Effect of a 16-week Combined Supervised Exercise Program after bariatric surgery on Sarcopenia parameters based on FNIH, EWGSOP2, EASO/ESPEN criteria – The results of the EXPOBAR randomized trial program

doi:10.21203/rs.3.rs-4850725/v1

Introduction:

Bariatric surgery is a recognized treatment option for severe obesity, and its effectiveness in reducing weight and controlling obesity-related conditions has been demonstrated. However, it can also lead to decreased skeletal muscle mass and strength, increasing the risk of sarcopenia after surgery. This randomized clinical trial studied the effects of a 16-week supervised combined exercise program on sarcopenia in bariatric surgery patients.

Methods

Thirty-seven surgery candidates participated in the EXPOBAR (EXercise POst BARiatric) program and were randomized into experimental or control groups. The intervention lasted 16 weeks, starting one month after surgery, and included a supervised combined aerobic and resistance exercise intervention. The outcomes, including body composition and physical fitness parameters, were assessed at four time points. All participants underwent gastric bypass surgery (RYGB).

Results

The EXPOBAR trial revealed significant and meaningful effects of the exercise intervention on anthropometric indices, such as weight (p = 0.039) and waist circumference (p = 0.010). The EXPOBAR trial also showed that after bariatric surgery, there was a clear decrease in muscle mass, and this loss continued through the duration of follow-up, despite the exercise protocol. The most substantial improvements were observed in physical function and strength metrics (p = 0.005 and p < 0.001, respectively), along with a reduction in fat mass (p = 0.006), indicating the intervention’s effectiveness in enhancing both physical fitness and body composition.

Discussion

Current findings indicate that following an initial decrease due to bariatric surgery, a combined exercise intervention significantly improves functional physical capacity and strength. The exercise program in this study effectively reversed the surgery-induced loss in function and strength, reducing the number of patients at risk of sarcopenia. Physical and functional capacity are crucial noninvasive indicators for diagnosing muscle quality and sarcopenia.

Conclusion

Long-term management of sarcopenia and sarcopenic obesity in bariatric surgery patients requires frequent monitoring of body composition and muscle function. This approach is essential for tracking progress and optimizing treatment strategies over time. This study highlights the importance of integrating structured exercise programs into after bariatric surgery care to mitigate the risk of sarcopenia. Future options include nutritional protein supplementation and changes in the exercise protocol.

Trial registration

: The trial was registered at Clinicaltrials.gov (NCT03497546).

exercise

bariatric surgery

fat-free mass

sarcopenia

skeletal muscle mass

The high prevalence of obesity leads to increased mortality and morbidity. Bariatric surgery is one of the most effective treatments for severe obesity, but it is significantly associated with a reduction in skeletal muscle mass and function.
Sarcopenia is a disease characterized by a generalized loss of skeletal muscle mass and function and is associated with poor quality of life. It is also associated with diabetes, metabolic syndrome, and cardiovascular disease.

In the first months after bariatric surgery, muscle mass significantly decreased and continued to decline for up to 18 months, with muscle mass loss and strength greater than 20%.
Combined moderate-intensity exercise (which includes aerobic and strength training) and a progressive walking programme can increase muscle strength and metabolic improvements and can be effective in preventing and treating sarcopenic obesity.

Obesity is a significant public health issue because it is closely linked to increased mortality and morbidity rates. It is a chronic illness and is related to other chronic conditions, such as metabolic syndrome, diabetes, cardiovascular disease, psychological disorders and social problems (1).

Surgical treatment is considered the most effective management tool for morbid obesity and is known for its ability to induce substantial weight loss (60% or more excess weight) and improve associated obesity complications. However, the weight loss achieved after bariatric surgery is not only due to fat reduction but also due to a significant loss of lean tissue, accounting for up to 25% of the overall body mass reduction (2–4). This reduction in lean tissue mass, especially muscle mass, poses a challenge because it can decrease both resting and activity-related energy expenditure.

Healing after major surgical procedures can cause a significant increase in the body's need for protein. However, in the initial months following bariatric surgery, there is typically a significant decrease in food intake. This can result in temporary protein deficiency, especially after surgical interventions, which can affect the body's ability to absorb nutrients. This deficiency usually resolves once the patient's metabolism adjusts to the changes caused by surgery and food intake become sufficient and consistent according to needs (5–7).

The muscle requires energy to function properly, so a decrease in muscle mass can decrease both resting and activity-related energy expenditure. As a result, patients who are obese and have sarcopenia before surgery are less likely to lose weight and are more prone to regain weight than are those who have a healthy skeletal muscle system (8). After surgery, the combination of muscle tissue loss, temporary protein deficiency and surgical trauma can contribute to or worsen preexisting conditions of sarcopenia (9).

Furthermore, if muscle deficiency occurs or worsens after surgery, weight loss may slow or stop altogether, increasing the likelihood of obesity relapse. Additionally, sarcopenia increases the risk of metabolic complications and can ultimately compromise life expectancy, even if weight loss is achieved (10).

For bariatric patients with severe obesity, muscle deficiency can give rise to notable clinical complications following surgery. Preoperative sarcopenia has been shown to be a reliable indicator of complications and mortality during major abdominal surgery. Additionally, older individuals face an increased risk of cardiovascular events in the perioperative period. It is worth noting that the age of patients seeking metabolic/bariatric surgery may increase, leading to a greater number of individuals older than 60 years undergoing the procedure, which is when sarcopenia becomes a clinically significant issue (12). Therefore, it is crucial to carefully consider the occurrence of complications in obese patients with sarcopenia who undergo significant surgical bariatric procedures (11).

