Introduction

Despite the availability of non-surgical approaches to treat obesity, none of these interventions are as effective as surgery [1]. Bariatric and metabolic surgery is currently considered a safe, effective, and successful procedure to treat severe obesity and its associated medical problems assuring long-term results [2]. Presently, the dominant procedures are sleeve gastrectomy and gastric bypass, which account for approximately 90% of all operations performed worldwide. Both options have well-researched outcomes in the mid and long-term [3, 4]. However, weight loss induced by bariatric surgery represents a significant reduction not only in body fat, but also in muscle strength, muscle mass, and bone mineral mass [5]. In this setting, patients incur an increased risk of alterations in the skeletal muscle system [6].

Body composition changes appear to be one of the key outcomes after bariatric surgery. The potential rapid weight loss in the first year after surgery, associated with low-calorie diets, has been shown to significantly reduce muscle mass [7, 8]. The loss of muscle tissue may have negative implications for morbidity, physical performance and long-term weight regain [9].

One of the repercussions of the pronounced weight loss following bariatric surgery may be the onset of sarcopenia or modification of pre-existing sarcopenia. Sarcopenic obesity is a syndrome characterized by the coexistence of excessive body fat, low muscle mass, and reduced muscle strength [6, 10]. However, the early implementation of adequate nutritional support combined with physical activity may be a decisive anabolic stimulus for muscle protein synthesis and sarcopenia prevention [6].

The evidence for the effect of physical exercise in bariatric surgery patients, in general, does not go beyond the objective of weight loss. This narrows the therapeutic process of the person undergoing this type of surgery and the importance of exercise as a non-medical non-pharmacological therapy [11,12,13,14,15]. For this reason, some authors propose the need for the implementation of preventive programs that combine aerobic and strength exercises, which seems to be the most effective approach for overcoming the problem of sarcopeniia [16,17,18,19,20].

Previous reviews have addressed the benefits of physical exercise after bariatric surgery, as well as the type and characteristics of the intervention, suggesting that including accompanied physical exercise programs may be of great benefit to bariatric surgery patients. It promotes more significant improvements in body composition, namely a decrease in fat mass, and improvements in the skeletal muscle system, bone mineral density, and physical fitness [21, 22].

In this context, several authors suggest that reduced levels of physical activity and exercise are potent factors for the development of sarcopenia, and that combined exercise programs can be useful in preventing sarcopenia in this population [6, 23,24,25,26,27]. Prophylactic programs aimed at preventing sarcopenia in bariatric surgery patients seem to be crucial tools that may contribute to the long-term success of bariatric and metabolic surgery.

However, there is still poor evidence, few reviews, and sparse experimental data on the effects of supervised exercise on outcomes related to obesity surgery, like sarcopenia, especially in accordance with the FITT-VP principle. To highlight the various aspects to consider when developing an exercise training plan, the American College of Sports Medicine (ACSM) uses the FITT-VP principle to guide exercise prescription, which includes: Frequency (how often exercise is done each week), Intensity (the difficulty of the exercise), Time (duration of the exercise), Type (mode of exercise), Volume (total amount of exercise), and Progression (how the exercise program evolves) [28, 29]. In general, progression is recommended for an effective exercise prescription, but there is currently no evidence to support specific recommendations for this in bariatric surgery patients.

The main objective of this review is to examine the potential effects of exercise on the prevention of sarcopenia (muscle strength and functional capacity) in patients undergoing bariatric surgery. Additionally, we aim to systematically analyze the available metrics for evaluating sarcopenia in this setting and identify the characteristics of exercise that may be most useful to prevent sarcopenia after bariatric surgery. Secondary outcomes include health-related quality of life, physical activity, and cardiometabolic conditions.

Methods

Protocol and Registration

This systematic review was developed according to the Preferred items reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [30, 31]. It was also registered with the International Prospective Register of Systematic Reviews (PROSPERO), with registration number CRD42022324642 [23].

Search Strategy

The review was conducted in PubMed, Scopus, Web of Science, and Ebsco databases, and the search terms were subdivided into phases according to the defined criteria.

