Vagal Innervation Patterns Following Roux-en-Y Gastric Bypass in the Mouse

Overview

Journal Int J Obes (Lond)

Specialty Endocrinology

Date 2013 Apr 24

PMID 23609934

Citations 28

Authors

L Gautron

J F Zechner

V Aguirre

Affiliations

Soon will be listed here.

Abstract

This study investigated the anatomical integrity of the vagal innervation to the gastrointestinal tract following Roux-en-Y gastric bypass (RYGB) in the mouse. Specifically, the surgical procedure was performed in high-fat-fed reporter mice (Phox2b-Cre-tdTomato), in which the entire vagal innervation of the gastrointestinal tract was fluorescently labeled. As a result, our anatomical observations revealed both qualitative and quantitative changes of the vagal supply to the gut after RYGB. This included the extensive denervation of the glandular and distal stomach, and sites of surgical interventions (clipping and anastomosis). Furthermore, the stomach wall after RYGB frequently contained dystrophic axons and endings, suggestive of vagal neurodegeneration. In contrast, RYGB did not significantly modify the innervation to the rest of the intestines and glucostatic organs. In summary, the present study describes a previously unrecognized pattern of vagal remodeling and denervation following RYGB. Our findings may serve as a guideline for future investigations on the role of gut-brain communication in bariatric surgery.

Citing Articles

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References

Ardila-Hani A, Soffer E . Review article: the impact of bariatric surgery on gastrointestinal motility. Aliment Pharmacol Ther. 2011; 34(8):825-31. DOI: 10.1111/j.1365-2036.2011.04812.x. View

Troy S, Soty M, Ribeiro L, Laval L, Migrenne S, Fioramonti X . 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(3):201-11. DOI: 10.1016/j.cmet.2008.08.008. View

Nestoridi E, Kvas S, Kucharczyk J, Stylopoulos N . Resting energy expenditure and energetic cost of feeding are augmented after Roux-en-Y gastric bypass in obese mice. Endocrinology. 2012; 153(5):2234-44. DOI: 10.1210/en.2011-2041. View

Zechner J, Mirshahi U, Satapati S, Berglund E, Rossi J, Scott M . Weight-independent effects of roux-en-Y gastric bypass on glucose homeostasis via melanocortin-4 receptors in mice and humans. Gastroenterology. 2012; 144(3):580-590.e7. PMC: 3835150. DOI: 10.1053/j.gastro.2012.11.022. View

Kral J . Vagotomy for treatment of severe obesity. Lancet. 1978; 1(8059):307-8. DOI: 10.1016/s0140-6736(78)90074-0. View

Breen D, Rasmussen B, Kokorovic A, Wang R, Cheung G, Lam T . Jejunal nutrient sensing is required for duodenal-jejunal bypass surgery to rapidly lower glucose concentrations in uncontrolled diabetes. Nat Med. 2012; 18(6):950-5. DOI: 10.1038/nm.2745. View

Wang F, Powley T . Vagal innervation of intestines: afferent pathways mapped with new en bloc horseradish peroxidase adaptation. Cell Tissue Res. 2007; 329(2):221-30. DOI: 10.1007/s00441-007-0413-7. View

Berthoud H, Shin A, Zheng H . Obesity surgery and gut-brain communication. Physiol Behav. 2011; 105(1):106-19. PMC: 3118403. DOI: 10.1016/j.physbeh.2011.01.023. View

Bueter M, Lowenstein C, Ashrafian H, Hillebrand J, Bloom S, Olbers T . Vagal sparing surgical technique but not stoma size affects body weight loss in rodent model of gastric bypass. Obes Surg. 2010; 20(5):616-22. PMC: 3715840. DOI: 10.1007/s11695-010-0075-5. View

10.

Yamada H, Kojima K, Inokuchi M, Kawano T, Sugihara K . Efficacy of celiac branch preservation in Roux-en-y reconstruction after laparoscopy-assisted distal gastrectomy. Surgery. 2010; 149(1):22-8. DOI: 10.1016/j.surg.2010.03.002. View

11.

Berthoud H . The vagus nerve, food intake and obesity. Regul Pept. 2008; 149(1-3):15-25. PMC: 2597723. DOI: 10.1016/j.regpep.2007.08.024. View

12.

Scott M, Williams K, Rossi J, Lee C, Elmquist J . Leptin receptor expression in hindbrain Glp-1 neurons regulates food intake and energy balance in mice. J Clin Invest. 2011; 121(6):2413-21. PMC: 3104740. DOI: 10.1172/JCI43703. View

13.

Buchwald H, Williams S . Bariatric surgery worldwide 2003. Obes Surg. 2004; 14(9):1157-64. DOI: 10.1381/0960892042387057. View

14.

Shin A, Zheng H, Berthoud H . Vagal innervation of the hepatic portal vein and liver is not necessary for Roux-en-Y gastric bypass surgery-induced hypophagia, weight loss, and hypermetabolism. Ann Surg. 2011; 255(2):294-301. PMC: 3259289. DOI: 10.1097/SLA.0b013e31823e71b7. View

15.

Zhang T, Uchida T, Gomez G, Lluis F, Thompson J, Greeley Jr G . Neural regulation of peptide YY secretion. Regul Pept. 1993; 48(3):321-8. DOI: 10.1016/0167-0115(93)90160-a. View

16.

Mizrahi M, Ben Yaacov A, Ilan Y . Gastric stimulation for weight loss. World J Gastroenterol. 2012; 18(19):2309-19. PMC: 3353365. DOI: 10.3748/wjg.v18.i19.2309. View