The prevalence of sarcopenia in patients with obesity ranges from 10 to 50%, with wide variation likely the result of the absence of a standardized clinical approach to evaluate sarcopenia in both qualitative and quantitative terms.

The European Working Group on Sarcopenia in Older People (EWGSOP) established a structured approach to identify, evaluate, and address issues related to sarcopenia in 2010. In 2019, they published a consensus based on the presence of low lean mass and low muscle strength, the EWGSOP2. This document uses the Find-Assess-Confirm-Severity (F-A-C-S) algorithm, which is utilized in various fields, including medicine, psychology and risk management, among others (13,14).

Furthermore, in 2014, the Foundation of the National Institutes of Health (FNIH) published a standardized diagnostic approach with the Sarcopenia Project, which suggested adjusting the criteria to account for differences in body mass index (BMI) (15).

More recently, in 2022, the EASO and ESPEN recommended introducing weight adjustment, particularly for individuals with obesity who are at risk of developing sarcopenia (4), considering that sarcopenia and muscle mass loss are significant concerns for individuals undergoing bariatric surgery.

BMI is a crucial criterion for selecting patients for obesity surgery and an indicator used to assess an individual's body composition and overall health status (16). When defining sarcopenia parameters after bariatric surgery, BMI plays a significant role and reflects changes in body composition, particularly muscle mass and fat mass, which can impact a person's health following surgery. BMI is a widely used metric for assessing obesity and has also been suggested to be a valuable tool for defining sarcopenic obesity in this population (17).

Given that few studies have assessed sarcopenia and sarcopenic obesity after bariatric surgery, additional experimental studies are needed so that clear criteria can be defined regarding useful tools and procedures to prevent and treat sarcopenic obesity after bariatric surgery.

Several guidelines suggest a combination of moderate-intensity exercise to maintain muscle mass. The American College of Sports Medicine (ACSM) recommends a progressive exercise program for all individuals following the FITT-VP principle, which includes frequency, intensity, time, type, volume, and progression (18,19). Similarly, the American Society for Metabolic and Bariatric Surgery (ASMBS) advocates starting a progressive walking program on the first day after surgery, incorporating aerobic exercises and strength training for at least 30 minutes daily (20,21).

Regular and targeted exercise programs are fundamental for managing sarcopenia and sarcopenic obesity. Resistance training has been proven effective at promoting muscle strength, enhancing function and improving body composition by reducing excess adiposity (22–24).

Both strength training and aerobic training have been shown to improve strength and metabolism in obese individuals. However, the long-term incidence of sarcopenia after surgery remains unclear, underscoring the need for research on both short-term and long-term exercise programs.

Objectives

The main objective was to analyze the long-term effects of a 16-week supervised combined exercise program on sarcopenia incidence, sarcopenic obesity, and sarcopenia parameters in patients undergoing RYGP.

Study design

This randomized controlled study (NCT03497546) was developed at a single health institution, the Center for Integrated Responsibility of Bariatric Surgery and Metabolic Diseases (CRI. COM), performed at a Portugal Hospital (ULSAC) and at the University (ESDH-CHRC). The protocol has been previously described (25).

Recruitment took place between December 2021 and December 2023 from among candidates who met the diagnostic criteria for bariatric surgery. A team member of the two institutions managed all the procedures.

A bariatric surgeon and a sports specialist nurse contacted the patients and randomized them into the control group (CG) and intervention group (IG). The invitation to participate was made in the context of the outpatient office, and participants who agreed to participate in the study were given the free and informed consent form previously approved by both the University and Hospital Ethics Committee (HESE_CE_1917/21).

Exercise training began one month after surgery, with a frequency of three times per week, up to a maximum of 55 minutes per session, for 16 weeks. The study included four evaluations over a 17-month period. All assessments were conducted by researchers who were blinded to the study's objectives and the participants' group allocation to minimize potential biases and ensure the integrity of the data collected. This study protocol complied with the CONSORT 2010 recommendations (Fig. 1).

Eligibility criteria

The inclusion criteria for patients were as follows: were candidates for bariatric surgery, aged between 18 and 60 years, had a BMI between 35 and 50 kg/m2, were men and women, had no contraindications to exercise and agreed to participate voluntarily in the study. The BMI range was chosen to target individuals with moderate to severe obesity. Patients with other previous bariatric surgical interventions or bariatric surgery complications were excluded from the study.

Sample Size and Randomization

This was a prospective study, and the sample size was calculated by the G*power (26). A total of 17 participants were included in each group to enable the detection of a moderate estimated effect size (between-group differences) of at least 0.99 standard deviations in the outcome risk of sarcopenia [18]. Two-way independent sample t tests were performed with an alpha error of α = 0.05 and a power of 1-β = 0.80.

Patients proposed for bariatric surgery (gastric bypass-RYGB) were randomly assigned at the time of proposal by a systematic random process to usual care (CG) or usual care plus an exercise program (IG).

Outcomes

After surgery, all outcomes were assessed before and after the exercise program. The first assessments were performed before the training program, and the remaining three were performed at different moments after the exercise program.