The following search strategy was used in all databases: (“exercise” OR “physical activity”) AND (“bariatric surgery” OR “gastric bypass” OR “gastric sleeve”) AND (“sarcopenia” OR “skeletal muscle mass” OR “fat-free mass” OR “muscle mass”) (Table 1).

Table 1 Search strategy
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Using the PICO framework, the research strategy was: “What type (C) of exercise (I) promotes more prevention of sarcopenia (O) in patients undergoing bariatric surgery (P)?”.

Eligibility Criteria

In the first phase, the inclusion criteria were defined as follows: (1) studies written in all languages, (2) published after 2011 and based on the latest evidence of exercise recommendation, (3) randomized controlled studies, controlled clinical studies, and other experimental studies were considered. In the next phase, the studies included were: (4) studies in which the population are patients after bariatric surgery, (5) articles that evaluated muscle mass and function after bariatric surgery, and (6) studies in which the intervention is performed after bariatric surgery. Review studies and those that did not assess muscle mass or function were excluded.

Selection of Studies

After applying the first inclusion and exclusion criteria, the titles and abstracts of the articles was screened. Subsequently, the remaining articles were reviewed in full, and only the articles that met the inclusion criteria for this systematic literature review were selected (Fig. 1).

Fig. 1
figure 1

Flow diagram of the study selection process for the systematic literature review

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Outcome Measures

The primary outcome of this study was to evaluate the efficacy of exercise programs on sarcopenia prevention following bariatric surgery. To address this, we studied muscle strength and functional capacity after bariatric surgery. Additionally, we evaluated the types and characteristics of exercise programs according to the FITT-VP principle. Secondary outcomes included anthropometric measures, body composition, physical activity levels, performance, quality of life, and cardiometabolic risk.

Data Extraction

The information from the studies is presented in three tables (Tables 2, 3, 4), to systematize the research process.

Table 2 Main results obtained
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Table 3 Main characteristics of interventions
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Table 4 Evaluation variables and effects of different types of exercise
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Selection and Quality of the Studies

One of the authors (CM) performed the search strategy, after which three reviewers (CM, SM, and MC) independently screened the titles and abstracts of the articles, assessing their eligibility according to the inclusion criteria. Divergences were settled by another author (AR). The assessment of the quality of these studies was done by four authors (CM, MC, AR, JB) using the “Quality Assessment of Controlled Intervention Studies", obtained from the website “The NIH Quality Assessment”, across various existing dimensions [30, 32]. This tool defines the classification of studies according to their risk of bias. The general recommendations indicate that an individual evaluation of each study should be carried out. Thus, the studies were categorized as “Good,” “Fair,” or “Poor,” and the general classification of GOOD was considered for six of the eight evaluated studies (Table 5).

Table 5 Results of the analysis of the quality of studies—controlled intervention studies
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Results

Literature Research

In the initial search, 326 studies were found, 57 from Pubmed, 140 from Scopus, 106 from Web of Science, and 23 from Ebsco. After applying the exclusion criteria, 20 potentially relevant studies remained, but 12 were excluded after review of the full texts. All the remaining studies were experimental, including six randomized controlled trials (RCT), one quasi-experimental study, and one pilot study. In six studies, there was both an intervention group and a control group. One study included two intervention groups and a control group [33] and another included two intervention groups with different types of exercise [34]. Finally, eight studies were selected and analyzed, as shown in the diagram in Fig. 1, summarizing the research using an adapted PRISMA-P diagram.

Main Results

See Tables 2, 3, and 4.

Analysis of the Quality of Studies

See Table 5.

Types of Studies

The search strategy included publications in all languages, spanning the period between 2011 and 2022. However, only one study from 2011 was found, and six of the eight studies evaluated were published after 2017, with analyses limited to the immediate postoperative period. Only one study carried out the exercise program in a more extended postoperative period, up to 3 years after surgery [35].

The age range of subjects in almost all studies was 18 to 65 years old. Sample sizes ranged from 15 to 60 subjects, divided into an experimental group (GI) and a control group (CG). Only one study used two intervention groups and a control group; in this study, the largest sample size was 49 [33]. It should be noted that, in this case, the structured exercise was prescribed to the subjects and the monitoring was self-reported; there was no face-to-face monitoring.

