Skip to main content
SpringerLink
Log in

Additional effects of duodenojejunal bypass on glucose metabolism in a rat model of sleeve gastrectomy

  • Original Article
  • Published:
Surgery Today Aims and scope Submit manuscript

Abstract

Purpose

Sleeve gastrectomy with duodenojejunal bypass (SG-DJB) is expected to become a popular procedure in East Asia. The aim of this study was to evaluate the effects of duodenojejunal bypass on glucose metabolism in a rat model of sleeve gastrectomy (SG).

Methods

Twenty-four Sprague–Dawley rats were divided into two groups: SG-DJB and SG alone. 6 weeks after surgery, body weight, feed intake, and metabolic parameters were measured, and oral glucose tolerance tests (OGTT) were performed. The mRNA expression of factors related to gluconeogenesis and glucose transport was evaluated using jejunal samples. Protein expression of factors with significantly different mRNA expression levels was evaluated using immunohistochemistry.

Results

Body weight and metabolic parameters did not significantly differ between the two groups. During the OGTT, the SG-DJB group showed an early increase in serum insulin followed by an early decrease in blood glucose compared with the SG group. Expression levels of glucose transporter 1 (GLUT1) and sodium-glucose cotransporter 1 (SGLT1) mRNA and protein in the alimentary limb (AL) were greater in the SG-DJB group than in the SG group.

Conclusions

The additional effects of duodenojejunal bypass on glucose metabolism after SG may be related to increased expression of GLUT1 and SGLT1 in the AL.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Welbourn R, Pournaras DJ, Dixon J, Higa K, Kinsman R, Ottosson J, et al. Bariatric surgery worldwide: Baseline demographic description and one-year outcomes from the second IFSO global registry report 2013–2015. Obes Surg. 2018;28:313–22.

    Article  PubMed  Google Scholar 

  2. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87:4–14.

    Article  CAS  PubMed  Google Scholar 

  3. Schauer PR, Bhatt DL, Kirwan JP, Wolski K, Aminian A, Brethauer SA, et al. Bariatric surgery versus intensive medical therapy for diabetes—5-year outcomes. N Engl J Med. 2017;376:641–51.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Chang SH, Stoll CR, Song J, Varela JE, Eagon CJ, Colditz GA. The effectiveness and risks of bariatric surgery: an updated systematic review and meta-analysis, 2003–2012. JAMA Surg. 2014;149:275–87.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kasama K, Tagaya N, Kanehira E, Oshiro T, Seki Y, Kinouchi M, et al. Laparoscopic sleeve gastrectomy with duodenojejunal bypass: technique and preliminary results. Obes Surg. 2009;19:1341–5.

    Article  PubMed  Google Scholar 

  6. Seki Y, Kasama K, Haruta H, Watanabe A, Yokoyama R, Porciuncula JP, et al. Five-year-results of laparoscopic sleeve gastrectomy with duodenojejunal bypass for weight loss and type 2 diabetes mellitus. Obes Surg. 2017;27:795–801.

    Article  PubMed  Google Scholar 

  7. Seki Y, Kasama K, Yasuda K, Eri K, Watanabe N, Kurokawa Y. Metabolic surgery for inadequately controlled type 2 diabetes in nonseverely obese Japanese: a prospective, single-center study. Surg Obes Relat Dis. 2018;14:978–85.

    Article  PubMed  Google Scholar 

  8. Uno K, Seki Y, Kasama K, Wakamatsu K, Hashimoto K, Umezawa A, et al. Mid-term results of bariatric surgery in morbidly obese Japanese patients with slow progressive autoimmune diabetes. Asian J Endosc Surg. 2018;11:238–43.

    Article  PubMed  Google Scholar 

  9. Naitoh T, Kasama K, Seki Y, Ohta M, Oshiro T, Sasaki A, et al. Efficacy of sleeve gastrectomy with duodenal-jejunal bypass for the treatment of obese severe diabetes patients in Japan: a retrospective multicenter study. Obes Surg. 2018;28:497–505.

    Article  PubMed  Google Scholar 

  10. Lee WJ, Almulaifi A, Tsou JJ, Ser KH, Lee YC, Chen SC. Laparoscopic sleeve gastrectomy for type 2 diabetes mellitus: predicting the success by ABCD score. Surg Obes Relat Dis. 2015;11:991–6.

    Article  PubMed  Google Scholar 

  11. Lopez PP, Nicholson SE, Burkhardt GE, Johnson RA, Johnson FK. Development of a sleeve gastrectomy weight loss model in obese Zucker rats. J Surg Res. 2009;157:243–50.

    Article  PubMed  Google Scholar 

  12. Masuda T, Ohta M, Hirashita T, Kawano Y, Eguchi H, Yada K, et al. A comparative study of gastric banding and sleeve gastrectomy in an obese diabetic rat model. Obes Surg. 2011;21:1774–80.

