Journal of Clinical Densitometry, vol. 9, no. 4, 438e444, 2006 Ó Copyright 2006 by The International Society for Clinical Densitometry 1094-6950/06/9:438e444/$32.00 DOI: 10.1016/j.jocd.2006.09.001
Original Article
Caloric Expenditure in the Morbidly Obese Using Dual Energy X-ray Absorptiometry Thomas E. Vanhecke,* Barry A. Franklin, Martin A. Lillystone, Keisha R. Sandberg, Adam T. deJong, Kevin R. Krause, David L. Chengelis, and Peter A. McCullough Department of Medicine, Divisions of Cardiology, Nutrition and Preventive Medicine, William Beaumont Hospital, Royal Oak, MI
Abstract Total caloric expenditure is the sum of resting energy expenditure (REE) and caloric expenditure during physical activity. In this study, we examined total caloric expenditure in 25 morbidly obese patients (body mass index 35 kg/m2) using dual energy X-ray absorptiometry (DXA) scanning and cardiorespiratory exercise testing. Our results show average REE for all individuals was 2027 276 kcal/d and mean net caloric expenditure during 30 min of exercise was 115 16 kcals. Assuming the mean of all input values, a strict 1500 kcal/d diet combined with 150 min per wk of structured physical activity, the projected weight change was 7% (8.8 6.2 kg) for 6 mo. We conclude that morbidly obese individuals should be able to achieve only a modest weight loss by following minimal national guidelines. These data suggest that more aggressive energy expenditure and caloric restriction targets for long periods of time are needed to result in significant weight loss in this population. Key Words: Body composition; caloric expenditure; cardiorespiratory fitness; dual energy X-ray absorptiometry; exercise; weight loss.
(5). More recently, the Institute of Medicine recommended 60 min of moderate intensity of exercise per day with dietary restriction if weight management is the primary objective (6). In 2001, the American College of Sports Medicine (ACSM) updated its position on weight loss and prevention of weight gain for adults, and recommended that overweight adults progress gradually to 200e300 min of exercise per week (w 45 min/d) or O 2000 kcal/wk to obtain long-term benefits (7,8). Recent technology has increased the accuracy of estimating resting energy expenditure (REE), which has traditionally been measured by indirect calorimetry. Although the most widely used method of calculating REE is the Harris-Benedict equation or a modification of it (9,10), it was derived from a population of nonobese individuals and is inaccurate when used in overweight or obese individuals (11). Along with the obesity epidemic of the 21st century, more accurate methods of determining REE have been validated for use in obese individuals. Most of the newer equations consider adipose tissue as ‘‘energetically inert.’’ Therefore, REE is highly
Introduction Recent estimates suggest that more than half of the adults in today’s Western society will, over time, become overweight or obese (1). This is alarming when considering that deaths attributable to obesity are projected to soon overtake tobacco as the number one cause of preventable death in today’s society (2). Of those individuals attempting to lose weight, almost two-thirds of women and men reported engaging in regular physical activity; however, less than one-fifth met recommendations of eating fewer calories and participating in O 150 min/wk of physical activity (3,4). In 1998, the National Heart, Lung and Blood Institute advised 30 to 45 min of moderate activity 3 to 5 days per week along with dietary restriction for weight loss and maintenance Received 06/21/06; Revised 09/01/06; Accepted 09/01/06. *Address correspondence to: Thomas E. Vanhecke, MD, Department of Internal Medicine, William Beaumont Hospital, 3601 W. 13 Mile Rd., Royal Oak, MI 48073. E-mail: tvanhecke@gmail.com
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dependent on fat-free mass (FFM) or lean tissue mass (12). Prior to the advent of dual energy X-ray absorptiometry (DXA) scanning, difficulties in calculating FFM using anthropometry, underwater weighing, total body potassium, and heavy-water dilution techniques precluded rapid, accurate measurement of REE in obese individuals. As DXA scanning has become more prevalent, this technology has been shown to provide a valid and noninvasive measurement of FFM in obese subjects, thereby facilitating more accurate estimation of REE (12e14). Caloric expenditure during physical activity can be estimated noninvasively by a variety of methods. One such method derives peak or maximum caloric expenditure by measuring an individual’s aerobic capacity or VO2max, expressed as L/min, during a progressive treadmill stress test to exhaustion (15). The present study was designed to estimate the potential weight loss that would occur in morbidly obese individuals following a restricted caloric diet of 1500 kcal/d and 30 min moderate intensity of physical activity. In this experiment, the caloric expenditure associated with structured exercise was determined from the VO2max, whereas REE was estimated from variables obtained by DXA scanning.
