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Table of Contents
Vol. 62, No. 1, 2013
Issue release date: January 2013
Section title: Review Article
Free Access
Ann Nutr Metab 2013;62:14–25
(DOI:10.1159/000343788)

Exercising for Metabolic Control: Is Timing Important?

Haxhi J. · Scotto di Palumbo A. · Sacchetti M.
Department of Human Movement and Sport Sciences, University of Rome ‘Foro Italico’, Rome, Italy
email Corresponding Author

Massimo Sacchetti, PhD

Department of Human Movement and Sport Sciences

‘Foro Italico’ University of Rome

Piazza Lauro De Bosis 15, IT–00135 Rome (Italy)

E-Mail massimo.sacchetti@uniroma4.it


Abstract

Atherosclerosis-related cardiovascular disease and diabetes mellitus are leading causes of mortality in the world and both disorders are closely related to the postprandial phenomena. Regular exercise is being strongly advocated as a precious tool in easing the global burden of chronic disease. Although exercise intensity, duration and frequency are well established in current guidelines for healthy and diabetic individuals, there is still no consensus on the optimal timing of exercise in relation to the last meal. The present paper reviews the existing literature on the ‘when?’ of aerobic exercise for metabolic control in healthy and diabetic individuals. Effective control of postprandial phenomena might prove to be a useful tool in the prevention of chronic disease. Exercise appears to influence glycemic and triglyceridemic responses differently depending on the meal composition and time lapse from meals. In healthy individuals, fasted-state exercise favors postprandial triglyceridemic control and the insulin sensitivity related to it. However, there is a lack of data on this matter in diabetic patients. On the other hand, when postprandial glycemia is of concern, aerobic exercise works better when performed after a meal, both in healthy and in diabetic patients.

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Introduction

Metabolism is highly influenced by energy turnover. Hence, the interplay between nutrition (the energy supplier) and exercise (the energy consumer) is particularly relevant to metabolic control in both the healthy and those affected by chronic disease.

Exercise, along with nutrition and pharmacologic agents, is recognized as a strong modulator of postprandial glycemic and triglyceridemic responses [1]. Nutritional, pharmacologic, and exercise interventions might be applied to the same individual simultaneously and, considering the fact that the glycemic and lipemic responses are time dependent, the net result of the three interventions could depend, at least in part, on the time sequence in which they are implemented. For this matter, the present paper will review the existing literature on the ‘when?’ of exercising for metabolic control, more specifically postprandial metabolic control, with a focus on glycemia and lipemia in healthy and in diabetic individuals. Only studies investigating the effect of aerobic exercise have been included, as this modality of exercise is the most standardized, thus allowing for between-study comparisons.

Exercise as a Prevention and Treatment Tool

The scientific world has begun to pay special attention to exercise, since a sedentary lifestyle is an important environmental risk factor for many noncommunicable illnesses. In fact, inactivity-related diseases are nowadays considered the leading causes of mortality in the world. Cardiovascular diseases, obesity, metabolic syndrome, type 2 diabetes mellitus (T2D), and associated complications cause a nonnegligible socioeconomic burden [2].

Therefore, exercise plays an exceptional role in the prevention and treatment of such conditions. Together with medical nutrition therapy and pharmacologic therapy, exercise therapy is one of the mainstays of diabetes treatment as recommended by the American Diabetes Association [3]. However, while diabetic patients seem to comply well with dietetic and pharmacologic interventions, their exercise levels remain low [4]. This might be partially due to the difficulty in prescribing exercise the same way as a pharmacologic agent. Indeed, there are many elements of exercise prescription that have not been clearly defined yet. There are some quantitative and qualitative aspects of exercise that should be considered when prescribing it. Research has mainly focused on the quantitative issue, i.e. the dose-response relationship of exercise and health outcomes. Generally, there is agreement on an inverse and linear relationship between aerobic exercise and the rates of all-cause mortality, the incidence of mortality from cardiovascular disease, and the incidence of T2D [5], although this might be subject to interindividual variability [6]. Current guidelines recommend healthy adults accumulate at least 150 min per week of moderate-intensity or ≥75 min per week of vigorous-intensity aerobic exercise. Engaging in resistance exercise for an additional 2–3 days per week is recommended to further optimize the benefits of exercise [7]. Guidelines for diabetic patients are similar to the ones for healthy individuals [8].

While the scientific and medical communities have reached a consensus on the minimal dose of exercise, which certainly is the ‘heart’ of exercise prescription, there is still some detail missing in the ‘directions for use’ section. On a typical medical prescription, the ‘distance from meal’ would stand just beside the ‘frequency of use’ under the ‘directions for use’ section. However, we are lacking such indications regarding exercise.

Temporal optimization of exercise in relation to meal consumption might be important to further increase the benefits from the same amounts of exercise. This might prove particularly beneficial to patients who need to further improve health outcomes from exercise but cannot increase the intensity or duration of exercise beyond a certain limit.

Meal Consumption as a Metabolic Disrupter: Importance of Targeting Postprandial Phenomena

It is well known that the response to exercise is highly dependent on the nutrient availability provided by the food intake and on the related hormonal background. Meal consumption provokes a series of endocrine and paracrine time-dependent responses that vary with respect to meal volume and composition [9]. Some of these responses are then summed from one meal to the next. The 24-hour timeframe can thus be divided into two metabolically distinct periods: the postprandial period and the postabsorptive period [10]. While there is little variability of substrate concentrations in the postabsorptive state, there is an increase in glycemic and lipemic levels in response to a meal in the postprandial state. The transition from postabsorptive to postprandial involves a complex interplay of mechanisms that lead to a shift in substrate utilization, defining the so-called metabolic flexibility [11].

Postprandial events have long been acknowledged as risks for atherogenesis. Zilversmit [12] recognized atherosclerosis to be a postprandial phenomenon, referring mainly to postprandial lipoprotein remnants. The strong association between these two phenomena has been repeatedly confirmed ever since. A high-fat diet and a single high-fat meal have been accused of inducing functional derangements that lead the way to insulin resistance and T2D [13]. Diabetes, on the other hand, is an independent risk factor for atherosclerosis [14,15]. Also, it has been extensively suggested that a better control of the postprandial triglyceridemia may help prevent chronic diseases. Indeed, Kishore et al. [16] demonstrated that, in T2D, acute lowering of free fatty-acid levels significantly improves hepatic and peripheral glucose effectiveness, i.e. the ability of hyperglycemia to inhibit endogenous glucose production. Hence, hyperlipidemia may be considered both as a risk factor for the development of and as a target for the prevention of chronic disease.

