Abstract
Obesity predisposes an individual to develop numerous co-morbidities including type 2 diabetes and represents a major healthcare issue in many countries worldwide. Bariatric surgery can be an effective treatment option resulting in profound weight loss and improvements in metabolic health. However, not all patients achieve similar weight loss or metabolic improvements. Exercise is an excellent way to improve health, with well-characterized physiological and psychological benefits. This article reviews the evidence to determine whether there may be a role for exercise as a complementary adjunct therapy to bariatric surgery. Objectively measured physical activity data indicate that most bariatric surgery patients do not exercise enough to reap the health benefits of exercise. While there is a dearth of data on the effects of exercise on weight loss and weight loss maintenance following surgery, evidence from studies of caloric restriction and exercise suggest that similar adjunctive benefits may be extended to patients who perform exercise post bariatric surgery. Recent evidence from exercise interventions following bariatric surgery suggests that exercise may provide further improvements in metabolic health, compared to surgery induced weight loss alone. Additional randomized controlled exercise trials are now needed as the next step to more clearly define the potential for exercise to provide additional health benefits following bariatric surgery. This valuable evidence will inform clinical practice regarding much-needed guidelines for exercise following bariatric surgery.
Keywords: gastric bypass surgery, exercise, physical activity
The Problem: Obesity is a Disease with Few Effective Treatment Options
The incidence of obesity, defined as a body mass index (BMI) of >30 kg/m2, has reached epidemic levels in the US and other developed nations. In the U.S. between 2009 and 2010, the age-adjusted prevalence of obesity in adult men was 35.5% and 35.8% among in women1. Although there does appear to be a plateau with general obesity prevalence between 2011–2012 being similar to 2009–20102, projections indicate that by 2030, 86.3% of U.S. adults will be overweight or obese and 51% obese3. Moreover, the prevalence of severe obesity continues to rise4.
There are considerable negative health consequences associated with excess weight, to the extent that obesity has recently been classified as a disease by the American Medical Association5. Both overweight and obesity puts individuals at risk for adverse health outcomes including type 2 diabetes, cancer, hypertension and cardiovascular diseases6,7 as well as depression and other psychological disorders8 and is associated with significantly higher all-cause mortality9. Thus, it is critical to consider the most effective intervention strategies to lower the health risk and economic costs associated with obesity. Bariatric surgery is an effective treatment option with Roux-en-Y gastric bypass (RYGB) being the most commonly performed bariatric surgery procedure in the US. RYGB surgery results in dramatic weight loss and diabetes remission in a large percentage of patients15–17. In non-surgery patients, routine exercise is considered to be an important, if not necessary part of any long-term weight loss program, although performing exercise alone does not result in substantial body weight reduction in non-surgery patients18. Very little is known, however, about whether engaging in exercise post-surgery can provide additional improvement in health outcomes. This article will review the current evidence to determine whether there may be a role for exercise as a therapeutic option for the bariatric surgery patient with a focus on weight loss, maintenance of weight loss, and beneficial physiological/metabolic adaptations. While there are relatively few studies of exercise/physical activity in bariatric surgery patients to date, we will also consider evidence for the benefits of exercise from the context of non-surgery patients and diet induced calorie restriction. We will also identify future research directions and highlight important unanswered questions in this new and emerging field.
