Satish Kenchaiah, M.D., Jane C. Evans, D.Sc., Daniel Levy, M.D., Peter W.F. Wilson, M.D., Emelia J. Benjamin, M.D., Martin G. Larson, S.D., William B. Kannel, M.D., M.P.H., and Ramachandran S. Vasan, M.D.
Background Extreme obesity is recognized to be a risk factorfor heart failure. It is unclear whether overweight and lesserdegrees of obesity also pose a risk.
Methods We investigated the relation between the body-mass index(the weight in kilograms divided by the square of the heightin meters) and the incidence of heart failure among 5881 participantsin the Framingham Heart Study (mean age, 55 years; 54 percentwomen). With the use of Cox proportional-hazards models, thebody-mass index was evaluated both as a continuous variableand as a categorical variable (normal, 18.5 to 24.9; overweight,25.0 to 29.9; and obese, 30.0 or more).
Conclusions In our large, community-based sample, increasedbody-mass index was associated with an increased risk of heartfailure. Given the high prevalence of obesity in the UnitedStates, strategies to promote optimal body weight may reducethe population burden of heart failure.
Heart failure is a major health problem that is increasing inscope.1 Despite recent therapeutic advances, morbidity and mortalityafter the onset of heart failure remain substantial.1 Consequently,prevention of heart failure through identification and managementof risk factors and preclinical phases of the disease is a priority.2In this context, several studies have evaluated body-mass index(the weight in kilograms divided by the square of the heightin meters) as a risk factor for left ventricular remodelingand overt heart failure. In these investigations, obesity hasbeen consistently associated with left ventricular hypertrophyand dilatation,3,4,5,6 which are known precursors of heart failure.7,8Whereas extreme obesity has been associated with heart failure,9data are limited regarding the influence of overweight and lesserdegrees of obesity on the risk of heart failure.10,11,12 Accordingly,we investigated the relation of body-mass index with the riskof heart failure in a community-based sample.
Methods
Participants
The design and selection criteria of the Framingham Heart Studyhave been described previously.13,14 Participants in the 15thbiennial examination of the original cohort (1976 through 1979,2632 subjects) and the second offspring study examination (1979through 1983, 3863 subjects) were eligible for the present investigation.We excluded 614 attendees (9.5 percent) for the following reasons:age under 30 years (271 subjects), underweight (body-mass indexless than 18.5 [85 subjects]),15,16 heart failure at base-lineexamination (84 subjects), missing information on covariates(172 subjects), and lack of follow-up data (2 subjects). Afterthese exclusions, 5881 subjects (3177 women and 2704 men) remainedeligible. Written informed consent was obtained from the studyparticipants, and the research protocol was reviewed and approvedby the institutional review board of the Boston University Schoolof Medicine.
Estimation of Adiposity and Covariates
At each examination, a medical history was taken, a physicalexamination (including anthropometric measurements and measurementof blood pressure) was performed, a 12-lead electrocardiogramwas obtained, and risk factors for cardiovascular disease wereassessed. Height and weight were measured according to a standardizedprotocol. The body-mass index was calculated and was used asan estimate of overweight and obesity.16 The criteria and methodsof measurement of all covariates have been described previously.17
Outcome
Surveillance for the development of cardiovascular events wascontinuous for all participants. A panel of three experiencedphysicians reviewed suspected cardiovascular events by examininghospital records and information from outside physicians.17In this investigation, the primary outcome of interest was theoccurrence of a first episode of heart failure, as defined bythe Framingham Heart Study criteria.18 The simultaneous presenceof at least two major criteria or one major criterion in conjunctionwith two minor criteria was required to establish a diagnosisof heart failure. Major criteria included paroxysmal nocturnaldyspnea or orthopnea, jugular venous distention, pulmonary rales,radiographic cardiomegaly, acute pulmonary edema, a third heartsound, central venous pressure above 16 cm of water, hepatojugularreflux, and weight loss of at least 4.5 kg in five days in responseto treatment for heart failure. Minor criteria included bilateralankle edema, nocturnal cough, dyspnea on ordinary exertion,hepatomegaly, pleural effusion, and a heart rate of at least120 beats per minute. Minor criteria were acceptable only ifthey could not be attributed to another medical condition (suchas chronic lung disease, cirrhosis, ascites, or the nephroticsyndrome).
