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Obesity Is a Common Comorbidity in Children With Congenital and Acquired Heart Disease Nelangi M. Pinto, Bradley S.

Marino, Gil Wernovsky, Sarah D. de Ferranti, Amy Z. Walsh, Meena Laronde, Kristen Hyland, Stanley O. Dunn, Jr and Meryl S. Cohen Pediatrics 2007;120;e1157 DOI: 10.1542/peds.2007-0306

The online version of this article, along with updated information and services, is located on the World Wide Web at:
http://pediatrics.aappublications.org/content/120/5/e1157.full.html

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 2007 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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ARTICLE

Obesity Is a Common Comorbidity in Children With Congenital and Acquired Heart Disease
Nelangi M. Pinto, MDa, Bradley S. Marino, MD, MPP, MSCEa, Gil Wernovsky, MDa, Sarah D. de Ferranti, MD, MPHb, Amy Z. Walsh, RNb, Meena Laronde, RNb, Kristen Hyland, BAa, Stanley O. Dunn, Jr, BAa, Meryl S. Cohen, MDa
aDivision of Cardiology, Department of Pediatrics, Childrens Hospital of Philadelphia, Philadelphia, Pennsylvania; bDepartment of Cardiology, Childrens Hospital Boston, Boston, Massachusetts

The authors have indicated they have no nancial relationships relevant to this article to disclose.

ABSTRACT
OBJECTIVES. Obesity may pose additional cardiovascular risk to children with acquired and congenital heart disease. Many children with heart disease are sedentary as a result of physician-, parent-, and/or self-imposed restrictions. The aim of this study was to evaluate the impact of the epidemic of obesity on children with heart disease. PATIENTS AND METHODS. A cross-sectional review was performed of children evaluated

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Key Words obesity, pediatric, congenital heart disease, BMI Abbreviations NHANESNational Health and Nutrition Examination Survey CHOPChildrens Hospital of Philadelphia CHBChildrens Hospital Boston EP electrophysiology
Accepted for publication Apr 16, 2007 Address correspondence to Meryl S. Cohen, MD, Division of Cardiology, Childrens Hospital of Philadelphia, 2nd Floor, Main Building, 34th Street and Civic Center Boulevard, Philadelphia, PA 19104. E-mail: cohenm@ email.chop.edu PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright 2007 by the American Academy of Pediatrics

in 2004 at 2 cardiology outpatient clinics. Differences in the prevalence of obese (BMI 95%) and overweight (BMI 85%95%) children were compared with national data and healthy control subjects. Dictated letters were reviewed to determine whether obesity was discussed with referring practitioners.
RESULTS. Of 2921 patients assessed, 1523 had heart disease. Diagnostic subgroups

included mild heart disease (n 401), arrhythmia (n 447), biventricular repair (n 511), univentricular palliation (Fontan; n 108), and heart transplantation (n 56). More than 25% of the patients with heart disease were obese or overweight; the prevalence of obese and overweight children was signicantly lower only in the Fontan group (15.9%). Pediatric cardiologists failed to document obesity or weight counseling in the majority of clinic letters.
CONCLUSIONS. Obesity is common in children with congenital and acquired heart disease. Pediatric cardiologists demonstrate inadequate communication regarding this problem to referring practitioners. Healthy-lifestyle counseling and routine exercise in children with heart disease may be underemphasized.

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the last half century. The most recent data published by the Center for Disease Controls serial National Health and Nutrition Examination Survey (NHANES) indicates a 45% increase in the prevalence of obese children in the past decade.1 Childhood obesity has been shown to be a signicant predictor of obesity in adulthood.2,3 Furthermore, childhood obesity is associated with systemic hypertension, type 2 diabetes, and endothelial dysfunction and is an independent predictor of coronary artery disease and premature death in adults.47 Obese adolescents exhibit changes in left ventricular mass related to an increased cardiac workload.8 Even with normal ventricular mass, overweight children exhibit subtle changes in diastolic function that may have implications for their future cardiovascular health.9 The impact of obesity on long-term cardiovascular health may be particularly important to children with preexisting congenital or acquired heart disease. Although much emphasis is placed on preventive medicine in adult cardiology, it is not often a focus of the pediatric cardiology outpatient visit despite recent guidelines on protecting future cardiovascular health in childhood.10 Children with congenital heart disease may have unique risk factors that contribute to the development of obesity. Children with certain types of heart disease may be at risk for failure to thrive in early infancy. Thus, practitioners have historically focused on encouraging weight gain, particularly in early childhood, when longterm eating habits begin to develop. Moreover, children with some forms of heart disease are commonly cautioned against certain types of physical activity. Recently, it has been shown that formal activity restriction in children with heart disease may be a predictor of the development of obesity.11 Very limited data exist about the prevalence of obesity in children with congenital and acquired heart disease. Because survival is now expected into adulthood for many of these patients,12 identifying the degree to which this additional cardiovascular risk factor exists within this population is likely to have important implications for long-term outcomes. The purpose of this study was to estimate the prevalence of obesity and overweight in children with heart disease, to assess the impact of obesity on systolic blood pressure measurement in this population, and to determine whether weight counseling was documented in referral correspondence to primary care physicians. PATIENTS AND METHODS Charts from outpatient cardiology clinic visits at 2 centers, Childrens Hospital of Philadelphia (CHOP) and Childrens Hospital Boston (CHB), for the calendar year 2004 were reviewed. All of the patients aged 6 to 19 years at the time of their visit were candidates for inclusion (the same age group highlighted by the National
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HILDHOOD OBESITY HAS increased dramatically in

