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Cohen Pediatrics 2013;131;e236; originally published online December 10, 2012; DOI: 10.1542/peds.2012-1157
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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2013 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.
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MD. For children in the SV. www. R3E 3P4. Canada. Department of Pediatrics. MDe aDepartment of Pediatrics and Child Health. including feeding difﬁculties. stratiﬁed by CHD category. and head circumference-for-age (HCFAZ) at traditional ages for preventive visits. MSCE. and head circumference. Pediatrics 2013. 2013 . The simultaneous decrease suggests a role for altered growth regulation in children with CHD. impaired growth as measured by weight. E-mail: cdaymont@mich. METHODS: We performed a retrospective matched cohort study. New Haven. analyzed the data. and head circumference occurs simultaneously rather than sequentially.a. length.Growth in Children With Congenital Heart Disease WHAT ’S KNOWN ON THIS SUBJECT: Children with congenital heart disease (CHD) are at increased risk for poor growth. Dr Prosnitz participated in the acquisition of data. dYale-New Haven Children’s Hospital. growth. and SR categories. Online. abstract OBJECTIVE: We sought to describe growth in young children with congenital heart disease (CHD) over time. critically revised the manuscript for important intellectual content. CR. MD. Ninth Revision IGF-1—Insulin-like growth factor 1 LFAZ—length-for-age z score NR—no repair R-C—repair-combined SR—simple repair SV—single ventricle WFLZ—weight-for-length z score WHO—World Health Organization WFAZ—weight-for-age z score Dr Daymont participated in the conception and design of the study. WHAT THIS STUDY ADDS: In children with CHD. identifying children with CHD in a large primary care network in Pennsylvania. critically revised the manuscript for important intellectual content. CONCLUSIONS: Children with CHD experience early. RESULTS: We evaluated 856 cases: 37 with single ventricle (SV) physiology. Philadelphia.pediatrics. Dr Neal participated in the acquisition of data. simultaneous decreases in growth trajectory across weight. Manitoba. increased caloric requirements. 0031-4005. cBoston Children’s Hospital. drafted the manuscript. 2012 Address correspondence to Carrie Daymont. MD MSCE. length-for-age (LFAZ). peaked near 4 months.b Ashley Neal. University of Manitoba. and approved the ﬁnal manuscript as submitted.aappublications. HC data were available between 1 week and 24 months. nutrition. 1098-4275). at those ages. and approved the ﬁnal manuscript as submitted. and SR groups. The primary endpoint was the difference in mean World Health Organization z score for cases and controls for weight-forage (WFAZ). and eDivision of Cardiology.131:e236–e242 e236 DAYMONT et al Downloaded from pediatrics.ca PEDIATRICS (ISSN Numbers: Print. Cohen.c Aaron Prosnitz. FUNDING: Dr Daymont’s time was supported by the Manitoba Health Research Council and The Manitoba Institute of Child Health. and approved the ﬁnal manuscript as submitted.2012-1157 Accepted for publication Aug 20. Winnipeg. and 608 requiring no repair. and statistically signiﬁcant (Student ’s t test P . simultaneous.d and Meryl S.2012-1157 doi:10. supporting the theory that altered growth regulation likely plays an important role in the poor growth of children with CHD. Winnipeg. Connecticut. Several factors may play a role in poor growth. and Delaware and matching them 10:1 with control subjects. weight-for-length (WFLZ). There were fewer and smaller decreases in the no-repair group between 2 and 18 months.1542/peds. large. CR. Massachusetts. contributed to the interpretation of results. . bThe Manitoba Institute of Child Health. AUTHORS: Carrie Daymont. The Perelman School of Medicine at the University of Pennsylvania. and approved the ﬁnal manuscript as submitted. critically revised the manuscript for important intellectual content. Winnipeg.org at Indonesia:AAP Sponsored on January 2. and the effects of cardiac lesions on growth regulation. decreases in mean HCFAZ generally paralleled decreases in WFAZ and LFAZ in the SV. Copyright © 2013 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no ﬁnancial relationships relevant to this article to disclose.org/cgi/doi/10. 159 requiring simple repair (SR). MD. 52 requiring complex repair (CR). failure to thrive ABBREVIATIONS CHD—congenital heart disease CR—complex repair HC—head circumference HCFAZ—head circumference-for-age z score ICD-9—International Classiﬁcation of Diseases. Canada. and persisted through 24 or 36 months. New Jersey. Canada. and Dr Cohen participated in the conception and design of the study. length. The Manitoba Institute of Child Health. The Children’s Hospital of Philadelphia.1542/peds.05) decreases in WFAZ and LFAZ appeared within the ﬁrst month of life. Boston. 655A-715 McDermot Ave. Pennsylvania KEY WORDS congenital heart disease.