In addition to postprandial lipemia, postprandial hyperglycemia and glycemic peaks have been demonstrated to produce harmful byproducts and increase reactive oxygen species, which are nowadays retained as the most important common characteristic of chronic disease [17,18]. Be it a cause or a consequence of diabetes, postprandial hyperglycemia has been identified as an important risk factor in the development of macro- and microvascular complications of diabetes through different possible mechanisms [17,18,19,20,21,22,23,24]. Accordingly, the IDF has identified postmeal glycemia as a target of diabetes treatment [24,25]. The impression that might be created by the existing prevailing evidence is that only glycemia beyond the diabetic threshold level increases the risk of cardiovascular diseases. There is evidence, however, that the risk of cardiovascular events progressively increases with increasing of the so-called normal, nondiabetic glucose values [26].

It is now well established that chronic exposure to hyperglycemia (glucocentric approach) and hyperlipemia (lipocentric approach) can cause insulin resistance and T2D [27]. Diabetes, in turn, may result in failure to maintain normal postprandial and fasting values of the two, which then results in chronic complications. Hence, controlling postprandial hyperglycemia and hyperlipemia in healthy and diabetic individuals may result in a two-fold benefit. It may prevent diabetes and atherosclerosis-associated disorders in the healthy, while on the other hand in diabetic patients it may offer protection against diabetes progression and the development of its associated cardiovascular complications.

Exercise, with its effect on postprandial events, may be fundamental in interrupting the vicious cycle of chronic disease. Studies reviewed here point out that factors related to either exercise or meal characteristics, and the time interval between them, appear to importantly influence the effect of exercise.

Materials and Methods

To identify relevant reports on the effect of exercise on triglyceridemia and glycemia and the interaction with meal intake, a literature survey was carried out in PubMed (http://www.ncbi.nlm.nih.gov/pubmed/) and ScienceDirect (http://www.sciencedirect.com/). The following filters were applied to the search: human studies, published in the last 20 years, English language. Aerobic exercise, postprandial glycemia, postprandial lipemia, time lapse from meal, pre- versus postmeal exercise, and diabetes were used as keywords. Additional relevant articles were identified from the reference lists of selected articles and from a hand search of pertinent journals.

Selected articles were further examined for eligibility. Only experimental studies, with a randomized, counterbalanced crossover design investigating the effect of either a single bout of aerobic exercise or a training program were included in the present review.

Inclusion criteria are presented in table 1.

Table 1

Inclusion criteria for the reviewed studies

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Results

The relevant studies reviewed here are summarized in tables 2 and 3. Twenty-six studies were included in the final selection, 8 of which directly compared prior exercise with after-meal exercise [28,29,30,31,32,33,34,35]. The remaining 18 studies investigated the effect of exercise on postprandial events, modulating some parameters related to meals and exercise (i.e. exercise intensity and duration, meal size and composition) [36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53].

Table 2

Studies comparing premeal and postmeal exercise

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Table 3

Studies investigating the effect of aerobic exercise on postprandial events

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Aerobic Exercise and Postprandial Lipemia: Fasted versus Fed

Zhang et al. [35] compared the effects of 60 min of treadmill walking at 60% of the maximal oxygen consumption (Vo2max), performed either in the fasted state or after the consumption of high-fat meals. The authors concluded that exercising in the fasted state produces superior results with regard to postprandial plasmatic triglycerides (TG) and high-density lipoprotein (HDL) cholesterol concentrations. Particularly, the same exercise session performed the evening before a meal seemed to provide better overall postprandial lipoprotein concentrations compared to exercising either 24 h before or shortly prior to a meal, suggestive of an important role of lipoprotein lipase (LPL) in the lipid-lowering effect of exercise [35,36,54]. Katsanos and Moffatt [32], on the other hand, found a greater effect of exercise versus nonexercise but no significant difference between shortly pre- and postmeal walking. However, the heart rate response to postprandial exercise was higher, suggesting that fasting exercise, even if not more effective, might be more advisable than postmeal exercise.

Fasted exercise seems to rule in favor of postprandial lipemic control even when mixed meals rather than high-fat meals are consumed. According to Enevoldsen et al. [29], 60 min of cycling at 55% Vo2max performed 30 min before a standard mixed breakfast resulted in lower concentrations and an average integrated increase of plasmatic very low-density lipoprotein triacylglycerol (VLDL-TG), a lower triacylglycerol area under the curve (TG-AUC), and lower concentrations of plasmatic insulin compared to the same exercise 60 min postprandially. Also, prebreakfast cycling produced higher whole-body and adipose tissue lipolitic rates [29]. Recently, Hashimoto et al. [31] indicated that moderate-intensity exercise 20 min after a moderate-fat meal might be more favorable in terms of exogenous TG. It should be mentioned, however, that the authors clearly stated that due to the small number of participants and the specific design of the study the results should be interpreted with caution.

It may be concluded, from the studies comparing the two modalities, that exercising in the fasted state rather than in the fed state more effectively attenuates the lipemic effect of a meal, especially when high in fat content. Accordingly, the majority of studies investigating the effect of exercise on the TG response to a meal focus on different amounts of exercise performed in the afternoon prior to a test meal. The beneficial effect of prior exercise on postprandial lipemia could probably be related to the activation of either muscular or plasmatic LPL. In fact, changes in muscle LPL activity and plasmatic LPL concentration appear to be well correlated to changes in triglyceridemia, which makes this enzyme a plausible, yet partial, explanation for the TG-lowering effect of exercise. [40,42]. Considering that exercise-induced LPL activation does not occur until 4 h postexercise and lasts for 18–24 h after an exercise session [55,56,57], LPL can certainly not be responsible for changes in TG levels outside this time frame. The latter may explain, in part, the finding that exercise results in a better lipidic response when performed 12 h prior, rather than 1 or 24 h prior, to a high-fat meal in healthy [35] or hypertriglyceridemic individuals [54].

