According to a new study, published in the Journal of Clinical Endocrinology and Metabolism, health scientists at the Universities of Bath and Birmingham found that by changing the timing of when you eat and exercise, people can better control their blood sugar levels.
The six-week study, which involved thirty men classified as obese or overweight and compared results from two intervention groups (who ate breakfast before / after exercise) and a control group (who made no lifestyle changes), found that people who performed exercise before breakfast burned double the amount of fat than the group who exercised after breakfast.
They found that increased fat use is mainly due to lower insulin levels during exercise when people have fasted overnight, which means that they can use more of the fat from their fat tissue and the fat within their muscles as a fuel.
To test proof-of-principle the initial study involved only men, but future studies will look to translate these findings for different groups including women.
Whilst this did not lead to any differences for weight loss over six weeks, it did have ‘profound and positive’ effects on their health because their bodies were better able to respond to insulin, keeping blood sugar levels under control and potentially lowering the risk of diabetes and heart disease.
Building on emerging evidence that the timing of meals in relation to exercise can shift how effective exercise is, the team behind this study wanted to focus on the impact on the fat stores in muscles for individuals who either worked out before or after eating and the effect this had on insulin response to feeding.
Dr. Javier Gonzalez of the Department for Health at the University of Bath explained: “Our results suggest that changing the timing of when you eat in relation to when you exercise can bring about profound and positive changes to your overall health.
“We found that the men in the study who exercised before breakfast burned double the amount of fat than the group who exercised after.
Importantly, whilst this didn’t have any effect on weight loss, it did dramatically improve their overall health.
“The group who exercised before breakfast increased their ability to respond to insulin, which is all the more remarkable given that both exercise groups lost a similar amount of weight and both gained a similar amount of fitness.
The only difference was the timing of the food intake.”
Over the six-week trial, the scientists found that the muscles from the group who exercised before breakfast were more responsive to insulin compared to the group who exercised after breakfast, in spite of identical training sessions and matched food intake.
The muscles from those who exercised before breakfast also showed greater increases in key proteins, specifically those involved in transporting glucose from the bloodstream to the muscles.
For the insulin response to feeding after the 6-week study, remarkably, the group who exercised after breakfast were in fact no better than the control group.
Co-author Dr. Gareth Wallis of the University of Birmingham added: “This work suggests that performing exercise in the overnight-fasted state can increase the health benefits of exercise for individuals, without changing the intensity, duration or perception of their effort. We now need to explore the longer-term effects of this type of exercise and whether women benefit in the same way as men.”
Obesity is an escalating global epidemic, and is a consequence of a chronic positive energy imbalance.
In addition to reducing calorie intake, regular exercise is a commonly proposed strategy for facilitating weight loss or weight maintenance (1).
Exercise increases energy expenditure and thus alters energy balance, thereby potentially favoring the conditions for reductions in body and fat mass. Despite this, exercise training interventions often report smaller than expected fat and body mass losses (2, 3).
This modest response can be explained by compensation of energy balance behaviors (either by the activity stimulating energy intake, or decreasing physical activity outside of the prescribed exercise, or a combination of these factors), and this can reduce the energy deficit created by the energy expended through exercise (4).
A similar example of this compensation is that breakfast omission at rest (i.e., reduced energy intake) decreases morning nonexercise physical activity in lean and obese humans (5, 6).
In particular, altering carbohydrate balance may have implications for subsequent energy balance (7). Endogenous carbohydrate stores (liver and muscle glycogen) have a smaller capacity than lipid stores [<3000 kcal in a lean 75-kg male compared with >100,000 kcal for lipids (8, 9)].
Due to this limited storage capacity, the glycogenostatic theory (7) proposes that endogenous carbohydrate stores are closely regulated, and because of this, glycogen depletion may increasingly stimulate compensatory energy intake in order to favor the replenishment of these stores
. For example, in humans there is some (albeit limited) evidence that individuals who display higher rates of carbohydrate utilization when exercising are more likely to compensate with a higher postexercise energy intake (8, 10, 11).
Although short-term (1–3 d) alterations in glycogen availability with exercise or diet do not always result in a measurable compensation in energy intake (8), mice overexpressing hepatic protein targeted at glycogen (which increases liver glycogen concentrations) also display reduced energy intake and increased energy expenditure (12).
If carbohydrate metabolism is indeed a driver of subsequent energy intake, any strategies that attenuate carbohydrate use during exercise may help protect against compensation through postexercise energy intake (thereby reducing any erosion of the exercise-induced energy deficit).
One strategy that reduces the rate of whole-body carbohydrate utilization during exercise is pre-exercise fasting (i.e. breakfast omission) (13).
Furthermore, because breakfast omission under resting conditions does not result in energy intake compensation at lunch (14, 15), any potential protection against a subsequent higher energy intake (by a lower carbohydrate utilization during exercise when fasting) is unlikely to be compromised due to the lower pre-exercise food intake (i.e., with the omission of breakfast).
