Systematic Reviews
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Diabetes. Apr 15, 2015; 6(3): 534-542
Published online Apr 15, 2015. doi: 10.4239/wjd.v6.i3.534
Effect of aerobic and anaerobic exercises on glycemic control in type 1 diabetic youths
Andrea Lukács, László Barkai
Andrea Lukács, László Barkai, Faculty of Health Care, University of Miskolc, 3515 Miskolc-Egyetemváros, Hungary
László Barkai, Velkey László Center for Child Health, 3501 Miskolc, Hungary
Author contributions: Both authors contributed to this manuscript.
Conflict-of-interest: No conflict of interest stated by any authors.
Data sharing: This manuscript does not describe basic or clinical research, therefore data sharing statement is not relevant.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: László Barkai, MD, PhD, DSc, Faculty of Health Care, University of Miskolc, 3515 Miskolc-Egyetemváros, Hungary. barkai.l@t-online.hu
Telephone: +36-46-565111 Fax: +36-46-366961
Received: July 29, 2014
Peer-review started: July 30, 2014
First decision: October 14, 2014
Revised: January 2, 2015
Accepted: January 15, 2015
Article in press: January 19, 2015
Published online: April 15, 2015

Abstract

AIM: To evaluate the long-term effect of aerobic and/or anaerobic exercise on glycemic control in youths with type 1 diabetes.

METHODS: Literature review was performed in spring and summer 2014 using PubMed/MEDLINE, Google Scholar, Scopus, and ScienceDirect with the following terms: aerobic, anaerobic, high-intensity, resistance, exercise/training, combined with glycemic/metabolic control, glycated haemoglobin A1c (HbA1c) and type 1 diabetes. Only peer-reviewed articles in English were included published in the last 15 years. It was selected from 1999 to 2014. Glycemic control was measured with HbA1c. Studies with an intervention lasting at least 12 wk were included if the HbA1c was measured before and after the intervention.

RESULTS: A total of nine articles were found, and they were published between the years of 2002-2011. The sample size was 401 diabetic youths (166 males and 235 females) with an age range of 10-19 years except one study, in which the age range was 13-30 years. Study participants were from Australia, Tunisia, Lithuania, Taiwan, Turkey, Brazilia, Belgium, Egypt and France. Four studies were aerobic-based, four were combined aerobic and anaerobic programs, and one compared aerobic exercise to anaerobic one. Available studies had insufficient evidence that any type of exercise or combined training would clearly improve the glycemic control in type 1 diabetic youth. Only three (two aerobic-based and one combined) studies could provide a significant positive change in glycemic control.

CONCLUSION: The regular physical exercise has several other valuable physiological and health benefits that justify the inclusion of exercise in pediatric diabetes treatment and care.

Key Words: Type 1 diabetes mellitus, Glycemic control, Exercise, Aerobic, Anaerobic

Core tip: Diabetic patients should be aware that exercise interferes with the glucose homeostasis. Anaerobic exercise can increase glycemia, whereas the aerobic exercise may cause a decrease during the exercise and post-exercise. By evaluating the long-term effect of exercise on glycemic control in type 1 diabetic youths according to the major metabolic pathway involved in energy utilization (aerobic or anaerobic), we found insufficient evidence in the latest literature that any type of exercise or combined aerobic and anaerobic training would clearly improve the glycemic control. The regular physical exercise has several other valuable benefits that justify the inclusion of exercise in pediatric diabetes treatment and care.



INTRODUCTION

Physiological, social and emotional benefits of regular exercise and physically active lifestyle are well documented mostly in a healthy population[1-4], but they are also important for diabetic patients regardless of the type of diabetes[5-8]. For type 1, successful diabetes management is based on individualized insulin therapy, adjusted diet and regular exercise[9].