Madison, WI) to determine FFM (17,18). The DXA scans were analyzed using the PIXImus2 software (version 1.46.007, GE Healthcare, Madison, WI) with the head region excluded. As per the manufacturer’s guidelines, the DXA scanners were calibrated for body composition measurements on a daily basis. Values for whole body bone mineral density (BMD [g/cm2]), bone mineral content (BMC [g]), bone area (cm2), total tissue mass (calculated by the software [g]), total area (cm2), fat content (g), lean content (total tissue mass minus fat content [g]), and percent of fat (fat content divided by total tissue mass) were obtained. Body weight (kg) was measured on a calibrated scale immediately prior to scanning. Regions of interest, such as trunk, arms, and legs were selected and analyzed separately for BMD and tissue composition.
Methods
REE Calculation
Estimation of REE A BMI-specific algorithm, derived from a large, cross-sectional population of individuals from modern Western society (14) was used to estimate REE (kcal/d) in all study participants. Using the body composition data collected by DXA scanning, 24-hour REE was estimated using the following algorithm for obese individuals (BMI O 30) (14):
Study Population Eligibility criteria for inclusion in this analysis were: (1) body mass index (BMI) 35 kg/m2, (2) absence of severe lung disease requiring chronic oxygen therapy or limiting cardiopulmonary disease, (3) ability to perform cardiopulmonary exercise testing (CPX) to exhaustion, demonstrating a peak respiratory exchange ratio (RER) 1.10, and (4) ability to undergo DXA scanning for body composition analysis (subjects could not exceed 200 kg and had to be within the scanning region). This study was conducted from 2004 to 2005 and data were analyzed in 2005. The study was approved and monitored by the Human Investigations Committee at William Beaumont Hospital.
Cardiopulmonary Exercise Testing Subjects underwent peak or symptom-limited CPX testing using Bruce treadmill protocols. Subjects enrolled in this study completed symptom-limited CPX testing using a progressive protocol as described in a prior report (16). Heart rate and blood pressure were measured at rest in the supine and standing positions and during each stage of exercise. Respiratory variables, heart rate, blood pressure, and perceived exertion were determined at submaximal and maximal exercise. Continuous metabolic data were obtained during testing, which included oxygen consumption (VO2; mL/min, or metabolic equivalents), minute ventilation, carbon dioxide production (VCO2), and RER (VCO2/VO2).
Body Composition Analysis All patients underwent body composition testing via DXA scanning (Lunar/GE Medical Systems, GE Healthcare, Journal of Clinical Densitometry
REEðKcal=dÞ 5 ð0:05685 FMM½kg þ 0:04022FM½kg þ 0:808 sex 0:01402 age½yr þ 2:818Þ 239:01 (sex*: male 5 1; female 5 0)
Estimation of Physical Activity Energy Expenditure Energy expenditure during structured physical activity was estimated using metabolic variables obtained during CPX testing. Because oxygen uptake during CPX testing may be expressed in absolute terms (i.e., L/min), VO2 can be converted to a rate of energy expenditure because 1 L of O2 consumed approximates 5 kcal of energy (15). Calculations were based on VO2max using the following method: caloric expenditure in kcal/min 5 (VO2max in L/min) 5 kcal/L. We estimated the projected weekly net caloric expenditure for men and women who exercise regularly for 30 min/d for 5 d/wk at a moderate intensity (50% VO2max) by subtracting the REE from total caloric expenditure during physical activity. The net rate of oxygen uptake is the consumption rate above resting oxygen uptake, and it is used to describe the caloric cost of exercise.
