Effects of gastric remnant gastrectomy following gastric bypass surgery on weight loss and glucose metabolism in rats with obesity and type 2 diabetes mellitus_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

GUO Pei ¹ , HOU Dongsheng ² , YAO Libin ² , HONG Jian ² , ZHU Xiaocheng ² ,  SHAO Yong ²

1. Graduate School, Xuzhou Medical University, Xuzhou, Jiangsu 221004, P. R. China;
2. Department of Gastrointestinal Surgery, Affiliated Hospital of Xuzhou Medical University, Xuzhou, Jiangsu 221002, P. R. China;

Corresponding author：

SHAO Yong, Email: shaoyutong1975@163.com

Keywords：

type 2 diabetes mellitus; obesity; gastric bypass; gastric remnant; weight loss; anti-diabetic

DOI：

10.7507/1007-9424.202102012

Video：

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Objective To investigate the effect of the remnant stomach after gastric bypass (GB) surgery on the weight loss and glucose metabolism in rats with obese and type 2 diabetes mellitus (T2DM).Methods High fat feeding for one month combined with intraperitoneal injection of low-dose streptozotocin was used to induce obese rats with T2DM. Twenty-four rats with obese and type T2DM successfully established were randomly divided into resectional gastric bypass (R-GB) group, GB surgery (GB group), and sham operation (SO) group, eight rats in each group. The weight loss and anti-diabetic effect of the R-GB and GB were compared. Body weight, food intake, and fasting blood glucose (FBG) were measured at week 1 before operation and week 1–8 after the operation. Oral glucose tolerance test (OGTT) and insulin tolerance test (ITT) were performed using tail venous blood at week 1 before operation and on week 8 after operation (at 0, 30, 60, 90, and 120 min). The levels of serum glucagon like peptide-1 (GLP-1), gastrin, insulin, and glucagon at week 1 before operation and at week 8 after operation were detected, meanwhile the homeostasis model assessment insulin resistance (HOMA-IR) index was calculated.Results ① The body weight and food intake of the rats in the R-GB group and GB group were lower than those in the SO group after operation (P<0.05) and which were lower than before operation (P<0.05), but the differences were not significant between the R-GB group and GB group after operation (P>0.05). ② The levels of FBG in the R-GB group only at week 1–4 after operation were lower than those before operation (P<0.05), while which in the GB group at week 1–8 after operation were lower than those before operation and were lower than in the SO group (P<0.05), but which in the R-GB group only at week 2–4 after operation were lower than in the SO group and which were higher than that in the GB group from 3 to 8 weeks after operation (P<0.05). ③ The area under receiver operating characteristic curves (AUCs) of blood glucoses of OGTT and ITT and HOMA-IR index at week 8 after operation were lower than those before operation (P<0.05) in the GB group and which were lower than those the other two groups (P<0.05). ④ The AUC of gastrin level at week 8 after operation was lower than that before operation in the R-GB group and which lower than that in the other two groups (P<0.05). The AUC values of insulin and glucagon levels at week 8 after operation were lower than those before operation in the GB group and which lower than those in the other two groups (P<0.05). The AUC of GLP-1 level at week 8 after operation was higher than that before operation in the GB group and which higher than that in the other two groups (P<0.05).Conclusions GB could remarkably improve glucose metabolism and weight loss in obese rat with T2DM. Gastric remnant gastrectomy following GB has a remarkable anti-diabetic effect, but it doesn’t effect on weight loss.

Citation： GUO Pei, HOU Dongsheng, YAO Libin, HONG Jian, ZHU Xiaocheng, SHAO Yong. Effects of gastric remnant gastrectomy following gastric bypass surgery on weight loss and glucose metabolism in rats with obesity and type 2 diabetes mellitus. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2021, 28(10): 1280-1286. doi: 10.7507/1007-9424.202102012 Copy