Center for Health Statistics from the 1999 2002 NHANES).2 Exclusion criteria included factors independently associated with obesity or failure to thrive, such as a known genetic syndrome, mechanical support (such as a tracheostomy or gastrostomy tube), a diagnosis of protein-losing enteropathy, or referral specically for hyperlipidemia or obesity. Systematic selection of patients was achieved by sampling every third patient by date of visit at CHOP and by sampling every third patient by alphabetized last name at CHB. Patients with multiple visits during the year had only their most recent clinic visit included. Cardiology outpatient letters are the equivalent of clinic notes at CHOP and CHB. Data collected from cardiology outpatient letters included gender, age at visit, weight, height, heart rate, blood pressure, primary cardiac diagnosis, type of surgical or catheter intervention if performed, and documentation of discussion of weight. Documented blood pressure data were 1-time measurements obtained with either a Dinamap automated blood pressure monitor or by manual sphygmomanometer at the time of the clinic visit. Patients were grouped into 5 diagnostic heart disease categories: (1) mild heart disease that has not been treated with either surgical or catheter intervention (eg, mild valvar disease, hemodynamically insignicant septal defects, or Kawasakis disease); (2) primary rhythm disturbances in patients with structurally normal hearts (electrophysiology [EP]); (3) congenital heart disease with surgical and/or catheterdirected intervention culminating in a biventricular circulation (biventricular repair); (4) complex congenital heart disease (typically a univentricular heart) resulting in Fontan palliation (Fontan); and (5) cardiac transplantation. Clinic control subjects were healthy patients referred to the 2 outpatient clinics and discharged with a diagnosis of no heart disease (eg, chest pain, palpitations, or functional murmurs). BMI was calculated from weight and height data and then plotted on Centers for Disease Control and Prevention BMI curves to determine age- and gender-appropriate percentiles. For the purposes of this study, obese was dened as BMI 95th percentile and overweight was dened as BMI in the 85th to 95th percentile.13 Blood pressure measurements were similarly converted to percentiles that were standardized for age, gender, and height.14 Statistical Analysis Descriptive data were expressed as means with SDs (normally distributed continuous variables), as medians and ranges (nonnormally distributed continuous data), or as proportions (categorical and dichotomous variables). Continuous variables were evaluated for central tendency and variability with the Shapiro-Francia test. Systolic blood pressure percentiles were graphed by boxand-whisker plots. Diastolic blood pressure data were

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not analyzed, because they are inherently unreliable by automated measurement. The Wilcoxon rank-sum test was used to compare differences in age and BMI between control subjects and patients with heart disease. Fishers exact test was used to compare dichotomous variables, including gender, the presence of obesity and heart disease, diagnostic categories, and documentation of weight counseling. The Wilcoxon rank-sum test was also used to determine whether there was any difference in age or blood pressure percentile based on overweight category. Obesity and overweight proportions for the total cohort, each center, the heart disease group, and individual diagnostic categories were obtained from contingency tables. The prevalence of obesity and overweight were compared against the Centers for Disease Control and Prevention NHANES control data,1 cohort patients without heart disease who were treated as internal control subjects, and between the 2 centers using the 2-sample test of binomial proportions. This test was also used to compare weight counseling between centers. RESULTS After selection, 2921 patients met criteria for this study. Study population characteristics are described in Table 1. There was no difference in age or gender between the clinic control subjects and patients with heart disease. Table 2 describes the breakdown of patients at each center. Patients without heart disease (clinic control subjects: n 1398 [47.9%]) made up the largest percentage of the study population, both in total and at each center. A signicantly higher percentage of patients with mild heart disease and biventricular repair were selected from CHB, whereas more EP patients were selected from CHOP. Table 3 describes patients with heart disease from both centers. There was no difference in age between the patients with heart disease who were obese and overweight and those with a normal BMI. The overall prevalence of obesity in the total cohort was 15.2%, and combined obesity and overweight was 29.1%. This was not different from the Centers for Disease Control and Prevention NHANES national prevalence data for children aged 6 to 19 years of 16% obese and 31% either obese or overweight (Fig 1A).1 Healthy patients without heart disease (clinic control subjects) were no different in their prevalence of obesity and

