Appetite-regulatory hormone responses on the day following a prolonged bout of moderate-intensity exercise
TL;DR: It is indicated that short-term energy deficits induced by exercise initially prompt a compensatory response by chronic but not acute hormonal regulators of appetite and energy balance within this 24h time-frame however there is no conscious recognition of the perturbation to energy balance.
About: This article is published in Physiology & Behavior.The article was published on 2015-03-15 and is currently open access. It has received 27 citations till now. The article focuses on the topics: Appetite.
Summary (3 min read)
Jump to: [Introduction] – [Participants] – [Pre-assessment and Study Familiarisation] – [Main Experimental Trials] – [Food Provision & Test Meals] – [Blood Biochemistry] – [Statistical Analysis] – [Appetite Hormone Responses] – [Appetite Responses] and [Discussion]
Introduction
- The relationship between exercise and appetite regulation has important implications regarding the role of exercise in weight management (33) .
- The body's appetite regulatory system includes several peptides of gastro-intestinal, pancreatic and adipose tissue origin, which communicate acute nutrient status and chronic energy availability to the central nervous system (28) .
- Notably however, these alterations appear to be transient.
- Circulating levels of acylated ghrelin are distinctly suppressed during exercise of moderate intensity or higher (10, 29, 31) .
Participants
- Participants were weight stable (< 2 kg change in body mass in the last three months), non-smokers, free of cardiometabolic disease, had a BMI within the healthy range (18.5 -24.9 kgm 2 ) and were not taking any medications or supplements.
- Participants were recreationally active i.e. typically games players, but were not accustomed to undertaking endurance exercise regularly.
Pre-assessment and Study Familiarisation
- Before main trials, participants attended the laboratory where they were familiarised with the study procedures and underwent necessary pre-assessments.
- Participants completed questionnaires assessing health status and physical activity habits after which measurements of height, weight and waist circumference were taken.
- Participants then completed two treadmill running tests; 1) a progressive 16 min submaximal test to determine the relationship between treadmill running speed and oxygen consumption; 2) a maximum oxygen uptake test ( 2 O V max).
- These tests have been described in depth previously (10) .
Main Experimental Trials
- In subsequent weeks participants completed two main experimental trials (exercise and control) separated by a washout period of at least seven days.
- Each main trial was composed of an intervention phase (day one) and a data collection phase (day two).
- During main trials participants were provided with all of their food which was consumed at set times that were standardised across trials.
- Herein, participants ran on a motorised treadmill (Technogym Excite Med, Cesena, Italy) for 90 min at a speed predicted to elicit 70% of their maximum oxygen uptake.
- After lunch participants went home where they remained until returning to the laboratory the following morning.
Food Provision & Test Meals
- On day one of main trials participants received all of their food pre-packaged from the study team with the food provided being identical in the exercise and control trial.
- The amount of food each participant received was calculated as 1.4x their estimated basal metabolic rate (42) .
- On day one breakfast consisted of white bread and chocolate spread (carbohydrate 64%, fat 25%, protein 11% -20% of daily energy provision).
- Each participant received the exact same meal i.e. the meal was not normalised to participants' daily energy requirements.
- To keep hydrated participants drank 250 mL of water one hour after each test meal (1 h and 5 h).
Blood Biochemistry
- During day two of main trials venous blood samples were collected via a 21G cannula (Venflon, Becton Dickinson, Helsingborg, Sweden) that was kept patent throughout by flushing with isotonic saline (0.9% w/v sodium chloride).
- To preserve the integrity of the acylated ghrelin sample, monovettes for this peptide were pre-treated with a serine protease inhibitor as described previously (10) .
- Samples for total PYY were collected into ice-cooled syringes containing 10µL/mL di-peptidyl peptidase-4 inhibitor (Millipore, Watford, UK) and after mixing were immediately dispensed into EDTA tubes containing aprotinin (Nordic Pharma Ltd, Reading, UK) (500 KIU/mL).
- Plasma was obtained after spinning whole blood samples at 1600 g for 10 min in a refrigerated centrifuge (4 o C) and was stored at -80 o C until analysis.
- Concentrations of plasma acylated ghrelin (SPI BIO, Montigney le Bretonneux, France), total PYY (Millipore, Watford, UK), leptin (R and D Systems Europe Ltd., Abingdon, UK) & insulin (Mercodia, Uppsala, Sweden) were determined using enzyme-linked immunosorbant assay kits.
Statistical Analysis
- Data were analysed using the Statistical Package for the Social Sciences (SPSS) software version 21.0 for Windows.
- Two-way repeated measures ANOVA were used to examine responses over time for appetite regulatory hormones and appetite perceptions.
- Where significant differences were found these were explored using post hoc analysis using the Bonferroni correction for multiple comparisons.
