Impact of adaptive gastric electrical stimulation on weight, food intake, and food intake rate in dogs.


Journal

Artificial organs
ISSN: 1525-1594
Titre abrégé: Artif Organs
Pays: United States
ID NLM: 7802778

Informations de publication

Date de publication:
Jun 2022
Historique:
revised: 04 11 2021
received: 02 09 2021
accepted: 07 12 2021
pubmed: 22 12 2021
medline: 21 5 2022
entrez: 21 12 2021
Statut: ppublish

Résumé

Gastric electrical stimulation (GES) has been studied for decades as a promising treatment for obesity. Stimulation pulses with fixed amplitude and pulse width are usually applied, but these have limitations with regard to overcoming habituation to GES and inter-subject variation. This study aims to analyze the efficacy of an adaptive GES protocol for reducing food intake and maintaining lean weight in dogs. Six beagle dogs were implanted with a remotely programmable gastric stimulator. An adaptive protocol was designed to increase the stimulation energy proportionally to the excess of food consumption, with respect to the dogs' maintenance energy requirements. After surgery and habituation to experimental conditions, the dogs went through both a control and a stimulation period of 4 weeks each, in a randomized order. The stimulation parameters were adapted daily. Body weight, food intake, food intake rate, and postprandial cutaneous electrogastrograms (EGG) were recorded to assess the effect of adaptive GES. Adaptive GES decreased food intake and food intake rate (p < 0.05) resulting in weight maintenance. In the absence of GES, the dogs gained weight (p < 0.05). Postprandial EGG dominant frequency was accelerated by GES (p < 0.05). The strategy of adapting the stimulation energy was effective in causing significant mid-term changes. Adaptive GES is effective for reducing food intake and maintaining lean weight. The proposed adaptive strategy may offer benefits to counter habituation and adapt to inter-subject variation in clinical use of GES for obesity.

Sections du résumé

BACKGROUND BACKGROUND
Gastric electrical stimulation (GES) has been studied for decades as a promising treatment for obesity. Stimulation pulses with fixed amplitude and pulse width are usually applied, but these have limitations with regard to overcoming habituation to GES and inter-subject variation. This study aims to analyze the efficacy of an adaptive GES protocol for reducing food intake and maintaining lean weight in dogs.
METHODS METHODS
Six beagle dogs were implanted with a remotely programmable gastric stimulator. An adaptive protocol was designed to increase the stimulation energy proportionally to the excess of food consumption, with respect to the dogs' maintenance energy requirements. After surgery and habituation to experimental conditions, the dogs went through both a control and a stimulation period of 4 weeks each, in a randomized order. The stimulation parameters were adapted daily. Body weight, food intake, food intake rate, and postprandial cutaneous electrogastrograms (EGG) were recorded to assess the effect of adaptive GES.
RESULTS RESULTS
Adaptive GES decreased food intake and food intake rate (p < 0.05) resulting in weight maintenance. In the absence of GES, the dogs gained weight (p < 0.05). Postprandial EGG dominant frequency was accelerated by GES (p < 0.05). The strategy of adapting the stimulation energy was effective in causing significant mid-term changes.
CONCLUSION CONCLUSIONS
Adaptive GES is effective for reducing food intake and maintaining lean weight. The proposed adaptive strategy may offer benefits to counter habituation and adapt to inter-subject variation in clinical use of GES for obesity.

Identifiants

pubmed: 34932224
doi: 10.1111/aor.14156
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1055-1067

Subventions

Organisme : Fonds De La Recherche Scientifique - FNRS
ID : 33666414

Informations de copyright

© 2021 International Center for Artificial Organs and Transplantation and Wiley Periodicals LLC.

