β-Glucan-enriched bread reduces energy intake and modifies plasma ghrelin and peptide YY concentrations in the short term

Abstract

Dietary fibre consumption may help to control appetite and to reduce calorie intake. Underlying molecular mechanisms were not fully investigated. The aim of this study was to evaluate the effect of barley β-glucans on short-term appetite and on satiety-related hormones in healthy subjects. Fourteen volunteers were selected and randomly assigned to have isocaloric breakfasts including a 3% β-glucan-enriched bread (βGB) or a control bread (CB). Post-breakfast individual self-records of appetite ratings and measure of calorie intake at an ad libitum lunch as well as measure of blood glucose, insulin, ghrelin and PYY concentrations, were performed. βGB determined a significant higher reduction of hunger and increase of fullness and satiety than CB. Accordingly, a 19% reduction of energy intake at lunch subsequent to βGB consumption compared to CB, was recorded. A 23% lower AUC_60–180 of plasma ghrelin and a 16% higher total AUC of PYY response after βGB than CB consumption, independent from insulin response, was found. Glucose response was also blunted by βGB vs CB. Barley β-glucans were able to control appetite in the short term by modulating sensations and reducing energy intake. Data suggested for the first time that satiety effect of β-glucans are mediated by ghrelin and PYY.

Introduction

Social, psychological and neuroendocrine factors control food intake by a very complex physiologic system that modulates hunger and satiety trough pre-absorptive and post-absorptive signals (Blundell, 1999, Gerstein et al., 2004, Murphy and Bloom, 2006, Porrini et al., 1995, Rolls et al., 1998, Stubbs et al., 2000). The characteristics of food such as palatability, energy density, volume, form and nutrient composition as well as hormones secreted by digestive tract play a fundamental role in these fine mechanisms (Barkeling et al., 1995, De Graaf et al., 2004, De Graaf et al., 1992, Stubbs et al., 2000).

Among hormones, ghrelin plays a role in the satiety cascade and it has been proposed as a valid biomarker of satiety both in the short and long term (Cummings et al., 2002a, Cummings et al., 2002b, Wren et al., 2001). It is a peripheral hormone synthesized in the fundus of the stomach and also in other parts of the gastrointestinal tract (Ariyasu et al., 2001, Kamegai et al., 2000). In normal-weight subjects plasma ghrelin concentrations decreased after oral and intravenous administration of glucose, but the intake of an equivalent volume of water did not influence ghrelin concentrations, suggesting that ghrelin secretion is not affected by stomach expansion (Shiiya et al., 2002). Ghrelin has a direct effect on appetite as its concentration was correlated with appetite ratings (De Graaf et al., 2004).

Peptide YY (PYY) has opposite effects to ghrelin. It is released primarily from the distal gastrointestinal tract (colon) and acts as an agonist (stimulator) on the Y2 receptor in the hypothalamus. This receptor inhibits the release of neuropeptide YY, which is a potent appetite stimulator, thus PYY acts as suppressor of food intake (Batterham et al., 2002, Batterham et al., 2003). Although it has been demonstrated that dietary nutrients, such as carbohydrates, dietary fibre, fats and proteins, may influence PYY response in the short term, the role of PYY as biomarker of satiety needs to be further confirmed (De Graaf et al., 2004, Karhunen et al., 2008).

Among dietary constituents that can modulate appetite and food intake, dietary fibre had documented effects on increasing satiety, thus playing a potential role in the control of energy balance (Howarth, Saltzman, & Roberts, 2001). The evidence about the satiety efficacy of different types of dietary fibre, are not conclusive: results varied with the type of dietary fibre and with administration protocols (i.e. dietary fibre-rich foods vs pure supplements) (Slavin & Green, 2007). A recent review dealing with dietary fibre and satiety (Slavin & Green, 2007) concluded that in short-term studies an improvement of appetite control and a reduction of energy intake at the meal following dietary fibre consumption was directly correlated to the amount of fibre consumed and to its viscosity.

Among viscous dietary fibre, β-(1,3)(1,4) glucans (hereinafter named β-glucans) included into foods by addition of oat or barley as well as by concentrated extracts, were initially studied for their immunomodulatory activity (Estrada et al., 1997) and more recently for their ability to modify CVD risk through modulation of blood lipid profile (Keenan et al., 2007).

Only few clinical studies investigated the effect of barley or oat β-glucans on appetite and energy intake and they were carried out on overweight and obese subjects. Unfortunately, in these studies appetite and calorie intake were among secondary objectives and inconsistent results reporting either positive (Bourdon et al., 1999, Rytter et al., 1996) or negative (Kaplan and Greenwood, 2002, Saltzman et al., 2001) effects were obtained.

In this study the satiety effect of a bread containing 3% barley β-glucans was investigated in healthy subjects by assessing appetite ratings and energy intake and measuring peripheral glucose and hormone concentrations.