- Statistical significance was accepted at the 5% level.
- The sample size for this investigation was determined using data derived from the authors' previous research which detected compensatory acylated ghrelin responses to food restriction (31) .
Appetite Hormone Responses
- On the morning of day two plasma acylated ghrelin concentrations were no different between the exercise and control trial (P = 0.56) (Figure 2 upper panel).
- Two-way repeated measures ANOVA (trial x time) revealed significant time (P < 0.001) and interaction (P = 0.009) main effects for acylated ghrelin indicating divergent changes over time between trials.
- After correction for multiple comparisons using the Bonferroni method no differences were found at individual time points between trials.
- The plasma leptin AUC showed significantly reduced circulating levels across the entirety of day two (Table 1 ).
- At baseline on day two fasting plasma concentration of insulin were no different between the exercise and control trial (Figure 3 upper panel).
Appetite Responses
- There were no significant differences in fasting appetite perceptions on day two (hunger, fullness, satisfaction and PFC) between the exercise and control trial (all P > 0.05) (Figure 4 ).
- For each appetite perception two-way repeated measures ANOVA (trial x time) revealed a main effect of time (all P < 0.001) representing changes in response to test meals.
Discussion
- Several studies have shown that there are no acute compensatory changes in appetite or appetite regulatory hormones on the day during which an acute bout of exercise is performed (6, 10, 31) .
- Paradoxically, circulating levels of acylated ghrelin were actually lower following a lunch time meal consumed 24 h after the end of exercise.
- A more long term influence of PYY on energy homeostasis has also been suggested by associations that have been found between PYY, substrate oxidation and resting metabolic rate (25, 48) .
- Notably, the consensus arising from previous work, and supported here, are that substantial reductions in circulating leptin occur after exercise when associated with sufficiently high energy expenditure (> 3348 kJ) and following a latency period of ~24-48 h (17, 45, 53) .
- In the present investigation the authors sought to explore this relationship further within a controlled laboratory setting by assessing changes in subjective appetite parameters on the day after exercise.
Did you find this useful? Give us your feedback
Citations
More filters
Journal Article•
TL;DR: The authors showed that post-prandial elevation of PYY3-36 may act through the arcuate nucleus Y2R to inhibit feeding in a gut-hypothalamic pathway.
Abstract: Food intake is regulated by the hypothalamus, including the melanocortin and neuropeptide Y (NPY) systems in the arcuate nucleus. The NPY Y2 receptor (Y2R), a putative inhibitory presynaptic receptor, is highly expressed on NPY neurons in the arcuate nucleus, which is accessible to peripheral hormones. Peptide YY3-36 (PYY3-36), a Y2R agonist, is released from the gastrointestinal tract postprandially in proportion to the calorie content of a meal. Here we show that peripheral injection of PYY3-36 in rats inhibits food intake and reduces weight gain. PYY3-36 also inhibits food intake in mice but not in Y2r-null mice, which suggests that the anorectic effect requires the Y2R. Peripheral administration of PYY3-36 increases c-Fos immunoreactivity in the arcuate nucleus and decreases hypothalamic Npy messenger RNA. Intra-arcuate injection of PYY3-36 inhibits food intake. PYY3-36 also inhibits electrical activity of NPY nerve terminals, thus activating adjacent pro-opiomelanocortin (POMC) neurons. In humans, infusion of normal postprandial concentrations of PYY3-36 significantly decreases appetite and reduces food intake by 33% over 24 h. Thus, postprandial elevation of PYY3-36 may act through the arcuate nucleus Y2R to inhibit feeding in a gut–hypothalamic pathway.
1,960 citations
TL;DR: Blood redistribution during exercise may be important for suppressing ghrelin, while other mechanisms involving cytokine release, changes in plasma glucose and insulin concentrations, SNS activity, and muscle metabolism likely mediate changes in the anorexigenic signals PYY and GLP-1.
131 citations
TL;DR: The balance of evidence suggests that adiposity and sex do not modify appetite or energy intake responses to acute or chronic exercise interventions, but individuals with higher habitual physical activity levels may better adjust energy intake in response to energy balance perturbations.
Abstract: Exercise facilitates weight control, partly through effects on appetite regulation. Single bouts of exercise induce a short-term energy deficit without stimulating compensatory effects on appetite, whilst limited evidence suggests that exercise training may modify subjective and homeostatic mediators of appetite in directions associated with enhanced meal-induced satiety. However, a large variability in responses exists between individuals. This article reviews the evidence relating to how adiposity, sex, and habitual physical activity modulate exercise-induced appetite, energy intake, and appetite-related hormone responses. The balance of evidence suggests that adiposity and sex do not modify appetite or energy intake responses to acute or chronic exercise interventions, but individuals with higher habitual physical activity levels may better adjust energy intake in response to energy balance perturbations. The effect of these individual characteristics and behaviours on appetite-related hormone responses to exercise remains equivocal. These findings support the continued promotion of exercise as a strategy for inducing short-term energy deficits irrespective of adiposity and sex, as well as the ability of exercise to positively influence energy balance over the longer term. Future well-controlled studies are required to further ascertain the potential mediators of appetite responses to exercise.
