Bariatric Surgery in Adults with Obesity: the Impact on Performance, Metabolism, and Health Indices

This systematic review summarizes current evidence on the impact of bariatric surgery (BS) on physical performance, metabolic, and health indices in adults with obesity. This systematic review suggests that BS induced significant reductions in body weight, fat mass, and fat-free mass in individuals with obesity. Additionally, BS may improve many physical fitness and health indicators. Observed improvements manifest during a distinct period of time. To date, studies on BS and performance have been small in number, nonrandomized in design, and not controlled regarding gender distribution and/or post-surgery follow-up. Future studies should further investigate concerns associated with understanding of BS outcomes to improve these outcomes with potential benefits for quality of life, disability, mortality, morbidity, and overall BS success.

The minute ventilation/carbon dioxide production VO 2 Oxygen uptake W W a t t W/H Waist-to-hip ratio WC Waist circumference 50%VO 2 RP Post-exercise Oxygen Uptake Recovery Kinetics

Introduction
Severe obesity, defined as a body mass index (BMI) of at least 35 kg m 2 [1], is strongly associated with several health complications [2][3][4] along with significant impairments in physical capacity and overall fitness parameters [5][6][7][8]. Bariatric surgery (BS) is emerging as an important option for those suffering from severe obesity when nonsurgical weight loss methods have been exhausted. In addition to the direct impact on weight loss, BS improves many health indicators during the post-operative period [9][10][11][12][13]. These changes were correlated with the quality of life and overall health parameters [13]. Changes attributed to BS at post-operative stages have focused mainly on body weight and composition changes, metabolic control, and energy adaptation [9,10,[14][15][16][17] alongside some research that has investigated physical functioning and fitness capacity outcomes. These latter outcomes are known to be relevant in the obesity context especially since they are considered important mediators in developing risk factors for cardiovascular disease in this population [18][19][20].
In light of what was discussed above, this systematic review aimed to summarize recent findings on the effects of BS alone, without any exercise prescription or lifestyle modification, on the most relevant cardiorespiratory (e.g., oxygen uptake, heart rate), performance (e.g., muscular strength, distance covered), and health (e.g., autonomic nervous system modulation, metabolic parameters) outcomes in adults with obesity undergoing BS.
A good understanding of the effects of BS on cardiorespiratory, performance, and health outcomes is highly recommended for future intervention studies to improve these outcomes with potential benefits for quality of life, disability, mortality, morbidity, and overall BS success.

Eligibility Criteria
This systematic review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement [21]. The population, intervention, comparator, outcomes, and study design (PICOS) approach was used to identify the inclusion criteria (Table 1). Only studies with a longitudinal design, of any duration, that have examined effects of BS on anthropometric characteristics and body composition (e.g., body weight, body fat, body mass index), physical performance (e.g., muscular strength, physical capacity), cardiorespiratory fitness and function (e.g., oxygen uptake, heart rate, heart rate variability), and energy expenditure and metabolism parameters (e.g., total energy expenditure, insulin resistance, lipid oxidation), in individuals with obesity undergoing any recognized surgical bariatric procedure, were eligible for inclusion. Studies were included in the current systematic review if they were in accordance with the following criteria: (1) published in peerreviewed journals; (2) included adults and older of both genders; (3) compared BS outcomes at pre-and at post-surgery. Studies were excluded if they (1) assessed other types of interventions (in addition to the surgery), (2) reported only subjective measures, or (3) were not written in English. Moreover, review articles were not included in the current systematic review.