1.	Zheng Y, Ley SH, Hu FB. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol, 2018, 14(2): 88-98.
2.	American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of medical care in diabetes—2021. Diabetes Care, 2021, 44(Suppl 1): S15-S33.
3.	Ferraz-Bannitz R, Welendorf CR, Coelho PO, et al. Bariatric surgery can acutely modulate ER-stress and inflammation on subcutaneous adipose tissue in non-diabetic patients with obesity. Diabetol Metab Syndr, 2021, 13(1): 19.
4.	Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med, 2014, 370(21): 2002-2013.
5.	Mizandari M, Keshavarz P, Azrumelashvili T, et al. Left gastric artery embolization for obesity treatment: A systematic review and meta-analysis of human and animal studies. Abdom Radiol (NY), 2021 Apr 7. Online ahead of print.
6.	Woźniewska P, Diemieszczyk I, Groth D, et al. The influence of patient’s age on metabolic and bariatric results of laparoscopic sleeve gastrectomy in 2-year observation. BMC Surg, 2020, 20(1): 323.
7.	Brethauer SA, Aminian A, Romero-Talamás H, et al. Can diabetes be surgically cured? Long-term metabolic effects of bariatric surgery in obese patients with type 2 diabetes mellitus. Ann Surg, 2013, 258(4): 628-636.
8.	Hayoz C, Hermann T, Raptis DA, et al. Comparison of metabolic outcomes in patients undergoing laparoscopic Roux-en-Y gastric bypass versus sleeve gastrectomy—A systematic review and meta-analysis of randomised controlled trials. Swiss Med Wkly, 2018, 148: w14633.
9.	Hayashi SY, Faintuch J, Yagi OK, et al. Does Roux-en-Y gastrectomy for gastric cancer influence glucose homeostasis in lean patients? Surg Endosc, 2013, 27(8): 2829-2835.
10.	Zhou D, Jiang X, Jian W, et al. Comparing the effectiveness of total gastrectomy and gastric bypass on glucose metabolism in diabetic rats. Obes Surg, 2016, 26(1): 119-125.
11.	Widjaja J, Dolo PR, Zhang Q, et al. Bypassed and preserved stomach resulted in superior glucose control in Sprague-Dawley rats with streptozotocin-induced diabetes. Sci Rep, 2019, 9(1): 9981.
12.	Meguid MM, Ramos EJ, Suzuki S, et al. A surgical rat model of human Roux-en-Y gastric bypass. J Gastrointest Surg, 2004, 8(5): 621-630.
13.	Taylor DK, Mook DM. Isoflurane waste anesthetic gas concentrations associated with the open-drop method. J Am Assoc Lab Anim Sci, 2009, 48(1): 61-64.
14.	Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
15.	Strong VE, Wu AW, Selby LV, et al. Differences in gastric cancer survival between the U. S. and China. J Surg Oncol, 2015, 112(1): 31-37.
16.	Braghetto I, Csendes A, Korn O, et al. Laparoscopic resectional gastric bypass in patients with morbid obesity: Experience on 112 consecutive patients. J Gastrointest Surg, 2011, 15(1): 71-80.
17.	Park JY, Kim YJ. Laparoscopic resectional gastric bypass: Initial experience in morbidly obese Korean patients. Surg Today, 2015, 45(8): 1032-1039.
18.	Rehfeld JF, Friis-Hansen L, Goetze JP, et al. The biology of cholecystokinin and gastrin peptides. Curr Top Med Chem, 2007, 7(12): 1154-1165.
19.	Saillan-Barreau C, Dufresne M, Clerc P, et al. Evidence for a functional role of the cholecystokinin-B/gastrin receptor in the human fetal and adult pancreas. Diabetes, 1999, 48(10): 2015-2021.
20.	Rooman I, Lardon J, Bouwens L. Gastrin stimulates beta-cell neogenesis and increases islet mass from transdifferentiated but not from normal exocrine pancreas tissue. Diabetes, 2002, 51(3): 686-690.
21.	Téllez N, Joanny G, Escoriza J, et al. Gastrin treatment stimulates β-cell regeneration and improves glucose tolerance in 95% pancreatectomized rats. Endocrinology, 2011, 152(7): 2580-2588.
22.	Sasaki S, Miyatsuka T, Matsuoka TA, et al. Activation of GLP-1 and gastrin signalling induces in vivo reprogramming of pancreatic exocrine cells into beta cells in mice. Diabetologia, 2015, 58(11): 2582-2591.
23.	Bödvarsdóttir TB, Hove KD, Gotfredsen CF, et al. Treatment with a proton pump inhibitor improves glycaemic control in Psammomys obesus, a model of type 2 diabetes. Diabetologia, 2010, 53(10): 2220-2223.
24.	Singh PK, Hota D, Dutta P, et al. Pantoprazole improves glycemic control in type 2 diabetes: a randomized, double-blind, placebo-controlled trial. J Clin Endocrinol Metab, 2012, 97(11): E2105-E2108.
25.	Cao Y, Cao X, Liu XM. Expression of cholecystokinin2-receptor in rat and human L cells and the stimulation of glucagon-like peptide-1 secretion by gastrin treatment. Acta Histochem, 2015, 117(2): 205-210.
26.	Sandoval D. CNS GLP-1 regulation of peripheral glucose homeostasis. Physiol Behav, 2008, 94(5): 670-674.
27.	Thaler JP, Cummings DE. Minireview: Hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology, 2009, 150(6): 2518-2525.
28.	Pournaras DJ, Osborne A, Hawkins SC, et al. Remission of type 2 diabetes after gastric bypass and banding: mechanisms and 2 year outcomes. Ann Surg, 2010, 252(6): 966-971.
29.	Buteau J. GLP-1 receptor signaling: Effects on pancreatic beta-cell proliferation and survival. Diabetes Metab, 2008, 34 Suppl 2: S73-S77.
30.	Fosgerau K, Jessen L, Lind Tolborg J, et al. The novel GLP-1-gastrin dual agonist, ZP3022, increases β-cell mass and prevents diabetes in db/db mice. Diabetes Obes Metab, 2013, 15(1): 62-71.
31.	Suarez-Pinzon WL, Power RF, Yan Y, et al. Combination therapy with glucagon-like peptide-1 and gastrin restores normoglycemia in diabetic NOD mice. Diabetes, 2008, 57(12): 3281-3288.
32.	Rehfeld JF. Incretin physiology beyond glucagon-like peptide 1 and glucose-dependent insulinotropic polypeptide: cholecystokinin and gastrin peptides. Acta Physiol (Oxf), 2011, 201(4): 405-411.
33.	Hutch CR, Sandoval D. The role of GLP-1 in the metabolic success of bariatric surgery. Endocrinology, 2017, 158(12): 4139-4151.

