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Published in: Obesity Surgery 8/2015

01-08-2015 | Original Contributions

Sleeve Gastrectomy Does Not Cause Hypertrophy and Reprogramming of Intestinal Glucose Metabolism in Rats

Authors: Michael B. Mumphrey, Zheng Hao, R. Leigh Townsend, Laurel M. Patterson, Hans-Rudolf Berthoud

Published in: Obesity Surgery | Issue 8/2015

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Abstract

Background

Clinical studies have shown similar rapid improvements in body mass and glycemic control after Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG). Evidence suggests that adaptive intestinal tissue growth and reprogramming of intestinal glucose disposal play a key role in the beneficial effects on glucose homeostasis after RYGB, but it is not known whether such adaptive changes also occur after sleeve gastrectomy.

Methods

High-fat diet-induced obese rats were subjected to either VSG or RYGB, and intestinal growth and functional adaptations were assessed by using morphometric, immunohistochemical, and immuno-blot techniques, 3 months after surgery or sham surgery.

Results

The cross-sectional areas of the Roux and common limbs are significantly increased after RYGB compared with sham surgery (Roux limb: 17.1 ± 4.0 vs. 5.5 ± 0.1 mm2; common limb: 11.7 ± 0.6 vs. 5.1 ± 0.5 mm2; p < 0.01), but the cross-sectional area of the corresponding jejunum is not different from controls after VSG. Similarly, mucosal thickness and the number of GLP-1 cells are not increased after VSG. Protein expression of hexokinase II is increased fourfold (p < 0.01) in the Roux limb after RYGB, but not in the jejunum after VSG.