There is contrasting evidence regarding the lipid-lowering effect of fed-state exercise. Zhang et al. [35] and Tobin et al. [53] found no effect of postmeal moderate-intensity aerobic exercise after a high-fat meal in healthy individuals. Conversely, two other studies found a beneficial effect of postmeal exercise on the lipemic response to a high-fat meal [32,41]. However, as previously pointed out in the study of Katsanos and Moffatt [32], prior exercise could be more advisable due to the fact that it provokes less discomfort and cardiac response [32]. Therefore, postmeal exercise might also have an attenuating effect on postprandial lipemia, probably less pronounced and certainly involving different physiological mechanisms compared to exercise in the fasted state.

With regard to postprandial lipemic control, several investigations have compared fasted and postmeal exercise effects in healthy adults. The situation is completely different as far as diabetic patients are concerned, which makes our analysis rather difficult in the case of such patients. There is no study we know of that investigates the difference in lipemic response to a meal when exercise is performed prior to or after the meal in diabetic patients. It would be reasonable to assume that, as diabetes is a metabolic disorder involving primarily the metabolism of energetic substrates like glucose and lipids, the lipemic response to both meals and exercise might differ in diabetic patients.

Accordingly, diabetic patients, compared to a healthy control group, show higher basal levels of plasmatic TG and glucose, and these levels increase twice as much after a high-fat meal [53]. Alssema et al. [58] reported that a high-carbohydrate meal elicits greater TG, glucose, and insulin responses in T2D postmenopausal women when compared to age-matched healthy counterparts. One hour of moderate-intensity exercise, introduced after a fatty meal, is reported to attenuate meal-induced hyperlipidemia, reducing the total TG and VLDL-TG, in diabetics but not in healthy individuals [53]. Thus, the findings in normal individuals cannot be always transferred to those affected by disease.

Other Factors Influencing the Hypolipemic Effect of Exercise

In the setting of high-fat meals, the results have constantly been in favor of exercise and, as previously mentioned, if exercise sessions were to take place with sufficient time prior to a meal, their lipid-lowering effects would be more evident [32,35,36,39,40,42,54,59,60], with no significant difference between continuous and accumulated bouts [48]. Such results cannot be completely transferred to the generally recommended mixed, moderate-fat meals an adult is to consume in order to preserve health [61].

Meal composition and exercise amount are important additional factors influencing the effect of exercise. Contrasting results have been reported from studies investigating the effect of moderate-intensity exercise or its caloric equivalent on the lipemic response to a moderate-fat meal. Pfeiffer et al. [50,51] investigated the effect of ‘moderate-dose’ exercise performed before a moderate-fat meal and the yielded results suggested that exercise might lose its lipemic lowering effect in such conditions. Also, postprandial lipemia remained unaltered when increasing the ‘dose’ of exercise, i.e. duration [50] or energy expenditure [51]. Kolifa et al. [44], on the other hand, found a lowering effect of prior exercise on total TG but not the TG response to a meal when a moderate-fat-containing meal is consumed 14 h after a cycling session. The same appears to be true when an ad libitum breakfast and lunch are consumed the day after an exercise session of relatively high energy expenditure (33.5 kJ/kg body mass) [38]. This free feeding pattern is certainly closer to real life than standard laboratory meals, and the fact that exercise conserved its lipid-lowering effect independently of meal characteristics suggests that when such high doses of exercise are administered to healthy adults, meal size and composition become of secondary importance. In fact, Gill et al. [39] found out that exercise showed a dose-dependent, exercise-specific effect on TG, which further supports the finding of Farah et al. [38]. Nevertheless, the duration of exercise necessary to accumulate 33.5 kJ/kg body mass in the latter was between 65 and 110 min, which makes it rather unlikely to be performed on a daily basis in order to attenuate postmeal hyperlipidemia.

In summary, it can be said that the effect of prior exercise on lipidemia in healthy adults cannot be determined by a single factor but is rather determined by the mutual interplay of exercise dose and meal size and composition. The response to a big, high-fat meal is likely to be influenced even by moderate doses of exercise, whereas the response to a moderate-fat meal is not. Likewise, when high amounts of energy expenditure are achievable, meal characteristics may be less important. The latter could be of comfort on touristic trips when, along with sightseeing that involves long walks, one can also enjoy the traditional cuisine without guilt.

Glycemic Response to Aerobic Exercise in Healthy Individuals – Fasted versus Fed

Postprandial glycemia, or more precisely hyperglycemia, remains a central issue in the management of diabetes. Glycemia is easily modulated by lifestyle and pharmacological interventions, with the former as important as drugs in diabetic patients [43] and the single most relevant intervention in healthy individuals.

Naturally, research on glycemic control done on diabetic patients outweighs that done on healthy nondiabetic subjects. Results from a few studies on healthy individuals will shortly be examined as a basis of comparison between the two conditions. Very few studies compared the glycemic responses to exercise performed pre- or postmeals in healthy individuals. A specific study that compares these two exercise timings is the study from Van Proeyen et al. [34]. It being a longitudinal study, its results show the cumulative effect of regular training, either in the fasted state or in the fed state, when on a hyper-caloric, high-fat diet. This kind of diet may not be the typical eating pattern of healthy individuals whose purpose is to preserve their health. Nevertheless, for those who in the long or short term consume high volumes of fat-rich food, exercise timing might make the difference. Indeed, the study in question manages to demonstrate that 4 days per week of endurance exercise training performed in the fasted state is significantly superior to fed-state exercise in terms of whole-body glucose tolerance, insulin sensitivity, and muscle adaptations, i.e. AMP-activated protein kinase α phosphorylation, GLUT-4 (glucose transporter 4), etc. [34].

Evaluating the immediate responses to a similar amount of endurance exercise performed before carbohydrate intake, it appears that such exercise results in no significant main effect on plasma glucose and insulin, although it might alter the kinetics of these parameters [62].

