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* Department of Pediatrics, Royal Brompton and Harefield National Health Service Trust, Harefield Hospital, Middlesex, United Kingdom
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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Methods. Children <3.5 years old were assessed before transplantation (n = 35) and compared with a group of children awaiting conventional cardiac surgery, a group undergoing bone marrow transplantation, and a group of healthy children. Development was measured by using the Ruth Griffiths Mental Development Scales, and behavior was measured with the Achenbach Child Behavior Checklist.
Results. Within the transplant group, 17 had congenital heart disease (CHD), and 18 had cardiomyopathy (CM). Although the overall mean developmental scores were within the normal range for the transplant, conventional cardiac surgery, and bone marrow transplantation groups, scores were significantly lower than those of the healthy group. Within the transplant group, those with CHD had a significantly lower mean developmental quotient than those with CM. Furthermore, the CHD patients obtained significantly lower scores than those with CM on areas of development covering locomotor abilities, speech and hearing, eye-hand coordination, and performance.
Conclusions. In common with other groups of ill children, patients awaiting heart or heart-lung transplantation are at risk for developmental delay. Diagnosis is a salient factor in determining outcome in most areas of development. Psychosocial interventions need to be targeted to maximize developmental potential before transplantation.
Key Words: development • behavior • heart transplantation
Abbreviations: CHD, congenital heart disease • CM, cardiomyopathy • BMT, bone marrow transplantation • DQ, developmental quotient • CBCL/2-3, Child Behavior Checklist for ages 2 to 3 year • CI, confidence interval
Chronic illness in infancy compromises development,1–5 with gross motor and language development in particular being affected.6 For children with congenital heart disease (CHD), developmental and cognitive impairment have been reported, particularly in those with cyanotic lesions.7–12 Neonates with CHD have exhibited disorganized and frenetic motor movements13 and developmental delay,14 and a significant proportion have neurobehavioral abnormalities.15 An additional risk factor for poor outcome in infants with CHD is prematurity.16 By contrast, there is no documented evidence that young children with acquired heart disease such as cardiomyopathy (CM) have any significant degree of developmental or cognitive impairment.
Heart or heart-lung transplantation is now the treatment of choice for children with end-stage heart or lung disease. Increasingly, attention is focusing on the psychological concomitants of such treatments for school-aged children and adolescents. In 1 of the few investigations into preschool-aged children, a study of neurodevelopmental outcome in infants 4 months after heart transplantation found that 11 of the 57 infants studied had abnormal neurologic examinations, with hypotonia being the most common abnormality.17 Additional follow-up revealed some deterioration in developmental skills after 1 year of age and increasingly poorer attention to tasks and less social interaction in the second year of life.18 Another study found that children transplanted before 2 years of age had delayed development and delayed speech and hearing and performed at a lower level than children who had undergone other types of cardiac surgery requiring cardiopulmonary bypass.19 However, studies to date have been retrospective, and there is little documented information about the developmental and behavioral status of infants and young children before undergoing transplantation or about how the development of such children compares with that of other groups of ill children or with that of healthy children.
The present study, focusing on children <3.5 years old, was designed to address limitations in the existing literature. To our knowledge, this is the first controlled, prospective evaluation of developmental functioning in younger children awaiting heart or heart-lung transplantation. Three comparison groups were used, consisting of a group of children awaiting conventional surgery for correction of congenital heart lesions, a second group of children before undergoing bone marrow transplantation (BMT), and another group of healthy children. Data on the comparison groups have been reported previously.20
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Children and families were included in the study if they lived in the United Kingdom or Eire and spoke English as their first language and the child was <3.5 years old and being assessed for acceptance onto the waiting list at Harefield Hospital for heart or heart-lung transplantation. During the study period, there were 52 admissions that met the criteria for inclusion in the study, 35 of which were seen for psychological assessment. Of those patients not recruited into the study, 6 died soon after hospital admission, 4 were transplanted before they could be recruited, and in 7 cases, parents declined to participate, in most cases because their children were very ill and they themselves were too distressed to take part. Of the 35 patients recruited, 26 underwent developmental testing. In 9 cases, meaningful assessment of the child’s developmental status was not possible because of the poor physical condition of the patients. The conventional heart surgery sample comprised a consecutive series of children admitted for elective surgery who were 0 to 3.5 years old and were recruited from 3 specialist units in London over a period of 2 years. The BMT sample was made up of a consecutive series of children recruited over 33 months from 4 specialist units. The healthy group was recruited from 2 London health centers.20,21
Measures
Children in all 4 groups were assessed by using the Ruth Griffiths Mental Development Scales.22,23 For children <2 years old, there are 5 subscales: locomotor, personal/social, speech and hearing, eye-hand coordination, and performance. A sixth, the practical reasoning scale, is added from the third year onward (this scale applied to only 21 children in the sample and is not reported in the results). An overall developmental quotient (DQ) is also calculated, with scores between 85 and 115 being considered to be within the normal range. In common with other measures of development, the scales rely on a degree of parental reporting and focus more heavily on sensory motor function than tests for older age groups. Their validity as a predictive measure of later intelligence, therefore, has been questioned,24–26 but the features on which the scales focus are those considered pertinent to the development of preschool children. The scales are the most widely used in the United Kingdom,27 and they have been used with chronically ill and handicapped children.28–31
Children in the transplant group were assessed at the time that they were accepted onto the waiting list for transplant. Those in the conventional heart surgery and BMT groups were assessed after admission for their procedure. All the developmental assessments were conducted by a psychologist specifically trained in the administration of the Ruth Griffiths scales.
