Cardiac Abnormalities Associated with Morbid Obesity

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1Department of Surgery, Instituto Nacional de la Nutrición Salvador Zubirán, Vasco de Quiroga 15, Tlalpan 14000, Mexico, D.F. Mexico. 2Department of ...

World J. Surg. 22, 993–997, 1998

WORLD Journal of

SURGERY © 1998 by the Socie´te´ Internationale de Chirurgie

Cardiac Abnormalities Associated with Morbid Obesity Miguel F. Herrera, M.D.,1 Jorge Oseguera, M.D.,2 Rosa Gamino, S.W.,1 Carlos Gutie´rrez-Cirlos, M.D.,3 Florencia Vargas-Vorackova, M.D.,4 Jorge Gonza´lez-Barranco, M.D.,5 Juan A. Rull, M.D.3 1

Department of Surgery, Instituto Nacional de la Nutricio ´n Salvador Zubira´n, Vasco de Quiroga 15, Tlalpan 14000, Mexico, D.F. Mexico Department of Cardiology, Instituto Nacional de la Nutricio ´n Salvador Zubira´n, Vasco de Quiroga 15, Tlalpan 14000, Mexico, D.F. Mexico 3 Department of Internal Medicine, Instituto Nacional de la Nutricio ´n Salvador Zubira´n, Vasco de Quiroga 15, Tlalpan 14000, Mexico, D.F. Mexico 4 Department of Gastroenterology, Instituto Nacional de la Nutricio ´n Salvador Zubira´n, Vasco de Quiroga 15, Tlalpan 14000, Mexico, D.F. Mexico 5 Obesity Clinic, Instituto Nacional de la Nutricio ´n Salvador Zubira´n, Vasco de Quiroga 15, Tlalpan 14000, Mexico, D.F. Mexico 2

Abstract. Morbidly obese patients are at increased risk for structural and functional abnormalities of the heart. This paper summarizes the effects of obesity on the heart, the effect of weight reduction on cardiac function, the impact of coronary artery disease on cardiac cardiomyopathy, and our experience in obesity heart disease at the Instituto Nacional de la Nutricio ´n in Mexico.

Morbid (extreme) obesity has been defined as body weight greater than 100% above ideal body weight or a body mass index (BMI) . 40 kg/m2 [1]. The prevalence of obesity, defined as BMI . 27 kg/m2, in Mexico ranges from 21% to 60% [2, 3]. In 1993 the branch of epidemiology of the Mexican Health Department reported a prevalence of significant obesity (BMI . 35 kg/m2) of 6.1% [4]. Morbidly obese patients are at increased risk for heart disease [5]. Abnormalities can occur in cardiac structure or function or in the coronary arteries. It has been recognized that abnormalities in cardiac structure and function occur more commonly when patients have been obese for 15 years or longer than in those with obesity of shorter duration [6]. This paper summarizes the effects of obesity on the heart, the effect of weight reduction on cardiac function, and our experience in cardiopathy of the obese patient at the Instituto Nacional de la Nutricio ´n in Mexico. Obesity-related Cardiomyopathy Smith and Willius in a postmortem study showed that heart weight increases in direct relation to body weight, and that extremely obese patients have excessive epicardial fat, whereas left ventricular (LV) fat content remains normal [7]. The increased cardiac weight is due to an increase in LV weight resulting from eccentric wall hypertrophy [8]. Eccentric LV hypertrophy, the most common abnormality in the heart of morbidly obese patients, comprises chamber dilation and some wall thickening, as seen in other conditions in which cardiac output is chronically increased [9]. Correspondence to: M.F. Herrera, M.D.