The experimental studies were based on exercise programs initiated after bariatric surgery. Only one study started a program at a later stage, 37 months after surgery [35].

These studies were based on structured physical exercise programs, lasting between 12 and 24 weeks, mainly starting between 1 and 3 months after surgery. All studies had evaluations before the intervention which, in most cases, were done before surgery [33, 34, 36,37,38,39]. All studies had evaluations after the program.

The objective was to evaluate the effect of structured physical exercise, whether aerobic, resistance or combined exercise, on body composition. A pilot study evaluated the short-term effect of two types of exercise, aerobic and aerobic combined with resistance on functional capacity and body composition. These exercise programs were not applied face-to-face but were carried out at home, with self-registration and monitoring [34]. Training plans with elastic bands were provided in the study with three groups.

Anthropometry and Body Composition

Anthropometric and body composition assessments were carried out with bioimpedance [33, 35,36,37, 39] or Dual-energy X-ray absorptiometry (DEXA) [40]; in half of the studies, waist and hip measurements were also evaluated [35,36,37,38].

Combined exercise resulted in significant improvements in all body composition metrics, including a significant increase in muscle mass, in addition to quality of life, physical fitness and decreased weight regain [33,34,35,36].

All studies showed different results in the intervention group when compared to the control group, regardless of the type of exercise. However, significant differences were observed in some studies, namely, in fat mass reduction (P = 0.039 [34]; P < 0.001 [35]; P = 0.002 [36]), muscle mass increase (P = 0.038 [33]; P < 0.05 [34]), and the percentage of excess weight loss [35], with supervised combined, resistance, endurance, and progressive exercise. There was no difference between the groups in the study that had two intervention groups, aerobic and aerobic exercise plus strength [33]. Despite not having significant results, the combined exercise group had better outcomes than the aerobic-only group [33].

Even in programs initiated later after surgery, at 12 to 24 months, combined exercise produced significantly better results in terms of body composition, namely muscle mass. Similar results were found in two other studies, with evidence that combined exercise significantly reduced fat mass, and increased muscle and bone mass, and led to more pronounced reductions in waist and hip measurements [34, 35].

Physical Function

Muscle strength was assessed in 6 of the studies using the handgrip test [33, 34, 36, 37, 39, 40] and/or one repetition maximum (1RM), including 1RM leg extension [40] and 1RM Chest and leg press [37].

One study assessed muscle quality by measuring the cross-sectional area of the right thigh muscle by magnetic resonance imaging [40].

Regarding functional capacity, there were assessments in 4 studies, with the six-minute walk test (6MWT) [34], shuttle walk test [36], 12-min walk run test [33], and sit-to-stand [33, 34, 36, 37], with the latter being used in three studies.

Physical fitness was assessed in three studies through Maximum oxygen consumption (VO2max) [35, 37, 38], and the Borg scale perceived exertion was assessed in two studies [34, 38].

The results for muscular strength, mainly assessed by handgrip, showed improvements in all intervention groups, although they were significant only with combined exercise (P < 0.05) [34]. The sit-to-stand and 1RM leg extension tests also showed significant differences in the combined exercise group.

It is important to mention that, in the study where the investigators evaluated the cross-sectional area of the right thigh muscle through magnetic resonance imaging, no significant differences were found following resistance training [40].

VO2max has been an important assessment of physical fitness and is considered an important parameter to analyze morbidities associated with excess weight in individuals with obesity [39]. It has not only been shown to be an important parameter to assess exercise capacity, but also a significant independent predictor of cardiovascular risk and overall mortality [40].

Only 3 studies evaluated physical fitness through VO2max, all of which reported significant improvements in the intervention group, regardless of the type of exercise. There is evidence that improvements in lung function following surgery can lead to a significant increase in VO2max, and that supervised resistance training an improve muscle strength and functional autonomy, thereby increasing a patient’s functional capacity [37]. The improvement in VO2max is mainly due to increased peak blood flow, which increases the maximum rate at which oxygen is supplied and utilized by the skeletal muscle system [28, 29].