Conclusions

Adaptive hypertrophy and reprogramming of glucose metabolism in the small intestine are not necessary for VSG to improve body composition and glycemic control. The similar beneficial effects of VSG and RYGB on glucose homeostasis might be mediated by different mechanisms.
Literature
1.
go back to reference Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med. 2014;370:2002–13.PubMedCrossRef Schauer PR, Bhatt DL, Kirwan JP, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med. 2014;370:2002–13.PubMedCrossRef
2.
go back to reference Chambers AP, Smith EP, Begg DP, et al. Regulation of gastric emptying rate and its role in nutrient-induced GLP-1 secretion in rats after vertical sleeve gastrectomy. Am J Physiol Endocrinol Metab. 2014;306:E424–32.PubMedCentralPubMedCrossRef Chambers AP, Smith EP, Begg DP, et al. Regulation of gastric emptying rate and its role in nutrient-induced GLP-1 secretion in rats after vertical sleeve gastrectomy. Am J Physiol Endocrinol Metab. 2014;306:E424–32.PubMedCentralPubMedCrossRef
3.
go back to reference Evrard S, Aprahamian M, Hoeltzel A, et al. Trophic and enzymatic adaptation of the intestine to biliopancreatic bypass in the rat. Int J Obes Relat Metab Disord. 1993;17:541–7.PubMed Evrard S, Aprahamian M, Hoeltzel A, et al. Trophic and enzymatic adaptation of the intestine to biliopancreatic bypass in the rat. Int J Obes Relat Metab Disord. 1993;17:541–7.PubMed
4.
go back to reference Borg CM, le Roux CW, Ghatei MA, et al. Biliopancreatic diversion in rats is associated with intestinal hypertrophy and with increased GLP-1, GLP-2 and PYY levels. Obes Surg. 2007;17:1193–8.PubMedCrossRef Borg CM, le Roux CW, Ghatei MA, et al. Biliopancreatic diversion in rats is associated with intestinal hypertrophy and with increased GLP-1, GLP-2 and PYY levels. Obes Surg. 2007;17:1193–8.PubMedCrossRef
5.
go back to reference le Roux CW, Borg C, Wallis K, 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.PubMedCrossRef le Roux CW, Borg C, Wallis K, 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.PubMedCrossRef
6.
go back to reference Taqi E, Wallace LE, de Heuvel E, et al. The influence of nutrients, biliary-pancreatic secretions, and systemic trophic hormones on intestinal adaptation in a Roux-en-Y bypass model. J Pediatr Surg. 2010;45:987–95.PubMedCrossRef Taqi E, Wallace LE, de Heuvel E, et al. The influence of nutrients, biliary-pancreatic secretions, and systemic trophic hormones on intestinal adaptation in a Roux-en-Y bypass model. J Pediatr Surg. 2010;45:987–95.PubMedCrossRef
7.
go back to reference Saeidi N, Meoli L, Nestoridi E, et al. Reprogramming of intestinal glucose metabolism and glycemic control in rats after gastric bypass. Science. 2013;341:406–10.PubMedCentralPubMedCrossRef Saeidi N, Meoli L, Nestoridi E, et al. Reprogramming of intestinal glucose metabolism and glycemic control in rats after gastric bypass. Science. 2013;341:406–10.PubMedCentralPubMedCrossRef
8.
go back to reference Mumphrey MB, Patterson LM, Zheng H, et al. 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.PubMedCentralPubMedCrossRef Mumphrey MB, Patterson LM, Zheng H, et al. 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.PubMedCentralPubMedCrossRef
9.
10.
go back to reference Martin GR, Beck PL, Sigalet DL. Gut hormones, and short bowel syndrome: the enigmatic role of glucagon-like peptide-2 in the regulation of intestinal adaptation. World J Gastroenterol. 2006;12:4117–29.PubMedCentralPubMed Martin GR, Beck PL, Sigalet DL. Gut hormones, and short bowel syndrome: the enigmatic role of glucagon-like peptide-2 in the regulation of intestinal adaptation. World J Gastroenterol. 2006;12:4117–29.PubMedCentralPubMed
11.
go back to reference Martin GR, Wallace LE, Sigalet DL. Glucagon-like peptide-2 induces intestinal adaptation in parenterally fed rats with short bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2004;286:G964–72.PubMedCrossRef Martin GR, Wallace LE, Sigalet DL. Glucagon-like peptide-2 induces intestinal adaptation in parenterally fed rats with short bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2004;286:G964–72.PubMedCrossRef
12.
go back to reference Sigalet DL, Bawazir O, Martin GR, et al. Glucagon-like peptide-2 induces a specific pattern of adaptation in remnant jejunum. Dig Dis Sci. 2006;51:1557–66.PubMedCrossRef Sigalet DL, Bawazir O, Martin GR, et al. Glucagon-like peptide-2 induces a specific pattern of adaptation in remnant jejunum. Dig Dis Sci. 2006;51:1557–66.PubMedCrossRef
