Developmental and Behavioral Status of Infants and Young Children Awaiting Heart or Heart-Lung Transplantation
* 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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Objective. Research into cognitive development and behavior in children undergoing heart or heart-lung transplantation has focused mainly on older children, with investigation of children undergoing transplantation as infants or toddlers being largely retrospective. This study was conducted, therefore, to obtain pretransplant baseline measures of development and behavior for preschool-aged children.
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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Institutional approval for the study was obtained from all the units taking part, and individual consent was obtained from the parents of each child.
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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Seventeen of the children in the transplant group had CHD; the remaining 18 had CM. There were 21 girls and 14 boys. Mean age at assessment was 1.5 years (range: 0.1–3.4 years). The mean ages of the CHD and CM samples did not differ significantly (CHD mean: 1.8 years; CM mean: 1.3 years) and neither did the gender distribution (CHD: 10 girls [59%]; CM: 11 girls [61%]). The 9 children who were too ill to be developmentally assessed, of whom 6 had CHD and 3 had CM, did not differ in age or gender distribution from those children who underwent developmental testing. However, a greater proportion of these children died before transplant (n = 3 [33%[) compared with those who were able to undergo testing, 6 (23%) of whom died on the waiting list. The majority of patients in the transplant group were waiting for an orthotopic heart transplant (n = 30), with 4 on the waiting list for heart-lung transplantation and 1 waiting for a heterotopic heart transplant. The conventional heart surgery group comprised 25 children, 11 of whom had cyanotic heart disease and 14 of whom had acyanotic heart disease. The 15 children in the BMT group had either metabolic or acquired diseases for which BMT was the treatment of choice. One child in each of the conventional heart surgery and BMT groups was too ill to undergo developmental testing.
Characteristics of the 4 groups of children are given in Table 1.
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Parental Interview
Thirteen (37%) of the transplant patients required admission to a special care infant unit after birth, which was not significantly different than the prevalence in the conventional cardiac surgery group (40%) but was higher than seen in the BMT and healthy groups (7% in each group). Children with CHD had been diagnosed for significantly longer than those with CM (t = 3.73; 95% confidence interval [CI]: 0.61–2.27; P < .005), and a greater proportion with CHD had been admitted to a special care infant unit after birth (
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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Differences Within the Transplant Group
Patients with CHD had a significantly lower mean DQ than those with CM and obtained significantly lower scores than those with CM in all areas of development with the exception of personal/social skills (Table 4). All 3 children who had overall DQ scores of
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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The children who were waiting for a heart-lung transplant obtained lower sores on all the developmental parameters than those on the waiting list for a heart transplant, with these differences reaching significance on the overall DQ (t = 2.38; 95% CI: 3.75–52.17; P < .05).
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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Information from the parental interview indicated that the 2 main behavioral concerns that parents had in all 3 illness groups were dependency and inactivity. Within the transplant group, 13 (37%) children were considered by their parents to have "behavior problems." (This information was not available for the other 3 groups.)
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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Our study provides previously unavailable information on the developmental functioning and behavior of a group of children waiting for a heart or heart-lung transplant. The inclusion of 3 comparison groups is an additional strength of the study and allowed for some discrimination between the effects of chronic illness in general and heart disease in particular. Furthermore, inclusion of children with both CHD or CM permitted a more detailed analysis of the impact of heart disease of differing etiology on development. There are also limitations that must be borne in mind when interpreting the results. In particular, the sample is relatively small, especially when considering comparisons between the CHD and CM cohorts within the transplant group, and the findings therefore might be liable to type II statistical errors. Although every effort was made to recruit all patients consecutively accepted onto the waiting list, for practical reasons this was not completely successful. The most significant reason for nonrecruitment was the poor physical condition of the patient, thus there is a selection bias in the sample that was finally recruited. This was unavoidable but has implications for the application of our results across the total population on the waiting list for transplant.
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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Received for publication Dec 12, 2002; Accepted Jun 6, 2003.
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 |
|---|
|
TOPABSTRACTMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
- Eiser C. Psychological sequelae of brain tumours in childhood: a retrospective study. Br J Clin Psychol.1981; 20 :35 –38[Web of Science][Medline]
- So SKS, Chang PN, Najarian JS, Mauer SM, Simmons RL, Nevins TE. Growth and development in infants after renal transplantation. J Pediatr.1987; 110 :343 –350[CrossRef][Web of Science][Medline]
- Stewart SM, Uauy R, Waller DA, Kennard BD, Andrews WS. Mental and motor development correlates in patients with end-stage biliary atresia awaiting liver transplantation.
