
106.88 101.67 96.67 88.33 80.00 83.00 99.08
12.31 17.59 15.29 19.30 2.83 8.89 15.82
0.46 0.11 0.22 0.78 1.33 1.13 0.06
Abbreviations: ATNA ¼ Amiel-Tison neurological assessment CP ¼ Cerebral palsy FIQ ¼ Full Scale IQ MCP ¼ Minimal cerebral palsy PIQ ¼ Performance IQ VIQ ¼ Verbal IQ WISC-III ¼ Wechsler Intelligence Scale for Childrenethird edition
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J. Kodric et al. / Pediatric Neurology 51 (2014) 681e687
FIGURE. Distribution of FIQ scores at different ages according to categories of neurological signs assessed by ATNA. ATNA, Amiel-Tison neurological assessment; ATT1, intermediate with one sign; ATT2, intermediate with two signs; ATT3, Amiel-Tison triad; CP, cerebral palsy; FIQ, Full Scale IQ; MCP, minimal cerebral palsy; PIQ, Performance IQ; VIQ, Verbal IQ.
VIQ. Children with the ATT, MCP, and CP had significantly lower results compared with the normative mean. The mean score for verbal abilities (VIQ) was higher than the mean score for nonverbal abilities (PIQ) in the group of children with MCP and CP, whereas the profile was reversed in the group of children with the ATT. The categories of neurological signs assessed by ATNA at 2 years were significantly correlated with the FIQ, VIQ, and PIQ at school age (Table 3). The correlation between the category of neurological signs at 3 months and cognitive outcome at school age was significant for FIQ and PIQ and approaching significance for VIQ, whereas the correlation between neurological signs at term age and cognitive outcome was not significant. The sensitivity of neurological signs assessed by ATNA to identify children with mildly abnormal cognitive outcomes and the negative predictive value were high at term age, 3 months, and 2 years, whereas the specificity and positive predictive value were low at all three ages (Table 4). Eight children needed special education assistance in mainstream schools; none of whom had a normal
neurological status at 3 months corrected age and at 2 years. Two of them had two neurological signs; three had the ATT, one MCP, and two had CP. Parents of two other children (one in the intermediate group with two signs and one from the group with CP at 2 years) reported significant learning problems, although the children had not yet been recognized as children with special education needs at school. Discussion
The risk of cognitive disability in preterm infants is higher than in term controls, although it is reported that most of the children born prematurely have IQs within the normal range.15 The results of the cognitive outcome measures in our group (FIQ, VIQ, and PIQ) are consistent with this observation because they were not significantly different from the normative data, and the variability was in the expected range. Results of all children on the Full Scale, Verbal Scale, and Performance Scale were in the normal or mildly abnormal range (>70), with most of the children achieving scores of 85 or higher. Aylward described a
J. Kodric et al. / Pediatric Neurology 51 (2014) 681e687 TABLE 3. The Correlations Between ATNA at Three Different Assessment Periods and Full Scale, Verbal, and Nonverbal IQ of WISC-III
ATNA
WISC-III FIQ
VIQ
r 0.261 95% CI 0.01 to 0.49 P 0.11 At 3 mo corrected age r 0.355 95% CI 0.07-0.56 P 0.03 At 2 yr r 0.608 95% CI 0.35-0.77 P