When hypertension accompanies severe obesity, a combination of concentric and eccentric hypertrophy is present. The use of noninvasive techniques has provided further insight into the mechanisms of heart disease in the morbidly obese patient. Echocardiography studies in obese patients have reported LV enlargement in 8% to 40%, increased LV wall thickness in 6% to 56%, increased LV mass in 64% to 87%, left atrial (LA) enlargement in 10% to 40%, and right ventricular (RV) enlargement in 32% of patients [10 –12]. It is now established that the BMI strongly correlates with LV mass, wall thickness, and cavity dimension, even after adjusting for age and blood pressure [13]. Hemodynamic Alterations The massively obese state is accompanied by marked hemodynamic abnormalities. Extreme obesity causes an increased total blood volume and cardiac output in direct proportion to the amount of weight gained [14]. The total blood volume increases as a result of an increase in the size of the vascular bed in the excess adipose tissue. The splanchnic blood flow is only slightly increased, and cerebral and renal blood flow are close to normal. It has been calculated that the blood volume and cardiac output of a person weighing 170 kg are roughly twice those of a 70-kg subject [15]. Oxygen consumption also increases with obesity in close relation to body weight. The increased cardiac output is due to an increase in the stroke volume, stroke work, and cardiac work to serve the metabolic requirements of excessive fat. Mean values for cardiac output in terms of absolute flow are high, although the cardiac index is usually within the normal range [14, 15]. Mean arterial pressure, systemic vascular resistance, pulmonary capillary wedge pressure, pulmonary artery pressure, and RV enddiastolic pressure exceed those predicted for healthy subjects [16]. Pulmonary hypertension is a consequence of elevated LV diastolic pressure, and in some cases the obesity hypoventilation syndrome acts as a second etiologic factor. The response of mildly obese patients to exercise is comparable to that of subjects at ideal weight [17]. A study evaluating the impact of exercise on obese patients showed that bicycle exercise

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Table 1. Comparative analysis of echocardiographic values. Obese patients

Normal-weight individuals (n 5 30) Measurement

Result

p

Total group (n 5 30)

LVIDD (cm) LVSF (%) ST (cm) ARD (cm) LAD (cm) LAD/ARD ratio RVIDD (cm) RVIDD/LVIDD (%) RVAWT (cm) LVM (g) EF slope (mm/s) LVEDV (ml) LVESV (ml) SV (ml) CO (L/min) CO/weight (cc/kg) R/Th ratio

4.31 6 0.60 34 6 8 0.80 6 0.14 2.67 6 0.48 2.83 6 0.48 1.050 6 0.097 1.06 6 4.50 42.8 6 9.1 0.5 6 0.2 127 6 30 91.6 6 28.9 87 6 26 32 6 16 54 6 17 3.9 6 1.0 66 6 22 2.86 6 0.65

, 0.0005 , 0.05 , 0.005 , 0.005 , 0.0005 , 0.0005 , 0.05 NS NS , 0.0005 , 0.0005 , 0.0005 , 0.0005 , 0.005 , 0.0005 , 0.0005 , 0.05

5.1 6 0.6 28.0 6 8.5 1.1 6 0.3 3.0 6 0.5 3.7 6 0.6 1.3 6 0.2 2.3 6 1.0 46 6 19 0.5 6 0.1 256 6 83 65 6 30 127 6 34 64 6 33 66 6 20 5.4 6 1.6 41.5 6 15.8 2.52 6 0.50

Without hypertension (n 5 15) 5.20 6 0.56 27.9 6 9.4 0.99 6 0.15 2.92 6 0.26 3.7 6 0.7 1.3 6 0.2 2.04 6 0.80 51 6 23 0.5 6 0.1 257 6 60 69.2 6 32.0 132 6 33 61 6 28 64 6 20 5.4 6 1.7 46.2 6 15.9 2.57 6 0.40

p NS NS NS NS NS NS NS NS NS NS NS NS NS

With hypertension (n 5 15) 5.02 6 0.65 28.4 6 7.6 1.17 6 0.29 3.0 6 0.6 3.74 6 0.50 1.30 6 0.23 2.6 6 1.1 40.1 6 15.3 0.5 6 0.2 256 6 100 56.6 6 31.0 122 6 35 58 6 23 68 6 21 5.3 6 1.5 40.1 6 15.8 2.48 6 0.63

From Cueto Garcı´a et al. [12], with permission. All values are mean 6 standard deviation. LVIDD: left ventricular internal diastolic dimension; LVSF: left ventricular shortening fraction; ST: septal thickness; ARD: aortic dimension; LAD: left atrial dimension; RVIDD/LVIDD: right/left ventricular internal diastolic dimension; RVAWT: right ventricular anterior wall thickness; LVM: left ventricular mass; EF: ejection fraction; LVEDV: left ventricular end-diastolic volume; LVESV: left ventricular end-systolic volume; SV: stroke volume; CO: cardiac output; R/Th: relative LV wall thickness. Table 2. Associated conditions in 22 obese patients undergoing surgical treatment. Associated condition

No.

%

Arterial hypertension Smoking Hyperlipidemia Diabetes

9 7 7 5

41 32 32 23

Table 3. Preoperative electrocardiographic abnormalities (n 5 11). Abnormality

No.