Estimated Weight Loss Estimated weight loss over time can be predicted if total energy expenditure and daily caloric intake are known as described in a prior report (10). The daily net caloric deficit for a unit period of time can determined by taking the daily caloric intake (1500 kcal conventional weight loss diet) and Volume 9, 2006
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Fig. 1. Theoretical model of conventional weight loss by following recommended guidelines of dietary restriction and physical activity. subtracting the REE along with the net caloric expenditure of physical activity (see Fig. 1).
Statistical Analysis Baseline characteristics were expressed as mean standard deviation or counts with proportions as appropriate. Univariate comparisons were made with the Student’s t test, Fisher’s Exact test, the c2 test, and the c2 test for trend as appropriate. A p value ! 0.05 was considered statistically significant. Pearson’s correlation was used for bivariate comparisons.
study participants was 10.5 1.7 kcal/min. Using peak caloric expenditure data, the net caloric expenditure during 30 minutes of moderate intensity physical activity was 115 15 kcal. The estimated weekly gross caloric expenditure during exercise was 575 15 kcal. Likewise, the weekly net caloric expenditure during exercise (total caloric expenditure during exercise minus REE) was 575 81 kcals. If 7700 kcal in energy expenditure were required for a 1 kg weight loss (10),
Results Our study population was comprised of 20 women and 5 men with an average age of 47.6 11 years and an average body mass index of 48.2 4.7 kg/m2. Of these participants, 16% participated in regular exercise, 8% had coronary artery disease, 40% had diabetes, and 52% had hypertension. The average baseline systolic blood pressure was 133.7 18.1 mmHg, average diastolic blood pressure was 84.0 11.1 mmHg, and average heart rate was 78.6 10.5. During CPX, the average peak systolic blood pressure was 188.1 22.0 mmHg, average diastolic blood pressure was 81.8 9.5 mmHg, and average heart rate was 153 17. Study participants on average achieved a maximum VO2 (mL/min), and VCO2 (mL/min) of 2096 349 and 2318 521, respectively. During CPX testing, all participants reached physiological maximum effort, as signified by an RER 1.10. Cardiopulmonary exercise testing revealed an average peak VO2 (mL/ kg/min) of 16.5 2.7. Mean peak caloric expenditure for Journal of Clinical Densitometry
Fig. 2. Predicted daily caloric expenditure of all participants. Volume 9, 2006
Caloric Expenditure in the Morbidly Obese Using DXA participants would expect to lose 0.08 kg/wk. For 6 mo of perfect compliance, a loss of 2.0 kg could be expected from exercise alone. In Fig 2, the daily caloric expenditure of study participants as projected by CPX and body composition analysis is shown. The REE was estimated by using a BMI-specific calculation as previously described in the methods. This calculation used the variables of FFM and FM obtained by DXA body composition analysis to estimate REE. Using this calculation, the average REE on all subjects was 2027 276 kcal/d. In Fig. 3, the REE against FFM for all individuals as measured by variables obtained during CPX and DXA scanning is depicted. For all participants, the mean daily caloric expenditure (REE Ăž net caloric expenditure from 30 min of exercise) was 2147 216 kcal/d. The projected weight loss for a given time period that is expected to occur in individuals following a strict weightloss prescription based on national guidelines was estimated using the generated data previously mentioned. For these obese individuals, the projected weight losses that would occur for 1, 3, 6, and 12 months were calculated, assuming 1500, 1200, and 1000 kcal/d diets. Fig. 4 charts the mean projected weight losses that would be expected in the study population. As seen in Fig. 4, after 6 mo of strict compliance to a 1500 kcal/d diet with adherence to 150 min of structured or formal exercise per week, our study population could expect to lose at least 1.5 0.6 kg in 1 mo, 4.4 1.9 kg in 3 mo, 8.8 6.2 kg in 6 mo, and 17.7 7.6 kg in 12 mo.
