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Changes in Energy Expenditure of Patients with Obesity Following Bariatric Surgery: a Systematic Review of Prospective Studies and Meta-analysis

  • Kun Li
  • Wentao Shi
  • Feng Zhao
  • Chengcan Yang
  • Qiancheng Dai
  • Bing Wang
  • Yousheng LiEmail author
Review Article

Abstract

We herein summarize the available literature on the effects of bariatric surgery (BS) on energy expenditure in individuals with obesity. We conducted a systematic literature review, and 35 prospective studies met our inclusion criteria. The findings indicate that BS contributes to increased diet-induced thermogenesis (DIT) and decreased total energy expenditure (TEE) and resting energy expenditure (REE) in patients with obesity. The meta-analysis demonstrated a significant decrease in TEE and REE within 6 months following BS. With the sustained decrease in REE, there was no further decrease in TEE between the 6- and 12-month follow-up. Increased DIT might explain the variance between the patterns of REE and TEE change. The postoperative decrease in REE/FFM and increase in REE/BW were observed. The changes in substrate utilization might be consistent with the change in the respiration quotient postoperatively.

Keywords

Bariatric surgery Energy metabolism Diet-induced thermogenesis (DIT) Respiration quotient (RQ) Substrate oxidation 

Notes

Acknowledgements

My deepest gratitude goes to Professor Yousheng Li for his constant encouragement and guidance. Without his consistent and illuminating instruction, this study could not have reached its present form.

Funding/Support

This study was supported by the Fundamental Research Program Funding of Ninth People’s Hospital affiliated to Shanghai Jiao Tong University School of Medicine (JYZZ022).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflicts of interest.

Ethical Statement

For this type of study (systematic review and meta-analysis), formal consent is not required.

Informed Consent Statement

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

Supplementary material

11695_2019_3851_Fig7_ESM.png (375 kb)
Supplementary Figure 1

Forest plot comparing RQ between the preoperative and postoperative periods. RQ: respiration quotient. (PNG 374 kb)

11695_2019_3851_MOESM1_ESM.tif (295 kb)
High resolution image (TIF 295 kb)
11695_2019_3851_Fig8_ESM.png (303 kb)
Supplementary Figure 2

Sensitivity analysis of the meta-analysis of the effect of bariatric surgery. (PNG 303 kb)

11695_2019_3851_MOESM2_ESM.tif (328 kb)
High resolution image (TIF 327 kb)
11695_2019_3851_Fig9_ESM.png (310 kb)
Supplementary Figure 3

Funnel plots assessing publication bias. (PNG 310 kb)

11695_2019_3851_MOESM3_ESM.tif (253 kb)
High resolution image (TIF 252 kb)

