Changes of Resting Energy Expenditure in Type 2 Diabetes Rats After Roux-en-Y Gastric Bypass

Abstract

Background

This study aimed to investigate the changes of resting energy expenditure (REE) induced by Roux-en-Y gastric bypass (RYGB) in diabetic rats.

Methods

Thirty male Goto-Kakizaki rats were randomly divided into RYGB, sham RYGB (SR), and control groups. Glucose metabolism, energy expenditure, triiodothyronine, and bile acid levels were measured. Body composition in different groups was compared after sacrifice.

Results

RYGB induced significant diabetic improvement, with decreased maximum food intake and body weight. There was no significant difference in the REE between the groups before surgery (P = 0.74), while the REE of the RYGB group (1.15 ± 0.17 ml/h/g) was higher than that of the SR group (0.99 ± 0.13 ml/h/g) and the control group (0.97 ± 0.13 ml/h/g, P = 0.031) at the 20th postoperative week. The ratio of white adipose tissue in the RYGB group was lower (P = 0.02), and the ratio of brown adipose tissue was higher than that of the SR group and the control group (P = 0.045). Moreover, a higher bile acid level was detected in the RYGB group (6.4 ± 1.8 μmol/L) than in the SR group (4.2 ± 1.7 μmol/L) and the control group (4.0 ± 2.0 μmol/L, P = 0.025).

Conclusions

RYGB induces a higher REE level in diabetic rats. The circulating bile acid level was enhanced after surgery.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Wild S, Roglic G, Green A, et al. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27(5):1047–53. Epub 2004/04/28

    PubMed  Article  Google Scholar 

  2. 2.

    Camilleri M, Staiano A. Insights on obesity in children and adults: individualizing management. Trends Endocrinol Metab. 2019;30(10):724–34. Epub 2019/08/10

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  3. 3.

    Still CD, Wood GC, Benotti P, et al. Preoperative prediction of type 2 diabetes remission after Roux-en-Y gastric bypass surgery: a retrospective cohort study. Lancet Diabetes Endocrinol. 2014;2(1):38–45. Epub 2014/03/01

    PubMed  PubMed Central  Article  Google Scholar 

  4. 4.

    Mazidi M, de Caravatto PP, Speakman JR, et al. Mechanisms of action of surgical interventions on weight-related diseases: the potential role of bile acids. Obes Surg. 2017;27(3):826–36. Epub 2017/01/17

    PubMed  Article  Google Scholar 

  5. 5.

    Nilaweera KN, Speakman JR. Regulation of intestinal growth in response to variations in energy supply and demand. Obesity Reviews: an Official Journal of the International Association for the Study of Obesity. 2018;19(Suppl 1):61–72. Epub 2018/12/05

    CAS  Article  Google Scholar 

  6. 6.

    Neinast MD, Frank AP, Zechner JF, et al. Activation of natriuretic peptides and the sympathetic nervous system following Roux-en-Y gastric bypass is associated with gonadal adipose tissues browning. Mol Metab. 2015;4(5):427–36.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. 7.

    Clemmensen C, Finan B, Muller TD, et al. Emerging hormonal-based combination pharmacotherapies for the treatment of metabolic diseases. Nat Rev Endocrinol. 2019;15(2):90–104. Epub 2018/11/18

    PubMed  Article  Google Scholar 

  8. 8.

    Heshka S, Lemos T, Astbury NM, et al. Resting energy expenditure and organ-tissue body composition 5 years after bariatric surgery. Obes Surg. 2019;15 Epub 2019/10/17

  9. 9.

    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. Epub 2012/04/27

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    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. Epub 2003/06/21

    CAS  PubMed  Article  Google Scholar 

  11. 11.

    Wilms B, Ernst B, Thurnheer M, et al. Resting energy expenditure after Roux-en Y gastric bypass surgery. Surgery for Obesity and Related Diseases: Official Journal of the American Society for Bariatric Surgery. 2018;14(2):191–9. Epub 2017/12/25

    Article  Google Scholar 

  12. 12.

    Nahon KJ, Doornink F, Straat ME, et al. Effect of sitagliptin on energy metabolism and brown adipose tissue in overweight individuals with prediabetes: a randomised placebo-controlled trial. Diabetologia. 2018;61(11):2386–97. Epub 2018/08/27

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Liu T, Li H, Ding G, et al. Comparative genome of GK and Wistar rats reveals genetic basis of type 2 diabetes. PLoS One. 2015;10(11):e0141859. Epub 2015/11/04

    PubMed  PubMed Central  Article  Google Scholar 

  14. 14.

    Shah H, Shin AC. Meal patterns after bariatric surgery in mice and rats. Appetite. 2019;146:104340. Epub 2019/07/03

    PubMed  Article  Google Scholar 

  15. 15.

    Burgos-Ramos E, Canelles S, Frago LM, et al. Improvement in glycemia after glucose or insulin overload in leptin-infused rats is associated with insulin-related activation of hepatic glucose metabolism. Nutr Metab (Lond). 2016;13:19. Epub 2016/03/05. eng

    Article  Google Scholar 

  16. 16.

