- Email: [email protected]
Glycemic reductions following water- and land-based exercise in patients with type 2 diabetes mellitus
Accepted Manuscript Glycemic reductions following water- and land-based exercise in patients with type 2 diabetes mellitus Rodrigo Sudatti Delevatti, Carolina Dertzbocher Feil Pinho, Ana Carolina Kanitz, Cristine Lima Alberton, Elisa Corrêa Marson, Luciana Peruchena Bregagnol, Salime Chedid Lisboa, Beatriz D. Schaan, Luiz Fernando Martins Kruel PII:
S1744-3881(16)30039-1
DOI:
10.1016/j.ctcp.2016.05.008
Reference:
CTCP 655
To appear in:
Complementary Therapies in Clinical Practice
Received Date: 7 March 2016 Revised Date:
8 May 2016
Accepted Date: 9 May 2016
Please cite this article as: Delevatti RS, Feil Pinho CD, Kanitz AC, Alberton CL, Marson EC, Bregagnol LP, Lisboa SC, Schaan BD, Kruel LFM, Glycemic reductions following water- and land-based exercise in patients with type 2 diabetes mellitus, Complementary Therapies in Clinical Practice (2016), doi: 10.1016/j.ctcp.2016.05.008. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT PAGE TITLE
Title: Glycemic reductions following water- and land-based exercise in patients with
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type 2 diabetes mellitus
Rodrigo Sudatti Delevatti1,2, Carolina Dertzbocher Feil Pinho1, Ana Carolina Kanitz1,3, Cristine Lima Alberton4, Elisa Corrêa Marson1, Luciana Peruchena Bregagnol1, Salime
1
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Chedid Lisboa1, Beatriz D. Schaan5,6, Luiz Fernando Martins Kruel1
Exercise Research Laboratory, Department of Physical Education, Universidade
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Federal do Rio Grande do Sul, Brazil. 2
Faculdade Sogipa de Educação Física, Brazil.
3
Faculty of Physical Education, Universidade Federal de Uberlândia, Minas Gerais,
Brazil. 4
Department of Physical Education, Federal University of Pelotas, Rio Grande do Sul,
Brazil.
Endocrine Division, Hospital de Clinicas de Porto Alegre, Rio Grande do Sul, Brazil.
6
Internal Medicine Department. Faculty of Medicine, Universidade Federal do Rio
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Grande do Sul, Brazil.
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5
Author for correspondence: Rodrigo Sudatti Delevatti.
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Felizardo Street, 750, Swimming Center, 18 room. Postal code: Porto Alegre, RS, Brazil Fone/Fax: 55 51 3308-5820 E-mail: [email protected]
ACCEPTED MANUSCRIPT 1 Abstract Purpose: To assess the acute glucose responses to the first sessions of three mesocycles of water- and land-based aerobic exercise. Methods: The water-based exercise group (WBE, n=14; 54.1 ± 9.1 years) performed deep water walking and/or running, while the land-based exercise group (LBE, n=11; 60.1 ±
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7.3 years) performed walking and/or running on athletic track. In the first mesocycle, patients trained at 85-90% of their anaerobic threshold (AT) for 35 minutes, progressing to 90-95% of the AT in the second mesocycle, and 95-100% of the AT in the last mesocycle. Capillary glucose was assessed before and immediately after the first session of each mesocycle. Results: There was glycemic
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reduction (p < 0.001) in all sessions, with relative reductions of 19%, 29% and 24% for the WBE and 24%, 29% and 27% for the LBE in the mesocycles 1, 2 and 3, respectively. There were not found differences between groups and between mesocycles. Conclusions: The acute response of blood
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glucose to aerobic training between 85 and 100% of the heart rate of AT is effective and independent of the environment in which it is performed. Clinical trial reg. no. NCT01956357, clinicaltrials.gov.
Keywords: Exercise, Diabetes Mellitus, Glycemia.
