Long-term body composition improvement in post-menopausal women following bariatric surgery: a cross-sectional and case–control study

in European Journal of Endocrinology
View More View Less
  • 1 Division of Endocrinology, Diabetology, and Metabolism, Lausanne University Hospital, Lausanne, Switzerland
  • | 2 Center for Primary Care and Public Health (Unisanté), University of Lausanne, Lausanne, Switzerland
  • | 3 Department of Visceral Surgery, Lausanne University Hospital, Lausanne, Switzerland
  • | 4 Department of Surgery, Riviera-Chablais Hospital, Rennaz, Switzerland
  • | 5 Faculty of Biology and medicine, University of Lausanne, Lausanne, Switzerland
  • | 6 Interdisciplinary Center for Bone Diseases, Lausanne University Hospital, Lausanne, Switzerland

Correspondence should be addressed to L Favre; Email: Lucie.Favre@chuv.ch
Open access

Objective

Bariatric surgery (BS) induces loss of body fat mass (FM) with an inexorable loss of lean mass (LM). Menopause leads to deleterious changes in body composition (BC) related to estrogen deficiency including LM loss and increase in total and visceral adipose tissue (VAT). This study aims to describe the long-term weight evolution of post-menopausal women after Roux-en-Y gastric bypass (RYGB) and to compare the BC between BS patients vs post-menopausal non-operated women.

Design

Cross-sectional study of 60 post-menopausal women who underwent RYGB ≥2 years prior to the study with nested case–control design.

Methods

Post-menopausal BS women were matched for age and BMI with controls. Both groups underwent DXA scan, lipids and glucose metabolism markers assessment.

Results

Median follow-up was 7.5 (2–18) years. Percentage of total weight loss (TWL%) was 28.5 ± 10%. After RYGB, LM percentage of body weight (LM%) was positively associated with TWL% and negatively associated with nadir weight. Forty-one post-BS women were age- and BMI-matched with controls. Post-BS patients showed higher LM% (57.7% (±8%) vs 52.5% (±5%), P  = 0.001), reduced FM% (39.4% (±8.4%) vs 45.9% (±5.4%), P  < 0.01) and lower VAT (750.6 g (±496) vs 1295.3 g (±688), P  < 0.01) with no difference in absolute LM compared to controls. While post-BS women showed a better lipid profile compared to controls, no difference was found in glucose markers.

Conclusions

Post-menopausal women after RYGB have a lower FM and VAT, preserved LM and a better lipid profile compared to controls. Weight loss after RYGB seems to have a persistent positive impact on metabolic health.

Abstract

Objective

Bariatric surgery (BS) induces loss of body fat mass (FM) with an inexorable loss of lean mass (LM). Menopause leads to deleterious changes in body composition (BC) related to estrogen deficiency including LM loss and increase in total and visceral adipose tissue (VAT). This study aims to describe the long-term weight evolution of post-menopausal women after Roux-en-Y gastric bypass (RYGB) and to compare the BC between BS patients vs post-menopausal non-operated women.

Design

Cross-sectional study of 60 post-menopausal women who underwent RYGB ≥2 years prior to the study with nested case–control design.

Methods

Post-menopausal BS women were matched for age and BMI with controls. Both groups underwent DXA scan, lipids and glucose metabolism markers assessment.

Results

Median follow-up was 7.5 (2–18) years. Percentage of total weight loss (TWL%) was 28.5 ± 10%. After RYGB, LM percentage of body weight (LM%) was positively associated with TWL% and negatively associated with nadir weight. Forty-one post-BS women were age- and BMI-matched with controls. Post-BS patients showed higher LM% (57.7% (±8%) vs 52.5% (±5%), P  = 0.001), reduced FM% (39.4% (±8.4%) vs 45.9% (±5.4%), P  < 0.01) and lower VAT (750.6 g (±496) vs 1295.3 g (±688), P  < 0.01) with no difference in absolute LM compared to controls. While post-BS women showed a better lipid profile compared to controls, no difference was found in glucose markers.

Conclusions

Post-menopausal women after RYGB have a lower FM and VAT, preserved LM and a better lipid profile compared to controls. Weight loss after RYGB seems to have a persistent positive impact on metabolic health.

Introduction

Obesity is associated with numerous health conditions including cardiovascular disease, diabetes, and several cancers (1). The dramatic worldwide increase of the prevalence of obesity during the last decades has become a major public health problem (2). While lifestyle intervention alone generally fails to achieve sustained long-term weight loss, bariatric surgery (BS) has proven to be an effective therapy for sustained weight loss in severe obesity (3, 4). Roux-en-Y gastric bypass (RYGB) is one of the most commonly performed surgeries worldwide. It is a restrictive and malabsorptive surgery that results in a decrease in body fat mass (FM) including visceral adipose tissue (VAT) and an improvement in metabolic parameters and cardiovascular risk (5). However, it also leads to inexorable loss in lean mass (LM), ranging from 10 to 45% 12 months after RYBG (6, 7, 8, 9, 10, 11, 12, 13, 14, 15). While long-term studies on body composition (BC) after BS are scarce, significant loss in LM during the first 18 months post-RYGB and a tendency for LM stabilization or slight increase afterwards have been reported (6, 15, 16). Loss in LM may have deleterious metabolic consequences. Indeed, LM contributes to insulin-mediated glucose uptake (17), increases resting energy expenditure and high-density lipoprotein cholesterol levels and produces myokines that prevent metabolic deterioration (17, 18). LM is also essential for muscular strength and the body’s functional capacity (19). Thus, counseling for dietary protein and micronutrients intake as well as regular physical activity is part of the long-term treatment for surgical patients in order to limit LM loss (20, 21). Studies comparing BC in RYGB-operated patients vs age- and BMI-matched controls are limited, reporting similar (22, 23) or higher LM in the surgical group (24, 25). So far, no guidelines are available to define the pathological loss of LM during follow-up. Female sex, age and malnutrition are generally considered as risk factors for LM loss (26).

Menopause is characterized by the lack of menstrual cycles for more than a year and occurs at an average age of 50 years (27). It is accompanied by a significant increase in body weight related to estrogen deficiency. In particular, menopause is associated with an increase in FM and a loss of LM (28, 29). The stronger increase in VAT after menopause leads to a shift from a gynoid to an android pattern of fat distribution (28). Recent study indicates that hormone replacement therapy (HRT) improves BC in post-menopausal women (29).

In this study, we aimed first to describe the long-term body weight and metabolic evolution of a post-menopausal cohort with previous RYGB, and secondly, to compare the BC between two post-menopausal populations: bariatric women vs non-operated controls, matched for age and BMI. Herein, we show that post-menopausal women, at least 2 years after RYGB, have a decreased FM% and VAT, conserved LM% and a better lipid profile as compared to controls.

Methods

Study design and participants

This is a cross-sectional descriptive cohort with a nested case–control design. The study was performed in a single academic center, at the Centre Hospitalier Universitaire Vaudois (CHUV) in Lausanne.

BS patients were recruited from the Cohort Obesity of Lausanne (COOL) which is a longitudinal observational cohort established from 2015 for all patients operated at the CHUV since 1999 to investigate long-term effects of BS (30). All bariatric procedures were performed after a complete and multidisciplinary evaluation at CHUV and eligible patients presented with a BMI ≥40 or ≥35 kg/m2 with the presence of at least one comorbidity and failure of conservative treatment for over 2 years (31). Laparoscopic RYGB was performed by the same surgical team by creating a 15 mL gastric pouch, a retrocolic 100–150 cm Roux alimentary limb, a 21-mm circular stapled gastrojejunostomy and a linear stapled jejunostomy. All patients were advised on diet and physical activity and received supplements (daily multivitamin and calcium 1000 mg/vitamin D 800 UI) according to Swiss guidelines on obesity (31). Inclusion criteria were women aged >50 years with one BC analysis by dual-energy X-ray absorptiometry (DXA) at least 2 years post-surgery and persistent amenorrhea for >12 months at the time of the DXA. Finally, as it has previously been reported that nadir weight after RYGB is usually reached between the first and the second year after surgery (3), patients with a follow-up shorter than 2 years after surgery were excluded. Patients with established alcohol dependence after surgery were excluded, possibly impacting the LM. Sixty post-menopausal women were eligible out of 396 (Supplementary Fig. 1, see section on supplementary materials given at the end of this article).

