Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Bariatric and Metabolic Surgery Original Article
  • Published:

Neural and humoral changes associated with the adjustable gastric band: insights from a rodent model

International Journal of Obesity volume 36, pages 1403–1411 (2012)Cite this article

Subjects

Abstract

BACKGROUND:

Bariatric surgical procedures, including the laparoscopic adjustable gastric band (LAGB), are currently the only effective treatments for morbid obesity, however, there is no clear understanding of the mechanisms underpinning the efficacy of LAGB. The aim of this study is to examine changes in activation of the sensory neuronal pathways and levels of circulating gut hormones associated with inflation of an AGB.

DESIGN AND RESULTS:

The trajectory within the central nervous system of polysynaptic projections of sensory neurons innervating the stomach was determined using the transsynaptically transported herpes simplex virus (HSV). Populations of HSV-infected neurons were present in the brainstem, hypothalamus and cortical regions associated with energy balance. An elevation of Fos protein was present within the nucleus of the solitary tract, a region of the brainstem involved in the control of food intake, following acute and chronic band inflation. Two approaches were used to test (1) the impact of inflation of the band alone (on a standard caloric background) or (2) the impact of a standard caloric meal (on the background of the inflated band) on circulating gut hormones. Importantly, there was a significant elevation of glucagon-like peptide-1 (GLP-1) and peptide YY (PYY) following oral gavage of a liquid meal in animals with pre-inflated bands. There was no impact of inflation of the band alone on circulating GLP-1, PYY or ghrelin in animals on a standard caloric background.

CONCLUSION:

These data are consistent with the notion that the LAGB exerts its effects on satiety, reduced food intake and reduced body weight by the modulation of both neural and hormonal responses with the latter involving an elevation of meal-related levels of GLP-1 and PYY. These data are contrary to the view that the surgery is purely ‘restrictive’.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Dansinger ML, Tatsioni A, Wong JB, Chung M, Balk EM . Meta-analysis: the effect of dietary counseling for weight loss. Ann Intern Med 2007; 147: 41–50.

    Article  Google Scholar 

  2. Padwal R, Li SK, Lau DC . Long-term pharmacotherapy for overweight and obesity: a systematic review and meta-analysis of randomized controlled trials. Int J Obes Relat Metab Disord 2003; 27: 1437–1446.

    Article  CAS  Google Scholar 

  3. Vetter ML, Faulconbridge LF, Webb VL, Wadden TA . Behavioral and pharmacologic therapies for obesity. Nat Rev Endocrinol 2010; 6: 578–588.

    Article  CAS  Google Scholar 

  4. O’Brien PE, McPhail T, Chaston TB, Dixon JB . Systematic review of medium-term weight loss after bariatric operations. Obes Surg 2006; 16: 1032–1040.

    Article  Google Scholar 

  5. Stefater MA, Perez-Tilve D, Chambers AP, Wilson-Perez HE, Sandoval DA, Berger J et al. Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology 2010; 138: 2426–2436, 2436 e1–3.

    Article  CAS  Google Scholar 

  6. Korner J, Inabnet W, Febres G, Conwell IM, McMahon DJ, Salas R et al. Prospective study of gut hormone and metabolic changes after adjustable gastric banding and Roux-en-Y gastric bypass. Int J Obes (Lond) 2009; 33: 786–795.

    Article  CAS  Google Scholar 

  7. Shin AC, Zheng H, Townsend RL, Sigalet DL, Berthoud HR . Meal-induced hormone responses in a rat model of Roux-en-Y gastric bypass surgery. Endocrinology 2010; 151: 1588–1597.

    Article  CAS  Google Scholar 

  8. Stylopoulos N, Davis P, Pettit JD, Rattner DW, Kaplan LM . Changes in serum ghrelin predict weight loss after Roux-en-Y gastric bypass in rats. Surg Endosc 2005; 19: 942–946.

    Article  CAS  Google Scholar 

  9. Rubino F, Schauer PR, Kaplan LM, Cummings DE . Metabolic surgery to treat type 2 diabetes: clinical outcomes and mechanisms of action. Annu Rev Med 2010; 61: 393–411.

    Article  CAS  Google Scholar 

  10. Kashyap SR, Daud S, Kelly KR, Gastaldelli A, Win H, Brethauer S et al. Acute effects of gastric bypass versus gastric restrictive surgery on beta-cell function and insulinotropic hormones in severely obese patients with type 2 diabetes. Int J Obes (Lond) 2010; 34: 462–471.

    Article  CAS  Google Scholar 

  11. Keating CL, Dixon JB, Moodie ML, Peeters A, Playfair J, O’Brien PE . Cost-efficacy of surgically induced weight loss for the management of type 2 diabetes: a randomized controlled trial. Diabetes Care 2009; 32: 580–584.

    Article  Google Scholar 

  12. Zheng H, Shin AC, Lenard NR, Townsend RL, Patterson LM, Sigalet DL 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–R1282.