- Anthropometry and body composition

Weight was measured with a digital scale (Tanita MC 780-P MA), and height was determined by a manual stadiometer. This assessment was made before breakfast and at least six hours after eating, without shoes or wearing light clothes. Waist circumference was determined using a measuring tape, and BMI was calculated (weight/height²)(27,28). Dual-energy X-ray absorptiometry (DEXA) (DXA, Hologic QDR, Hologic, Inc., Bedford, MA, USA) was used to estimate body composition (fat mass and skeletal muscle mass) (29).

- Sarcopenia screening – FIND

In clinical practice, the EWGSOP2 and EASO/ESPEN both recommend the use of the SARC-F for sarcopenia screening and assessment (13,14,30). All participants completed this tool at the four time points.

This tool consists of five questions: strength (S), assistance walking (A), rising from a chair (R), climbing stairs (C), and falling (F). A total score is calculated out of 10 for each question, ranging from "not at all" to "very difficult". The recommended cutoff value for predicting sarcopenia is ≥ 4 points. Low values indicate no risk of sarcopenia (31–33).

- Sarcopenia Diagnosis – ASSESS

Skeletal muscle strength:

Sarcopenia is primarily diagnosed by searching for weak muscles. To assess evidence of sarcopenia, the EWGSOP2 recommends the use of grip strength or a chair stand measure with specific cutoff points for each test.

The handgrip strength test was performed using manual pressure dynamometry (Jamar®) to assess the muscle strength of the upper limbs. The participants were told to stand with their elbows straight and completely relaxed. The muscle strength test value was determined by recording the greatest grip strength value obtained after two trials with each hand (36,37).

The sit-to-stand test, which requires participants to alternate between standing and sitting for thirty seconds as often as they could, was used to assess the muscle strength of the lower limbs (38). The chair stand test provides a trustworthy and useful way to measure strength because it assesses both endurance and strength (17,39).

A handgrip strength of less than 27 kg for men and less than 16 kg for women (34) or > 15 s for five rises on the chair rise test (5-times sit-to-stand) were the chosen cut-offs. The timed chair stand test is a variation that counts how many times a patient can rise and sit in the chair over a 30-second interval (35).

- Sarcopenia confirmation – CONFIRM

Skeletal muscle mass:

Different methods can be used to report skeletal muscle mass, such as dual-energy X-ray absorptiometry (DEXA), bioelectrical impedance analysis (BIA) or muscle cross-sectional area (MRI) analysis. Given that DEXA is a widely used technique for determining skeletal muscle mass, it was chosen for all four assessments (30).

Appendicular skeletal muscle mass (ASM) was determined as the total skeletal muscle mass of the four limbs. This muscle mass is attached to the skeleton and plays a fundamental role in systemic movement and posture maintenance (15).

The upper and lower extremity muscle masses (arm + leg muscle mass [kg]) were summed and divided by height (meters) squared (m2) to calculate the skeletal muscle index (ASMMI) or the Baumgartner index (ASMMI = ASM/height²) (40,41). Sarcopenia assessment results vary among groups, but the ASMMI score is the most widely considered variable (13).

As recommended by the EWGSOP2, the following ASMM and ASSMI cutoff values were used in the present study: ASSM < 20 kg and ASSMI < 7.0 kg/m2 for males and ASSM < 15 kg and ASSMI < 5.5 kg/m2 for females (14). As such, we propose the use of the Baumgartner index as a cutoff for ASMM/weight < 28.27% for males and < 23.47% for females. The FNIH uses another ratio, which is considered ASMM/BMI < 0.789 for males and < 0.512 for females.

Sarcopenia Severity Level - SEVERITY

Physical Performance:

Once the diagnosis of sarcopenia was established, the severity was assessed using the 400-meter walk test, which assesses walking endurance and ability. During the test, participants were allowed to take up two rest breaks and were required to perform 20 laps of 20 meters each as quickly as possible (42,43). When the test was not finished or took longer than six minutes to complete, the participants were classified as having low physical performance (13).

The algorithm for diagnosing sarcopenia and sarcopenic obesity

Sarcopenia according to the EWGSOP2 criteria: Based on low muscle strength, low muscle mass and low physical performance (male grip strength < 27 kg, ASMM < 20 kg, ASMMI < 7.0 kg/m2, and 400 m walk test ≥ 6 min; female grip strength < 16 kg, ASMM < 15 kg, ASMMI < 5.7 kg/m2, and 400 m walk test ≥ 6 min), sarcopenia was diagnosed and classified according to severity (13).

Sarcopenic obesity according to EASO/ESPEN and FNIH: The parameters BMI, waist circumference (WC), and ASMM score based on weight and BMI (BMI > 30 kg/m2, WC ≥ 102 cm for males and ≥ 88 cm for females; ASMM/weight < 28.27% for males and < 23.47% for females; and ASMM/BMI < 0.789 for males and < 0.512 for females) were added to the EWGSOP-2 variables (4,15).

Intervention

The exercise combined aerobic and strength training in the same session in a progressive combined training program. The exercise prescriptions included information about frequency, intensity, time, type, volume, and progression (FITT-VP) (18).

Based on the recommendations of the World Health Organization (WHO) (44) and the ACSM (18), the duration of the program was 16 weeks, with a frequency of three times a week, for up to 55 minutes per session and starting one month after surgery. Each session started with a 5-minute warm-up and finalized with a 10-minute cool-down, with stretching and flexible work.

Patients assigned to the IG engaged in a combined exercise training program lasting for 16 weeks. Each exercise session included the following components: (a) a 5-minute specific warm-up; (b) phase 1 – resistance training (weeks 1–4); (c) phase 2 – hypertrophy training (weeks 5–10); (d) phase 3 – strength training (weeks 11–16); and a 10-minute cool-down for flexibility (myofascial release, mobility, static and dynamic stretching). The detailed combined exercise programmed is presented in Fig. 2.