References

  1. 1.
    Afshin A, Forouzanfar MH, Reitsma MB, et al. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med. 2017;377(1):13–27.CrossRefGoogle Scholar
  2. 2.
    Faria SL, Faria OP, Buffington C, et al. Energy expenditure before and after Roux-en-Y gastric bypass. Obes Surg. 2012;22(9):1450–5.CrossRefGoogle Scholar
  3. 3.
    de Cleva R, Mota FC, Gadducci AV, et al. Resting metabolic rate and weight loss after bariatric surgery. Surg Obes Relat Dis. 2018;14(6):803–7.CrossRefGoogle Scholar
  4. 4.
    Westerterp KR. Diet induced thermogenesis. Nutr Metab (Lond). 2004;1(1):5.CrossRefGoogle Scholar
  5. 5.
    Higgins J, Altman DG. Assessing risk of bias in included studies. Cochrane handbook for systematic reviews of interventions: Cochrane book series; 2008. pp. 187–241.Google Scholar
  6. 6.
    Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ. 2009;339:b2700.CrossRefGoogle Scholar
  7. 7.
    Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–5.CrossRefGoogle Scholar
  8. 8.
    Busetto L, Perini P, Giantin V, et al. Relationship between energy expenditure and visceral fat accumulation in obese women submitted to adjustable silicone gastric banding (ASGB). Int J Obes Relat Metab Disord. 1995;19(4):227–33.Google Scholar
  9. 9.
    Flancbaum L, Choban PS, Bradley LR, et al. Changes in measured resting energy expenditure after Roux-en-Y gastric bypass for clinically severe obesity. Surgery. 1997;122(5):943–9.CrossRefGoogle Scholar
  10. 10.
    Sundstrom J, Bruze G, Ottosson J, et al. Weight loss and heart failure: a nationwide study of gastric bypass surgery versus intensive lifestyle treatment. Circulation. 2017;135(17):1577–85.CrossRefGoogle Scholar
  11. 11.
    Adams TD, Davidson LE, Hunt SC. Weight and metabolic outcomes 12 years after gastric bypass. N Engl J Med. 2018;378(1):93–6.CrossRefGoogle Scholar
  12. 12.
    Benedetti G, Mingrone G, Marcoccia S, et al. Body composition and energy expenditure after weight loss following bariatric surgery. J Am Coll Nutr. 2000;19(2):270–4.CrossRefGoogle Scholar
  13. 13.
    Bobbioni-Harsch E, Morel P, Huber O, et al. Energy economy hampers body weight loss after gastric bypass. J Clin Endocrinol Metab. 2000;85(12):4695–700.CrossRefGoogle Scholar
  14. 14.
    Van Gemert WG, Westerterp KR, Van Acker BAC, et al. Energy, substrate and protein metabolism in morbid obesity before, during and after massive weight loss. Int J Obes. 2000;24(6):711–8.CrossRefGoogle Scholar
  15. 15.
    Das SK, Roberts SB, McCrory MA, et al. Long-term changes in energy expenditure and body composition after massive weight loss induced by gastric bypass surgery. Am J Clin Nutr. 2003;78(1):22–30.CrossRefGoogle Scholar
  16. 16.
    Coupaye M, Bouillot JL, Coussieu C, et al. One-year changes in energy expenditure and serum leptin following adjustable gastric banding in obese women. Obes Surg. 2005;15(6):827–33.CrossRefGoogle Scholar
  17. 17.
    Carey DG, Pliego GJ, Raymond RL. Body composition and metabolic changes following bariatric surgery: effects on fat mass, lean mass and basal metabolic rate: six months to one-year follow-up. Obes Surg. 2006;16(12):1602–8.CrossRefGoogle Scholar
  18. 18.
    Galtier F, Farret A, Verdier R, et al. Resting energy expenditure and fuel metabolism following laparoscopic adjustable gastric banding in severely obese women: relationships with excess weight lost. Int J Obes (Lond). 2006;30(7):1104–10.CrossRefGoogle Scholar
  19. 19.
    Thivel D, Brakonieki K, Duche P, et al. Surgical weight loss: impact on energy expenditure. Obes Surg. 2013;23(2):255–66.CrossRefGoogle Scholar
  20. 20.
    Carrasco F, Papapietro K, Csendes A, et al. Changes in resting energy expenditure and body composition after weight loss following Roux-en-Y gastric bypass. Obes Surg. 2007;17(5):608–16.CrossRefGoogle Scholar
  21. 21.
    De Castro CM, De Lima Montebelo MI, Rasera Jr I, et al. Effects of Roux-en-Y gastric bypass on resting energy expenditure in women. Obes Surg. 2008;18(11):1376–80.CrossRefGoogle Scholar
  22. 22.
    Tamboli RA, Hossain HA, Marks PA, et al. Body composition and energy metabolism following Roux-en-Y gastric bypass surgery. Obesity (Silver Spring). 2010;18(9):1718–24.CrossRefGoogle Scholar
  23. 23.