TABLE 2 Clinic Population According to Diagnostic Category


Category (N Control patients Mild heart disease EP Biventricular repair Fontan Transplant
aP

All 2921), % 47.9 13.7 15.3 17.5 3.7 1.9

(n

CHOP 1620), % 48.6 12.6 19.2 14.3 3.3 2.0

(n

CHB 1301), % 46.9 15.9 10.5 21.5 4.1 1.8

Pa

.37 .05 .001 .001 .32 .89

values are comparisons between CHOP and CHB.

overweight than those in the NHANES population, suggesting that the 2 outpatient control populations were representative of these national data. Patients with any type of heart disease (combined assessment of mild heart disease, biventricular repair, Fontan, EP, and transplant groups) had a lower prevalence of obese (13.8%) and combined obese and overweight patients (26.2%) than the healthy clinic controls (P .032 and P .001, respectively). When patients with heart disease were divided into diagnostic categories, transplant, EP, and mild heart disease groups had a similar prevalence of obesity and overweight as the healthy control population (Fig 1B). Patients with palliated congenital heart disease, both biventricular repair and Fontan, had a lower prevalence of obesity and overweight (Fig 1B). Although the prevalence was statistically lower than in the healthy control patients, 23.9% of patients with a biventricular repair and 15.9% of Fontan patients were obese or overweight. Healthy control patients from CHB had a statistically lower prevalence of obesity than those seen at CHOP, but the prevalence of obesity in children with heart disease was similar at both centers. In addition, there was no difference in the prevalence of overweight between the centers in either the healthy control or heart disease patients. Figure 2 compares the systolic blood pressure percentiles for normal weight, overweight, and obese patients (unadjusted for medication use). For those with any form of heart disease, the systolic blood pressure percentile was signicantly higher in the obese and overweight groups compared with those with normal BMI (P .001). This trend was also shown in the healthy clinic control subjects. Discussion of weight, as documented by clinic letters,

TABLE 1 Study-Cohort Characteristics


Characteristic (N Male gender, % Age, median (range), y BMI percentile, median (range) All 2921) Clinic Control Subjects (n 1398) 53.4 13.0 (6.019.0) 69.2 (0.399.8) Patients With HD (n 1523) 56.5 12.0 (6.019.0) 61.8 (0.399.9) Pa .09 .12 .001

55.1 13.0 (6.019.0) 65.5 (0.399.5)

HD indicates heart disease. a P values are 2-sided for comparisons between control subjects and patients with heart disease.

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TABLE 3 Selected Variables According to BMI Category for Patients With Heart Disease
Characteristic Age, median (range), y Systolic BP, median (range), % Normal BMI 12.0 (6.019.0) 62.10 (0.04100.00) Overweight 13.0 (6.019.0) 75.70 (0.0699.90) Obese 11.0 (6.019.0) 79.90 (0.95100.00) Pa .90/.26 .001b

BP indicates blood pressure a P values are 2-sided, normal versus overweight/normal versus obese. b The P value is the same for both comparisons.

FIGURE 1 Prevalence of obesity and overweight. A, Prevalence of national data (from NHANES 1999 2002) compared with the clinic cohort and patients with heart disease (HD). The heart-disease group includes all patients who had mild heart disease, EP, biventricular repair (2V), univentricular palliation, and transplant (see text for details). a P .03 when compared with control patients. B, Prevalence of national data and clinic controls against categories of heart disease. b P .01 for comparisons with national data and controls. The P values not given were all not signicant.