Pediatrics.1987; 79
:882
–888
[Abstract/Free Full Text] - Davis ID, Chang P, Nevins TE. Successful renal transplantation accelerates development in young uremic children.
Pediatrics.1990; 86
:594
–600
[Abstract/Free Full Text] - Wayman KI, Cox KL, Esquivel CO. Neurodevelopmental outcome of young children with extrahepatic biliary atresia 1 year after liver transplantation. J Pediatr.1997; 131 :894 –898[CrossRef][Web of Science][Medline]
- Polinsky MS, Kaiser BA, Stover JB, Frankenfield M, Baluarte HJ. Neurologic development of children with severe chronic renal failure from infancy. Pediatr Nephrol.1987; 1 :157 –165[CrossRef][Web of Science][Medline]
- Gonzalez-Pardo L, Miles M, Taylor M, Mattioli L. Congenital heart disease: developmental and neurological evaluation in preschool children. J Kans Med Soc.1981; 82 :115 –118[Medline]
- O’Dougherty M, Wright FS, Garmezy N, Loewenson RB, Torres F. Later competence and adaptation in infants who survive severe heart defects. Child Dev.1983; 54 :1129 –1142[Web of Science][Medline]
- Newburger JW, Silbert AR, Buckley LP, Fyler DC. Cognitive function and age at repair of transposition of the great arteries in children. N Engl J Med.1984; 310 :1495 –1499[Abstract]
- Aram DM, Ekelman BL, Ben-Shachar G, Levinsohn MW. Intelligence and hypoxemia in children with congenital heart disease: fact or artifact? J Am Coll Cardiol.1985; 6 :889 –893[Abstract]
- DeMaso DR, Beardslee WR, Silbert AR, Fyler DC. Psychological functioning in children with cyanotic heart defects. J Dev Behav Pediatr.1990; 11 :289 –294[Web of Science][Medline]
- Stieh J, Kramer HH, Harding P, Fischer G. Gross and fine motor development is impaired in children with cyanotic congenital heart disease. Neuropediatrics.1999; 30 :77 –82[Web of Science][Medline]
- Samango-Sprouse C, Suddaby EC. Developmental concerns in children with congenital heart disease. Curr Opin Cardiol.1997; 12 :91 –98[Web of Science][Medline]
- Aisenberg RB, Rosenthal A, Nadas AS, Wolff PH. Developmental delay in infants with congenital heart disease-correlation with hypoxemia and congestive heart failure. Pediatr Cardiol.1982; 3 :133 –137[Web of Science][Medline]
- Limperopoulos C, Majnemer A, Shevell MI, Rosenblatt B, Roblicek C, Tchervenkov C. Neurodevelopmental status of newborns and infants with congenital heart defects before and after open heart surgery. J Pediatr.2000; 137 :638 –645[CrossRef][Web of Science][Medline]
- Dees E, Lin H, Cotton RB, Graham TP, Dodd DA. Outcome of preterm infants with congenital heart disease. J Pediatr.2000; 137 :653 –659[CrossRef][Web of Science][Medline]
- Baum M, Chinnock R, Ashwal S, Peverini R, Trimm F, Bailey L. Growth and neurodevelopmental outcome of infants undergoing heart transplantation. J Heart Lung Transplant.1993; 12 :S211 –S217[Web of Science][Medline]
- Baum M, Freier C, Freeman KR, Chinnock RE. Developmental outcomes and cognitive functioning in infant and child heart transplant recipients. Prog Pediatr Cardiol.2000; 11 :159 –163[CrossRef][Web of Science][Medline]
- Fleisher BE, Baum D, Brudos G, et al. Infant heart transplantation at Stanford: growth and neurodevelopmental outcome.
Pediatrics.2002; 109
:1
–7
[Abstract/Free Full Text] - Wray J, Sensky T. Controlled study of preschool development after surgery for congenital heart disease.