Behavior of children 2 to 3 years old was assessed with the Child Behavior Checklist for ages 2 to 3 (CBCL/2-3).32 This questionnaire was only administered to children in the transplant group and was completed for 9 of the 15 eligible children. The CBCL/2-3 was filled in by parents to obtain a rating of the child’s behavioral/emotional status. There are 6 narrow-band syndrome scales (social withdrawal, depressed, sleep problems, somatic problems, aggressive, and destructive) together with 2 broad-band scales (internalizing and externalizing behavior) and a total problem score. In contrast to the version for older children, there are no gender differences in the scoring profiles. Normative and clinical sample mean scores are available, and satisfactory reliability and validity have been reported.32 The measure has been used previously with children with CHD.33,34
In addition, parents took part in a semistructured interview that included questions about their child’s behavior and medical history. The length and weight of the transplant patients were also measured and plotted on appropriate growth charts. Length measurements were also available for the conventional heart surgery group.
Statistical Analysis
Developmental measures were compared by 1-way analysis of variance, and Scheffe’s multiple comparison tests were used to identify the source of any significant differences between the 4 groups. Performance of the CHD and CM subgroups was compared by using independent t tests. Correlations were measured by using Spearman’s correlation coefficients, and multivariate analysis was performed to determine the extent to which medical factors may explain any variance in the overall DQ scores. Scores on the CBCL/2-3 are presented as mean total and broad-band and narrow-band scores. Sample sizes were too small for statistical analysis of any differences between the CHD and CM subgroups.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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Characteristics of the 4 groups of children are given in Table 1.
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2: 5.23; P < .05). Ten (59%) children in the CHD group had undergone previous cardiac surgery, which differed significantly from the CM group (2: 15.5; P < .001). Children with CHD had spent more time in the hospital (mean: 26 weeks) and had more admissions to the hospital than those with CM (mean time in hospital: 10 weeks), but the difference was not significant. Twenty-two (63%) transplant patients had feeding problems as infants, 13 of whom had CHD, but the proportion of children with feeding problems did not differ significantly between those with CHD and those with CM.
Developmental Testing
With the exception of locomotor development in the transplant group, all the mean subtest scores and overall DQ scores for the transplant, conventional surgery, BMT, and healthy groups were within the normal range. Although all individual DQs were within the normal range in the conventional heart surgery, BMT, and healthy groups, in the transplant group 3 children (12%) had an overall DQ score of 
70 (2 standard deviations below the mean), and an additional 6 children had scores of between 71 and 85.
Comparison With the Reference Groups
Scores were significantly lower on the locomotor, personal/social, and speech and hearing subscales for children in each of the 3 illness groups than for the group of healthy children (Table 2), but on the eye-hand coordination and performance subscales the differences were significant only for the transplant and healthy groups. There were no significant differences on any parameters of development between the 3 illness groups. In terms of individual scores, 10 children in the transplant group, 4 children in the conventional cardiac surgery group, and 2 children in the BMT group had locomotor scores of 70. All individual scores in the healthy group were within the normal range (Table 3).
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70 had CHD. On the individual subtests, a higher proportion of children with CHD obtained scores below the normal range than those with CM (Table 3), with this being most evident on the locomotor subscale.
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Bivariate correlations indicated that previous surgery, age at diagnosis, diagnosis, and type of transplant for which the child was waiting were all correlated significantly with overall DQ (r > .4 and P < .05 in all cases). Multivariate analysis indicated that diagnosis and age accounted for 57% of the variance in overall DQ, with lower overall DQ score associated with a diagnosis of CHD (t = 5.34; P < .005) and younger age (t = 2.52; P < .05).