and primary care site. deﬁned as Risk Adjustment for Congenital Heart Surgery 1 class 3 or higher. and before January 31. renal. 2009. neuromuscular. comparing the mean attained z score for cases and controls for each of the four CHD classes separately. gender. We used a 1-week range of ages for the 1. The records included data from 33 practices in urban.and 2-week visits.5–7 The timing of growth differences may provide insight into both the causes of poor growth and critical periods for possible intervention. length or height. and 18-month visits. and head circumference (HC) recorded before January 31. genetic.and 36-month visits. affecting ∼8 in 1000 children.org at Indonesia:AAP Sponsored on January 2. we evaluated growth at the ages of typical preventive visits. respiratory. Each chart was reviewed individually by at least 1 author to conﬁrm a true diagnosis of CHD. each case was matched to 10 control subjects in the primary care network database by year of birth (61 year).9 Cases were classiﬁed on the basis of indicated or planned repair at the last evaluable visit rather than whether repair had occurred at the time of the last evaluated visit. we sought to evaluate longitudinal growth in young children with CHD of variable severity compared with the growth of healthy peers. 2-.8 including “malignancy. We used electronic medical record data from a large primary care network. Growth status in these vulnerable children may be associated with neurodevelopmental outcomes in addition to adult height and weight. as has been shown in other populations. with International Classiﬁcation of Diseases. and the other age groups included visits at the ages at which children were most commonly seen for preventive visits in the network. New Jersey. a 2-week range for the 1-. Therefore. and a 2-month range for the 24.1 In addition to the management of the speciﬁc heart defect. Cases were categorized into 1 of 4 categories of CHD: single-ventricle (SV) physiology. Number 1. January 2013 e237 Downloaded from pediatrics. Attained growth z scores for each parameter (as well as weight-forlength were determined for the World Health Organization (WHO) 2006 growth standard by using data from the WHO Anthro macro. Some controls were excluded during analysis because of insufﬁcient growth measurements at the evaluated ages. 2013 . Measures All measurements for weight. values that were extreme but consistent with a subjects’ other growth parameters were included. Children born prematurely (before 37 weeks of gestation) and those with ICD-9 codes for noncardiac complex chronic conditions (as deﬁned by Feudtner et al. and semirural locations in Pennsylvania. 1 value per subject per age group was selected. 15-. years in the electronic record. practitioners are often challenged by issues related to the facilitation of normal growth and development in this population. suburban. poor oral-motor skills. and metabolic. immunodeﬁciency. When $1 value was available for a subject in an age group. 9-. Practices in the network started using the electronic record between August 2001 and June 2006.ARTICLE Congenital heart disease (CHD) is the most common congenital anomaly. 2-ventricle heart disease requiring complex repair (CR). and associated genetic and noncardiac disease. otherwise selection was random. were excluded from the analysis. Primary Analysis The ages at which growth data were available for each patient varied widely. Chart review was used to determine the age at repair. METHODS We performed a retrospective cohort study comparing attained growth in children with CHD to matched controls without CHD as well as published references. we were unable to evaluate each case’s growth compared with its own controls at each age. gastrointestinal. Visits designated as preventive visits were retained preferentially. and 4-month visits. Site group (urban versus all others) was used to match when there were insufﬁcient controls in a site. deﬁned as Risk Adjustment for Congenital Heart Surgery class 1 or 2. the physiologic impact of the primary cardiac defect. and other congenital anomalies”8). Instead. a 1-month range for the 6-. The analyses were limited to the ﬁrst 36 months of life because of the relative scarcity of measurements after that age. and Delaware.11–13 Evaluation of growth parameters in a different cohort from the same primary care network indicated that the distribution of growth parameters in this regional population was not welldescribed by the WHO growth curves or by the Centers of Disease Control growth reference. 