Developmental outcomes and cognitive functioning in infant and child heart transplant recipients
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1 Ž. Progress in Pediatric Cardiology Developmental outcomes and cognitive functioning in infant and child heart transplant recipients Marti Baum, M. Catherin Freier, Kimberly R. Freeman, Richard E. Chinnock Departments of Pediatrics and Psychology, Loma Linda Uni ersity Children s Hospital, Loma Linda, CA 92354, USA Abstract Pediatric heart transplantation has become a mainstay in the treatment of end-stage heart disease in infants and children. There is, however, sparse information on post-transplant developmental and cognitive functioning. At Loma Linda University Children s Hospital 223 infants have undergone heart transplantation surgery with a survival rate of 73% Ž n This article reports on four areas of investigation of this cohort of infants. Infant de elopment: Two studies were done utilizing the Bayley Scales of Infant Development Ž mean 100, S.D The first study Ž n 48. showed mean values within the normal range Mental Development Index Ž MDI. 87; Psychomotor Developmental Index Ž PDI. 90. The second study Ž n 23. showed developmental scores within normal limits in 4 8 month olds with a tendency for decline in development at months Ž MDI 83, PDI 77.. Child de elopment: Ninty-one infant recipients were greater than 5 years old. Forty-five children were excluded because of long distances from the hospital, second transplantation, abnormal karyotype, primary language non-english, or invalid testing. The Wechsler Preschool and Primary Scale of Intelligence-Revised testing of 5 6-year-olds Ž n 23. showed a Full Scale IQ of 74, Performance IQ of 76, and Verbal IQ of 77. The Wechsler Intelligence Scale for Children III testing of 7 10-year-olds Ž n 23. showed a Full Scale IQ of 86, Performance IQ of 89, and Verbal IQ of 86. The Wechsler Individual Achievement Test Ž mean 100, S.D. 15. yielded a Total Composite of 91, Mathematics Composite of 86, Language Composite of 98, and a Reading Composite of 94. Visual spatial skills: Visual motor integration Žmean 100, S.D. 15. was evaluated in 5 10-year-olds with a mean of 87; however, 52% of the children had scores below 1 S.D. Subtests from the Wechsler scales that assess visual motor and visual spatial skills indicated significant deficits. Beha ior: Younger children Ž n 33. demonstrated behaviors indicative of social isolation. Older children Ž n 36. showed behavior that was within the normal limits, but depression was noted in a significant number of them. Conclusions: Infant heart transplant recipients demonstrate IQ and achievement levels within the normal range, but there is a significant amount of variability with more children than would be expected scoring in the lower ranges. Children with heart transplantation are at risk for visual spatial skill deficits. Young children are at risk for social isolation while symptoms of depression are noted in older children Elsevier Science Ireland Ltd. All rights reserved. Keywords: Developmental outcome; Pediatric heart transplant; Infant heart transplant; Congenital heart disease; Cognitive function 1. Introduction Pediatric heart transplantation has evolved for almost two decades to become an accepted medical treatment for end-stage heart disease in children. Since the first infant heart transplantation in 1985, improvements in the management of graft survival Corresponding author. Present address: Department of Psychology, Loma Linda University, Loma Linda, CA 92354, USA. Tel.: address: kfreier@psych.llu.edu Ž M. C. Freier. and in the control of infection have been significant, leading to the current focus on quality of life outcomes after transplantation. It is no longer sufficient to focus only on the rates of survival. Now it is appropriate to carefully study the quality of life of these surviving children. While medical outcomes of heart transplantation in children have been reported, the few studies of cognitive and developmental outcomes have found either no developmental delays or average levels of intellectual functioning 1,2. There are even fewer studies of the outcomes of patients who have had heart transplantation surgery in in $ - see front matter 2000 Elsevier Science Ireland Ltd. All rights reserved. Ž. PII: S