Behavior
Two of the 9 children for whom CBCL data were available obtained scores above the cutoff of 63 (Table 5), and both had CHD. On the individual narrow-band scales, 1 child scored above the cutoff on each of the social-withdrawal, depression, and sleep problems scales. No children scored above the cutoff on the aggressive or destructive scales, but 5 of the 9 (56%) scored above the cutoff on the somatic problems scale.
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Growth
The growth parameters for the CHD and CM subgroups, total transplant group, and conventional cardiac surgery group are shown in Fig 1. Children with CHD were significantly smaller (height and weight) than those with CM. There were no differences between the total transplant and conventional cardiac surgery groups in terms of height, but comparison of the CHD subgroup and conventional surgery group did indicate a significant difference.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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The transplant, conventional cardiac surgery, BMT, and healthy groups all obtained overall DQ scores within the normal range, and all subscale mean scores, with the exception of the locomotor subscale mean score in the transplant group, were also within the normal range. However, the healthy group achieved higher scores than would be expected from the standardized norms for the tests.22,23 The most likely explanation for this is that the standardized norms for the tests are no longer appropriate. In support of this view, a study of 447 infants tested with the Ruth Griffiths scales found a significantly higher DQ than that originally suggested.26 The same argument has also been made in a study of children with CHD using other infant scales of development, in which scores were not significantly different than the standardized means for the test, but the normative values were also no longer accurate.35
Comparison of the transplant and reference groups indicated that all 3 illness groups achieved significantly lower scores than the healthy group, which supports previous studies of CHD8,12,14,36 and children undergoing BMT37 and corroborates other findings of compromised development attributable to chronic illness per se.1–5 Although the lack of difference between the 3 illness groups supports a noncategorical rather than a disease-specific approach38 to determining the impact of chronic illness on development, the significant differences within the transplant group highlight the importance of the effects of underlying diagnosis on development. Children with CHD achieved significantly lower scores than those with CM in all areas of development except for personal/social skills. There are a number of possible explanations for these results, some of which have been previously postulated for our conventional cardiac surgery patients.20 First, children with cardiac disease are often less physically able to interact with their environment because of the limiting nature of their condition. In common with all tests of infant development, the Ruth Griffiths scales depend to a significant extent on physical activity. Furthermore, impaired physical abilities have a detrimental impact on the development of other skills such as exploratory behavior. Although the children with CM were also likely to experience some of the same physical restrictions due to poor cardiac function, for a number of the patients the illness had been of recent onset and development had been normal before this, which is reflected in the greater impairment on the locomotor scale of the CHD patients compared with the CM group than on the other subscales. In contrast to those with CHD, some of the patients with CM had lost previously acquired physical skills such as walking. Second, the effects of prolonged illness and hospitalization are likely to have had an impact on development. All children in the transplant group had spent some time in the hospital, but those with CHD had spent longer periods in the hospital, were more likely to have been admitted to a special care infant unit, and had had more admissions than those with CM. It is well documented that there is a critical period of 6 months to 4 years during which hospitalization can have a particularly detrimental psychological effect on a child39,40 due to factors such as the physical environment and the number of different people involved in caring for the child, as well as factors related to the illness and treatment. Children in the transplant group, and particularly those with CHD, had previously undergone procedures under general anesthetic. Increasing numbers of procedures under general anesthetic and periods of hospitalization have been associated with adverse effects on development in preschool-aged children.30
An additional factor is that of feeding difficulties, particularly in infants, which was reported for three quarters of our patients with CHD and half of those with CM. Feeding problems are common during the first year of life41 and have been reported in up to 30% of healthy infants.42 Infants with CHD can be difficult to feed,43 and parental anxiety and feelings of inadequacy associated with feeding problems may result in parents withdrawing emotional support from their child.44,45 Development thus may be hindered by the physical and emotional difficulties associated with feeding, and these may be contributory factors not only to the differences between the CHD and CM subgroups but also to the differences between the ill and healthy groups.
Although the emotional significance attached to the heart can create significant adjustment difficulties,46 a factor that is clearly relevant for both the CHD and CM subgroups, the congenital nature of the lesion can result in feelings of parental guilt.47,48 This in turn can affect parental attitudes to the child. Maternal overprotectiveness has been reported previously for children with CHD,49,50 and emotional adjustment of the child is also likely to be related to parental stress.11 The psychological factors associated with having a child with CHD influence parental attitudes toward the child,51 which in turn are likely to have a significant impact on their child’s development. Some mothers in the transplant group, particularly those whose children had CHD, did not take their child out or allow them to attend playgroups, etc. This was also a feature of the conventional cardiac surgery and BMT groups and tended to reflect maternal anxiety concerning the risk of infection or the child being physically overwhelmed because of their small size. Such restrictions limited the child’s social interactions and are likely to have had an impact on the development of speech and socialization skills, resulting in poorer performance in these areas for all illness groups compared with the healthy group and in the CHD group compared with the CM group.
