Vagal Innervation of Intestine Contributes to Weight Loss After Roux-en-Y Gastric Bypass Surgery in Rats

Obesity Surgery

Volumn 24, Issue 12, 2014, Pages 2145-2151

  Hao, Zheng ^a   Townsend, R Leigh ^a   Mumphrey, Michael B ^a   Patterson, Laurel M ^a   Ye, Jianping ^a   Berthoud, Hans Rudolf ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

Author keywords

Adiposity; Bariatric surgery; Fat preference; Rat; Vagus nerve

Indexed keywords

ANIMAL; DISEASE MODEL; FOOD INTAKE; INNERVATION; INTESTINE; MALE; OBESITY, MORBID; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; STOMACH BYPASS; VAGOTOMY; VAGUS NERVE; WEIGHT REDUCTION;

ANIMALS; APPETITE REGULATION; DISEASE MODELS, ANIMAL; GASTRIC BYPASS; INTESTINES; MALE; OBESITY, MORBID; RATS; RATS, SPRAGUE-DAWLEY; VAGOTOMY; VAGUS NERVE; WEIGHT LOSS;

EID: 84939894575     PISSN: 09608923     EISSN: 17080428     Source Type: Journal    
DOI: 10.1007/s11695-014-1338-3     Document Type: Article

References (37)