Postprandially performed exercise, on the other hand, might not offer the same results. In healthy women, light to moderate-intensity walking or cycling immediately after a high-glycemic breakfast (i.e. cornflakes and milk, 1 g carbohydrate per kg body weight), attenuates the glycemic response (incremental area under the curve; iAUC) to a meal [43,49] compared to rest. When comparing 15-min bouts with 40-min bouts, the hypoglycemic effect appears to be proportional to the duration in the same way it is proportional to the intensity, leading to the suggestion that this lowering effect is primarily determined by energy expenditure during exercise [49]. Furthermore, those who might be benefiting more from 30–40 min of moderate-intensity exercise, or shorter-duration but higher-intensity exercise, are individuals showing more elevated glycemic responses at rest [49,52] and sedentary, middle-aged subjects, the latter compared to trained, young subjects [43]. Even more interesting is the fact that the glucose-lowering effect of postmeal exercise is reported to be comparable to that of hypoglycemic drugs [43]. A more vigorous postprandial exercise has been reported to transiently increase blood glucose values compared to pre-exercise [52]. In contrast, Charlot et al. [37] reported that 75 min of high-intensity cycling, compared to rest, yield sustained lower glycemia throughout the exercise session and may also exert an influence on the following meal, delaying peak postlunch glycemia with no significant difference in total glucose AUCs. However, the generalizability and practical relevance of such results may need further investigation. What we can almost certainly affirm is that, in the immediate term, moderate volumes of exercise produce better glycemic effects in healthy adults if performed after a meal, compared to preprandial exercise.

Effect of Exercise on Postprandial Glycemia in Diabetic Individuals: Time Interval from a Meal

As we previously emphasized, diabetic patients differ from healthy subjects in their metabolic and hormonal responses to meals. Accordingly, T2D patients respond more abruptly to either a high-carbohydrate meal or a high-fat meal, in terms of glucose and insulin iAUCs, when compared to nondiabetic subjects [53,58].

Applying exercise as a treatment in diabetic patients involves two major issues. Firstly, exercise should be safe. Secondly, it should be effective. Fulfilling these two criteria would potentially prevent any risks of acute (hypoglycemia) or chronic (mainly cardiovascular) complications and thus successfully manage diabetes. It would be rather intuitive to think that, as both exercise and meals provoke a glycemic response, the time interval from a meal would be tightly connected to the safety and effectiveness of exercise. In addition, one particular aspect that should always be taken into consideration when examining blood glucose control in diabetic patients is the categorization of effects according to the oral hypoglycemic drugs being taken by patients in the meantime.

As for the safety of exercise in T2D patients, the major concern refers to exercising in the fasted state, especially in patients using insulin-secreting drugs, due to the risk of eliciting hypoglycemia, with the latter being a recognized precipitating factor for myocardial ischemia [63]. However, there is convincing evidence that the actual risk of fasted exercise causing hypoglycemia is virtually inexistent for diabetes patients on diet only and/or oral hypoglycemic drugs, sulfonylureas included [33,64,65,66,67,68]. Even more interesting are the findings of Gaudet-Savard et al. [30] showing that the glycemic response to exercise is primarily determined by pre-exercise plasmatic concentrations of glucose. Hence, the same fasted exercise may either decrease or have no effect on glycemia, depending on the pre-exercise starting point.

With regard to the effectiveness of exercise in lowering blood glucose, it has been repeatedly demonstrated that 60 min of cycling at 60% Vo2max is most effective in lowering blood glucose when performed postprandially [30,33,68]. These results apply to both standard (mixed meal) and nonstandard (ad libitum) meal conditions [33,68]. The hypoglycemic effect of exercise appears to be greatest in the late postprandial period, i.e. 4–5 h, especially in patients on a combination of metformin and sulfonylureas, or sulfonylureas alone [30,33]. As with the effect of exercise in the fasted state, in the fed state also, postexercise glycemia will depend on the pre-exercise blood glucose levels [30].

Further dividing the postprandial period into pre- and postmeal times, evidence from Colberg et al. [28] demonstrates that as little as 20 min of postmeal, but not premeal, self-paced walking significantly attenuates the glycemia after a standard dinner.

The beneficial effects of aerobic exercise are generally attributed to its intensity [69]. However, evidence from Larsen et al. [45,46] and Manders et al. [47] shows that higher intensities are not necessarily a synonym of better postprandial glycemic control. On the contrary, apart from being a more comfortable and feasible option for diabetic patients, moderate to low intensity iso-energetic exercise is not different in terms of glycemic response, compared to higher intensities. Indeed, high and low intensities, when matched for energy cost, produce similar effects on postprandial and nocturnal glucose concentrations [47]. Furthermore, low-intensity, but not high-intensity, exercise lowers the 24-hour glucose responses and prevalence of hyperglycemia, as demonstrated by continuous monitoring of blood glucose [47].

Discussion and Conclusions

Statements like: ‘exercise is good for your health’ or ‘ exercise may prevent chronic disease’, have become common knowledge nowadays, but while life is becoming faster – fast food, fast transportation, fast clicks – moving is becoming slow. While man works to perfect technology, lifestyle takes a few steps back and chronic disease thrives. It is in this era that time seems to be the main unresolved issue with regard to inactivity. Fortunately, time is not only a problem – it may also be a solution.

In the studies presently reviewed, timing appeared to interfere with the resulting metabolic effect of an exercise session. The same amount of aerobic exercise (generally referring to the total energy expended during exertion) was demonstrated to produce completely different results, ranging from no effect to significantly lower triglyceridemia or glycemia.

Interestingly, in healthy individuals, exercising in the fasted state rules strongly in favor of TG control [32,35,36,39,40,42,54,59,60], leaving glycemia basically unaltered [33,64,65,66,67,68]. On the other hand, regularly training in this state prevents weight gain and lipid-induced insulin resistance in people consuming hypercaloric and high-fat diets [34].

These results might be of particular relevance in those countries where the traditional diet is very rich in fat. Hence, regular exercise before breakfast might be the most effective in overcoming the lipid-induced detrimental effects of such a diet. When high-fat content is only occasional among the usual meals of healthy individuals, exercising in the morning or in the evening before an occasional high-fat meal would probably bring more ‘cheers’ to that family Sunday lunch. Of note, however, is the observation made by Pfeiffer et al. [50,51] that the same type and amount of exercise is least likely to have significant effects on postprandial TG when the lipemic impact of meals is only moderate to low. Hence, it can be affirmed that in specific life settings, such as high-fat meals, fasted-state exercise could probably be more effective in attenuating the diabetogenic and atherogenic effect of postprandial phenomena, and consequently in preventing chronic disease.