Non-operated controls were selected from OsteoLaus, another local cohort of 1475 post-menopausal women 50 to 80 years, enrolled from general population, which aims to study bone health (32). These controls were enrolled as they had a BC analysis performed in the same DXA device as in the COOL cohort (n = 1234). OsteoLaus data were collected between March 2015 and February 2018.

All participants (operated and controls) were post-menopausal at the time of the DXA and were questioned on current menopausal HRT use. OsteoLaus and COOL studies were approved by the Institutional Ethics Committee of the University of Lausanne, and written informed consent was obtained from all participants.

Study variables

Anthropometric measurements and medical history were collected at the time of the DXA examination for all participants. In operated patients, data were collected before RYGB as well. Participants were weighed barefoot in light clothes (0.2–0.4 kg) with a precision of 0.1 kg. Height was measured with a fixed wall stapediometer with a precision of 0.1 cm. Excess weight was defined as the pre-surgical weight minus ideal body weight (based on a BMI of 25 kg/m2). The % excess weight loss (EWL%) was defined as the pre-surgical weight minus the follow-up weight, divided by excess weight and multiplied by 100. The % total weight loss (TWL%) was defined as the pre-surgical weight minus the follow-up weight divided by the pre-surgical weight and multiplied by 100. Nadir weight was defined as the lowest weight achieved during follow-up.

Weight regain was calculated as the post-operative weight minus the nadir weight divided by the nadir weight and multiplied by 100. Dyslipidemia was defined as the presence of one or more abnormal serum lipid concentrations (LDL >3 mmol/L, triglycerides >2.3 mmol/L) or use of statins (33). The diagnosis of diabetes (type 2 diabetes (T2D)) included glycated haemoglobin (HbA1c) ≥6.5%, fasting glycemia ≥7 mmol/L, a 2-hour glycemia during 75 g oral glucose tolerance test ≥11.1 mmol/L or the use of diabetes medication. T2D remission was defined as an HbA1c level <6.5% and a fasting glucose concentration <7 mmol/L in the absence of any antidiabetic medication.

Standard biological assays were performed in the accredited clinical chemistry laboratory of CHUV. Glucose, HbA1c, insulin, hepatic tests (aspartate transaminase, alanine transaminase, gamma-glutamyl transferase), lipids, thyroid-stimulating hormone, uric acid, albumin and creatinine were measured after an overnight fast in a range of 6 months before or after DXA in both cohorts. Blood tests of controls were used for comparison when available.

BC analysis was assessed in both groups using Lunar iDXA (GE Healthcare) (7). Participants were placed centered on the scanning field in a supine position, with palms down and arms at sides, slightly separated from the trunk. Regions of interest included total body, trunk, android, gynoid, upper limbs and lower limbs. The android region lower boundary was defined at the top of the iliac crest and the upper boundary as 20% of the distance between the pelvis and neck cuts. The upper boundary of the gynoid region was set below the pelvis cut at 1.5× android height. Gynoid height is determined as 2× android region height (34). For each region, total mass, FM and LM were calculated by the Lunar iDXA software. VAT was determined using DXA CoreScan software which has been demonstrated to be highly reliable compared to MRI (35). For the study, total FM and LM, android and gynoid FM and LM and VAT were evaluated. FM and LM were expressed as absolute values and as a percentage of body weight. Three indexes were calculated: appendicular lean mass index (ALMI) was calculated as the ratio of the addition of the four limbs LM (kg) over height (m) squared; lean mass index (LMI) was calculated by dividing LM (kg) by the square of height (m); fat mass index (FMI) was calculated by dividing total FM (kg) by the height (m) squared.

Different definitions have been published for sarcopenia diagnosis, which is consensually defined by a loss of muscle mass and muscle strength. Cut-off values for defining sarcopenia according to ALMI vary between 4.42 and 5.67 kg/m2 in women (36, 37). We used the values below 5.67 kg/m2 to exclude sarcopenia, as previously shown (37).

Statistical analysis

Standard descriptive analyses were used to summarize the study variables (e.g. frequencies and percentages for categorical variables and means ± s.d. for continuous variables).

In order to find the predictors of LM percentage (LM%) and ALMI in the post-RYGB cohort, we examined age, time of follow-up, TWL% and nadir weight as predictor variables using univariable and multivariable linear regressions. In the multivariable model, the variables were centered and we considered an interaction factor between TWL% and nadir weight in addition to the four predictor variables. VAT was compared between participants with and without T2D before RYGB using the Student’s t-test. The same comparison was made by adjusting for FM percentage of total body mass (FM%) using multivariable linear regression. The same analyses were conducted between patients with and without T2D after RYGB.

The patients who underwent RYGB were matched for age and BMI at the time of their BC analysis with non-operated controls at a ratio of 1:1 using the propensity scores. The propensity scores were estimated using a logistic regression. Optimal pair matching was performed using the MatchIt package (38) in the R statistical software. Participants outside the common support region were discarded in analyses comparing the two groups. Continuous and categorical variables were compared between the two groups using Student's t-test and Fisher's exact test, respectively. For continuous variables, adjusted differences for age and BMI were calculated using linear regression.

Results

Description of long-term body weight evolution in the post-menopausal RYBG cohort

In the complete bariatric group (n = 60), mean age was 57 (±5.7) years, median follow-up was 7.5 (2–18) years after RYGB, and mean age at the time of surgery was 48.8 (±6.8) years. The TWL% was 28.48 (±9.97)% and the mean EWL% was 67.46 (±29.24)%. The nadir weight was reached after a mean of 24 (5–162) months. Prevalence of metabolic comorbidities in patients before and after RYGB at follow-up time is shown in Table 1. Remission rate after RYGB for T2D, hypertension and dyslipidemia were 68.7 (n = 11/16), 61.8 (n =21/34) and 68.0% (n =34/50), respectively.

Table 1

Weight evolution of operated patients. Data expressed as mean (s.d.) or median (min–max). TWL, total weight loss defined as the operative weight minus the follow-up weight divided by the operative weight and multiplied by 100. EWL, excess weight loss defined as the operative weight minus the follow-up weight, divided by excess weight and multiplied by 100. Nadir weight defined as the lowest weight achieved during the follow-up.

VariableBefore RYGB (n = 60)Post RYGB (n = 60)
Weight, (kg)117.27 (22.17)83.9 (20)
BMI, (kg/m2)45.92 (7.29)32.9 (7.4)
Follow-up, (years)7.5 (2–18)
Weight loss, (kg)33.4 (14.3)
TWL, (%)28.5 (10)
EWL, (%)67.4 (29.2)
Nadir weight, (kg)73.4 (13.7)
Time of nadir weight, months24 (5–62)
Type 2 diabetes, n (%)16 (26.7)6 (10.0)
Hypertension, n (%)34 (56.7)14 (23.3)
Dyslipidemia, n (%)50 (83.3)16 (26.7)

After RYGB, LM% was positively associated with TWL% and negatively associated with nadir weight, time of follow-up and weight regain using univariable regression (Fig. 1). As LM% was associated with the time of follow-up and possibly influencing body weight evolution, a multiple linear regression model, adjusted for age and time of follow-up was used, showing that LM% was positively correlated with TWL% and negatively associated with nadir weight (Supplementary Table 1). Conversely, ALMI was negatively associated with TWL% and positively associated with nadir weight both in univariable and multiple linear regression analysis (Fig. 2 and Supplementary Table 2). ALMI was also directly associated with the extent of weight regain.

Figure 1
Figure 1

Univariable linear regressions of the association between percentage of lean mass on total body mass (LM%) as outcome variable, and % total weight loss (TWL%) (A), nadir weight (B) time of follow-up (C) and weight regain (D) as predictor variables in the RYGB cohort. R2, Spearman’s coefficient. A full color version of this figure is available at https://doi.org/10.1530/EJE-21-0895.

