) Physical Exercise for Type 1 Diabetes Mellitus Cochrane Database of Systematic Reviews

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Does Do Improve Glycaemic Control in Type 1 Diabetes? A Systematic Review and Meta-Analysis

• Amy Kennedy,
• Krishnarajah Nirantharakumar,
• Myriam Chimen,
• Terence T. Pang,
• Karla Hemming,
• Rob C. Andrews,
• Parth Narendran

x

• Published: March 15, 2013
• https://doi.org/10.1371/journal.pone.0058861

Figures

Abstruse

Objective

Whilst regular exercise is advocated for people with type one diabetes, the benefits of this therapy are poorly delineated. Our objective was to review the evidence for a glycaemic benefit of exercise in type one diabetes.

Enquiry Pattern and Methods

Electronic database searches were carried out in MEDLINE, Embase, Cochrane'southward Controlled Trials Register and SPORTDiscus. In addition, nosotros searched for as nevertheless unpublished only completed trials. Glycaemic do good was defined as an comeback in glycosylated haemoglobin (HbA1c). Both randomised and non-randomised controlled trials were included.

Results

Thirteen studies were identified in the systematic review. Meta-analysis of twelve of these (including 452 patients) demonstrated an HbA1c reduction merely this was not statistically significant (standardised mean difference (SMD) −0.25; 95% CI, −0.59 to 0.09).

Conclusions

This meta-analysis does non reveal evidence for a glycaemic do good of exercise as measured past HbA1c. Reasons for this finding could include increased calorie intake, insulin dose reductions around the time of exercise or lack of power. We likewise suggest that HbA1c may not exist a sensitive indicator of glycaemic command, and that improvement in glycaemic variability may not be reflected in this measure. Practise does nonetheless have other proven benefits in blazon 1 diabetes, and remains an important part of its management.

Citation: Kennedy A, Nirantharakumar Thousand, Chimen M, Pang TT, Hemming M, Andrews RC, et al. (2013) Does Exercise Improve Glycaemic Control in Blazon 1 Diabetes? A Systematic Review and Meta-Assay. PLoS I 8(3): e58861. https://doi.org/10.1371/journal.pone.0058861

Editor: Andrea Vergani, Children's Hospital Boston, United states of america

Received: Oct 18, 2012; Accustomed: February 7, 2013; Published: March xv, 2013

Copyright: © 2013 Kennedy et al. This is an open up-admission commodity distributed under the terms of the Artistic Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original writer and source are credited.

Funding: The authors have no support or funding to study.

Competing interests: The authors accept read the journal's policy and have the following conflicts: AK has received sponsorship to nourish a scientific meeting from NovoNordisk, RA has been on the informational board for GSK, received honorariums and/or sponsorship to attend a scientific meeting from NovoNordisk, GSK, Sanofi Aventis and Lilly, KH has been an good witness in several legal cases, and PN has received advisory board invitations and speaker honorariums from NovoNordisk. This annunciation of interest does not change the authors' adherence to all the PLOS ONE policies on sharing data and materials.

Introduction

The current UK guidelines for do and physical activity are that all individuals undertake at least 150 minutes of moderate-intensity, or 75 minutes of high-intensity, aerobic physical activity per week. [i] The American Diabetes Clan (ADA) has similar recommendations for all people with diabetes. [2] The evidence base of operations for these recommendations for patients with diabetes is fatigued largely from studies of the general population and those with type 2 diabetes. [iii] Studies on the benefits of exercise in blazon 1 diabetes are less robust.

The currently recognised wellness benefits of exercise in blazon ane diabetes have been reviewed previously. [iii] To date, there is bear witness that exercise improves physical fitness, insulin resistance, lipids and macrovascular adventure in people with type 1 diabetes. [iii] However, the results of studies on exercise and glycaemic control are alien. Information technology is of import to analyze this consequence because glycaemic command is considered by both patients and health care professionals to exist the mainstay of type i diabetes management. Furthermore, and in contrast to studies in blazon 1 diabetes, a diverseness of unlike forms (aerobic/resistance) of exercise have a demonstrable do good on glycaemic control in type 2 diabetes [four], [v].