The first phase included 20 minutes of interval training, encompassing circuit strength training. Each posterior phase has an increment of 10 minutes in the central block, always with an interval assessment of the patient’s adaptive response, based on heart rate reserve and the Borg scale (45).

Three personal trainers with training in sports sciences assessed physical fitness and prescribed and accompanied the training sessions. All training sessions took place in a fitness facility three times per week on nonconsecutive days from 7 to 10 a.m. The patients participated in the sessions in small groups (1–3) and were educated and motivated to exercise regularly.

Statistical methods

The statistical analysis was performed with SPSS version 27.0 (IBM SPSS, Inc., Chicago, IL, USA) to determine the outcomes. To assess whether the incidence of risk and diagnosis of sarcopenia were dependent on exercise, the chi-square test was used, and a type I error probability of 0.05 was used for all the inferential analyses. Categorical variables are expressed as frequencies and percentages, and continuous variables are expressed as the mean and standard deviation. The percentages were compared using the chi-square test or Fisher’s exact test. Data normality was assessed with the Shapiro‒Wilk test, and group differences were examined with an independent t test or a Mann‒Whitney test. To compare dependent variables, two-way ANOVA with sphericity and homogeneity tests, Spearman correlation, and regression logistic analyses were performed considering the intervention group and control group and the four sequential assessments (one pre- and three post-intervention programs).

A total of 37 patients participated in this study. The mean age was 46.9 (± 11.4) years, and the mean BMI was 42.9 (± 5.14) kg/m². All patients were previously sedentary before surgery. Of the study participants, 15 patients (33.3%) had T2DM, 13 (28.8%) had arterial hypertension, 19 (42%) had dyslipidemia, 10 (22.2%) had hypothyroidism, and 17 (37.8%) had obstructive sleep syndrome apnea (OSAP).

The participants were randomly assigned to the IG or CG. At baseline, no significant differences were observed between the groups (p>0.05), with the exception of weight, which was greater in the IG (103±14.5 V, 91.8±14.7; p=0.025), as presented in Table 1.

Table 1. Patient baseline characteristics in the intervention and control groups

Variables (Mean ± SD)	Intervention Group	Control Group	*p value*
Age (years)	43.68 ± 11.00	50.53 ± 10.97	0.071
*Anthropometry*
Weight (kg)	103 ± 14.5	91.8 ± 14.7	0.025
BMI (kg/m²)	37.8 ± 5.38	37 ± 4.53	0.639
Waist circumference (cm)	112 ± 9.68	110 ± 11.4	0.459
*Body Composition*
Fat mass (kg)	44.26 ± 12.16	44.47 ± 9.97	0.957
Body fat (%)	44.2 ± 6.46	45.5 ± 4.99	0.489
Total SMM mass (kg)	52.09 ± 9.05	48.01 ± 9.47	0.195
ASMM (kg)	22.29 ± 3.92	19.72 ± 4.79	0.086
ASMMI (kg)/m²)	8.09 ± 1.03	7.92 ± 1.47	0.672
ASMM/Weight (%)	21.7 ± 3.44	21.4 ± 3.18	0.795
ASMM/BMI	0.601 ± 0.14	0.535 ± 0.12	0.130
*Physical function and strength*
Handgrip (kg)	22.4 ± 10.6	18.1 ± 6.44	0.154
30 s Sit-to-stand test (s)	14.2 ± 2.35	12.8 ± 3.33	0.138
400-m walk test (m)	7.24 ± 2.26	8.79 ± 3.40	0.113

To determine the prevalence of sarcopenia and sarcopenic obesity, three algorithms were used to assess the parameters of these diseases (Table 2).

Table 2 Main outcomes of the EXPOBAR trial

BMI: body mass index, SMM: skeletal muscle mass, ASMM: appendicular skeletal muscle mass, ASMMI: appendicular skeletal muscle mass index.

ANOVA was used to assess the global group effect at all time points. The post hoc test revealed results within each group; a p value <0.05 indicated statistical significance.

^a- T0 vs T1 post hoc test, Bonferroni significance; ^b- T1 vs T2 post hoc test, Bonferroni significance; ^c- T1 vs T3 post hoc test, Bonferroni significance; ^d- T2 vs T3 post hoc test, Bonferroni significance;

^e_ T0 vs T3 post hoc test, Bonferroni correction, significant.

⁺Small effect size (0.01-0.06); ^# Medium effect size (0.06-0.14); * Large effect size (>0.14)

Variables

(Mean ± SE)

Moment

Before

Exercise

After Exercise

Global Group Effect

Intervention effect

Moment*Group

Baseline

T0

4-month

T1

6-month

T2

12-month

T3

p value

Effect size (η²)

T0 vs T1

T1 vs T2

T2 vs T3

T0 vs T3

Group

p value

Effect size (η²)

p value

Effect size (η²)

p value

Effect size (η²)

p value

Effect size (η²)

Anthropometry

Weight (kg)

IG

CG

103.2 ± 14.5

91.8 ± 14.7

83.1 ± 10.9^a

75.4 ± 14.7^a

75 ± 9.2^b

69.9 ± 12.1^b

74 ± 9.9^{c e}

70.8 ± 12.0^{c e}

0.039

0.078^#

0.137

0.064^#

0.280

0.034^#

0.191

0.050

0.048

0.111^#

BMI (kg/m²)