occurred in only 13.3% of obese patients and 8.7% of overweight patients who were followed for acquired and congenital heart disease. There was no statistically signicant difference between the frequency of documented weight discussion between CHOP and CHB. DISCUSSION Similar to the alarming trend of obesity in otherwise healthy children, our study shows that there is a disturbingly high prevalence of obesity and overweight in children with the additional risk factors of congenital or acquired heart disease. More than one quarter of children with heart disease are obese or overweight.
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The impact of obesity on other pediatric patient populations with chronic diseases, such as cystic brosis, end-stage renal disease, and acute myeloid leukemia, has been reported previously.1517 To our knowledge, there are no previous large studies that look at the scope of obesity in pediatric patients with heart disease from multiple geographic regions. The current study, including 1500 patients with acquired or congenital heart disease, allowed for comparison among different categories of pediatric heart disease. The prevalence rates of obesity were similar across all of these groups, with the exception of patients with the most complex heart disease who have undergone the Fontan procedure. This is

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A
100

80

SBP p ercentile
FIGURE 2 Systolic blood pressure (SBP) percentiles according to BMI class. A, For patients with heart disease, systolic blood pressure percentile was increasingly higher in obese and overweight patients when compared with those with normal BMI. B, This difference was also seen in clinic controls. These gures were unadjusted for medication use. P .001 for each comparison of overweight and obese against normal-BMI patients.

60

40

20

Normal

Overweight

Obese

BMI class

B
100

80

SBP p ercentile

60

40

20

Normal

Overweight

Obese

BMI class

not surprising, because patients with univentricular hearts often have chronic, long-term issues, including heart failure and failure to thrive.18 Although the health risks associated with obesity in the general pediatric population are well established,19,20 the truly long-term outcomes for pediatric patients with heart disease await longer follow-up. Life span for children with congenital heart disease is less than normal.21,22 Congenital and acquired coronary disease and underlying vascular abnormalities in childhood are likely to be exacerbated by obesity, which is independently associated with endothelial dysfunction and hy-

pertension.20,23 In particular, certain populations, such as those with congenital abnormalities of coronary blood ow,24,25 acquired abnormalities, such as graft vasculopathy after cardiac transplantation26 or Kawasaki disease,27 or those who have had surgical manipulation of the coronary arteries (eg, the arterial switch or Ross operations),28,29 have been shown to have abnormalities in coronary function in later childhood and may be at increased risk for atherosclerosis as adults. This risk may also be exacerbated in children with previous repair of coarctation of the aorta where impairment of endothelial function and increased carotid intimal thickness have
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been identied.30 Although the long-term impact of superimposed obesity on congenital and acquired heart disease remains unknown, it is likely to increase morbidity and mortality as it does in adults with heart disease.31,32 Previous studies have detailed relationships among blood pressure, hypertension, and obesity.23 A recent study of a primary pediatric outpatient population found that obese and overweight children had higher systolic and diastolic blood pressures than normal-weight patients.33 Our study found that obese and overweight patients with heart disease were signicantly more likely to have increased systolic blood pressure percentiles during 1-time measurement in the outpatient setting. Although this study was not designed to evaluate hypertension in this population, the trend toward higher blood pressure in obese patients raises concern. In children with congenital heart disease, hypertension may not only impact their long-term cardiovascular health but may also have more immediate implications for their underlying disease (such as valvar and ventricular dysfunction). Given the severity of univentricular heart disease, obesity and overweight (in 15.9% of the Fontan group) in this high-risk population are likely to have a negative impact secondary to the risks associated with increased afterload and ventricular mass. Despite a signicant proportion of children who are obese and overweight in both outpatient practices, cardiovascular practitioners at both centers failed to document obesity and/or weight counseling in 85% of these patients with heart disease. Although it is unknown whether such a discussion took place during the visit itself, lack of documentation to the referring physician in the clinic letter and/or note suggests that communication regarding the problem of obesity in association with heart disease did not occur with the primary practitioner. As specialists, pediatric cardiologists tend to focus their clinic visit on the primary reason for referral. In addition, they may believe that their patients and parents will not be receptive to weight counseling at their heart clinic visit. Pediatric cardiologists have historically focused on adequacy of repair and/or progression of congenital or acquired heart disease. As in adult medicine, awareness and discussion of weight control, exercise, and other lifestyle issues must become an important part of the evaluation of obese children with heart disease in the cardiology outpatient setting. Weight may be one of the few modiable risk factors for children with heart disease. Pediatric cardiologists are frequently asked to provide recommendations for physical activity restriction in their patients with congenital and acquired heart disease or potentially life-threatening arrhythmias. These recommendations are extrapolated from published guidelines for competitive athletics in children with heart disease.34 In a retrospective study reviewing patients over a mee1162 PINTO et al