The main concern in the case of iso- or hyper-caloric mixed meals, generally with moderate fat content but high in carbohydrate (50–60%), would be postprandial hyperglycemia rather than postprandial lipemia. Concordant results in healthy and diabetic individuals clearly demonstrate that the glycemic response to mixed meals is most effectively attenuated by postmeal exercise [30,33,43,49,62,68]. As little as a 20-min walk after a meal [28] holds the potential to prevent cardiovascular disease and diabetes progression.

Certainly, the aforementioned effects are dose dependent, and modulations of exercise timing with the intent to optimize metabolic control are to be considered as an adjunct of the most powerful determinant of the metabolic effect – energy expenditure. As formerly demonstrated, the amount of energy expended in an activity majorly determines the benefit in lipemia and glycemia, making exercise intensity tradable with and as important as duration [39,45,46,47]. This concept becomes very important as we consider the array from young to old adults and from healthy to diabetic individuals. For healthy young adults who cannot afford to spend much time exercising, it could be more feasible to engage in short, intense bouts of exercise, whereas in old diabetic patients, where high-intensity exercise might not always be indicated or pleasant, trading intensity for duration would be as effective. Moreover, such an approach in these subjects might prove safer and sometimes more effective in terms of specific aspects of glycemic control [47].

In summary, once an optimal exercise ‘dose’ is achieved by healthy or diabetic individuals, modulating exercise timing might further optimize the metabolic benefit of aerobic exercise. Hence, modulating ‘dose-related’ parameters of exercise – i.e. intensity and duration – and the timing of a bout, one can flexibly adjust exercise sessions according to real-life limitations and situations. For instance, in the case of working healthy adults for whom lack of time is probably the main reason for skipping exercise sessions, a high-intensity bout of short duration might be a worthy option. Moreover, in a setting of either habitual or occasional high-fat meals that same session would be greatly beneficial if performed in the fasted state. Differently, in diabetic patients for whom postprandial glycemia is the main treatment target, postmeal exercise might aid in reaching the target. It would seem sensible to speculate that dividing a daily session into two parts, one in the fasted state and one in the postprandial state, could provide maximal benefit for both triglyceridemia and glycemia. The latter, if true, would be of particular relevance to hypertriglyceridemic diabetic patients, but this issue remains to be addressed by future research.

We can now provide and answer to the question ‘should exercise be done before or after a meal?’. Aerobic exercise should be performed before or after a meal, depending on the meal composition and metabolic outcome. Premeal exercise should be done to control lipidemia and postmeal exercise to manage hyperglycemia.