Références

The GBD 2015 Obesity Collaborators, Afshin A, Forouzanfar MH, Reitsma MB, Sur P, Estep K, et al. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med. 2017;377(1):13-27.
Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9·1 million participants. Lancet. 2011;377(9765):557-67.
Dobbs R, Sawers C, Thompson F, Manyika J, Woetzel J, Child P, et al. Overcoming obesity: an initial economic analysis. Jakarta: McKinsey Global Institute. 2014;120.
Ng M, Fleming T, Robinson M, Thomson B, Graetz N, Margono C, et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet. 2014;384(9945):766-81.
Yao G, Kang L, Li J, Long Y, Wei H, Ferreira CA, et al. Effective weight control via an implanted self-powered vagus nerve stimulation device. Nat Commun. 2018;9(1):5349.
Weiner JP, Goodwin SM, Chang H-Y, Bolen SD, Richards TM, Johns RA, et al. Impact of bariatric surgery on health care costs of obese persons. JAMA Surg. 2013;148(6):555.
Wang YC, McPherson K, Marsh T, Gortmaker SL, Brown M. Health and economic burden of the projected obesity trends in the USA and the UK. Lancet. 2011;378(9793):815-25.
O’Brien PE. Bariatric surgery: mechanisms, indications and outcomes. J Gastroenterol Hepatol. 2010;25(8):1358-65.
Nguyen NT, Vu S, Kim E, Bodunova N, Phelan MJ. Trends in utilization of bariatric surgery, 2009-2012. Surg Endosc. 2016;30(7):2723-7.
Angrisani L, Santonicola A, Iovino P, Vitiello A, Zundel N, Buchwald H, et al. Bariatric surgery and endoluminal procedures: IFSO Worldwide Survey 2014. Obes Surg. 2017;27(9):2279-89.
Colquitt JL, Pickett K, Loveman E, Frampton GK. Surgery for weight loss in adults. Cochrane Database Syst Rev. 2014;2014:CD003641.
Cha R, Marescaux J, Diana M. Updates on gastric electrical stimulation to treat obesity: systematic review and future perspectives. World J Gastrointest Endosc. 2014;6(9):419.
Colucci RA. Bariatric surgery in patients with type 2 diabetes: a viable option. Postgrad Med. 2012;124(1):24-33.
Encinosa WE, Bernard DM, Du D, Steiner CA. Recent improvements in bariatric surgery outcomes. Med Care. 2009;47(5):531-5.
Virji A, Murr MM. Caring for patients after bariatric surgery. Am Fam Physician. 2006;73(8):1403-8.
Maisiyiti A, Chen JDZ. Systematic review on gastric electrical stimulation in obesity treatment. Expert Rev Med Devices. 2019;16(10):855-61.
Lebovitz HE. Interventional treatment of obesity and diabetes: an interim report on gastric electrical stimulation. Rev Endocr Metab Disord. 2016;17(1):73-80.
Yin J, Chen JDZ. Therapeutic potential of gastric electrical stimulation for obesity. In: Cheng LK, Pullan AJ, Farrugia G, editors. New advances in gastrointestinal motility research. Vol. 10. Dordrecht: Springer; 2013; p. 113-28.
Guo X, Li Y, Yao S, Chen S, Du Y, Wang Z. Parameter selection and stimulating effects of an adjustable gastric electrical stimulator in dogs. Obes Surg. 2014;24(1):78-84.
Song G-Q, Zhu H, Lei Y, Yuan C, Starkebaum W, Yin J, et al. Gastric electrical stimulation optimized to inhibit gastric motility reduces food intake in dogs. Obes Surg. 2015;25(6):1047-55.
Qin C, Chen JDZ, Zhang J, Foreman RD. Modulatory effects and afferent pathways of gastric electrical stimulation on rat thoracic spinal neurons receiving input from the stomach. Neurosci Res. 2007;57(1):29-39.
Song GQ, Hou X, Sun Y, Yang B, Qian W, Chen JDZ. Effects of retrograde gastric electrical stimulation with pulse trains on gastric emptying of solids and plasma hormones in dogs. Am J Surg. 2007;194(1):122-7.
Zhang J, Tang M, Chen JDZ. Gastric electrical stimulation for obesity: the need for a new device using wider pulses. Obesity. 2009;17(3):474-80.
Zhang J, Maude-Griffin R, Zhu H, Sun Y, Starkebaum W, Firestone E, et al. Gastric electrical stimulation parameter dependently alters ventral medial hypothalamic activity and feeding in obese rats. Am J Physiol Gastrointest Liver Physiol. 2011;301(5):912-8.
Guo X, Li Y, Yao S, Chen S, Du Y, Wang Z. The effects of individualized gastric electrical stimulation on food craving and gastrointestinal peptides in dogs. Neuromodulation. 2014;17(5):483-8.
Tang M, Zhang J, Chen JDZ. Central mechanisms of gastric electrical stimulation involving neurons in the paraventricular nucleus of the hypothalamus in rats. Obes Surg. 2006;16(3):344-52.
Paulus GF, van Avesaat M, van Rijn S, Alleleyn A, Swain JM, Abell TL, et al. Multicenter, phase 1, open prospective trial of gastric electrical stimulation for the treatment of obesity: first-in-human results with a novel implantable system. Obes Surg. 2020;30(5):1952-60.
Zhang J, Chen JDZ. Systematic review: applications and future of gastric electrical stimulation. Aliment Pharmacol Ther. 2006;24(7):991-1002.
Xu X, Zhu H, Chen JDZ. Pyloric electrical stimulation reduces food intake by inhibiting gastric motility in dogs. Gastroenterology. 2005;128(1):43-50.