Here, we perform a systematic review and meta-analysis of randomised controlled and not-randomised parallel group trials of exercise training and glycaemic do good in blazon 1 diabetes. Nosotros utilise glycosylated haemoglobin (HbA1c) as the measure of glycaemic control.

Methods

Data Sources and Searches

The electronic databases searched were MEDLINE (Ovid), Embase (Ovid), Cochrane library (Wiley) and SPORTDiscus (EBSCO) up until August 2011. An updated search of Medline was performed up until May 2012. A diversity of search terms were used for individuals with type ane diabetes (population) and concrete activity (intervention). We did not restrict our search to the issue or report design to maximise the sensitivity of our search. Nor did nosotros place whatever date or language restrictions. Our secondary search strategy included scanning bibliographies of the retrieved manufactures and searching for unpublished studies using key trial registries (clinicaltrials.gov, Current Controlled Trials Registry, WHO hosted International Clinical Trials Registry Platform - ICTRP). The primary search strategy is outlined in the Appendix S1. The systematic review and meta-assay is reported co-ordinate to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [vi].

Study Choice

Inclusion criteria were defined based on population, intervention, comparator, outcome and study design. Population were adults and children with type 1 diabetes. Where the studies reported data for both type one and 2 diabetes, authors were contacted to obtain information for type 1 diabetes alone. Interventions that aimed to increase the practise through either supervised or unsupervised preparation were included. We did not exclude studies based on the intensity or type of exercise. Only trials that involved a not-intervention group of participants with type ane diabetes were included. Studies where any other intervention was given to the participants (e.one thousand. dietary intervention) were simply included if they were given to both intervention and control arms. We included both randomised and not randomised parallel controlled trials.

The primary outcome measure was change in HbA1c, with HbA1c data extracted before and afterwards the intervention. In those studies where complete HbA1c data was non reported, we contacted the authors for clarification. Our secondary event measure out was adverse events (hypoglycaemia).

Data Extraction and Written report Quality

Initial selection was based on title and abstract. The original article was obtained where it was unclear whether the study met our inclusion criteria. Two reviewers (AK and MC) selected the studies independently. Where there was disagreement between the 2 reviewers, resolution was through a meeting with PN and KN. Reasons for exclusion were documented and are bachelor from the authors on request. Where necessary, strange language papers were translated.

A data extraction and quality assessment form was developed based on the template suggested by Centre for Review and Dissemination (CRD) for systematic reviews in their guidelines [7] Data extraction was performed by AK and checked by KN for accurateness and for any missing information. Extracted data included details of the study population, intervention characteristics, outcome measures, and areas of potential bias. Biases evaluated in randomised controlled trials (RCT) included acceptable sequence generation, satisfactory allocation concealment, follow-up and exclusion biases, blinding of consequence assessors and intention to treat analysis. In not RCTs we evaluated any baseline differences in participants, biases in resource allotment, follow-up and exclusion and if belittling method was specified in the study protocol.

Data Synthesis and Analysis

Each of the trials measured the outcome (HbA1c) both earlier and after the intervention period, and for both control and intervention arms. Trials did not report paired difference summary statistics and so we could not obtain paired difference measures. Rather, information technology was necessary to extract information on hateful, standard deviations, and number of participants both before and later on the intervention period and for both intervention and control arms for each trial. For trials which reported the standard mistake of the mean (SEM), nosotros converted this to a standard deviation (SD) by multiplying by the square root of the number of participants in that arm. Any studies that only reported median values without any measure of variation (such as inter-quartile range) could not be included in the analysis.

For whatever trials which were multiple intervention arm trials we extracted and summarised the trial information for each arm. We then combined the intervention arms into a single combined arm by estimating the weighted mean values (both earlier and later on) and estimating the weighted SD using the usual pooled standard SD [9]. A like arroyo was taken where there were two control arms.

