Changes in hedonic hunger and food reward after a similar weight loss induced by a very low-energy diet or bariatric surgery

Marthe Isaksen Aukan, Ingrid Øfsti Brandsaeter, Silje Skårvold, Graham Finlayson, Siren Nymo, Silvia Coutinho, Catia Martins, Marthe Isaksen Aukan, Ingrid Øfsti Brandsaeter, Silje Skårvold, Graham Finlayson, Siren Nymo, Silvia Coutinho, Catia Martins

Abstract

Objective: The aim of this study was to compare changes in hedonic hunger and food reward in individuals with severe obesity achieving 10% to 15% weight loss with a very low-energy diet (VLED) alone or VLED and bariatric surgery.

Methods: Patients scheduled for sleeve gastrectomy (SG) or Roux-en-Y gastric bypass (RYGB) initiated a VLED 2 weeks prior to surgery and continued the diet for 8 weeks postoperatively. BMI-matched controls underwent a VLED for 10 weeks. Hedonic hunger was assessed with the Power of Food Scale, and food reward with the Leeds Food Preference Questionnaire, pre and post intervention.

Results: A total of 44 participants completed the study: 15 SG, 14 RYGB, and 15 controls (61%, 79% and 69% females, respectively; BMI: 40.5 ± 0.5 kg/m2 ; age: 43.9 ± 1.4 years). Average weight loss was 18.3 ± 0.6 kg (16%), comprising 13.5 ± 0.5 kg fat mass, with no significant differences between groups. Similar reductions in hedonic hunger were observed in all groups. Overall, food reward was similarly reduced in SG and RYGB groups, whereas controls showed little or no change.

Conclusions: Independent of modality, weight loss seems to reduce hedonic hunger, but bariatric surgery leads to several additional favorable changes in food reward and preferences.

Trial registration: ClinicalTrials.gov NCT04051190.

Conflict of interest statement

The authors declared no conflict of interest.

© 2022 The Authors. Obesity published by Wiley Periodicals LLC on behalf of The Obesity Society (TOS).

Figures

FIGURE 1
FIGURE 1
Study design. BL, baseline; PA, physical activity; RYGB, Roux‐en‐Y gastric bypass; SG, sleeve gastrectomy; VLED, very low‐energy diet; W11, week 11; WL, weight loss [Color figure can be viewed at wileyonlinelibrary.com]
FIGURE 2
FIGURE 2
Flow diagram of the study. RYGB, Roux‐en‐Y gastric bypass; SG, sleeve gastrectomy [Color figure can be viewed at wileyonlinelibrary.com]
FIGURE 3
FIGURE 3
Power of Food Scale scores. Data presented as mean ± SE. Asterisks denote significant differences over time (***p < 0.001, **p < 0.01) BL, baseline; RYGB, Roux‐en Y gastric bypass; SG, sleeve gastrectomy; W11, week 11