Right ventricular enlargement Right atrial enlargement Left atrial enlargement Right ventricular afterload Left ventricular afterload

5 3 2 1 1

One patient had two abnormalities.

produces a substantial increase in maximal oxygen consumption, arteriovenous oxygen difference, cardiac output, stroke volume, heart rate, mean arterial pressure, mean pulmonary artery pressure, and mean pulmonary wedge pressure [18]. In a comparative study of 10 morbidly obese patients and 10 normal-weight patients reported in 1982 [19], impairment of cardiac performance in obese patients owing to LV dysfunction was found during the surgical procedure and the early postoperative phase. Thus the LV function of morbidly obese patients is also compromised by the stresses of surgery and anesthesia. Alpert and colleagues studied 39 morbidly obese patients to determine the factors influencing LV systolic function and found that LV fractional shortening correlated inversely with the LV internal dimensions during diastole and systole, LV end-systolic wall stress, and systolic blood pressure and LV mass [20]. In a study of 23 nonhypertensive morbidly obese patients, the same group found an increase of LV mass. Elevated LV filling pressure has been also observed by echocardiography in patients with morbid obesity. Chakko and colleagues reported prolongation of the mitral deceleration time [21]. RV function has also been studied, and depression of the right ventricular ejection fraction has been found [22].

Obesity cardiomyopathy is characterized by high cardiac output, pulmonary and systemic circulatory congestion, ventricular volume overload, and eccentric hypertrophy. According to Alpert and Hashimi, the following pathophysiologic sequence leads to obesity-related cardiomyopathy [23]: Excessive accumulation of fat produces an increase in circulatory blood volume, and cardiac output increases in proportion to the degree of obesity due to an increase in stroke volume. Systemic vascular resistance then decreases to accommodate the increase in cardiac output. The increase in circulating blood volume and cardiac output produces an increase in LV wall stress. The resultant increase in afterload predisposes to LV diastolic dysfunction due to a reduction in LV wall stress. Coronary Heart Disease The relation between obesity and coronary heart disease is under considerable debate. Several epidemiologic studies, such as the Framingham Study [24] the Coronary Heart Mortality Risk Study [25], the Honolulu Heart Study [26], the Paris Prospective Study [27, 28], and the Study of Men Born in 1913 [29] suggest a relation between central obesity and coronary heart disease; and many of them have demonstrated a relation between central obesity and

Herrera et al.: Cardiac Abnormalities with Morbid Obesity

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Table 4. Comparative analysis of echocardiographic variables before and after surgery. Before surgery

Three years after surgery

Patient

LAD

LVIDD

ST

LVPWT

RVIDD

LVMI

EF

LAD

LVIDD

ST

LVPWT

RVIDD

LVMI

EF

1 2 3 4 5 6 7 8

4.8 5.0 3.6 5.0 5.2 3.5 5.2 4.5

4.9 5.2 4.9 5.1 5.7 4.9 3.6 4.8

1.1 1.8 1.8 1.6 1.8 1.4 1.1 1.2

1.0 1.1 0.8 1.3 1.5 1.3 1.4 1.1

— 2.9 1.1 3.8 — 2.3 2.1 2.5

105 99 60 121 173 135 114 89

62 70 65 64 59 71 63 66

3.7 4.6 3.7 4.0 4.6 3.1 5.2 4.9

4.8 4.9 5.1 4.7 4.3 4.5 5.0 5.1

1.0 1.4 1.1 1.5 1.0 1.0 1.4 1.4

1.0 1.0 1.1 1.3 1.5 0.8 1.7 0.9

— 2.0 2.1 3.2 — — 1.6 1.7

109 97 125 156 178 142 261 117

62 61 53 58 60 47 68 74

LAD: left atrial dimension (cm); LVIDD: left ventricular internal diastolic dimension (cm); ST: interventricular septal thickness (cm); LVPWT: left ventricular posterior wall thickness (cm); RVIDD: right ventricular internal diastolic dimension (cm); LVMI: left ventricular mass index (g/m2); EF: ejection fraction (%).

