Hedonic Eating in Prader–Willi Syndrome Is Associated with Blunted PYY Secretion

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Hedonic Eating in Prader–Willi Syndrome Is Associated with Blunted PYY Secretion View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by AIR Universita degli studi di Milano Food & Nutrition Research ISSN: 1654-6628 (Print) 1654-661X (Online) Journal homepage: http://www.tandfonline.com/loi/zfnr20 Hedonic eating in Prader–Willi syndrome is associated with blunted PYY secretion A. E. Rigamonti, S. Bini, F. Piscitelli, A. Lauritano, V. Di Marzo, C. Vanetti, F. Agosti, A. De Col, E. Lucchetti, G. Grugni & A. Sartorio To cite this article: A. E. Rigamonti, S. Bini, F. Piscitelli, A. Lauritano, V. Di Marzo, C. Vanetti, F. Agosti, A. De Col, E. Lucchetti, G. Grugni & A. Sartorio (2017) Hedonic eating in Prader–Willi syndrome is associated with blunted PYY secretion, Food & Nutrition Research, 61:1, 1297553, DOI: 10.1080/16546628.2017.1297553 To link to this article: http://dx.doi.org/10.1080/16546628.2017.1297553 © 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. Published online: 02 May 2017. Submit your article to this journal View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=zfnr20 Download by: [Università degli Studi di Milano] Date: 02 May 2017, At: 06:08 FOOD & NUTRITION RESEARCH, 2017 VOL. 61, 1297553 http://dx.doi.org/10.1080/16546628.2017.1297553 ORIGINAL ARTICLE Hedonic eating in Prader–Willi syndrome is associated with blunted PYY secretion A. E. Rigamontia, S. Binia,F.Piscitellib, A. Lauritanob,V.DiMarzob,C.Vanettic,F.Agostid,A.DeCold,E.Lucchettid, G. Grugnid,e and A. Sartoriod,e aDepartment of Clinical Sciences and Community Health, University of Milan, Milan, Italy; bEndocannabinoid Research Group, Institute of Biomolecular Chemistry, Consiglio Nazionale delle Ricerche, Pozzuoli, Italy; cDepartment of Medical Biotechnology and Translational Medicine, University of Milan, Milan, Italy; dExperimental Laboratory for Auxo-Endocrinological Research, Istituto Auxologico Italiano, IRCCS, Milan and Piancavallo (VB), Italy; eDivision of Auxology, Istituto Auxologico Italiano, IRCCS, Piancavallo (VB), Italy ABSTRACT ARTICLE HISTORY Hedonic and homeostatic hunger represent two different forms of eating: just for pleasure or Received 4 November 2016 following energy deprivation, respectively. Consumption of food for pleasure was reported to be Accepted 13 February 2017 associated with increased circulating levels of both the orexigenic peptide ghrelin and some KEYWORDS specific endocannabinoids in normal-weight subjects and patients with morbid obesity. To date, Palatable food; PYY; ghrelin; the effects of palatable food on these mediators in Prader–Willi syndrome (PWS) are still CCK; endocannabinoids; unknown. To explore the role of some gastrointestinal orexigenic and anorexigenic peptides Prader-Willi syndrome; and endocannabinoids (and some related congeners) in chocolate consumption, we measured hunger; satiety changes in circulating levels of ghrelin, cholecystokinin (CCK), peptide YY (PYY), anandamide (AEA), 2-arachidonoyl-glycerol (2-AG), palmitoylethanolamide (PEA) and oleoylethanolamide (OEA) in eight satiated adult PWS patients after consumption of chocolate and, on a separate day, of a non-palatable isocaloric food with the same macronutrient composition. Evaluation of hunger and satiety was also performed by visual analogic scale. The anticipatory phase and the consumption of food for pleasure were associated with decreased circulating levels of PYY. An increase in PEA levels was also observed. By contrast, circulating levels of ghrelin, CCK, AEA, 2-AG and OEA did not differ before and after the exposure/ingestion of either chocolate or non- palatable foods. Hunger and satiety were similar in the hedonic and non-palatable sessions. In conclusion, when motivation to eat is promoted by highly palatable foods, a depressed post- prandial PYY secretion is observed in PWS. Although preliminary, these findings seem to hypothesize a possible role of PYY agonists in the management of PWS patients. Abbreviations: AEA, Anandamide; 2-AG, 2-arachidonoyl-glycerol; CB1, cannabinoid receptor type 1; OEA, oleoylethanolamide; PEA, palmitoylethanolamide; PWS: Prader-Willi syndrome; VAS, visual analog scales Introduction hormonal responses (at peripheral level), which involve several appetite-regulating substances [2,3]. A huge In animals and humans, eating is stimulated not only number of gastrointestinal endocrine cells produces by the need to restore energy homeostasis (homeostatic and secretes satiety hormones in response to food hunger), but also by the rewarding