Literature Search Strategy
Literature searches were conducted in four electronic databases, including PubMed, ISI Web of Knowledge, Web of Science, and SPORTDiscus. The following key terms (and synonyms searched for by the MeSH database) were included and combined using the operators "AND," "OR," and "NOT": "anthropometric characteristics" or "body composition" or "physical performance" or "physical capacity" or "fitness" or "physical activity level" or "functional capacity" or "muscular performance" or "muscular strength" or "anaerobic capacity" or "aerobic capacity" or "cardiorespiratory function" or "cardiopulmonary function" or "energy expenditure" or "respiratory quotient" or "energy metabolism" or "cardiac autonomic control" or "heart rate variability" or "metabolic parameters" or and "bariatric surgery" or "obesity surgery" or "weight loss surgery" or "metabolic surgery" or "gastric bypass" or "gastric banding" or "sleeve gastrectomy" or "biliopancreatic diversion" or "duodenal switch." The search was completed with a manual search of reference lists from key papers. Since the scope of this review is large in terms of outcome measures, a systematic review and not a metaanalysis was performed.

Study Selection
The final screening was performed by the principal investigator (GJ) based on the relevance of the inclusion and exclusion criteria and the identified items for assessing the effects of BS on anthropometric characteristics and body composition (e.g., body weight, body fat, body mass index), physical performance (e.g., muscular strength, physical capacity), cardiorespiratory fitness and function (e.g., oxygen uptake, heart rate, heart rate variability), and energy expenditure and metabolism parameters (e.g., total energy expenditure, insulin resistance, lipid oxidation), in adults with obesity of both gender undergoing BS using PICOS criteria. If the citation showed any potential relevance, the abstract was screened. When abstracts indicated potential inclusion, full-text articles were reviewed.

Post-operative Body Composition Changes and Weight Loss
Due to the research context, all of the studies include postoperative body composition and weight loss as their primary outcome. Body composition changes and weight loss were generally reported as FM (%, kg), FFM (%, kg), BW (kg), BMI (kg/m 2 ), AC (cm), waist circumference (cm), hip circumference (cm), and W/H ratio. All studies reported a significant improvement in post-operative body composition and weight loss (Tables 3 and 4). These improvements were detected at  [9,14,16,24,26,27,33,34,37,39,45,55,66]. Some studies examined FFM changes over different post-operative periods and reported significant decreases in FFM (kg) values after a short postoperative follow-up (2 months) for up to 2 years.

Post-operative Physical Activity Level and Performance
Twenty-four of 48 studies examined the impact of BS on many performance components (Tables 3 and 4) and/or on the post-surgery physical activity levels ( Table 3) and used different assessment methods (objective and subjective) to compare outcomes with pre-surgery points. A majority of studies reported the impact of BS on exercise and functional capacity by evaluating various indices, such as gait speed and the time to rise from a chair five times [23]; the distance covered in meters [9,31,32,41,44]; exercise duration [28,31,35,47,54,56,61,64,66]; perceived exhaustion [32,63]; and the Functional Independence Measure [63]. These studies reported a favorable impact of BS on these outcomes [9,23,28,31,32,35,41,44,47,54,56,61,63]. In contrast, only Wilms et al. [64] did not find any favorable effect of BS on the distance covered ≥ 24 months post-surgery. Muscular performance has been evaluated by reporting absolute and relative grip strength [23,47,49,56], peak power, developed in Watts or relative to body weight [64], or leg extension performance [47]. Some results demonstrated that BS had a beneficial effect on grip strength [23] while other studies found no beneficial effect on grip strength, [47,49,56] and that it had a beneficial effect on leg extension performance [47] and on peak power relative to body weight [64].     Nine out of 48 of the selected studies assessed post-surgery physical activity levels and compared them to the pre-surgery period (Tables 3 and 4). Four of the studies used the validated Physical Activity Questionnaire [9,23,25,39] to evaluate subjective physical activity levels and did not report any changes in the post-surgery period compared to baseline. One study that utilized self-developed surveys to assess physical activity [16] showed an increase in the physical activity (PA) level at the 6th month post-surgery evaluation. Bond et al. [25] compared subjective evaluations using the Paffenbarger Physical Activity Questionnaire (PPAQ) and objective measurements using a triaxial accelerometer. They reported that 55% of responders meet the international guideline recommendations when subjectively assessed versus 5% who meet these recommendations when objectively assessed. For Liu et al. [38], the PA level reported via accelerometer did not improve 6 months after BS. Das et al. [29], Tam et al. [58], and Van Germet et al. [62] used a metabolic chamber for indirect calorimetry during the post-surgery period and found no significant changes [29,62] and even decreases [58] in the PA index among patients.