Statistical Analysis
We used Cox proportional-hazards regression models,19 stratifiedaccording to cohort (original or offspring), to examine therelation of body-mass index to the incidence of heart failure.We performed both sex-specific and sex-stratified analyses.Body-mass index was evaluated as both a continuous variable(with increases in risk calculated per increment of 1) and acategorical variable. Subjects with values of 18.5 to 24.9 wereclassified as normal (the reference group), those with valuesof 25.0 to 29.9 as overweight, and those with values of 30.0or more as obese.15,16 We adjusted for the following base-linecovariates: age, smoking status, alcohol consumption, totalserum cholesterol level, and presence or absence of valve disease,hypertension, diabetes mellitus, electrocardiographic left ventricularhypertrophy, and myocardial infarction (all defined at baseline). We constructed trend models to determine whether therewas a continuous gradient of heart-failure risk across categoriesof body-mass index. To evaluate the risk of heart failure associatedwith varying degrees of obesity, we performed analyses thatcategorized the obese group into three classes with body-massindexes of 30.0 to 34.9 (group 1), 35.0 to 39.9 (group 2), and40.0 or more (group 3).15,16 We also evaluated models withbody-mass index and all covariates treated as time-dependentvariables (updated every four years, including adjustment forthe occurrence of interim myocardial infarction).
Elevated body-mass index could predispose persons to heart failureby promoting atherogenic traits such as hypertension, diabetesmellitus, and dyslipidemia, which, in turn, could result inmyocardial infarction. Therefore, we constructed hierarchicalstatistical models using covariates defined at base line, withadjustment for potential confounders (age, cigarette smoking,alcohol consumption, and valve disease) and for all these variablesplus covariates that are known to be along the causal pathwayfrom excess weight to heart failure (e.g., hypertension, electrocardiographicleft ventricular hypertrophy, diabetes mellitus, high totalserum cholesterol level, and myocardial infarction). We alsoevaluated stepwise models with body-mass index, systolic bloodpressure, alcohol intake, and total serum cholesterol as continuousmeasures (other covariates were dichotomous).
We examined models incorporating interaction terms to evaluatevariation in the effect of body-mass index on the risk of heartfailure according to age, sex, smoking status, alcohol consumption,and the presence or absence of valve disease, hypertension,diabetes mellitus, and myocardial infarction (all defined atbase line).
We estimated the category-specific population attributable risk(PAR), expressed as a percentage, as a function of the proportionof cases occurring in a given category of body-mass index (pd)and the multivariable-adjusted relative risk (RR, equivalentto hazard ratios from models with covariates defined at baseline) with the following equation:20
PAR = pd [(RR – 1) / RR] x 100.
To obtain insight into the type of heart failure (systolic vs.diastolic) associated with increasing body-mass index, we reviewedechocardiographic reports for a subgroup of participants whounderwent evaluation of left ventricular systolic function within30 days after their first hospitalization for heart failurebetween 1989 and 1998. Heart failure was presumed to be dueto systolic dysfunction (systolic heart failure) if the estimatedleft ventricular ejection fraction was less than 50 percent,whereas a left ventricular ejection fraction of 50 percent ormore was considered to be consistent with diastolic heart failure.21The proportion of patients with heart failure who had a leftventricular ejection fraction under 40 percent, indicating moderateor severe left ventricular systolic dysfunction, was also examined.
Although underweight subjects were excluded from the primaryanalyses, we performed supplementary analyses comparing therisk of heart failure in these subjects with that in subjectswith a normal body-mass index.
A two-sided P value of less than 0.05 was considered to indicatestatistical significance. All analyses were performed with SASsoftware (version 6.12).22
Table 1. Base-Line Characteristics According to the Category of Body-Mass Index.
Body-Mass Index and the Risk of Heart Failure
During a mean follow-up of 14 years (maximum, 21.8), heart failuredeveloped in 496 participants (258 women and 238 men). The crudecumulative incidence (Figure 1) and the age-adjusted incidencerates (Table 2) of heart failure increased across categoriesof body-mass index for both men and women.
Figure 2. Risk of Heart Failure in Obese Subjects, According to Category of Body-Mass Index at the Base-Line Examination.
I bars represent the 95 percent confidence intervals for the hazard ratios. Hazard ratios were adjusted for age, total serum cholesterol level, cigarette smoking, alcohol consumption, and presence or absence of valve disease, hypertension, diabetes mellitus, electrocardiographic evidence of left ventricular hypertrophy, and myocardial infarction at base line. Normal weight (body-mass index, 18.5 to 24.9) was the reference category. Hazard ratios on the y axis are shown on a logarithmic scale. Data for men in obesity class 3 are not provided because of the small sample (eight subjects).
