Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Animal Models

Alterations in energy expenditure in Roux-en-Y gastric bypass rats persist at thermoneutrality

International Journal of Obesity volume 40, pages 1215–1221 (2016)Cite this article

Subjects

Abstract

Background:

The compensatory decrease in energy expenditure (EE) in response to body weight loss is attenuated by Roux-en-Y gastric bypass (RYGB) surgery in rats. The thermoneutral zone (TNZ) is at higher temperatures in rodents than in humans. Consequently, rodents may be under moderate cold stress if EE is measured at room temperature, leading to increased EE due to adaptive thermogenesis. We speculated that the reported alterations in EE of RYGB rats at room temperature are caused by higher adaptive thermogenesis and are therefore not present at thermoneutrality.

Methods:

Male Wistar rats were randomized for RYGB or sham surgery. Some sham rats were body weight matched (BWM) to the RYGB rats by food restriction, the others received ad libitum access to food (AL). EE, body temperature, physical activity and food intake were measured at ambient temperatures between 22 and 32 °C to determine the TNZ. Adaptive thermogenesis requires β3-adrenergic receptor-mediated uncoupling protein-1 (UCP-1) expression in brown adipose tissue (BAT). The in vivo thermogenic capacity of BAT was determined by administering the β3-adrenergic agonist CL316,243, and UCP-1 protein expression was measured at room temperature.

Results:

The TNZ was between 28 and 30 °C for AL and RYGB and between 30 and 32 °C for BWM rats, respectively. In contrast to AL and BWM rats, EE was not significantly higher at room temperature than at thermoneutrality in RYGB rats, reflecting a lack of adaptive thermogenesis. Consistently, both the thermogenic capacity of BAT and UCP-1 expression were decreased in RYGB compared with AL rats at room temperature.

Conclusions:

Our data confirm that the decrease in EE after body weight loss is attenuated by RYGB surgery and show that this effect persists at thermoneutrality. Contrary to our hypothesis, we found that adaptive thermogenesis at room temperature is reduced in RYGB rats.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. Zheng H, Shin AC, Lenard NR, Townsend RL, Patterson LM, Sigalet DL et al. Meal patterns, satiety, and food choice in a rat model of Roux-en-Y gastric bypass surgery. Am J Physiol Regul Integr Comp Physiol 2009; 297: R1273–R1282.

    Article  CAS  Google Scholar 

  2. Bueter M, Lowenstein C, Olbers T, Wang M, Cluny NL, Bloom SR et al. Gastric bypass increases energy expenditure in rats. Gastroenterology 2010; 138: 1845–1853.

    Article  Google Scholar 

  3. Stylopoulos N, Hoppin AG, Kaplan LM . Roux-en-Y gastric bypass enhances energy expenditure and extends lifespan in diet-induced obese rats. Obesity (Silver Spring) 2009; 17: 1839–1847.

    Article  Google Scholar 

  4. Mokadem M, Zechner JF, Margolskee RF, Drucker DJ, Aguirre V . Effects of Roux-en-Y gastric bypass on energy and glucose homeostasis are preserved in two mouse models of functional glucagon-like peptide-1 deficiency. Mol Metab 2014; 3: 191–201.

    Article  CAS  Google Scholar 

  5. Wadden TA, Foster GD, Letizia KA, Mullen JL . Long-term effects of dieting on resting metabolic rate in obese outpatients. JAMA 1990; 264: 707–711.

    Article  CAS  Google Scholar 

  6. Faria SL, Faria OP, Cardeal Mde A, de Gouvea HR, Buffington C . Diet-induced thermogenesis and respiratory quotient after Roux-en-Y gastric bypass. Surg Obes Relat Dis 2012; 8: 797–802.

    Article  Google Scholar 

  7. Faria SL, Faria OP, Cardeal Mde A, Ito MK, Buffington C . Diet-induced thermogenesis and respiratory quotient after Roux-en-Y gastric bypass surgery: a prospective study. Surg Obes Relat Dis 2014; 10: 138–143.

    Article  Google Scholar 

  8. Faria SL, Kelly E, Faria OP . Energy expenditure and weight regain in patients submitted to Roux-en-Y gastric bypass. Obes Surg 2009; 19: 856–859.

    Article  Google Scholar 

  9. Iannelli A, Martini F, Rodolphe A, Schneck AS, Gual P, Tran et al. Body composition, anthropometrics, energy expenditure, systemic inflammation, in premenopausal women 1 year after laparoscopic Roux-en-Y gastric bypass. Surg Endosc 2014; 28: 500–507.

