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Published online in Wiley Online Library (wileyonlinelibrary.com) ORIGINAL ARTICLE Caloric restriction and aerobic exercise in sarcopenic and non-sarcopenic obese women: an observational and retrospective
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Published online in Wiley Online Library (wileyonlinelibrary.com) ORIGINAL ARTICLE Caloric restriction and aerobic exercise in sarcopenic and non-sarcopenic obese women: an observational and retrospective study Sébastien Barbat-Artigas 1,2, Sophie Garnier 3, Sandra Joffroy 3, Éléonor Riesco 4, Frédéric Sanguignol 5, Bruno Vellas 6,7, Yves Rolland 6,7, Sandrine Andrieu 7,8, Mylène Aubertin-Leheudre 2,9,10 & Pascale Mauriège 11 * 1 Département de Biologie, Université du Québec À Montréal, Montréal, Canada; 2 Groupe de Recherche en Activité Physique Adaptée, Université du Québec À Montréal, Montréal, Canada; 3 Faculty of Sport Sciences and Human Kinetics, Université P. Sabatier, Toulouse, France; 4 University of Sherbrooke, and Research Center on Aging CSSS- IUGS Sherbrooke, Canada; 5 Clinique du Château de Vernhes, Bondigoux, France; 6 Service de Médecine Interne et de Gérontologie Clinique, Gérontopôle de Toulouse, Hôpital La Grave-Casselardit, Toulouse, France; 7 Unité Inserm 1027 Faculté de Médecine de Toulouse Toulouse, France; 8 Department of Epidemiology and Public Health and Gerontopole, Department of Geriatric Medicine, Toulouse University Hospital, Toulouse, France; 9 Département de Kinanthropologie, Université du Québec À Montréal, Montréal, Canada; 10 Centre de Recherche de l Institut Universitaire de Gériatrie de Montréal (CRIUGM), Montréal, Canada; 11 Department of Kinesiology, Université Laval, Québec, Canada Abstract Background Sarcopenic obese (SO) individuals are a unique subset of subjects that combines obesity and sarcopenia. Traditional weight loss programmes including aerobic exercises may worsen their condition by further reducing their lean mass. The objective of this observational and retrospective study was to verify the effect of a mixed weight loss programme combining caloric restriction and exercise on body composition, and lipid-lipoprotein profile of obese women according to their sarcopenic status. Methods One hundred and forty-six obese women (body mass index 30 kg/m 2 and fat mass 40%) participated to the 3 week usual and institutionalized weight-reducing programme combining a dietary plan (1400 ± 200 kcal/day) and aerobic exercise (1 h/day, 6 days/week) of a specialized medical institution. The lean body mass index (LMI; lean mass/height 2 ) was calculated, and women in the lowest tertile of LMI were considered SO. Results At baseline, SO women were older, and their body weight and LMI were lower than non-sarcopenic obese (N-SO) women (p 0.05). N-SO and SO women similarly lost fat mass and improved their lipid-lipoprotein profile (p 0.05), while differences in LMI between groups persisted at the end of the weight-reducing programme. Indeed, N-SO women lost lean mass (p 0.05) while SO did not. Conclusions These findings suggest that a short weight loss programme combining caloric restriction and aerobic exercise may significantly reduce fat mass and improve lipid-lipoprotein profile in obese women, independently of their sarcopenic status. Such programmes may have deleterious effects on lean mass in N-SO subjects, only. Keywords Lean body mass; Aerobic exercise; Diet; Lipid-lipoprotein profile Received: 25 September 2014; Revised: 13 August 2015; Accepted: 1 September 2015 *Correspondence to: Pascale Mauriège, Department of Kinesiology, Faculty of Medicine, Laval University, PEPS, local 0290C, G1V 0A6 Québec, Canada: Tel: (418) ext 7268, Fax: (418) , Introduction As the prevalence of obesity increases dramatically, weight gain has become a major public health issue. Accordingly, 66.3% of adults in the United States are currently overweight and 35.5% are obese. 1 Similarly, 47.3% of French people aged 18 and over are overweight, and 15% of them are obese. 2 Obesity, mainly because of an increased visceral adipose tissue accumulation, was shown to be a predisposing factor of metabolic syndrome, cardiovascular diseases, type 2 diabetes, some cancers, and functional impairments. 3 5 Furthermore, obesity is known to reduce the length of life of 2015 The Authors. Journal of Cachexia, Sarcopenia and Muscle published by John Wiley & Sons Ltd on behalf of the Society of Sarcopenia, Cachexia and Wasting Disorders This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. 2 S. Barbat-Artigas et al. severely obese individuals by an estimated 5 to 20 years 6 and is suggested to negatively affect the future life expectancy of the population. 7 Diet, aerobic exercise, and especially the combination of both, are considered the cornerstone of obesity management. 