Citation: European Journal of Endocrinology 186, 2; 10.1530/EJE-21-0895

Figure 2
Figure 2

Univariable linear regressions of the association between appendicular lean mass index (ALMI) as outcome variable and % total weight loss (TWL%) (A), nadir weight (B), time of follow-up (C) and weight regain (D) as predictor variables, in the RYGB cohort. R2, Spearman’s coefficient. A full color version of this figure is available at https://doi.org/10.1530/EJE-21-0895.

Citation: European Journal of Endocrinology 186, 2; 10.1530/EJE-21-0895

Concerning the relationship between VAT and metabolic comorbidities, women with T2D before surgery (n = 16) showed a significantly higher VAT after RYGB compared to operated patients without T2D before surgery (1473 ± 1130 g vs 902 ± 677 g, P = 0.02). Similarly, women with T2D after surgery (n = 6) showed a greater amount of VAT compared to non-diabetic women (1997 ± 1667 g vs 949 ± 657 g, P  < 0.01). These data were confirmed by multivariable analysis after adjusting for FM% (P  = 0.02 and P  < 0.01 for T2D before and after surgery, respectively). No significant difference in VAT was found according to the presence or absence of hypertension and dyslipidemia before and after RYGB (data not shown).

Improved body composition in post-menopausal RYGB women versus age and BMI-matched controls

As the operated patients had a higher BMI and younger age than the controls, we were able to match on an individual basis a subsample of 41 out of the 60 patients from the surgical group to 41 controls (Supplementary Fig. 1). Mean age was 58.4 (±6.2) years vs 59.4 (±3.2) years (P  = 0.4) and mean BMI was 29.6 (±4.9) kg/m2 vs 31.1 (±5.6) kg/m2 (P  = 0.2) in operated patients vs controls, respectively. Two out of 41 post-RYGB women were on HRT vs 8/41 in controls, P  < 0.04 (Table 2).

Table 2

Body composition results of operated patients (post-RYGB) vs controls. Data are expressed as mean (s.d). Comparisons were adjusted for BMI and age (adjusted P-value).

VariablePost-RYGB (n = 41)Controls (n = 41)Raw differenceP -valueAdjusted differenceAdjusted P -value
Age, (years)58.4 (6.2)59.4 (3.2)1 (1.1)NA0.47 (1.0)NA
BMI, (kg/m2m)29.63 (4.99)31.08 (5.65)1.45 (1.2)NA1.02 (1.1)NA
HRT, n (%)2/41 (4.9%)8/41 (19.5%)0.04
Total body mass, (kg)74.7 (11.8)80.6 (14.5)5.9 (2.9)0.052.8 (1.4)0.05
Total FM, (kg)30.9 (9.9)36.52 (10.3)6.4 (2.2)0.0053.9 (0.9)<0.001
Total FM, (%)39.4 (8.4)45.88 (5.3)6.46 (1.6)<0.0014.89 (0.9)<0.001
Total LM, (kg)42.4 (4.7)41.7 (4.8)−0.7 (1.0)0.5−1.3 (0.9)0.18
Total LM, (%)57.7 (8.0)52.5 (5.0)− 5.14 (1.5)<0.001−3.7 (0.9)<0.001
Trunk FM, (kg)14.5 (6.0)19.7 (6.4)5.2 (1.3)<0.0013.7 (0.5)<0.001
Trunk FM, (%)39.4 (11.2)48.4 (7.6)−7.3 (2.3)<0.001−5.9 (1.3)<0.001
Trunk LM, (kg)20.7 (2.4)19.5 (2.2)−1.2 (0.5)0.02− 1.4 (0.5)0.005
Trunk LM, (%)58.8 (10.9)51.6 (7.6)−7.3 (2.2)0.002−5.9 (1.3)<0.001
Android FM, (kg)2.4 (1.2)3.5 (1.3)1.1 (0.3)<0.0010.8 (0.1)<0.001
Android FM, (%)40.8 (12.7)51.5 (9.0)10.8 (2.4)<0.0018.3 (1.5)<0.001
Android LM, (kg)3.2 (0.4)3.1 (0.4)−0.1 (0.9)0.1−0.2 (0.9)0.04
Gynoid FM, (kg)5.0 (1.5)6.1 (1.6)1.1 (0.4)0.0020.7 (0.2)<0.001
Gynoid FM, (%)44.6 (7.5)48.2 (4.9)3.6 (1.4)0.012.4 (1.1)0.03
Gynoid LM, (kg)6.1 (0.8)6.4 (0.8)0.3 (0.2)0.060.3 (0.1)0.1
FMI11.7 (3.9)14.0 (4.0)2.3 (0.9)0.0081.3 (0.2)<0.001
ALMI7.2 (0.9)7.4 (1.0)0.2 (0.2)0.4−0.01 (0.1)0.9
LMI16.4 (1.6)16.0 (1.7)−0.4 (0.4)0.26−0.7 (0.3)0.005
VAT, (g)751 (496)1 295 (688)544 (132)<0.001423 (84)<0.001

P-values <0.05 are displayed in bold.

ALMI, appendicular lean mass index appendicular (lean mass/squared height); FM, fat mass; FMI, fat mass index (fat mass/ squared height); HRT, hormone replacement therapy; LM, lean mass; LMI, lean mass index (lean mass/squared height); NA: not applicable; VAT, visceral adipose tissue.

Post-RYGB women exhibited significantly decreased total FM% (39.4 ± 8.4% vs 45.9 ± 5.4%, P  < 0.01) associated with lower VAT (751 ± 496 g vs 1 295 ± 688 g, P  < 0.001) and android fat (40.8 ± 12.7% vs 51.5 ± 9%, P  < 0.001) as compared to non-operated controls (Fig. 3 and Table 2). Consequently, post-RYGB women had higher LM% (57.7 ± 8% vs 52.5 ± 5%, P  < 0.001). Except for the trunk region, there was no difference in any regional LM. Absolute LM, ALMI and LMI were similar in both groups and none of the post-RYGB women had pathological ALMI, thus ruling out the diagnosis of sarcopenia in this group. When comparisons were further adjusted for BMI and age, LMI and android LM were significantly higher in the operated group compared to the controls.

Figure 3
Figure 3

Differences in % fat mass of total body weight, % lean mass of total body mass and visceral adipose tissue (VAT) in post-RYGB women patients vs controls. Data are expressed as mean ± s.d. Statistical analysis was done using Student’s t-test. *P -value <0.001.

Citation: European Journal of Endocrinology 186, 2; 10.1530/EJE-21-0895

Improved lipid profile in post-menopausal women after RYGB vs age and BMI-matched controls

Post-RYGB women showed a better lipid profile compared to controls (total cholesterol 4.8 ± 0.9 mmol/L vs 5.5 ± 0.9 mmol/L, P  < 0.001; LDL 2.4 ± 0.8 mmol/L vs 3.4 ± 0.8 mmol/L, P  < 0.001; HDL 1.9 ± 0.4 mmol/L vs 1.6±0.4 mmol/L P  = 0.008) with a reduced prevalence of dyslipidemia (P  = 0.02). No significant difference was found in the prevalence of T2D between the two groups (Table 3). Fasting glucose levels and Homeostatic Model Assessment for Insulin Resistance were similar between groups.

Table 3

Clinical parameters of post-RYGB patients and non-operated controls.