properties of highly consumption and digestion. These hormones, includ- palatable foods, mainly fatty and/or sugar-sweet meals, ing cholecystokinin (CCK), peptide YY (PYY) and despite a state of satiety and positive energy balance glucagon-like peptide 1 (GLP-1), suppress homeostatic (hedonic hunger) [1]. Scientific interest is focused on hunger and promote satiety [4]. In addition to these investigating the physiological and pathophysiological anorexigenic peptides, there is an orexigenic peptide mechanisms underlying hedonic hunger in order to produced by the stomach, named ghrelin, which is characterize new pharmacological targets to counteract capable to stimulate not only homeostatic, but also obesity and other eating disorders. hedonic hunger [5,6]. These effects are mediated by Animal studies have demonstrated that homeostatic activation of the receptor, GHS-R1a, which is expressed and hedonic eating are regulated by different, although not only in the hypothalamus (controlling homeostatic overlapping, neural pathways (at central level) and CONTACT A. E. Rigamonti [email protected] Department of Clinical Sciences and Community Health, University of Milan, via Vanvitelli 32, 20129 Milan, Italy © 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 2 A. E. RIGAMONTI ET AL. hunger), but also in tegmental and mesolimbic areas few studies have investigated post-prandial GLP-1, (involved in food-related reward) [5]. CCK and PYY in PWS, besides reporting conflicting Food intake is also stimulated by the endocannabi- results [21,26–30]. Interestingly, an unexpected noids anandamide (AEA) and 2-arachidonoyl-glycerol increase of the post-prandial responses of PYY and (2-AG), two lipid mediators that act mainly at central GLP-1 to fast feeding was observed in adult PWS level by activating the cannabinoid type 1 (CB1) recep- patients, suggesting a potential involvement of these tors, which in turn are widely distributed in several anorexigenic peptides in the pathophysiology of this brain areas, including those involved in the homeo- eating disorder [31]. static and hedonic control of feeding [7,8]. To the best of our knowledge, post-prandial concen- Hedonic hunger has been also investigated in trations of orexigenic and anorexigenic peptides such humans. In this context, Monteleone et al. [9–11] as ghrelin, CCK and PYY have not been assessed in showed that normal-weight, healthy subjects, when PWS patients in the context of hedonic vs homeostatic administered with palatable food, exhibited increased hunger. Additionally, to date, no one has measured circulating levels of both ghrelin and 2-AG, and that post-prandial levels of endocannabinoids in PWS this post-prandial response was disrupted in women patients. with anorexia nervosa, an eating disorder associated Thus, in order to investigate the potential associa- with altered secretion of many appetite-regulating sub- tion of endocannabinoids and gastrointestinal peptides, stances. In another work, circulating levels of CCK specifically, ghrelin, PYY and CCK, with hedonic eat- were reported to be decreased when normal-weight ing in PWS, we have measured here changes in the healthy subjects were exposed to palatable food [12]. circulating levels of these appetite-regulating sub- Furthermore, Rigamonti et al. [13] demonstrated that stances before and after the exposure to and consump- patients with essential morbid obesity exhibited tion of chocolate, a well-known highly palatable food, increased circulating levels of ghrelin, AEA and 2-AG in satiated PWS patients. after anticipation and consumption of chocolate, with no differences in PYY and GLP-1 concentrations. Again in obese individuals, Monteleone et al. [14] Materials and methods reported that plasma levels of 2-AG increased after eating a favourite food, and decreased after eating the Subjects non-favourite food; the levels of AEA, instead, Eight male patients with PWS, aged 19–42 yr decreased progressively in non-hedonic eating, whereas (mean ± SD = 35.6 ± 8.3 yr), having a mean they showed a decrease only immediately after the BMI ± SD 38.8 ± 10.1 kg/m2, hospitalized for a short exposure to the favourite food, followed by a subse- period of time for periodical re-evaluation of their quent increase towards pre-meal levels. clinical conditions, were enrolled into the study. The Prader–Willi syndrome (PWS) is a neurogenetic subjects were recruited from the Division of Auxology disorder, characterized, in addition to other clinical at Istituto Auxologico Italiano, IRCCS, Verbania, Italy. signs and symptoms, by hyperphagia resulting in severe All
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