Discussion According to this study, modest weight loss should be achievable by morbidly obese individuals who adhere to minimum recommended weight loss guidelines. Unlike previous studies that rely heavily on weight or BMI-based predictive models, this study used DXA scanning coupled with CPX testing to indirectly measure REE and physical activity energy expenditure in this morbidly obese population. In clinical practice, measurement of BMD for osteoporosis screening is still the most widely used application of DXA
Fig. 3. Resting energy expenditure vs. fat-free mass. Journal of Clinical Densitometry
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Fig. 4. Mean projected weight loss of participants engaging in 150 min/wk of exercise on a restricted caloric intake diet. technology (19). However, there are many other useful clinical and research applications of this technology, such as measuring soft-tissue composition as used in this study (20). Measuring body composition by DXA has been validated as a precise, easy, fast, and safe method of determining fat mass, fat-free mass, and bone mass with minimal exposure to radiation. The DXA measurements are useful in many different populations including pediatric, adult, and those with specific medical conditions (i.e., obesity and human immunodeficiency virus-lipodystrophy). A recent review outlines many of the applications of DXA technology in clinical medicine, including endocrine, nutritional disorders, and metabolic disorders (20). For example among the obese, DXA can be used to assess the degree, variety, and morphology of body adiposity, thereby providing prognostic information associated with comorbidities that are otherwise missed using previous methods of body composition assessment (2). As a result, many physicians, nutrition specialists, and allied healthcare professionals are incorporating DXA technology into clinical practice to obtain precise information on body composition to direct treatment, monitor therapy, and assess the effectiveness of interventions such as weight loss (21). In this study, we used DXA to estimate the energy expenditure of a morbidly obese population, thus increasing accuracy of traditional methods involving weight or BMI-based calculations. The obesity conducive environment of modern society has created a pandemic of cardiovascular, pulmonary, and metabolic diseases (2). Our DXA and CPX-derived calculations project a mean weight loss of 7% (8.8 6.2 kg) of initial weight for a 6-mo time period in morbidly obese individuals following these physical activity and dietary guidelines. If these calculations hold true, the associated weight loss should clearly improve health and cardiorespiratory fitness in this population. To date, 3 clinically relevant, randomized controlled trials have been conducted, all sponsored by Weight Volume 9, 2006
442 Watchers (22e24). Two of these trials reported an average weight loss of w 5% after 3e6 months in individuals who completed the program (22e24). In these two trials, other than attendance, compliance with weight loss recommendations was not measured. It is difficult to compare our findings with the results of these studies, because the exact dietary intake of participants was not recorded. However, it is assumed that on the Weight Watcher’s diet the daily caloric intake is approximately 1500 kcal/d (22). Conversely, individuals in our model with strict dietary compliance who engaged in 150 min/wk of physical activity should lose approximately 7% of their body weight after 6 months. A recent study compared the effectiveness of Atkins, Zone, Weight Watchers, and Ornish diets in overweight individuals for 6 mo to 1 yr (25). This trial demonstrated similar weight reduction across all 4 diets with a range of 3.2 to 3.6 kg lost after 6 mo and 2.1 to 3.3 kg retained losses after 1 yr (25). Previous studies of the overweight and mildly obese generally reported consistent mean weight reductions of ! 4 kg for 6e12 mo (26). Most of these programs did not feature exercise as a major component; none used the combination of DXA and cardiorespiratory fitness testing to project realistic weight loss reductions (8). Thus, our data suggest that programs combining caloric restriction and structured exercise could increase the projected weight loss by 25e50%. Although randomized controlled trials of commercial weight loss programs are limited, several case series are available. Tsai et al. (27) in a systematic review concluded that evidence to support the use of the major commercial and selfhelp weight loss programs is lacking. Two of the published case series included in this review used a meal replacement (OPTIFAST, Novartis Nutrition Corporation, Minneapolis, MN) weight-reduction program. Collectively, these reports suggest that individuals who completed the meal replacement diet consisting of shakes and bars in place of food could expect to lose 15% to 25% of their initial weight after 3 to 6 mo and maintain 8% to 9% of weight loss after 1 yr of treatment (27). Our findings predict a mean weight reduction of 7% after 6 months compared with the 15% to 25% reduction observed with these reports. This discrepancy may be due to some key differences between our weight loss model and the program used by these meal replacement studies. Our model was patterned after national recommendations or more popular weight loss diets, such as Weight Watchers with a caloric restriction of 1500 kcal/d (5e7,22,25). Conversely, meal replacement programs allow fewer calories per day as compared with national recommendations. Another key difference was the degree of obesity of participants. The mean BMI of both meal replacement study groups who use OPTIFAST was w 38 kg/m2, compared with a mean BMI of 48 kg/m2 for our obese population. Finally, Tsai et al. (27) urged caution when interpreting case series reports such as these meal replacement studies, as these are considered ‘‘best-case scenarios’’ for losing weight. Clearly, programs with more severe caloric restriction have higher rates of noncompliance and dropout. Tsai et al. (27) reported that the dropout rates within these two case Journal of Clinical Densitometry