Exercise As An Adjunct Therapy For Further Weight Loss And Improved Body Composition Following Bariatric Surgery
Bariatric surgery produces significant weight loss and drastic improvements in metabolic health. It is not an infallible treatment option, however, and long-term effectiveness has not been clearly defined. One problem is the lack of studies reporting long term (>1 year) follow-up in cohorts with adequate retention rates14. A number of reports suggest that 10–30% of bariatric surgery patients experience suboptimal weight loss20,23,24. However, this number may be significantly higher when patients who drop out of the study are accounted for25. While further studies are needed to understand the physiological and behavioral origins of inter-patient variation in surgery induced weight loss, current evidence indicate that greater BMI, age, diagnosis of type 2 diabetes, cognitive function, personality, and mental health are strong predictors of suboptimal weight loss26–28. For bariatric surgery patients who experience suboptimal weight loss, exercise may prove to be an important adjunct therapy. Indeed, exercise administered alone is not generally viewed to cause substantial body weight reduction18. The consensus on the ability of exercise to induce weight loss is described in the Physical Activity Guidelines Committee Report, which states that exercise alone typically results in weight loss of <3% of initial body weight29. However, exercise in combination with diet induced caloric restriction does produce an additive reduction in body weight18, even in individuals with severe obesity30. However, there is scant equivalent evidence in the context of bariatric surgery. A recent study, which examined the efficacy of a 6-month exercise intervention (120 min/wk. of mostly treadmill walking) on severely obese participants, did not observe any additional impact on RYGB surgery-induced weight loss or fat mass31. These findings are similar to those of Shah et al. who showed that a high volume exercise prescription following bariatric surgery had no impact on body weight and waist circumference when compared to a control group32. One report indicated that excess weight loss was improved at 12-, but not 36-months postoperatively by attending semi-structured exercise education classes33. The lack of an exercise effect on weight in these intervention studies is likely due to the strong influence of surgery. These data do not, however, rule out the possibility that a higher dose/intensity of exercise may elicit additional weight loss, or alter body composition or regional adiposity in a favorable way, following surgery. For example, in non-surgery patients, aerobic exercise is particularly effective at reducing visceral adipose tissue (VAT)34, a fat depot that is strongly linked to hepatic insulin resistance and type 2 diabetes35.
A systematic review by Chaston et al. suggests that loss of fat free mass (skeletal muscle, bone and organs) accounted for 31.3% of weight loss with RYGB surgery39. The clinical significance of FFM loss has not been fully investigated, but may be undesirable if excessive40. FFM accounts for a significant portion of resting energy expenditure (REE)41 and regulation of core body temperature, and it has been hypothesized that FFM loss may predispose weight regain in the long term42. For the older bariatric surgery patient, the loss of skeletal muscle and bone density may have a negative impact on physical function, progression of sarcopenia and quality of life43. Exercise, particularly resistance exercise, is an excellent way to maintain muscle mass in older adults44 and may also be effective for the older bariatric surgery patient. In the context of diet induced calorie restriction, a number of randomized studies have shown that during 16 weeks of weight loss on a low calorie diet, supervised exercise alleviated the loss of FFM45–47. A report by Metcalf et al., indicates that duodenal switch patients who self report as exercisers (30 min of exercise per session, >3 sessions a week) have 28% higher loss of fat mass and 8% higher gain in lean mass when compared to a non-exercise group48. To date, the published data support a potential role for exercise to elicit positive changes in body composition following bariatric surgery. Large randomized controlled exercise trials with comprehensive phenotyping (metabolic and body composition) of participants are needed to provide the next level of evidence to investigate the possibility of exercise as a feasible adjunct therapy to bariatric surgery.
Exercise For Weight Loss Maintenance Following Bariatric Surgery?
A proportion of bariatric surgery patients also experience significant weight regain and attenuation in the recovery from comorbidities49–51. In the context of diet induced calorie restriction, maintaining weight loss is a well-recognized problem, with one report suggesting that 12–18 months following weight loss, 33–50% of initial weight loss is regained52. However, exercise has been shown to be beneficial for long term weight loss maintenance following calorie restriction53. Data from the National Weight Control Registry (NWCR)54 and from other investigations55,56 suggest that moderate intensity exercise is critical for maintaining weight loss. For example, an exercise intervention study by Jakicic et al., indicates that the addition of 275 min/wk. of physical activity in combination with a reduction in energy intake is necessary for maintenance of a 10% weight loss in overweight women53. The importance of higher doses of exercise to maintain weight loss has also been reported18. However, similar evidence has not been generated in the context of bariatric surgery, and it is not yet clear whether exercise may assist weight loss maintenance following surgery. Further exercise intervention trials are now needed to determine whether this is the case.
Can Exercise Provide Additional Metabolic Improvement Following Bariatric Surgery?