Post-operative Cardiorespiratory Fitness and Energy Expenditure
Details of the effects of BS on different cardiorespiratory fitness and energy indices expenditure are summarized in Tables 3 and 4. Eleven studies evaluated the effects of BS on cardiorespiratory capacity (oxygen consumption, oxygen uptake efficiency, heart rate max, ventilatory equivalent, lung capacity, and breathing frequency) using a treadmill [27,28,31,35,44,47,48] or an ergometer [30,39,64,66].
Carrasco et al. [16] Digital scale and a scale-mounted stadiometer + isotopic dilution with deuterium oxide (total body water) + Open-circuit indirect calorimetry using a ventilated chamber system + Simple survey to assess PA + HOMA-IR        Five studies [16,33,55,57,62] reported changes in substrate oxidation during the pre-operative and followup period. Compared with the pre-operative value, CHO oxidation decreased at the 3rd [57,62] and 12th month [57,62] post-surgery or had not changed at the 14th month post-surgery [55]. In terms of fat oxidation, Carrasco et al. [16] reported a significant increase in fasting lipid oxidation at 6 months post-surgery and a decrease [55] at 17 months post-surgery, and Tamboli et al. reported a decrease at 12 months post-surgery. In contrast, no changes were reported by Galtier et al. [33] at the 6th, 12th, and 18th months post-surgery [33].

Discussion
This systematic literature review indicates that undergoing bariatric surgery may procure several health benefits and improve some fitness and performance indicators regardless of the procedure. These improvements may be achieved after short-and/or mid-term post-operative periods. Despite these promising results, more consideration of candidate profiles prior to BS in addition to a longer follow-up with multiple visits is highly recommended to gain a fuller understanding of the influence of BS on the selected outcomes.

Post-operative Body Composition Changes and Weight Loss
Despite heterogeneity in participant age, baseline BMI, the surgical procedure used, and the technique used to assess body composition, studies revealed significant reductions in body weight and fat mass and a decrease in fat-free mass in individuals with obesity who underwent BS.
The significant body weight loss reported by studies on BS was essentially attributed to reducing energy intake and decreased absorption of nutrients [16,24]. However, it is important to mention that weight loss is also influenced by variations in the surgical technique, such as the size of the gastric pouch, the alimentary limb length, and the gastrojejunostomy diameter. In fact, the variation in the operative technique affects energy intake among patients leading to the interindividual variability of weight loss after surgery. On the other hand, many authors suggested that the metabolic adaptation that accompanies weight loss, in addition to variations in plasma levels of mediators derived from adipose tissue, such as leptin, was related mostly to loss of fat mass rather than to a decrease in fat-free mass [16,68,69].
Although caloric restriction seems to be the dominant mechanism in body weight reduction and weight loss maintenance, Gemert et al. [62] suggested that a decrease in CHO intake resulted in lower insulin levels, which increased lipolysis and decreased CHO and protein oxidation, procures a beneficial effect on weight loss success.
To conclude, a multitude of factors may be involved in explaining body composition changes and weight loss among BS patients. Considering that an appropriate and permanent reduction in energy intake is essential for long-term weight management in patients who have undergone BS, examining other potential explanations for the variability in weight loss between patients will help potentiate short-and long-term weight loss post-bariatric surgery.