13.
go back to reference Kaji T, Tanaka H, Redstone H, et al. Temporal changes in the intestinal growth promoting effects of glucagon-like peptide 2 following intestinal resection. J Surg Res. 2009;152:271–80.PubMedCrossRef Kaji T, Tanaka H, Redstone H, et al. Temporal changes in the intestinal growth promoting effects of glucagon-like peptide 2 following intestinal resection. J Surg Res. 2009;152:271–80.PubMedCrossRef
14.
go back to reference Hua Z, Turner JM, Sigalet DL, et al. Role of glucagon-like peptide-2 deficiency in neonatal short-bowel syndrome using neonatal piglets. Pediatr Res. 2013;73:742–9.PubMedCrossRef Hua Z, Turner JM, Sigalet DL, et al. Role of glucagon-like peptide-2 deficiency in neonatal short-bowel syndrome using neonatal piglets. Pediatr Res. 2013;73:742–9.PubMedCrossRef
15.
go back to reference Ljungmann K, Hartmann B, Kissmeyer-Nielsen P, et al. Time-dependent intestinal adaptation and GLP-2 alterations after small bowel resection in rats. Am J Physiol Gastrointest Liver Physiol. 2001;281:G779–85.PubMed Ljungmann K, Hartmann B, Kissmeyer-Nielsen P, et al. Time-dependent intestinal adaptation and GLP-2 alterations after small bowel resection in rats. Am J Physiol Gastrointest Liver Physiol. 2001;281:G779–85.PubMed
16.
go back to reference Romero F, Nicolau J, Flores L, et al. Comparable early changes in gastrointestinal hormones after sleeve gastrectomy and Roux-En-Y gastric bypass surgery for morbidly obese type 2 diabetic subjects. Surg Endosc. 2012;26:2231–9.PubMedCrossRef Romero F, Nicolau J, Flores L, et al. Comparable early changes in gastrointestinal hormones after sleeve gastrectomy and Roux-En-Y gastric bypass surgery for morbidly obese type 2 diabetic subjects. Surg Endosc. 2012;26:2231–9.PubMedCrossRef
17.
go back to reference Cummings BP, Bettaieb A, Graham JL, et al. Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology. 2012;153:3620–32.PubMedCentralPubMedCrossRef Cummings BP, Bettaieb A, Graham JL, et al. Vertical sleeve gastrectomy improves glucose and lipid metabolism and delays diabetes onset in UCD-T2DM rats. Endocrinology. 2012;153:3620–32.PubMedCentralPubMedCrossRef
18.
go back to reference Kunnecke B, Verry P, Benardeau A, et al. Quantitative body composition analysis in awake mice and rats by magnetic resonance relaxometry. Obes Res. 2004;12:1604–15.PubMedCrossRef Kunnecke B, Verry P, Benardeau A, et al. Quantitative body composition analysis in awake mice and rats by magnetic resonance relaxometry. Obes Res. 2004;12:1604–15.PubMedCrossRef
19.
go back to reference Helmio M, Victorzon M, Ovaska J, et al. Comparison of short-term outcome of laparoscopic sleeve gastrectomy and gastric bypass in the treatment of morbid obesity: a prospective randomized controlled multicenter SLEEVEPASS study with 6-month follow-up. Scand J Surg. 2014;103:175–81.PubMedCrossRef Helmio M, Victorzon M, Ovaska J, et al. Comparison of short-term outcome of laparoscopic sleeve gastrectomy and gastric bypass in the treatment of morbid obesity: a prospective randomized controlled multicenter SLEEVEPASS study with 6-month follow-up. Scand J Surg. 2014;103:175–81.PubMedCrossRef
20.
go back to reference Peterli R, Steinert RE, Woelnerhanssen B, et al. Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes Surg. 2012;22:740–8.PubMedCentralPubMedCrossRef Peterli R, Steinert RE, Woelnerhanssen B, et al. Metabolic and hormonal changes after laparoscopic Roux-en-Y gastric bypass and sleeve gastrectomy: a randomized, prospective trial. Obes Surg. 2012;22:740–8.PubMedCentralPubMedCrossRef
21.
go back to reference Chambers AP, Jessen L, Ryan KK, et al. Weight-independent changes in blood glucose homeostasis after gastric bypass or vertical sleeve gastrectomy in rats. Gastroenterology. 2011;141:950–8.PubMedCentralPubMedCrossRef Chambers AP, Jessen L, Ryan KK, et al. Weight-independent changes in blood glucose homeostasis after gastric bypass or vertical sleeve gastrectomy in rats. Gastroenterology. 2011;141:950–8.PubMedCentralPubMedCrossRef
Metadata
Title
Sleeve Gastrectomy Does Not Cause Hypertrophy and Reprogramming of Intestinal Glucose Metabolism in Rats
Authors
Michael B. Mumphrey
Zheng Hao
R. Leigh Townsend
Laurel M. Patterson
Hans-Rudolf Berthoud
Publication date
01-08-2015
Publisher
Springer US
Published in
Obesity Surgery / Issue 8/2015
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-014-1547-9

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