1. Mingrone G, Panunzi S, De Gaetano A, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 2012;366:1577–85.
2. 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.
3. Arnold M, Mura A, Langhans W, et al. Gut vagal afferents are not necessary for the eating-stimulatory effect of intraperitoneally injected ghrelin in the rat. J Neurosci. 2006;26:11052–60.
4. Reidelberger RD, Hernandez J, Fritzsch B, et al. Abdominal vagal mediation of the satiety effects of CCK in rats. Am J Physiol Regul Integr Comp Physiol. 2004;286:R1005–12.
5. Merchenthaler I, Lane M, Shughrue P. Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol. 1999;403:261–80.
6. Yamamoto H, Kishi T, Lee CE, et al. Glucagon-like peptide-1-responsive catecholamine neurons in the area postrema link peripheral glucagon-like peptide-1 with central autonomic control sites. J Neurosci. 2003;23:2939–46.
7. Koda S, Date Y, Murakami N, et al. The role of the vagal nerve in peripheral PYY3-36-induced feeding reduction in rats. Endocrinology. 2005;146:2369–75.
8. Smith GP, Jerome C, Norgren R. Afferent axons in abdominal vagus mediate satiety effect of cholecystokinin in rats. Am J Physiol. 1985;249:R638–41.
9. Date Y, Murakami N, Toshinai K, et al. The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology. 2002;123:1120–8.
10. Batterham RL, Cowley MA, Small CJ, et al. Gut hormone PYY(3-36) physiologically inhibits food intake. Nature. 2002;418:650–4.
11. Abbott CR, Monteiro M, Small CJ, et al. The inhibitory effects of peripheral administration of peptide YY(3-36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal–brainstem–hypothalamic pathway. Brain Res. 2005;1044:127–31.
12. Berthoud HR. Vagal and hormonal gut–brain communication: from satiation to satisfaction. Neurogastroenterol Motil. 2008;20 Suppl 1:64–72.
13. Wang GJ, Tomasi D, Backus W, et al. Gastric distention activates satiety circuitry in the human brain. Neuroimage. 2008;39:1824–31.
14. Phillips RJ, Powley TL. Gastric volume rather than nutrient content inhibits food intake. Am J Physiol. 1996;271:R766–9.
15. Kissileff HR, Carretta JC, Geliebter A, et al. Cholecystokinin and stomach distension combine to reduce food intake in humans. Am J Physiol Regul Integr Comp Physiol. 2003;285:R992–8.
16. Miranda A, Mickle A, Medda B, et al. Altered mechanosensitive properties of vagal afferent fibers innervating the stomach following gastric surgery in rats. Neuroscience. 2009;162:1299–306.
17. Berthoud HR, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Auton Neurosci. 2000;85:1–17.
18. Berthoud HR, Patterson LM, Neumann F, et al. Distribution and structure of vagal afferent intraganglionic laminar endings (IGLEs) in the rat gastrointestinal tract. Anat Embryol (Berl). 1997;195:183–91.
19. Zagorodnyuk VP, Chen BN, Brookes SJ. Intraganglionic laminar endings are mechano-transduction sites of vagal tension receptors in the guinea-pig stomach. J Physiol. 2001;534:255–68.
20. Zheng H, Shin AC, Lenard NR, et al. Meal patterns, satiety, and food choice in a rat model of Roux-en-Y gastric bypass surgery. Am J Physiol Regul Integr Comp Physiol. 2009;297:R1273–82.
21. Furnes MW, Stenstrom B, Tommeras K, et al. Feeding behavior in rats subjected to gastrectomy or gastric bypass surgery. Eur Surg Res. 2008;40:279–88.
22. Bjorklund P, Laurenius A, Een E, et al. Is the roux limb a determinant for meal size after gastric bypass surgery? Obes Surg. 2010;20:1408–14.
23. Grundy D. Neuroanatomy of visceral nociception: vagal and splanchnic afferent. Gut. 2002;51 Suppl 1:i2–5.
24. Hao Z, Zhao Z, Berthoud HR, et al. Development and verification of a mouse model for roux-en-Y gastric bypass surgery with a small gastric pouch. PLoS ONE. 2013;8:e52922.
25. Powley TL, Fox EA, Berthoud HR. Retrograde tracer technique for assessment of selective and total subdiaphragmatic vagotomies. Am J Physiol. 1987;253:R361–70.
26. Berthoud HR, Powley TL. Identification of vagal preganglionics that mediate cephalic phase insulin response. Am J Physiol. 1990;258:R523–30.
27. Shin AC, Zheng H, Townsend RL, et al. Longitudinal assessment of food intake, fecal energy loss, and energy expenditure after Roux-en-Y gastric bypass surgery in high-fat-fed obese rats. Obes Surg. 2013;23:531–40.
28. Bueter M, Lowenstein C, Ashrafian H, et al. Vagal sparing surgical technique but not stoma size affects body weight loss in rodent model of gastric bypass. Obes Surg. 2010;20:616–22.
29. Wang Y, Liu J. Combination of bypassing stomach and vagus dissection in high-fat diet-induced obese rats—a long-term investigation. Obes Surg. 2010;20:375–9.
30. Perathoner A, Weiss H, Santner W, et al. Vagal nerve dissection during pouch formation in laparoscopic Roux-Y-gastric bypass for technical simplification: does it matter? Obes Surg. 2009;19:412–7.
31. Raybould HE, Tache Y. Capsaicin-sensitive vagal afferent fibers and stimulation of gastric acid secretion in anesthetized rats. Eur J Pharmacol. 1989;167:237–43.
32. Kelly L, Morales S, Smith BK, et al. Capsaicin-treated rats permanently overingest low- but not high-concentration sucrose solutions. Am J Physiol Regul Integr Comp Physiol. 2000;279:R1805–12.
33. Schwartz GJ, Salorio CF, Skoglund C, et al. Gut vagal afferent lesions increase meal size but do not block gastric preload-induced feeding suppression. Am J Physiol. 1999;276:R1623–9.
34. Berthoud HR, Shin AC, Zheng H. Obesity surgery and gut–brain communication. Physiol Behav. 2011;105:106–19.
35. Berthoud HR, Kressel M, Raybould HE, et al. Vagal sensors in the rat duodenal mucosa: distribution and structure as revealed by in vivo DiI-tracing. Anat Embryol (Berl). 1995;191:203–12.
36. Powley TL, Spaulding RA, Haglof SA. Vagal afferent innervation of the proximal gastrointestinal tract mucosa: chemoreceptor and mechanoreceptor architecture. J Comp Neurol. 2011;519:644–60.
37. Cox JE. Cholecystokinin satiety involves CCKA receptors perfused by the superior pancreaticoduodenal artery. Am J Physiol. 1998;274:R1390–6.