127 citations
TL;DR: How iron deficiency may interact with each component of the female athlete triad, that is, energy status, reproductive function, and bone health, is described.
Abstract: Despite the severity and prevalence of iron deficiency in exercising women, few published reports have explored how iron deficiency interacts with another prevalent and severe condition in exercising women: the ‘female athlete triad.’ This review aims to describe how iron deficiency may interact with each component of the female athlete triad, that is, energy status, reproductive function, and bone health. The effects of iron deficiency on energy status are discussed in regards to thyroid function, metabolic fuel availability, eating behaviors, and energy expenditure. The interactions between iron deficiency and reproductive function are explored by discussing the potentially impaired fertility and hyperprolactinemia due to iron deficiency and the alterations in iron metabolism due to menstrual blood loss and estrogen exposure. The interaction of iron deficiency with bone health may occur via dysregulation of the growth hormone/insulin-like growth factor-1 axis, hypoxia, and hypothyroidism. Based on these discussions, several future directions for research are presented.
64 citations
Cites background from "Appetite-regulatory hormone respons..."
...On the other hand, an energy deficiency achieved via increased exercise energy expenditure suppresses ghrelin and increases PYY, GLP-1, and PP serum concentrations in the hours following exercise [98–100] and even suppresses serum ghrelin concentrations the day after exercise [101]....
[...]
TL;DR: The concept of dynamic energy balance is reviewed, including two mathematical models developed to improve weight-loss predictions based on changes in diet and exercise and these models are now available on the Internet.
Abstract: Weight management for athletes and active individuals is unique because of their high daily energy expenditure; thus, the emphasis is usually placed on changing the diet side of the energy balance equation. When dieting for weight loss, active individuals also want to preserve lean tissue, which means that energy restriction cannot be too severe or lean tissue is lost. First, this brief review addresses the issues of weight management in athletes and active individuals and factors to consider when determining a weight-loss goal. Second, the concept of dynamic energy balance is reviewed, including two mathematical models developed to improve weight-loss predictions based on changes in diet and exercise. These models are now available on the Internet. Finally, dietary strategies for weight loss/maintenance that can be successfully used with active individuals are given. Emphasis is placed on teaching the benefits of consuming a low-ED diet (e.g., high-fiber, high-water, low-fat foods), which allows for the consumption of a greater volume of food to increase satiety while reducing energy intake. Health professionals and sport dietitians need to understand dynamic energy balance and be prepared with effective and evidence-based dietary approaches to help athletes and active individuals achieve their body-weight goals.
62 citations
References
More filters
TL;DR: The correlation of the model's estimates with patient data accords with the hypothesis that basal glucose and insulin interactions are largely determined by a simple feed back loop.
Abstract: The steady-state basal plasma glucose and insulin concentrations are determined by their interaction in a feedback loop. A computer-solved model has been used to predict the homeostatic concentrations which arise from varying degrees beta-cell deficiency and insulin resistance. Comparison of a patient's fasting values with the model's predictions allows a quantitative assessment of the contributions of insulin resistance and deficient beta-cell function to the fasting hyperglycaemia (homeostasis model assessment, HOMA). The accuracy and precision of the estimate have been determined by comparison with independent measures of insulin resistance and beta-cell function using hyperglycaemic and euglycaemic clamps and an intravenous glucose tolerance test. The estimate of insulin resistance obtained by homeostasis model assessment correlated with estimates obtained by use of the euglycaemic clamp (Rs = 0.88, p less than 0.0001), the fasting insulin concentration (Rs = 0.81, p less than 0.0001), and the hyperglycaemic clamp, (Rs = 0.69, p less than 0.01). There was no correlation with any aspect of insulin-receptor binding. The estimate of deficient beta-cell function obtained by homeostasis model assessment correlated with that derived using the hyperglycaemic clamp (Rs = 0.61, p less than 0.01) and with the estimate from the intravenous glucose tolerance test (Rs = 0.64, p less than 0.05). The low precision of the estimates from the model (coefficients of variation: 31% for insulin resistance and 32% for beta-cell deficit) limits its use, but the correlation of the model's estimates with patient data accords with the hypothesis that basal glucose and insulin interactions are largely determined by a simple feed back loop.
29,217 citations
TL;DR: A model is described that delineates the roles of individual hormonal and neuropeptide signalling pathways in the control of food intake and the means by which obesity can arise from inherited or acquired defects in their function.