From the estimated mean and SD values for HbA1c both before and later the intervention menstruation, nosotros then estimated the hateful difference (afterwards-before) and SD in both the control and intervention artillery. It was necessary to estimate the SD for these modify furnishings as no estimates of correlation (or SDs of changes) were reported in the original trial reports. We used a conservative estimate for the correlation (0.5) as advocated [viii].

All trials reported on the outcome HbA1c. However, because HbA1c-DCCT standardisation simply occurred in 1997, we summarised handling effects using the standardised mean departure (SMD) of Hedges adapted 1000 [9].

Clinical, methodological and statistical heterogeneity were explored. Clinical heterogeneity was explored by because the clinical diversity of the written report participants in terms of their age and study elapsing. Methodological heterogeneity was explored past exploring variations in randomised and non randomised studies. Statistical heterogeneity was tested using Cochran's Q, a statistic based on the chi-square test and quantified by the I-square test. Results were and so pooled across studies using a random effects meta-analysis (since the degree of heterogeneity was also large to warrant a stock-still furnishings assay) using the generic changed variance method. Nosotros pooled over all studies within the subgroups of kid and developed studies. We further investigated the effect of age and duration of intervention by including the pooled (over control and intervention arms) weighted hateful age and duration as covariates in a meta-regression model. Residual levels of heterogeneity were investigated by comparing I-squared values before and later on adjustment for covariates (age and duration).

Risk of pocket-sized study bias (or publication bias) was explored using the contour enhanced funnel plot, stratifying by age of study population (adult or kid) and was further evaluated by the Egger test.

Results

The database searches identified a total of three,740 potentially relevant papers (effigy one). One further paper was identified through follow-upwardly of a conference abstract (identified in the original searches). After removing duplicates and screening by considering titles and abstracts, 94 total-text articles were assessed. Of these, xiv studies met the pre-determined inclusion criteria. I study [x] did not written report separate results for subjects with type ane diabetes and these were not available afterward contacting the authors. Hence, thirteen studies were considered suitable for inclusion in the systematic review. The trials included both adults and children (Table ane), with nine of the 13 trials recruiting children and young adults (nether 18 years of historic period). Many studies involved merely aerobic practice (9/13), three studies involved both aerobic and resistance activities, and i did not specify the exercise type.

Of the thirteen included studies, 8 were randomised controlled trials. Randomisation procedures were not reported in any of these studies. In one written report the reported randomisation method (alternate subjects assigned to each group) resulted in it beingness classified as not-randomised parallel group trial for the purposes of this review. [11] In one study [12], the randomisation process was carried out prior to consent beingness sought. Allocation concealment and blinding were simply reported in 1 study. [13] Losses to follow-up and exclusions were documented in all studies. Of the eight RCTs included in this study, five were analysed according to the intention to treat principle. Iv out of the v not-randomised parallel group trials used a protocol based assay. Adherence to the training plan was not reported in v studies. Where information technology was reported, adherence ranged between 62 and 100%. 'Quality' measures of the included studies are listed in Table 2.

Exercise and HbA1c

The report past D'Hooge et al [xiii] could not exist included in the meta-analysis because median HbA1c without interquartile range was reported. This study reported a 0.1% fall in median HbA1c in the intervention group and a 0.2% fall in control group with exercise.

The remaining 12 studies (452 patients) were included in the meta-assay. The overall, pooled information showed a not-significant SMD reduction in HbA1c of −0.25% with exercise training (95% CI, −0.59 to 0.09; p = 0.144; I-squared = 57.0%, Figure 2). A greater SMD reduction in HbA1c was seen in the eight studies of children and young adults, merely here too this was not significant (SMD, −0.37; 95% CI, −0.77 to 0.02; p = 0.066; I-squared = 57.2%). No effect was seen in developed studies, of which there were four, (SMD, 0; 95% CI, −0.five to 0.v; p = 0.998; I-squared = 23.five%).