2000. were obtained from the electronic medical record.15–17 To identify a population against which to compare growth. The birth age group consisted only of measurements on the ﬁrst day of life. 2-ventricle heart disease requiring simple repair (SR). Patient Selection We identiﬁed children born after January 1. Ninth Revision (ICD-9) codes for structural CHD who had been seen in a primary care practice and had at least 2 weight measurements before age 3 PEDIATRICS Volume 131.10 Growth parameters that were determined likely to be nonrepresentative of actual growth based on the deviation of the recorded value from inverse distance-weighted means of the subject’s growth parameters were excluded from analysis. and 2-ventricle heart disease requiring no repair (NR).aappublications.2–4 Risk factors for poor growth are multifactorial and may include the increased metabolic demands of congestive heart failure. race. Therefore. 2010. 12-.
length-for-age (LFAZ). Z scores using Centers for Disease Control growth curves were also signiﬁcantly different from zero at many ages.org at Indonesia:AAP Sponsored on January 2. results were almost identical to that of the primary analysis. We evaluated the statistical signiﬁcance of the differences by using the Student ’s t test with a threshold of P = . Mixed effects models were designed by using the “xtmixed” command in Stata 11. Ultimately. and SR groups were all lower than control z scores at birth. For children with CHD requiring repair. our primary analysis was performed as planned by using the difference between case and control mean WHO z scores at the various time points as the primary endpoint. 64 116 visits from 856 cases and 7674 controls were included in the primary analysis (Supplemental Table 3). weight-for-length (WFLZ). and 1. and HC-for-age (HCFAZ) between cases and controls in each group at each time point. the SV. Differences between CHD categories were evaluated by using logistic regression.5% of length. Characteristics of included cases are described in Table 1 with primary diagnostic categories in Table 2. This project was approved by the Institutional Review Board at the Children’s Hospital of Philadelphia.18 Therefore. e238 DAYMONT et al Downloaded from pediatrics. All available measurements. Cases with the ﬁrst or second repair done after 365 days of life were excluded from this analysis. the ICD-9 code had been used to indicate potential CHD that was not conﬁrmed with diagnostic testing. A sensitivity analysis was performed including interpolated data to replace excluded values. were included in this analysis. larger and statistically signiﬁcant RESULTS Identiﬁed Cases There were 1862 potential cases initially identiﬁed based on ICD-9 codes for CHD (Fig 1). For this analysis. were likely to be nonrepresentative of the subjects’ growth. 2013 . the greatest difference between cases and controls was seen near 4 months of age. Differences between CHD categories were evaluated by using linear regression. Statistical signiﬁcance of the difference between cases and controls was evaluated by using Fisher’s exact test with a threshold of P = .2% of HC measurements were excluded because they FIGURE 1 Flow sheet describing exclusion of ineligible cases.05) at many ages for all 4 growth parameters (Fig 2). The proportion of subjects with a z score #1. 0.aappublications. During data cleaning. . 2. but differences were relatively small and were statistically signiﬁcant (P . including those taken at ages not traditionallyassociated withpreventivevisits. All analyses were performed by using Stata 11. .88 (corresponding to the third percentile) was also compared for cases and controls. LFAZ.The primary endpoint was the difference in mean growth WHO z score for weight-for-age (WFAZ).2.2 to compare the change in slopes (Dz score/time in years) of WFAZ before and after a certain time point for cases and controls clustered at the level of subject nested within case group (a case and its matched controls). Exploratory Analysis of Age and Repair Status Across CHD severity and growth parameters. in most of these cases.8% of weight. LFAZ. Growth in Controls The means and SDs for WFAZ. WFA and LFA z scores for cases in the SV. and SR groups were analyzed together as the repair-combined (R-C) group to have sufﬁcient sample size.05) only for LFA in the SR group (Fig 2 and Fig 3). Comparison of Means At birth. Three hundred twenty potential cases were excluded because the subject did not have CHD.05.05. CR. We compared the change in WFAZ slopes before and after 4 months of age for cases and controls and then compared the change in WFAZ slopes before and after the age at the cases’ second surgery (or ﬁrst surgery if only 1 surgery was done). CR. An exploratory post hoc analysis was designed to compare the association of improvement in WFAZ with age and with repair status in the R-C group. and HCAZ for controls were signiﬁcantly different from zero (P .