In models adjusted only for age, smoking status, alcohol consumption,and valve disease, the hazard ratios for heart failure per increaseof 1 in the body-mass index were 1.08 (95 percent confidenceinterval, 1.06 to 1.11) in women and 1.07 (95 percent confidenceinterval, 1.04 to 1.11) in men. In these models, in comparisonwith subjects with a normal body-mass index, the hazard ratiosfor heart failure were 1.53 (95 percent confidence interval,1.15 to 2.04) for overweight women, 2.24 (95 percent confidenceinterval, 1.62 to 3.11) for obese women, 1.35 (95 percent confidenceinterval, 0.99 to 1.85) for overweight men, and 2.34 (95 percentconfidence interval, 1.60 to 3.41) for obese men. Additionaladjustment for hypertension, diabetes mellitus, high total serumcholesterol level, electrocardiographic left ventricular hypertrophy,and myocardial infarction (variables along the causal pathway)led to a slight attenuation of the hazard ratios in men butnot in women (Table 3, models IA and IB). In models with stepwiseselection of covariates (at an alpha level of <0.05), age,myocardial infarction, valve disease, and systolic blood pressureentered ahead of body-mass index. The hazard ratio for heartfailure associated with body-mass index was nearly identicalto that shown in model IA in Table 3.
Effect Modification
The effect of body-mass index on the risk of heart failure didnot vary with age, sex, smoking status, alcohol consumption,or the presence or absence of valve disease or diabetes mellitus(P>0.10). However, we noted effect modification with hypertension(P=0.03) and myocardial-infarction status (P=0.02). The hazardratio for the trend in the risk of heart failure across body-massindex categories was lower in subjects with hypertension (1.30;95 percent confidence interval, 1.11 to 1.52) than in subjectswithout hypertension (1.66; 95 percent confidence interval,1.33 to 2.07). Increased body-mass index was not associatedwith an increased risk of heart failure in those with myocardialinfarction at base line (148 subjects; hazard ratio for trendacross categories, 0.80; 95 percent confidence interval, 0.50to 1.30) as compared with those without myocardial infarction(5733 subjects; hazard ratio, 1.50; 95 percent confidence interval,1.31 to 1.71). The statistical power to detect hazard ratiosof 1.5, 2.0, and 2.5 for heart failure (for trend across body-massindex categories at an alpha level of <0.05) in subjectswith myocardial infarction at base line was 0.38, 0.81, and0.96, respectively.
Population Attributable Risk
The population attributable risk of heart failure due to overweightwas 14.0 percent in women and 8.8 percent in men. The correspondingpopulation attributable risks due to obesity were 13.9 percentin women and 10.9 percent in men.
Echocardiographic Evaluation
Of the 120 participants who underwent echocardiographic evaluationwithin 30 days of their first hospitalization for heart failure(24 percent of those with heart failure), 75 percent (21 of28) of those with a normal body-mass index, 65 percent (37 of57) of overweight subjects, and 66 percent (23 of 35) of obesesubjects had a left ventricular ejection fraction of less than50 percent (indicative of systolic heart failure). The proportionsof subjects with heart failure who had a left ventricular ejectionfraction of less than 40 percent in the normal, overweight,and obese groups were 53.6 percent, 52.6 percent, and 42.9 percent,respectively.
Risk of Heart Failure in Underweight Subjects
Only 3 of the 76 underweight subjects (64 women and 12 men)had heart failure on follow-up. In sex-stratified models, underweightsubjects had a multivariable-adjusted hazard ratio of 0.95 (95percent confidence interval, 0.37 to 2.45) as compared withthose with a normal body-mass index.
The smaller effect of body-mass index on the risk of heart failurein subjects with hypertension probably indicates a decreasedcontribution of obesity to the risk of heart failure in thepresence of this major risk factor. The lack of effect of body-massindex on the risk of heart failure in subjects with myocardialinfarction, however, must be interpreted with caution becauseof the small sample. In a subgroup of subjects who underwentechocardiographic evaluation within 30 days after their firsthospitalization for heart failure, obesity was associated withboth systolic and diastolic heart failure.
Three prior community-based studies reported an associationof increased body-mass index with an increased risk of heartfailure.10,11,12 However, they did not use the contemporarybody-mass index classification,15,16 and ascertainment of heartfailure was based primarily on hospital-discharge codes or deathcertificates. Furthermore, none of these studies assessed theentire range of body-mass index values or modeled covariatesas time-dependent variables. Only one study10 adjusted for theoccurrence of an interim myocardial infarction.