Abstract: New information regarding neuronal circuits that control food intake and their hormonal regulation has extended our understanding of energy homeostasis, the process whereby energy intake is matched to energy expenditure over time. The profound obesity that results in rodents (and in the rare human case as well) from mutation of key signalling molecules involved in this regulatory system highlights its importance to human health. Although each new signalling pathway discovered in the hypothalamus is a potential target for drug development in the treatment of obesity, the growing number of such signalling molecules indicates that food intake is controlled by a highly complex process. To better understand how energy homeostasis can be achieved, we describe a model that delineates the roles of individual hormonal and neuropeptide signalling pathways in the control of food intake and the means by which obesity can arise from inherited or acquired defects in their function.
6,178 citations
TL;DR: Weight loss due to food restriction was associated with a decrease in plasma leptin in samples from mice and obese humans, suggesting differences in its secretion rate from fat.
Abstract: Leptin, the gene product of the obese gene, may play an important role in regulating body weight by signalling the size of the adipose tissue mass. Plasma leptin was found to be highly correlated with body mass index (BMI) in rodents and in 87 lean and obese humans. In humans, there was variability in plasma leptin at each BMI suggesting that there are differences in its secretion rate from fat. Weight loss due to food restriction was associated with a decrease in plasma leptin in samples from mice and obese humans.
3,763 citations
"Appetite-regulatory hormone respons..." refers background in this paper
...Leptin and insulin act as chronic mediators of energy balance, with circulating concentrations being present in proportion to stored energy within adipose tissue [5]....
[...]
TL;DR: Changes in PV calculated from the increase in plasma protein concentration averaged 7.5(z compared with 12.2 y0 calculated from changes in Hb and Hct, the difference could be accounted for by a loss of 6v10 plasma protein from the circulation.
Abstract: DILL, D. B., AND I>. L. &STILL. Calculation of pcrccntage changes in volumes of blood, plasma, and red cells in dehydration. J. Appl. Physiol. 37(2): 247-248. 1974.-Observations on hematocrit (Hct) and hemoglobin (Hb) were Inade in six men before and after running long enough to cause a 4y0 decrease in body weight. Subscripts B and A were used to denote before dehydration and after dehydration, respectively. Relations were derived between BVn, BVA, Hbn, HbA, Hctg, and HctA with which one can calculate the percentage decreases in BV, CV, and PV, as well as the concentration of hemoglobin in red cells, g. 100 ml-l (MCHC). When subjects reach the same level of dehydration the water loss from the various body compartments may vary reflecting difference in salt losses in sweat. Changes in PV calculated from the increase in plasma protein concentration averaged 7.5(z compared with 12.2 y0 calculated from changes in Hb and Hct. The difference could be accounted for by a loss of 6v10 plasma protein from the circulation.
3,405 citations
"Appetite-regulatory hormone respons..." refers methods in this paper
...At baseline and 4 h measurements of haematocrit and haemoglobin were taken to estimate changes in plasma volume using the method described by Dill & Costill [27]....
[...]
TL;DR: The hypothesis that ghrelin plays a physiological role in meal initiation in humans is supported by the clear preprandials rise and postprandial fall in plasma ghrelIn levels.
Abstract: The recently discovered orexigenic peptide ghrelin is produced primarily by the stomach and circulates in blood at levels that increase during prolonged fasting in rats. When administered to rodents at supraphysiological doses, ghrelin activates hypothalamic neuropeptide Y/agouti gene-related protein neurons and increases food intake and body weight. These findings suggest that ghrelin may participate in meal initiation. As a first step to investigate this hypothesis, we sought to determine whether circulating ghrelin levels are elevated before the consumption of individual meals in humans. Ghrelin, insulin, and leptin were measured by radioimmunoassay in plasma samples drawn 38 times throughout a 24-h period in 10 healthy subjects provided meals on a fixed schedule. Plasma ghrelin levels increased nearly twofold immediately before each meal and fell to trough levels within 1 h after eating, a pattern reciprocal to that of insulin. Intermeal ghrelin levels displayed a diurnal rhythm that was exactly in phase with that of leptin, with both hormones rising throughout the day to a zenith at 0100, then falling overnight to a nadir at 0900. Ghrelin levels sampled during the troughs before and after breakfast correlated strongly with 24-h integrated area under the curve values (r = 0.873 and 0.954, respectively), suggesting that these convenient, single measurements might serve as surrogates for 24-h profiles to estimate overall ghrelin levels. Circulating ghrelin also correlated positively with age (r = 0.701). The clear preprandial rise and postprandial fall in plasma ghrelin levels support the hypothesis that ghrelin plays a physiological role in meal initiation in humans.
2,869 citations