dian of 8 years, Stefan et al11 reported that activity restriction in children with congenital heart disease was associated with the development of obesity. Even children who were of healthy weight at baseline had a higher risk of becoming obese over time if their activity was restricted. Physical activity limitation is a risk factor unique to children with heart disease. Importantly, physical activity restrictions in children with heart disease are not solely determined by practitioner recommendations. Indeed, these limitations may sometimes be initiated by parents or be self-imposed.35 Children with heart disease are often sedentary even when not limited by their physiology.3537 Massin et al37 reported recently that children who had undergone the arterial switch operation were much less likely than their peers to participate in moderate or vigorous activity even when no restrictions had been placed by their cardiologists. Decreased activity may lead to deconditioning, decreased exercise capacity, and lower quality of life. A sedentary lifestyle associated with congenital heart disease is known to carry into adulthood and predict increased morbidity and mortality in this population.38 Several recent studies have shown the benets of physical training programs in both adults and children with congenital heart disease.39,40 Practitioners may need to refocus counseling during outpatient visits, providing careful instructions for appropriate and safe exercise regimens with regard to the underlying condition, in addition to more traditional counseling regarding exercise restrictions. Given the fact that patients with acquired and congenital heart disease have not escaped the epidemic of obesity, it is especially important for practitioners to adapt current activity guidelines from the American Heart Association10 and Bethesda conference34 for this purpose. STUDY LIMITATIONS Although the overall study population was quite large, small numbers in the transplant subgroup resulted in limited power to compare this group with the control subjects. Data collection was limited to childrens hospitals in Boston and Philadelphia and may not account for regional differences in obesity rates in other areas in the United States. In fact, control patients from CHB had slightly lower prevalence of overweight and obesity than those from CHOP, suggesting a slight difference in the underlying rate of pediatric obesity between the 2 cities. The data are also subject to the referral biases of each center. Data on race and its impact on the prevalence of obesity were not collected as part of this study. It should be emphasized that data were limited to the information contained in the dictated clinic letters and notes. Therefore, we were unable to assess whether obesity and weight counseling may have occurred during the ofce visit without documentation. Important contributing data, such as parental weight and patient

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activity levels, were not collected in this retrospective study, because this information was not consistently found in the clinic letters. In addition, we were only able to evaluate 1 comorbidity of obesity, blood pressure, from the data collected. In this population, the impact of the underlying heart disease on blood pressure may have been a confounder to its relationship to weight. All of the measurements used for analysis were obtained at only 1 point in time. This is especially important with regard to potential variability associated with blood pressure measurements in an outpatient ofce setting. Medications that might affect the outcome variables (eg, antihypertensive medication and steroids) were also not assessed in this analysis. CONCLUSIONS Obesity is a common signicant additional risk factor for long-term cardiovascular disability in children with congenital and acquired heart disease, a population that is already at increased risk of shortened life expectancy. Although this study has important implications for the practice of outpatient pediatric cardiology, additional investigation is required to identify both common and potentially unique contributors to this problem, such as formal or perceived exercise restriction. Additional study is also required to truly understand the impact of overweight on the long-term outcome and cardiovascular health of children with underlying heart disease. Appropriate interventions for obese pediatric cardiac patients need to be developed. Given the known benets of normal weight and exercise participation, advising against inactivity, obesity, and other unhealthy lifestyle choices and communicating these concerns to the referring physician should be important parts of the pediatric cardiologists care of children with cardiac disease. REFERENCES
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Obesity Is a Common Comorbidity in Children With Congenital and Acquired Heart Disease Nelangi M. Pinto, Bradley S. Marino, Gil Wernovsky, Sarah D. de Ferranti, Amy Z. Walsh, Meena Laronde, Kristen Hyland, Stanley O. Dunn, Jr and Meryl S. Cohen Pediatrics 2007;120;e1157 DOI: 10.1542/peds.2007-0306
Updated Information & Services References including high resolution figures, can be found at: http://pediatrics.aappublications.org/content/120/5/e1157.full. html This article cites 39 articles, 18 of which can be accessed free at: http://pediatrics.aappublications.org/content/120/5/e1157.full. html#ref-list-1 This article has been cited by 2 HighWire-hosted articles: http://pediatrics.aappublications.org/content/120/5/e1157.full. html#related-urls This article, along with others on similar topics, appears in the following collection(s): Heart & Blood Vessels http://pediatrics.aappublications.org/cgi/collection/heart_and_ blood_vessels Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://pediatrics.aappublications.org/site/misc/Permissions.xht ml Information about ordering reprints can be found online: http://pediatrics.aappublications.org/site/misc/reprints.xhtml

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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 2007 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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