Post-operative Physical Activity Levels and Performance
The effect of BS on post-surgery physical activity levels has been evaluated either subjectively using self-reported questionnaires [9,23,25], structured interviews [29], or simple surveys performed by the participants [16], or objectively using an accelerometer [25,38]. There is a great variation in how exercise is measured and the minimal threshold to define a physically active patient. Of these subjective evaluations, the results reported no changes in physical activity levels during the post-surgery period [9,23,29,39]. For Campos et al. [9], despite the reported improvements in body composition, cardio-respiratory performance, and functional capacity 6 months post-surgery, participants were still sedentary. These results might be related to a lack of consistency in performing physical exercise, as was experienced prior to surgery. Only one study by Carrasco et al. [16] reported an increase in physical activity and a decrease in sedentary behavior. This increase was related to weight loss. When using an accelerometer, Bond et al. [25] reported a near fivefold decrease in MVPA among participants compared to using a selfreported evaluation, and only one participant met the physical activity recommendations. Due to the lack of data on baseline variables regarding a "voluntary" change in physical activity level after bariatric surgery, how to determine post-surgery physical activity practices in bariatric surgery patients is still unknown.
Despite heterogeneity in participant age, baseline profile, surgical procedure used, and test performed, studies reported a positive impact of BS on many performance indicators among the patients. These improvements were related to muscular strength and physical function. For Alba et al. [22], relative muscle strength and physical performance improved between 6 and 12 months post-operatively despite declines in lean mass and absolute muscle strength. Moreover, Alba et al. [22] reported a significant improvement in physical performance, attributed to the person's ability to perform activities of daily living, as reported recently by Campos et al. [9] among women with morbid obesity 6 months postoperatively after performing the incremental shuttle walk test (ISWT). De Souza et al. [32], Maniscalco et al. [41], Silva et al. [56], Tompkins et al. [60], and Vargas et al. [63] reported an increase in distance when performing a 6-min walking test (6-mWT) with a concomitant decrease in the rating of perceived exertion [32,60,63], and body mass and BMI decreases were the strongest predictors of that improvement [41,56,63].
A lower muscle strength was associated with the loss of lean body mass, which accompanied the reduction in fat mass, particularly in the first months after surgery [70,71]. Future studies evaluating both muscle mass and function, as well as fiber-type composition, will help better address this issue.