VariablePost-RYGB (n = 41)Controls (n = 41)P -value
Glucose, (mmol/L)5.2 (0.9)5.4 (1.1)0.3
Insulin, (mmol/L)7.5 (4.5)12.1 (10.6)0.06
HOMA-IR1.7 (1.1)3.1 (3.6)0.07
Uric acid, (µmol/L)264.3 (64.8)289.8 (62.7)0.08
Total cholesterol, (mmol/L)4.8 (0.9)5.5 (0.9)<0.001
LDL, (mmol/L)2.4 (0.8)3.4 (0.8)<0.001
HDL, (mmol/L)1.9 (0.4)1.6 (0.4)0.008
Triglycerides, (mmol/L)1.2 (0.5)1.2 (0.4)0.1
TSH, (mU/L)2.6 (1.2)2.9 (1.3)0.4
Albumin, (g/L)42.8 (3.9)42.5 (2.4)0.7
Creatinine, (µmol/L)65.1 (15.7)70.1 (8.8)0.08
AST, (U/L)25.9 (7.4)22.1 (5.9)0.02
ALT, (U/L)25.8 (9.5)23.9 (9.2)0.4
γGT, (U/L)19.6 (10.5)24.7 (22.2)0.2
Type 2 diabetes, n (%)3/39 (7.7)3/39 (7.7)1
Hypertension, n (%)10/39 (25.6)14/39 (35.9)0.46
Dyslipidemia, n (%)13/39 (33.3)24/39 (61.5)0.02

Data expressed as mean (s.d). P -values <0.05 are displayed in bold.

ALT, alanine transaminase; AST, aspartate transaminase; HDL, high density lipoprotein; HOMA-IR, homeostatic model assessment for insulin resistance; LDL, low density lipoprotein, TSH, thyroid-stimulating hormone; γGT, gamma-glutamyl transferase.

Discussion

The results of the present study indicate a favorable long-term BC after RYGB in post-menopausal women. Indeed, we demonstrated decreased FM percentage and VAT content and conserved LM in operated women as compared to age- and BMI-matched controls. This is an important finding as the majority of the patients who undergo BS are women. To date, no other study has specifically investigated the changes in BC after BS in post-menopausal patients. However, two studies with slightly younger populations investigating the changes in BC after RYGB in both males and females also showed higher LM% and reduced FM% 2 years following surgery vs BMI-, age- and sex-matched controls (24, 25). Yet, the menopausal status was not reported. Other studies with similar design found no significant difference in BC between groups (22, 23, 39). Differing methodologies (DXA, bioimpedance and plethysmography) could account for the inconsistent results (22, 25); bioimpedance being affected by hydration and plethysmography leading to an underestimate of FM in obesity (40). In addition, the wide range of follow-up interval for RYBG from 12 months (23) to 2–5 years (22, 24, 25) could also influence the results, as also shown in the present study (Figs 1 and 2). The difference found in FM and VAT are partially consistent with a previous study, which reported similar results with VAT, but not with other body fat measurements (41).

This study demonstrated that absolute LM value, LMI and ALMI were not significantly different between operated vs non-operated women. BMI was not significantly different between the two groups. However, as the mean difference in BMI was 1.5 point and 1 year in age, all comparison in BC compartments were further adjusted for BMI and age. After adjustment, all results were confirmed and we found that LMI was significantly higher in post-RYGB patients.

Thus, it was important and unexpected to show the positive effects of RYGB on LM preservation in post-menopausal patients, as post-menopausal bariatric populations might present multiple risk factors for LM loss and sarcopenia including low estrogen, age, physical inactivity, low protein intake and hypovitaminosis D (42). Existing literature on the effect of HRT on BC is controversial, showing either absence or a beneficial effect on BC. Recent data from the large OsteoLaus cohort demonstrated that HRT was associated with reduced android and visceral FM with no benefit on LM (29). In the present study, despite a higher prevalence of HRT, the control group showed a greater amount of FM, android FM and VAT. Thus, we do not believe that HRT represents a confounding factor that could affect BC results.

As LM is inversely related to factors associated with cardiovascular risk (17) and VAT expansion increases cardiometabolic risk (43), we can postulate that improved BC after RYGB could protect these patients in the long-term against metabolic and cardiovascular complications (44). Moreover, LM is the main determinant of basal metabolism (19) and it contributes to long-term preservation of body weight. The beneficial effect of RYGB on metabolic parameters was also shown herein by the significant remission rates for T2D, hypertension and dyslipidemia after surgery in the operated group. We described a higher VAT in operated women with T2D at the time of surgery as compared to non-diabetic. Previous studies reported that diabetic patients have greater amount of VAT before surgery compared to normoglycemic subjects (7). These data highlight the association between fat distribution and T2D, even later after surgery, via the well-known lipolytic and pro-inflammatory profile of the VAT.

However, when we compared the surrogate markers of insulin resistance between controls and RYGB patients, we could not detect a significant difference, as previously shown (24, 41). The discrepancy between our results and previous reports may be due to the differences in sex and age, with a possible negative effect of estrogen deficit and aging on insulin sensitivity, mitigating glucose outcomes after RYGB in our cohort. Yet, we showed that operated patients displayed a better cholesterol profile. Our data are consistent with a previous study comparing 69 post-RYGB patients (BMI<30 kg/m2, 2 years after RYGB) with age-, sex- and BMI-matched controls demonstrating lower LDL and FM associated with higher LM (24).

The present study highlights several predictors of LM changes after RYGB. A regression analysis adjusted for age and time of follow-up demonstrated that a lower nadir weight was associated with greater LM%. Consistently, LM% was positively correlated with TWL%. This could be explained by an increased muscle mass possibly associated with increased physical activity. Alternatively, post-RYGB patients might preferentially lose FM rather than LM. This is consistent with results from Davidson et al. (6) showing that LM% of post-RYGB patients increased between 1 and 5 years after RYGB. Taken together, these data suggest a predictive value for nadir weight and TWL% on LM%, later after RYGB. LM% was also negatively influenced by time of follow-up, reflecting a possible loss of LM over time. In contrast to LM%, higher nadir weight and lower TWL% predicted greater ALMI, suggesting that this functional compartment of muscle mass could be differentially affected by weight loss after surgery, compared to full body LM. This hypothesis is supported by the higher amount of trunk LM found post-RYGB in operated patients compared to controls (Table 2). Further, Heshka et al. demonstrated that RYGB patients have greater trunk organ mass and lower skeletal mass compared to non-operated controls (39).

As expected, LM% negatively correlate with weight regain suggesting a subsequent redistribution in BC with an increase in FM percentage. However, weight regain predicted for a greater ALMI. This is consistent with an expansion in both LM and FM.

Strengths and limitations

The strengths of this study are the use of high-quality gold-standard methods for BC, the analysis of a specific subpopulation, post-menopausal women, matched with controls and the long follow-up period after surgery. Limitations include a modest sample size in the subsample of 41 matched surgical patients to controls and the exclusion of surgical patients with higher BMI and/or younger age. In particular, the results on VAT analysis in the surgical group according to diabetes might be affected by extreme values and the small sample size. Another limitation consists in the lack of preoperative BC data with the analysis of the actual evolution after surgery. Patients and controls were not matched for ethnicity, as this information was not available. However, Heymsfield et al. (42) established that race is not a major contributor of BC proportions when BMI is held constant. Although all operated patients received the same nutrition and physical activity recommendation, we did not collect specific data on physical activity levels and food intake.

Conclusion

RYGB in women lead to an improvement of BC that persists in the long-term. Preservation in LM after RYGB might indicate a low risk of sarcopenia in post-menopausal women. While these findings appear promising for BS patients, further studies are warranted to assess BC evolution in the long-term in elderly population.

Supplementary materials

This is linked to the online version of the paper at https://doi.org/10.1530/EJE-21-0895.

Declaration of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of this study.

Funding

This work did not receive any specific grant from any funding agency in the public, commercial or not-for-profit sector.

Acknowledgements

The authors are grateful to all clinicians collecting data for the Cohort Obesity Lausanne. The authors would like to thank James S Acierno, PhD and Dionysios Chartoumpekis, MD-PhD for critically reading the manuscript and helpful discussion.