2 160 ( ) M. Baum et al. Progress in Pediatric Cardiology fancy. However, cognitive outcomes in children with complicated heart conditions have been reported. In 143 infants with transposition of the great arteries, studies at 1 year of age revealed a Mental Developmental Index of 95 and a Psychomotor Developmental Index of A study of older children using the McCarthy Scales of Children s Ability revealed a lower IQ with a mean of Using the Stanford Binet Test of Intelligence, another study of infants and children after open-heart surgery found an intelligence quotient of Infant development At Loma Linda University Children s Hospital Ž LLUCH. a preliminary study of infant heart transplant recipients used the Bayley Scales of Infant Development Ž BSID. to test mental and psychomotor development and to examine infant behavior. Fortyeight infants between 4 and 30 months of age were tested 6. The mean developmental indexes for both mental Ž mean 87. and motor skills Ž mean 90. were within normal limits. A more recent LLUCH study examined the developmental outcomes of infant heart transplant recipients as it relates to medical and surgical risk factors 7. The Bayley Scales of Infant Development-II was used to assess 23 infant heart transplant recipients Ž 14 males and 9 females. at one or more age levels. The mean wait for transplant was 48 days with a range of days. The study found that early cognitive functioning was within normal limits, consistent with the earlier study. However, the study revealed mild to moderate declines in developmental skills after 1 year of age, as shown in Fig. 1. In studies of behavior, it was noted that infant orientation and engagement declined significantly throughout the second year of life, as reflected in poorer attention to tasks and less social interaction. Additionally, infants with greater than 30 min of profound hypothermic cardiac arrest Ž PHCA. performed significantly worse than those with less than 30 min of PHCA on both the mental and psychomotor indexes. Serious medical complications that occurred before the first assessment, such as transplant rejection and infection, predicted lower scores on the Psychomotor Developmental Index at the 4 8-month assessment Ž r 0.55, P The infant heart transplant recipients in both of these studies generally demonstrated normal limits of cognitive and motor skill development. However, medical factors need to be considered as a potential risk factor for delayed development. Fig. 1. Bayley Scales of Infant Development-II, Mental and Motor Indexes by age group. 3. Child development Neurodevelopmental outcomes were studied in children over the age of 5 years who had heart transplants in infancy. The study population was extracted from 225 children who had transplants at LLCH at less than 1 year of age. Of the patients, 165 were alive, a survival rate of 73%. Ninty-one of the infants were older than 5 years. Of these, 37 were excluded because of a second heart transplant, distant location, or abnormal karyotype, leaving 54 children for the study. Eight children s tests were considered invalid due to incomplete data or foreign language interference, leaving 46 subjects who had complete data for analysis. The presenting congenital cardiac diagnosis was predominately Hypoplastic Left Heart Syndrome Ž n 33, 72%.. One child had a cardiomyopathy, two had tumors, and 10 had a variety of other complex congenital heart defects. All the children were less than 1 year of age at the time of transplantation Ž mean 52 days, 28 days median, range days. Ž Table 1.. The majority of the infants Ž 57%. underwent heart transplantation as newborns less than 30 days of age. Approximately one-quarter of the infants had heart transplantation in the second month of life and the remainder were transplanted at 2 12 months of age. The study used a battery of neurodevelopmental tests including an evaluation of cognitive functioning. The Wechsler Preschool and Primary Scale of Intelligence-Revised Ž WPPSI-R. was used for 5 6-year-olds and the Wechsler Intelligence Scale for Children-III Ž WISC-III. was used for 7 10-year-olds. The Wechsler Individual Achievement Test Ž WIAT. was used to assess achievement in 36 of the school age children aged 5 10 years. There were 23 children in the 5 6-year age group who were assessed by the WPPSI-R with a mean Full Scale IQ of 74, mean Performance Subscale IQ of 76,