Vanhecke et al. series were 45% and 56% after 6 mo. For weight loss recommendations to be effective, program participants must have reachable goals and realistic expectations. Recent observations by Slentz et al. (28) suggest that despite changes in diet, increased activity is necessary for weight maintenance and that the caloric imbalance in overweight subjects can often be reversed by just 30 min of walking every day. The present findings suggest that this would be clearly sufficient for weight maintenance in a morbidly obese population and would actually induce substantial weight loss (28). On the other hand, Slentz et al.’s (28) subjects were overweight to obese (mean: BMI, 29.7 kg/m2) as compared with our morbidly obese cohort (mean: BMI, 48.2 kg/m2), and their methodology did not estimate caloric expenditure during structured physical activity. Several studies assert that physical activity and exercise do more for weight loss and that regular exercise and physical activity maintain a higher level of REE once an individual starts losing weight because they maintain FFM (29). A limitation of our study with the present model is that we were unable to predict serial changes in REE that may occur with weight loss. Although some reports assert that the reason why weight loss is difficult in obese subjects and why formerly obese subjects are prone to regain weight is because REE decreases with weight loss (30e32). Others refute this notion and suggest noncompliance as the primary reason for these outcomes (33,34). Moreover, even if the REE decreased slightly with a modest weight loss, it could be compensated for by very light to light activity bouts throughout the day, at least in part, or an increased duration of structured exercise (i.e., beyond 30 min/d), or both. Finally, because low fitness is an independent predictor of mortality in normal weight, overweight, and obese individuals, physicians and allied health professionals should encourage their patients to incorporate structured exercise or increased lifestyle activity, or both, as part of a weight-reduction regimen (35,36). Undoubtedly, more research is needed to determine why discrepancies exist between projected weight loss in morbidly obese adults and what is commonly reported in clinical trials. Obesity may be a self-sustaining condition, making substantial weight loss through conventional measures (i.e., diet/exercise) extremely difficult. Future research should focus on long-term alterations, if any, in REE, and its contribution (or impediment) to weight loss in morbidly obese adults. There are several limitations to this study. Given our small study population, these results should be considered preliminary at best. Moreover, our small study sample precludes analysis of different subsets including gender and the overrepresentation of women in our study population may have influenced our results. Performing DXA scans to measure body composition in the morbidly obese can be challenging. Unlike the DXA scanner used in this study, many older DXA scanners or those marketed primarily for use in measuring BMD are unable to accommodate extremely obese patients who exceed the weight limit or are too wide to fit under the scanner area (37). Commercial manufacturers of DXA scanners now offer models that are more accommodating for the very obese Volume 9, 2006
Caloric Expenditure in the Morbidly Obese Using DXA (38). Obese individuals often have other comorbidities, such as chronic back pain, pulmonary impairments, or other comorbid conditions that prevent them from lying still while supine as required by the scan. However, some of these limitations can be overcome with several innovative approaches as outlined in a recent review (37). For example, extrapolating data from one or two half-body scans in an extremely obese individual who is unable to fit within the scan boundary is one solution (37). Finally, hardware type, software, body thickness, and scan mode affect the reliability of DXA to measure body composition (38). We did not validate the reliability or accuracy of our DXA measurements in this study, thereby limiting the accuracy and reproducibility of our study results.
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9. 10. 11.
12.
13.
Conclusions According to our findings, weight loss recommendations of 150 min of moderate intensity of exercise per week and a dietary restriction of 1500 kcal/d, if sustained, should clearly induce a modest weight loss in the morbidly obese. According to current predictive models, morbidly obese individuals would lose w 7% of initial weight after 6 mo of following these recommendations. Considerably more aggressive dietary and exercise targets or very long periods of time would be needed for normalization of body weight in the morbidly obese given these projections. Controlled trials in the morbidly obese population are needed to determine the optimal ‘‘weight-loss prescription’’ required to adequately treat obesity and to achieve these derived weight-loss goals.