References

  • 1

    GBD 2015 Obesity Collaborators, Afshin A, Forouzanfar MH, Reitsma MB, Sur P, Estep K, Lee A, Marczak L, Mokdad AH & Moradi-Lakeh M et al. Health effects of overweight and obesity in 195 countries over 25 years. New England Journal of Medicine 2017 377 1327. (https://doi.org/10.1056/NEJMoa1614362)

    • Search Google Scholar
    • Export Citation
  • 2

    Europe Approaches to Obesity. World Health Organisation, 2020. (available at: https://www.euro.who.int/en/health-topics/noncommunicable-diseases/obesity/data-and-statistics)

    • Search Google Scholar
    • Export Citation
  • 3

    Adams TD, Davidson LE, Litwin SE, Kim J, Kolotkin RL, Nanjee MN, Gutierrez JM, Frogley SJ, Ibele AR & Brinton EA et al.Weight and metabolic outcomes 12 years after gastric bypass. New England Journal of Medicine 2017 377 11431155. (https://doi.org/10.1056/NEJMoa1700459)

    • Search Google Scholar
    • Export Citation
  • 4

    Schauer PR, Bhatt DL, Kashyap SR. Bariatric surgery or intensive medical therapy for diabetes after 5 years. New England Journal of Medicine 2017 376 1997. (https://doi.org/10.1056/NEJMc1703377)

    • Search Google Scholar
    • Export Citation
  • 5

    Busetto L, Dicker D, Azran C, Batterham RL, Farpour-Lambert N, Fried M, Hjelmesæth J, Kinzl J, Leitner DR & Makaronidis JM et al. Practical recommendations of the obesity management task force of the European Association for the study of obesity for the post-bariatric surgery medical management. Obesity Facts 2017 10 597632. (https://doi.org/10.1159/000481825)

    • Search Google Scholar
    • Export Citation
  • 6

    Davidson LE, Yu W, Goodpaster BH, DeLany JP, Widen E, Lemos T, Strain GW, Pomp A, Courcoulas AP & Lin S et al.Fat-free mass and skeletal muscle mass five years after bariatric surgery. Obesity 2018 26 11301136. (https://doi.org/10.1002/oby.22190)

    • Search Google Scholar
    • Export Citation
  • 7

    Favre L, Marino L, Roth A, Acierno Jr J, Hans D, Demartines N, Pitteloud N, Suter M, Collet TH. The reduction of visceral adipose tissue after Roux-en-Y gastric bypass is more pronounced in patients with impaired glucose metabolism. Obesity Surgery 2018 28 40064013. (https://doi.org/10.1007/s11695-018-3455-x)

    • Search Google Scholar
    • Export Citation
  • 8

    Tamboli RA, Hossain HA, Marks PA, Eckhauser AW, Rathmacher JA, Phillips SE, Buchowski MS, Chen KY, Abumrad NN. Body composition and energy metabolism following Roux-en-Y gastric bypass surgery. Obesity 2010 18 17181724. (https://doi.org/10.1038/oby.2010.89)

    • Search Google Scholar
    • Export Citation
  • 9

    Schneider J, Peterli R, Gass M, Slawik M, Peters T, Wolnerhanssen BK. Laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass lead to equal changes in body composition and energy metabolism 17 months postoperatively: a prospective randomized trial. Surgery for Obesity and Related Diseases 2016 12 563570. (https://doi.org/10.1016/j.soard.2015.07.002)

    • Search Google Scholar
    • Export Citation
  • 10

    Bazzocchi A, Ponti F, Cariani S, Diano D, Leuratti L, Albisinni U, Marchesini G, Battista G. Visceral fat and body composition changes in a female population after RYGBP: a two-year follow-up by DXA. Obesity Surgery 2015 25 443451. (https://doi.org/10.1007/s11695-014-1422-8)

    • Search Google Scholar
    • Export Citation
  • 11

    Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codoceo J, Inostroza J, Basfi-Fer K, Papapietro K & Rojas J et al.Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obesity Surgery 2009 19 4146. (https://doi.org/10.1007/s11695-008-9638-0)

    • Search Google Scholar
    • Export Citation
  • 12

    Chaston TB, Dixon JB, O'Brien PE. Changes in fat-free mass during significant weight loss: a systematic review. International Journal of Obesity 2007 31 743750. (https://doi.org/10.1038/sj.ijo.0803483)

    • Search Google Scholar
    • Export Citation
  • 13

    Das SK, Roberts SB, Kehayias JJ, Wang J, Hsu LK, Shikora SA, Saltzman E, McCrory MA. Body composition assessment in extreme obesity and after massive weight loss induced by gastric bypass surgery. American Journal of Physiology: Endocrinology and Metabolism 2003 284 E1080E1088. (https://doi.org/10.1152/ajpendo.00185.2002)

    • Search Google Scholar
    • Export Citation
  • 14

    Buhler J, Rast S, Beglinger C, Peterli R, Peters T, Gebhart M, Meyer-Gerspach AC, Wölnerhanssen BK. Long-term effects of laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass on body composition and bone mass density. Obesity Facts 2020 14 131140.

    • Search Google Scholar
    • Export Citation
  • 15

    Nuijten MAH, Monpellier VM, Eijsvogels TMH, Janssen IMC, Hazebroek EJ, Hopman MTE. Rate and determinants of excessive fat-free mass loss after bariatric surgery. Obesity Surgery 2020 30 31193126. (https://doi.org/10.1007/s11695-020-04654-6)

    • Search Google Scholar
    • Export Citation
  • 16

    Vatier C, Henegar C, Ciangura C, Poitou-Bernert C, Bouillot JL, Basdevant A, Oppert JM. Dynamic relations between sedentary behavior, physical activity, and body composition after bariatric surgery. Obesity Surgery 2012 22 12511256. (https://doi.org/10.1007/s11695-012-0619-y)

    • Search Google Scholar
    • Export Citation
  • 17

    Lee MJ, Kim EH, Bae SJ, Choe J, Jung CH, Lee WJ, Kim HK. Protective role of skeletal muscle mass against progression from metabolically healthy to unhealthy phenotype. Clinical Endocrinology 2019 90 102113. (https://doi.org/10.1111/cen.13874)

    • Search Google Scholar
    • Export Citation
  • 18

    Farnsworth E, Luscombe ND, Noakes M, Wittert G, Argyiou E, Clifton PM. Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. American Journal of Clinical Nutrition 2003 78 3139. (https://doi.org/10.1093/ajcn/78.1.31)

    • Search Google Scholar
    • Export Citation
  • 19

    Marks BL, Rippe JM. The importance of fat free mass maintenance in weight loss programmes. Sports Medicine 1996 22 273281. (https://doi.org/10.2165/00007256-199622050-00001)

    • Search Google Scholar
    • Export Citation
  • 20

    Mechanick JI, Apovian C, Brethauer S, Garvey WT, Joffe AM, Kim J, Kushner RF, Lindquist R, Pessah-Pollack R & Seger J et al.Clinical practice guidelines for the perioperative nutrition, metabolic, and nonsurgical support of patients undergoing bariatric procedures – 2019 update: cosponsored by American Association of Clinical Endocrinologists/American College of Endocrinology, the Obesity Society, American Society For Metabolic & Bariatric Surgery, Obesity Medicine Association, and American Society of Anesthesiologists – executive summary. Endocrine Practice 2019 25 13461359. (https://doi.org/10.4158/GL-2019-0406)

    • Search Google Scholar
    • Export Citation
  • 21

    Busetto L, Dicker D, Azran C, Batterham RL, Farpour-Lambert N, Fried M, Hjelmesæth J, Kinzl J, Leitner DR & Makaronidis JM et al.Practical recommendations for the post-bariatric surgery medical management. Obesity Surgery 2018 28 21172121. (https://doi.org/10.1007/s11695-018-3283-z)

    • Search Google Scholar
    • Export Citation
  • 22

    Skogar M, Holmback U, Hedberg J, Riserus U, Sundbom M. Preserved fat-free mass after gastric bypass and duodenal switch. Obesity Surgery 2017 27 17351740. (https://doi.org/10.1007/s11695-016-2476-6)

    • Search Google Scholar
    • Export Citation
  • 23

    Ciangura C, Bouillot JL, Lloret-Linares C, Poitou C, Veyrie N, Basdevant A, Oppert JM. Dynamics of change in total and regional body composition after gastric bypass in obese patients. Obesity 2010 18 760765. (https://doi.org/10.1038/oby.2009.348)