IG

CG

37.8 ± 5.40

37 ± 4.53

30.4 ± 4.43^a

30.2 ± 4.17^a

27.5 ± 4.01^b

28.2 ± 4.34

27.1 ± 3.8^{c e}

28.7 ± 4.93^{c e}

0.142

0.052⁺

0.531

0.012⁺

0.307

0.031⁺

0.112

0.072^#

0.106

0.075^#

Waist circumference (cm)

IG

CG

112.2 ± 9.68

109.5 ± 11.4

97.2 ± 8.4^a

97.2 ± 12.8^a

90.5 ± 8.49^b

94.2 ± 12.2

88.2 ± 8.8^e

93.6 ± 11^e

0.010

0.105*

0.316

0.030⁺

0.027

0.136^*

0.292

0.033⁺

0.023

0.143*

Total Weight Loss (%)

IG

CG

12.8 ± 2.72

13.1 ± 4.32

29.5 ± 5.92^a

29 ± 4.58^a

36.1 ± 7.5^b

33.8 ± 7.17^b

37 ± 8.08^{c e}

32.5 ± 9.76^{c e}

0.161

0.049⁺

0.675

0.005⁺

0.336

0.027⁺

0.111

0.073⁺

0.106

0.075^#

Body Composition

Fat mass (kg)

IG

CG

44.26±12.16

44.47 ± 9.97

27.66±13.55^a

34.42±7.92^a

25.22 ± 9.14

34.19 ± 6.99

23.37 ± 9.45^e

30.45 ± 12.6 ^e

0.006

0.114*

0.001

0.272*

0.744

0.003⁺

0.521

0.012⁺

0.052

0.107^#

Body fat (%)

IG

CG

44.2 ± 6.42

45.5 ± 4.99

36.6 ± 2.29^a

40.6 ± 7.26^a

31.9 ± 7.96^b

37.4 ± 6.34^b

30.4 ± 6.22^{c e}

37 ± 7.71^e

0.044

0.076^#

0.095

0.080^#

0.200

0.048^#

0.650

0.006⁺

0.010

0.180*

Total SMM mass (kg)

IG

CG

52.10 ± 9.04

48.01 ± 9.47

45.43 ± 13.2^a

44.65±9.54^a

44.53 ± 9.59

39.99±5.08^b

37.1±12.7^{c d e}

37.14 ± 5.06^{c e}

0.138

0.052⁺

0.169

0.055⁺

0.133

0.065^#

0.003

0.233*

0.219

0.044⁺

ASMM (kg)

IG

CG

22.29 ± 3.92

19.72 ± 4.79

20.45 ± 3.71^a

17.53±4.11^a

18.94±4.14^b

15.91±4.06^b

17.02±3.8^{c d e}

13.86 ± 4.31^{c d e}

0.705

0.014⁺

0.386

0.022⁺

0.817

0.002⁺

0.766

0.003⁺

0.362

0.024⁺

ASMMI (kg)/m²)

IG

CG

8.09 ± 1.03

7.92 ± 1.48

7.43 ± 0.99^a

7.03 ± 1.22^a

6.85 ± 1,20^b

6.39 ± 1.28^b

6.17 ±1.05^{c d e}

6.17 ± 1.05^{c d e}

0.186

0.046⁺

0.163

0.056⁺

0.718

0.004⁺

0.395

0.021⁺

0.078

0.088^#

ASMM/Weight (%)

IG

CG

21.7 ± 3.44

21.4 ± 3.18

24.08 ± 4.35^a

23.3 ± 3.13^a

25.3 ± 4.68

22.8 ± 3.71

22.9±3.39^d

19.8 ± 5.82^cd

0.030

0.084^#

0.129

0.066^#

0.237

0.041^#

0.476

0.015⁺

0.014

0.164*

ASMM/BMI

IG

CG

0.601± 0.14

0.535 ± 0.12

0.687 ± 0.17^a

0.580±0.11

0.701 ± 0.18

0.570±0.14

0.635±0.1^d

0.496 ± 0.19^cd

0.041

0.077^#

0.063

0.098^#

0.286

0.033⁺

0.781

0.002⁺

0.020

0.150*

Physical function and strength

Handgrip (kg)

IG

CG

22.4 ± 10.62

18.1 ± 6.44

24.8 ± 8.44

16.8 ± 5.25

26.9 ± 7.51

17.7 ± 5.11

27.4 ± 7.21

17.3 ± 5.44^e

0.005

0.120*

0.025

0.140*

0.288

0.033⁺

0.590

0.009⁺

0.014

0.166*

Sit-to-stand test (s)

IG

CG

14.2 ± 2.35

12.8 ± 3.33

15.9 ± 3.3^a

13.2 ± 2.88

16.5 ± 2.17

13.1 ± 2.45

16.8 ± 2.41^e

12.8 ± 2.70

<0.001

0.162*

0.040

0.118*

0.323

0.029⁺

0.073

0.092^#

<0.001

0.319*

400-m walk test (m)

IG

CG

7.24 ± 2.26

8.79 ± 3.40

6.05 ± 1.86^a

8.74 ± 3.05

5.82 ± 1.58

9.58 ± 3.58^c

5.57 ± 1.19^e

10.14 ± 4.1^{c d}

<0.001

0.303*

0.021

0.146*

0.007

0.193*

0.033

0.126*

<0.001

0.424*

The EXPOBAR trial showed that the intervention had significant and meaningful effects on several anthropometric measures, body composition parameters, physical function and strength outcomes. While several variables, such as BMI and ASMM score, had nonsignificant global group effects (p=0.142, p=0.705), they still had significant effects at 4, 6 and 12 months according to the post hoc test (p<0.05). However, muscle mass decreased continuously after surgery in both groups despite the exercise protocol used in the intervention group.