3 ( ) M. Baum et al. Progress in Pediatric Cardiology Table 1 Pre-transplant congenital cardiac diagnoses and age of transplant Congenital cardiac diagnosis Hypoplastic Left Heart Syndrome 33 Cardiomyopathy 1 Tumor 2 Other complex congenital defects 10 Number of children Age at transplant Percentage 0 30 days days or more days 24 and mean Verbal Subscale IQ of 77. There were 23 children in the 7 10-year age group who were tested with the WISC with mean Full Scale IQ of 86, mean Performance Subscale IQ of 89, and mean Verbal Subscale IQ of 86 Ž Table 2.. Achievement skills were evaluated in 36 children, 5 10 years of age, with a mean score of 91. The mean composite scores for each of the following areas was as follows: Reading Composite 94, Mathematics Composite 86, and Language Composite 98 Ž Table 3.. Younger children had mean levels of intellectual functioning in the low average range while older children had mean levels in the average range. Both younger and older children demonstrated average achievement skills. 4. Visual spatial skills Visual spatial skills were tested in 44 of the 46 children using the Beery Visual-Motor Integration Ž VMI.. Their mean total score for the group was 87 Ž S.D. 18. with a range of Although the mean fell within the normal range for visual-motor integration, it is significant that 52% of the children had scores 1 S.D. below the mean. This indicated that Table 2 Wechsler Intelligence Scale IQ scores, WPPSI-R for children 5 6 years old and WISC-III for children 7 10 years of age Wechsler Intelligence Scales Mean S.D. 15 Range WPPSI-R Full Scale IQ Verbal Scale IQ Performance IQ WISC-III Full Scale IQ Verbal Scale IQ Performance IQ Table 3 Wechsler individual achievement composite scores for children 5 10 years of age Wechsler Individual Achievement Test Mean S.D. Range WIAT Total Composite Score Reading Composite Mathematics Composite Language Composite in many children visual-motor skills were delayed. As a result of these visual-spatial concerns, this area of development was specifically studied in a larger cohort of infant heart transplant patients at LLUCH 8. Testing of 58 children, 5 10 years of age, yielded similar results with a mean VMI score of 86 ŽS.D Other subtests from the Wechsler scales that test for visual-motor and visual-spatial skills revealed skills significantly below the level in normal children of the same age. These skills included assembly of puzzles of objects and abstract designs. The mean for these tasks Ž 6.98 and 6.72, respectively. fell within the low average range of function. The 32 younger 5- and 6-yearolds also did tasks that included mazes and drawing geometric figures. The means for these tasks Ž5.38 and 5.88, respectively. fell within the borderline range of functioning. The 26 children, 7 10 years old, performed a timed task that involved the ability to transfer symbols. The mean performance on this task Ž revealed skills within the average range. The results of this study indicated that children who received heart transplants as infants had significant deficits in visual-spatial and visual-motor skills. The younger children performed significantly worse on these tasks than the older ones. The results emphasize the importance of evaluating visual-spatial and visual-motor domains in children after heart transplantation. 5. Behavior The parent s perceptions of their child s development was evaluated using the Personality Inventory for Children Ž PIC. 9. Measured variables included general behavioral characteristics such as anxiety, depression, social functioning, and perceived cognitive abilities. The study included 113 children who were at least 3 years of age and who had received their heart transplant during the 1st year of life. According to the parent s reports, older children, 6 10 years of age, had no clinically significant elevated values, whereas younger children, 3 5 years old, showed a number of clinical concerns including perceived cognitive delays and high degrees of social isolation. These younger children tended to play alone and indoors and they
4 162 ( ) M. Baum et al. Progress in Pediatric Cardiology Table 4 Parent report of child behaviors on the Personality Inventory for Children Personality Inventory for Standard scores Standard scores Children: Behavior Subscales Ages 3 5 Ages 6 10 Delinquency Withdrawal Anxiety Psychosis a Hyperactivity Social skills Somatic concerns Depression a Clinically significant. Reflects social isolation rather than psychotic behavior. had fewer friends Ž Table 4.. Additionally, parents of the younger patients expressed greater concerns for protecting their child from everyday dangers. Another study at LLUCH supports the findings that patients who have had heart transplantation in infancy have few behavioral concerns as older children 10. This study compared long-term psychosocial development in infant heart transplant recipients, to children with congenital heart disease Ž CHD. and to control children without heart conditions. Measurements of psychosocial development, including depressive symptoms and social competence, were based on mothers perceptions of their child s functioning. The results indicated that the children who had infant heart transplantation experienced fewer overall problems as compared to children with CHD, and they more closely resembled non-clinical control children. There was, however, significant variability in symptoms of depression within the transplant group, suggesting that a sizable subgroup of children Ž 39%. have some clinical level of depression. 