Physical Exercise

Physical activity was evaluated in 3 studies by IPAQ [34, 36], in 2 studies with accelerometer [36, 38], in 2 studies by self-report [33, 37], and 1 study by indirect calorimetry [38]. Self-monitored diet was only evaluated in 3 studies [33, 36, 38], with metabolism calculated in one of these studies [39].

In all studies, structured physical exercise was directly proportional to weight loss and improvement in body composition, that is, more physical exercise led to better body composition outcomes. Even in studies with no significant differences, the results were always different in the groups subject to intervention, that is, the groups with intervention obtained better results on body composition.

Significant differences in body composition were observed only in the groups performing combined exercise (P = 0.039; P = 0.013) [34, 35]. No significant improvements were observed in interventions with resistance or aerobic exercise alone, despite better results relative to the control group.

Combined exercise achieved an improvement in anthropometric parameters, specifically muscle mass, even when started one year after surgery [36] (P = 0.034) and three years after surgery (P < 0.001) [35].

Discussion

This systematic review aims to analyze the effects of exercise on prevention of sarcopenia in patients undergoing bariatric surgery. The reviewed studies focused on combined resistance and aerobic training, all demonstrating promising results in improving body composition but with different results in terms of the skeletal muscle system and, consequently, in muscle strength and function.

Bariatric surgery often leads to significant weight loss, but it can also affect body composition, including a reduction in skeletal muscle mass [41, 42]. While decreased skeletal muscle mass may occur despite exercise, engaging in regular physical activity post-bariatric surgery can still offer significant benefits. Exercise can help individuals maintain a healthier body composition by preserving or improving muscle mass and reducing the overall loss of muscle tissue compared to those not exercising [43].

It’s important to highlight the distinction between muscle condition/function and muscle morphology, especially concerning the impact of exercise after surgery [44]. In essence, exercise may not fully prevent changes in muscle morphology following bariatric surgery, but it can substantially enhance muscle condition and functionality, ensuring that the remaining muscle mass performs optimally and contributes to an individual’s overall well-being [33, 37, 45].

Combined training was analyzed in four studies, starting either shortly after surgery or three years after surgery. Significant changes in anthropometric measurements and body composition were observed in intervention groups (aerobic and combined) but without a significant difference in BMI between groups. That is, without a great variation in weight, there are significant improvements in body composition, namely maintenance and even improvement in muscle mass and quality [34].

A previous study demonstrated a mean loss of 21% of fat-free mass (17.5%–31.3%) and 22% of lean body mass one year after surgery [44]. Given that most changes occur in the first month after surgery, the best time to implement an exercise program might be in the initial weeks after surgery [33].

Furthermore, a combined 12-week exercise program with three progressive phases, 50%–80% intensity, aerobic, and resistance exercise, was found to significantly improve body composition, physical function, cardiovascular function, and functional capacity [36]. These data suggest that combined exercise may be more effective than aerobic exercise alone in increasing muscle mass, even when started in the weight stabilization phase. In one study, the loss of muscle mass at the end of the 12-week exercise intervention amounted to 13% of the total reduction in body mass. This number is lower than previously observed and did not negatively affect handgrip strength and functional capacity [44].

Some guidelines also move in this direction, recommending moderate intensity combined exercise to maintain the skeletal muscle system. Although there are still no definitive guidelines for exercise after surgery, the American College of Sports Medicine (ACSM) states that, once patients are discharged from the surgery, they should follow a progressive exercise program based on the FITT-VP principle (frequency, intensity, time, type, volume, progression) for weight loss and maintenance, for individuals with overweight and obesity [29]. Also, the American Society for Metabolic and Bariatric Surgery (ASMBS) recommends, in addition to preoperative exercises, patients should start a progressive walking program on the first postoperative day, including both aerobic exercises and strength training ≥ 30 min/day [46, 47].

In one study with combined exercise, the program started 37 weeks after surgery, based on previous observations that maximum weight loss is achieved between 12 and 24 months after surgery [35]. Likewise, other studies observed a significant weight recovery between 24 and 36 months [48], and between 24 and 48 months after surgery [9]. The investigators monitored the subjects from the 1st month after surgery and found that the patients achieved their maximum fat loss between months 7 and 13 after surgery. From that moment on, an increase in fat mass was observed in both groups, being significantly higher 37 months after surgery [35].