    Article  CAS  Google Scholar 

  13. Monteiro MP, Monteiro JD, Aguas AP, Cardoso MH . A rat model of restrictive bariatric surgery with gastric banding. Obes Surg 2006; 16: 48–51.

    Article  Google Scholar 

  14. Endo Y, Ohta M, Kai S, Kitano S . An obese rat model of bariatric surgery with gastric banding. Obes Surg 2007; 17: 815–819.

    Article  Google Scholar 

  15. 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: 201–211.

    Article  CAS  Google Scholar 

  16. Kampe J, Brown WA, Stefanidis A, Dixon JB, Oldfield BJ . A rodent model of adjustable gastric band surgery-implications for the understanding of underlying mechanisms. Obes Surg 2009; 19: 625–631.

    Article  CAS  Google Scholar 

  17. Baringer JR, Swoveland P . Recovery of herpes-simplex virus from human trigeminal ganglions. N Engl J Med 1973; 288: 648–650.

    Article  CAS  Google Scholar 

  18. Dix RD, Baringer JR, Panitch HS, Rosenberg SH, Hagedorn J, Whaley J . Recurrent herpes simplex encephalitis: recovery of virus after Ara-A treatment. Ann Neurol 1983; 13: 196–200.

    Article  CAS  Google Scholar 

  19. Rinaman L, Hoffman GE, Dohanics J, Le WW, Stricker EM, Verbalis JG . Cholecystokinin activates catecholaminergic neurons in the caudal medulla that innervate the paraventricular nucleus of the hypothalamus in rats. J Comp Neurol 1995; 360: 246–256.

    Article  CAS  Google Scholar 

  20. Paxinos G, Watson C . The Rat Brain in Stereotaxic Coordinates. Academic: Sydney, Australia, 1998.

    Google Scholar 

  21. Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR . Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 1989; 283: 248–268.

    Article  CAS  Google Scholar 

  22. Barraco R, el-Ridi M, Ergene E, Parizon M, Bradley D . An atlas of the rat subpostremal nucleus tractus solitarius. Brain Res Bull 1992; 29: 703–765.

    Article  CAS  Google Scholar 

  23. Ter Horst GJ, de Boer P, Luiten PG, van Willigen JD . Ascending projections from the solitary tract nucleus to the hypothalamus. A Phaseolus vulgaris lectin tracing study in the rat. Neuroscience 1989; 31: 785–797.

    Article  CAS  Google Scholar 

  24. Norgren R . Projections from the nucleus of the solitary tract in the rat. Neuroscience 1978; 3: 207–218.

    Article  CAS  Google Scholar 

  25. Ricardo JA, Koh ET . Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res 1978; 153: 1–26.

    Article  CAS  Google Scholar 

  26. Schwartz MW, Woods SC, Porte Jr D, Seeley RJ, Baskin DG . Central nervous system control of food intake. Nature 2000; 404: 661–671.

    Article  CAS  Google Scholar 

  27. Schwartz MW, Woods SC, Seeley RJ, Barsh GS, Baskin DG, Leibel RL . Is the energy homeostasis system inherently biased toward weight gain? Diabetes 2003; 52: 232–238.

    Article  CAS  Google Scholar 

  28. Elmquist JK, Coppari R, Balthasar N, Ichinose M, Lowell BB . Identifying hypothalamic pathways controlling food intake, body weight, and glucose homeostasis. J Comp Neurol 2005; 493: 63–71.

    Article  CAS  Google Scholar 

  29. Seeley RJ, Woods SC . Monitoring of stored and available fuel by the CNS: implications for obesity. Nat Rev Neurosci 2003; 4: 901–909.

    Article  CAS  Google Scholar 

  30. Elmquist JK, Elias CF, Saper CB . From lesions to leptin: hypothalamic control of food intake and body weight. Neuron 1999; 22: 221–232.

    Article  CAS  Google Scholar 

  31. Wang GJ, Tomasi D, Backus W, Wang R, Telang F, Geliebter A, et al. Gastric distention activates satiety circuitry in the human brain. Neuroimage 2008; 39: 1824–1831.

    Article  Google Scholar 

  32. Oldfield BJ, Bicknell RJ, McAllen RM, Weisinger RS, McKinley MJ . Intravenous hypertonic saline induces Fos immunoreactivity in neurons throughout the lamina terminalis. Brain Res 1991; 561: 151–156.

    Article  CAS  Google Scholar 

  33. Favretti F, Segato G, Ashton D, Busetto L, De Luca M, Mazza M et al. Laparoscopic adjustable gastric banding in 1,791 consecutive obese patients: 12-year results. Obes Surg 2007; 17: 168–175.

    Article  Google Scholar 

  34. Sjostrom L, Narbro K, Sjostrom CD, Karason K, Larsson B, Wedel H et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med 2007; 357: 741–752.

    Article  Google Scholar 

  35. Phillips RJ, Powley TL . Tension and stretch receptors in gastrointestinal smooth muscle: re-evaluating vagal mechanoreceptor electrophysiology. Brain Res Rev 2000; 34: 1–26.