coronary heart disease independent of coexistent coronary risk factors. However, there is no consensus about identifying obesity as an independent risk factor. The Honolulu Heart Study and the Paris Prospective study showed that for any given BMI the risk for coronary heart disease increased, as did the trunk fat index (an index of central adiposity). The Framingham Study and the Normative Aging Study identified the age at onset of obesity as an important factor in the development of coronary heart disease. On the other hand, the severity of obesity has not been shown to alter the development of coronary heart disease. Exercise-induced wall motion abnormalities mimicking coronary disease have been reported even in the presence of a normal, resting LV end-diastolic fraction [30]. This pattern is consistent with functional ischemia, as it has been found in the absence of angiographic coronary disease. Often in states of cardiac hypertrophy, coronary blood flow reserve becomes limiting as the ventricular mass increases and metabolic demands of the myocardium increase. The inability of the left ventricle to maintain adequate function predisposes to congestive heart disease. Autopsy data on patients with morbid obesity dying of congestive heart failure, on the other hand, have demonstrated little coronary artery disease [31]. There is also little information about the effect of weight loss on the progression of coronary artery disease. Arterial Hypertension There is strong evidence that severe obesity is frequently accompanied by arterial hypertension [32]. The Second National Health and Examination Survey (NHANES-II) demonstrated an increased risk of hypertension (2.9-fold) in overweight patients compared with normal-weight individuals [33]. The presence of hypertension is related not only to excess body fat but to the waist/hip ratio (truncal obesity). The adverse effects of obesity and hypertension on cardiac work are additive. The combination of obesity and hypertension significantly increase the development of congestive heart failure, and autopsy studies have shown the greatest heart weight in obese, hypertensive patients [34]. Effect of Weight Reduction on Cardiac Function Weight reduction and maintenance of a lower body weight are necessary for long-term benefit. Decreases in body oxygen con-

sumption, blood volume, cardiac output, stroke volume, and blood pressure can be achieved by weight reduction [35]. These changes are accompanied by decreases in LV volume and diastolic pressure at rest and during exercise. Echocardiographic studies performed before and after weight reduction have shown lower ventricular volume with an increase in the ejection fraction [36]. Experience at the Instituto Nacional de la Nutricio ´n In 1982 a prospective study performed in our institution evaluated echocardiographic findings in obese patients [12]. M-mode echocardiography was performed on 30 extremely obese patients and 30 normal-weight individuals. Among the obese patients, 15 were normotensive and 15 hypertensive. The comparative analysis of obese patients and normal controls is presented in Table 1. With the aim of comparing possible changes in cardiac function in a group of 22 morbidly obese patients who underwent surgery at our institution, a prospective study was conducted in 1992. All patients underwent cardiopulmonary evaluation before surgery that included chest radiography and electrocardiography (ECG). M-mode, bidimensional, and Doppler echocardiograms were obtained when clinically indicated. The following parameters were routinely investigated: cavity dimensions, parietal thickness, ventricular mass, and ejection fraction. Patients were closely followed after surgery, and the examinations were repeated 3 years after surgery. The ECGs were interpreted according to the criteria proposed by Hiss and colleagues [37]. The mean (6 SD) age of our patients was 46 6 9 years, with 14 women and 8 men. The mean (6 SD) weight of the total group before surgery was 143 6 31 kg, with a corresponding BMI of 54 6 7 kg/m2. At the 3-year follow-up the weight was 94 6 22 kg and the BMI 36 6 7 kg/m2. Associated conditions are shown in Table 2. Three patients presented with clinical symptoms/signs of cardiac insufficiency. The cardiothoracic index was measured on chest radiographs of all patients. A mean cardiac index of 0.53 was found before surgery, with a statistically significant reduction to 0.48 (p , 0.05) at the latest follow-up. A total of 10 ECGs were read as normal before surgery and remained normal afterward. Abnormal preoperative ECGs were found in 11 patients. The most common nonconductive abnormalities are shown in Table 3. Low voltage was found in six patients before surgery and persisted in four after weight reduction. Three patients had conduction system abnormalities; two