Exercise used as prevention and therapy in diabetes is not a new concept in the literature. Even the ancient Ayurvedic physician, Susruta Shamita (born around 600 B.C.), noted the reduction in the sweetness of urine from diabetic patients with excecise, and included moderate exercise within his treatment regimens[10]. In 1919, Allen proved that exercise reduced blood glucose level and improved acutely the tolerance to a carbohydrate load[11]. After the discovery of insulin in 1921[12], Lawrence demonstrated that exercise has an effect on insulin requirements and glucose uptake[13]. Joslin believed in “troika” (group of three) in the treatment of diabetes, symbolizing insulin, diet and exercise correlation[14]. Regular exercise helps to improve overall health and fitness, and reduces risk factors for vascular complications. Diabetic youths with regular exercise have improved blood lipid profile, and increased insulin sensitivity, primarily in the skeletal muscles, which leads to a reduced need for insulin[15-17]. The American Diabetes Association recommends all levels of physical exercise including leisure activities, recreational sport and competitive sport for youths with type 1 diabetes mellitus (T1DM) if they are in good blood glucose control and have no long-term complications[18]. Until the sympathetic nervous and endocrine systems control the blood glucose level at the physiological levels during and after physical exercise in healthy subjects[19], the regulation is external in diabetic patients considering many internal influences. Youths with T1DM should be aware that exercise interferes with the glucose homeostasis, although there are individual differences in blood glucose response due to type, duration and intensity of the exercise, the pre-exercise level of counterregulatory hormones, and blood glucose concentrations[20,21]. Several studies examined the role of physical activity and exercise in the treatment of T1DM and considered it an important component. The evidence for improvement in glycemic control is equivocal. Some studies suggest a positive effect[22-27], whereas others fail to show this effect[28-34]. Scientific questions remain concerning what is the exact effect of different types of exercise on glycemic control in youths with T1DM.

In this systematic literature review, we evaluated the latest studies examining the long-term effect of aerobic and/or anaerobic exercise on glycemic control in youths with T1DM. We also made distinguishing between concepts of physical activity, physical fitness, and aerobic-anaerobic exercise. Finally, we considered clinical applications and future directions.

Conceptualisation

Physical activity: Physical activity encompasses body movement produced by skeletal muscles which requires energy consumption[35]. Physical activity can range from sports to any other lifestyle activities including school and out-of-school activities, weekend activities where youths play, are active and expend energy. There is evidence that behavioural patterns of physical activity in childhood are maintained throughout adulthood[36,37]. This term is often used interchangeably with regular exercise and physical fitness in studies, although they are different concepts[38].

Exercise: Exercise has been defined as any form of body movement that results in an increase in metabolic demand with the intention of developing one or more components of physical fitness. It is generally planned, structured and systematic[35]. Regular exercise improves physical fitness. Exercise is characterised by five components: type [dynamic (isotonic) or static (isometric), and both of them can be performed aerobically or anaerobically on the basis of energy utilization][39], intensity (degree of effort that individual puts into exercise), duration (the length of each training session), repetition (number of times individual performs a complete movement of a given exercise) and frequency (number of exercise sessions per week)[40].

Fitness: Fitness refers to the “possession of adequate levels of strength, endurance, and mobility to provide for successful participation in occupational effort, recreational pursuits, familial obligation, and that is consistent with a functional phenotyp expression of the human genotype”[41]. Physical fitness determines cardiovascular, respiratory, and musculosceletal systems in order to perform physically demanding activities such as exercise, sport, or work. Fit youth has normal body fat, good immune system and, in general, is in a physiologic state of well-being.

Aerobic-anaerobic exercise: Whether an activity is aerobic or anaerobic depends primarily on its intensity and duration. Most physical exercises are characterised by both static and dynamic contractions as well as aerobic and anaerobic metabolism. Thus, exercise is classified by their dominant features.

Aerobic exercise includes any type of exercise, typically those performed at moderate levels of intensity for extended periods of time that maintains an increased heart rate. Activities such as cycling, swimming, jogging, rowing, cross-country skiing, and aerobic dancing require oxygen to produce ATP. Regular aerobic exercise improves maximal oxygen consumption and overall endurance performances. Anaerobic exercise is used to promote strength, power, and speed. Generally, anaerobic exercise has a short duration and high intensity activity. Unlike aerobic exercise, it does not depend on exogenous oxygen. Activities such as heavy weightlifting, all types of sprint (running, cycling, or swimming) or any hard exercises require anaerobic metabolism. During exercise various forms of energy sources are utilized markedly depending on the intensity and duration of exercise, but the activity is classified typically based on the predominantly used system. The anaerobic energy system is used for resistance training and increasing speed[42]. During high intensity (anaerobic) exercise almost the entire metabolic fuel source is glucose, whereas during low intensity (aerobic) exercise fat utilization increases and glucose oxidation decrease[43]. Both types of exercise increase the mechanical efficiency of the heart (cardiac adaptation), changes in morphology and functionality of the left ventricle[44].

