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ORIGINAL CONTRIBUTIONS

The Effect of Aerobic or Aerobic-Strength Exercise

on Body Composition and Functional Capacity in Patients with BMI ≥ 35 after Bariatric Surgery: a Randomized Control Trial

Alireza Hassannejad1&Alireza Khalaj2&Mohammad Ali Mansournia3&

Mastaneh Rajabian Tabesh1&Zahra Alizadeh1,4

Published online: 19 May 2017

#Springer Science+Business Media New York 2017

Abstract

BackgroundAlthough previous studies suggested that bariat- ric surgery is the most effective and sustainable treatment method for morbid obesity in long term, but without changing in lifestyle, maintaining optimal weight loss is almost impossible.

Methods Sixty morbid obese patients (BMI≥35) were eval- uated before and after 12 weeks of bariatric surgery in order to compare the impact of two different exercise programs on body composition and functional capacity outcomes.

Participants were divided into three groups: aerobic (A), aerobic-strength (AS), and control (C) group. Aerobic capac- ity was assessed with 12-min walk-run test (12MWRT). One- repetition maximum (1RM) test was performed to evaluation upper limb muscle strength. Lower extremity functional ca- pacity was assessed by sit-to-stand test.

Results Weight, percent body fat (PBF), and fat mass (FM) reduced greater in the trial groups in comparison to the C group (P< 0.05). In the AS group, the reduction of fat-free mass (FFM) was significantly lower than that in the other groups. Mean changes in 12MWRT increased significantly in the intervention groups. The mean change in the sit-to- stand scores was not statistically significant between the three groups. Comparing the intervention groups showed that mean changes in 1RM variables increased in AS group (P= 0.03).

Conclusions The data suggests a positive effect of exercise on weight and PBF decrease after surgery, and it leads to signif- icant improvement on aerobic capacity. Moreover, doing resisted exercise caused greater preserving of lean mass.

Keywords Bariatric surgery . Functional capacity . Body composition . Exercise . Obesity

Introduction

The worldwide prevalence of obesity and morbid obesity has increased rapidly [1]. Monitoring trends suggest increasing prevalence of obesity since 1980 [2]. In 2014, 600 million of the world’s population was obese [3] and if this trend goes on in the same way, more than 3 billion people will suffer from either overweight or obesity by 2030 [4]. Obesity is a major health concern in Iran too [5]. World Health Organization Alireza Hassannejad and Alireza Khalaj are contributed equally to the

study.

* Zahra Alizadeh [email protected] Alireza Hassannejad

[email protected] Alireza Khalaj

[email protected]

Mohammad Ali Mansournia [email protected] Mastaneh Rajabian Tabesh [email protected]

1 Sports Medicine Research Center, Tehran university of Medical Sciences, Tehran, Iran

2 Obesity Treatment Center, Department of Surgery, Shahed University, Tehran, Islamic Republic of Iran

3 Department of Epidemiology and Biostatistics, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

4 Department of Sports and Exercise Medicine, Tehran University of Medical Sciences, No7, Ale-ahmad Highway, Opposite of the Shariati Hospital, Tehran 14395-578, Iran

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reported that prevalence of obesity was almost 20.1% in male and 30.5% in women at 2014 [6].

While obesity is highly associated with complications such as Type II diabetes, hypertension, dyslipidemia, sleeps apnea syndrome, cardiovascular disease, and certain types of cancer and musculoskeletal problems [7], finding an effective treat- ment method is a serious challenge for all countries. Different approaches of nutritional, pharmaceutical, psychological, complementary therapies, and surgical interventions have been suggested for coping with obesity [8–11]. Studying the outcomes of these methods revealed that none of the non- surgical interventions are as effective as the surgical proce- dures [11–13].

Moreover, previous results suggested that the surgery is the most effective and sustainable method in long term. Not only are outcomes of the surgical weight loss superior to non- surgical methods, but also bariatric surgery leads to significant changes in metabolic regulations and obesity complication and decreases morbidity and mortality [11,14–17]. As a re- sult, the bariatric surgery is a popular method in treating mor- bid obesity and improving health-related quality of life [18].