In sensitivity analysis, there was no clan between report design and HbA1c reduction: SMD for randomised studies was −0.24 (95% CI −0.71 to 0.23) and for non-randomised studies −0.25 (95% CI −0.59 to 0.09). The degree of heterogeneity observed in the randomised studies was I-squared = 66.4% whereas this was lower in the non-randomised studies (I-squared = 33.iv%).

Meta regression of HbA1c confronting length of study duration suggested a non-significant association between HbA1c reduction and longer intervention (regression co-efficient, −0.034; 95% CI, −0.084 to 0.016; p = 0.163, figure 3A). Similarly, at that place was a non-significant association of HbA1c and increasing historic period (regression co-efficient, 0.024; 95% CI, −0.013 to 0.060; p = 0.179, figure 3B). The I-squared value before adjustment for co-variates was 57%, and reduced to l.4% afterward adjustment for age; and to 34.2% afterwards adjustment for duration.

The funnel plot (figure S1) suggests evidence of small study or publication bias with under representation of studies reporting negative effects (Eggers test p value = 0.003).

Practise and Agin Events

Hypoglycaemia frequency was mentioned in but five studies. [eleven], [13]–[16] One study [fourteen] reported a similar frequency of hypoglycaemia in both the intervention and control grouping. Campaigne et al [xvi] reported only one episode of hypoglycaemia, which occurred during a grooming session. Salem et al [15] found no difference in hypoglycaemia rates between the groups exercising once or three times per calendar week, only did non comment on the hypoglycaemia frequency in the control group. Conversely, Yki-Jarvinen et al [11] found that hypoglycaemia rates were increased in the first 2 weeks of the training program but diminished thereafter, and D'Hooge et al [13] reported frequent hypoglycaemia episodes both during and later practice in the intervention group.

Word

This meta-analysis does non reveal a glycaemic benefit of exercise in people with type ane diabetes. However, sub-analyses suggests that exercise may confer a glycaemic benefit in the young, and when undertaken for longer periods. Whilst agin event reporting was poor, these studies demonstrate that exercise tin can be undertaken by people with type 1 diabetes without significant hypoglycaemia. This is of import considering qualitative studies take previously reported hypoglycaemia to be a barrier to practise in type 1 diabetes [17], [18].

We used predetermined inclusion criteria designed to identify as many relevant studies as possible, and conducted this assay in accordance with PRISMA guidelines. [6] However, this study is limited by the availability and quality of the obtained data. We were unable to obtain the necessary data from all identified trials, either because the information was not presented in a mode that enabled extraction for assay or because nosotros were unable to contact the authors of the report. There is evidence from our analysis that studies showing a negative effect of practise on glycaemia may not have been published (or identified during our search of unpublished trials), and so that the effect size shown in this meta-analysis is perhaps overestimated.

At that place was considerable variation in the intervention (form and intensity of exercise, elapsing of intervention), which may have contributed to the heterogeneity of study results. Withal, ADA guidance on exercise for people with type 1 diabetes is express only to elapsing and intensity [ii], therefore, inclusion and comparison of studies with unlike exercise interventions is, in our opinion valid.