In addition to weight loss, bariatric surgery also rapidly improves glycemic control and insulin sensitivity, effects that occur over discrete time periods following surgery and are mediated by a number of mechanisms. Within weeks of surgery, caloric restriction improves hepatic insulin sensitivity as evidenced by decreased in HOMA-IR, a surrogate index of hepatic insulin sensitivity57,58. Hyperinsulinemic euglycemic clamp with stable isotopic tracer methodology confirms that endogenous glucose production, an indicator of hepatic insulin sensitivity, improves soon after RYGB surgery59. Studies utilizing the glucose clamp method also reveal that the immediate metabolic benefits of bariatric surgery do not extend to improvements in peripheral tissue insulin sensitivity59,62. Indeed, a report showed that 1-month following RYGB surgery and substantial weight loss (~11%), peripheral insulin sensitivity did not improve59. This is significant, however, as skeletal muscle is the primary peripheral tissue responsible for disposal of ~80% of glucose following a meal. The long term improvements in peripheral tissue insulin sensitivity following bariatric surgery occur in proportion to weight loss54,55 which typically consist of a ~50% reduced whole body fat mass and a ~60% decrease in visceral adipose tissue after one year73,74. However, even with significant weight loss one year following RYBG surgery, peripheral insulin sensitivity remains low compared to lean metabolically healthy individuals7,75,10,11. In this context, exercise may be beneficial to improve peripheral tissue insulin sensitivity following surgery induced weight loss. Recently, a number of studies have examined whether an exercise training intervention following bariatric surgery provides additional improvements in glycemic control (Table 1). Shah et al., found that a 12-week exercise program following RYGB and gastric banding surgery improved glucose tolerance32. Results from a larger randomized controlled trial indicate that moderate aerobic exercise elicits additional improvements in insulin sensitivity and glucose effectiveness, i.e., the ability of glucose per se to facilitate glucose disposal, along with improved cardiorespiratory fitness during RYGB surgery-induced weight loss. These findings are significant as glucose effectiveness is an important contributor to glucose control76, is an independent predictor of diabetes across race/ethnic groups and varying degrees of obesity, and is reduced with impaired glucose tolerance, diabetes and aging77.
Table 1.
Source | Exercise Modality | Duration | No. of Patients |
Surgical Procedure | Principle Finding |
---|---|---|---|---|---|
Shah, 2011 | High-Volume Exercise Program (Cycling, treadmill walking, rowing) | 12 weeks | 33 | Gastric Banding & RYGB | Feasible in 50% of participants Improved Cardiovascular Fitness Improved postprandial incremental AUC |
Stegen, 2011 | Supervised Endurance and Strength Training Program | 4 months | 15 | RYGB | Improved Cardiorespiratory Fitness Improved Strength No effect on body composition |
Coen, 2015 | Treadmill Walking 120min/wk. | 6 months | 128 | RYGB | Improved Peripheral SI & SG Improved Cardiorespiratory Fitness No effect on Body composition |
Rothwell, 2014 | Exercise Educational Program Resistance Training and Pilates | 6 weeks | 137 | Gastric Banding | Greater %EWL at 12- but not 36-months for participants who attended >1 session |
Huck, 2014 | Supervised Resistance Training | 12 weeks | 15 | RYGB | Improved Cardiorespiratory Fitness Improved Strength |
Abbreviations: AUC; Area under the curve, RYGB; Roux-en-Y Gastric Bypass, SI; Insulin Sensitivity Index, SG; Glucose Effectiveness, %EWL; percent excess weight loss
Few studies have examined the myocellular mechanisms of improved muscle insulin sensitivity with surgery induced weight loss, however, reduced ectopic lipid deposition in type I and type II myofibers78 and improvements in mitochondrial function79,80 likely play key roles. Other mechanisms of improved muscle insulin sensitivity are likely similar to those described for calorie restriction induced-weight loss, including reduced inflammation, oxidative stress and improved fatty acid oxidation81,82. The addition of exercise to surgery induced weight loss stimulates increased metabolic flux and unique adaptations that may underlie further improvements in muscle insulin sensitivity (Figure 1). These include angiogenesis and increase capillary density, adaptations that also increase delivery of insulin and glucose to muscle83–85. Exercise also improves fat oxidation in skeletal muscle, mitochondrial function, metabolic flexibility and reduces lipotoxic species including ceramides that are thought to mediate insulin resistance86–88. It is beyond the scope of this review to detail all of these mechanisms, and so the reader is referred to other articles that review myocellular responses to exercise89,90. There is, however, an abundance of evidence that regular exercise elicits a wide array of adaptations that work in concert to improve skeletal muscle insulin sensitivity and glucose control and may also benefit whole body metabolic health via release of myokines into the circulation91. These positive exercise adaptations in conjunction with bariatric surgery induced weight loss likely underlie further improvements in muscle insulin sensitivity and potentially other aspects of whole body health.