At 2 months. and 20.1%) 367 (60%) 75 (12%) Because gender and race were used as matching criteria. the proportions are the same in controls as for cases. In the combined repair group. There were substantial differences between controls and cases requiring repair in length as well as weight. signiﬁcant increase in slopes (Dz score/time in years) for WHO weight z score before and after 4 months (b = 4. increasing z scores were. Differences in growth were smaller after 4 months of age but persisted through age 36 months. Exploratory Analysis of Age and Repair Status There were 25 973 visits from 180 cases and 1643 controls included in the following analyses. and 2. Comparison of Proportion Below the Third Percentile There was no difference in the proportion of cases and controls with growth parameters below the third percentile (z score #1.1. length. 21. 2. and 20. 21.1 was performed. 20.3 at 0.6 (SV). Among cases in the R-C group. but a substantial decrease in HCFAZ persisted for cases in the CR and SR groups. There was a large. Few HC measurements were available at birth and 36 months in the electronic record.5). the pattern of differences in HCFAZ between cases and controlswas generally similar to the pattern seen for weight and length with a few important exceptions. the odds ratios for the R-C group were 12. so only measurements between 1 week and 24 months were evaluated. 95% conﬁdence interval 1. and 9 months (HCFAZ). NA.ARTICLE TABLE 1 Characteristics of Cases Characteristic n (cases) n (controls) Median age (d) at ﬁrst repair Male Race Asian Black/African American Native American White Other SV 37 344 4 23 (62%) 0 (0%) 12 (32%) 0 (0%) 24 (65%) 1 (3%) CR 52 464 5 31 (60%) 2 (4%) 11 (21%) 0 (0%) 32 (62%) 7 (13%) SR 159 1377 126 85 (53%) 12 (8%) 43 (27%) 2 (1%) 92 (58%) 10 (6%) NR 608 5489 NA 260 (43%) 15 (2%) 150 (25%) 1 (.5 (CR). 20. 3. HC was measured less often than weight and length. TABLE 2 Diagnostic Categories of Cases with CHD by Repair Category CHD Diagnostic Categories SV CR SR NR Hypoplastic left heart 14 syndrome Tricuspid atresia 5 Unspeciﬁed single ventricle 13 abnormality Double-outlet right ventricle 1 4 Pulmonary valve abnormalities 4 2 13 84 Transposition of the great 21 arteries Truncus arteriosus 3 Atrioventricular canal 9 Coronary abnormalities 3 Tetralogy of Fallot 5 24 Total anomalous pulmonary 1 1 venous return Partial anomalous pulmonary 1 venous return Aortic abnormalities 1 19 Aortic valve abnormalities 3 6 75 Pulmonic artery abnormalities 2 2 Patent ductus arteriosus 23 24 Atrial septal defect (including 17 54 patent foramen ovale) Ventricular septal defect 40 360 Vascular ring 8 2 Mitral or tricuspid valve 6 abnormalities Other 5 1 Total 37 52 159 608 DISCUSSION Within weeks of birth. statistically signiﬁcant deﬁcits in weight. For WFAZ.4 at 4 months (SV).9 (WFAZ). not applicable.6 (SR). cases were signiﬁcantly more likely than controls to be less than the third percentile for all growth parameters starting at 1 month of age and persisting through 24 months (WFAZ).6 at 2 months (SR). differences in proportions for cases and controls were statistically signiﬁcant at fewer ages. temporally.org at Indonesia:AAP Sponsored on January 2.9 (HCFAZ) and for the NR group were 3. The median age at second repair (or ﬁrst if only 1 was performed) was 130 days (interquartile range 46–213). and HC trajectory compared with matched controls without CHD from the same PEDIATRICS Volume 131.aappublications.2.9). Between 2 weeks and 24 months. ex- cept WFAZ in the SR group. The decreases in mean WFAZ between cases in the NR group and matched controls were small compared with the decreases for children requiring repair but were signiﬁcant between 2 and 18 months. 36 months (LFAZ). children with CHD show large. 