    • Search Google Scholar
    • Export Citation
  • 24

    Andersson DP, Dahlman I, Eriksson Hogling D, Backdahl J, Toft E, Qvisth V, Näslund E, Thorell A, Rydén M, Arner P. Improved metabolism and body composition beyond normal levels following gastric bypass surgery: a longitudinal study. Journal of Internal Medicine 2019 285 92101. (https://doi.org/10.1111/joim.12824)

    • Search Google Scholar
    • Export Citation
  • 25

    Strain GW, Ebel F, Honohan J, Gagner M, Dakin GF, Pomp A, Gallagher D. Fat-free mass is not lower 24 months postbariatric surgery than nonoperated matched controls. Surgery for Obesity and Related Diseases 2017 13 6569. (https://doi.org/10.1016/j.soard.2016.03.003)

    • Search Google Scholar
    • Export Citation
  • 26

    Petermann-Rocha F, Chen M, Gray SR, Ho FK, Pell JP, Celis-Morales C. Factors associated with sarcopenia: a cross-sectional analysis using UK Biobank. Maturitas 2020 133 6067. (https://doi.org/10.1016/j.maturitas.2020.01.004)

    • Search Google Scholar
    • Export Citation
  • 27

    McKinlay SM, Brambilla DJ, Posner JG. The normal menopause transition. Maturitas 1992 14 103115. (https://doi.org/10.1016/0378-5122(9290003-m)

  • 28

    Abdulnour J, Doucet E, Brochu M, Lavoie JM, Strychar I, Rabasa-Lhoret R, Prud’homme D. The effect of the menopausal transition on body composition and cardiometabolic risk factors: a Montreal-Ottawa New Emerging Team group study. Menopause 2012 19 760767. (https://doi.org/10.1097/gme.0b013e318240f6f3)

    • Search Google Scholar
    • Export Citation
  • 29

    Papadakis GE, Hans D, Gonzalez Rodriguez E, Vollenweider P, Waeber G, Marques-Vidal P, Lamy O. Menopausal hormone therapy is associated with reduced total and visceral adiposity: the OsteoLaus cohort. Journal of Clinical Endocrinology and Metabolism 2018 103 19481957. (https://doi.org/10.1210/jc.2017-02449)

    • Search Google Scholar
    • Export Citation
  • 30

    Vionnet N, Favre L, Fournier P, Demartine N, Suter M, Pralong FP. The Lausanne Obesity Cohort: why and how? Revue Medicale Suisse 2016 12 581583.

  • 31

    (SMOB) Swiss Society for the Study of Morbid Obesity. Directives médicales pour le traitement de l’obésité – © SMOB, 2018.

  • 32

    Shevroja E, Marques-Vidal P, Aubry-Rozier B, Hans G, Rivadeneira F, Lamy O, Hans D. Cohort profile: the OsteoLaus study. International Journal of Epidemiology 2019 48 10461047g. (https://doi.org/10.1093/ije/dyy276)

    • Search Google Scholar
    • Export Citation
  • 33

    European Association for Cardiovascular Prevention & Rehabilitation, Reiner Z, Catapano AL, De Backer G, Graham I, Taskinen M-R, Wiklund O, Agewall S, Alegria E, Chapman MJ & Durrington M et al. ESC/EAS Guidelines for the management of dyslipidaemias: the task force for the management of dyslipidaemias of the European Society of Cardiology (ESC) and the European Atherosclerosis Society (EAS). European Heart Journal 2011 32 17691818.

    • Search Google Scholar
    • Export Citation
  • 34

    Dordevic AL, Bonham M, Ghasem-Zadeh A, Evans A, Barber E, Day K, Kwok A, Truby H. Reliability of compartmental body composition measures in weight-stable adults using GE iDXA: implications for research and practice. Nutrients 2018 10 1484. (https://doi.org/10.3390/nu10101484)

    • Search Google Scholar
    • Export Citation
  • 35

    Reinhardt M, Piaggi P, DeMers B, Trinidad C, Krakoff J. Cross calibration of two dual-energy X-ray densitometers and comparison of visceral adipose tissue measurements by iDXA and MRI. Obesity 2017 25 332337. (https://doi.org/10.1002/oby.21722)

    • Search Google Scholar
    • Export Citation
  • 36

    Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y & Sayer AA et al.Sarcopenia: revised European consensus on definition and diagnosis. Age and Ageing 2019 48 1631. (https://doi.org/10.1093/ageing/afy169)

    • Search Google Scholar
    • Export Citation
  • 37

    Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J & Breuille D et al.Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International Working Group on Sarcopenia. Journal of the American Medical Directors Association 2011 12 249256. (https://doi.org/10.1016/j.jamda.2011.01.003)

    • Search Google Scholar
    • Export Citation
  • 38

    Ho DEI K, King G, Stuart EA. MatchIt: nonparametric preprocessing for parametric causal inference. Journal of Statistical Software 2011 42 128.

    • Search Google Scholar
    • Export Citation
  • 39

    Heshka S, Lemos T, Astbury NM, Widen E, Davidson L, Goodpaster BH, DeLany JP, Strain GW, Pomp A & Courcoulas AP et al.Resting energy expenditure and organ-tissue body composition 5 years after bariatric surgery. Obesity Surgery 2020 30 587594. (https://doi.org/10.1007/s11695-019-04217-4)

    • Search Google Scholar
    • Export Citation
  • 40

    Frisard MI, Greenway FL, Delany JP. Comparison of methods to assess body composition changes during a period of weight loss. Obesity Research 2005 13 845854. (https://doi.org/10.1038/oby.2005.97)

    • Search Google Scholar
    • Export Citation
  • 41

    Hoffstedt J, Andersson DP, Eriksson Hogling D, Theorell J, Naslund E, Thorell A, Ehrlund A, Rydén M, Arner P. Long-term protective changes in adipose tissue after gastric bypass. Diabetes Care 2017 40 7784. (https://doi.org/10.2337/dc16-1072)

    • Search Google Scholar
    • Export Citation
  • 42

    Heymsfield SB, Peterson CM, Thomas DM, Heo M, Schuna Jr JM. Why are there race/ethnic differences in adult body mass index-adiposity relationships? A quantitative critical review. Obesity Reviews 2016 17 262275. (https://doi.org/10.1111/obr.12358)

    • Search Google Scholar
    • Export Citation
  • 43

    Rosenquist KJ, Pedley A, Massaro JM, Therkelsen KE, Murabito JM, Hoffmann U, Fox CS. Visceral and subcutaneous fat quality and cardiometabolic risk. JACC: Cardiovascular Imaging 2013 6 762771. (https://doi.org/10.1016/j.jcmg.2012.11.021)

    • Search Google Scholar
    • Export Citation
  • 44

    Adams TD, Gress RE, Smith SC, Halverson RC, Simper SC, Rosamond WD, Lamonte MJ, Stroup AM, Hunt SC. Long-term mortality after gastric bypass surgery. New England Journal of Medicine 2007 357 753761. (https://doi.org/10.1056/NEJMoa066603)

    • Search Google Scholar
    • Export Citation

 

     European Society of Endocrinology

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 1339 1340 119
PDF Downloads 541 541 61
  • View in gallery

    Univariable linear regressions of the association between percentage of lean mass on total body mass (LM%) as outcome variable, and % total weight loss (TWL%) (A), nadir weight (B) time of follow-up (C) and weight regain (D) as predictor variables in the RYGB cohort. R2, Spearman’s coefficient. A full color version of this figure is available at https://doi.org/10.1530/EJE-21-0895.

  • View in gallery

    Univariable linear regressions of the association between appendicular lean mass index (ALMI) as outcome variable and % total weight loss (TWL%) (A), nadir weight (B), time of follow-up (C) and weight regain (D) as predictor variables, in the RYGB cohort. R2, Spearman’s coefficient. A full color version of this figure is available at https://doi.org/10.1530/EJE-21-0895.

  • View in gallery

    Differences in % fat mass of total body weight, % lean mass of total body mass and visceral adipose tissue (VAT) in post-RYGB women patients vs controls. Data are expressed as mean ± s.d. Statistical analysis was done using Student’s t-test. *P -value <0.001.