1. Introduction
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Most current treatments for type 2 diabetes involve physical activity and dietary modifications in addition to medical management, all of which are crucial for glycemic control [1]. Structured and supervised training programs have been found to have a greater impact on glycemic control than general increases in physical activity alone [2]. Aerobic training is found to produce both acute and
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chronic benefits for these patients, including metabolic and cardiovascular beneficial effects, as well as higher quality of life and wellbeing [3-7]. It can be performed in different ways (cycling, running,
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walking, rowing, stepping and others), differing in terms of total recruited muscle mass, type of impact or energy expenditure, which may be of important for patients with diabetes [8]. Few studies analyse the effects of different modes of aerobic exercise on glucose levels in type 2 diabetes. Running is one of the most studied modalities of aerobic exercise; however, the progression of training variables such as duration and intensity may expose patients to moderate to high impact forces on their musculoskeletal system. Importantly, as patients with diabetes are prone to chronic complications, including peripheral neuropathy that increases risk of foot lesions, it is important to find alternatives for the progression of training. Different environments where exercise training is performed could minimize injuries and ulcerations caused by the impact directly absorbed in the foot in contact with the
ACCEPTED MANUSCRIPT 2 ground. Alternative forms of exercises for patients with diabetes are those performed in water, where the impact forces can be attenuated, especially for the lower limbs [9]. Among the modalities of aerobic exercise performed in aquatic environment, water aerobics can be highlighted, as the ground reaction force can be reduced by up to 1.2 times the body weight [10]. Moreover, deep-water running is another
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interesting modality because the practitioners perform aerobic exercise at high loads with reduced risk of injury, as a float vest is used, keeping the body in an upright position, preventing contact between the feet and the bottom of the pool [11].
Some small studies have addressed the possible metabolic benefits of exercise performed in the
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aquatic environment, but the results were inconclusive, especially because of the quasi-experimental design of the study [12] and small sample of individuals evaluated [12,13]. Moreover, comparisons of exercise training glycemic effects in patients with type 2 as performed on land or in water, is a yet few
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discussed subject. Recently, a randomized clinical trial [14] demonstrated similar glucose control, by HbA1c levels, after aquatic or dry-land aerobic training in patients with type 2 diabetes. Despite of the clinical importance of this finding, to our knowledge, studies with similar design (water- versus landbased exercise) analyzing acute glycemic effect in this population have not been conducted. Although long-term glycemic control is the primary goal of diabetes treatment [1], knowledge regarding the acute impact of exercise on glucose responses in this population is crucial in ensuring the
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safety and quality of exercise interventions, as chronic glucoregulatory benefit of exercise training is the result of the added effects of each bout of exercise [15]. However, studies with this objective often compare different sessions, differing in relation to the training variables in a particular state of trainability. This provides knowledge of the isolated impact of a session, in which the increased
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intensity, increased volume and the consequent change in the state of trainability can change the magnitude of glycemic reduction. Therefore, the present study aimed to analyze the acute glucose
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responses in the first sessions of three mesocycles of aerobic training periodization. Additionally, the present study aimed to analyze the acute glucose responses to aerobic training in water as compared to similar training performed on land. We hypothesized that the magnitude of glycemic reduction is maintained during a periodization with progression of intensity, that is, no differences would be observed among mesocycles. We hypothesized that the training in water would provide glycemic reductions similar to those derived from training on land.
2. Material and methods 2.1 Subjects
ACCEPTED MANUSCRIPT 3 All participants were fully informed of the procedures involved in the study, and provided written consent prior to participation. The study was conducted in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans and was approved by the Research Ethics Committees of the Universidade Federal do Rio Grande do Sul
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(protocol number 108.997) and of the Hospital de Clínicas de Porto Alegre (protocol number 54475). The sample consisted of 25 patients with type 2 diabetes (14 men) who had not undertaken any physical exercise in the previous three months and were receiving their usual medical treatment. Patients were identified from the records of the Endocrine Division of a tertiary hospital and also were
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recruited through advertisements in local newspapers between June and July 2012. They were randomly assigned to water-based (WBE; n=14) or land-based exercise (LBE; n=11), by picking an envelope with predefined group numbers, stratified according to gender. Patients with the following
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conditions were excluded from the sample: uncontrolled hypertension, autonomic neuropathy, severe peripheral neuropathy, proliferative diabetic retinopathy, severe nonproliferative diabetic retinopathy, decompensated heart failure, limb amputations, chronic renal failure (MDRD-GFR < 30 ml/min) [16] or any muscle or joint impairments which prevented individuals from engaging in physical exercise. The presence of these conditions was confirmed by medical history as well as clinical and laboratory examinations. All patients had undergone electrocardiogram (ECG) stress testing in the six months
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preceding the study.
