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

  • Hiroomi TakayamaEmail author
  • Masayuki Ohta
  • Kazuhiro Tada
  • Kiminori Watanabe
  • Takahide Kawasaki
  • Yuichi Endo
  • Yukio Iwashita
  • Masafumi Inomata
Original Article
  • 17 Downloads

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.

Keywords

Sleeve gastrectomy with duodenojejunal bypass Sleeve gastrectomy Glucose metabolism GLUT1 SGLT1 

Notes

Acknowledgements

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

Compliance with ethical standards

Conflict of interest

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

References

  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. 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.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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.CrossRefGoogle Scholar
  23. 23.
    Batterham RL, Cummings DE. Mechanisms of diabetes improvement following bariatric/metabolic surgery. Diabetes Care. 2016;39:893–901.CrossRefGoogle Scholar
  24. 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.CrossRefGoogle Scholar
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 28.
    Kahn BB. Facilitative glucose transporters: regulatory mechanisms and dysregulation in diabetes. J Clin Invest. 1992;89:1367–74.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 30.
    Mueckler M. Facilitative glucose transporters. Eur J Biochem. 1994;219:713–25.CrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 32.
    Wright EM, Loo DD, Hirayama BA. Biology of human sodium glucose transporters. Physiol Rev. 2011;91:733–94.CrossRefGoogle Scholar
  33. 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.CrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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;13:15CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Hiroomi Takayama
    • 1
    Email author
  • Masayuki Ohta
    • 1
  • Kazuhiro Tada
    • 1
  • Kiminori Watanabe
    • 1
  • Takahide Kawasaki
    • 1
  • Yuichi Endo
    • 1
  • Yukio Iwashita
    • 1
  • Masafumi Inomata
    • 1
  1. 1.Department of Gastroenterological and Pediatric SurgeryOita University Faculty of MedicineYufuJapan

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