    Article  PubMed  Google Scholar 

  13. Sun D, Liu S, Zhang G, Chen W, Yan Z, Hu S. Type 2 diabetes control in a nonobese rat model using sleeve gastrectomy with duodenal-jejunal bypass (SGDJB). Obes Surg. 2012;22:1865–73.

    Article  PubMed  Google Scholar 

  14. Donglei Z, Liesheng L, Xun J, Chenzhu Z, Weixing D. Effects and mechanism of duodenal-jejunal bypass and sleeve gastrectomy on GLUT2 and glucokinase in diabetic Goto-Kakizaki rats. Eur J Med Res. 2012;17:15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kim M, Son YG, Kang YN, Ha TK, Ha E. Changes in glucose transporters, gluconeogenesis, and circadian clock after duodenal-jejunal bypass surgery. Obes Surg. 2015;25:635–41.

    Article  PubMed  Google Scholar 

  16. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.

    Article  CAS  PubMed  Google Scholar 

  17. Tominaga M, Ohta M, Kai S, Iwaki K, Shibata K, Kitano S. Increased heat-shock protein 90 expression contributes to impaired adaptive cytoprotection in the gastric mucosa of portal hypertensive rats. J Gastroenterol Hepatol. 2009;24:1136–41.

    Article  CAS  PubMed  Google Scholar 

  18. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, et al. Primer3–new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Goncalves D, Barataud A, De Vadder F, Vinera J, Zitoun C, Duchampt A, et al. Bile routing modification reproduces key features of gastric bypass in rat. Ann Surg. 2015;262:1006–15.

    Article  PubMed  Google Scholar 

  20. Yan Y, Zhou Z, Kong F, Feng S, Li X, Sha Y, et al. Roux-en-Y gastric bypass surgery suppresses hepatic gluconeogenesis and increases intestinal gluconeogenesis in a T2DM rat model. Obes Surg. 2016;26:2683–90.

    Article  PubMed  Google Scholar 

  21. Pories WJ, Swanson MS, MacDonald KG, Long SB, Morris PG, Brown BM, et al. Who would have thought it? An operation proves to be the most effective therapy for adult-onset diabetes mellitus. Ann Surg. 1995;222:339–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Seeley RJ, Chambers AP, Sandoval DA. The role of gut adaptation in the potent effects of multiple bariatric surgeries on obesity and diabetes. Cell Metab. 2015;21:369–78.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Batterham RL, Cummings DE. Mechanisms of diabetes improvement following bariatric/metabolic surgery. Diabetes Care. 2016;39:893–901.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Langer FB, Reza Hoda MA, Bohdjalian A, Felberbauer FX, Zacherl J, Wenzl E, et al. Sleeve gastrectomy and gastric banding: effects on plasma ghrelin levels. Obes Surg. 2005;15:1024–9.

    Article  CAS  PubMed  Google Scholar 

  25. Peterli R, Wolnerhanssen B, Peters T, Devaux N, Kern B, Christoffel-Courtin C, et al. Improvement in glucose metabolism after bariatric surgery: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy: a prospective randomized trial. Ann Surg. 2009;250:234–41.

    Article  PubMed  Google Scholar 

  26. Ryan KK, Tremaroli V, Clemmensen C, Kovatcheva-Datchary P, Myronovych A, Karns R, et al. FXR is a molecular target for the effects of vertical sleeve gastrectomy. Nature. 2014;509:183–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Troy S, Soty M, Ribeiro L, Laval L, Migrenne S, Fioramonti X, et al. Intestinal gluconeogenesis is a key factor for early metabolic changes after gastric bypass but not after gastric lap-band in mice. Cell Metab. 2008;8:201–11.

    Article  CAS  PubMed  Google Scholar 

  28. Kahn BB. Facilitative glucose transporters: regulatory mechanisms and dysregulation in diabetes. J Clin Invest. 1992;89:1367–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yoshikawa T, Inoue R, Matsumoto M, Yajima T, Ushida K, Iwanaga T. Comparative expression of hexose transporters (SGLT1, GLUT1, GLUT2 and GLUT5) throughout the mouse gastrointestinal tract. Histochem Cell Biol. 2011;135:183–94.

    Article  CAS  PubMed  Google Scholar 

  30. Mueckler M. Facilitative glucose transporters. Eur J Biochem. 1994;219:713–25.

    Article  CAS  PubMed  Google Scholar 

  31. Ouiddir A, Planes C, Fernandes I, VanHesse A, Clerici C. Hypoxia upregulates activity and expression of the glucose transporter GLUT1 in alveolar epithelial cells. Am J Respir Cell Mol Biol. 1999;21:710–8.