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had right bundle branch block, one had left anterior hemiblock, and one had first-degree atrioventricular block. All three abnormalities remained unchanged after surgery. Isolated ventricular premature beats were found in one patient before surgery and remained unchanged at the latest follow-up. All preoperative echocardiograms were abnormal. The most common abnormality was interventricular septal hypertrophy (88%) with or without posterior LV wall hypertrophy. Four patients presented concentric and three eccentric LV hypertrophy. The LV mass index was elevated in five patients (63%), and in six patients left atrial enlargement also occurred. The echocardiographic findings are summarized in Table 4. After surgically induced weight reduction, the left atrial enlargement persisted in four patients, and the LV enlargement was reduced in all patients. In two of four patients with preoperative concentric LV hypertrophy, the abnormality disappeared after surgery. The LV mass index and ejection fraction remained unchanged after weight reduction. Two patients showed pulmonary hypertension before surgery and after weight reduction, and the pulmonary pressure become normal in both. Re´sume´ Les patients atteints d’obe´site´ morbide ont un risque accru d’anomalies structurales et anatomiques du coeur. Ce travail re´sume les effets de l’obe ´site´ sur le coeur, l’effet de la re´duction du poids sur la fonction cardiaque, l’impact de la maladie coronarienne sur la cardiomyopathie et notre expe´rience avec la maladie coronarienne `a l’Instituto Nacional de la Nutricion `a Mexico. Resumen Los pacientes con obesidad mo ´rbida se encuentran en condicio ´n de mayor riesgo en cuanto a desarrollar anormalidades estructurales y funcionales en el corazo ´n. En este artı´culo se resumen los efectos de la obesidad sobre el corazo ´n, el efecto de la reduccio ´n de peso sobre la funcio ´n cardı´aca y el impacto de la enfermedad coronaria sobre la cardiomiopatı´a, ası´ como nuestra experiencia con la enfermedad cardı´aca por obesidad en el Instituto Nacional de Nutricio ´n de Me´xico. References 1. National Institutes of Health Consensus Development Conference: Health implications of obesity. Ann Intern Med 103(Suppl. 6):977, 1985 2. Cueto, L., Brito, E., Barrera, G.J., Gutie´rrez, A.M.: Prevalencia de factores de riesgo en buro ´cratas de la Ciudad de Me´xico. Arch Inst Cardiol Mex 59:19, 1989 3. Gonza´lez, V.C., Stern, P.M.: Obesidad como factor de riesgo cardiovascular en Me´xico: estudio en poblacio ´n abierta. Rev. Invest. Clin. 45:13, 1993 4. Ramos-Carricarte, A.: Epidemiology of obesity. In: ed. Obesity: A Clinical Approach, A. Ramos-Carricarte, editor. Me´xico: Disen ˜o y Servicios Gra´ficos, 1997, pp. 17–29 5. Drenick, E.J., Bale, G.S., Seltzer, F. Johnson, D.G.: Excessive mortality and causes of death in morbidly obese men. J.A.M.A. 243:443, 1980 6. Nakajima, T., Fujioka, S., Tokunaga, K., Hirobe, K., Matsuzawa, Y., Tarui, S.: Non-invasive study of left ventricular performance in obese patients: influence of duration on obesity. Circulation 71:481, 1985 7. Smith, H.L., Willius, F.A.: Adiposity of the heart. Arch. Intern. Med. 52:929, 1973