1. Zheng Y, Ley SH, Hu FB. Global aetiology and epidemiology of type 2 diabetes mellitus and its complications. Nat Rev Endocrinol, 2018, 14(2): 88-98.
2. American Diabetes Association. 2. Classification and diagnosis of diabetes: Standards of medical care in diabetes—2021. Diabetes Care, 2021, 44(Suppl 1): S15-S33.
3. Ferraz-Bannitz R, Welendorf CR, Coelho PO, et al. Bariatric surgery can acutely modulate ER-stress and inflammation on subcutaneous adipose tissue in non-diabetic patients with obesity. Diabetol Metab Syndr, 2021, 13(1): 19.
4. Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med, 2014, 370(21): 2002-2013.
5. Mizandari M, Keshavarz P, Azrumelashvili T, et al. Left gastric artery embolization for obesity treatment: A systematic review and meta-analysis of human and animal studies. Abdom Radiol (NY), 2021 Apr 7. Online ahead of print.
6. Woźniewska P, Diemieszczyk I, Groth D, et al. The influence of patient’s age on metabolic and bariatric results of laparoscopic sleeve gastrectomy in 2-year observation. BMC Surg, 2020, 20(1): 323.
7. Brethauer SA, Aminian A, Romero-Talamás H, et al. Can diabetes be surgically cured? Long-term metabolic effects of bariatric surgery in obese patients with type 2 diabetes mellitus. Ann Surg, 2013, 258(4): 628-636.
8. Hayoz C, Hermann T, Raptis DA, et al. Comparison of metabolic outcomes in patients undergoing laparoscopic Roux-en-Y gastric bypass versus sleeve gastrectomy—A systematic review and meta-analysis of randomised controlled trials. Swiss Med Wkly, 2018, 148: w14633.
9. Hayashi SY, Faintuch J, Yagi OK, et al. Does Roux-en-Y gastrectomy for gastric cancer influence glucose homeostasis in lean patients? Surg Endosc, 2013, 27(8): 2829-2835.
10. Zhou D, Jiang X, Jian W, et al. Comparing the effectiveness of total gastrectomy and gastric bypass on glucose metabolism in diabetic rats. Obes Surg, 2016, 26(1): 119-125.
11. Widjaja J, Dolo PR, Zhang Q, et al. Bypassed and preserved stomach resulted in superior glucose control in Sprague-Dawley rats with streptozotocin-induced diabetes. Sci Rep, 2019, 9(1): 9981.
12. Meguid MM, Ramos EJ, Suzuki S, et al. A surgical rat model of human Roux-en-Y gastric bypass. J Gastrointest Surg, 2004, 8(5): 621-630.
13. Taylor DK, Mook DM. Isoflurane waste anesthetic gas concentrations associated with the open-drop method. J Am Assoc Lab Anim Sci, 2009, 48(1): 61-64.
14. Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA Cancer J Clin, 2016, 66(2): 115-132.
15. Strong VE, Wu AW, Selby LV, et al. Differences in gastric cancer survival between the U. S. and China. J Surg Oncol, 2015, 112(1): 31-37.
16. Braghetto I, Csendes A, Korn O, et al. Laparoscopic resectional gastric bypass in patients with morbid obesity: Experience on 112 consecutive patients. J Gastrointest Surg, 2011, 15(1): 71-80.
17. Park JY, Kim YJ. Laparoscopic resectional gastric bypass: Initial experience in morbidly obese Korean patients. Surg Today, 2015, 45(8): 1032-1039.