6. Discussion To date there is little published information on developmental and cognitive outcomes in children after heart transplantation. And there is even less information about these outcomes in children who have heart transplantation in infancy. There are, however, studies of infants and children who have undergone open-heart surgery which can be helpful as a comparison group of patients. Furthermore, some studies have evaluated children with hypoplastic left heart syndrome who have had the Norwood surgical procedures in infancy. Using the Denver Developmental Screening Test, normal developmental outcomes were found in 16 infants who had heart transplants for a variety of congenital heart defects, most of them with hypoplas- tic left heart syndrome 11. These results may not be conclusive however, because the outcomes were based on a screening tool and not on a comprehensive assessment. In another study, 13 transplant children, from 6 months to 4.5 years of age, had a normal mean subtest score using the Ruth Griffiths developmental scales. However, the heart transplantation children did have significantly lower scores than the 10 normal children in the reference group of 15 congenital heart disease patients. While each of the studies presented above used different types of evaluation and studied a variety of age ranges, there was a trend for the means of infant and toddler neurodevelopmental tests to fall within the normal range. These outcomes are not unlike data from other studies that evaluate neurodevelopmental outcomes in infants undergoing cardiac surgical repair 3,12,13. It should be noted that studies of infants undergoing open heart surgery have provided some evidence that increased duration of deep hypothermic circulatory arrest is significantly associated with a risk of lower psychomotor developmental scores 3,7. Several studies of children who have undergone open heart surgery in infancy have found mean levels of cognitive function in the average range for intelligence 4,5, A study of 11 children who underwent the Norwood procedures in infancy reported that 82% had significant neurodevelopmental delays 17. In a more recent study 14 children who had the Norwood procedures had an average median IQ of 88 18, and a large study revealed similar results with a mean IQ of 83 in 29 children 19. Another study reported a mean verbal IQ of 88 and a mean performance IQ of 81.7, indicating cognitive functioning in the average range. The studies described in this review reflect concerns about visual spatial deficits. A study of children who had surgery for congenital heart disease found that visual-motor integration scores were more than 1 S.D. below the mean among those with and without cyanosis; other gross motor delays were noted as well 20. Other than the studies presented in this review, no other studies have specifically examined child psychosocial functioning in infant heart transplant recipients. In children receiving a heart transplant at age 16 or younger and who were at least 3 months posttransplant, evaluations of psychosocial functioning found that the children displayed less social competence and more psychological dysfunction as compared to normals 21. Psychological dysfunction was most suggestive of depression, and it was associated with increased parenting stress and limited family resources. These studies suggest that depression may be an important issue in transplant recipients regardless of the age of surgery.
5 ( ) M. Baum et al. Progress in Pediatric Cardiology Conclusions Cognitive development in infants and children with heart transplantation falls within the average range. However as a group, the mean is slightly lower than non-clinical populations. The risk for developmental delay and cognitive difficulty is greater for these patients. Older children have better performances than younger ones in intelligence assessments, visual spatial skills, and parent-reported behaviors, perhaps because of fewer social restrictions and richer educational environments at the older ages. Furthermore, it is important to note that the question of underlying brain abnormalities has been raised in children with hypoplastic left heart syndrome 22. Abnormal neurobehavioral and neurological abnormalities have been described in presurgical infants with congenital heart defects 23. This invokes concern about potential intrauterine risks or even fetal neuroanatomical abnormalities associated