    Article  CAS  PubMed  Google Scholar 

  32. Wright EM, Loo DD, Hirayama BA. Biology of human sodium glucose transporters. Physiol Rev. 2011;91:733–94.

    Article  CAS  PubMed  Google Scholar 

  33. Gorboulev V, Schurmann A, Vallon V, Kipp H, Jaschke A, Klessen D, et al. Na(+)-D-glucose cotransporter SGLT1 is pivotal for intestinal glucose absorption and glucose-dependent incretin secretion. Diabetes. 2012;61:187–96.

    Article  CAS  PubMed  Google Scholar 

  34. Cavin JB, Couvelard A, Lebtahi R, Ducroc R, Arapis K, Voitellier E, et al. Differences in alimentary glucose absorption and intestinal disposal of blood glucose after Roux-en-Y gastric bypass vs sleeve gastrectomy. Gastroenterology. 2016;150:454–64e9.

    Article  CAS  PubMed  Google Scholar 

  35. Mumphrey MB, Hao Z, Townsend RL, Patterson LM, Berthoud HR. Sleeve gastrectomy does not cause hypertrophy and reprogramming of intestinal glucose metabolism in rats. Obes Surg. 2015;25:1468–73.

    Article  PubMed  PubMed Central  Google Scholar 

  36. 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;252:50–6.

    Article  PubMed  Google Scholar 

  37. 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;341:406–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hansen CF, Bueter M, Theis N, Lutz T, Paulsen S, Dalboge LS, et al. Hypertrophy dependent doubling of L-cells in Roux-en-Y gastric bypass operated rats. PLoS One. 2013;8:e65696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mumphrey MB, Patterson LM, Zheng H, Berthoud HR. Roux-en-Y gastric bypass surgery increases number but not density of CCK-, GLP-1-, 5-HT-, and neurotensin-expressing enteroendocrine cells in rats. Neurogastroenterol Motil. 2013;25:e70–9.

    Article  CAS  PubMed  Google Scholar 

  40. Pathak P, Liu H, Boehme S, Xie C, Krausz KW, Gonzalez F, et al. Farnesoid X receptor induces Takeda G-protein receptor 5 cross-talk to regulate bile acid synthesis and hepatic metabolism. J Biol Chem. 2017;292:11055–69.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Tsuchiya T, Naitoh T, Nagao M, Tanaka N, Watanabe K, Imoto H, et al. Increased bile acid signals after duodenal-jejunal bypass improve non-alcoholic steatohepatitis (NASH) in a rodent model of diet-induced NASH. Obes Surg. 2018;28:1643–52.

    Article  PubMed  Google Scholar 

  42. Bloch O, Broide E, Ben-Yehudah G, Cantrell D, Shirin H, Rapoport MJ. Nutrient induced type 2 and chemical induced type 1 experimental diabetes differently modulate gastric GLP-1 receptor expression. J Diabetes Res. 2015;2015:561353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lozano I, Van der Werf R, Bietiger W, Seyfritz E, Peronet C, Pinget M, et al. High-fructose and high-fat diet-induced disorders in rats: impact on diabetes risk, hepatic and vascular complications. Nutr Metab. 2016;13:15

    Article  CAS  Google Scholar 

  44. Kawasaki T, Ohta M, Kawano Y, Masuda T, Gotoh K, Inomata M, et al. Effects of sleeve gastrectomy and gastric banding on the hypothalamic feeding center in an obese rat model. Surg Today. 2015;45:1560–6.

    Article  CAS  PubMed  Google Scholar 

  45. Miyachi T, Nagao M, Shibata C, Kitahara Y, Tanaka N, Watanabe K, et al. Biliopancreatic limb plays an important role in metabolic improvement after duodenal-jejunal bypass in a rat model of diabetes. Surgery. 2016;159:1360–71.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Ms. Yuiko Aso and Mayumi Wada for their technical assistance with the experiments.

Author information

Authors and Affiliations

  1. Department of Gastroenterological and Pediatric Surgery, Oita University Faculty of Medicine, 1-1 Idaigaoka, Hasama-machi, Yufu, Oita, 879-5593, Japan

    Hiroomi Takayama, Masayuki Ohta, Kazuhiro Tada, Kiminori Watanabe, Takahide Kawasaki, Yuichi Endo, Yukio Iwashita & Masafumi Inomata

Authors
  1. Hiroomi Takayama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Masayuki Ohta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuhiro Tada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kiminori Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Takahide Kawasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yuichi Endo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yukio Iwashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Masafumi Inomata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hiroomi Takayama.

Ethics declarations

Conflict of interest

This work was supported by JSPS KAKENHI Grant Number JP16K10505. The authors declare that they have no conflicts of interest.

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

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Takayama, H., Ohta, M., Tada, K. et al. Additional effects of duodenojejunal bypass on glucose metabolism in a rat model of sleeve gastrectomy. Surg Today 49, 637–644 (2019). https://doi.org/10.1007/s00595-019-1772-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00595-019-1772-x

Keywords

Search

Navigation