References

    1. Wing RR, Phelan S. Long‐term weight loss maintenance. Am J Clin Nutr. 2005;82(suppl 1):222S‐225S.
    1. Sundström J, Bruze G, Ottosson J, Marcus C, Näslund I, Neovius M. Weight loss and heart failure: a nationwide study of gastric bypass surgery versus intensive lifestyle treatment. Circulation. 2017;135:1577‐1585.
    1. Al‐Najim W, Docherty NG, le Roux CW. Food intake and eating behavior after bariatric surgery. Physiol Rev. 2018;98:1113‐1141.
    1. Murphy KG, Dhillo WS, Bloom SR. Gut peptides in the regulation of food intake and energy homeostasis. Endocr Rev. 2006;27:719‐727.
    1. Berthoud HR, Münzberg H, Morrison CD. Blaming the brain for obesity: integration of hedonic and homeostatic mechanisms. Gastroenterology. 2017;152:1728‐1738.
    1. Berthoud HR. Homeostatic and non‐homeostatic pathways involved in the control of food intake and energy balance. Obesity (Silver Spring). 2006;14(suppl 5):197S‐200S.
    1. Berridge KC. ‘Liking’ and ‘wanting’ food rewards: brain substrates and roles in eating disorders. Physiol Behav. 2009;97:537‐550.
    1. Volkow ND, Wang GJ, Fowler JS, et al. "Nonhedonic" food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect. Synapse. 2002;44:175‐180.
    1. Lutter M, Nestler EJ. Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr. 2009;139:629‐632.
    1. Giesen JCAH, Havermans RC, Douven A, Tekelenburg M, Jansen A. Will work for snack food: the association of BMI and snack reinforcement. Obesity (Silver Spring). 2010;18:966‐970.
    1. Schultes B, Ernst B, Wilms B, Thurnheer M, Hallschmid M. Hedonic hunger is increased in severely obese patients and is reduced after gastric bypass surgery. Am J Clin Nutr. 2010;92:277‐283.
    1. Bartoshuk LM, Duffy VB, Hayes JE, Moskowitz HR, Snyder DJ. Psychophysics of sweet and fat perception in obesity: problems, solutions and new perspectives. Philos Trans R Soc Lond B Biol Sci. 2006;361:1137‐1148.
    1. Carvalho‐Ferreira JP, Finlayson G, da Cunha DT, Caldas G, Bandoni D, de Rosso VV. Adiposity and binge eating are related to liking and wanting for food in Brazil: a cultural adaptation of the Leeds food preference questionnaire. Appetite. 2019;133:174‐183.
    1. Epstein LH, Carr KA, Lin H, Fletcher KD, Roemmich JN. Usual energy intake mediates the relationship between food reinforcement and BMI. Obesity (Silver Spring). 2012;20:1815‐1819.
    1. Nymo S, Coutinho SR, Jørgensen J, et al. Timeline of changes in appetite during weight loss with a ketogenic diet. Int J Obes (Lond). 2017;41:1224‐1231.
    1. Sumithran P, Prendergast LA, Delbridge E, et al. Long‐term persistence of hormonal adaptations to weight loss. N Engl J Med 2011;365:1597‐1604.
    1. Oustric P, Gibbons C, Beaulieu K, Blundell J, Finlayson G. Changes in food reward during weight management interventions ‐ a systematic review. Obes Rev. 2018;19:1642‐1658.
    1. Ullrich J, Ernst B, Wilms B, Thurnheer M, Hallschmid M, Schultes B. The hedonic drive to consume palatable foods appears to be lower in gastric band carriers than in severely obese patients who have not undergone a bariatric surgery. Obes Surg. 2013;23:474‐479.
    1. Deloose E, Janssen P, Lannoo M, Van der Schueren B, Depoortere I, Tack J. Higher plasma motilin levels in obese patients decrease after Roux‐en‐Y gastric bypass surgery and regulate hunger. Gut. 2016;65:1110‐1118.
    1. Ammon BS, Bellanger DE, Geiselman PJ, Primeaux SD, Yu Y, Greenway FL. Short‐term pilot study of the effect of sleeve gastrectomy on food preference. Obes Surg. 2015;25:1094‐1097.
    1. Primeaux SD, Tzeng TH, Allerton TD, et al. Differences in short‐term food preferences following vertical sleeve gastrectomy and Roux‐en‐Y gastric bypass surgery. Obes Res Clin Pract. 2015;9:628‐632.
    1. Leahey TM, Bond DS, Raynor H, et al. Effects of bariatric surgery on food cravings: do food cravings and the consumption of craved foods "normalize" after surgery? Surg Obes Relat Dis. 2012;8:84‐91.
    1. Olbers T, Björkman S, Lindroos A, et al. Body composition, dietary intake, and energy expenditure after laparoscopic Roux‐en‐Y gastric bypass and laparoscopic vertical banded gastroplasty: a randomized clinical trial. Ann Surg. 2006;244:715‐722.