Arch Dis Child.1999; 80
:511
–516
[Abstract/Free Full Text] - Pot-Mees C. The Psychosocial Effects of Bone Marrow Transplantation in Children. Delft, The Netherlands: Eburon Delft; 1989
- Griffiths R. The Abilities of Babies: A Study in Mental Measurement. Thetford, United Kingdom: Lowe & Brydone Ltd; 1954
- Griffiths R. The Abilities of Young Children: A Comprehensive System of Mental Measurement for the First Eight Years of Life. London, United Kingdom: Child Development Research Centre; 1970
- Rasof B, Linde LM, Dunn OJ. Intellectual development in children with congenital heart disease. Child Dev.1967; 38 :1043 –1053[CrossRef][Web of Science][Medline]
- Aldridge Smith J, Bidder RT, Gardner SM, Gray OP. Griffiths Scales of Mental Development and different users. Child Care Health Dev.1980; 6 :11 –16[CrossRef][Web of Science][Medline]
- Hanson R, Aldridge-Smith J, Hume W. Achievements of infants on items of the Griffiths Scales: 1980 compared with 1950. Child Care Health Dev.1985; 11 :91 –104[CrossRef][Web of Science][Medline]
- Tyler B, Miller K. The use of tests by psychologists: report on a survey of BPS members. Bull Br Psychol Soc.1986; 39 :405 –410[Web of Science]
- Bidder RT, Bryant G, Gray OP. Benefits to Down’s syndrome children through training their mothers.
Arch Dis Child.1975; 50
:383
–386
[Abstract/Free Full Text] - Balestrini MR, Zanette M, Micheli R, Fornari M, Solero CL, Broggi G. Hemispheric cerebral tumors in children. Long-term prognosis concerning survival rate and quality of life–considerations on a series of 64 cases operated upon. Childs Nerv Syst.1990; 6 :143 –147[CrossRef][Web of Science][Medline]
- Ludman L, Spitz L, Lansdown R. Intellectual development at 3 years of age of children who underwent major neonatal surgery. J Pediatr Surg.1993; 28 :130 –134[CrossRef][Web of Science][Medline]
- Van Mourik ID, Beath SV, Brook GA, Cash AJ, Mayer AD, Buckels JA, Kelly DA. Long-term nutritional and neurodevelopmental outcome of liver transplantation in infants aged less than 12 months. J Pediatr Gastroenterol Nutr.200; 30 :269 –275
- Achenbach TM, Edelbrock C, Howell CT. Empirically based assessment of the behavioral/emotional problems of 2- and 3- year-old children. J Abnorm Child Psychol.1987; 15 :629 –650[CrossRef][Web of Science][Medline]
- Utens EMWJ, Versluis-Den Bieman HJ, Witsenburg M, Bogers AJJC, Verhulst FC, Hess J. Cognitive and behavioural and emotional functioning of young children awaiting elective cardiac surgery or catheter intervention. Cardiol Young.2001; 11 :153 –160[Web of Science][Medline]
- Bellinger DC, Wypij D, du Plessis AJ, et al. Developmental and neurologic effects of alpha-stat versus Ph-stat strategies for deep hypothermic cardiopulmonary bypass in infants. J Thorac Cardiovasc Surg.2001; 121 :374 –383
- Bellinger DC, Wernovsky G, Rappaport LA, et al. Cognitive development of children following early repair of transposition of the great arteries using deep hypothermic circulatory arrest.
Pediatrics.1991; 87
:701
–701
[Abstract/Free Full Text] - O’Dougherty M, Wright FS, Loewenson RB, Torres F. Cerebral dysfunction after chronic hypoxia in children.
Neurology.1985; 35
:42
–46
[Abstract/Free Full Text] - Smedler A-C, Bolme P. Neuropsychological deficits in very young bone marrow transplant recipients. Acta Paediatr.1995; 84 :429 –433[Web of Science][Medline]
- Stein REK, Jessop DJ. A noncategorical approach to chronic childhood illness. Public Health Rep.1982; 97 :354 –362[Web of Science][Medline]
- Vernon DTA, Schulman JL, Foley JM. Changes in children’s behavior after hospitalization. Some dimensions of response and their correlates.