Post-operative Cardiorespiratory Fitness and Energy Expenditure
Individuals with severe obesity suffer from impaired cardiorespiratory fitness [72][73][74] that manifests primarily with a decreased VO 2peak . In response to BS, studies reported significant increases in VO 2peak relative to body weight fitness [27,28,30,31,35,39,44,47,52,54,61,66] and in lung function [9,41,66], suggesting improved aerobic fitness. However, absolute values were either unchanged [27,52,54,64,66] or decreased [28,30,35,39,44,47]. In the absence of any scheduled physical conditioning or exercise intervention, the improvement in VO 2peak relative to weight as well as the decreases in absolute VO 2peak post-surgery is mainly attributed to weight loss and body composition changes. However, it is important to note that a significant proportion of weight loss following bariatric surgery comes from muscle mass, especially in the initial post-surgical period [71,74], and oxidative muscle metabolism [70].
Therefore, it is unclear whether the increased aerobic capacity post-surgery reflects a fundamental improvement at the muscular and cardiorespiratory structure levels or is simply due to a lower energy requirement associated with exercise and reduced strain on the cardiopulmonary system during exercise. More recently, Daniel et al. [28] explored short-and long-term postsurgical effects on aerobic fitness parameters (absolute VO 2peak , OUES, and the time constant Tau (τ) in VO 2 kinetics) in a homogenous population after LSG. For these authors, the restoration of overall aerobic capacity could be achieved in the longterm post-surgery, allowing an improvement in overall aerobic performance. The latter will also depend on other physiological, environmental, and behavioral characteristics. Consequently, future studies should use multiple time points to give a better understanding as well as have an extended follow-up period, and they should consider other predictors of aerobic performance (e.g., stroke volume, aerobic enzyme, muscle fiber types) that are known to significantly affect these parameters.
Regarding REE, a meta-analysis by Astrup et al. [75] reported that post-operative weight loss is associated with a reduction in REE. For Carrasco et al. [16], the reduction in weight was associated with a significant decrease in the REE/ FFM ratio, and greater decreases were shown for those with higher REEs at baseline. In this context, many studies supported that a greater energy expenditure at the pre-surgical stage might be compensatory for energy intake increases when restricted nutritional intake is applied in the postoperative state; this compensation would disappear, leading to a greater reduction in REE in patients with obesity [16,29]. Another factor that would explain REE decreases in the post-surgical phase is fat mass loss. Carrasco et al. [16] observed a positive correlation between REE changes and the reduction in body fat at the 6-month follow-up. It seems that REE adaptation may be influenced by the reduction in adipose tissue and variations in plasma levels of mediators derived from this tissue in addition to other factors such favorable changes in eating habits, physical activity, and nutritional behavior [76][77][78], and on the absence of metabolic factors that predispose individuals to regain weight [77,79].
In terms of REE, TEE decreased significantly post-surgery among patients with obesity [29,51,57]. For Tamboli et al. [57], the decrease in TEE did not appear to follow the same pattern as the REE change after BS. A decline in TEE was observed until 6 months post-surgery, while no significant difference was reported at 12 months post-operatively. This decrease was proportional to the weight change within 6 months after surgery, and no further change in TEE occurred with ongoing weight loss. One possible explanation for this is the change in the PA level and diet-induced thermogenesis.
Obesity alters heart rate variability (HRV) that will manifest as a decrease in HRV due to decreased adrenoreceptor responsiveness, withdrawal of parasympathetic (vagal) tone, and/or increased sympathetic activity [83,84]. Weight loss improves parasympathetic cardiac modulation, observed as an increase in HRV [85]. Many studies have reported a significant association between weight loss and HRV improvement. For Alam et al. [22], several indices showed a prompt and persistent improvement with progressive weight loss, mainly for the QTVI, which improved as early as 1 month following surgery, and this change was further improved at the 12-month follow-up. Similarly, Maser et al. [42] showed that an average 28% reduction in BMI was accompanied by very significant improvements in all measures of HRV. Other factors, such as hormonal and metabolic factors, have been assessed to elucidate whether one or more of these factors are associated with modifications of cardiac autonomic balance post-surgery. For example, Bobbioni-Harsch et al. [24] showed that in addition to body weight loss, energy intake explained 20% of the variations in the time domain profile 3 months post-surgery. Kokkinos et al. [36] found that PHF and TP were both increased, indicating amelioration of cardiac autonomic function overall and the reversal of vagal impairment. Machado et al. [40] reported an overall HRV increase 6 months post-surgery, and this increase was more evident in men. Moreover, cardiac parasympathetic activity also increased but only in younger patients. Finally, HRV improvement was associated with lipid profile improvement at the 6th and 12th months post-surgery [46] and with insulin resistance decreases [65].

Limitations
It is important to note that the evidence presented in this review comes from different BS's procedures, e.g., metabolic versus restrictive, which compares different parameters difficult to interpret. While metabolic surgery, mainly gastric bypass and biliopancreatic diversion, is used to treat metabolic diseases, especially type 2 diabetes, the restrictive surgery is considered weight loss surgery. Considering that surgical technique is beyond the scope of this systematic review, however, most of our selected studies have been performed with patients who underwent a gastric bypass (GB) procedure, which may help sort out some interpretation. Moreover, studies were heterogeneous, and full descriptions of inclusion criteria and the adjustment by other covariates such as participant characteristics and duration of follow-up were not always reported. Finally, it is still important to mention that the lack of randomized control trial studies is really significant, and most of the studies recruited are very small in sample size in parallel to a short follow-up time which makes the results less appealing.

Conclusion
This review summarizes the benefits of BS alone for several performance and health indicators in adults with obesity. A key conclusion is that BS has a positive impact on body composition, physical functioning, metabolic parameters, and autonomic nervous system modulation and, to some extent, on energy expenditure, physical activity level, muscular strength, and peak oxygen consumption. As an effective approach to reducing body weight when nonsurgical methods are exhausted, the improvements procured by BS have been achieved both in a shorter period (less than 1 month) and with more extended period (more than 1 year); however, some studies reported that some of these benefits might disappear later on. Therefore, further studies are needed to determine the appropriate recommendations that still imprecise until today, focusing on managing post-surgery outcomes mainly by considering lifestyle modification that is likely to be of significant benefit.