    1. Bueter M, Miras AD, Chichger H, et al. Alterations of sucrose preference after Roux‐en‐Y gastric bypass. Physiol Behav. 2011;104:709‐721.
    1. Nance K, Eagon JC, Klein S, Pepino MY. Effects of sleeve gastrectomy vs. Roux‐en‐Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity. Nutrients. 2017;10:18. doi:10.3390/nu10010018
    1. Holinski F, Menenakos C, Haber G, Olze H, Ordemann J. Olfactory and gustatory function after bariatric surgery. Obes Surg. 2015;25:2314‐2320.
    1. Jakicic JM, Marcus M, Gallagher KI, et al. Evaluation of the SenseWear Pro Armband to assess energy expenditure during exercise. Med Sci Sports Exerc. 2004;36:897‐904.
    1. Lowe MR, Butryn ML, Didie ER, et al. The Power of Food Scale. A new measure of the psychological influence of the food environment. Appetite. 2009;53:114‐118.
    1. Oustric P, Thivel D, Dalton M, et al. Measuring food preference and reward: application and cross‐cultural adaptation of the Leeds Food Preference Questionnaire in human experimental research. Food Qual Prefer. 2020;80:103824. doi:10.1016/j.foodqual.2019.103824
    1. Iepsen EW, Lundgren J, Holst JJ, Madsbad S, Torekov SS. Successful weight loss maintenance includes long‐term increased meal responses of GLP‐1 and PYY3‐36. Eur J Endocrinol. 2016;174:775‐784.
    1. Cameron JD, Goldfield GS, Cyr MJ, Doucet E. The effects of prolonged caloric restriction leading to weight‐loss on food hedonics and reinforcement. Physiol Behav. 2008;94:474‐480.
    1. O'Neil PM, Theim KR, Boeka A, Johnson G, Miller‐Kovach K. Changes in weight control behaviors and hedonic hunger during a 12‐week commercial weight loss program. Eat Behav. 2012;13:354‐360.
    1. Ross KM, Eastman A, Ugwoaba UA, Demos KE, Lillis J, Wing RR. Food reward sensitivity, impulsivity, and weight change during and after a 3‐month weight loss program. PLoS One. 2020;15:e0243530. doi:10.1371/journal.pone.0243530
    1. Cushing CC, Benoit SC, Peugh JL, Reiter‐Purtill J, Inge TH, Zeller MH. Longitudinal trends in hedonic hunger after Roux‐en‐Y gastric bypass in adolescents. Surg Obes Relat Dis. 2014;10:125‐130.
    1. Ullrich J, Ernst B, Wilms B, Thurnheer M, Schultes B. Roux‐en Y gastric bypass surgery reduces hedonic hunger and improves dietary habits in severely obese subjects. Obes Surg. 2013;23:50‐55.
    1. Beaulieu K, Casanova N, Oustric P, et al. Matched weight loss through intermittent or continuous energy restriction does not lead to compensatory increases in appetite and eating behavior in a randomized controlled trial in women with overweight and obesity. J Nutr. 2020;150:623‐633.
    1. Oustric P, Beaulieu K, Casanova N, et al. Food liking but not wanting decreases after controlled intermittent or continuous energy restriction to ≥5% weight loss in women with overweight/obesity. Nutrients. 2021;13:182. doi:10.3390/nu13010182
    1. Martin CK, Rosenbaum D, Han H, et al. Change in food cravings, food preferences, and appetite during a low‐carbohydrate and low‐fat diet. Obesity (Silver Spring). 2011;19:1963‐1970.
    1. Laurenius A, Werling M, le Roux CW, Fandriks L, Olbers T. Dumping symptoms is triggered by fat as well as carbohydrates in patients operated with Roux‐en‐Y gastric bypass. Surg Obes Relat Dis. 2017;13:1159‐1164.
    1. Wang GJ, Volkow ND, Logan J , et al. Brain dopamine and obesity. Lancet. 2001;357(9253):354‐357.
    1. Karlsson HK, Tuominen L, Helin S, Salminen P, Nuutila P, Nummenmaa L . Mesolimbic opioid‐dopamine interaction is disrupted in obesity but recovered by weight loss following bariatric surgery. Transl Psychiatry. 2021;11(1):259. doi:10.1038/s41398-021-01370-2
    1. Gibbons C, Blundell J, Tetens Hoff S, Dahl K, Bauer R, Baekdal T. Effects of oral semaglutide on energy intake, food preference, appetite, control of eating and body weight in subjects with type 2 diabetes. Diabetes Obes Metab. 2021;23:581‐588.
    1. Dye L, Blundell JE. Menstrual cycle and appetite control: implications for weight regulation. Hum Reprod. 1997;12:1142‐1151.
    1. Chao A, Grilo CM, White MA, Sinha R. Food cravings mediate the relationship between chronic stress and body mass index. J Health Psychol. 2015;20:721‐729.

Source: PubMed

Sponsorer og samarbeidspartnere

Medisinsk tilstand

Legemiddelintervensjoner

3
Abonnere