2013 . The difference in slopes before and after repair was smaller (b = 2.2 (NR). There was no difference in mean HCFAZ between cases and controls in the NR group.5 months (NR). January 2013 e239 Downloaded from pediatrics. In the NR group. The odds ratios for being less than the third percentile for cases versus controls were generally large in the postnatal period. Accordingly.3 at 2 months (CR). decreases in WFLZ were generally smaller than for WFAZ. Number 1.1 (LFAZ). Peak differences for LFAZ were 21. early.5 (HCFAZ).6–4. 4. differences appeared by 1 week of age. differences in the R-C group were signiﬁcantly larger than for the NR group at 1. 2. 95% conﬁdence interval 3. There were also no differences in HCFAZ between cases and controls in the SV group at 9 months and older.88) at birth in either the R-C or NR categories (Fig 4). 20. Even at those ages. and 6 months.1 (WFAZ).8 (LFAZ).7–2. This overall pattern of ﬁndings was robust to sensitivity analyses excluding data from the ﬁrst month after surgery and using the age at ﬁrst surgery rather than second surgery when . Peak differences for WFAZ occurred at 4 months of age in each category: 21. more strongly associated with age than with repair status.
and 0.aappublications. and HC in early infancy.8% of cases.org at Indonesia:AAP Sponsored on January 2. at 6 months of age. Statistically signiﬁcant differences (P . and the magnitude of differences in WFAZ at 1 year for cases in the CR and SR groups was similar to those described by Knirsch et al. and the conﬁrmation of diagnoses with chart review rather than reliance solely on billing codes. For example. the expected proportion of microcephaly would have been 3%. the relatively large sample size. which may be hemodynamically signiﬁcant early in life even if they later self-resolve.05 using Student ’s t test) are marked with a small plus. Extensive efforts were also made to identify e240 DAYMONT et al Downloaded from pediatrics. The largest differences in weight occurred at 4 months of age. .6 times as likely as controls to have microcephaly.20 A small increase in the risk of poor growth is seen even in the population of patients with CHD that does not require surgery (NR group). The strengths of our study include comparison of growth of cases with a control population rather than solely with published references. and it would have appeared that cases were only 1. Full catch-up growth was not seen by 36 months for children with CHD requiring repair. 5.19. Therefore. dramatically underestimating the difference between children with CHD and healthy children from the same population. The majority of subjects in this group had ventricular septal defects. The magnitude and timing of differences for WFAZ and LFAZ for cases in the SV group were similar to those published by Williams et al in 2011.9 times as likely as healthy children to have microcephaly.05) differences between case and control groups at $1 month.FIGURE 2 Means and 95% conﬁdence intervals at typical ages for preventive visits for WHO z scores for cases and controls. cases were 11. primary care network. Values for male and female subjects are combined by converting female z scores to the equivalent weight for male subjects and plotting on the male growth curve. 2013 . Analysis of cases using z scores without comparison with peers would have mischaracterized the differences between these children with CHD and healthy children. Means are plotted when data were available for at least 6 cases. If we had compared them only to the WHO standards.5% of controls in the C-R group had microcephaly (HC less than third percentile). . Children with CHD requiring repair were much more likely to be below the third percentile for weight. FIGURE 3 Median weight for cases requiring CR and matched controls plotted on WHO growth curve. All time points demonstrated statistically signiﬁcant (P . length.