Measuring the intensity of exercise using maximal heart rate: Maximal heart rate (HRmax) is one of the most commonly used values in clinical settings and physiology. HR increases nearly linearly with the increase in the intensity of exercise; and this is the simplest physiological response to measure. As maximal exercise intensity is approached, HR begins to plateau even as the exercise workload continues to increase. This HRmax is a reliable value and it remains constant for a longer period[45]. To estimate HRmax for children, formula 208 - 0.7 × age in years is applied[46,47]. There are several more and less accurate types of estimation existing for determining the exercise intensity[48]. Aerobic training zone is around between 60%-70% of the HRmax. Between 70%-85% of HRmax, the youths are in the mixed zone, and above 85% of HRmax the anaerobic metabolism will come to the fore.

Effects of different types of exercise on blood glucose level in type 1 diabetes patients

Different types of exercise produce different effects on blood glucose level. If the carbohydrate intake and the insulin dosage are not in line with the exercise the patient does, it will result in metabolic disturbances[49]. The most common problems are the evaluation of pre-exercise level of blood glucose, evaluation of the intensity and duration of the expected exercise, and to take into consideration the time of day when the patient exercises, because of the body’s different physiological insulin need[49]. Exercise functions like insulin, so the balance between the insulin therapy and diet could be facilitated if the daily schedule for exercise and the exercise parameters are consistent[50], although this goal is almost impossible to obtain in the real life for youths. Findings from exercise training studies support the concept that moderate intensity aerobic workload increases the risk of hypoglycemia during the exercise and several hours after the exercise. High-intensity training with anaerobic utilization may increase the blood glucose level due to the release of adrenaline and noradrenalin in the blood, which then stimulates the liver to release glucose faster than normal. The exercise-induced rise in glucose level is followed by hypoglycemia after hours of finishing the exercise as counterregulatory hormone levels decrease[21,51-53]. Both aerobic and anaerobic exercise training regimens improve glucose uptake and insulin sensitivity[21,54]. School-aged children engage a combination of moderate- and high-intensity sessions in their everyday sport activities. Their exercise is often spontaneous and unplanned. Thus, a different plan is needed for each type of exercise to optimize blood glucose level, but problems with the management are well recognised. Patients differ in tolerance to exercise and insulin requirements and it is impossible to give precise guidelines suitable for everyone with T1DM, therefore experiences with regular blood glucose testing are inevitable. Continuous glucose monitoring may assist the active diabetic participants to follow the changes in blood glucose level and give information about the individual response to the exercise[21,54]. There are several guidelines to discuss safe sport participation in children and adolescents with T1DM[5,55-59]. These guidelines can be adjusted to own measurements and awareness of the usual responses to a particular type of exercise.

MATERIALS AND METHODS
Study eligibility

A systematic review was performed in spring and summer 2014 using PubMed/Medline, Google Scholar, Scopus, and ScienceDirect with the following terms: aerobic, anaerobic, high-intensity, resistance, exercise/training, combined with glycemic/metabolic control and type 1 diabetes. Only peer-reviewed articles in English were included published in the last 15 years with at least five subjects per group. Studies were selected from 1999 to 2014 that measured the long-term effect of aerobic and/or anaerobic exercise on glycemic control in type 1 diabetic children, adolescents and young adults without diabetes complications. Glycemic control was measured with glycated haemoglobin A1c (HbA1c). As the HbA1c provides an average of blood glucose control over a 12-wk period, we included studies with an intervention lasting at least 12 wk if the HbA1c was measured before and after the intervention. The flow diagram of study selection is shown in Figure 1.

Figure 1
Figure 1 Flow diagram illustrating selection of the included studies.
Statistical analysis

This manuscript does not describe basic or clinical research using biostatistics for raw data, therefore biostatistics statement is not relevant.