2.2 Anthropometric measurements
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Prior to the intervention, patients underwent anthropometric measurements at our exercise research laboratory. Body mass and height were assessed using a digital scale and a stadiometer
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(FILIZOLA; São Paulo, Brazil). These values were used to calculate patient body mass index (BMI) using the following formula: mass (kg)/height² (m). Waist circumference was measured at the midpoint between the iliac crest and the last rib.
2.3 Capillary glycemia
Capillary glycemia was assessed before and immediately after the first session of each training mesocycle using a clinical glucometer (Accu-Check Performa, Roche, São Paulo, Brazil), which
ACCEPTED MANUSCRIPT 4 assesses glycemic levels in approximately 5 seconds and an Accu-Chek – Multiclix lancet device (São Paulo, Brazil).
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2.4 Intervention
Patients underwent 9-week training programs involving deep-water walking or running with a life vest (WBE group) or walking or running on an athletic track (LBE group). Both groups underwent interval-training programs consisting of a three-week adaptation period followed by three mesocycles
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of three weeks each. Training was conducted three times per week (Monday, Wednesday and Friday), and each 45-minute session was divided into a warm-up period (5 min), followed by the main training program (35 min) and a cool down section (5 min). The intensity of the exercise prescribed was
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adjusted according to each subject heart rate deflection point, which was determined by progressive exercise tests conducted in the water [17] or on land [18] for the water- and land-based groups, respectively. This method was chosen due to its ease of application and association with the second ventilatory threshold in patients with type 2 diabetes [18], a precise indicator of the relative stress caused by exercise [19]. The HRDP was observed in the HR-by-intensity graph. The analysis were carried out by two independent, blinded, experienced exercise physiologists. Participants were asked to
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wear heart rate (HR) monitors (RSX 300, Polar) during exercise to control training intensity. Each individual was asked to read and report their HR to one of the three teachers who supervised the waterand land-based exercise sessions. Each teacher then used a table containing subjects' training HR ranges to provide feedback on the recommended exercise intensity for each patient. The 9-week
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training program prescribed to each participant is described in table 1.
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Table 1. Nine-week aerobic training program. Mesocycle
Week
Training sessions
1
1* - 3
7x (4 min 85 at 90% ATHR with/ 1min at <85% ATHR)
7x (4 min 90 at 95% ATHR with/ 1min at <85% ATHR) 2 4* - 6 7x (4 min 95 at 100% ATHR with/ 1min at <85% ATHR) 3 7* - 9 Note: ATHR: Anaerobic threshold heart rate; *weeks in which capillary glycemia was assessed.
Duration (main part) 35 min 35 min 35 min
2.5 Statistical analysis Patients’ characteristics data are presented as mean and standard deviation or median and interquartil range (P25-P75) for continuous variables and by number of patients (n) for categorical
ACCEPTED MANUSCRIPT 5 variables. Baseline comparisons were performed using Student’s t-test and U of Mann Whitney for continuous variables and by Fisher’s exact test for categorical variables. A generalized estimation equation (GEE) was used to assess reductions in glucose levels in different mesocycles and different environments of training; considering the three factors involved in
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the analysis (time, mesocycle, and group). As the model of training in both groups was identical, an analysis was also conducted without the group factor (time, mesocycle), aiming only to assess reductions in glucose levels in different mesocycles of the training periodization. The three factors (time, mesocycle, and group) and two factors (time and mesocycle) analysis were performed with all
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patients and excluding the insulin users. Multiple comparisons were performed with the Bonferroni correction. The level of significance was set at α < 0.05. All analyses were performed using the
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Statistical Package for the Social Sciences (SPSS) software, version 19.0.
3. Results
3.1. Patients’ characteristics
Patients’ characteristics regarding disease duration, age, anthropometric measurements and medications use are showed in table 2. Only BMI was higher in WBE group at baseline. For the other
profile.
Table 2. Patients’ characteristics.