    Article  Google Scholar 

  10. Carey DG, Pliego GJ, Raymond RL, Skau KB . Body composition and metabolic changes following bariatric surgery: effects on fat mass, lean mass and basal metabolic rate. Obes Surg 2006; 16: 469–477.

    Article  Google Scholar 

  11. Gordon CJ . Temperature Regulation in Laboratory Rodents. Cambridge University Press: New York, NY, USA, 1993.

    Book  Google Scholar 

  12. Dacks PA, Rance NE . Effects of estradiol on the thermoneutral zone and core temperature in ovariectomized rats. Endocrinology 2010; 151: 1187–1193.

    Article  CAS  Google Scholar 

  13. Swift RW . The effect of feed on the critical temperature for the albino rat. J Nutr 1944; 30: 359–364.

    Article  Google Scholar 

  14. Ashrafian H, le Roux CW . Metabolic surgery and gut hormones - a review of bariatric entero-humoral modulation. Physiol Behav 2009; 97: 620–631.

    Article  CAS  Google Scholar 

  15. le Roux CW, Bueter M . The physiology of altered eating behaviour after Roux-en-Y gastric bypass. Exp Physiol 2014; 99: 1128–1132.

    Article  Google Scholar 

  16. Cannon B, Nedergaard J . Brown adipose tissue: function and physiological significance. Physiol Rev 2004; 84: 277–359.

    CAS  Google Scholar 

  17. Bueter M, Abegg K, Seyfried F, Lutz TA, le Roux CW . Roux-en-Y gastric bypass operation in rats. J Vis Exp 2012; 64: e3940.

    Google Scholar 

  18. Lockie SH, Heppner KM, Chaudhary N, Chabenne JR, Morgan DA, Veyrat-Durebex C et al. Direct control of brown adipose tissue thermogenesis by central nervous system glucagon-like peptide-1 receptor signaling. Diabetes 2012; 61: 2753–2762.

    Article  CAS  Google Scholar 

  19. Weir JB . New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 1949; 109: 1–9.

    Article  Google Scholar 

  20. Tanaka H, Kanosue K, Nakayama T, Shen Z . Grooming, body extension, and vasomotor responses induced by hypothalamic warming at different ambient temperatures in rats. Physiol Behav 1986; 38: 145–151.

    Article  CAS  Google Scholar 

  21. Chen YI, Cypess AM, Sass CA, Brownell AL, Jokivarsi KT, Kahn CR et al. Anatomical and functional assessment of brown adipose tissue by magnetic resonance imaging. Obesity (Silver Spring) 2012; 20: 1519–1526.

    Article  CAS  Google Scholar 

  22. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD et al. Measurement of protein using bicinchoninic acid. Anal Biochem 1985; 150: 76–85.

    Article  CAS  Google Scholar 

  23. Gassmann M, Grenacher B, Rohde B, Vogel J . Quantifying Western blots: pitfalls of densitometry. Electrophoresis 2009; 30: 1845–1855.

    Article  CAS  Google Scholar 

  24. Gordon CJ . Relationship between preferred ambient temperature and autonomic thermoregulatory function in rat. Am J Physiol 1987; 252: R1130–R1137.

    CAS  PubMed  Google Scholar 

  25. Poole S, Stephenson JD . Body temperature regulation and thermoneutrality in rats. Q J Exp Physiol Cogn Med Sci 1977; 62: 143–149.

    CAS  PubMed  Google Scholar 

  26. Rossi M, Nannipieri M, Anselmino M, Pesce M, Muscelli E, Santoro G et al. Skin vasodilator function and vasomotion in patients with morbid obesity: effects of gastric bypass surgery. Obes Surg 2011; 21: 87–94.

    Article  Google Scholar 

  27. Le Roux CW, Aylwin SJ, Batterham RL, Borg CM, Coyle F, Prasad V et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg 2006; 243: 108–114.

    Article  Google Scholar 

  28. Shin AC, Zheng H, Townsend RL, Sigalet DL, Berthoud HR . Meal-induced hormone responses in a rat model of Roux-en-Y gastric bypass surgery. Endocrinology 2010; 151: 1588–1597.

    Article  CAS  Google Scholar 

  29. Werling M, Vincent RP, Cross GF, Marschall HU, Fandriks L, Lonroth H et al. Enhanced fasting and post-prandial plasma bile acid responses after Roux-en-Y gastric bypass surgery. Scand J Gastroenterol 2013; 48: 1257–1264.

    Article  Google Scholar 

  30. Ahmad NN, Pfalzer A, Kaplan LM . Roux-en-Y gastric bypass normalizes the blunted postprandial bile acid excursion associated with obesity. Int J Obes (Lond) 2013; 37: 1553–1559.