RESULTS

A total of nine articles was evaluated from nine different countries including Australia[30], Tunisia[60], Lithuania[61], Taiwan[62], Turkey[63], Brazilia[64], Belgium[65], Egypt[66] and France[67], and they were published between the years of 2002-2011. The list of articles is presented in Table 1. Across included studies the total sample size was 401 (166 males and 235 females) with an age range of 10-19 years except one study, in which the age range was 13-30 years[64]. Four studies were aerobic-based[60-63], four were combined aerobic and anaerobic programs[30,65-67], and one compared aerobic exercise to anaerobic one[64]. The Turkish study[63] conducted a Pilates program that is considered low-impact aerobic workout[68]. All studies had diabetic control group except one[61].

Table 1 Study characteristics, objective and result regarding glycemic control.
SourceRCTObjectiveSample size/genderAge (y/o) genderInterventionDuration, frequencySignificant positive change in GC
Aouadi et al[60], (2011) TunisianNoEffect of aerobic training on glycemic control and lipid profileEG1: 11 (twice) EG2: 11 (4 times) DC: 11 no exerc12-14 33 MSupervised aerobic exercise3 and 6 mo, twice vs four times a week (60 min)Yes, but only 6 mo with four times a week duration
Sideraviciūte et al[61], (2006) LithuanianNoEffect of long-term physical activity in water on glucose controlEG: 19 (HC: 21)14-19 19 FSupervised aerobic exercise14 wk, twice a week (45 min)Yes
Wong et al[62], (2010) TaiwanNoEffect of home-based exercise programme on HbA1c and peak oxygen uptakeEG: 12 video-, 5 self directed DC: 117-17 8 M, 20 FUnsupervised aerobic exercise12 wk, three times a week (30 min)No
Tunar et al[63], (2012) TurkishYesEffect of pilates training on metabolic control and physical performanceEG: 17 DC: 1412-17 15 M, 16 FSupervised aerobic exercise12 wk, three times a week (40 min)No
Ramalho et al[64], (2006) BrazilianYesEffect of aerobic vs resistance training on metabolic controlEG: 7 DC: 613-30 3 M, 10 FBoth aerobic and anaerobic exercise were supervised12 wk, three times a week (40 min)Sig. increase in aerobic group, not sig. decrease in anaerobic group
D'hooge et al[65], (2011) BelgianYesEffect of combined exercise training on metabolic control, physical fitness and quality of lifeEG: 8 DC: 810-17 7 M, 9 FSupervised combined exercise20 wk, twice a week (70 min)No
Roberts et al[30], (2002) AustralianYesWhether the change of the glycemic control after intervention is dependent on the initiation of quality of glycemic controlEG1: 12 HbA1c > 9% EG2: 12 HbA1c < 9% DC1: 12 HbA1c > 9% DC2: 12 HbA1c < 9%Circa 11-17 24 M, 24 F12 wk supervised 12 wk unsuper-vised combined exercise24 wk, three times a week (45 min)No
Salem et al[66], (2010) EgyptianYesEffect of exercise on glycemic control, plasma lipids, blood pressure, severity and frequency of hypoglycemia, anthropometric measurements and insulin doseEG1: 75 (once) EG2: 73 (3 times) DC: 4812-18 76 M, 121 FSupervised combined exercise6 mo, once and three times a week (70 min)Yes, in both exercise groups
Heyman et al[67], (2007) FrenchYesEffect of exercise on quality of life, physical fitness, body composition, lipid and apolipoprotein profiles, and adiponectin and leptin levelsEG: 9 DC: 713-18 16 FSupervised combined exercise6 mo, 2 h supervised, and 1 h unsupervisedNo
Effects of different types of exercise on glycemic control in youths with T1DM

Studies investigating aerobic exercise: Studies measuring the effect of aerobic exercise on glycemic control presented variable results[60-63]. Only one study recognised a significant improvement in HbA1c after 12-wk exercise (girls swimming twice a week for 45 min a week)[61]. In a study investigating the impact of the frequency of the supervised aerobic training on glycemic control, exercise three times a week (one hour) for three months had no significant impact on glycemic control, but exercise four times a week (one hour) for 6 mo resulted in a significant improvement[60]. Neither guided or self-directed home-based aerobic exercise program nor supervised Pilates exercise had a significant effect on glycosylated haemoglobin after a 12-wk session[62,63].

