Skip to main content
Top
Published in: European Journal of Nutrition 4/2016

01-06-2016 | Original Contribution

Responses of peripheral endocannabinoids and endocannabinoid-related compounds to hedonic eating in obesity

Authors: A M Monteleone, V Di Marzo, P Monteleone, R Dalle Grave, T Aveta, M El Ghoch, F Piscitelli, U Volpe, S Calugi, M Maj

Published in: European Journal of Nutrition | Issue 4/2016

Login to get access

Abstract

Purpose

Hedonic eating occurs independently from homeostatic needs prompting the ingestion of pleasurable foods that are typically rich in fat, sugar and/or salt content. In normal weight healthy subjects, we found that before hedonic eating, plasma levels of 2-arachidonoylglycerol (2-AG) were higher than before nonhedonic eating, and although they progressively decreased after food ingestion in both eating conditions, they were significantly higher in hedonic eating. Plasma levels of anandamide (AEA), oleoylethanolamide (OEA) and palmitoylethanolamide (PEA), instead, progressively decreased in both eating conditions without significant differences. In this study, we investigated the responses of AEA, 2-AG, OEA and PEA to hedonic eating in obese individuals.

Methods

Peripheral levels of AEA, 2-AG, OEA and PEA were measured in 14 obese patients after eating favourite (hedonic eating) and non-favourite (nonhedonic eating) foods in conditions of no homeostatic needs.

Results

Plasma levels of 2-AG increased after eating the favourite food, whereas they decreased after eating the non-favourite food, with the production of the endocannabinoid being significantly enhanced in hedonic eating. Plasma levels of AEA decreased progressively in nonhedonic eating, whereas they showed a decrease after the exposure to the favourite food followed by a return to baseline values after eating it. No significant differences emerged in plasma OEA and PEA responses to favourite and non-favourite food.