If moderate-intensity (55% VO2 peak) endurance-type exercise is performed in the overnight fasting state, whole-body carbohydrate utilization is lower (and fat utilization is higher) than with exercise after breakfast (13).
Interestingly, humans do not fully compensate with energy intake at a subsequent meal if breakfast is omitted before exercise (15, 16), which extends observations made about breakfast consumption during resting conditions (5).
These findings are consistent with a role for carbohydrate balance in the regulation of energy balance. However, an objective assessment of daily energy balance (when energy intake and energy expenditure are assessed in a free-living setting) after exercise with prior breakfast consumption compared with omission has never been conducted.
This limitation is especially important in light of findings that the omission of breakfast at rest decreases light intensity (i.e., non-exercise) physical activity energy expenditure (5, 6). Whether the carbohydrate status (content or rate of utilization) of a specific tissue (liver or muscle glycogen) is a more potent regulator of postexercise energy balance also remains unknown. Indeed, no study has specifically assessed a relationship between muscle or liver carbohydrate utilization and postexercise energy balance in humans. Investigating this response would provide mechanistic insights into the regulation of postexercise energy balance, and this information could then be applied to refine exercise and nutritional strategies (e.g., pre-exercise fasting to lower liver glycogen concentrations compared with exercise to deplete muscle glycogen).
Therefore, the main aim of this experiment was to investigate the role of carbohydrate availability during exercise on net energy balance over 24 h. In addition, the application of glucose tracer methods (to assess hepatic glucose output and utilization) combined with indirect calorimetry was implemented to address a secondary aim of exploring the tissue-specific regulation of energy balance.
Discussion
This is the first study to assess the effect of pre-exercise feeding compared with fasting on all components of energy balance over 24 h, with inclusion of both within-lab and free-living periods. We showed that breakfast omission before exercise (FE) is not fully compensated for with postexercise energy intake, and not compensated for at all with subsequent free-living energy expenditure, creating a more negative daily energy balance compared with breakfast consumption prior to exercise (BE).
Our results also demonstrate that plasma glucose utilization during FE demonstrated a stronger relationship with energy intake compensation than muscle glycogen utilization, whole-body lipid utilization, or exercise energy expenditure.
Plasma glucose utilization was also the only carbohydrate source to demonstrate a positive relationship with energy intake compensation. Because plasma glucose during exercise when fasting is primarily derived from hepatic sources, this result supports a potential role for liver carbohydrate status in the regulation of postexercise energy balance. These data offer new insights into responses to feeding and exercise that are readily applicable to typical daily living (29, 30).
We showed that the energy deficit created by exercise was not compensated for through a higher energy intake at an ad libitum lunch in an exercise compared with a rest trial (BE compared with BR), but was partially compensated for with a higher energy intake later in the day (in a free-living setting).
In contrast, breakfast omission before exercise (FE) was partially compensated for at lunch, but not further compensated for later in the day.
These findings suggest that the compensation for the energy deficits created by exercise and pre-exercise breakfast omission likely occur over different time periods. The energy intake responses we report with pre-exercise breakfast omission are in line with previous observations that when healthy men perform 60 min of running after breakfast, their evening and 24-h energy intakes are higher than if they exercised before breakfast (16). As fasting prior to exercise reduces carbohydrate utilization during exercise (13), these
results are consistent with a theory that the status of endogenous carbohydrate stores (i.e., liver and muscle glycogen) may play a role in energy balance regulation (7).
Further evidence supporting the role of carbohydrate metabolism in regulating energy balance comes from our current, and prior (15), observations that the more negative within-lab energy balance in the FE trial was attributable to a negative fat balance, because carbohydrate balance was similar to that observed in the BE trial.
The ability to fully apply these energy intake findings to daily living is, however, incomplete without an assessment of free-living energy expenditure.
Here, we also demonstrate that pre-exercise breakfast omission is not fully compensated for via nonexercise physical activity energy expenditure when this is based on objective measures of physical activity in a free-living environment.
Thus, we provided a more complete picture of energy balance after breakfast compared with fasting before exercise. Indeed, the physical activity monitor we used has been validated in laboratory and free-living settings (including against doubly-labeled water) (25, 31, 32).
Overall, our results show the following:
1) even with the inclusion of a free-living component, fasting prior to exercise creates a more negative daily energy balance compared with when a pre-exercise breakfast is consumed; and
2) whole-body carbohydrate balance may contribute to energy balance regulation (at least in the postexercise period).
Previously, it was unclear if a specific carbohydrate store was a primary regulator of postexercise energy balance. Here, we show that plasma glucose disposal rates and plasma glucose appearance rates during exercise in FE (which primarily represents the mobilization and utilization of glucose from hepatically derived sources, because no carbohydrate was ingested before or during exercise in the FE trial) were the only carbohydrate-related outcomes (i.e., not due to muscle glycogen utilization) to demonstrate a positive relation with energy intake compensation.