There are a number of potential explanations for the findings of this meta-analysis. Firstly, the programmes of exercise may not have been of sufficient duration. This is supported by our sub-analysis which shows a trend for HbA1c reduction with longer duration of intervention. Based on pooled data from these studies, and bold that the charge per unit of glycaemic benefit persists in a linear style, nosotros approximate that studies of greater than 25 weeks duration would be needed to obtain an HbA1c reduction in the region of 0.5%. This has implications for the design of future trials. Secondly, as has been demonstrated in some studies of type two diabetes, [19] the intensity of the exercise program may be important. Inadequate reporting of practice intensity in the current type one diabetes studies makes this difficult to analyse. Increased calorie intake, either every bit a source of fuel to manage hypoglycaemia or every bit a reward, is another possible reason why our analysis failed to detect a glycaemic benefit of practise. The interventions in the current studies were associated with additional sugar intake, and this is in line with ADA guidance as a means of avoiding hypoglycaemia. Notwithstanding diet in general was poorly recorded in these studies. Laaksonen et al [20] did endeavor to record dietary intake. In those participants where this was achieved, dietary intake appeared similar betwixt training and control groups. There is therefore a need for studies in which dietary intake is controlled for, or calorie intake clearly recorded. In that location have been studies of combined nutrition and exercise interventions [21] which were excluded from our analysis as the dietary advice was given to the training arm alone. This written report did show an HbA1c reduction with combined dietary and physical action (viii.9±2.6 to 8.6±two.1% vs viii.7±2.0 to eight.8±2.3% in the control arm), although it did not reach significance. Insulin dose aligning is another approach to avoiding hypoglycaemia around exercise, and a reduction in insulin dosage may business relationship for the absenteeism of a reduction in HbA1c. Of the 11 studies that reported insulin dosage pre- and post-training, five reported a decrease in insulin requirement. [xi], [13], [15], [22], [23] Those studies with two intervention artillery [15], [22] both reported greater insulin dose reductions in the higher intensity arms. However, half-dozen studies reported no significant modify in insulin dose with their grooming intervention and just two of these reported a reduction in HbA1c. [16], [24] These studies therefore fail to clarify whether the lack of glycaemic do good of exercise tin be attributed to changes in diet or insulin dose.

HbA1c has been used as a measure of glycaemic control in our assay but this may not be the most advisable measure of glycaemic command. To illustrate, glycaemic variability has been suggested to contribute to the development of microvascular complications in type ii diabetes. [25] Unfortunately, none of the exercise studies in our assay have examined glycaemic variability. In that location is recent evidence from patients with insulin treated blazon 2 diabetes that the time spent in hyperglycaemia is reduced in the 24 hrs following exercise (without an increase in hypoglycaemia), [26]. Conversely in type 1 diabetes, wide blood glucose variability has been reported effectually exercise in the few studies that have been conducted [27].

In contrast to our results, a contempo meta-assay by Tonoli et al [28] reported a pregnant but small-scale HbA1c lowering effect of exercise in type 1 diabetes (Cohen's d −0.27;95% CI −0.06 to −0.47). This paper however used different criteria for written report selection. It included studies with no control group, or control subjects without diabetes. We purposefully excluded these trials to control for the effect of participation in a clinical trial. Our meta-assay also included studies that were excluded in the Tonoli analysis [11], [14], [15], [16], [22], [23], [24]. We believe these differences accounts for the differing conclusions of the two meta-analyses. Tonoli et al [28] did however concord that studies of strength grooming exercises showed no overall improvement in glycaemic command.

Overall there is a lack of large well-conducted studies on glycaemic benefits of exercise in type one diabetes. Our systematic review identified thirteen studies, from which data on 452 patients has been used for assay. In contrast, a recent meta-analysis of do intervention in type 2 diabetes (which did detect an HbA1c lowering effect) analysed 47 RCTs including more than than 8500 patients. [4] Farther research is therefore required to demonstrate a glycaemic do good of do in blazon i diabetes. Nosotros would suggest the following areas are worth because when designing this inquiry.

1. designing larger trials lasting at to the lowest degree six months
2. trial blueprint that is randomised and well controlled (with matched type 1 diabetic subjects and recording of dietary intake)
3. examining the effect of practise on glycaemic variability
4. examining the event of exercise intensity, and the incorporation of a dietary programme on glycaemic benefit
5. examining the consequence of age and duration of diabetes on glycaemic do good

Whilst this meta-analysis did not detect a glycaemic benefit to exercise, there are other well defined benefits in type one diabetes. These include reduction in macrovascular risk, bloodshed, and comeback in wellbeing. [iii] Therefore, we suggest practice should keep to play an important role in the management of blazon 1 diabetes, whilst its glycaemic benefits are more thoroughly investigated.

Supporting Information

Author Contributions

Designed study: AK KN MC TP KH RA PN. Performed searches and reviewed articles: AK KN MC PN. Analyzed the information: AK KN TP KH. Contributed reagents/materials/analysis tools: KN KH. Wrote the paper: AK KN MC TP KH RA PN.

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