Study investigating anaerobic exercise: We found only one study that measured the efficacy of resistance (anaerobic) and aerobic exercise in parallel. Both groups were trained three times a week (40 min) for 12 wk under supervision by a physical trainer and an endocrinologist. Interestingly, the HbA1c increased in the aerobic group significantly after 12 wk, whereas a non-significant reduction was observed in the resistance training group[64].

Studies investigating combined exercise program: Four randomised controlled trials examined the effect of combined (aerobic and anaerobic) exercise on glycemic control[30,65-67]. Supervised combined aerobic and resistance training twice a week (70 min) for 20 wk resulted in no significant change in glycemic control[65]. In a 12-wk supervised training followed by a 12-wk unsupervised training, HbA1c level remained unchanged regardless of the baseline HbA1c level[30]. There were two trials that explored the effect of supervised combined exercise on glycemic control for a longer duration (6 mo)[66,67]. The Egyptian study found significant improvements in HbA1c level in both training groups exercising three times a week and once a week. However, patients exercising three times a week produced significantly greater improvements[66]. In the Heyman’s study, the participants completed a two-hour supervised training and a one-hour unsupervised training a week including aerobic and strength exercises. The author could not prove a significant effect on glycated hemoglobin after a 6-mo session[67].

DISCUSSION

The primary aim of diabetes treatment and care is to achieve as stable glycemic control as possible in order to prevent or delay the long-term complications[69]. Regular exercise is recommended for diabetic youths for several psychological and health benefits[7,70]. It is evidence-based that regular exercise has a preventive and curative role in type 2 diabetes, but its physiological role in type 1 diabetes is not fully explored. Exercise physiology in diabetes is described thoroughly by Robertson et al[7] and Riddell et al[53,59]. Another issue that remains unresolved is related to the type of exercise: aerobic or anaerobic workout is most beneficial for glycemic control. We evaluated the studies from the previous 15 years that investigated the long-term effect of exercise on glycemic control in youths with T1DM according to the major metabolic pathway involved in energy utilization (predominantly aerobic or predominantly anaerobic). Results of investigated studies are open to debate. Most studies found no significant improvement in glycemic control regarding the aerobic[62,63] and combined exercise intervention[30,65,67]. The only study investigating the anaerobic effect on glycemic control presented a positive tendency, although there was no statistically significant effect[64]. One of the possible reasons for these varied results could be the small sample sizes. The glucose profile varies greatly in patients with T1DM before, during and after exercise, and can be very different in patients with similar HbA1c. All except one study[66] had less than 20 participants in a group in our studies. The other reason could be the short period. It seems that at least 6 mo of exercise intervention might lead to significant results[60,66]. Kennedy et al[71] also noticed in their systematic review and meta-analysis that longer duration of intervention shows a trend for HbA1c reduction. We had a total of 401 samples in our studies and the Egyptian study[66] alone offered 187 participants. Weighting its results, it might be supposed that combined long-term exercise intervention is more beneficial for the glycemic control, than aerobic or anaerobic alone. Irvine et al[72] in their systematic review with 372 patients with T2DM have reported that (anaerobic) progressive resistance exercise is not significantly better than aerobic exercise in improving glycosylated haemoglobin. There was a lack of evidence to suggest that one type of exercise was better than another[72]. Yang et al[73] in their systematic review with 595 patients with T2DM also enunciated that either form of exercise appears to have comparable effects on glycemic control. A meta-analysis by Tonoli et al[74] with type 1 diabetic participants explored a tendency for improvement in glycaemic control due to aerobic or combined training, but they could not confirm this statistically. Individual studies on aerobic training had no significant evidence, but “in total” demonstrated a reduction in HbA1c, although they carefully interpret their results because of insufficient data on these topics[74]. Neither Kennedy’s meta-analysis in children and adults[71] nor Kavookjian’s systematic review in the adult population[75] revealed evidence for statistically significant glycemic benefits of exercise. Kennedy et al[71] suggest that HbA1c may not be a sensitive indicator of glycaemic control, and that improvement in glycaemic variability may not be reflected in this measure. Tight metabolic control is very important for diabetic individuals, and the regular physical exercise is part of the diabetes management. Available studies provide insufficient evidence that any type of exercise or combined training would clearly improve the glycemic control in type 1 diabetic young patients. Long-term exercise-induced glycemic benefits are based on the continuous effect of each successive bout of exercise. Glycemic variability can be detected by continuous glucose monitoring that could help individuals to learn their own response to different type of physical exercise; and it might be a more appropriate marker to explore the exercise-induced beneficial effect than HbA1c[71]. Youths with T1DM are recommended to be engaged in a sport they like, and do it regularly as much as possible at the same period of the day. Having the appropriate exercise physiology knowledge, they can accumulate own experiences regarding exercise in addition to insulin requirement and dietary program that may result in stable glucose levels. The insulin-diet-exercise adjustment must be personalized and discussed with the patient’s endocrinologist. The regular exercise is associated with numerous health benefits and chronically ill youths enjoy the same benefits as the healthy counterparts[1,70].