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anthropometric measurements, disease duration, age and medications used, the groups showed a similar
LBE (n = 11) 5/6
p 0.695
54.3 ± 9.1
60.1 ± 7.3
0.102
5.4 ± 3.7
8.4 ± 5.8
0.134
6.4 (6 – 9.8)
6.1 (6.0 – 7.8)
0.536
34.5 ± 3.9
29.9 ± 3.6
0.007
111.7 ± 10.7
104.0 ± 11.6
0.107
0.68 ± 0.1
0.64 ± 0.1
0.218
Metformin
11
11
1.000
Sulphonylurea
5
3
0.230
DPP-4 inhibitors
1
2
1.000
Pioglitazone
1
0
0.565
Diuretics
3
6
1.000
Age (years)
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WBE (n = 14) 8/6
Gender (F/M)
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Duration of diabetes (years) HbA1c (%)
2
BMI (kg/m )
Waist circumference (cm) WHR
Medical treatment
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2
0.661
ACE inhibitors
2
3
0.623
ARA II
4
3
1.000
Calcium channel blockers
1
1
1.000
Aspirin
4
3
1.000
Statins
6
6
0.695
Insulin
3
1
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Beta-blockers
0.604
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WBE: training program involving deep-water walking or running; LBE: training program involving walking or running on an athletic track; BMI: body mass index. WHR: WHR: waist to height ratio, DPP-4: dipeptidyl peptidase-4; ACE: angiotensin conversion enzyme; ARA: Angiotensin receptor antagonists; Data are expressed as mean ± SD, except glycated hemoglobin, which is expressed as median and interquartile range (P25–P75); categorical variables are presented as numbers of patients (n). Comparisons were performed using Student’s t-test and U of Mann Whitney for continuous variables and by Fisher’s exact test for categorical variables.
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3.2. Glycemic effect - Three factors analysis (time x mesocycle x group)
All sessions of training determined a reduction in glucose levels (time effect: p <0.001), with relative reductions of 19%, 29% and 24% for the WBE and 24%, 29% and 27% for the LBE in the mesocycles 1, 2 and 3, respectively, without differences between mesocycles (mesocycle effect: p = 0.383) and groups (group effect: p = 0.329) (Fig. 1).
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Considering that exogenous insulin use could potentiate exercise glucose-lowering effect, we performed an analysis excluding these patients using insulin, being 3 of the WBE and 1 of the LBE. The results, however, were very similar: exercise sessions determined reduction in glucose levels (time effect: p < 0,001), with relative reductions of 19%, 29% and 25% for the WBE and 21%, 27% and 27%
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for the LBE in the mesocycles 1, 2 and 3, respectively, without differences between mesocycles (mesocycle effect: p = 0.824) and groups (group effect: p = 0.595) (Fig. 2).
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3.3. Glycemic effect - Two factors analysis (time x mesocycle) As the model of training in both environments was identical, an analysis was conducted without the group factor (time x mesocycle), to increase the power of the analysis about the glycemic responses in different mesocycles of the training periodization. In this analysis, glycemic reductions (time effect: p<0.001) were similar between mesocycles (mesocycle effect: p = 0.278). As in the analysis involving different environments, we also conduct an overall analysis excluding patients taking exogenous insulin. In this analysis, glucose levels were reduced (effect time: p <0.001) in all mesocycles, without difference between these (mesocycle effect: p = 0.785). No hypoglycemic episodes or other adverse effects were reported over the course of the study.
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Figure 1 – Glucose levels before (black bars) and after (white bars) the exercise sessions in the three mesocycles of water- (WBE, n=14) and land- (LBE, n=11) based exercise in all patients. Time effect: p < 0.001; mesocycle effect: p = 0.383; group effect: p = 0.329; interaction effect: p < 0.001. Data are reported as mean and standard error. *p<0.05 vs. before session; Generalized estimated equation; Bonferroni correction.
Figure 2 – Glucose levels before (black bars) and after (white bars) the exercise sessions in the three mesocycles of water- (WBE, n=11) and land- (LBE, n=10) based exercise in patients excluding those
ACCEPTED MANUSCRIPT 8 using insulin. Time effect: p < 0.001; mesocycle effect: p = 0.824; group effect: p = 0.595; interaction effect: p = 0.001). Data are reported as mean and standard error. *p<0.05 vs. before; Generalized estimated equation; Bonferroni correction.
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Discussion
This study showed that acute exercise sessions performed in different training environments are equally effective in reducing glycemia, in water or on land. Each of the three mesocycles of both training programs resulted in similar glucose reductions, underscoring the importance of the
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progression of training variables, especially intensity, ensuring that exercise sessions continue to have a significant impact on the glycemic metabolism of patients with type 2 diabetes over time.