Finally, a number of medical factors are likely to contribute to the differences in development between the CHD and CM groups. As well as a longer duration of illness in the CHD children, a number of children in this group had undergone previous cardiac surgery with circulatory arrest and low-flow cardiopulmonary bypass, which can be associated with motor delay.52,53 Furthermore, in contrast to those with CM, some children in the CHD groups had cyanotic lesions, and hypoxia may also have had an impact on development.8,12,36 Growth was impaired more markedly in the CHD group, and some parents would have been aware that poor growth reflected associated morbidity,54 thus increasing their own anxieties.
Little has been written about the behavior of chronically ill preschool-aged children, and the results we obtained by using the CBCL/2-3 need to be interpreted with caution due to the small sample size and lack of corresponding data for the reference groups. However, the data indicate that internalizing, rather than externalizing, behavior patterns predominated in the transplant population and that this applied particularly to those children with CHD. This pattern of behavior has been found in studies of older children with CHD55,56; however, in a study using the CBCL with young children with CHD, internalizing and externalizing behaviors were equally prevalent.33 Not surprisingly, with children waiting for a transplant, somatic problems were the most prevalent, but these results are likely to be confounded by the actual poor physical condition of the patients and highlight the difficulties of assessing behavior in chronically ill children using measures that include somatic items. There was a trend for the mean subscale scores for social-withdrawal, depressed, and somatic problems to be higher than the norms for the test, whereas the transplant patients had relatively low scores on the externalizing scales of aggressive and destructive behavior. Practically, transplant patients are, in many cases, unable to integrate with their peer group, and an additional number of them are prevented from doing so as a result of parental anxiety and overprotective behavior. This, combined with their physical condition, would suggest that patterns of behavior of social isolation and depression are to be anticipated, and indeed depressive symptomatology is recognized as a feature of the behavior of young children.57 An additional factor to consider is that the child’s mother completed the measure, and it is acknowledged that maternal mental health can influence her perception of her child’s behavior58–60 and that behavioral and emotional adjustment of children with CHD is related more to maternal perceptions than to disease severity or degree of functional limitation.61
Developmental delay in young children with chronic illness is multifactorial in origin, with a number of common factors across illness groups. However, there are also a number of disease-specific factors that differentiate those with CHD from those with CM and highlight the importance of considering diagnosis when discussing patients waiting for heart or heart-lung transplantation. Additional follow-up is now required to determine the impact, if any, of improved cardiac function as a result of transplantation on development and behavior, and to assess whether children with heart disease who show deficits in preschool years remain at risk for cognitive delay. The indications from posttransplant studies18,62,63 are that children who have undergone transplantation are at risk for developmental delay and behavioral difficulties. Risk factors for poor psychosocial outcome need to be identified, and prospective evaluation is needed to determine whether pretransplant functioning predicts posttransplant functioning. If it does, psychosocial interventions need to be targeted pretransplant to reduce posttransplant psychological morbidity, such as improved management of feeding problems, intensive developmental intervention, the facilitation of adaptive coping in parents, and strategies to reduce and improve the management of parental anxiety.
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FOOTNOTES |
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Reprint requests to (J.W.) Pediatric Surgical Unit, Harefield Hospital, Harefield, Middlesex UB9 6JH, United Kingdom. E-mail: j.wray{at}rbh.nthames.nhs.uk
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REFERENCES |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
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This article has been cited by other articles:
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  C. E. Canter, R. E. Shaddy, D. Bernstein, D. T. Hsu, M. R.K. Chrisant, J. K. Kirklin, K. R. Kanter, R. S.D. Higgins, E. D. Blume, D. N. Rosenthal, et al. Indications for Heart Transplantation in Pediatric Heart Disease: A Scientific Statement From the American Heart Association Council on Cardiovascular Disease in the Young; the Councils on Clinical Cardiology, Cardiovascular Nursing, and Cardiovascular Surgery and Anesthesia; and the Quality of Care and Outcomes Research Interdisciplinary Working Group Circulation, February 6, 2007; 115(5): 658 - 676. [Abstract] [Full Text] [PDF]
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