There are miscellaneous results regarding the long-term effect of various forms of exercise on glycemic control. Meta-analyses also suffered from the insufficient randomised controlled trials with greater sample sizes to examine the short- and long-term effect of glycemic control on different exercise modalities in youths with T1DM. Patients and health professionals may want more information they currently received, but there are concerns that the results would be overestimated. Different forms of exercise generate different skills in youths. They need a comprehensive form of exercise to help their healthy many-sided physical development. Diabetic patients should be aware that glycemic control is influenced by multiple factors (initial blood glucose level, insulin absorption, time of the day), and shows individual responses to exercise. It is advisable that young patients choose some kind of sports or physical exercise they like and be engaged with it for a longer time. Clinical treatment and management should be adjusted to the exercise form and the diabetic patients should acquire how to change nutrition and insulin dose according to their daily physical exercise. Patients who can monitor themselves intensively around periods of activity can learn how to keep glucose levels in an acceptable range.

Although current studies have insufficient evidence of the beneficial effect of any type of exercise on glycemic control, any type of regular physical exercise has several other valuable physiological and health benefits that justify the inclusion of exercise in pediatric diabetes treatment and care.

ACKNOWLEDGMENTS

This research was partially carried out with the contribution of the Workgroup for Health Sciences, Center of Excellence of Applied Materials Science and Nano-Technology at the University of Miskolc.

COMMENTS
Background

Regular exercise is recommended for diabetic youth for several psychological and health benefits, but its physiological role in type 1 diabetes is not fully explored. So far, there are only few studies evaluating the long-term effect of different types of exercise on glycemic control.

Research frontiers

In this systematic literature review, the authors evaluated the latest studies examining the long-term effect of aerobic and/or anaerobic exercise on glycemic control in youths with type 1 diabetes. They also made distinguishing between concepts of physical activity, physical fitness, and aerobic-anaerobic exercise.

Innovations and breakthroughs

Most studies found no significant improvement in glycemic control regarding the aerobic and combined exercise intervention. The only one study evaluating anaerobic exercise observed a non-significant reduction in glycemic control. It might be supposed that longer duration (at least 6 mo) and more frequent (more than twice a week) exercise has a positive effect on glycemic control, but it is not proved yet.

Applications

Although current studies have insufficient evidence of the beneficial effect of any type of exercise on glycemic control, any type of regular physical exercise has several other valuable physiological and health benefits that justify the inclusion of exercise in pediatric diabetes treatment and care.

Terminology

Aerobic exercise includes any type of exercise, typically those performed at moderate levels of intensity for extended periods of time that maintains an increased heart rate. Anaerobic exercise is used to promote strength, power, and speed. Generally, it has a short duration and high intensity activity. Unlike aerobic exercise, it does not depend on exogenous oxygen.

Peer-review

The manuscript covers an important topic in type 1 diabetes management. The contribution that the manuscript provides is an overview of the dearth of scientific evidence to support exercise intervention in this population.

Footnotes

P- Reviewer: Faulkner MS, Sanlioglu AD S- Editor: Ji FF L- Editor: Wang TQ E- Editor: Liu SQ

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