with abnormal cardiac function in utero. The impact of such potential risks on cognitive functioning has not been studied or addressed. Additional longitudinal studies of genetic, medical, and developmental factors are needed to identify other risks for the infant and young child undergoing heart transplantation. Acknowledgements The authors are indebted to Jeanette Allen, RN for her organization and persistence in subject recruitment and to Stephen Ashwal, M.D. for his support of this work. References 1 Dunn JM, Cavarocchi NC, Balsra RK et al. Pediatric heart transplantation at St. Christopher s Hospital for children. J Heart Transplant 1987;6Ž. 6 : Wray J, Pot-Mees C, Zeitlin H, Radley-Smith R, Yacoub M. Cognitive function and behavioral status in pediatric heart and heart lung transplant recipients: the Harefield experience. Br Med J 1994;309: Bellinger DC, Rappaport LA, Wypij D, Wernovsky G, Newburger JW. Patterns of developmental dysfunction after surgery during infancy to correct transposition of the great arteries. J Dev Behav Pediatr 1997;18Ž. 2 : Wells FC, Coghill S, Caplan HL, Lincoln C, Kirklin JW. Duration of circulatory arrest does influence the psychological development of children after cardiac operation in early life. J Thorac Cardiovasc Surg 1983;86Ž. 6 : Miller G, Tesman JR, Ramer JC, Baylen BG, Myers JL. Outcome after open-heart surgery in infants and children. J Child Neurol 1996;11: Baum M, Chinnock R, Ashwal S. Growth and neurodevelopmental outcome of infants undergoing heart transplantation. J Heart Lung Transplant 1993;12Ž. 6 Pt2:S211 S Freier MC, Mallery S, Baum MF, Vaz C. Medical and surgical variables influence neurodevelopmental outcome in infant heart transplant recipients. Presented at the 11th Annual Convention of the American Psychological Society, Denver, CO, Freier MC, Freeman K, Griffone S, Baum M. Visual-spatial and visual-motor processing in pediatric heart transplant recipients. Presented at the 106th Annual Convention of the American Psychological Association. San Francisco, CA, Freier MC, Baum MF, Chinnock RE, Freeman K, Vaz C, Larsen R. Parent perception of child development post infant heart transplantation. Presented at the Third Loma Linda International Conference on Pediatric Heart & Lung Transplantation. Rancho Mirage, California, Freeman K. Family and child psychosocial functioning of infant heart transplant recipients. Unpublished doctoral dissertation. Loma Linda University, Loma Linda, CA, Backer C, Zales V, Harrison H, Idriss F, Benson D, Mavroudis C. Intermediate term results of infant orthotopic cardiac transplantation from two centers. J Thorac Cardiovasc Surg 1991;101: Rappaport LA, Wypij D, Bellinger DC. Relation of seizures after cardiac surgery in early infancy to neurodevelopmental outcome. Circulation 1998;97: Haneda K, Itoh T, Ohmi M, Mohri H. Effects of cardiac surgery on intellectual function in infants and children. Cardiovasc Surg 1996;4Ž. 3 : Clarkson PM, MacArthur BA, Barratt-Boyes BG, Whitlock RM, Neutze JM. Developmental progress after cardiac surgery in infancy using hypothermia and circulatory arrest. Circulation 1980;62Ž. 4 : Farrell DM. Current results of the Boston circulatory arrest study preliminary findings on four year evaluation. Presented at National Conference on Pediatric Perfusion, Indianapolis, IN, Hovels-Gurich HH, Seghaye MC, Dabritz S, Messmer BJ, von Bernuth G. Cognitive and motor development in preschool and school-aged children after neonatal arterial switch operation. J Thorac Cardiovasc Surg 1997;114Ž. 4 : Rogers BT, Msall ME, Buck GM. Neurodevelopmental outcome of infants with hypoplastic left heart syndrome. J Pediatr 1995;126Ž. 3 : Kern JH, Hinton VJ, Nereo NE, Hayes CJ, Gersony WM. Early developmental outcome after the Norwood procedure for hypoplastic left heart syndrome. Pediatrics 1998;102 Ž. 5 : Mahle WT, Wernosvsky G, Gerdes M et al. Neurodevelopmental outcome of school-age children with hypoplastic left heart syndrome. Circulation 1998;1785 Suppl Campbell LA, Kirkpatrick SE, Berry CC. Psychoeducational assessment of children with congenital heart disease undergoing cardiac surgery. Calif School Psychol 1997;2: Uzark KC, Sauer SN, Lawrence KS et al. The psychosocial impact of pediatric heart transplantation. J Heart Lung Transplant 1992;11: Glauser T, Rorke L, Weinberg P, Clancy R. Congential brain anomalies associated with the hypoplastic left heart syndrome. Pediatrics 1990;85Ž. 6 : Limperopoulos C, Majnemer A, Shevell M, Rosenblatt B, Rohlicek C, Tchervenkov C. Neurologic status of newborns with congenital heart defects before open heart surgery. Pediatrics 1999;103Ž. 2 :
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