Am J Dis Child.1966; 111
:581
–593
[Abstract/Free Full Text] - Goslin ER. Hospitalization as a life crisis for the preschool child: a critical review. J Community Health.1978; 3 :321 –346[CrossRef][Medline]
- Stein A, Barnes J. Feeding and sleeping disorder. In: Rutter M, Taylor E, eds. Child and Adolescent Psychiatry: Modern Approaches. Fourth ed. Oxford, United Kingdom: Blackwell Scientific Publications; 2002
- Jenkins S, Owen C, Bax M, Hart H. Continuities of common behavior problems in preschool children. J Child Psychol Psychiatry.1984; 25 :75 –89[Web of Science][Medline]
- Clemente C, Barnes J, Shinebourne E, Stein A. Are infant behavioural feeding difficulties associated with congenital heart disease? Child Care Health Dev.2001; 27 :47 –59[CrossRef][Web of Science][Medline]
- Gudermuth S. Mothers’ reports of early experiences of infants with congenital heart disease. Matern Child Nurs J.1975; 4 :155 –164[Medline]
- D’Antonio IJ. Mothers’ responses to the functioning and behavior of cardiac children in child-rearing situations. Matern Child Nurs J.1976; 5 :206 –259
- Wray J, Sensky T. How does the intervention of cardiac surgery affect the self-perception of children with congenital heart disease? Child Care Health Dev.1998; 24 :57 –72[CrossRef][Web of Science][Medline]
- Cohn JK. An empirical study of parents’ reaction to the diagnosis of congenital heart disease in infants. Soc Work Health Care.1996; 23 :67 –79
- Menahem S. Counselling strategies for parents of infants with congenital heart disease. Cardiol Young.1998; 8 :400 –407[Web of Science][Medline]
- Linde LM, Rasof B, Dunn OJ, Rabb E. Attitudinal factors in congenital heart disease.
Pediatrics.1966; 38
:92
–101
[Abstract/Free Full Text] - Offord DR, Cross LA, Andrews EJ, Aponte JF. Perceived and actual severity of congenital heart disease and effect on family life.
Psychosomatics.1972; 13
:390
–396
[Free Full Text] - Lobo ML. Parent-infant interaction during feeding when the infant has congenital heart disease. J Pediatr Nurs.1992; 7 :97 –105[Medline]
- Hovels-Gurich HH, Seghaye M-C, 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; 114
:578
–585
[Abstract/Free Full Text] - Bellinger DC, Jonas RA, Rappaport LA, et al. Developmental and neurological status of children after heart surgery with hypothermic circulatory arrest or low-flow cardiopulmonary bypass.
New Engl J Med.1995; 332
:549
–555
[Abstract/Free Full Text] - Gomelsky A, Holden EW, Ellerbeck KA, Brenner JI. Predictors of developmental outcomes in children with complete transposition. Cardiol Young.1998; 8 :352 –357[Web of Science][Medline]
- Oates RK, Turnbull JAB, Simpson JM, Cartmill TB. Parent and teacher perceptions of child behaviour following cardiac surgery. Acta Paediatr.1994; 83 :1303 –1307[Web of Science][Medline]
- Utens EMWJ, Verhulst FC, Meijboom FJ, et al. Behavioural and emotional problems in children and adolescents with congenital heart disease. Psychol Med.1993; 23 :415 –424[Web of Science][Medline]
- Graham P. Child Psychiatry: A Developmental Approach. Oxford, United Kingdom: Oxford University Press; 1986
- Angold A, Weissman MM, John K, et al. Parent and child reports of depressive symptoms in children at low and high risk of depression. J Child Psychol Psychiatry.1987; 28 :901 –915[Web of Science][Medline]
- Mulhern RK, Fairclough DL, Smith B, Douglas SM. Maternal depression, assessment methods and physical symptoms affect estimates of depressive symptomatology among children with cancer.
J Pediatr Psychol.1992; 17
:313
–326
[Abstract/Free Full Text] - Webster-Stratton C. Stress: a potential description of parent perceptions and family interactions. J Clin Child Psychol.1990; 19 :302 –312[CrossRef][Web of Science]
- DeMaso DR, Campis LK, Wypij D, Bertram S, Lipshitz M, Freed M. The impact of maternal perceptions and medical severity on the adjustment of children with congenital heart disease.
J Pediatr Psychol.1991; 16
:137
–149
[Abstract/Free Full Text] - Wray J, Pot-Mees C, Zeitlin H, Radley-Smith R, Yacoub M. Cognitive function and behavioural status in paediatric heart and heart-lung transplant recipients: the Harefield experience.
BMJ.1994; 309
:837
–841
[Abstract/Free Full Text] - Suddaby EC, Samango-Sprouse C, Vaught DR, Custer DA. Neurodevelopmental outcome of infant cardiac recipients. J Transplant Coordination.1996; 6 :9 –13
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