According to annual reports of American Society for Metabolic and Bariatric Surgery (ASMBS) in 2015, 196,000 bariatric surgeries have been performed. Sleeve gastrectomy (SG) was the most common procedure. Roux-en-Y gastric bypass (RYGB) and gastric bypass revision were in the sec- ond and third places, respectively [19]. However, such inva- sive procedures do not eliminate unhealthy habits [20], so lifestyle changes such as healthy eating pattern and appropri- ate physical activity may improve surgical results [18].

Since patients who have undergone bariatric surgery may confront some difficulties during exercise, due to obesity com- plications such as arthritis, it is crucial to examine whether physical activities can increase the weight loss results or not.

Besides, finding the best exercise prescription is an important issue as a part of the postsurgical guideline to enhance loss of body fat mass and maintaining lean body mass [21].

Therefore, the main aim of the study was to evaluate the impact of aerobic and strength exercise after the bariatric sur- gery on weight loss and body composition outcomes. The other important contribution was to investigate the improve- ment in functional capacity.

Methods and Procedures Subjects

The present study comprises a prospective clinical trial. Sixty white patients (15 male and 45 female), aged 20–50-year-olds, were recruited and underwent Roux-en-Y gastric bypass (n = 27) surgery or sleeve gastrectomy (n = 33) at three

hospitals by one bariatric surgeon, between December 2015 and July 2016.

The study sample included patients with BMI≥35 kg/m2. Patients were excluded if they were pregnant or postmeno- pausal, had uncontrolled diabetes, severe cardiovascular dis- ease, uncontrolled hypertension, chronic obstructive pulmo- nary disease, and neurological or musculoskeletal disorders that would limit the exercise capacity or any history of previ- ous weight loss surgery.

Subjects who showed any kind of symptoms of musculo- skeletal problems (unusual fatigue or burning sensation in the muscles, local or diffuse pain or stiffness in the knee, back or ankle, etc.) that would limit exercise capacity after surgery or took any medications which have any effect on weight loss or appetite were excluded from the study.

Experimental Design and Procedures

Randomization was performed using balanced block random- ization with 10 blocks of 6 (2 A, 2 B, and 2 C). Sixty subjects were randomized to an aerobic (A), aerobic-strength (AS), or a control group.

Two intervention groups (A and AS) were conducted to do walking during the first 4 weeks after surgery and grad- ually increase speed in tolerated threshold. The individuals were asked to walk 150 min per week according to the recommendations of American College of Sports Medicine (ACSM) [22]. From week 5 to 12, total time of walking increased to 150–200 min/week, 3–5 days/week in both groups with moderate intensity. The intensity of ex- ercise was suggested 12–14 according to Borg Scale. The Borg Scale is a relative scale which is specified by num- bers from 6 to 20 in order to assess how hard one feels when he/she is exercising. The numbers show Brating of perceived exertion (RPE)^of performed exercise [23]. All subjects in the AS group were educated to do three ses- sions of strength exercise 20–30 min, as well as walking from week 5 to 12. The green elastic band was given to female subjects and the blue one for male subjects.

Shoulder and hip strengthening exercises with the elastic bands were educated including extension, flexion, abduc- tion, and adduction according to ACSM guideline for re- sistance training [24]. A booklet containing training photos with full description was given to the AS group (see at- tachments). No exercise was prescribed to the control group. However, after the end of the study, similar to the intervention groups, the control group received an appro- priate exercise program.

Informed consent was obtained from all the individual par- ticipants included in the study. All protocols for the experi- ments were approved by the institute of Ethical Committee, Tehran, University of Medical Sciences (TUMS) and Health Services (IRCT201512297903N7).

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Measurements

Twelve-minute walk-run test (12MWRT), sit-to-stand test (STS), and one repetition maximum test (1RM); anthropomet- ric indices; physical activity patterns; and food intake were gathered by a Sport Medicine Specialist, 1 week prior to the surgery and 12 weeks after surgery.

Twelve-Minute Walk-Run Test

Two 12 MWRT tests were carried out in order to assess aero- bic functional capacity in the participants both before and after the surgery. Participants were requested to walk or run as far as possible on the treadmill during 12 min.

One Repetition Maximum Test

Two 1RM assessments were performed to monitor changes in upper limb muscle strength before and after the surgery. The 1RM was specified by making each subject lift a given weight which the examiner estimated could be repeated less than 10 times. Between each attempt, 1–2 min of rest was provided and the maximum number of repetitions was recorded [25].