14.
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References 1. Vasan RS, Pencina MJ, Cobain M, Freiberg MS, D’Agostino RB. 2005 Estimated risks for developing obesity in the Framingham Heart Study. Ann Intern Med 143:473e480. 2. Mokdad AH, Marks JS, Stroup DF, Gerberding JL. 2004 Actual causes of death in the United States, 2000. JAMA 291: 1238e1245. 3. Serdula MK, Mokdad AH, Williamson DF, Galuska DA, Mendlein JM, Heath GW. 1999 Prevalence of attempting weight loss and strategies for controlling weight. JAMA 282:1353e1358. 4. Bish CL, Blanck HM, Serdula MK, Marcus M, Kohl HW, Khan LK. 2005 Diet and physical activity behaviors of Americans trying to lose weight: 2000 behavioral risk factor surveillance system. Obes Res 13:596e607. 5. National Heart, Lung, and Blood Institute and National Institute of Diabetes and Digestive and Kidney Diseases. 1998 Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adultsdThe Evidence Report, National Institutes of Health. Bethesda, MD. 6. Institute of Medicine. 2002 Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein, and amino acids, National Academies Press: Washington, DC. 7. Jakicic JM, Clark K, Coleman E, et al. 2001 American College of Sports Medicine position stand. Appropriate intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc 33:2145e2156. 8. Yanovski SZ, Bain RP, Williamson DF. 1999 Report of a National Institutes of Health-Centers for Disease Control and Prevention workshop on the feasibility of conducting randomized clinical trial to estimate the long-term health effects of Journal of Clinical Densitometry
18. 19. 20. 21. 22. 23. 24.
25.
26.
intentional weight loss in obese persons. Am J Clin Nutr 69: 366e372. Frankenfield DC, Muth Er, Rowe WA. 1998 The Harris-Benedict studies of human basal metabolism: History and limitations. American Dietetic Association. J Am Diet Assoc 98:439e445. Foster GD, McGuckin BG. 2001 Estimating resting energy expenditure in obesity. Obes Res 9:367Se372S. Heymsfield SB, Gallagher D, Kotler DP, Wang Z, Allison DB, Heshka S. 2002 Body-size dependence of resting energy expenditure can be attributed to nonenergetic homogeneity of fat-free mass. Am J Physiol Endocrinol Metab 282:132e138. Wang Z, Heshka S, Gallagher D, Boozer CN, Kotler DP, Heymsfield SB. 2000 Resting energy expenditure-fat-free mass relationship: new insights provided by body composition modeling. AJP eEndo 279:539e545. Kistorp CN, Toubro S, Astrup A, Svendsen OL. 2000 Measurements of body composition by dual-energy x-ray absorptiometry improve prediction of energy expenditure. Ann NY Acad Sci 904:79e84. Muller MJ, Bosy-Westphal A, Klaus S, et al. 2004 World Health Organization equations have shortcomings for predicting resting energy expenditure in persons from a modern, affluent population: generation of a new reference standard from a retrospective analysis of German database of resting energy expenditure. Am J Clin Nutr 80:1379e1390. American College of Sports Medicine. 2005 The ACSM guidelines for exercise testing and prescription, 7th ed. Metabolic Calculations. Lippincott Williams & Wilkins, New York. Appendix D, 287. Gallagher MJ, Franklin BF, Ehrman JK, Keteyian SJ, Brawner CA, deJong AT, McCullough PA. 2005 Comparative impact of morbid obesity vs heart failure on cardiorespiratory fitness. Chest 127:2197e2203. Svendsen OL, Haarbo J, Hassager C, Christiansen C. 1993 Accuracy of measurements of body composition by dual energy x-ray absorptiometry in vivo. Am J Clin Nutr 57:605. Kiebzak GM, Leamy LJ, Pierson LM, Nord RH, Zhang ZY. 2000 Measurement precision of body composition