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  21. Haffner SM: The importance of hyperglycemia in the nonfasting state to the development of cardiovascular disease. Endocr Rev 1998;19:583–592.
  22. Cavalot F, Petrelli A, Traversa M, Bonomo K, Fiora E, Conti M, Anfossi G, Costa G, Trovati M: Postprandial blood glucose is a stronger predictor of cardiovascular events than fasting blood glucose in type 2 diabetes mellitus, particularly in women: lessons from the San Luigi Gonzaga Diabetes Study. J Clin Endocrinol Metab 2006;91:813–819.
  23. Ceriello A, Esposito K, Piconi L, Ihnat MA, Thorpe JE, Testa R, Boemi M, Giugliano D: Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes 2008;57:1349–1354.
  24. Kim MK, Jung HS, Yoon CS, Ko JH, Jun HJ, Kim TK, Kwon MJ, Lee SH, Ko KS, Rhee BD, Park JH: The effect of glucose fluctuation on apoptosis and function of INS-1 pancreatic beta cells. Korean Diabetes J 2010;34:47–54.
    External Resources
  25. Ceriello A, Colagiuri S: International Diabetes Federation guideline for management of postmeal glucose: a review of recommendations. Diabet Med 2008;25:1151–1156.
  26. Coutinho M, Gerstein HC, Wang Y, Yusuf S: The relationship between glucose and incident cardiovascular events: a metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years. Diabetes Care 1999;22:233–240.
  27. Bruce CR, Hawley JA: Improvements in insulin resistance with aerobic exercise training: a lipocentric approach. Med Sci Sports Exerc 2004;36:1196–1201.
  28. Colberg SR, Zarrabi L, Bennington L, Nakave A, Thomas Somma C, Swain DP, Sechrist SR: Postprandial walking is better for lowering the glycemic effect of dinner than pre-dinner exercise in type 2 diabetic individuals. J Am Med Dir Assoc 2009;10:394–397.
    External Resources
  29. Enevoldsen LH, Simonsen L, Macdonald IA, Bulow J: The combined effects of exercise and food intake on adipose tissue and splanchnic metabolism. J Physiol 2004;561:871–882.
  30. Gaudet-Savard T, Ferland A, Broderick TL, Garneau C, Tremblay A, Nadeau A, Poirier P: Safety and magnitude of changes in blood glucose levels following exercise performed in the fasted and the postprandial state in men with type 2 diabetes. Eur J Cardiovasc Prev Rehabil 2007;14:831–836.
    External Resources
  31. Hashimoto S, Ootani K, Hayashi S, Naito M: Acute effects of shortly pre- versus postprandial aerobic exercise on postprandial lipoprotein metabolism in healthy but sedentary young women. J Atheroscler Thromb 2011;18:891–900.
  32. Katsanos CS, Moffatt RJ: Acute effects of premeal versus postmeal exercise on postprandial hypertriglyceridemia. Clin J Sport Med 2004;14:33–39.
    External Resources
  33. Poirier P, Tremblay A, Catellier C, Tancrede G, Garneau C, Nadeau A: Impact of time interval from the last meal on glucose response to exercise in subjects with type 2 diabetes. J Clin Endocrinol Metab 2000;85:2860–2864.
  34. Van Proeyen K, Szlufcik K, Nielens H, Pelgrim K, Deldicque L, Hesselink M, Van Veldhoven PP, Hespel P: Training in the fasted state improves glucose tolerance during fat-rich diet. J Physiol 2010;588:4289–4302.
  35. Zhang JQ, Thomas TR, Ball SD: Effect of exercise timing on postprandial lipemia and HDL cholesterol subfractions. J Appl Physiol 1998;85:1516–1522.
  36. Aldred HE, Perry IC, Hardman AE: The effect of a single bout of brisk walking on postprandial lipemia in normolipidemic young adults. Metabolism 1994;43:836–841.
  37. Charlot K, Pichon A, Chapelot D: Exercise prior to a freely requested meal modifies pre and postprandial glucose profile, substrate oxidation and sympathovagal balance. Nutr Metab (Lond) 2011;8:66.
  38. Farah NM, Malkova D, Gill JM: Effects of exercise on postprandial responses to ad libitum feeding in overweight men. Med Sci Sports Exerc 2010;42:2015–2022.
  39. Gill JM, Herd SL, Hardman AE: Moderate exercise and post-prandial metabolism: issues of dose-response. J Sports Sci 2002;20:961–967.
  40. Gill JM, Herd SL, Vora V, Hardman AE: Effects of a brisk walk on lipoprotein lipase activity and plasma triglyceride concentrations in the fasted and postprandial states. Eur J Appl Physiol 2003;89:184–190.
  41. Hardman AE, Aldred HE: Walking during the postprandial period decreases alimentary lipaemia. J Cardiovasc Risk 1995;2:71–78.
  42. Herd SL, Kiens B, Boobis LH, Hardman AE: Moderate exercise, postprandial lipemia, and skeletal muscle lipoprotein lipase activity. Metabolism 2001;50:756–762.
  43. Hostmark AT, Ekeland GS, Beckstrom AC, Meen HD: Postprandial light physical activity blunts the blood glucose increase. Prev Med 2006;42:369–371.
    External Resources
  44. Kolifa M, Petridou A, Mougios V: Effect of prior exercise on lipemia after a meal of moderate fat content. Eur J Clin Nutr 2004;58:1327–1335.
  45. Larsen JJ, Dela F, Kjaer M, Galbo H: The effect of moderate exercise on postprandial glucose homeostasis in NIDDM patients. Diabetologia 1997;40:447–453.
  46. Larsen JJ, Dela F, Madsbad S, Galbo H: The effect of intense exercise on postprandial glucose homeostasis in type II diabetic patients. Diabetologia 1999;42:1282–1292.
  47. Manders RJ, Van Dijk JW, van Loon LJ: Low-intensity exercise reduces the prevalence of hyperglycemia in type 2 diabetes. Med Sci Sports Exerc 2010;42:219–225.
  48. Murphy MH, Nevill AM, Hardman AE: Different patterns of brisk walking are equally effective in decreasing postprandial lipaemia. Int J Obes Relat Metab Disord 2000;24:1303–1309.
  49. Nygaard H, Tomten SE, Hostmark AT: Slow postmeal walking reduces postprandial glycemia in middle-aged women. Appl Physiol Nutr Metab 2009;34:1087–1092.
    External Resources
  50. Pfeiffer M, Ludwig T, Wenk C, Colombani PC: The influence of walking performed immediately before meals with moderate fat content on postprandial lipemia. Lipids Health Dis 2005;4:24.
    External Resources
  51. Pfeiffer M, Wenk C, Colombani PC: The influence of 30 minutes of light to moderate intensity cycling on postprandial lipemia. Eur J Cardiovasc Prev Rehabil 2006;13:363–368.
    External Resources
  52. Szewieczek J, Dulawa J, Strzalkowska D, Hornik B, Kawecki G: Impact of the short-term, intense exercise on postprandial glycemia in type 2 diabetic patients treated with gliclazide. J Diabetes Complications 2007;21:101–107.
    External Resources
  53. Tobin LW, Kiens B, Galbo H: The effect of exercise on postprandial lipidemia in type 2 diabetic patients. Eur J Appl Physiol 2008;102:361–370.
  54. Zhang JQ, Ji LL, Nunez G, Feathers S, Hart CL, Yao WX: Effect of exercise timing on postprandial lipemia in hypertriglyceridemic men. Can J Appl Physiol 2004;29:590–603.
    External Resources
  55. Kantor MA, Cullinane EM, Herbert PN, Thompson PD: Acute increase in lipoprotein lipase following prolonged exercise. Metabolism 1984;33:454–457.
  56. Kantor MA, Cullinane EM, Sady SP, Herbert PN, Thompson PD: Exercise acutely increases high density lipoprotein-cholesterol and lipoprotein lipase activity in trained and untrained men. Metabolism 1987;36:188–192.
  57. Kiens B, Lithell H, Mikines KJ, Richter EA: Effects of insulin and exercise on muscle lipoprotein lipase activity in man and its relation to insulin action. J Clin Invest 1989;84:1124–1129.
  58. Alssema M, Schindhelm RK, Dekker JM, Diamant M, Nijpels G, Teerlink T, Scheffer PG, Kostense PJ, Heine RJ: Determinants of postprandial triglyceride and glucose responses after two consecutive fat-rich or carbohydrate-rich meals in normoglycemic women and in women with type 2 diabetes mellitus: the Hoorn Prandial Study. Metabolism 2008;57:1262–1269.
  59. Tsetsonis NV, Hardman AE: Reduction in postprandial lipemia after walking: influence of exercise intensity. Med Sci Sports Exerc 1996;28:1235–1242.
  60. Malkova D, Hardman AE, Bowness RJ, Macdonald IA: The reduction in postprandial lipemia after exercise is independent of the relative contributions of fat and carbohydrate to energy metabolism during exercise. Metabolism 1999;48:245–251.
  61. Seagle HM, Strain GW, Makris A, Reeves RS: Position of the American Dietetic Association: weight management. J Am Diet Assoc 2009;109:330–346.
    External Resources
  62. Long W 3rd, Wells K, Englert V, Schmidt S, Hickey MS, Melby CL: Does prior acute exercise affect postexercise substrate oxidation in response to a high carbohydrate meal? Nutr Metab (Lond) 2008;5:2.
    External Resources
  63. Duh E, Feinglos M: Hypoglycemia-induced angina pectoris in a patient with diabetes mellitus. Ann Intern Med 1994;121:945–946.
  64. Jenkins AB, Furler SM, Bruce DG, Chisholm DJ: Regulation of hepatic glucose output during moderate exercise in non-insulin-dependent diabetes. Metabolism 1988;37:966–972.
  65. Colberg SR, Hagberg JM, McCole SD, Zmuda JM, Thompson PD, Kelley DE: Utilization of glycogen but not plasma glucose is reduced in individuals with NIDDM during mild-intensity exercise. J Appl Physiol 1996;81:2027–2033.
  66. Riddle MC, McDaniel PA, Tive LA: Glipizide-GITS does not increase the hypoglycemic effect of mild exercise during fasting in NIDDM. Diabetes Care 1997;20:992–994.
  67. Gudat U, Bungert S, Kemmer F, Heinemann L: The blood glucose lowering effects of exercise and glibenclamide in patients with type 2 diabetes mellitus. Diabet Med 1998;15:194–198.
  68. Poirier P, Mawhinney S, Grondin L, Tremblay A, Broderick T, Cleroux J, Catellier C, Tancrede G, Nadeau A: Prior meal enhances the plasma glucose lowering effect of exercise in type 2 diabetes. Med Sci Sports Exerc 2001;33:1259–1264.
  69. Snowling NJ, Hopkins WG: Effects of different modes of exercise training on glucose control and risk factors for complications in type 2 diabetic patients: a meta-analysis. Diabetes Care 2006;29:2518–2527.
    External Resources