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It is especially relevant to point out the glycemic reduction benefit of water-based exercise, since water aerobics have reduced impact compared to land-based exercises and deep-water walking and running is performed without contact between the feet and the bottom of the pool, decreasing the likelihood of lesions [9,11]. As such, water-based activities may be ideal for principle of continuity, with progression of physiological stimuli, such as those proposed in the periodization adopted in the present study. This finding is especially relevant in the case of type 2 diabetes due to the frequent
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association of this condition with functional disability [18], which may have difficulties from engaging on land-based walking or running. Moreover, no other clinical trial has investigated acutely the glycemic response to water-based exercises as compared to land-based sessions. Additionally to training environment, the design of the present study enabled us to discuss the
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association between training progression and glucose reduction, that has not been sufficiently studied in patients with type 2 diabetes. By keeping the duration of sessions stable, but increasing its intensity of
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exercises every three weeks, we could progress in volume and intensity of training over the course of periodization. A glycemic reduction of approximately 26% was shown in both types of exercise (average of 46 and 47 mg/dl absolute reduction in the WBE and LBE, respectively), which is similar to previous data of land-based exercise training for 12 weeks [6]. It is important to highlight that in that report, only exercise volume was increased, by increasing the duration over the course of the intervention, maintaining a mean intensity of 40% of oxygen uptake reserve over the mesocycles. Analyzing simultaneously this progression of training and the one used in the present study, we have two models that focus on different variables, but with similar magnitude of glycemic reduction. While Terada et al. (2013) [6] worked with a progression focused on the duration of the training sessions, the present study worked with a progression based especially in intensity. Both strategies of periodization
ACCEPTED MANUSCRIPT 9 seem appropriate, and can be used as needed. The different progressions can be adapted to the profile of patients: while subjects with limited training at high intensities (ie. land-based exercise, leading to higher joint impact), can progress in training duration, subjects with few available time for training may fix the duration of sessions and increase the intensity.
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The importance of exercise programs with progressively increasing intensity was also evidenced by the present findings. The similar glycemic response observed between mesocycles suggests that the adaptation to a specific treatment intensity may lead to an attenuation in glycemic responses. The exercise intensity (85-90% of anaerobic threshold heart rate) which initially caused
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glycemic reduction in 35 minutes may not be a sufficient physiological stress to maintain the same magnitude of reduction over the course of 9 weeks, when patients would likely have adapted to this level of effort, and would have had to expend less energy during the session, if the duration was
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maintained. However, further analyses of acute glucose responses to different training programs are required to confirm this hypothesis. Additionally, it is of great importance to know the acute metabolic effects of aerobic training at different intensities related to the anaerobic threshold, as this has been little studied in patients with type 2 diabetes, and the results yet are inconclusive. A strength of the present study is the determination of the anaerobic threshold through heart rate deflection method, which has low cost and easy application [18], expanding the application
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possibilities of exercise sessions. Besides, a special concern has been given to intensity precription in water-based exercise, being recommended to perform a progressive test in water environment, as in present study, due to several physiological alterations that occur in water-test when compared to landtest, as lower oxygen uptake and heart rate [17]. For this reason, the parameters of land-based tests are
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not suitable for intensity determination in water environment, which generally overestimates the intensity of water-based exercise.
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Another important issue to discuss is the effect of using or not exogenous insulin on glycemic responses and possible causing hypoglycemia of exercise. In a study [19] analyzing the effect of a single session of aerobic exercise performed on a cycle ergometer, with moderate intensity (35-50% of maximal power), a similar glycemic reduction effect was shown between insulin users and nonusers, differing only with respect to glycemic variability and the prevalence of hypoglycemia, higher in the insulin users. Regarding glycemic reduction effect of exercise, results of Van Djik et al. [19] are similar to results of the present study, that showed magnitude of reduction very similar when analyzing all patients or only those not using exogenous insulin.
ACCEPTED MANUSCRIPT 10 Conclusions
In conclusion, exercise performed on land or in water determine effective and similar acute glycemic responses. The progression of training variables, especially intensity, is important in ensuring
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this glucose reduction. It is tempting to speculate that long-term glycemic control, whether on land or in water would be improved.