variables using the Lunar DPX-L Densitometer. J Clin Densitom 3:35e41. Miller PD, Zapalowski C, Kulack CA, Bilezikian JP. 1999 Bone densitometry: the best way to detect and to monitor therapy. J Clin Endocrinol Metab 84:1867e1871. Albanese CV, Diessel E, Genant HK. 2003 Clinical applications of body composition measurements using DXA. J Clin Densitom 6:75e85. Nakata Y, Tanaka K, Mizuki T, Yoshida T. 2004 Body composition measurements by dual-energy x-ray absorptiometry differ between two analysis modes. J Clin Densitom 7:443e447. Heshka S, Anderson JW, Atkinson RL, et al. 2003 Weight loss with self-help compared with a structured commercial program: a randomized trial. JAMA 289:1792e1798. Anderson JW, Brinkman-Kaplan VL, Lee H, Wood CL. 1994 Relationship of weight loss to cardiovascular risk factors in morbidly obese individuals. J Am Coll Nutr 13:256e261. Anderson JW, Hamilton CC, Crown-Weber E, Riddlemoser M, Gustafson NJ. 1991 Safety and efficacy of a multidisciplinary very-low-calorie diet program for selected obese individuals. J Am Diet Assoc 91:1582e1584. Dansinger ML, Gleason JA, Griffith JL, Selker HP, Schaefer EJ. 2005 Comparison of the Atkins, Ornish, Weight Watchers and Zone diets for weight loss and heart disease risk reduction. JAMA 293:43e53. Anderson JW, Konz EC, Frederich RC, Wood CL. 2001 Longterm weight-loss maintenance: a meta-analysis of US studies. Am J Clin Nutr 74:579e584.
Volume 9, 2006
444 27. Tsai AG, Wadden TA. 2005 Systematic review: an evaluation of major commercial weight loss programs in the United States. Ann Intern Med 142:56e66. 28. Slentz CA, Duscha BD, Johnson JL, et al. 2004 Effects of the amount of exercise on body weight, body composition, and measures of central obesity. Arch Intern Med 164:31e39. 29. Weinsier RL, Nagy TR, Hunter GR, Darnell BE, Hensrud DD, Weiss HL. 2000 Do adaptive changes in metabolic rate favor weight regain in weight-reduced individuals? An examination of the set-point theory. Am J Clin Nutr 72:1088e1094. 30. Wyatt HR, Grunwald GK, Seagle HM, et al. 1999 Resting energy expenditure in reduced-obese subjects in the national weight control registry. Am J Clin Nutr 69:1189e1193. 31. Thompson JL, Manore MM, Thomas JR. 1996 Effects of diet and diet-plus-exercise programs on resting metabolic rate: a meta-analysis. Int J Sport Nutr 6:41e46. 32. Ravussin E, Lillioja S, Knowler WC, et al. 1988 Reduced rate of energy expenditure as a risk factor for body-weight gain. N Engl J Med 318:467e472.
Journal of Clinical Densitometry
Vanhecke et al. 33. Das SK, Roberts SB, McCrory Ma, et al. 2003 Long-term changes in energy expenditure and body composition after massive weight loss induced by gastric bypass surgery. Am J Clin Nutr 78:22e30. 34. Connolly J, Romano R, Patruno M. 1999 Selections from current literature: effects of dieting and exercise on resting metabolic rate and implications for weight management. Fam Pract 16:196e201. 35. Barlow CE, Kohl HW III, Gibbons LW, Blair SN. 1995 Physical fitness, mortality and obesity. Int J Obes Relat Metab Disord 19(Supp 14):S41eS44. 36. Wei M, Kampert JB, Barlow CE, et al. 1999 Relationship between low cardiorespiratory fitness and mortality in normalweight, overweight, and obese men. JAMA 282:1547e1553. 37. Brownbill RA, Ilich JZ. 2005 Measuring body composition in overweight individuals by dual energy x-ray absorptiometry. BMC Medical Imaging 5:1e7. 38. Cordero-MacIntyre ZR, Peters W, Libanati CR, Espana RC, Abila SO, Howell WH, Lohman TG. 2002 Reproducibility of DXA in obese women. J Clin Densitom 5:35e44.
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