    Article  CAS  Google Scholar 

  31. Pournaras DJ, Glicksman C, Vincent RP, Kuganolipava S, Alaghband-Zadeh J, Mahon D et al. The role of bile after Roux-en-Y gastric bypass in promoting weight loss and improving glycaemic control. Endocrinology 2012; 153: 3613–3619.

    Article  CAS  Google Scholar 

  32. Cummings BP, Bettaieb A, Graham JL, Stanhope KL, Kowala M, Haj FG et al. Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology 2012; 153: 3620–3632.

    Article  CAS  Google Scholar 

  33. Saeidi N, Nestoridi E, Kucharczyk J, Uygun MK, Yarmush ML, Stylopoulos N . Sleeve gastrectomy and Roux-en-Y gastric bypass exhibit differential effects on food preferences, nutrient absorption and energy expenditure in obese rats. Int J Obes (Lond) 2012; 36: 1396–1402.

    Article  CAS  Google Scholar 

  34. Stefater MA, Perez-Tilve D, Chambers AP, Wilson-Perez HE, Sandoval DA, Berger J et al. Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology 2010; 138: 2426–2436.

    Article  CAS  Google Scholar 

  35. Le Roux CW, Borg C, Wallis K, Vincent RP, Bueter M, Goodlad R et al. Gut hypertrophy after gastric bypass is associated with increased glucagon-like peptide 2 and intestinal crypt cell proliferation. Ann Surg 2010; 252: 50–56.

    Article  Google Scholar 

  36. Saeidi N, Meoli L, Nestoridi E, Gupta NK, Kvas S, Kucharczyk J et al. Reprogramming of intestinal glucose metabolism and glycemic control in rats after gastric bypass. Science 2013; 341: 406–410.

    Article  CAS  Google Scholar 

  37. Wilms B, Ernst B, Schmid SM, Thurnheer M, Schultes B . Enhanced thermic effect of food after Roux-en-Y Gastric bypass surgery. J Clin Endocrinol Metab 2013; 98: 3776–3784.

    Article  CAS  Google Scholar 

  38. Werling M, Olbers T, Fandriks L, Bueter M, Lonroth H, Stenlof K et al. Increased postprandial energy expenditure may explain superior long term weight loss after Roux-en-Y gastric bypass compared to vertical banded gastroplasty. PLoS One 2013; 8: e60280.

    Article  CAS  Google Scholar 

  39. Graessler J, Qin Y, Zhong H, Zhang J, Licinio J, Wong ML et al. Metagenomic sequencing of the human gut microbiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics J 2012; 13: 514–522.

    Article  Google Scholar 

  40. Kong LC, Tap J, Aron-Wisnewsky J, Pelloux V, Basdevant A, Bouillot JL et al. Gut microbiota after gastric bypass in human obesity: increased richness and associations of bacterial genera with adipose tissue genes. Am J Clin Nutr 2013; 98: 16–24.

    Article  CAS  Google Scholar 

  41. Li JV, Ashrafian H, Bueter M, Kinross J, Sands C, le Roux CW et al. Metabolic surgery profoundly influences gut microbial-host metabolic cross-talk. Gut 2011; 60: 1214–1223.

    Article  CAS  Google Scholar 

  42. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y et al. Human gut microbiota in obesity and after gastric bypass. Proc Natl Acad Sci USA 2009; 106: 2365–2370.

    Article  CAS  Google Scholar 

  43. Osto M, Abegg K, Bueter M, le Roux CW, Cani PD, Lutz TA . Roux-en-Y gastric bypass surgery in rats alters gut microbiota profile along the intestine. Physiol Behav 2013; 119: 92–96.

    Article  CAS  Google Scholar 

  44. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes 2009; 58: 1509–1517.

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. M Bueter and T A Lutz: These authors contributed equally to this work.

Authors and Affiliations

  1. Institute of Veterinary Physiology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland

    K Abegg & T A Lutz

  2. Department of Surgery I, University of Wurzburg, Wurzburg, Germany

    C Corteville

  3. Division of Visceral and Transplantation Surgery, Department of Surgery, University Hospital Zurich, Zurich, Switzerland

    M Bueter

  4. Center of Integrative Human Physiology, University of Zurich, Zurich, Switzerland

    M Bueter & T A Lutz

Authors
  1. K Abegg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C Corteville
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M Bueter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T A Lutz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T A Lutz.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abegg, K., Corteville, C., Bueter, M. et al. Alterations in energy expenditure in Roux-en-Y gastric bypass rats persist at thermoneutrality. Int J Obes 40, 1215–1221 (2016). https://doi.org/10.1038/ijo.2016.55

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2016.55

This article is cited by

Search

Advanced search

Quick links