List of abbreviations
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WBE: Water-based exercise; LBE: Land-based exercise; MDRD-GFR: Glomerular filtration rate using the Modification of Diet in Renal Disease formula;
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ECG: Electrocardiogram; HR: Heart rate. Conflict of interest: None'. Authors' contributions
R.S.D, B.D.S and L.F.M.K designed the study, obtained the funding, researched and analyzed
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data, wrote the manuscript, contributed to the discussion, reviewed and edited the manuscript. A.C.K and C.L.A researched and analyzed data, contributed to the discussion, reviewed and edited the manuscript. E.C.M, C.D.F.P, S.C.L and L.P.B participated in the collection and tabulation of data.
Acknowledgements
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All authors approve the final version of manuscript.
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The authors would like to thank the FIPE/HCPA, CAPES, CNPq and FAPERGS for their research support.
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[21] Van Djik JW, Manders RJF, Canfora EE, Van Mechelen W, Hartgens F, Stehouwer CDA, et al. Exercise and 24-h glycemic control: equal effects for all type 2 diabetes patients?. Med Sci Sports
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ACCEPTED MANUSCRIPT HIGHLIGHTS
•
Water- and land-based aerobic exercise sessions reduce equally glycemia.
•
Mesocycles with different intensities result in similar glucose reductions.
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Progression of intensity is important for maintenance of glucose reductions.
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•
S1744-3881(16)30039-1
DOI:
10.1016/j.ctcp.2016.05.008
Reference:
CTCP 655
To appear in:
Complementary Therapies in Clinical Practice
Received Date: 7 March 2016 Revised Date:
8 May 2016
Accepted Date: 9 May 2016
Please cite this article as: Delevatti RS, Feil Pinho CD, Kanitz AC, Alberton CL, Marson EC, Bregagnol LP, Lisboa SC, Schaan BD, Kruel LFM, Glycemic reductions following water- and land-based exercise in patients with type 2 diabetes mellitus, Complementary Therapies in Clinical Practice (2016), doi: 10.1016/j.ctcp.2016.05.008. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT PAGE TITLE
Title: Glycemic reductions following water- and land-based exercise in patients with
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type 2 diabetes mellitus
Rodrigo Sudatti Delevatti1,2, Carolina Dertzbocher Feil Pinho1, Ana Carolina Kanitz1,3, Cristine Lima Alberton4, Elisa Corrêa Marson1, Luciana Peruchena Bregagnol1, Salime
1
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Chedid Lisboa1, Beatriz D. Schaan5,6, Luiz Fernando Martins Kruel1
Exercise Research Laboratory, Department of Physical Education, Universidade
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Federal do Rio Grande do Sul, Brazil. 2
Faculdade Sogipa de Educação Física, Brazil.
3
Faculty of Physical Education, Universidade Federal de Uberlândia, Minas Gerais,
Brazil. 4
Department of Physical Education, Federal University of Pelotas, Rio Grande do Sul,
Brazil.
Endocrine Division, Hospital de Clinicas de Porto Alegre, Rio Grande do Sul, Brazil.
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Internal Medicine Department. Faculty of Medicine, Universidade Federal do Rio
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Grande do Sul, Brazil.
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Author for correspondence: Rodrigo Sudatti Delevatti.
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Felizardo Street, 750, Swimming Center, 18 room. Postal code: Porto Alegre, RS, Brazil Fone/Fax: 55 51 3308-5820 E-mail: [email protected]
ACCEPTED MANUSCRIPT 1 Abstract Purpose: To assess the acute glucose responses to the first sessions of three mesocycles of water- and land-based aerobic exercise. Methods: The water-based exercise group (WBE, n=14; 54.1 ± 9.1 years) performed deep water walking and/or running, while the land-based exercise group (LBE, n=11; 60.1 ±
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7.3 years) performed walking and/or running on athletic track. In the first mesocycle, patients trained at 85-90% of their anaerobic threshold (AT) for 35 minutes, progressing to 90-95% of the AT in the second mesocycle, and 95-100% of the AT in the last mesocycle. Capillary glucose was assessed before and immediately after the first session of each mesocycle. Results: There was glycemic
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reduction (p < 0.001) in all sessions, with relative reductions of 19%, 29% and 24% for the WBE and 24%, 29% and 27% for the LBE in the mesocycles 1, 2 and 3, respectively. There were not found differences between groups and between mesocycles. Conclusions: The acute response of blood
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glucose to aerobic training between 85 and 100% of the heart rate of AT is effective and independent of the environment in which it is performed. Clinical trial reg. no. NCT01956357, clinicaltrials.gov.