β-cell function and hepatic insulin sensitivity also improve in the weeks following surgery. Studies that used frequently sampled intravenous glucose tolerance (FSIVGT) test to assess intrinsic β-cell function indicate that first phase insulin secretion and disposition index increase in type 2 diabetics one month following RYGB surgery60–62. Indeed, it was recently shown that preoperative β-cell function in patients with type 2 diabetes is important for surgery induced-improvement in β-cell function independent of postprandial release of glucagon-like peptide 1 release92. Again, these are aspects of metabolic function that regular exercise post-surgery may further improve. An 8-month high amount/vigorous intensity exercise program in sedentary overweight adults reduced the acute insulin response and improved disposition index, both indices of β-cell function, when compared to low amount/moderate intensity group93. Others have also shown that exercise can improve β-cell function94. Regular exercise can also improve hepatic insulin sensitivity95,96, potentially via reduction in intrahepatic lipid content97. When exercise was administered with caloric restriction, the intervention was better at reversing free fatty acid induced hepatic insulin resistance, when compared to an eucaloric exercise intervention98. Taken together, these studies describe the powerful effect of exercise to improve metabolic health by impacting multiple organ systems (muscle, liver and pancreas/β-cell), which likely provide additive benefit to bariatric surgery induced weight loss.
There have been a small number of exercise intervention studies in bariatric surgery patients that that have examined other aspects of health (Table 1), including cardiorespiratory fitness, an important cardiometabolic risk factor that is associated with risk of all-cause mortality116. Stegen et al., showed that a 4-month strength/endurance can improve cardiorespiratory fitness and physical function117, a finding that might have implications for older participants who undergo bariatric surgery. Coen et al. also showed that a moderate aerobic exercise intervention (6 months/walking) improved fitness in obese non-diabetic bariatric surgery patients31. Huck et al., reported that resistance training can improve cardiorespiratory fitness and muscle strength in bariatric surgery patients118. This evidence suggests that exercise is feasible for bariatric surgery patients and provides improvements in fitness and muscle strength in addition to the benefits of bariatric surgery-induced weight loss, data that strongly advocate for the inclusion of an exercise program to optimize health benefits during active weight loss following bariatric surgery.
How Physically Active Are Bariatric Surgery Patients?
Given the clear potential for exercise as an adjunct therapeutic option to bariatric surgery, the question arises: do bariatric surgery patients exercise? And do they exercise enough to elicit benefits in health? The physical activity habits of bariatric surgery patients have not been clearly described. A number of studies have compared psychosocial behaviors following substantial weight loss with bariatric surgery and dietary caloric restriction, and indicate that surgery patients have unique eating and physical activity behaviors. A case-controlled study by Klem et al., used data from the NWCR and compared gender, weight and weight loss matched surgery versus non-surgery weight loss subjects103. They found that surgical cases reported significantly lower kcals expended by medium and high intensity physical activity. A second case controlled study by Bond et al., also utilized data from the NWCR, found that surgical participants expended fewer overall calories through physical activity and particularly during high intensity activity104. A secondary analysis was conducted by splitting physical activity caloric expenditure into two categories (0–2000 and >2000 kcal) based on American College of Sports Medicine (ACSM) exercise guidelines for weight loss maintenance105. The results showed that a significantly smaller percentage of surgical participants (33%) compared to non-surgical participants (62%) reported expending >2000kcal per week104. Given the low level of physical activity reported, it is doubtful that there is any metabolic benefit being imparted to the patient.