Other investigators have reported that a low body-mass indexis associated with increased mortality among patients with heartfailure.23,24 Our study had limited power to evaluate the riskof heart failure in underweight subjects. In this context, itis important to draw a distinction between the role of elevatedbody-mass index as a risk factor for heart failure and its effecton survival after the onset of heart failure.
The strength of the association, the stepwise increase in therisk of heart failure across increasing categories of body-massindex, the demonstration of a temporal sequence (with increasedbody-mass index preceding the development of heart failure),and the consistency of results in multiple analyses suggesta causal relation between increased body-mass index and heartfailure. There are several plausible mechanisms for such anassociation. Increased body-mass index is a risk factor forhypertension,25 diabetes mellitus,26,27 and dyslipidemia,16all of which augment the risk of myocardial infarction,28,29an important antecedent of heart failure.10,11,12,30 In addition,hypertension and diabetes mellitus independently increase therisk of heart failure.10,11,12,30,31 Elevated body-mass indexis associated with altered left ventricular remodeling,3,4,5,6,8possibly owing to increased hemodynamic load,32,33 neurohormonalactivation,34 and increased oxidative stress.35 Recently, Zhouet al. raised the possibility of a direct effect of obesityon the myocardium by demonstrating cardiac steatosis and lipoapoptosisin an animal model of obesity.36
The strengths of our investigation include the large community-basedsample, standardized assessment of body-mass index, consistentuse of the same diagnostic criteria for heart failure, and thelong period of follow-up. Nonetheless, it is important to acknowledgeseveral limitations. Although a diagnosis of heart failure wasmade only after a careful review of the records by a panel ofthree physicians, it is still possible that symptoms (such asdyspnea) and signs (such as ankle edema) may be misconstruedas indicating heart failure more often in obese persons.37 Pedaledema was more common among obese subjects with heart failure,but the distributions of major and all other minor heart-failurecriteria were similar among subjects with heart failure in thethree categories of body-mass index (data not shown). Exclusionof pedal edema as a minor criterion in the obese subjects didnot alter the diagnosis of heart failure by the Framingham HeartStudy adjudication panel in any instance. Other evidence againstmisclassification of subjects with heart failure as the explanationfor the observed association includes the substantial increasein the risk of heart failure among those who were overweightand those with lesser degrees of obesity, and the finding ina subgroup analysis that 43 percent of obese subjects with heartfailure had moderately or severely impaired left ventricularsystolic function. Finally, because our sample was predominantlywhite, we avoided confounding by race but at the same time,we reduced the generalizability of our findings to other racesand ethnic groups.
Our findings suggest that obesity is an important risk factorfor heart failure in both women and men. Approximately 11 percentof cases of heart failure among men and 14 percent among womenin the community are attributable to obesity alone. The contributionof obesity to the risk of heart failure has not been adequatelyrecognized, and our observational data suggest that effortsto promote optimal body weight may reduce the risk of heartfailure. Our results are particularly relevant given the alarmingtrend toward increasing obesity in the United States.16
Supported in part by a contract (N01-HC-25195) with the NationalHeart, Lung, and Blood Institute; by grants from Roche Laboratories(to Dr. Wilson) and Servier Amérique (to Dr. Kannel);and by a Research Career Award (1K24 HL04334) from the NationalHeart, Lung, and Blood Institute (to Dr. Vasan).
Source Information
From the Framingham Heart Study, Framingham, Mass. (S.K., J.C.E., D.L., P.W.F.W., E.J.B., M.G.L., W.B.K., R.S.V.); the Section of Preventive Medicine (D.L., E.J.B., M.G.L., W.B.K., R.S.V.) and the Cardiology Section (E.J.B., R.S.V.), Boston University School of Medicine, Boston; the Cardiology Division, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston (D.L.); and the National Heart, Lung, and Blood Institute, Bethesda, Md. (D.L.).
Address reprint requests to Dr. Vasan at the Framingham Heart Study, 73 Mt. Wayte Ave., Suite 2, Framingham, MA 01702, or at vasan{at}fram.nhlbi.nih.gov.
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Obesity and the Risk of Heart Failure
O'Brien G., Maurer M. S., Taegtmeyer H., Wilson C. R., Dart R. A., Jenny-Avital E. R., Kenchaiah S., Levy D., Vasan R. S., Massie B. M.
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Correspondence
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