Effects of endurance running and dietary fat on circulating ghrelin and peptide YY.

Author:Russel, Ryan R.
Position::Research article - Clinical report
 
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Introduction

It is well documented that intense (but not necessarily moderate or light) exercise may induce a transient suppression of hunger that has been reported in both humans (Broom et al., 2007; Burns et al., 2007; King and Blundell, 1995; King et al., 1994; Kissileff et al., 1990; Westerterp-Plantenga et al., 1997) and experimental animals (Routtenberg and Kuznesof, 1967). This short-term suppression of hunger, termed exercise-induced anorexia (King et al., 1997), however, is not reported in all studies (Imbeault et al., 1997; Pomerleau et al., 2004) and may be influenced by the mode (King et al., 1997), duration (King et al., 1994; Westerterp-Plantenga et al., 1997), and intensity (King et al., 1994; Thompson et al., 1988) of the exercise, and the body weight/adiposity of the exerciser (Kissileff et al., 1990). Several studies, for example, have documented increased hunger following 75-minutes of continuous swimming [(Verger et al., 1992)ref in (King et al., 1997)] and 2 hours of sports-specific athletic activity (Verger et al., 1994). This is in agreement with the anecdotal reports from athletes who commonly report that intense running and sports related training induces transient anorexia while swimming and cycling promotes appetite stimulation (Larson-Meyer, unpublished observations). While it is not well understood whether exercise-associated alterations in hunger (or appetite) impacts long-term energy balance (King et al., 1997), exercise-induced anorexia may potentially influence exercise recovery by delaying the onset of eating (King and Blundell, 1995; King et al., 1997) or reducing energy and nutrient intake (Kissileff et al., 1990; Westerterp-Plantenga et al., 1997) in the 30-60 minutes following exercise. Carbohydrate and protein intake in the immediate post-exercise period is needed for rapid replacement of muscle and liver glycogen and the building and repair of muscle tissue (Rodriguez et al., 2009).

Little is known about the specific mechanisms responsible for exercise-associated changes in appetite and hunger. While investigators have hypothesized that modulation of appetite may be related to elevations in body temperature (Andersson and Larsson, 1961) or blood lactate concentrations (Baile et al., 1970; Racotta and Russek, 1977), such changes alone are not likely to be mechanistically responsible for exercise-induced alterations in appetite. The recent discovery of several new gut peptides involved in appetite regulation and energy homeostasis, however, lends promising mechanisms which may help explain both training and individual (between-subject) differences in hunger, appetite and food intake following different modes, intensities and durations of acute exercise. In particular, the gut peptides ghrelin and peptide YY (PYY) are of interest because they appear to regulate hunger and food intake for up to 24-hours (Wren et al., 2001) and are not specifically controlled by body fat stores, as are the adipokines leptin and adoponectin (Cummings and Overduin, 2007). Ghrelin is a 28 amino acid gastric hormone that is released from the enteroendocrine cells of the stomach and large intestine that stimulates appetite (Cummings and Overduin, 2007; Cummings et al., 2002) and promotes gastric motility (Cummings and Overduin, 2007) whereas peptide YY 3-36 (PYY) is a 36 amino acid peptide secreted from L-cells in the intestinal mucosa that suppresses appetite and gastric emptying (Adrian et al., 1985; Cummings and Overduin, 2007; le Roux and Bloom, 2005). Ghrelin is at its highest concentration during fasting and decreases postprandially (Cummings et al., 2002), whereas PYY is lowest during fasting and increases postprandially in proportion to energy intake (Adrian et al., 1985; le Roux and Bloom, 2005). Ghrelin and PYY remain altered for 1-2 hours posstprandial and then gradually rise and fall, progressively, back toward fasting concentrations. Ghrelin has been shown to be more effectively suppressed postprandial by a high-carbohydrate (as opposed to a high-fat or high-protein) meal (Erdmann et al., 2003; Monteleone et al., 2003); whereas PYY may be more effectively elevated after a fat- compared to a carbohydrate-rich meal (Adrian et al., 1985). It is not known, however, how short- or long-term alterations in macronutrients (i.e., a long-term high-carbohydrate vs. high-fat diet) impact these gut peptides. In addition, studies have suggested that ghrelin (Broom et al., 2007; Christ et al., 2006; Ghanbari-Niaki, 2006; Kraemer et al., 2004b) and PYY (Martins et al., 2007) may be influenced by a single-bout of exercise but results are not conclusive (Burns et al., 2007; Erdmann et al., 2007; Kraemer et al., 2004a; Martins et al., 2007; Schmidt et al., 2004).