A handful of studies have objectively measured physical activity in bariatric surgery patients using accelerometers or pedometers with mixed results (Table 2)111–114. Among the most thorough examination to date on PA levels following bariatric surgery, King et al. examined data from 310 participants in the Longitudinal Assessment of Bariatric Surgery-2 study who wore an activity monitor for ≥10hr/day for ≥3days pre- and 1-year post-surgery114. Overall, these participant increased PA by 1457 steps/day, however, there was a wide variation in change (from 7648 fewer steps/day to an increase of 17,205 steps/day). Furthermore, they engaged in a median of 23 high-cadence min/wk. in bouts of ≥10 mins, and only 11% reached ≥150 high-cadence min/wk. in bouts of ≥10 mins following surgery. Conversely, and depending on the PA variable examined, between 23.6 and 29% of participants were ≥5% less active 1-year post surgery, compared to pre-surgery. These data tell us that there is massive variation in change in PA following surgery, with a majority not increasing PA and some even decreasing PA. Importantly, all of the studies that objectively measured PA suggest that the majority of patients accrue significantly less than the 150min/wk. recommended in the physical activity guidelines by the American Diabetes Association (ADA) and American College of Sports Medicine (ACSM) and likely do not derive any metabolic benefit.
Table 2.
Source | Methodology | Time Point | No. of Patients |
Surgical Procedure | Principle Finding |
---|---|---|---|---|---|
Bond, 2010 | Accelerometers Paffenbarger PA Questionnaire | Pre- & 6 months post-Op | 20 | Gastric Band (65%) RYGB (35%) | Non-significant decreases in MVPA Change in objectively measured moderate/vigorous intensity PA is less than self-reported change |
Chapman, 2014 | Ankle Pedometer Tri-Axial Accelerometer | 12–18 months post-GB 6–18 months post-SG | 40 | Gastric Band (62.5%) Sleeve Gastrectomy (37.5%) | ~5% of time in MVPA Median daily step count was 9108±4360 |
Josobeno, 2011 | Tri-Axial Accelerometer | 2–5 years post-Op | 40 | RYGB | %EWL was associated with MVPA |
King, 2012 | Wrist Accelerometer | Pre-op & 1 year post-Op | 310 | RYGB (69.0%) Gastric Band (21.6%) | PA increased significantly post-Op Wide variation in change in PA 24–29% of participants were ≥5% less PA post-Op |
Abbreviations: RYGB; Roux-en-Y Gastric Bypass, %EWL; percent excess weight loss, Moderate-to-Vigorous Physical Activity; MVPA, PA; Physical Activity, SG; Sleeve Gastrectomy, GB; Gastric Banding
Unanswered Questions and Future Directions.
There are number of pertinent questions that remain unanswered relating to the clinical and physiological role of exercise following bariatric surgery:
What is a feasible and effective physical activity intervention following surgery in terms of dose (duration and intensity) and modality (walking, swimming, cycling)?
Does increased exercise/PA provide additive weight loss or fat mass loss, particularly visceral fat, following bariatric surgery?
Is regular exercise an important factor for long-term weight loss maintenance following bariatric surgery?
Does exercise/PA target specific health risks (co-morbidities) in the post bariatric surgery population? Do these occur independent of change in weight of body composition?
Loss of lean mass, including muscle and bone, following surgery may have detrimental consequences on physical function and mobility in older adults and may impact energy expenditure and predispose weight regain.
Does exercise following surgery preserve lean muscle mass in specific subgroups of surgery patients, for example 1) those who rapidly lose weight (and lean mass) following surgery 2) elderly subjects who may be prone to greater loss of lean mass following surgery compared to young.
Does exercise following bariatric surgery improve muscle function, reduce osteoarthritis, knee pain, and improve quality of life in older adults?
Summary.
Obesity, severe obesity and associated co-morbidities are long term and major healthcare problems in the U.S. and worldwide. Bariatric surgery is the most effective treatment option for many but the benefits are not universal to all patients. Furthermore, the long term (>1 year) effectiveness of bariatric surgery still remains unclear. Exercise clearly elicits a multitude of beneficial health effects. We now have objective evidence that bariatric surgery patients are not very physically active and thus represent a patient population who may benefit greatly from exercise. Further randomized controlled trials are now needed as the next step to more clearly define the exercise dose/intensity needed to provide additional health benefits following bariatric surgery and to elucidate the mechanisms by which these improvements are mediated. This valuable evidence will also inform clinical practice regarding much-needed guidelines for exercise following bariatric surgery.
Acknowledgments
The authors wish to thank the members of the Goodpaster/Coen laboratory for stimulating discussions on the topics of exercise and bariatric surgery. This work was supported in part by grants from the National Institute on Ageing (AG044437, PMC) and the National Institute of Diabetes and Digestive and Kidney Diseases (DK078192, BHG).
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