The final result was calculated using the formula 1RM = (weight lifted)/(1–0.02 * RTF) [26].

Sit-To-Stand

Lower extremity muscle functional capacity was measured by sit-to-stand test. In order to perform STS, individuals were requested to sit on an armless chair (height 44.5 cm and seat- ing depth of 38 cm). The chair was leaned against the wall to minimize the risk of falling. Each participant fully sat down into the chair and stood up again without the use of the arms in a period of 60 s. The total number of times that the patient stands was recorded by the examiner.

Height, Weight, and Anthropometric Indices

Weight, skeletal muscle mass (SMM), fat-free mass (FFM), and percent body fat (PBF) were calculated by Body Impedance Analyzer in body 370 (Biospace America, Inc), and height was measured by using a standard tape.

Physical Activity Pattern

Physical activity patterns were evaluated according to the in- formation obtained from the daily activity log books that each participant of the aerobic and aerobic-strength group were required to fill. Completion method was explained by the Sports Medicine Specialist at the training session before the surgery.

Dietary Intake

Each subject was educated about having standard high-protein diet (600 to 800 cal for first 4 weeks, 800–1000 cal for weeks 4 to 8, and 1000–1200 cal for weeks 8 to 12). Daily food intake was assessed by 24-h food record, a validated tech- nique, at baseline and 12 weeks postsurgery. The outcomes were analyzed for nutrient intakes using the University of Minnesota Nutrition Data System for Research, version 5.0–

3.5. All the trainings and assessments were done by a trained nutritionist.

Statistical Analysis

Continuous variables were described as mean (SD) and cate- gorical variables were summarized as numbers (percentile).

To assess the association between anthropometric variables and functional capacity variables at the end of follow-up study groups, adjusted for the baseline (of values of those variables) age, sex, and BMI, we used multiple linear regression models (equivalent to analysis of variant ANCOVA). With the type I error of 0.05, a therapeutic effect equivalent to 1 standard deviation, loss-to-follow-up rate of 20%, and sample size of 20 in each group, the power of study will be equal to 80%. The results were summarized as mean difference and 0.95 (CI) aligned withPvalue <0.05. For data analysis, we used Stata 13 software.

Results

Sixty subjects (45 females and 15 males) with BMI equal to or greater than 35 were recruited in the study. Participants were randomly divided into three groups: aerobic exercise (n= 20), aerobic-strength exercise (n= 20), and control (n= 20) group (Fig.1).

Baseline demographics and anthropometric measurements are reported in Table1.

Apart from BMI, no significant differences were found in the baseline demographics and anthropometric measurements (P > 0.05). However, comparing the three groups showed greater BMI in A group (P= 0.04); so in the later analysis, this item was adjusted. Of the 60 individuals, 27 subjects underwent RYGB and 33 subjects underwent sleeve gastrec- tomy. Statistical analysis showed that the distribution of the procedures was similar in the study groups (P= 0.24).

The pattern of anthropometric changes within the three groups in baseline and 12 weeks postsurgery and comparison of anthropometric indices between groups are shown in Tables2and3, respectively.

No significant differences were found between mean changes in BMI and SMM between the three groups (Table 3). However, weight, PBF, and FM reduced

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significantly in the A and AS groups in comparison to the control group (P< 0.05). Additionally, no significant differ- ence was found in the mean changes in FFM between A and C groups but FFM reduction in C group was significantly great- er than that in the AS group (P= 0.03).

Changes in aerobic and strength functional capacity in the three groups over time are presented in Table4. Comparison

of changes in the functional capacity between the three groups is shown in Table5.

As listed in Table 5, the mean change in the sit-to-stand scores was not statistically significant between the three groups (p > 0.05). Mean changes in 12MWRT variables in- creased significantly in the intervention groups (p < 0.05).