    Castagneto Gissey L, Iesari S, Le Roux CW, et al. Twenty-four hour energy expenditure and skeletal muscle gene expression changes after bariatric surgery. Obes Facts. 2013;6:36.Google Scholar
  24. 24.
    Iannelli A, Anty R, Schneck AS, et al. Evolution of low-grade systemic inflammation, insulin resistance, anthropometrics, resting energy expenditure and metabolic syndrome after bariatric surgery: a comparative study between gastric bypass and sleeve gastrectomy. J Visc Surg. 2013;150(4):269–75.CrossRefGoogle Scholar
  25. 25.
    Faria SL, Faria OP, Cardeal MDA, et al. Diet-induced thermogenesis and respiratory quotient after Roux-en-Y gastric bypass surgery: a prospective study. Surg Obes Relat Dis. 2014;10(1):138–43.CrossRefGoogle Scholar
  26. 26.
    Iannelli A, Martini F, Rodolphe A, et al. Body composition, anthropometrics, energy expenditure, systemic inflammation, inpremenopausal women 1 year after laparoscopic Roux-en-Y gastric bypass. Surg Endosc Other Interv Tech. 2014;28(2):500–7.CrossRefGoogle Scholar
  27. 27.
    Knuth ND, Johannsen DL, Tamboli RA, et al. Metabolic adaptation following massive weight loss is related to the degree of energy imbalance and changes in circulating leptin. Obesity (Silver Spring). 2014;22(12):2563–9.Google Scholar
  28. 28.
    Rabl C, Rao MN, Schwarz JM, et al. Thermogenic changes after gastric bypass, adjustable gastric banding or diet alone. Surgery. 2014;156(4):806–12.CrossRefGoogle Scholar
  29. 29.
    Butte N, Brandt M, Wong W, et al. Energetic adaptations persist after bariatric surgery in severely obese adolescents. Obesity (Silver Spring). 2015;23:591–601.CrossRefGoogle Scholar
  30. 30.
    Hasani M, Mirahmadian M, Taheri E, et al. The effect of laparoscopic gastric plication surgery on body composition, resting energy expenditure, thyroid hormones, and physical activity in morbidly obese patients. Bariatric Surgical Practice and Patient Care. 2015;10(4):173–9.CrossRefGoogle Scholar
  31. 31.
    Werling M, Fändriks L, Olbers T, et al. Roux-en-Y gastric bypass surgery increases respiratory quotient and energy expenditure during food intake. PLoS One. 2015;10(6):e0129784.CrossRefGoogle Scholar
  32. 32.
    Schneider J, Peterli R, Gass M, et al. Laparoscopic sleeve gastrectomy and Roux-en-Y gastric bypass lead to equal changes in body composition and energy metabolism 17 months postoperatively: a prospective randomized trial. Surg Obes Relat Dis. 2016;12(3):563–70.CrossRefGoogle Scholar
  33. 33.
    Tam CS, Redman LM, Greenway F, et al. Energy metabolic adaptation and cardiometabolic improvements one year after gastric bypass, sleeve gastrectomy, and gastric band. J Clin Endocrinol Metab. 2016;101(10):3755–64.CrossRefGoogle Scholar
  34. 34.
    Tam CS, Rigas G, Heilbronn LK, et al. Energy adaptations persist 2 years after sleeve gastrectomy and gastric bypass. Obes Surg. 2016;26(2):459–63.CrossRefGoogle Scholar
  35. 35.
    Westerterp KR, Donkers JH, Fredrix EW, et al. Energy intake, physical activity and body weight: a simulation model. Br J Nutr. 1995;73(3):337–47.CrossRefGoogle Scholar
  36. 36.
    Moehlecke M, Blume CA, Rheinheimer J, et al. Early reduction of resting energy expenditure and successful weight loss after Roux-en-Y gastric bypass. Surg Obes Relat Dis. 2017;13(2):204–9.CrossRefGoogle Scholar
  37. 37.
    Bettini S, Bordigato E, Fabris R, et al. Modifications of resting energy expenditure after sleeve gastrectomy. Obes Surg. 2018:1–6.Google Scholar
  38. 38.
    Ravelli MN, Schoeller DA, Crisp AH, et al. Accuracy of total energy expenditure predictive equations after a massive weight loss induced by bariatric surgery. Clin Nutr ESPEN. 2018;26:57–65.CrossRefGoogle Scholar
  39. 39.
    Wilms B, Ernst B, Thurnheer M, et al. Resting energy expenditure after Roux-en Y gastric bypass surgery. Surg Obes Relat Dis. 2018;14(2):191–9.CrossRefGoogle Scholar
  40. 40.
    Wolfe BM, Schoeller DA, McCrady-Spitzer SK, et al. Resting metabolic rate, total daily energy expenditure, and metabolic adaptation 6 months and 24 months after bariatric surgery. Obesity (Silver Spring). 2018;26(5):862–8.CrossRefGoogle Scholar
  41. 41.
    Iesari S, Le Roux CW, De Gaetano A, et al. Twenty-four hour energy expenditure and skeletal muscle gene expression changes after bariatric surgery. J Clin Endocrinol Metab. 2013;98(2):E321–7.CrossRefGoogle Scholar