The most substantial improvements were observed in physical function and strength metrics, suggesting that the intervention was effective at enhancing physical fitness, with a significant group effect (p<0.001) and large effect size (η²=0.303). Additionally, handgrip strength and lower body strength had significant group effects (p=0.005 and p<0.001, respectively) and large effect sizes (η²=0.120 and η²=0.162). There were notable and meaningful increases in the measured outcomes over all interval periods, and these increases were substantial enough to have practical benefits or applications (table 2).

The latest and most important guidelines about this subject were used. The EWGSOP2 group consensus used the FACS sequence assessment, while the EASO/ESPEN and FNIH algorithms were based on weight and BMI criteria (Table 3).

Table 3 Logistic regression analysis of the ability of different algorithms to diagnose sarcopenia – EASO, EWGSOP2, FNIH

BMI: Body mass index

The intervention effect was reported to the baseline. A p value <0.05 was considered to indicate statistical significance.

	Intervention Group				Control Group				*Intervention effect* vs baseline
Major risk and severity (%)	*Pre-Exercise*	*After Exercise*			*Pre-Exercise*	*After Exercise*			p value
Major risk and severity (%)	Baseline T0	4-month T1	6-month T2	12-month T3	Baseline T0	4-month T1	6-month T2	12-month T3	4-month	6-month	12-month
EASO
SCREENING - High BMI	100%	31.6%	31.6%	26.3%	100%	35.3%	35.3%	41.2%	0.892	0.629	0.280
SCREENING - High Waist circumference	100%	73.7%	42.1%	10.5%	100%	82.4%	58.8%	58.8%	0.995	0.293	0.113
SCREENING - SARC-F	84.2%	5.3%	10.5%	0%	88.2%	70.6%	58.8%	0%	< 0.001	0.005	1.000
DIAGNOSIS – Altered functional skeletal muscle	47.4%	15.8%	5.3%	10.5%	70.6%	64.7%	52.9%	52.9%	0.005	0.008	0.011
DIAGNOSIS – Altered body composition	89.5%	42.1%	52.6%	84.2%	88.2%	70.6%	88.2%	94.1%	0.179	0.464	0.728
STAGING – STAGE II: With complications	100%	15.8%	5.3%	10.5%	100%	100%	100%	100%	0.034	0.002	< 0.001
EWGSOP2
SCREENING - SARC-F	84.2%	5.3%	10.5%	0%	88.2%	70.6%	58.8%	0%	< 0.001	0.005	1.000
ASSESS - Skeletal muscle strength	47.4%	15.8%	5.3%	10.5%	70.6%	64.7%	52.9%	52.9%	0.005	0.008	0.011
CONFIRM - Skeletal muscle mass	0%	0%	15.8%	47.4%	0%	11.8%	29.4%	52.9%	0.077	0.325	0.294
SEVERITY - Physical performance	73,7%	42.1%	31.6%	21.1%	70.6%	76.5%	82.4%	94.1%	0.034	0.002	< 0.001
FNIH
SKELETAL MUSCLE STRENGTH	47.4%	15.8%	5.3%	10.5%	70.6%	64.7%	52.9%	52.9%	0.005	0.008	0.011
SKELETAL MUSCLE MASS	47.4%	21.1%	15.8%	26.3%	64.7%	23.5%	47.1%	76.5%	0.858	0.050	0.004

The first step in all the algorithms is screening. The FACS uses the SARC-F questionnaire to determine risk. The EASO and ESPEN use both BMI and waist circumference. Before the exercise programme, all patients met these two last criteria as positive criteria. Immediately after the exercise program, the patients presented different screening results (IG 5.3% versus CG 70.6%, p<0.001), with a decreased risk in the IG after the exercise intervention. The same result was obtained at six months (10.5% for the IG versus 58.8% for the CG; p=0.005).

According to the results of assessing, confirming, and diagnosing sarcopenia, there was a decrease after the exercise intervention in the IG (47.4% to 15.8%) and a small difference in the CG (70.6% to 64.7%). This difference was significant after the exercise program (p=0.005), at 6 months (p=0.008) and 12 months (p=0.011). To confirm the diagnosis, three different indices and cut-offs were used to assess muscle mass.

The ASMMI did not significantly differ between the groups. When the EASO/ESPEN criteria were applied based on weight, the results were similar. Different results were found for the FNIH criteria, which did not significantly improve after the exercise intervention (IG 21.1% versus CG 23.5%) but did improve long-term after exercise at 6 (IG 15.8% versus CG 41.7%) and 12 months (IG 26.3% versus CG 76.5%).

The severity of sarcopenia was significantly different immediately after and long after the exercise program (p=0.034, p=0.002, p<0.001).

To perform a more detailed analysis of the results associated with physical exercise and its temporal impact on the risk and incidence of sarcopenia, a logistic regression was carried out to analyze the causal relationship in addition to the associations already described. There was a greater number of participants at risk of sarcopenia in the CG than in the control group (5.3% versus 70.6%, respectively; p<0.001). This effect was maintained at 6 months (p=0.005) but not at 12 months (p>0.05).