  • 1

    GBD 2015 Obesity Collaborators, Afshin A, Forouzanfar MH, Reitsma MB, Sur P, Estep K, Lee A, Marczak L, Mokdad AH & Moradi-Lakeh M et al. Health effects of overweight and obesity in 195 countries over 25 years. New England Journal of Medicine 2017 377 1327. (https://doi.org/10.1056/NEJMoa1614362)

    • Search Google Scholar
    • Export Citation
  • 2

    Europe Approaches to Obesity. World Health Organisation, 2020. (available at: https://www.euro.who.int/en/health-topics/noncommunicable-diseases/obesity/data-and-statistics)

    • Search Google Scholar
    • Export Citation
  • 3

    Adams TD, Davidson LE, Litwin SE, Kim J, Kolotkin RL, Nanjee MN, Gutierrez JM, Frogley SJ, Ibele AR & Brinton EA et al.Weight and metabolic outcomes 12 years after gastric bypass. New England Journal of Medicine 2017 377 11431155. (https://doi.org/10.1056/NEJMoa1700459)

    • Search Google Scholar
    • Export Citation
  • 4

    Schauer PR, Bhatt DL, Kashyap SR. Bariatric surgery or intensive medical therapy for diabetes after 5 years. New England Journal of Medicine 2017 376 1997. (https://doi.org/10.1056/NEJMc1703377)

    • Search Google Scholar
    • Export Citation
  • 5

    Busetto L, Dicker D, Azran C, Batterham RL, Farpour-Lambert N, Fried M, Hjelmesæth J, Kinzl J, Leitner DR & Makaronidis JM et al. Practical recommendations of the obesity management task force of the European Association for the study of obesity for the post-bariatric surgery medical management. Obesity Facts 2017 10 597632. (https://doi.org/10.1159/000481825)

    • Search Google Scholar
    • Export Citation
  • 6

    Davidson LE, Yu W, Goodpaster BH, DeLany JP, Widen E, Lemos T, Strain GW, Pomp A, Courcoulas AP & Lin S et al.Fat-free mass and skeletal muscle mass five years after bariatric surgery. Obesity 2018 26 11301136. (https://doi.org/10.1002/oby.22190)

    • Search Google Scholar
    • Export Citation
  • 7

    Favre L, Marino L, Roth A, Acierno Jr J, Hans D, Demartines N, Pitteloud N, Suter M, Collet TH. The reduction of visceral adipose tissue after Roux-en-Y gastric bypass is more pronounced in patients with impaired glucose metabolism. Obesity Surgery 2018 28 40064013. (https://doi.org/10.1007/s11695-018-3455-x)

    • Search Google Scholar
    • Export Citation
  • 8

    Tamboli RA, Hossain HA, Marks PA, Eckhauser AW, Rathmacher JA, Phillips SE, Buchowski MS, Chen KY, Abumrad NN. Body composition and energy metabolism following Roux-en-Y gastric bypass surgery. Obesity 2010 18 17181724. (https://doi.org/10.1038/oby.2010.89)

    • Search Google Scholar
    • Export Citation
  • 9

    Schneider J, Peterli R, Gass M, Slawik M, Peters T, Wolnerhanssen BK. Laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass lead to equal changes in body composition and energy metabolism 17 months postoperatively: a prospective randomized trial. Surgery for Obesity and Related Diseases 2016 12 563570. (https://doi.org/10.1016/j.soard.2015.07.002)

    • Search Google Scholar
    • Export Citation
  • 10

    Bazzocchi A, Ponti F, Cariani S, Diano D, Leuratti L, Albisinni U, Marchesini G, Battista G. Visceral fat and body composition changes in a female population after RYGBP: a two-year follow-up by DXA. Obesity Surgery 2015 25 443451. (https://doi.org/10.1007/s11695-014-1422-8)

    • Search Google Scholar
    • Export Citation
  • 11

    Carrasco F, Ruz M, Rojas P, Csendes A, Rebolledo A, Codoceo J, Inostroza J, Basfi-Fer K, Papapietro K & Rojas J et al.Changes in bone mineral density, body composition and adiponectin levels in morbidly obese patients after bariatric surgery. Obesity Surgery 2009 19 4146. (https://doi.org/10.1007/s11695-008-9638-0)

    • Search Google Scholar
    • Export Citation
  • 12

    Chaston TB, Dixon JB, O'Brien PE. Changes in fat-free mass during significant weight loss: a systematic review. International Journal of Obesity 2007 31 743750. (https://doi.org/10.1038/sj.ijo.0803483)

    • Search Google Scholar
    • Export Citation
  • 13

    Das SK, Roberts SB, Kehayias JJ, Wang J, Hsu LK, Shikora SA, Saltzman E, McCrory MA. Body composition assessment in extreme obesity and after massive weight loss induced by gastric bypass surgery. American Journal of Physiology: Endocrinology and Metabolism 2003 284 E1080E1088. (https://doi.org/10.1152/ajpendo.00185.2002)

    • Search Google Scholar
    • Export Citation
  • 14

    Buhler J, Rast S, Beglinger C, Peterli R, Peters T, Gebhart M, Meyer-Gerspach AC, Wölnerhanssen BK. Long-term effects of laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass on body composition and bone mass density. Obesity Facts 2020 14 131140.

    • Search Google Scholar
    • Export Citation
  • 15

    Nuijten MAH, Monpellier VM, Eijsvogels TMH, Janssen IMC, Hazebroek EJ, Hopman MTE. Rate and determinants of excessive fat-free mass loss after bariatric surgery. Obesity Surgery 2020 30 31193126. (https://doi.org/10.1007/s11695-020-04654-6)

    • Search Google Scholar
    • Export Citation
  • 16

    Vatier C, Henegar C, Ciangura C, Poitou-Bernert C, Bouillot JL, Basdevant A, Oppert JM. Dynamic relations between sedentary behavior, physical activity, and body composition after bariatric surgery. Obesity Surgery 2012 22 12511256. (https://doi.org/10.1007/s11695-012-0619-y)

    • Search Google Scholar
    • Export Citation
  • 17

    Lee MJ, Kim EH, Bae SJ, Choe J, Jung CH, Lee WJ, Kim HK. Protective role of skeletal muscle mass against progression from metabolically healthy to unhealthy phenotype. Clinical Endocrinology 2019 90 102113. (https://doi.org/10.1111/cen.13874)

    • Search Google Scholar
    • Export Citation
  • 18

    Farnsworth E, Luscombe ND, Noakes M, Wittert G, Argyiou E, Clifton PM. Effect of a high-protein, energy-restricted diet on body composition, glycemic control, and lipid concentrations in overweight and obese hyperinsulinemic men and women. American Journal of Clinical Nutrition 2003 78 3139. (https://doi.org/10.1093/ajcn/78.1.31)

    • Search Google Scholar
    • Export Citation
  • 19

    Marks BL, Rippe JM. The importance of fat free mass maintenance in weight loss programmes. Sports Medicine 1996 22 273281. (https://doi.org/10.2165/00007256-199622050-00001)

    • Search Google Scholar
    • Export Citation
  • 20

    Mechanick JI, Apovian C, Brethauer S, Garvey WT, Joffe AM, Kim J, Kushner RF, Lindquist R, Pessah-Pollack R & Seger J et al.Clinical practice guidelines for the perioperative nutrition, metabolic, and nonsurgical support of patients undergoing bariatric procedures – 2019 update: cosponsored by American Association of Clinical Endocrinologists/American College of Endocrinology, the Obesity Society, American Society For Metabolic & Bariatric Surgery, Obesity Medicine Association, and American Society of Anesthesiologists – executive summary. Endocrine Practice 2019 25 13461359. (https://doi.org/10.4158/GL-2019-0406)