Conclusion

Present findings compared with those obtained in our previously studied normal weight healthy subjects suggest deranged responses of endocannabinoids to food-related reward in obesity.
Literature
1.
go back to reference Lowe MR, Butryn ML (2007) Hedonic hunger: a new dimension of appetite? Physiol Behav 91:432–439CrossRef Lowe MR, Butryn ML (2007) Hedonic hunger: a new dimension of appetite? Physiol Behav 91:432–439CrossRef
2.
go back to reference Nummenmaa L, Hirvonen J, Hannukainen J, Immonen H, Lindroos M, Salminen P, Nuutila P (2012) Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity. PLoS One 7:e31089–e31089CrossRef Nummenmaa L, Hirvonen J, Hannukainen J, Immonen H, Lindroos M, Salminen P, Nuutila P (2012) Dorsal striatum and its limbic connectivity mediate abnormal anticipatory reward processing in obesity. PLoS One 7:e31089–e31089CrossRef
3.
go back to reference Swinburn B, Sacks G, Hall K, McPherson K, Finegood D, Moodie ML, Gortmaker SL (2011) The global obesity pandemic: shaped by global drivers and local environments. Lancet 378:804–814CrossRef Swinburn B, Sacks G, Hall K, McPherson K, Finegood D, Moodie ML, Gortmaker SL (2011) The global obesity pandemic: shaped by global drivers and local environments. Lancet 378:804–814CrossRef
4.
go back to reference Volkow N, Wang G, Tomasi D, Baler R (2013) The addictive dimensionality of obesity. Biol Psychiatry 73:811–818CrossRef Volkow N, Wang G, Tomasi D, Baler R (2013) The addictive dimensionality of obesity. Biol Psychiatry 73:811–818CrossRef
5.
go back to reference Koob G, Volkow N (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238CrossRef Koob G, Volkow N (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238CrossRef
6.
go back to reference Di Marzo V (2008) Targeting the endocannabinoid system: to enhance or reduce? Nat Rev Drug Discov 7:438–455CrossRef Di Marzo V (2008) Targeting the endocannabinoid system: to enhance or reduce? Nat Rev Drug Discov 7:438–455CrossRef
7.
go back to reference Cristino L, Becker T, Di Marzo V (2014) Endocannabinoids and energy homeostasis: an update. Biofactors 40:389–397CrossRef Cristino L, Becker T, Di Marzo V (2014) Endocannabinoids and energy homeostasis: an update. Biofactors 40:389–397CrossRef
8.
go back to reference Lo Verme J, Gaetani S, Fu J, Oveisi F, Burton K, Piomelli D (2005) Regulation of food intake by oleoylethanolamide. Cell Mol Life Sci 62:708–716CrossRef Lo Verme J, Gaetani S, Fu J, Oveisi F, Burton K, Piomelli D (2005) Regulation of food intake by oleoylethanolamide. Cell Mol Life Sci 62:708–716CrossRef
9.
go back to reference Movahed P, Jönsson BA, Birnir B, Wingstrand JA, Jørgensen TD, Ermund A, Sterner O, Zygmunt PM, Högestätt ED (2005) Endogenous unsaturated C18 N-acylethanolamines are vanilloid receptor (TRPV1) agonists. J Biol Chem 280:38496–38504CrossRef Movahed P, Jönsson BA, Birnir B, Wingstrand JA, Jørgensen TD, Ermund A, Sterner O, Zygmunt PM, Högestätt ED (2005) Endogenous unsaturated C18 N-acylethanolamines are vanilloid receptor (TRPV1) agonists. J Biol Chem 280:38496–38504CrossRef
10.
go back to reference Silvestri C, Di Marzo V (2013) The endocannabinoid system in energy homeostasis and the etiopathology of metabolic disorders. Cell Metab 17:475–490CrossRef Silvestri C, Di Marzo V (2013) The endocannabinoid system in energy homeostasis and the etiopathology of metabolic disorders. Cell Metab 17:475–490CrossRef
11.
go back to reference Adamczyk P, Miszkiel J, McCreary AC, Filip M, Papp M, Przegaliński E (2012) The effects of cannabinoid CB1, CB2 and vanilloid TRPV1 receptor antagonists on cocaine addictive behavior in rats. Brain Res 1444:45–54CrossRef Adamczyk P, Miszkiel J, McCreary AC, Filip M, Papp M, Przegaliński E (2012) The effects of cannabinoid CB1, CB2 and vanilloid TRPV1 receptor antagonists on cocaine addictive behavior in rats. Brain Res 1444:45–54CrossRef
12.
go back to reference Melis M, Muntoni AL, Pistis M (2012) Endocannabinoids and the processing of value-related signals. Front Pharmacol 3:7CrossRef Melis M, Muntoni AL, Pistis M (2012) Endocannabinoids and the processing of value-related signals. Front Pharmacol 3:7CrossRef
13.
go back to reference Monteleone P, Matias I, Martiadis V, De Petrocellis L, Maj M, Di Marzo V (2005) Blood levels of the endocannabinoid anandamide are increased in anorexia nervosa and in binge-eating disorder, but not in bulimia nervosa. Neuropsychopharmacology 30:1216–1221CrossRef Monteleone P, Matias I, Martiadis V, De Petrocellis L, Maj M, Di Marzo V (2005) Blood levels of the endocannabinoid anandamide are increased in anorexia nervosa and in binge-eating disorder, but not in bulimia nervosa. Neuropsychopharmacology 30:1216–1221CrossRef
14.
go back to reference Matias I, Gonthier MP, Orlando P, Martiadis V, De Petrocellis L, Cervino C, Petrosino S, Hoareau L, Festy F, Pasquali R, Roche R, Maj M, Pagotto U, Monteleone P, Di Marzo V (2006) Regulation, function, and dysregulation of endocannabinoids in models of adipose and beta-pancreatic cells and in obesity and hyperglycemia. J Clin Endocrinol Metab 91:3171–3180CrossRef Matias I, Gonthier MP, Orlando P, Martiadis V, De Petrocellis L, Cervino C, Petrosino S, Hoareau L, Festy F, Pasquali R, Roche R, Maj M, Pagotto U, Monteleone P, Di Marzo V (2006) Regulation, function, and dysregulation of endocannabinoids in models of adipose and beta-pancreatic cells and in obesity and hyperglycemia. J Clin Endocrinol Metab 91:3171–3180CrossRef
15.
go back to reference Monteleone P, Piscitelli F, Scognamiglio P, Monteleone AM, Canestrelli B, Di Marzo V, Maj M (2012) Hedonic eating is associated with increased peripheral levels of ghrelin and the endocannabinoid 2-arachidonoyl-glycerol in healthy humans: a pilot study. J Clin Endocrinol Metab 97:E917–E924CrossRef Monteleone P, Piscitelli F, Scognamiglio P, Monteleone AM, Canestrelli B, Di Marzo V, Maj M (2012) Hedonic eating is associated with increased peripheral levels of ghrelin and the endocannabinoid 2-arachidonoyl-glycerol in healthy humans: a pilot study. J Clin Endocrinol Metab 97:E917–E924CrossRef