Yin J, Chen JDZ. Implantable gastric electrical stimulation: ready for prime time? Gastroenterology. 2008;134(3):665-7.
Yin J, Chen JDZ. Retrograde gastric electrical stimulation reduces food intake and weight in obese rats. Obes Res. 2005;13(9):1580-7.
Donaldson PEK. The Craggs connector; a termination for Cooper cable. Med Biol Eng Comput. 1985;23:195-6.
Debelle A, de Rooster H, Bianchini E, Lonys L, Huberland F, Vanhoestenberghe A, et al. Optimization and assessment of a novel gastric electrode anchoring system designed to be implanted by minimally invasive surgery. Med Eng Phys. 2021;92:93-101.
Lonys L, Vanhoestenberghe A, Julémont N, Godet S, Delplancke M-P, Mathys P, et al. Silicone rubber encapsulation for an endoscopically implantable gastrostimulator. Med Biol Eng Comput. 2015;53(4):319-29.
Lonys L, Vanhoestenberghe A, Huberty V, Hiernaux M, Cauche N, Julémont N, et al. In vivo validation of a less invasive gastrostimulator. Artif Organs. 2017;41(11):E213-21.
Laflamme DP. Development and validation of a body condition score system for dogs. Canine Pract. 1997;22(4):10-5.
FEDIAF. Nutritional guidelines for complete and complementary pet food for cats and dogs. 2019: 1-96.
Yao S, Ke M, Wang Z, Xu D, Zhang Y, Chen JDZ. Retrograde gastric pacing reduces food intake and delays gastric emptying in humans: a potential therapy for obesity? Dig Dis Sci. 2005;50(9):1569-75.
Xing JH, Chen JDZ. Effects and mechanisms of long-pulse gastric electrical stimulation on canine gastric tone and accommodation. Neurogastroenterol Motil. 2006;18(2):136-43.
Neshev E, Onen D, Jalilian E, Mintchev M. Pre-pyloric neural electrical stimulation produces cholinergically-mediated reverse peristalsis in the acute canine model of microprocessor-invoked gastric motility for the treatment of obesity. Obes Surg. 2006;16(4):510-20.
Sanmiguel CP, Haddad W, Aviv R, Cunneen SA, Phillips EH, Kapella W, et al. The TANTALUS system for obesity: effect on gastric emptying of solids and ghrelin plasma levels. Obes Surg. 2007;17(11):1503-9.
Zhu H, Sallam H, Chen DD, Chen JDZ. Therapeutic potential of synchronized gastric electrical stimulation for gastroparesis: enhanced gastric motility in dogs. Am J Physiol Integr Comp Physiol. 2007;293(5):R1875-81.
Ouyang H, Xing J, Chen JDZ. Tachygastria induced by gastric electrical stimulation is mediated via alpha- and beta-adrenergic pathway and inhibits antral motility in dogs. Neurogastroenterol Motil. 2005;17(6):846-53.
Yin J, Chen J. Inhibitory effects of gastric electrical stimulation on ghrelin-induced excitatory effects on gastric motility and food intake in dogs. Scand J Gastroenterol. 2006;41(8):903-9.
Zhu H, Chen JDZ. Implantable gastric stimulation inhibits gastric motility via sympathetic pathway in dogs. Obes Surg. 2005;15(1):95-100.
Liu J, Hou X, Song G, Cha H, Yang B, Chen JD. Gastric electrical stimulation using endoscopically placed mucosal electrodes reduces food intake in humans. Am J Gastroenterol. 2006;101(4):798-803.
Qin C, Sun Y, Chen JDZ, Foreman RD. Gastric electrical stimulation modulates neuronal activity in nucleus tractus solitarii in rats. Auton Neurosci. 2005;119(1):1-8.
Cigaina V, Hirschberg AL. Gastric pacing for morbid obesity: plasma levels of gastrointestinal peptides and leptin. Obes Res. 2003;11(12):1456-62.
Ouyang H, Yin J, Chen JDZ. Gastric or intestinal electrical stimulation-induced increase in gastric volume is correlated with reduced food intake. Scand J Gastroenterol. 2006;41(11):1261-6.
Cigaina V. Gastric pacing as therapy for morbid obesity: Preliminary results. Obes Surg. 2002;12(S1):S12-6.
Chen JDZ. Mechanisms of action of the implantable gastric stimulator for obesity. Obes Surg. 2004;14(Suppl 1):S28-32.
Dargent J. Gastric electrical stimulation as therapy of morbid obesity: preliminary results from the French study. Obes Surg. 2002;12(2):21-5.
Ouyang H, Yin J, Chen JDZ. Therapeutic potential of gastric electrical stimulation for obesity and its possible mechanisms: a preliminary canine study. Dig Dis Sci. 2003;48(4):698-705.
Aelen P, Neshev E, Cholette M, Crisanti K, Mitchell P, Debru E, et al. Manipulation of food intake and weight dynamics using retrograde neural gastric electrical stimulation in a chronic canine model. Neurogastroenterol Motil. 2008;20(4):358-68.
Bohdjalian A, Prager G, Aviv R, Policker S, Schindler K, Kretschmer S, et al. One-year experience with TantalusTM: a new surgical approach to treat morbid obesity. Obes Surg. 2006;16(5):627-34.
Burger IH. Energy needs of companion animals: matching food intakes to requirements throughout the life cycle. J Nutr. 1994;124(suppl_12):2584S-93.
Horbach T, Thalheimer A, Seyfried F, Eschenbacher F, Schuhmann P, Meyer G. abiliti® closed-loop gastric electrical stimulation system for treatment of obesity: clinical results with a 27-month follow-up. Obes Surg. 2015;25(10):1779-87.