  42. 42.
    Browning MG, Franco RL, Cyrus JC, et al. Changes in resting energy expenditure in relation to body weight and composition following gastric restriction: a systematic review. Obes Surg. 2016;26(7):1607–15.CrossRefGoogle Scholar
  43. 43.
    Davidson LE, Yu W, Goodpaster BH, et al. Fat-free mass and skeletal muscle mass five years after bariatric surgery. Obesity. 2018;26(7):1130–6.CrossRefGoogle Scholar
  44. 44.
    Johannsen DL, Knuth ND, Huizenga R, et al. Metabolic slowing with massive weight loss despite preservation of fat-free mass. J Clin Endocrinol Metab. 2012;97(7):2489–96.CrossRefGoogle Scholar
  45. 45.
    Flancbaum L, Verducci J, Choban P. Changes in measured resting energy expenditure after Roux-en-Y gastric bypass for clinically severe obesity are not related to bypass limb-length. Obes Surg. 1998;8:437–43.CrossRefGoogle Scholar
  46. 46.
    Goldsmith R, Joanisse DR, Gallagher D, et al. Effects of experimental weight perturbation on skeletal muscle work efficiency, fuel utilization, and biochemistry in human subjects. Am J Physiol Regul Integr Comp Physiol. 2010;298(1):R79–88.CrossRefGoogle Scholar
  47. 47.
    Rosenbaum M, Nicolson M, Hirsch J, et al. Effects of weight change on plasma leptin concentrations and energy expenditure. J Clin Endocrinol Metab. 1997;82(11):3647–54.Google Scholar
  48. 48.
    Esterbauer H, Oberkofler H, Dallinger G, et al. Uncoupling protein-3 gene expression: reduced skeletal muscle mRNA in obese humans during pronounced weight loss. Diabetologia. 1999;42(3):302–9.CrossRefGoogle Scholar
  49. 49.
    Guijarro A, Osei-Hyiaman D, Harvey-White J, et al. Sustained weight loss after Roux-en-Y gastric bypass is characterized by down regulation of endocannabinoids and mitochondrial function. Ann Surg. 2008;247(5):779–90.CrossRefGoogle Scholar
  50. 50.
    Rosenbaum M, Goldsmith R, Bloomfield D, et al. Low-dose leptin reverses skeletal muscle, autonomic, and neuroendocrine adaptations to maintenance of reduced weight. J Clin Invest. 2005;115(12):3579–86.CrossRefGoogle Scholar
  51. 51.
    Muller MJ, Enderle J, Pourhassan M, et al. Metabolic adaptation to caloric restriction and subsequent refeeding: the Minnesota Starvation Experiment revisited. Am J Clin Nutr. 2015;102(4):807–19.CrossRefGoogle Scholar
  52. 52.
    le Roux CW, Borg C, Wallis K, et al. Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann Surg. 2010;252(1):50–6.CrossRefGoogle Scholar
  53. 53.
    Spak E, Bjorklund P, Helander HF, et al. Changes in the mucosa of the Roux-limb after gastric bypass surgery. Histopathology. 2010;57(5):680–8.CrossRefGoogle Scholar
  54. 54.
    Saeidi N, Meoli L, Nestoridi E, et al. Reprogramming of intestinal glucose metabolism and glycemic control in rats after gastric bypass. Science (New York). 2013;341(6144):406–10.CrossRefGoogle Scholar
  55. 55.
    Bueter M, Lowenstein C, Olbers T, et al. Gastric bypass increases energy expenditure in rats. Gastroenterology. 2010;138(5):1845–53.CrossRefGoogle Scholar
  56. 56.
    Kuipers F, Bloks VW, Groen AK. Beyond intestinal soap--bile acids in metabolic control. Nat Rev Endocrinol. 2014;10(8):488–98.CrossRefGoogle Scholar
  57. 57.
    Schmidt JB, Gregersen NT, Pedersen SD, et al. Effects of PYY3-36 and GLP-1 on energy intake, energy expenditure, and appetite in overweight men. Am J Phys Endocrinol Metab. 2014;306(11):E1248–56.CrossRefGoogle Scholar
  58. 58.
    Sloth B, Holst JJ, Flint A, et al. Effects of PYY1-36 and PYY3-36 on appetite, energy intake, energy expenditure, glucose and fat metabolism in obese and lean subjects. Am J Phys Endocrinol Metab. 2007;292(4):E1062–8.CrossRefGoogle Scholar
  59. 59.
    van den Beukel JC, Grefhorst A. Interactions between the gut, the brain and brown adipose tissue function. Front Horm Res. 2014;42:107–22.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of General Surgery, Shanghai Ninth People’s HospitalShanghai JiaoTong University School of MedicineShanghaiPeople’s Republic of China
  2. 2.Clinical Research Center, Shanghai Ninth People’s HospitalShanghai JiaoTong University School of MedicineShanghaiPeople’s Republic of China

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