    • Search Google Scholar
    • Export Citation
  • 21

    Busetto L, Dicker D, Azran C, Batterham RL, Farpour-Lambert N, Fried M, Hjelmesæth J, Kinzl J, Leitner DR & Makaronidis JM et al.Practical recommendations for the post-bariatric surgery medical management. Obesity Surgery 2018 28 21172121. (https://doi.org/10.1007/s11695-018-3283-z)

    • Search Google Scholar
    • Export Citation
  • 22

    Skogar M, Holmback U, Hedberg J, Riserus U, Sundbom M. Preserved fat-free mass after gastric bypass and duodenal switch. Obesity Surgery 2017 27 17351740. (https://doi.org/10.1007/s11695-016-2476-6)

    • Search Google Scholar
    • Export Citation
  • 23

    Ciangura C, Bouillot JL, Lloret-Linares C, Poitou C, Veyrie N, Basdevant A, Oppert JM. Dynamics of change in total and regional body composition after gastric bypass in obese patients. Obesity 2010 18 760765. (https://doi.org/10.1038/oby.2009.348)

    • Search Google Scholar
    • Export Citation
  • 24

    Andersson DP, Dahlman I, Eriksson Hogling D, Backdahl J, Toft E, Qvisth V, Näslund E, Thorell A, Rydén M, Arner P. Improved metabolism and body composition beyond normal levels following gastric bypass surgery: a longitudinal study. Journal of Internal Medicine 2019 285 92101. (https://doi.org/10.1111/joim.12824)

    • Search Google Scholar
    • Export Citation
  • 25

    Strain GW, Ebel F, Honohan J, Gagner M, Dakin GF, Pomp A, Gallagher D. Fat-free mass is not lower 24 months postbariatric surgery than nonoperated matched controls. Surgery for Obesity and Related Diseases 2017 13 6569. (https://doi.org/10.1016/j.soard.2016.03.003)

    • Search Google Scholar
    • Export Citation
  • 26

    Petermann-Rocha F, Chen M, Gray SR, Ho FK, Pell JP, Celis-Morales C. Factors associated with sarcopenia: a cross-sectional analysis using UK Biobank. Maturitas 2020 133 6067. (https://doi.org/10.1016/j.maturitas.2020.01.004)

    • Search Google Scholar
    • Export Citation
  • 27

    McKinlay SM, Brambilla DJ, Posner JG. The normal menopause transition. Maturitas 1992 14 103115. (https://doi.org/10.1016/0378-5122(9290003-m)

  • 28

    Abdulnour J, Doucet E, Brochu M, Lavoie JM, Strychar I, Rabasa-Lhoret R, Prud’homme D. The effect of the menopausal transition on body composition and cardiometabolic risk factors: a Montreal-Ottawa New Emerging Team group study. Menopause 2012 19 760767. (https://doi.org/10.1097/gme.0b013e318240f6f3)

    • Search Google Scholar
    • Export Citation
  • 29

    Papadakis GE, Hans D, Gonzalez Rodriguez E, Vollenweider P, Waeber G, Marques-Vidal P, Lamy O. Menopausal hormone therapy is associated with reduced total and visceral adiposity: the OsteoLaus cohort. Journal of Clinical Endocrinology and Metabolism 2018 103 19481957. (https://doi.org/10.1210/jc.2017-02449)

    • Search Google Scholar
    • Export Citation
  • 30

    Vionnet N, Favre L, Fournier P, Demartine N, Suter M, Pralong FP. The Lausanne Obesity Cohort: why and how? Revue Medicale Suisse 2016 12 581583.

  • 31

    (SMOB) Swiss Society for the Study of Morbid Obesity. Directives médicales pour le traitement de l’obésité – © SMOB, 2018.

  • 32

    Shevroja E, Marques-Vidal P, Aubry-Rozier B, Hans G, Rivadeneira F, Lamy O, Hans D. Cohort profile: the OsteoLaus study. International Journal of Epidemiology 2019 48 10461047g. (https://doi.org/10.1093/ije/dyy276)

    • Search Google Scholar
    • Export Citation
  • 33

    European Association for Cardiovascular Prevention & Rehabilitation, Reiner Z, Catapano AL, De Backer G, Graham I, Taskinen M-R, Wiklund O, Agewall S, Alegria E, Chapman MJ & Durrington M et al. ESC/EAS Guidelines for the management of dyslipidaemias: the task force for the management of dyslipidaemias of the European Society of Cardiology (ESC) and the European Atherosclerosis Society (EAS). European Heart Journal 2011 32 17691818.

    • Search Google Scholar
    • Export Citation
  • 34

    Dordevic AL, Bonham M, Ghasem-Zadeh A, Evans A, Barber E, Day K, Kwok A, Truby H. Reliability of compartmental body composition measures in weight-stable adults using GE iDXA: implications for research and practice. Nutrients 2018 10 1484. (https://doi.org/10.3390/nu10101484)

    • Search Google Scholar
    • Export Citation
  • 35

    Reinhardt M, Piaggi P, DeMers B, Trinidad C, Krakoff J. Cross calibration of two dual-energy X-ray densitometers and comparison of visceral adipose tissue measurements by iDXA and MRI. Obesity 2017 25 332337. (https://doi.org/10.1002/oby.21722)

    • Search Google Scholar
    • Export Citation
  • 36

    Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, Cooper C, Landi F, Rolland Y & Sayer AA et al.Sarcopenia: revised European consensus on definition and diagnosis. Age and Ageing 2019 48 1631. (https://doi.org/10.1093/ageing/afy169)

    • Search Google Scholar
    • Export Citation
  • 37

    Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, Abellan van Kan G, Andrieu S, Bauer J & Breuille D et al.Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International Working Group on Sarcopenia. Journal of the American Medical Directors Association 2011 12 249256. (https://doi.org/10.1016/j.jamda.2011.01.003)

    • Search Google Scholar
    • Export Citation
  • 38

    Ho DEI K, King G, Stuart EA. MatchIt: nonparametric preprocessing for parametric causal inference. Journal of Statistical Software 2011 42 128.

    • Search Google Scholar
    • Export Citation
  • 39

    Heshka S, Lemos T, Astbury NM, Widen E, Davidson L, Goodpaster BH, DeLany JP, Strain GW, Pomp A & Courcoulas AP et al.Resting energy expenditure and organ-tissue body composition 5 years after bariatric surgery. Obesity Surgery 2020 30 587594. (https://doi.org/10.1007/s11695-019-04217-4)

    • Search Google Scholar
    • Export Citation
  • 40

    Frisard MI, Greenway FL, Delany JP. Comparison of methods to assess body composition changes during a period of weight loss. Obesity Research 2005 13 845854. (https://doi.org/10.1038/oby.2005.97)

    • Search Google Scholar
    • Export Citation
  • 41

    Hoffstedt J, Andersson DP, Eriksson Hogling D, Theorell J, Naslund E, Thorell A, Ehrlund A, Rydén M, Arner P. Long-term protective changes in adipose tissue after gastric bypass. Diabetes Care 2017 40 7784. (https://doi.org/10.2337/dc16-1072)

    • Search Google Scholar
    • Export Citation
  • 42

    Heymsfield SB, Peterson CM, Thomas DM, Heo M, Schuna Jr JM. Why are there race/ethnic differences in adult body mass index-adiposity relationships? A quantitative critical review. Obesity Reviews 2016 17 262275. (https://doi.org/10.1111/obr.12358)

    • Search Google Scholar
    • Export Citation
  • 43

    Rosenquist KJ, Pedley A, Massaro JM, Therkelsen KE, Murabito JM, Hoffmann U, Fox CS. Visceral and subcutaneous fat quality and cardiometabolic risk. JACC: Cardiovascular Imaging 2013 6 762771. (https://doi.org/10.1016/j.jcmg.2012.11.021)

    • Search Google Scholar
    • Export Citation
  • 44

    Adams TD, Gress RE, Smith SC, Halverson RC, Simper SC, Rosamond WD, Lamonte MJ, Stroup AM, Hunt SC. Long-term mortality after gastric bypass surgery. New England Journal of Medicine 2007 357 753761. (https://doi.org/10.1056/NEJMoa066603)

    • Search Google Scholar
    • Export Citation