Auteurs

Adrien Debelle (A)

Bio, Electro and Mechanical Systems Department, Ecole polytechnique de Bruxelles, Université libre de Bruxelles, Brussels, Belgium.

Myriam Hesta (M)

Department of Veterinary Medical Imaging and Small Animal Orthopedics, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.

Hilde de Rooster (H)

Small Animal Department, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.

Erika Bianchini (E)

Small Animal Department, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.

Anne Vanhoestenberghe (A)

Aspire Centre for Rehabilitation Engineering and Assistive Technology, Department of Materials and Tissue, University College London, Stanmore, UK.

Emmelie Stock (E)

Department of Veterinary Medical Imaging and Small Animal Orthopedics, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.

Katrien Vanderperren (K)

Department of Veterinary Medical Imaging and Small Animal Orthopedics, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.

Ingeborgh Polis (I)

Small Animal Department, Faculty of Veterinary Medicine, Ghent University, Ghent, Belgium.

Hugo Smets (H)

Bio, Electro and Mechanical Systems Department, Ecole polytechnique de Bruxelles, Université libre de Bruxelles, Brussels, Belgium.

Joaquin Cury (J)

Bio, Electro and Mechanical Systems Department, Ecole polytechnique de Bruxelles, Université libre de Bruxelles, Brussels, Belgium.

Vicente Acuña (V)

Bio, Electro and Mechanical Systems Department, Ecole polytechnique de Bruxelles, Université libre de Bruxelles, Brussels, Belgium.

Alain Delchambre (A)

Bio, Electro and Mechanical Systems Department, Ecole polytechnique de Bruxelles, Université libre de Bruxelles, Brussels, Belgium.

Bernardo Innocenti (B)

Bio, Electro and Mechanical Systems Department, Ecole polytechnique de Bruxelles, Université libre de Bruxelles, Brussels, Belgium.

Jacques Devière (J)

Department of Gastroenterology, Hepatopancreatology, and Digestive Oncology, Erasme University Hospital, Université Libre de Bruxelles, Brussels, Belgium.

Antoine Nonclercq (A)

Bio, Electro and Mechanical Systems Department, Ecole polytechnique de Bruxelles, Université libre de Bruxelles, Brussels, Belgium.

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