However, the mean changes did not differ between the two Fig. 1 Flow chart of how

participants progressed through the study, and how many contributors completed each stage

Table 1 Basic demographic and anthropometric characteristics of the study population

Variable Control (n= 20) Aerobic (n= 20) Aerobic-strength (n= 20) pvalue

Age (year) 36.7 (6.2) 33.3 (8.4) 35.4 (8.1) 0.363

Sex (female) 16 (80) 15 (75) 14 (70) 0.774

Height (cm) 161.8 (7.5) 164.6 (8.8) 166.9 (8.8) 0.163

Weight (kg) 122.4 (24.9) 129.6 (19.2) 119.8 (15.3) 0.287

BMI 46.6 (6.9) 47.9 (6.7) 42.9 (3.9) 0.028

The values are expressed as mean (SD) except sex: number (percent). Statistical difference:p< 0.05 BMIbody mass index,Ffemale,Mmale

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intervention groups (P= 0.3). According to 1RM results, up- per limb muscle strength did not change significantly by aer- obic exercise in intervention groups in comparison with the control group but a significant increase was found in the AS group (P= 0.004). Comparing intervention groups showed that mean changes in 1RM variables increased in the AS group (P= 0.03).

Physical Activity

Adherence (day and time) to aerobic exercise prescription in the first 6 weeks post operation was not significantly different to the second 6 weeks, and no significant difference was ob- served between the two intervention groups (p> 0.05).

Results of 24-h Food Records

Regardless of the study group, patterns of change of calorie intake, percent and grams of carbohydrate, percent and grams of protein, and gram of fat from baseline to the end of the study were significantly decreased (the smallestPvalue re- ported was 0 < 001). No significant difference was seen in the 24-h food records between the three groups (the smallestP value reported was 0.12).

Discussion

The present study is a randomized clinical trial to evaluate the effects of bariatric surgery and 12 weeks of aerobic or aerobic- strength exercise on anthropometric indices and functional capacity of patients with body mass index equal to or higher than 35 kg/m2. Sixty patients entered the study and data from 55 patients were analyzed at the end.

Given that the method of surgery may have an impact on outcomes of anthropometric and functional capacity, distribu- tion of patients who had undergone RYGB or SG was evalu- ated in all the three groups, and no significant difference was found (p> 0.05).

The Impact of Physical Activity on Anthropometric Indices after Bariatric Surgery

According to ACSM guideline, normal PBF for men is considered 11.5–14.8 (20–29 years), 15.5–18.2 (30–

39 years), and 18.4–20.6 (40–49 years) in men. Normal PBF for women is considered 17.3–19.4, 18.2–20.8, and 20.8–23.8 in the mentioned age range, respectively.

However, lean body mass is calculated by specific formula based on total body weight and height. However, generally,

Table 3 Compare anthropometric measurements between the three groups

Variables Aerobic vs control Aerobic-strength vs control Aerobic-strength vs aerobic

Mean differences CI pvalue Mean differences CI pvalue Mean differences CI pvalue

Weight (kg) 4.3 7.6 to1.0 0.012 4.3 7.7 to0.9 0.015 0.02 3.5 to 3.5 0.988

BMI 0.8 2.2 to 0.6 0.279 0.5 1.9 to 0.9 0.487 0.3 1.2 to 1.8 0.722

FM 5.4 9.7 to1.1 0.014 6.2 10.6 to1.9 0.006 0.8 5.3 to 3.7 0.728

FAT% 3.7 7.0 to0.4 0.026 5.3 8.6 to1.9 0.003 1.6 5.0 to 1.9 0.367

FFM 2.4 0.9 to 5.8 0.155 3.7 0.2 to 7.3 0.038 1.3 2.3 to 4.9 0.473

SMM 0.2 1.7 to 1.3 0.799 0.2 1.3 to 1.8 0.757 0.4 1.1 to 2.0 0.580

Statistical difference:p< 0.05

CIconfidence interval,BMIbody mass index,FMfat mass,FAT%fat percent,FFMfat free mass,SMMskeletal muscle mass Table 2 Changes in

anthropometric measurements over time in the three groups

Variables Control (n= 19)

Aerobic (n= 18)

Aerobic-strength (n= 18)