Regarding sarcopenia screening and diagnosis, 64.7% of the CGs had a positive assessment for subsequent diagnosis of sarcopenia after exercise (p=0.005). In comparison, only 15.8% of the IG had the same positive assessment, highlighting the decrease in upper limb skeletal muscle strength in the CG. This relationship was maintained at 6 and 12 months (p=0.008, p=0.011). According to the results of the inferential statistical analysis, after exercise, there was a significant probability of confirming the diagnosis and changing the assessment of the level of sarcopenia between the IG and CG (p=0.002).

There were no significant differences in the EASO or EWGSOP2 score, but when the FNIH consensus was used (ASMM/BMI), the differences in the confirmation of sarcopenia were statistically significant at 6 months (p=0.05) and 12 months (p=0.004).

The EXPOBAR trial is the first randomized controlled trial in Portugal to evaluate the effects of supervised and structured physical exercise programs on the risk and diagnosis of sarcopenia induced by bariatric surgery using the tools and cut-offs recommended by current consensuses.

Conflict

ing findings have been reported in several studies and papers regarding the impact of weight loss on sarcopenia and muscle deficiency. The clinical and biological effects of metabolic/bariatric surgery on sarcopenia and muscle deficiency are still not fully understood.

The current findings revealed a significant increase in the risk of sarcopenia within the first month after surgery, highlighting the need to implement exercise programs to preserve muscle mass and function. This can occur during bariatric surgery, particularly because of the very marked initial weight loss (46). These alterations make it increasingly important to assess the risk of sarcopenia in patients undergoing bariatric surgery. The intense weight loss that occurs in the first few months can lead to an increase in falls and fractures (47,48) due to changes in proprioception (49) and the metabolic impact associated with bariatric surgery and obesity. These changes are closely associated with frailty and instability, especially among elderly people. However, sarcopenia has implications for more than elderly people (50,51).

The present data show that the risk of initial sarcopenia is important and that the risk of sarcopenia can be clinically assessed and managed with early intervention. Based on the evidence, if a patient is at risk of sarcopenia and has been diagnosed with sarcopenia, treatment measures for the disease should be taken (52). The first treatment option for sarcopenic obesity is to combine nutritional and exercise goals with the aim of reducing adipose tissue but also enhancing and preserving muscle mass and function (53). Due to the significantly increased risk observed in the first month after surgery, prehabilitation and early interventions after surgery should probably be implemented.

Different screening tools, strength tests and skeletal muscle mass indices have been proposed for assessing sarcopenia. These indices consider adjustment factors such as height squared, weight or BMI. By using these indices, healthcare professionals can better evaluate and diagnose sarcopenia (54). In this study, these indices were used to diagnose sarcopenia and sarcopenic obesity, revealing that while some body composition metrics did not show significant group effects, the improvements in muscle function and strength underscore the importance of using objective diagnostic criteria.

The intervention group experienced significant improvements in muscle function and physical performance, which emphasizes the potential of structured exercise programs to counteract the negative impacts of body composition on individuals associated with obesity, sarcopenia and bariatric surgery (10).

Bariatric surgery has an impact on adipose tissue, but in the first few months, it also has a relevant effect on muscle mass (55–57). This highlights the importance of introducing combined exercise (aerobic and strength training), as was the case in the present study, where an important impact of exercise on muscle quality and consequently a reduction in the risk of worsening and developing sarcopenia was found.

The ACSM recommends resistance exercise to improve the function of the musculoskeletal system (18). Combined with aerobic training, it can potentially improve cardiorespiratory promotion of anabolic muscle adaptation and consequently improve muscle quality and quantity (45,58,59). There was a difference in the evolution of these diagnostic criteria among the patients who practiced combined physical exercise, as reported in the last systematic review (60), but this difference was not statistically significant.

Body composition metrics, BMI and the ASMMI score did not significantly affect the participants in this study, raising questions about the overall effectiveness of the intervention. These include the intervention duration, the baseline fitness levels of participants, and potential differences in adherence to the intervention protocols. BMI, a general measure of body fat based on weight and height, and the ASMMI score, which specifically measures muscle mass in the limbs, did not significantly change. This could be due to several factors. These parameters might not have been sensitive enough to detect differences between the two groups because of the strong confounding effects caused by the surgical procedure.

These findings underline an important point regarding the FITT-VP principle recommended by the ACSM (24,61). The lack of differences in the results shows that adjusting at least one of the exercise parameters, namely, frequency or intensity, may be necessary to obtain better results. This can be done in accordance with the ASMBS guidelines by increasing the training frequency.

Nevertheless, the results showed that combined exercise significantly improved functional physical capacity and strength after an initial decline after bariatric surgery. In other words, exercise was able to reverse the functional and strength loss that was the result of the surgical procedure, with a reduction in the number of patients at risk of a diagnosis of sarcopenia after bariatric surgery. This finding aligns with previous research (62) indicating that weight loss can improve physical performance by reducing mechanical factors and improving mobility and walking time, although it was observed that there was a decrease in strength assessed by handgrip strength in the first year after bariatric surgery.

The study's long-term effects, particularly at 6 and 12 months, underscore the sustainability of improvements in muscle function and physical performance. At the 6-month mark, improvements in muscle function were evident, demonstrating that the initial gains were not short-lived. By 12 months, participants continued to exhibit enhanced physical performance, indicating that these benefits can be sustained with consistent exercise. These findings emphasize the critical importance of continuous exercise for maintaining and building upon the benefits observed. These sustained improvements suggest that regular exercise is essential not only for achieving initial gains but also for preserving and enhancing muscle function and physical performance over time.