This is the first evidence of a link between tissue-specific carbohydrate utilization during exercise and energy balance in humans. In our fasting exercise trial, participants with higher rates of plasma glucose disposal consumed more energy at lunch than during their rest trial.
This finding that a more rapid utilization of plasma glucose during exercise in FE (and a likely higher rate of utilization of carbohydrate from hepatic sources) may increase postexercise energy intake is consistent with research showing that a higher liver glycogen content in mice is associated with a lower energy intake and a lower body and fat mass (33).
That result suggests that the liver glycogen content may be a regulator of energy balance, and is consistent with the correlation we report because higher liver glucose utilization rates would be expected to deplete the liver glycogen content during exercise to a greater extent.
Future studies should now confirm this relationship through the use of a direct measure of net hepatic glycogen utilization, such as 13C magnetic resonance spectroscopy.
A possible link between the liver carbohydrate status and postexercise energy intake regulation may be explained by concentrations of circulating hormones. For example, exercise increases liver FGF-21 secretion (34), which may influence subsequent energy intake (35).
It has also been suggested that blood leptin concentrations may help to regulate carbohydrate metabolism and energy balance during periods of fasting (36). During rest, higher plasma leptin concentrations after a lunch meal have been previously observed in a breakfast compared with morning fasting trial (14).
This observation may be accounted for by a slow release of leptin in response to breakfast, a diurnal shift in leptin release with morning fasting, or a combination of both these effects (14). However, although we have confirmed that exercise increases plasma FGF-21 concentrations, we showed that neither plasma FGF-21 nor plasma leptin concentrations were altered by pre-exercise breakfast omission (FE) compared with pre-exercise breakfast consumption (BE).
The postprandial leptin response we observed after exercise was, however, similar to the response observed with breakfast omission at rest. Alternatively, a higher rate of liver carbohydrate utilization may influence energy balance via a liver-brain neural network (the hepatic branch of the vagus nerve) to the central nervous system, as has been demonstrated in rodents (12).
Although future research needs to further investigate any mechanisms linking overall and liver carbohydrate metabolism to energy balance in humans, the evidence presented here is the first to demonstrate that plasma glucose utilization during fasted exercise (and thus carbohydrate use from hepatic sources) is positively correlated with postexercise energy intake in humans.
Our results are most applicable to young, physically active men. However, as untrained individuals show increased liver glucose utilization during endurance-type exercise (compared to trained individuals) (37), it is possible that these people may be even more susceptible to a higher postexercise energy intake, which would (in theory) make it more difficult for these individuals to lose weight through exercise.
Although the regulatory mechanisms remain unclear, this study provides novel insights into the regulation of all behavioral components of daily energy balance after pre-exercise breakfast omission (FE) compared with breakfast consumption (BE).
Our findings must, however, be interpreted in light of the study design. Firstly, although the protocol included a free-living period, participants were constrained to a laboratory environment during the morning, and it is possible that behaviors that alter energy balance may have changed in a free-living environment during this time after fasting compared with fed exercise.
This restriction of physical activity likely contributed to the positive 24-h energy balance observed in the BR trial. In addition, participants also had a limited choice of food during the study and it is possible that energy intake may have differed under more free-living conditions.
Our results also only relate to breakfast omission and not altered breakfast timing. Despite this, under energy-balanced conditions (with the consumption of breakfast either pre- or postexercise) energy intake at an ad libitum lunch does not differ, despite alterations in substrate balance (38).
In light of that result and our current findings, future research should now investigate all components of energy balance with altered timing of breakfast and in free-living settings (rather than breakfast omission and the time-restricted feeding with fasting prior to exercise). Investigating energy balance responses to regular exercise in the fasting compared with fed state and with overweight populations should be another focus for future work.
This would provide insights as to whether the 24-h energy balance responses we report here translate into enduring changes in body mass or composition with repeated bouts of exercise in the fasting compared with the fed state.
Finally, although this study lacks characterization of other gut hormones that have been associated with energy intake, it has been shown that acylated ghrelin and glucagon-like peptide 1 responses to exercise in the fasting compared with fed states do not differ to any meaningful degree (15, 39, 40). Plasma insulin concentrations during and after exercise were also not altered to any great extent by pre-exercise feeding in our participants (17).
To conclude, pre-exercise breakfast omission is not fully compensated for by energy intake, and is not compensated for at all by nonexercise energy expenditure postexercise, creating a more negative 24-h energy balance compared with when breakfast is consumed before exercise.
We also show that postexercise energy intake compensation is positively correlated with plasma glucose utilization when exercise is performed when fasting, highlighting a possible role for liver carbohydrate status in energy-balance regulation. These results have important implications for the regulation of postexercise energy balance, and suggest that for healthy young men a short-term energy deficit may be more easily attained if breakfast is omitted before exercise.
More information:Journal of Clinical Endocrinology and Metabolism (2019). DOI: 10.1210/clinem/dgz104
Journal information: Journal of Clinical Endocrinology and Metabolism
Provided by University of Bath