    Obembe AO, Owu DU, Okwari OO, et al. Intestinal fluid and glucose transport in Wistar rats following chronic consumption of fresh or oxidised palm oil diet. ISRN Gastroenterol. 2011;2011:972838. Epub 2011/10/13

    PubMed  Google Scholar 

  17. 17.

    Owu DU, Antai AB, Udofia KH, et al. Vitamin C improves basal metabolic rate and lipid profile in alloxan-induced diabetes mellitus in rats. J Biosci. 2006;31(5):575–9. Epub 2007/02/16

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Ramracheya RD, McCulloch LJ, Clark A, et al. PYY-dependent restoration of impaired insulin and glucagon secretion in type 2 diabetes following Roux-en-Y gastric bypass surgery. Cell Rep. 2016;15(5):944–50. Epub 2016/04/28

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  19. 19.

    Camacho-Ramirez A, Prada-Oliveira JA, Ribelles-Garcia A, et al. The leading role of peptide tyrosine tyrosine in glycemic control after Roux-en-Y gastric bypass in rats. Obes Surg. 2020;30(2):697–706. Epub 2019/11/09

    PubMed  Article  Google Scholar 

  20. 20.

    Karahashi M, Hirata-Hanta Y, Kawabata K, et al. Abnormalities in the metabolism of fatty acids and triacylglycerols in the liver of the Goto-Kakizaki rat: a model for non-obese type 2 diabetes. Lipids. 2016;51(8):955–71. Epub 2016/07/04

    CAS  PubMed  Article  Google Scholar 

  21. 21.

    Skogar M, Holmback U, Hedberg J, et al. Preserved fat-free mass after gastric bypass and duodenal switch. Obes Surg. 2017;27(7):1735–40. Epub 2016/11/26

    PubMed  Article  Google Scholar 

  22. 22.

    Mirahmadian M, Hasani M, Taheri E, et al. Influence of gastric bypass surgery on resting energy expenditure, body composition, physical activity, and thyroid hormones in morbidly obese patients. Diabetes Metab Syndr Obes. 2018;11:667–72. Epub 2018/11/15

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    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. Epub 2016/08/05

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Bettini S, Bordigato E, Fabris R, et al. Modifications of resting energy expenditure after sleeve gastrectomy. Obes Surg. 2018;28(8):2481–6. Epub 2018/03/14

    PubMed  Article  Google Scholar 

  25. 25.

    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. Epub 2007/07/31

    PubMed  Article  Google Scholar 

  26. 26.

    Widen EM, Strain G, King WC, et al. Validity of bioelectrical impedance analysis for measuring changes in body water and percent fat after bariatric surgery. Obes Surg. 2014;24(6):847–54. Epub 2014/01/28

    PubMed  PubMed Central  Article  Google Scholar 

  27. 27.

    Nedergaard J, Cannon B. The changed metabolic world with human brown adipose tissue: therapeutic visions. Cell Metab. 2010;11(4):268–72. Epub 2010/04/09

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Orava J, Nuutila P, Lidell ME, et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 2011;14(2):272–9. Epub 2011/08/02

    CAS  PubMed  Article  Google Scholar 

  29. 29.

    Shan CX, Qiu NC, Liu ME, et al. Effects of diet on bile acid metabolism and insulin resistance in type 2 diabetic rats after Roux-en-Y gastric bypass. Obes Surg. 2018;28(10):3044–53. Epub 2018/05/04

    PubMed  Article  Google Scholar 

  30. 30.

    Sinal CJ, Tohkin M, Miyata M, et al. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell. 2000;102(6):731–44.

    CAS  PubMed  Article  Google Scholar 

  31. 31.

    Thomas C, Gioiello A, Noriega L, et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009;10(3):167–77.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Broeders EP, Nascimento EB, Havekes B, et al. The bile acid chenodeoxycholic acid increases human brown adipose tissue activity. Cell Metab. 2015;22(3):418–26. Epub 2015/08/04

    CAS  PubMed  Article  Google Scholar 

  33. 33.

    Watanabe M, Houten SM, Mataki C, et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature. 2006;439(7075):484–9.

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Staley C, Weingarden AR, Khoruts A, et al. Interaction of gut microbiota with bile acid metabolism and its influence on disease states. Appl Microbiol Biotechnol. 2017;101(1):47–64.

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489(7415):242–9.

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Westerterp KR. Control of energy expenditure in humans. Eur J Clin Nutr. 2017;71(3):340–4. Epub 2016/12/03

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

We thank the American Journal Experts for polishing the language.

Funding

This study was funded by the National Natural Science Foundation of China (grant number 81400797 and 81970763) and CAMS Innovation Fund for Medical Sciences (CIFMS) (2017-I2M-4-003).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Xiaodong He.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Chen, W., Yin, H., Zhang, N. et al. Changes of Resting Energy Expenditure in Type 2 Diabetes Rats After Roux-en-Y Gastric Bypass. OBES SURG 30, 2994–3000 (2020). https://doi.org/10.1007/s11695-020-04638-6

Download citation

Keywords

  • Type 2 diabetes mellitus
  • Bariatric surgery
  • Roux-en-Y gastric bypass
  • Bile acid