Before After Before After Before After

Weight (kg) 121.2 (25.0) 101.2 (22.7) 127.6 (18.8) 102.5 (18.4) 119.7 (13.6) 94.8 (9.7) BMI 46.6 (7.1) 38.1 (7.4) 48.1 (6.7) 38.6 (6.4) 43.0 (3.9) 34.2 (3.4) FM 61.7 (16.4) 50.7 (14.9) 65.8 (11.4) 48.8 (12.7) 57.2 (7.8) 39.3 (7.3) FAT% 50.9 (6.9) 49.6 (6.2) 51.4 (2.9) 47.2 (5.6) 47.9 (4.7) 41.5 (6.5) FFM 59.4 (14.9) 50.5 (10.3) 61.8 (9.0) 53.7 (8.5) 62.4 (10.2) 55.5 (8.9) SMM 32.4 (6.5) 28.6 (6.3) 34.8 (5.4) 29.9 (5.0) 35.2 (6.2) 30.8 (5.7) The values are expressed as mean (SD)

BMIbody mass index,FMfat mass,FAT%fat percent,FFMfat free mass,SMMskeletal muscle mass

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it is estimated that 60–90% of body weight belongs to lean body mass in average population [22].

Evidence shows that regular physical activity is one of the most important predictors of continued weight loss after bar- iatric surgery in the long term [27–29]. Outcomes of a system- atic review in 2012 suggested that exercising after bariatric surgery increased weight loss of 3.5 kg on average [30].

Also, Livhits et al. and Vatier et al. reported greater reduction in BMI (4.2%) and more weight loss in physically active in- dividuals after bariatric surgery, respectively [21,31].

Consistent with previous studies, our results suggest that aerobic or aerobic-strength exercise are associated with signif- icant changes in FM, PBF, and weight loss. BMI decreased in all groups without significant difference among them.

There are few studies in this area with some controversies which showed that no positive relation was evident between exercise and weight loss after bariatric surgery [32–35]. For example, one study showed that doing strength and resistance exercises did not increase weight loss and reduce PBF, FM, or FFM significantly 4 months after bariatric surgery, comparing to the control group. However, the number of participants in this study (eight subjects) was an important limitation [36].

In Castello et al.’s experience, 12 weeks of aerobic exercise after bariatric surgery, weight loss, and changes in BMI and FM were similar in both the control and intervention groups [32]. Their outcomes were similar to Shah and colleague’s finding that assessed the effect of high-volume exercise pro- gram on patients after surgery [35]. Although, the mentioned studies had some limitations, including small sample size or

not assessed calorie intake which may affect the positive re- sults of exercise. In the present study, patients received spec- ified diet and no significant differences were found in calorie intake between the three groups.

There was no evidence in comparison between the effects of aerobic or resistance exercise on weight loss after surgery.

According to our results, it seems that adding resistance exer- cise to the aerobic program did not have an additive effect on weight loss and trial groups had no significant differences in this item, but we found some positive effect of resistance exercise on FFM changes.

FFM is one of the most important anthropometric indices.

Webster et al. found that FFM reduction in obese individuals (mean BMI = 35 kg/m2) should not exceed more than 22% of the total amount of weight loss, because it involves resting met- abolic rate (RMR), regulating body temperature, and functional capacity [37]. So, greater loss of FFM in the long term raises the risk of weight gains in patients who have undergone bariatric surgery [38]. Unfortunately, 30–35% of weight loss is related to FFM in 6 months after RYGB which could be explained by rapid, excessive weight loss and inadequate protein intake [39].

According to our results, FFM was decreased in all the three groups but control and A group lost more FFM than did AS group. A longitudinal study that assessed the effects of exercise after obesity surgery found significant reduction (28%) in FM in the exercise group, while lean body mass (LMB) increased (8%), compared to the non-exercise group.

They concluded that adherence exercise program in the first 6 months following surgery has significant impact in Table 4 Functional capacity changes over time in the three groups

Variables Control (n= 15) Aerobic (n= 18) Aerobic-strength (n= 16)

Before After Before After Before After

12MWRT 540.6 (177.4) 757.5 (181.7) 702.2 (185.1) 973.8 (156.9) 776.0 (105.1) 1070.0 (141.7)

1RM 12.5 (6.7) 11.9 (7.0) 15.9 (7.1) 14.8 (6.2) 17.7 (9.4) 18.7 (9.0)

Sit-to-stand test 7.8 (5.3) 17.0 (6.2) 13.6 (6.6) 22.2 (8.4) 15.3 (4.6) 24.6 (6.0)

The values are expressed as mean (SD)