However, there was muscle mass loss in both groups, and this loss continued throughout the study duration, despite the exercise protocol used in the intervention group.

In the present study, when the complete diagnostic criteria defined by EASO/ESPEN and EWGSOP2 were used, no significant differences were found in either index, which may indicate that it might be essential to use the muscle strength criterion, which is probably the most important and decisive criterion for diagnosing sarcopenia in patients undergoing bariatric surgery.

The fundamental component and first step in defining the diagnosis of sarcopenia is muscle function. In a clinical context, the sarcopenia diagnostic index associated with weight is an essential parameter that significantly affects the outcome after long-term exercise, as is the case with the adjustment for BMI suggested by the FNIH (15).

Changes in sarcopenia parameters, such as physical function, are associated with changes in muscle mass and overall body weight, suggesting that BMI is a valuable parameter for adjusting the risk of sarcopenia. Physical and functional capacity are important indicators for diagnosing muscle quality, and they are noninvasive indicators. In studies involving individuals with other medical conditions and healthy individuals, it was already observed that muscle quality measured by the handgrip test is a more reliable indicator than the quantity of the muscle itself (63–66).

Sarcopenia is a particularly concerning problem in the context of bariatric surgery because it can impair physical function, increase the risk of frailty, and negatively impact overall health outcomes. Sarcopenia is a complex and multifactorial condition that is influenced by a variety of factors, including age, physical activity, nutritional status, and underlying medical conditions. Accurately defining sarcopenia parameters in after bariatric surgery patients is therefore crucial for the effective management and prevention of this condition.

Muscle strength, a variable not impacted by weight loss, might be a more useful indicator of sarcopenia in bariatric patients, whereas muscle mass is heavily influenced and confounded by weight loss.

Sarcopenia, characterized by a loss of muscle mass and function, is a growing concern in various populations, including those undergoing bariatric surgery. This study demonstrated significant improvements in the risk of sarcopenia, muscle quality, and functional capacity following a 16-week supervised combined exercise program, although the changes in muscle quantity were not statistically significant. These findings highlight the importance of incorporating exercise interventions, as recommended by the ACSM and the ASMBS, with an emphasis on increasing the frequency and intensity of training to effectively combat sarcopenia.

Long-term management of sarcopenia requires regular monitoring of both body composition and muscle function. Assessments of strength, skeletal muscle mass and functional status, along with periodic monitoring of body fat composition, are essential for tracking progress and optimizing treatment strategies over time. By going beyond BMI and addressing other parameters, such as physical function, healthcare providers can more accurately identify potential sarcopenia development after bariatric surgery, allowing appropriate intervention design.

Individualized care plans that consider the unique needs and circumstances of patients are crucial for achieving positive clinical outcomes. Preventive combined exercise programs are particularly important for patients undergoing bariatric surgery, as they can significantly improve strength and metabolic health, thereby enhancing long-term surgical outcomes.

Further research and clinical trials are warranted to refine and expand the current approaches available for managing sarcopenic obesity. Such efforts should aim to improve the quality of life and clinical outcomes for individuals affected by this complex condition, ensuring that interventions are both effective and sustainable over the long term.

Funding

Data Supporting this study are available upon reasonable request.

Ethical Approval

The procedures performed in this study were in accordance with the ethical standard for institutional research previously approved by both the University and Hospital Ethics Committees (HESE_CE_1917/21).

Informed Consent

Informed consent was obtained from all individual participants included in the study.

Declarations

of conflict interest

Funding

This work is funded by the Foundation for Science and technology, under the project UIDP/04923/2020

Author Contribution

Author Contributions: Conceptualization, C.M. and M.C.; methodology, C.M..; software, C.M., A.R.; validation, A.R., S.M. and M.C.; formal analysis, C.M.; investigation C.M. and M.C.; re-sources, A.R; data curation, M.C.; writing—original draft preparation, C.M. and M.C.; writ-ing—review and editing, M.C., A.R., J.B.; visualization, J.B.; supervision, S.M.; project administra-tion, C.M.; funding acquisition, M.C. All authors have read and agreed to the published version of the manuscript

Acknowledgement

We would like to acknowledge all our patients and also all professionals who contributed to the findings present in this study.

Data Availability

Corresponding author had full access to all the data and participants data are available upon request for authors. The authors have the responsibility for mantenance the integrity of anonymized format available from request.

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No competing interests reported.

Effect of a 16-week Combined Supervised Exercise Program after bariatric surgery on Sarcopenia parameters based on FNIH, EWGSOP2, EASO/ESPEN criteria – The results of the EXPOBAR randomized trial program

Status:

Version 1

Abstract

Introduction:

Methods

Results

Discussion

Conclusion

Trial registration

Figures

Key Points

Introduction

Objectives

Methods

Study design

Eligibility criteria

Sample Size and Randomization

Outcomes

- Sarcopenia Diagnosis – ASSESS

Skeletal muscle strength:

- Sarcopenia confirmation – CONFIRM

Skeletal muscle mass:

Sarcopenia Severity Level - SEVERITY

Physical Performance:

The algorithm for diagnosing sarcopenia and sarcopenic obesity

Intervention

Statistical methods

Results

Discussion

Conclusion

Declarations

Funding

Ethical Approval

Funding

Author Contribution

Acknowledgement

Data Availability

References

Additional Declarations

Status:

Version 1