    Article  CAS  Google Scholar 

  36. Blackshaw LA, Brookes SJH, Grundy D, Schemann M . Sensory transmission in the gastrointestinal tract. Neurogastroenterol Motil 2007; 19: 1–19.

    Article  CAS  Google Scholar 

  37. Dixon AF, Dixon JB, O’Brien PE . Laparoscopic adjustable gastric banding induces prolonged satiety: a randomized blind crossover study. J Clin Endocrinol Metab 2005; 90: 813–819.

    Article  CAS  Google Scholar 

  38. Monteiro MP, Ribeiro AH, Nunes AF, Sousa MM, Monteiro JD, Aguas AP et al. Increase in ghrelin levels after weight loss in obese Zucker rats is prevented by gastric banding. Obes Surg 2007; 17: 1599–1607.

    Article  Google Scholar 

  39. Harvey EJ, Arroyo K, Korner J, Inabnet WB . Hormone changes affecting energy homeostasis after metabolic surgery. Mt Sinai J Med 2010; 77: 446–465.

    Article  Google Scholar 

  40. Pedersen JB, Larsen JF, Drewes AM, Arveschoug A, Kroustrup JP, Gregersen H . Weight loss after gastric banding is associated with pouch pressure and not pouch emptying rate. Obes Surg 2009; 19: 850–855.

    Article  Google Scholar 

  41. de Jong JR, van Ramshorst B, Gooszen HG, Smout AJ, Tiel-Van Buul MM . Weight loss after laparoscopic adjustable gastric banding is not caused by altered gastric emptying. Obes Surg 2009; 19: 287–292.

    Article  CAS  Google Scholar 

  42. Burton PR, Yap K, Brown WA, Laurie C, O’Donnell M, Hebbard G et al. Changes in satiety, supra- and infraband transit, and gastric emptying following laparoscopic adjustable gastric banding: a prospective follow-up study. Obes Surg 2011; 21: 217–223.

    Article  Google Scholar 

  43. Burton PR, Yap K, Brown WA, Laurie C, O’Donnell M, Hebbard G et al. Effects of adjustable gastric bands on gastric emptying, supra- and infraband transit and satiety: a randomized double-blind crossover trial using a new technique of band visualization. Obes Surg 2010; 20: 1690–1697.

    Article  Google Scholar 

  44. Cummings DE, Overduin J . Gastrointestinal regulation of food intake. J Clin Invest 2007; 117: 13–23.

    Article  CAS  Google Scholar 

  45. Lin HC, Taylor IL . Release of peptide YY by fat in the proximal but not distal gut depends on an atropine-sensitive cholinergic pathway. Regul Pept 2004; 117: 73–76.

    Article  CAS  Google Scholar 

  46. Tadross JA, le Roux CW . The mechanisms of weight loss after bariatric surgery. Int J Obes (Lond) 2009; 33 (Suppl 1): S28–S32.

    Article  Google Scholar 

Download references

Author information

Author notes

  1. J Kampe and A Stefanidis: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Physiology, Monash University, Clayton, Victoria, Australia

    J Kampe, A Stefanidis, S H Lockie, A Odoi, S J Spencer & B J Oldfield

  2. Department of Surgery, Monash University, The Alfred Hospital, Melbourne, Victoria, Australia

    W A Brown

  3. Human Neurotransmitters Laboratory, Baker IDI Heart and Diabetes Institute, Melbourne, Victoria, Australia

    J B Dixon

  4. Department of General Practice, Obesity Research Unit, Monash University, Notting Hill, Victoria, Australia

    J B Dixon

  5. Allergan, Irvine, CA, USA

    J Raven

Authors
  1. J Kampe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A Stefanidis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S H Lockie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. W A Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J B Dixon
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A Odoi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. S J Spencer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. J Raven
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. B J Oldfield
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to B J Oldfield.

Ethics declarations

Competing interests

Professor Oldfield, Associate Professor Dixon and Dr Raven are the recipients of an Australian Research Council Linkage Grant (LP100200782), of which Allergan is an industry partner. Associate Professor Dixon reported that he is a consultant for Allergan Inc. and his institutions receive research support from Allergan Inc. Dr Brown reported receiving an honorarium from Allergan Inc. for attending a scientific advisory panel in London in 2009. Dr Brown is director of the Centre for Obesity Research and Education (CORE). CORE receives a grant from Allergan for research support. Dr Raven receives compensation as an employee for Allergan. As such, Dr Raven also has a financial holding in the form of company stock (Allergan). Dr Raven is the co-author on several patent applications associated with similar work, but ownership and all financial rights have been consigned to Allergan. The remaining authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kampe, J., Stefanidis, A., Lockie, S. et al. Neural and humoral changes associated with the adjustable gastric band: insights from a rodent model. Int J Obes 36, 1403–1411 (2012). https://doi.org/10.1038/ijo.2012.25

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2012.25

Keywords

This article is cited by

Search

Advanced search

Quick links