12MWRT12 min walk run test,1RMone repetition maximum

Table 5 Compare changes in functional capacity in three groups

Variables Aerobic vs control Aerobic-strength vs control Aerobic-strength vs aerobic

Mean differences CI pvalue Mean differences CI pvalue Mean differences CI pvalue

12MWRT 110.7 23.5 to 198.0 0.014 150.4 56.8 to 243.9 0.002 39.6 42.6 to 121.9 0.337

1RM 0.8 0.9 to 2.5 0.348 2.7 0.9 to 4.6 0.004 1.9 0.2 to 3.7 0.031

Sit-to-stand test 3.0 2.4 to 8.4 0.267 4.3 1.5 to 10.2 0.142 1.3 3.9 to 6.6 0.608

Statistical difference:p< 0.05

CIconfidence interval,12MWRT12-min walk run test,1RMone repetition maximum

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maintaining muscle mass [40]. Ng et al., evaluated efficacy of aerobic-strength exercise on weight loss after bariatric surgery and showed that supervised training led to preservation of lean body mass (LMB). So, fat mass loss was eight times more than LMB loss [41].

However, some studies suggested that the reduction of FFM is not affected by exercise program postoperatively due to excessive rapid weight loss [34–36]. Castello et al.

showed that 12 weeks of supervised aerobic exercise had no significant effect on FFM. In this study, the training and con- trol groups lost their muscle mass equally and the authors discussed that such outcome may be due to the type of exer- cise that was given to the participants [32]. Our data showed that although the AS group lost a lower amount of FFM in comparison to control and A group, the difference was not significant with A group. As we discussed earlier, it can be explained by regarding the high speed of FFM lost in the first months after surgery [32].

To the best of our knowledge, this is the first study to assess the differences between aerobic or aerobic-strength exercise on body composition and weight loss. Bariatric surgery pro- motes excessive weight loss and improves metabolic status and is considered as the most effective treatment in the major- ity of severely obese patients, but its long-term effects are still not clearly understood. Melton et al. showed that after bariat- ric surgery, 11% of patients could not achieve optimal weight loss for some reason, such as age, cognitive disorder, in- creased BMI, diabetes type II and etc. [42].

Since physical activity is known as an effective factor on weight loss after surgery [21,43], determining an optimized exercise prescription helping patients to reach optimal weight loss and improve body composition is an important aspect of follow-up system after bariatric surgery [42,44,45].

In conclusion, we found that aerobic or aerobic exercises promote higher weight loss in comparison to physically inac- tive patients postoperatively and has positive impact on fat mass reduction as well as preservative effect on muscle mass with adding resistance program.

The Impact of Physical Activity on Functional Capacity after Bariatric Surgery

According to our results, functional capacity was improved in both A and AS groups after surgery and 1RM was increased in AS group significantly. However, according to STS test re- sults, no significant difference was observed between the three groups. (Table5).

Obesity is related to mobility impairments and low aerobic capacity and muscle strength. Obese patients walk slower and have poor ability to change position from sitting to standing and weak balance [46]. Although studies have shown that physical activity increases after bariatric surgery, the pattern is still not fully understood [21,30] King et al. showed that

bariatric surgery leads to noticeable increase in physical activ- ity [47]. Other studies in this area confirmed the results and demonstrated that patients, who become physically active af- ter bariatric surgery, have greater functional capacity, includ- ing cardiovascular capacity and physical fitness [47–49].

This improvement in functional capacity after bariatric sur- gery could be attributed to postoperative weight loss or an increase in physical activity. A systematic review and meta- analysis at 2016 reported that physical activity increases after surgery, but the pattern and its relation to physical function and weight loss are unidentified yet [27].

Most of the studies have used SF-36 questionnaire in order to evaluate physical performance, and they demonstrated that bariatric surgery leads to significant increase in physical per- formance [18,47,50–59]. In some cases, functional tests such as 6MWT were used to assess functional capacity [46,48,57, 58,60–66]. Monitoring functional capacity after bariatric sur- gery in the mentioned studies showed positive results in mor- bidly obese patients [48, 57, 60, 63, 64, 67]. A systematic review and meta-analysis indicated that 6MWT distance in- creased to 75 m in 3–6 months postoperation and reached 184 m in 6–12 months after surgery [27]. Evaluation of post- operative functional capacity improvement without any phys- ical activity intervention was an important limitation in such studies. However, Castello et al. evaluated impact of aerobic exercise on functional capacity and reported significant in- crease in 6MWT only in the intervention group [32]. We used 12MWRT which was previously used for obese individuals [32,68,69] and found that the covered distance increased in the three groups but the AS and A groups covered longer distances in comparison with the control group (Table 5);

therefore, it could be concluded that doing aerobics and/or aerobic-strength exercise after bariatric surgery further in- creases functional capacity and patients meet more benefits of cardiovascular fitness. It should be noted that no significant difference was seen between the A and AS groups in this case.