According to the results of this study, progressive combined exercise programs, started with eight minutes until fifty minutes duration per session, performed two to four days per week, at 50%–75% of one maximum repetition and 60%–80% of maximum heart rate, resulted in significant reductions in the percentage of fat mass, a trend towards total weight reduction, and increases in the percentage of excess weight lost and muscle mass by the end of the exercise program. The monitoring of these subjects showed that, during the same period after the surgery, the weight and the percentage of fat mass continued to increase significantly in the control group, while there were significant reductions in the percentage of excess weight loss [35].

On the other hand, resistance training is an important potentiator of muscle strength and muscle quality. However, it does not lead to a significant increase in muscle mass or changes in the cross-section of the muscle [40]. In this same study, muscle quality, which is an important factor to consider after bariatric surgery, was evaluated through magnetic resonance imaging of the right thigh, namely the cross-sectional area of the right thigh muscle, with no alterations being observed. A possible explanation for the lack of increase in the cross-sectional area of the muscle may be an inadequate substrate availability for protein synthesis due to the severe caloric restriction induced by the surgery [33].

At the end of 12 weeks of aerobic exercise after bariatric surgery, weight loss, changes in BMI, and muscle strength levels were similar both in the control and intervention groups [45]. These results are similar to those of Shah et al. [38], who evaluated the effects of aerobic exercise in patients after surgery. Despite muscle mass outcomes being different, there are no significant differences between those practiced aerobic exercise and those who did not practice exercise [38, 49]. Aerobic exercise does not yiled better results in terms of the musculoskeletal system, and consequently, does not have better results in the prevention of sarcopenia.

In a more complete and ambitious study, researchers compared two types of training. While adding resistance to the aerobic exercise program did not have an additional effect on weight loss. Also, the experimental groups did not have significant differences in this item but found positive effects of combined exercise on improvement in muscle mass. According to these results, sarcopenia has less incidence with the practice of combined exercises. Furthermore, muscle mass was decreased in all three groups, but the control group and aerobic exercise group lost more muscle mass and strength than the combined exercise group [33].

Despite there were no significant differences in muscle mass, 12 weeks of supervised resistance training improved muscle strength in addition to providing progression in flexibility and strength of prehension [37]. Even in studies with a longer duration, 24 weeks, when starting just one month after the surgery, the results were similar [39]. This means that the exercise duration should increase, or on the other hand, it should be maintained in the long term.

These data show that a progressive, combined resistance and aerobic exercise program, performed three times a week, for at least 60 min, over 12 to 20 weeks, can also contribute to an increase in muscle mass directly proportional to muscle strength. This, in turn, improves physical performance and consequently decreases sarcopenia levels.

Conclusion

In this systematic review, we provide a general approach of the effectiveness of physical exercise on body composition, namely on muscle mass and strength and, consequently, on the levels of sarcopenia in bariatric surgery patients.

Aerobic exercise alone, or aerobic exercise combined with resistance, has been shown to promote greater weight loss compared to physically inactive patients. In the postoperative period, aerobic exercise has a positive impact on reducing fat mass, while the addition of resistance program plays an essential role in preserving muscle mass. On the other hand, combined exercise leads to improvement in the skeletal muscle system and consequently decreases the occurrence of postoperative sarcopenia. In the future, it is important to differentiate between muscle condition and function. Muscle condition refers to the actual performance and capabilities of the muscles, such as strength, endurance, flexibility, and overall functionality. Exercise, particularly combined training, can significantly impact muscle condition by improving strength, endurance, and functional capacity.

Implementing an individualized and supervised combined exercise program in the first weeks after surgery decreases weight, generates a reduction in fat mass, and a tendency to increase muscle mass. Furthermore, the integration of lifestyle interventions and consultations in clinical settings after bariatric surgery is crucial for ensuring long-term success and patient well-being. It is crucial that these interventions are accessible, tailored to individual needs, and embedded within the overall care pathway after bariatric surgery. Engaging patients in their own care and providing continuous support, long-term weight management and improved health outcomes become more attainable.