8 In France, 3 week weight loss programmes are available for overweight or obese individuals, once a year, by medical prescription. This 3 week period corresponds to the one covered by the French Medical Health Care System. These interventions developed by weight-loss centres and under medical supervision consist in modifying eating and physical activity habits and include psychological counselling. Physical activity usually includes aerobic exercises known to be more effective to reduce visceral fat, 9 but not necessarily resistance exercises, as the main objective of weight-reducing programmes focuses on weight loss rather than on increasing lean mass. Participants entering these programmes usually lose weight, but little is known on body composition and metabolic risk profile changes. Sarcopenic obese (SO) individuals are a unique population that combines high fat mass and low muscle mass, both conditions being frequently observed with ageing. 10 SO individuals are exposed to greater risks for poor health-related outcomes (such as the cardiometabolic syndrome) and disability than individuals presenting either obesity or sarcopenia alone Even more than obese, SO individuals would benefit from a weight loss programme. However, treating all obese individuals with a one-size fits all approach may be counterproductive, as the weight loss observed in weight-reducing programmes is usually because of losses of both fat mass and lean mass, which is susceptible to worsen the condition of SO individuals. 14 Yet, even when performed in a medical context, weight loss programmes do not include a systematic detection of sarcopenic individuals. The need to differentiate subgroups of obesity has already been illustrated by the example of the metabolically healthy but obese (MHO) individuals. Indeed, MHO exhibited cardioprotective traits despite having high levels of body adiposity. 15 However, programmes designed to improve their physical fitness have deteriorated their metabolic profile. 16,17 Therefore, the main objective of this observational and retrospective study was to verify the effect of a short mixed weight loss programme (combining a dietary plan and aerobic activities) routinely performed in a medical institution, on the body composition and metabolic risk profile of obese women according to their sarcopenic status. Methods Study population These secondary analyses were conducted from retrospective data obtained in 146 obese women (BMI 30 kg/m 2 and fat mass 40 %) referred by their personal physician to participate in a non-randomized short mixed weight-reducing programme at the Clinique du Château de Vernhes (Bondigoux, France) covered by the French Medical Health Care System As patients are subjected to the routine assays performed during the 3 week they spent at the Clinique du Château de Vernhes (i.e. anthropometry and body composition, lipid-lipoprotein, and haemodynamic measures), they only gave their written informed consent to the use of data collected. Thus, because of this specific design, this study could not be defined as a clinical trial per se but as a retrospective one. None of the women had identified disease (e.g. cardiomyopathy; endocrine disorders, which may cause irregular menstrual cycles; or orthopaedic limitations that could affect physical activity). Women on medication that could influence outcome mainly β-blockers, sympathomimetic drugs, cholesterol-lowering drugs (including statins), antihypertensive drugs, and thyroxin, for which a dosage change occurred during the previous 6 months or was expected during the course of the institutionalized weightreducing programme were excluded from this observational and retrospective study. Premenopausal women using oral contraceptives and postmenopausal women on hormone therapy were also excluded. All women were sedentary (exercising no more than 30 min per week). The study was approved by the Local Ethical Committee of the Clinique du Château de Vernhes (Bondigoux, France). Weight-reducing programme The institutionalized weight-reducing programme combined dietary and physical activity instructions and psychological counselling 6 days/week, during 3 weeks. This short duration corresponded to the period covered by the French Medical Health Care System. During this period, all women had four meals per day (breakfast, lunch, snack, and dinner), and received a standardized dietary plan estimated as 1400 ± 200 kcal/day (mean ± standard deviation, SD) according to patients usual caloric intake and hunger. The dietary plan was composed of 20 25% proteins, 25 30% lipids (saturated fatty acids being one third of total fatty acids), and 50 55% carbohydrates; no alcohol was allowed. Participants also followed a personalized physical training programme with cycle ergometer and walking 1 h/day, 6 days a week, for 3 weeks. The detailed physical training programme was previously described Subjects heart rate (HR) was continuously monitored using a cardiofrequencemeter (Polar, FS1 type, Kempele, Finland), and intensity of exercise was set at 50% of their hypothetical maximal HR