Author Contacts

Massimo Sacchetti, PhD

Department of Human Movement and Sport Sciences

‘Foro Italico’ University of Rome

Piazza Lauro De Bosis 15, IT–00135 Rome (Italy)

E-Mail massimo.sacchetti@uniroma4.it


Article / Publication Details

First-Page Preview
Abstract of Review Article

Received: 3/13/2012
Accepted: 9/15/2012
Published online: 11/27/2012
Issue release date: January 2013

Number of Print Pages: 12
Number of Figures: 0
Number of Tables: 3

ISSN: 0250-6807 (Print)
eISSN: 1421-9697 (Online)

For additional information: http://www.karger.com/ANM


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  22. Cavalot F, Petrelli A, Traversa M, Bonomo K, Fiora E, Conti M, Anfossi G, Costa G, Trovati M: Postprandial blood glucose is a stronger predictor of cardiovascular events than fasting blood glucose in type 2 diabetes mellitus, particularly in women: lessons from the San Luigi Gonzaga Diabetes Study. J Clin Endocrinol Metab 2006;91:813–819.
  23. Ceriello A, Esposito K, Piconi L, Ihnat MA, Thorpe JE, Testa R, Boemi M, Giugliano D: Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes 2008;57:1349–1354.
  24. Kim MK, Jung HS, Yoon CS, Ko JH, Jun HJ, Kim TK, Kwon MJ, Lee SH, Ko KS, Rhee BD, Park JH: The effect of glucose fluctuation on apoptosis and function of INS-1 pancreatic beta cells. Korean Diabetes J 2010;34:47–54.
    External Resources
  25. Ceriello A, Colagiuri S: International Diabetes Federation guideline for management of postmeal glucose: a review of recommendations. Diabet Med 2008;25:1151–1156.
  26. Coutinho M, Gerstein HC, Wang Y, Yusuf S: The relationship between glucose and incident cardiovascular events: a metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years. Diabetes Care 1999;22:233–240.
  27. Bruce CR, Hawley JA: Improvements in insulin resistance with aerobic exercise training: a lipocentric approach. Med Sci Sports Exerc 2004;36:1196–1201.
  28. Colberg SR, Zarrabi L, Bennington L, Nakave A, Thomas Somma C, Swain DP, Sechrist SR: Postprandial walking is better for lowering the glycemic effect of dinner than pre-dinner exercise in type 2 diabetic individuals. J Am Med Dir Assoc 2009;10:394–397.
    External Resources
  29. Enevoldsen LH, Simonsen L, Macdonald IA, Bulow J: The combined effects of exercise and food intake on adipose tissue and splanchnic metabolism. J Physiol 2004;561:871–882.
  30. Gaudet-Savard T, Ferland A, Broderick TL, Garneau C, Tremblay A, Nadeau A, Poirier P: Safety and magnitude of changes in blood glucose levels following exercise performed in the fasted and the postprandial state in men with type 2 diabetes. Eur J Cardiovasc Prev Rehabil 2007;14:831–836.
    External Resources
  31. Hashimoto S, Ootani K, Hayashi S, Naito M: Acute effects of shortly pre- versus postprandial aerobic exercise on postprandial lipoprotein metabolism in healthy but sedentary young women. J Atheroscler Thromb 2011;18:891–900.
  32. Katsanos CS, Moffatt RJ: Acute effects of premeal versus postmeal exercise on postprandial hypertriglyceridemia. Clin J Sport Med 2004;14:33–39.
    External Resources
  33. Poirier P, Tremblay A, Catellier C, Tancrede G, Garneau C, Nadeau A: Impact of time interval from the last meal on glucose response to exercise in subjects with type 2 diabetes. J Clin Endocrinol Metab 2000;85:2860–2864.
  34. Van Proeyen K, Szlufcik K, Nielens H, Pelgrim K, Deldicque L, Hesselink M, Van Veldhoven PP, Hespel P: Training in the fasted state improves glucose tolerance during fat-rich diet. J Physiol 2010;588:4289–4302.
  35. Zhang JQ, Thomas TR, Ball SD: Effect of exercise timing on postprandial lipemia and HDL cholesterol subfractions. J Appl Physiol 1998;85:1516–1522.
  36. Aldred HE, Perry IC, Hardman AE: The effect of a single bout of brisk walking on postprandial lipemia in normolipidemic young adults. Metabolism 1994;43:836–841.
  37. Charlot K, Pichon A, Chapelot D: Exercise prior to a freely requested meal modifies pre and postprandial glucose profile, substrate oxidation and sympathovagal balance. Nutr Metab (Lond) 2011;8:66.
  38. Farah NM, Malkova D, Gill JM: Effects of exercise on postprandial responses to ad libitum feeding in overweight men. Med Sci Sports Exerc 2010;42:2015–2022.
  39. Gill JM, Herd SL, Hardman AE: Moderate exercise and post-prandial metabolism: issues of dose-response. J Sports Sci 2002;20:961–967.
  40. Gill JM, Herd SL, Vora V, Hardman AE: Effects of a brisk walk on lipoprotein lipase activity and plasma triglyceride concentrations in the fasted and postprandial states. Eur J Appl Physiol 2003;89:184–190.
  41. Hardman AE, Aldred HE: Walking during the postprandial period decreases alimentary lipaemia. J Cardiovasc Risk 1995;2:71–78.
  42. Herd SL, Kiens B, Boobis LH, Hardman AE: Moderate exercise, postprandial lipemia, and skeletal muscle lipoprotein lipase activity. Metabolism 2001;50:756–762.
  43. Hostmark AT, Ekeland GS, Beckstrom AC, Meen HD: Postprandial light physical activity blunts the blood glucose increase. Prev Med 2006;42:369–371.
    External Resources