decreased growth factors. and the study did not formally assess HC. lower case numbers for speciﬁc categories of disease complexity. LFAZ. We also did not have sufﬁcient information to determine whether some patients were cyanotic before repair. the increase in growth factors may be more directly related to the repair. early.27 Although the authors postulate that these increases are related to improved postoperative nutrition.26 These higher demands are often most profound in the ﬁrst 6 months of life as pulmonary vascular resistance decreases.6 and many have increased metabolic demands as a result of their cardiac defect. When caloric intake is inadequate to meet demands. in children with CHD.aappublications.3 It is important to determine whether this decrease in HC growth in children with CHD is conﬁrmed in other studies and whether it is modiﬁable by nutritional or other treatments. The limitations of our study include its reliance on a single network. an important anabolic hormone affecting childhood growth. the lack of HC data at birth and in the neonatal period. and the variability in timing of growth measurements. Rather. The R-C includes subjects from the SV. and sustained decreases in growth trajectory compared with their peers. is a signiﬁcant limitation to our study. In this population. particularly those who are cyanotic. and hormonal changes.2. length (LFA). Number 1. Review of 3 published studies evaluating HC at birth in children with CHD does not reveal a consistent answer. which often results in resolution of congestive heart failure with improved cardiovascular physiology. which likely has a large impact on growth. such as genetic abnormalities.05 using Fisher’s exact test) are marked with a small red plus. particularly in the SV and CR groups. Prospective evaluation will be crucial to conﬁrm this ﬁnding and to determine if it is related to diet. and SR categories. FIGURE 4 Proportion of controls versus cases below the third percentile for weight (WFA). January 2013 HC become apparent.10th percentile and neurodevelopmental outcomes among children with CHD. and HC (HCA) for age. However.org at Indonesia:AAP Sponsored on January 2. effects are generally seen in weight before length and ﬁnally HC. and HCFAZ. the sample size of 101 subjects may not have been sufﬁcient to identify an association if one were present.22–25 One previous study found no association between prerepair weight . erroneous values without eliminating values from subjects with growth at the extremes of the distribution.7.ARTICLE to other factors. or primarily mediated by growth factors or other physiologic changes. Statistically signiﬁcant differences (P . Dinleyici et al identiﬁed decreases in insulin-like growth factor 1 (IGF-1). CR. The lack of HC values at birth and our subsequent inability to determine more precisely the time point at which differences in PEDIATRICS Volume 131. However. decreased growth in children with CHD may also be related CONCLUSIONS Children with complex CHD have large. The simultaneous change in all 3 parameters seen in this analysis e241 Downloaded from pediatrics.21 Another recent study identiﬁed increases in IGF-1 and its carrier protein insulin-like growth factor binding protein-3 after surgical repair in children with acyanotic CHD.19 Children with CHD frequently have feeding difﬁculties. 2013 . our exploratory analysis of time at repair did not suggest a strong independent association between repair and growth velocity in the overall population.20 It is important to identify the etiology of poor growth in CHD in order to guide attempts to improve growth. This simultaneous change in trajectory supports the idea that impaired growth in children with CHD requiring repair is mediated at least in part by factors unrelated to nutrition. Inadequate caloric intake certainly plays a role in poor growth for at least some children with CHD.21 A postnatal decrease in HC growth velocity in children with CHD would indicate a restriction of brain growth during the critical developmental period of infancy and may have lifelong effects on neurodevelopment. . such as the addition of solid foods at ∼4 months of age. a consistent improvement of growth velocity at ∼4 months was seen. However. its retrospective nature. no lag was seen between the decreased growth trajectory for cases in WFAZ.
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