Elsevier

Psychoneuroendocrinology

Volume 38, Issue 8, August 2013, Pages 1435-1441
Psychoneuroendocrinology

Gastroenteric hormone responses to hedonic eating in healthy humans

https://doi.org/10.1016/j.psyneuen.2012.12.009Get rights and content

Summary

Hedonic eating differentiates from homeostatic eating on two main aspects: the first one is that eating occurs when there is no need for calorie ingestion and the second one is that the food is consumed exclusively for its gustatory and rewarding properties. Gastroeneteric hormones such as ghrelin, colecystokinin-33 (CCK) and peptide YY3–36 (PYY3–36) are known to play a pivotal role in the homeostatic control of food intake. To the contrary, their role in hedonic eating has been never investigated. Here we report peripheral responses of CCK, PYY3–36 and ghrelin to the consumption of food for pleasure in well-nourished satiated healthy subjects.

Plasma levels of CCK, PYY3–36 and ghrelin were measured in 7 satiated healthy subjects before and after ad libitum consumption of both a highly pleasurable food (hedonic eating) and an isoenergetic non-pleasurable food (non-hedonic eating).

The consumption of food for pleasure was associated to a significantly increased production of the hunger hormone ghrelin and a significantly decreased secretion of the satiety hormone CCK. No significant changes in plasma PYY3–36 levels occurred in the two eating conditions.

These preliminary data demonstrate that in hedonic eating the peripheral hunger signal represented by ghrelin secretion is enhanced while the satiety signal of CCK production is decreased. This could be responsible for the persistence of peripheral cues allowing a continued eating as well as for the activation of endogenous reward mechanisms, which can drive food consumption in spite of no energy need, only for reward.

Introduction

In present times, because of the large availability of food in the environment, human beings are prompted to eat not only to maintain energy homeostasis but also just for pleasure. In the first case, named homeostatic eating, food ingestion is driven by acute negative energy imbalance and is independent from the palatability of the food. In the second case, named hedonic eating, the consumption of food occurs even if there is no need for caloric ingestion, and the food is consumed because of its gustatory rewarding properties, independently from calorie content (Lowe and Butryn, 2007). It is intuitive that hedonic eating may promote powerfully food intake in an environment where highly pleasurable foods are omnipresent and contribute to the diffusion of overweight and obesity. Therefore, understanding the physiological modulation of hedonic eating might help to contrast obesity and/or other eating disorders.

A huge amount of research clarified the physiological modulation of homeostatic eating. Briefly, in the condition of acute energy depletion, central and peripheral hunger modulators are released in order to promote food intake. The ingestion of food, in turn, stimulates the release of central and peripheral satiety signals and inhibits the secretion of hunger mediators with the aim to adapt food consumption to the organism's caloric needs so that energy balance is restored in the short-term and body weight remains stable in the long-term (Druce et al., 2004, Schwartz et al., 2007). Gastroenteric hormones, such as ghrelin, colecystokinin-33 (CCK) and peptide YY3–36 (PYY3–36) are known to play a pivotal role in this process. Indeed, the secretion of the gastric hunger hormone ghrelin increases during fasting and drops after food ingestion contributing to promote and stop eating, respectively (Cummings et al., 2005). Conversely, the production of the satiety-stimulating petides CCK and PYY3–36 rises after a satiating meal prompting the termination of food intake (Murphy and Bloom, 2006).

In order to maintain the drive to eat even when the subject is satiated, such as in hedonic eating, different responses of appetite modulators to the ingestion of food for pleasure can be supposed. In a previous study (Monteleone et al., 2012), we demonstrated that the consumption of food for pleasure was associated with increased peripheral levels of both ghrelin and the endocannabinoid 2-arachidonoyl glycerol (2-AG), and we speculated that these changes could prompt the drive to eat in a condition where there is no need for calorie ingestion. To the best of our knowledge, the role of CCK and PYY3–36 in hedonic eating has been never investigated. Therefore, here we report the peripheral responses of CCK, PYY3–36 and, again, ghrelin to the consumption of food for pleasure, in well-nourished satiated healthy subjects who took part in our previous study (Monteleone et al., 2012).

Section snippets

Subjects and methods

Plasma levels of CCK, PYY3–36 and, again, ghrelin were measured in seven out of the eight subjects, who participated in the previous study (Monteleone et al., 2012). The 7 healthy subjects were 3 men and 4 women, with a body mass index (BMI) < 25 kg/m2 (mean ± SD = 22.07 ± 2.5 kg/m2) and no antecedent of obesity. They were aged 21–33 years (mean ± SD = 25.2 ± 4.1 years) and had normal eating behaviours without food restriction or dieting or bingeing, as ascertained by a clinical interview. All were drug-free,

VAS scores

The hunger VAS scores before hedonic eating did not statistically differ from that before non-hedonic eating; VAS scores were significantly lower than respective scores before breakfast, but not significantly different from scores after breakfast. Similarly, the satiety VAS scores before hedonic eating did not statistically differ from that before non-hedonic eating; both scores were significantly higher than respective scores before breakfast but not significantly different from scores after

Discussion

This study confirms our previous finding that in satiated well-nourished healthy subjects the consumption of food for pleasure was associated with an increased secretion of circulating ghrelin (Monteleone et al., 2012) and shows for the first time that, after the ingestion of the pleasurable food, the production of plasma CCK was reduced while circulating levels of PYY3–36 did not show any significant change.

The observed ghrelin and CCK changes in hedonic eating are opposite to those occurring

Role of the funding sources

Funding for this study was provided by the Second University of Naples (SUN); the SUN had no further role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the paper for publication.

Conflict of interest

The authors declare that they do not have any conflict of interest.

Contributors

Prof. P. Monteleone and Prof. M. Maj designed the study, wrote the protocol, and wrote the manuscript; Dr. P. Scognamiglio and Dr. A.M. Monteleone and D. Perillo performed the clinical tests; Dr. B. Canestrelli performed laboratory assays; all the authors contributed to and approved the final version of the manuscript.

References (25)

  • D.E. Cummings et al.

    A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans

    Diabetes

    (2005)
  • J. De Lartigue et al.

    Cocaine- and amphetamine-regulated tran script: stimulation of expression in rat vagal afferent neurons by cholecystokinin and suppression by ghrelin

    Int. J. Neurosci.

    (2007)
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