18. Rehfeld JF, Friis-Hansen L, Goetze JP, et al. The biology of cholecystokinin and gastrin peptides. Curr Top Med Chem, 2007, 7(12): 1154-1165.
19. Saillan-Barreau C, Dufresne M, Clerc P, et al. Evidence for a functional role of the cholecystokinin-B/gastrin receptor in the human fetal and adult pancreas. Diabetes, 1999, 48(10): 2015-2021.
20. Rooman I, Lardon J, Bouwens L. Gastrin stimulates beta-cell neogenesis and increases islet mass from transdifferentiated but not from normal exocrine pancreas tissue. Diabetes, 2002, 51(3): 686-690.
21. Téllez N, Joanny G, Escoriza J, et al. Gastrin treatment stimulates β-cell regeneration and improves glucose tolerance in 95% pancreatectomized rats. Endocrinology, 2011, 152(7): 2580-2588.
22. Sasaki S, Miyatsuka T, Matsuoka TA, et al. Activation of GLP-1 and gastrin signalling induces in vivo reprogramming of pancreatic exocrine cells into beta cells in mice. Diabetologia, 2015, 58(11): 2582-2591.
23. Bödvarsdóttir TB, Hove KD, Gotfredsen CF, et al. Treatment with a proton pump inhibitor improves glycaemic control in Psammomys obesus, a model of type 2 diabetes. Diabetologia, 2010, 53(10): 2220-2223.
24. Singh PK, Hota D, Dutta P, et al. Pantoprazole improves glycemic control in type 2 diabetes: a randomized, double-blind, placebo-controlled trial. J Clin Endocrinol Metab, 2012, 97(11): E2105-E2108.
25. Cao Y, Cao X, Liu XM. Expression of cholecystokinin2-receptor in rat and human L cells and the stimulation of glucagon-like peptide-1 secretion by gastrin treatment. Acta Histochem, 2015, 117(2): 205-210.
26. Sandoval D. CNS GLP-1 regulation of peripheral glucose homeostasis. Physiol Behav, 2008, 94(5): 670-674.
27. Thaler JP, Cummings DE. Minireview: Hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology, 2009, 150(6): 2518-2525.
28. Pournaras DJ, Osborne A, Hawkins SC, et al. Remission of type 2 diabetes after gastric bypass and banding: mechanisms and 2 year outcomes. Ann Surg, 2010, 252(6): 966-971.
29. Buteau J. GLP-1 receptor signaling: Effects on pancreatic beta-cell proliferation and survival. Diabetes Metab, 2008, 34 Suppl 2: S73-S77.
30. Fosgerau K, Jessen L, Lind Tolborg J, et al. The novel GLP-1-gastrin dual agonist, ZP3022, increases β-cell mass and prevents diabetes in db/db mice. Diabetes Obes Metab, 2013, 15(1): 62-71.
31. Suarez-Pinzon WL, Power RF, Yan Y, et al. Combination therapy with glucagon-like peptide-1 and gastrin restores normoglycemia in diabetic NOD mice. Diabetes, 2008, 57(12): 3281-3288.
32. Rehfeld JF. Incretin physiology beyond glucagon-like peptide 1 and glucose-dependent insulinotropic polypeptide: cholecystokinin and gastrin peptides. Acta Physiol (Oxf), 2011, 201(4): 405-411.
33. Hutch CR, Sandoval D. The role of GLP-1 in the metabolic success of bariatric surgery. Endocrinology, 2017, 158(12): 4139-4151.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Effects of gastric remnant gastrectomy following gastric bypass surgery on weight loss and glucose metabolism in rats with obesity and type 2 diabetes mellitus

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