To the best of our knowledge, it is the first time that impact of aerobic and strength exercise training together was assessed on functional capacity after bariatric surgery. It seems that increase in aerobic functional capacity in both groups is due to aerobic exercise.

Muscle strength and functional capacity are important fac- tors to perform daily activities [70]. After bariatric surgery, patients experience rapid weight loss and surely, noticeable decrease in FFM happened [69,71]. High-speed weight loss, malabsorption due to surgery, and inadequate protein intake lead to muscle tissue wasting and reduction in the strength of muscles. Previous studies reported significant reduction in absolute strength after bariatric surgery [46,60,61,69,72].

In the study by Stegen et al., dynamic and static muscle strength was reduced considerably due to significant weight loss after the surgery [36]. Hue et al. demonstrated that al- though morbidly obese patients experienced significant

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muscle force loss after surgery, their body could be adapted well to this change due to body weight loss in relation to even decreased force [49]. However, studies in this area are limited.

Stegen et al. prescribed strength exercise training to eight pa- tients who underwent bariatric surgery and figured out that while fat-free mass loss is inevitable, postoperative exercise programs not only could preserve muscle strength but also had significant impact on increasing dynamic strength of most muscles. Moreover, the result of sit-to-stand test improves significantly [36]. According to Huck’s study, 12 weeks of supervised resistance training (RT) has improved functional strength (sit-to-stand test) in both the control and intervention groups and also showed some progression in flexibility and hand grip strength [34].

Along with previous studies, our study showed slight de- crease in pectoral muscle one-repetition maximum (1RM) in the control and A groups but significant increase in the AS group. Moreover, the number of times patients could stand up from the chair in sit-to-stand test improved in the three groups which indicated that bariatric surgery-induced weight loss had great impact on lower extremity function. It is assumed that the same results in the sit-to-stand test in all the three groups is related to the kind of exercises prescribed in the AS group or type of test performed.

Designing exercise program in patients undergoing bariatric surgery is critical in terms of increasing physical performance.

But, it remains unclear which exercise is better tolerated by operated patients and which type of exercise training could fur- ther increase functional capacity and muscle strength [27].

We conclude that doing aerobics or combined exercise could improve the impact of bariatric surgery on functional capacity, but further investigation is need.

Limitation and Strength

To the best of our knowledge, no study has been done to assess the impact of aerobic and strength exercise training together on body composition, aerobic and strength capacity, and weight loss after bariatric surgery. The limitations of the study were short duration of trial and lack of supervision on the exercise program. Longer follow-up may be needed to show further difference in body composition changes between the two surgery methods. The other limitation was heteroge- neous nutritional characteristics due to different procedures.

The sample size of our study was small which is indicated in the wide confidence intervals. The results should be con- firmed in the future studies with larger sample size.

Conclusion

In conclusion, 12 weeks of aerobic or aerobic-strength exer- cise after bariatric surgery leads to greater weight and fat mass

reduction in obese individuals with BMI ≥35 kg/m2. Doing exercise after surgery is more effective for improving the aer- obic performance than surgery alone. Moreover, adding strength exercise to aerobic exercise after bariatric surgery reduces muscle mass loss and increases 1RM. Further studies are needed in order to assess the long-term effects of exercise after weight loss surgery.

Acknowledgments This research has been supported by Tehran University of Medical Sciences and Health Services Grant (No:

IRCT201512297903N7).

Compliance with Ethical Standards

Conflict of Interest The authors declare that they have no conflict of interest.

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

Ethical Approval All procedures performed in the study were in accor- dance with the ethical standards of the Tehran University of Medical Sciences (TUMS) and Health Services Grant (No: IRCT201512297903N7) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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