16.
go back to reference World Health Organization (1998) Obesity: preventing and managing the global epidemic: report of a WHO consultation on obesity (WHO/NUT/NCD). WHO, Geneva World Health Organization (1998) Obesity: preventing and managing the global epidemic: report of a WHO consultation on obesity (WHO/NUT/NCD). WHO, Geneva
17.
go back to reference Annuzzi G, Piscitelli F, Di Marino L, Patti L, Giacco R, Costabile G, Bozzetto L, Riccardi G, Verde R, Petrosino S, Rivellese AA, Di Marzo V (2010) Differential alterations of the concentrations of endocannabinoids and related lipids in the subcutaneous adipose tissue of obese diabetic patients. Lipids Health Dis 9:43CrossRef Annuzzi G, Piscitelli F, Di Marino L, Patti L, Giacco R, Costabile G, Bozzetto L, Riccardi G, Verde R, Petrosino S, Rivellese AA, Di Marzo V (2010) Differential alterations of the concentrations of endocannabinoids and related lipids in the subcutaneous adipose tissue of obese diabetic patients. Lipids Health Dis 9:43CrossRef
18.
go back to reference Dixon JW (1992) BMDP statistical software. Release 7.0. University of California Press, Berkeley Dixon JW (1992) BMDP statistical software. Release 7.0. University of California Press, Berkeley
19.
go back to reference Melis T, Succu S, Sanna F, Boi A, Argiolas A, Melis MR (2007) The cannabinoid antagonist SR 141716A (Rimonabant) reduces the increase of extra-cellular dopamine release in the rat nucleus accumbens induced by a novel high palatable food. Neurosci Lett 419:231–235CrossRef Melis T, Succu S, Sanna F, Boi A, Argiolas A, Melis MR (2007) The cannabinoid antagonist SR 141716A (Rimonabant) reduces the increase of extra-cellular dopamine release in the rat nucleus accumbens induced by a novel high palatable food. Neurosci Lett 419:231–235CrossRef
20.
go back to reference Di Marzo V (2011) Endocannabinoids: an appetite for fat. Proc Natl Acad Sci USA 108:12567–12568CrossRef Di Marzo V (2011) Endocannabinoids: an appetite for fat. Proc Natl Acad Sci USA 108:12567–12568CrossRef
21.
go back to reference Piomelli D (2013) A fatty gut feeling. Trends Endocrinol Metab 24:332–341CrossRef Piomelli D (2013) A fatty gut feeling. Trends Endocrinol Metab 24:332–341CrossRef
22.
go back to reference Erlanson-Albertsson C, Lindqvist A (2010) Fructose affects enzymes involved in the synthesis and degradation of hypothalamic endocannabinoids. Regul Pept 161:87–91CrossRef Erlanson-Albertsson C, Lindqvist A (2010) Fructose affects enzymes involved in the synthesis and degradation of hypothalamic endocannabinoids. Regul Pept 161:87–91CrossRef
23.
go back to reference Di Chiara G (2000) Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol 393:295–314CrossRef Di Chiara G (2000) Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol 393:295–314CrossRef
24.
go back to reference Burger KS, Stice E (2012) Frequent ice cream consumption is associated with reduced striatal response to receipt of an ice cream-based milkshake. Am J Clin Nutr 95:810–817CrossRef Burger KS, Stice E (2012) Frequent ice cream consumption is associated with reduced striatal response to receipt of an ice cream-based milkshake. Am J Clin Nutr 95:810–817CrossRef
25.
go back to reference Avena NM, Rada P, Hoebel BG (2008) Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32:20–39CrossRef Avena NM, Rada P, Hoebel BG (2008) Evidence for sugar addiction: behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32:20–39CrossRef
26.
go back to reference Dagher A (2009) The neurobiology of appetite: hunger as addiction. Int J Obes (Lond) 33(Suppl 2):S30–S33CrossRef Dagher A (2009) The neurobiology of appetite: hunger as addiction. Int J Obes (Lond) 33(Suppl 2):S30–S33CrossRef
27.
go back to reference Ziauddeen H, Farooqi IS, Fletcher PC (2012) Obesity and the brain: how convincing is the addiction model? Nat Rev Neurosci 13:279–286CrossRef Ziauddeen H, Farooqi IS, Fletcher PC (2012) Obesity and the brain: how convincing is the addiction model? Nat Rev Neurosci 13:279–286CrossRef
28.
go back to reference Mahler SV, Smith KS, Berridge KC (2007) Endocannabinoid hedonic hotspot for sensory pleasure: anandamide in nucleus accumbens shell enhances ‘liking’ of a sweet reward. Neuropsychopharmacology 32:2267–2278CrossRef Mahler SV, Smith KS, Berridge KC (2007) Endocannabinoid hedonic hotspot for sensory pleasure: anandamide in nucleus accumbens shell enhances ‘liking’ of a sweet reward. Neuropsychopharmacology 32:2267–2278CrossRef
29.
go back to reference Smith KS, Mahler SV, Pecina S, Berridge KC (2010) Hedonic hotspots: generating sensory pleasure in the brain. In: Kringelbach ML, Berridge KC (eds) Pleasures of the Brain. Oxford University Press, Oxford, pp 27–49 Smith KS, Mahler SV, Pecina S, Berridge KC (2010) Hedonic hotspots: generating sensory pleasure in the brain. In: Kringelbach ML, Berridge KC (eds) Pleasures of the Brain. Oxford University Press, Oxford, pp 27–49
30.
go back to reference Dalton M, Blundell J, Finlayson GS (2013) Examination of food reward and energy intake under laboratory and free-living conditions in a trait binge eating subtype of obesity. Front Psychol 4:1–8CrossRef Dalton M, Blundell J, Finlayson GS (2013) Examination of food reward and energy intake under laboratory and free-living conditions in a trait binge eating subtype of obesity. Front Psychol 4:1–8CrossRef
Metadata
Title
Responses of peripheral endocannabinoids and endocannabinoid-related compounds to hedonic eating in obesity
Authors
A M Monteleone
V Di Marzo
P Monteleone
R Dalle Grave
T Aveta
M El Ghoch
F Piscitelli
U Volpe
S Calugi
M Maj
Publication date
01-06-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 4/2016
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-016-1153-9

Other articles of this Issue 4/2016

European Journal of Nutrition 4/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.