  44. Kolifa M, Petridou A, Mougios V: Effect of prior exercise on lipemia after a meal of moderate fat content. Eur J Clin Nutr 2004;58:1327–1335.
  45. Larsen JJ, Dela F, Kjaer M, Galbo H: The effect of moderate exercise on postprandial glucose homeostasis in NIDDM patients. Diabetologia 1997;40:447–453.
  46. Larsen JJ, Dela F, Madsbad S, Galbo H: The effect of intense exercise on postprandial glucose homeostasis in type II diabetic patients. Diabetologia 1999;42:1282–1292.
  47. Manders RJ, Van Dijk JW, van Loon LJ: Low-intensity exercise reduces the prevalence of hyperglycemia in type 2 diabetes. Med Sci Sports Exerc 2010;42:219–225.
  48. Murphy MH, Nevill AM, Hardman AE: Different patterns of brisk walking are equally effective in decreasing postprandial lipaemia. Int J Obes Relat Metab Disord 2000;24:1303–1309.
  49. Nygaard H, Tomten SE, Hostmark AT: Slow postmeal walking reduces postprandial glycemia in middle-aged women. Appl Physiol Nutr Metab 2009;34:1087–1092.
    External Resources
  50. Pfeiffer M, Ludwig T, Wenk C, Colombani PC: The influence of walking performed immediately before meals with moderate fat content on postprandial lipemia. Lipids Health Dis 2005;4:24.
    External Resources
  51. Pfeiffer M, Wenk C, Colombani PC: The influence of 30 minutes of light to moderate intensity cycling on postprandial lipemia. Eur J Cardiovasc Prev Rehabil 2006;13:363–368.
    External Resources
  52. Szewieczek J, Dulawa J, Strzalkowska D, Hornik B, Kawecki G: Impact of the short-term, intense exercise on postprandial glycemia in type 2 diabetic patients treated with gliclazide. J Diabetes Complications 2007;21:101–107.
    External Resources
  53. Tobin LW, Kiens B, Galbo H: The effect of exercise on postprandial lipidemia in type 2 diabetic patients. Eur J Appl Physiol 2008;102:361–370.
  54. Zhang JQ, Ji LL, Nunez G, Feathers S, Hart CL, Yao WX: Effect of exercise timing on postprandial lipemia in hypertriglyceridemic men. Can J Appl Physiol 2004;29:590–603.
    External Resources
  55. Kantor MA, Cullinane EM, Herbert PN, Thompson PD: Acute increase in lipoprotein lipase following prolonged exercise. Metabolism 1984;33:454–457.
  56. Kantor MA, Cullinane EM, Sady SP, Herbert PN, Thompson PD: Exercise acutely increases high density lipoprotein-cholesterol and lipoprotein lipase activity in trained and untrained men. Metabolism 1987;36:188–192.
  57. Kiens B, Lithell H, Mikines KJ, Richter EA: Effects of insulin and exercise on muscle lipoprotein lipase activity in man and its relation to insulin action. J Clin Invest 1989;84:1124–1129.
  58. Alssema M, Schindhelm RK, Dekker JM, Diamant M, Nijpels G, Teerlink T, Scheffer PG, Kostense PJ, Heine RJ: Determinants of postprandial triglyceride and glucose responses after two consecutive fat-rich or carbohydrate-rich meals in normoglycemic women and in women with type 2 diabetes mellitus: the Hoorn Prandial Study. Metabolism 2008;57:1262–1269.
  59. Tsetsonis NV, Hardman AE: Reduction in postprandial lipemia after walking: influence of exercise intensity. Med Sci Sports Exerc 1996;28:1235–1242.
  60. Malkova D, Hardman AE, Bowness RJ, Macdonald IA: The reduction in postprandial lipemia after exercise is independent of the relative contributions of fat and carbohydrate to energy metabolism during exercise. Metabolism 1999;48:245–251.
  61. Seagle HM, Strain GW, Makris A, Reeves RS: Position of the American Dietetic Association: weight management. J Am Diet Assoc 2009;109:330–346.
    External Resources
  62. Long W 3rd, Wells K, Englert V, Schmidt S, Hickey MS, Melby CL: Does prior acute exercise affect postexercise substrate oxidation in response to a high carbohydrate meal? Nutr Metab (Lond) 2008;5:2.
    External Resources
  63. Duh E, Feinglos M: Hypoglycemia-induced angina pectoris in a patient with diabetes mellitus. Ann Intern Med 1994;121:945–946.
  64. Jenkins AB, Furler SM, Bruce DG, Chisholm DJ: Regulation of hepatic glucose output during moderate exercise in non-insulin-dependent diabetes. Metabolism 1988;37:966–972.
  65. Colberg SR, Hagberg JM, McCole SD, Zmuda JM, Thompson PD, Kelley DE: Utilization of glycogen but not plasma glucose is reduced in individuals with NIDDM during mild-intensity exercise. J Appl Physiol 1996;81:2027–2033.
  66. Riddle MC, McDaniel PA, Tive LA: Glipizide-GITS does not increase the hypoglycemic effect of mild exercise during fasting in NIDDM. Diabetes Care 1997;20:992–994.
  67. Gudat U, Bungert S, Kemmer F, Heinemann L: The blood glucose lowering effects of exercise and glibenclamide in patients with type 2 diabetes mellitus. Diabet Med 1998;15:194–198.
  68. Poirier P, Mawhinney S, Grondin L, Tremblay A, Broderick T, Cleroux J, Catellier C, Tancrede G, Nadeau A: Prior meal enhances the plasma glucose lowering effect of exercise in type 2 diabetes. Med Sci Sports Exerc 2001;33:1259–1264.
  69. Snowling NJ, Hopkins WG: Effects of different modes of exercise training on glucose control and risk factors for complications in type 2 diabetic patients: a meta-analysis. Diabetes Care 2006;29:2518–2527.
    External Resources