World J. Surg. Vol. 22, No. 9, September 1998 8. Warnes, C.A., Roberts, W.C.: The heart in massive (more than 300 pounds or 136 kg) obesity: analysis of 12 patients studied at necropsy. Am. J. Cardiol. 54:1097, 1984 9. Carpenter, H.M.: Myocardial fat infiltration. Am. Heart J. 63:491, 1962 10. Zema, M.J., Caccavano, M.: Feasibility of detailed M-mode echocardiographic examination in markedly obese adults: prospective study of 50 patients. J. Clin. Ultrasound 10:31, 1982 11. Alpert, M.A., Terry, B.E., Kelly, D.L.: Effect of weight loss on cardiac chamber size, wall thickness and left ventricular function in morbid obesity. Am. J. Cardiol. 55:783, 1985 12. Cueto Garcia, L., Laredo, C., Arriaga, J., Gonza´lez-Barranco, J.: Echocardiographic findings in obesity. Rev. Invest. Clin. 34:235, 1982 13. Lauer, M.S., Anderson, K.M., Kannel, W.B., Levy, D.: The impact of obesity on left ventricular mass and geometry: the Framingham Heart Study. J.A.M.A. 266:231, 1991 14. Alexander, J.K.: Obesity and cardiac performance. Am. J. Cardiol. 14:860, 1965 15. Alexander, J.K., Dennis, D.W., Smith, W.G., Amad, K.H., Ducan, W.C., Austin, R.D.: Blood volume, cardiac output and distribution of systemic blood flow in extreme obesity. Cardiovasc. Res. Center Bull. 1:39, 1962 16. De Divitiis, O., Fazio, S., Petitto, M., Maddalena, G., Contaldo, F., Mancini, M.: Obesity and cardiac function. Circulation 64:477, 1981 17. Kaltman, A.J., Goldring, R.M.: Role of circulatory congestion in the cardiorespiratory failure of obesity. Am. J. Med. 60:645, 1976 18. Backman, L., Freyschuss, U., Hallberg, D., Melchor, A.: Cardiovascular function in extreme obesity. Acta Med. Scand. 193:437, 1973 19. Agarwal, N., Shibutani, K., San Filippo, J.A., del Guercio, L.R.M.: Hemodynamic and respiratory changes in surgery of the morbidly obese. Surgery 92:226, 1982 20. Alpert, M.A., Singh, A., Terry, B.E., Kelly, D.L., Villarreal, D., Mukerjin, V.: Effect of exercise on left ventricular systolic function and reserve in morbid obesity. Am. J. Cardiol. 63:1478, 1989 21. Chakko, S., Mayn, M., Allison, M.D., Fessler, K.M., Materson, B., Myerburg, R.J.: Abnormal left ventricular diastolic filling in eccentric left ventricular hypertrophy of obesity. Am. J. Cardiol. 68:95, 1991 22. Alpert, M.A., Singh, A., Terry, B.E., Kelly, D.L., El Deane, M.S.S., Mukerjl, V., Villarreal, D., Artis, A.K.: Effect of exercise and cavity size on right ventricular cavity size in morbid obesity. Am. J. Cardiol. 64:1361, 1989 23. Alpert, M.A., Hashimi, M.W.: Obesity and the heart. Am. J. Med. Sci. 306:117, 1993 24. Hubert, H.B., Feinleib, M., McNamara, P.M., Castelli, W.P.: Obesity as an independent risk factor for cardiovascular disease: a 26 year follow-up of participants in the Framingham Heart Study. Circulation 67:968, 1983 25. Jooste, P.L., Steenkamp, H.F., Benede, A.J.S., Rossouw, J.E.: Prevalence of overweight and obesity and its relationship to coronary heart disease in the CORIS study. S. Afr. Med. J. 74:101, 1988 26. Donahue, R.P., Bloom, E., Abbot, R.D., Bloom, E., Reed, D.M., Yano, F.: Central obesity and coronary heart disease in men. Lancet 1:821, 1987 27. Ducimetiere, P., Richard, J.L.: The relationship between subsets of anthropometric upper vs lower body measurements and coronary heart disease risk in middle aged men: the Paris Prospective Study I. Int. J. Obes. 13:111, 1989 28. Fontbonne, A., Tchobroustsky, G., Eschwege, E., Richards, J.L., Claude, J.R., Rosselin, G.E.: Coronary heart mortality risk: plasma insulin level is a more predictive marker than hypertension or abnormal glucose tolerance in overweight males: the Paris Prospective Study. Int. J. Obes. 12:557, 1988 29. Larsson, B., Svardsudd, K., Welin, L., Bjo ¨rntorp, L.P., Tibblin, G.: Abdominal adipose tissue distribution, obesity, and risk of cardiovascular disease and death: 13 year follow-up of participants in the study of men born in 1913. B.M.J. 28:1401, 1984 30. Murray, G., Cowan, G.M.S., Jr., Vander-Zwagg, R.: Exercise-induced wall motion abnormalities and resting left ventricular dysfunction in the morbidly obese as assessed by radionuclide ventriculography. Obes. Surg. 1:37, 1990 31. Amad, K.H., Brennan, J.C., Alexander, J.K.: The cardiac pathology of obesity. Circulation 32:740, 1965

Herrera et al.: Cardiac Abnormalities with Morbid Obesity 32. Kannel, W.B., Brand, N., Skinner, J.J., Dawber, T.R., McNamara, P.M.: Relation of adiposity to blood pressure and development of hypertension: the Framingham Study. Ann. Intern. Med. 67:48, 1978 33. Fifth report of The Joint National Committee on Detection, Evaluation and Treatment of High Blood Pressure. Arch. Intern. Med. 153:154, 1993 34. Benotti, P.N., Bistrian, B., Benotti, J.R., Blackburn, G., Forse, A.: Heart disease and hypertension in severe obesity: the benefits of weight reduction. Am. J. Clin. Nutr. 55:586S, 1992

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