calculated from the following equation: 220 age, where age is expressed in years. This intensity was fixed by the medical staff for safety reasons, and physical activity was performed under the supervision of medical staff. Weight-reducing programme and sarcopenic obesity 3 Anthropometry and body composition Body weight was measured to the nearest 0.1 kg using an electronic scale. Height was determined to the nearest 0.5 cm at head level, using a tape measure fixed to the wall. Fat mass and lean mass were measured by a standard electric bioimpedance technique (Bodystat 1500, Isle of Man, UK) Measurements were performed in the early morning after an overnight fast, with participants lying down for 10 to 15 min prior to the measurement. The measurement of total body water by the Bodystat 1500 has been validated against tritium dilution techniques. 21 According to the European Working Group on Sarcopenia in Older People, 22 electric bioimpedance is suitable for research and clinical settings as measurements, under standard conditions, were highly correlated with MRI predictions. Anthropometric and body composition measures were repeated twice and then averaged. Lean body mass index (LMI; kg/m 2 ) was calculated by dividing total lean mass (kg) by height squared (m 2 ). In the absence of threshold of sarcopenia with this method, women showing the lowest tertile of LMI (n = 50) were considered as SO, as previously reported when using bioelectrical impedance analysis, 23 and compared to women with the highest tertile considered as non-sarcopenic obese (N-SO; n = 50). Lipid-lipoprotein and haemodynamic profiles Blood samples were collected by the same nurse after a 12 h overnight fast and a 15 min rest period, during which patients were in a semi-recumbent position; patients had to remain inactive for 60 h before blood sampling to eliminate any acute effect of exercise on metabolic profile. Serum samples were stored at 80 C until use, and samples from each subject were analysed within a simple batch to minimize analytic variations. Fasting cholesterol, triacylglycerol, and high-density lipoprotein (HDL)-cholesterol levels were determined according to standardized laboratory procedures on a COBA MIRA PLUS automate (Roche Diagnostics). Fasting low-density lipoprotein (LDL)-cholesterol concentrations were estimated using the Friedewald equation. 24 Resting systolic and diastolic blood pressure (BP) were taken when subjects were lying down, with both arms relaxed and supported, after a rest period of at least 10 min, using an automated BP ambulatory unit (NAIS, Blood Pressure Unit). 18 Systolic and diastolic BP measurements were taken twice, at 5 min intervals, and the mean of the two measurements was used. Statistical analysis Data are expressed as the mean ± SD. A non-paired Student s t-test was used for the comparison between groups (N-SO vs. SO), at baseline and at the end of the 3 week programme. An analysis of variance (ANOVA) with repeated measures was used to detect changes in response to the treatment condition (pre- vs. post-weight reducing programme) and between groups. Analyses were performed using SPSS 17.0 (Chicago, IL). A p value of less than 0.05 was considered significant. Results Baseline participants characteristics Participants characteristics before the weight-reducing programme are presented in Table 1. At baseline, SO women were older and had lower body weight, BMI, and LMI than N-SO women (p 0.05). No between group-difference was observed regarding the lipid-lipoprotein and haemodynamic profiles. Effects of the weight-reducing programme Because of age differences at baseline, ANOVA was controlled for this variable. Body weight, BMI, and fat mass decreased in both N-SO and SO women (p 0.05) in response to the weight-reducing programme. LMI significantly decreased in N-SO subjects ( 1.8 ± 4.6%, p 0.01) but not in SO women ( 0.5 ± 2.1%, p = 0.11). Total cholesterol, HDL- and LDLcholesterol levels, as well as systolic BP decreased in both groups (p 0.05). Significant weight-reducing effect group interactions were observed for body weight, BMI, and LMI. Relative changes in BMI, LMI, and fat mass are shown in Figure 1. Alternative statistical analysis Furthermore, as the body weight difference between groups may not be entirely because of differences in lean mass, ANOVA controlling for age and fat mass was also performed. However, results were similar to those obtained after control for age only (not shown). Because postmenopausal women were more numerous in the SO than in the N-SO group (probably because SO women were older than N-SO ones), we also performed statistical analysis controlling for menopausal status instead of age, and found similar results. Finally no significant weightreducing effect menopausal status interaction was observed. Therefore, we did not decide to include menopausal status as a confounding factor, in our analyses. Discussion To the best of our knowledge, these are the first