The purpose of the current study was to determine: a) whether fasting ghrelin and PYY concentrations are altered by three days of a low-fat, high-carbohydrate (10% fat, 75% carbohydrate) or moderate-fat, moderate-carbohydrate (35% fat, 50% carbohydrate) diet in endurance-trained runners and; b) whether concentrations of these peptides are affected by a bout of intense endurance exercise which is likely to promote exercise-induced anorexia. We hypothesized that: a) ghrelin and PYY would be lower during fasting and non-fasting while on the low-fat, high-carbohydrate diet compared to the moderate-fat, moderate-carbohydrate diet; 2) and that ghrelin would be lowered and PYY elevated following strenuous endurance running, thereby providing a potential mechanism for exercise associated anorexia. The results of this study will provide valuable data to enhance our understanding of the influence of diet and exercise on ghrelin and PYY concentrations and the possible causes for exercise-induced alterations of appetite.

Methods

The subjects were 21 healthy endurance trained distance runners or triathletes between the ages of 18-44 for men (n = 11) and 18-54 for women (n = 10) who were recruited for a study assessing the effect of diet on intramyocellular lipid stores (Larson-Meyer et al., 2008). To qualify, participants had to be in good general health (as determined by a study physician), be performing regular endurance running (40 km*[wk.sup.-1], have performed at least two training runs 2 hours within the previous three months, and have a maximal aerobic fitness (V[O.sub.2]max) [greater than or equal to]50 ml*[kg.sup.-1]*[min.sup.-1] for women and [greater than or equal to]55 ml*[kg.sup.-1]*[min.sup.-1] for men. In addition, female participants had to have regularly occurring menstrual cycles (Larson-Meyer et al., 2008). Subjects were excluded if they smoked, demonstrated signs of a full or partial syndrome eating disorder, alcoholism or other substance abuse problems, were using prescription or over-the-counter medications or supplements (other than oral contraceptives) that could influence metabolism, or could not agree to consume all foods/beverages provided on the experimental diets. The study was approved by the Institutional Review Board of the Pennington Biomedical Research Center (PBRC). Volunteers were fully informed about the possible risks of all procedures before providing written informed consent.

Baseline testing

Approximately two to three weeks before initiation of the experimental protocol, V[O.sub.2]max was determined on a motor driven treadmill (MedTrack ST65, Quinton Industries, Inc, Bothell, WA) using a protocol specific for endurance-trained runners (Larson-Meyer et al., 2002; 2008; Russell et al., 2004), and body composition was assessed by dual-energy x-ray absorptiometry (DXA, Hologic QDR4500A). Following a 5-min warm-up, "workload" was increased by either speed (starting at the subject's typical warm-up speed and increasing by 0.5 MPH (13.4 m/min)) or grade (starting at 0 degrees and increasing by 2.5%) every min until exhaustion. Oxygen consumption (V[O.sub.2]) and carbon dioxide production (V[O.sub.2]) were measured using a metabolic cart (V-Max 29, SensorMedics, Yorba Linda, CA), and heart rate was monitored using a portable heart rate monitor (Polar S610, Polar Beat, Port Washington, NY). The highest V[O.sub.2], respiratory exchange ratio (RER) and heart rate achieved over a 20-s period within the last 2-min of exercise were recorded as the maximum values. Subjects had to achieve two out of three of the following criteria: 1) a leveling or plateau of V[O.sub.2] (defined as an increase of V[O.sub.2] of 1.10, and 3) maximum heart rate within 10 beats of age-predicted maximum. Following a 30-minute rest, subjects also performed a practice endurance performance test that consisted of a 90-min submaximal run at 65%V[O.sub.2]max (preload) followed by a time trial. The practice performance run was performed to familiarize the subjects with the treadmill and the endurance performance test.

Experimental protocol

The details of this randomly assigned cross-over experiment have been published elsewhere (D. E. Larson-Meyer et al., 2008). The investigators were blinded to the diet treatment (except metabolic kitchen personnel); whereas the participants were masked (i.e., they were not told of their diet assignment but may have been able to identify certain fat-altered foods). As shown in Figure 1, participants completed two separate test weeks (eight days each) that were spaced approximately 3-4 wk apart in men and one menstrual cycle (3-5 wk) in women. The test weeks consisted of an eight day session which included a baseline weight maintenance diet for the first 3 days (15% protein, 25% fat, 60% carbohydrate), followed by four days of an isoenergetic low-fat (10%...

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