retrospective analyses to report the effects of a short institutionalized weight-reducing programme combining a dietary plan and aerobic exercise on the body composition and metabolic risk 4 S. Barbat-Artigas et al. Table 1 Variables before and after the mixed weight-reducing programme All (n = 146) N-SO (n = 50) SO (n = 50) Variable Pre Post Pre Post Pre Post Age (years) 53 ± 9 51 ± ± 6 a Postmenopausal (%) a Height (cm) ± ± ± 6.2 Weight (kg) 92.7 ± ± 11.4 c ± ± 10.6 c 86.3 ± 8.9 a 84.0 ± 8.6 bcd BMI (kg/m 2 ) 35.4 ± ± 3.2 c 37.7 ± ± 3.0 c 33.2 ± 2.4 a 32.3 ± 2.4 bcd Fat mass (%) 47.6 ± ± 3.7 c 47.4 ± ± 3.5 c 48.0 ± ± 3.9 c Lean mass (kg) 48.3 ± ± 5.6 c 52.8 ± ± 5.6 c 44.6 ± 3.2 a 44.4 ± 3.4 bd LMI (kg/m 2 ) 18.5 ± ± 1.3 c 19.8 ± ± 1.2 c 17.2 ± 0.6 a 17.1 ± 0.7 bd Total cholesterol (mmol/l) 2.12 ± ± 0.40 c 2.21 ± ± 0.51 c 2.13 ± ± 0.34 c HDL-cholesterol (mmol/l) 0.52 ± ± 0.13 c 0.53 ± ± 0.11 c 0.53 ± ± 0.11 c LDL-cholesterol (mmol/l) 1.38 ± ± 0.39 c 1.38 ± ± 0.41 c 1.34 ± ± 0.33 c Triacylglycerol (mmol/l) 1.31 ± ± 0.31 c 1.30 ± ± ± ± 0.30 c Systolic BP (mmhg) 129 ± ± 13 c 126 ± ± ± ± 13 c Diastolic BP (mmhg) 75 ± ± 9 74 ± 5 74 ± ± ± 8 Blood analysis was performed on 57 women, 12 of which are in the N-SO group, and 30 in the SO group. BMI: Body mass index; LMI: Lean body mass index; BP: Blood pressure; N-SO: Non-sarcopenic-obese; SO: sarcopenic-obese. a Differences between N-SO and SO at baseline (p 0.05). b Differences between N-SO and SO at the end of the weight-reducing programme (p 0.05). c Weight-reducing effect (p 0.05). d Weight-reducing effect group interaction (p 0.05) after controlling for age. Figure 1 Relative changes (%) in BMI, LMI, and fat mass in nonsarcopenic-obese and sarcopenic-obese women following the mixed weight-reducing programme. Changes were calculated as relative differences between pre and post-weight loss values. BMI: Body mass index; LMI: Lean body mass index. *Differences between non-sarcopenic-obese (n = 50) and sarcopenic-obese (n = 50) women at p 0.05, after control for age differences. profile according to their sarcopenic status. Sarcopenic-obese individuals, even more than N-SO ones, would benefit from a fat mass reduction because negative effects of sarcopenia and obesity are cumulative. However, weight loss is also partially because of a loss of lean mass, which may worsen the condition of sarcopenic individuals whose functional capacity is already impaired by their initially low muscle mass. This issue is even more important as sarcopenic individuals are not screened when entering weight-loss programmes. Separating obese women based on their LMI revealed other morphological differences. Obviously, lean mass was lower in SO than in N-SO patients. This difference in lean mass also contributed to differences observed in total body weight and BMI. Furthermore, that sarcopenic-obese women were older than N-SO ones, is in good accordance with the fact that sarcopenia is an age-related process. However, controlling analysis for these differences did not influence our observations, thus suggesting that the sarcopenic-obese phenotype was not an artefact. Two important points have to be highlighted. First, SO women did not significantly lose lean mass, as reflected by their maintained LMI, in contrast to N-SO ones. Second, SO and N-SO women showed similar fat mass losses and improvements in their lipid-lipoprotein profile. The reason why SO women preserved their LMI is unclear but several factors may have contributed to this observation: (1) one may hypothesize that the intervention was too short to significantly decrease LMI. As illustrated in Figure 1, SO women showed a non-significant decrease of LMI (of 0.5%) that should have been more pronounced with a longer intervention; (2) the dietary plan was rather hyperproteinized, as the 20 25% of proteins reported in the present study is higher than the 15% content recommended by the French Agency for Food Safety for sedentary individuals, and (3) SO women had less muscle to lose, compared with N-SO ones. In our design, the SO group has a lower LMI than the N-SO one. One may thus hypothesize that SO women have a very low muscle mass to perform physical activity and that the physical activity programme (even if composed of aerobic exercises, at a relatively low intensity) was sufficient to maintain their muscle mass above this threshold. As illustrated by the recent systematic review and metaanalysis of Schwingshackl et al., 25 aerobic exercises are more efficient than resistance exercises in reducing body weight, waist circumference, and fat mass in overweight and obese Weight-reducing programme and sarcopenic obesity 5 individuals. This observation is in good accordance with our results and fully justifies the integration of aerobic exercises in weight-loss programmes. However, regarding lean mass, aerobic exercises are well known to be less suitable than resistance ones.
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