Keywords: Exercise, Diabetes Mellitus, Glycemia.
1. Introduction
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Most current treatments for type 2 diabetes involve physical activity and dietary modifications in addition to medical management, all of which are crucial for glycemic control [1]. Structured and supervised training programs have been found to have a greater impact on glycemic control than general increases in physical activity alone [2]. Aerobic training is found to produce both acute and
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chronic benefits for these patients, including metabolic and cardiovascular beneficial effects, as well as higher quality of life and wellbeing [3-7]. It can be performed in different ways (cycling, running,
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walking, rowing, stepping and others), differing in terms of total recruited muscle mass, type of impact or energy expenditure, which may be of important for patients with diabetes [8]. Few studies analyse the effects of different modes of aerobic exercise on glucose levels in type 2 diabetes. Running is one of the most studied modalities of aerobic exercise; however, the progression of training variables such as duration and intensity may expose patients to moderate to high impact forces on their musculoskeletal system. Importantly, as patients with diabetes are prone to chronic complications, including peripheral neuropathy that increases risk of foot lesions, it is important to find alternatives for the progression of training. Different environments where exercise training is performed could minimize injuries and ulcerations caused by the impact directly absorbed in the foot in contact with the
ACCEPTED MANUSCRIPT 2 ground. Alternative forms of exercises for patients with diabetes are those performed in water, where the impact forces can be attenuated, especially for the lower limbs [9]. Among the modalities of aerobic exercise performed in aquatic environment, water aerobics can be highlighted, as the ground reaction force can be reduced by up to 1.2 times the body weight [10]. Moreover, deep-water running is another
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interesting modality because the practitioners perform aerobic exercise at high loads with reduced risk of injury, as a float vest is used, keeping the body in an upright position, preventing contact between the feet and the bottom of the pool [11].
Some small studies have addressed the possible metabolic benefits of exercise performed in the
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aquatic environment, but the results were inconclusive, especially because of the quasi-experimental design of the study [12] and small sample of individuals evaluated [12,13]. Moreover, comparisons of exercise training glycemic effects in patients with type 2 as performed on land or in water, is a yet few
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discussed subject. Recently, a randomized clinical trial [14] demonstrated similar glucose control, by HbA1c levels, after aquatic or dry-land aerobic training in patients with type 2 diabetes. Despite of the clinical importance of this finding, to our knowledge, studies with similar design (water- versus landbased exercise) analyzing acute glycemic effect in this population have not been conducted. Although long-term glycemic control is the primary goal of diabetes treatment [1], knowledge regarding the acute impact of exercise on glucose responses in this population is crucial in ensuring the
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safety and quality of exercise interventions, as chronic glucoregulatory benefit of exercise training is the result of the added effects of each bout of exercise [15]. However, studies with this objective often compare different sessions, differing in relation to the training variables in a particular state of trainability. This provides knowledge of the isolated impact of a session, in which the increased
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intensity, increased volume and the consequent change in the state of trainability can change the magnitude of glycemic reduction. Therefore, the present study aimed to analyze the acute glucose
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responses in the first sessions of three mesocycles of aerobic training periodization. Additionally, the present study aimed to analyze the acute glucose responses to aerobic training in water as compared to similar training performed on land. We hypothesized that the magnitude of glycemic reduction is maintained during a periodization with progression of intensity, that is, no differences would be observed among mesocycles. We hypothesized that the training in water would provide glycemic reductions similar to those derived from training on land.
2. Material and methods 2.1 Subjects
ACCEPTED MANUSCRIPT 3 All participants were fully informed of the procedures involved in the study, and provided written consent prior to participation. The study was conducted in accordance with The Code of Ethics of the World Medical Association (Declaration of Helsinki) for experiments involving humans and was approved by the Research Ethics Committees of the Universidade Federal do Rio Grande do Sul
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(protocol number 108.997) and of the Hospital de Clínicas de Porto Alegre (protocol number 54475). The sample consisted of 25 patients with type 2 diabetes (14 men) who had not undertaken any physical exercise in the previous three months and were receiving their usual medical treatment. Patients were identified from the records of the Endocrine Division of a tertiary hospital and also were
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recruited through advertisements in local newspapers between June and July 2012. They were randomly assigned to water-based (WBE; n=14) or land-based exercise (LBE; n=11), by picking an envelope with predefined group numbers, stratified according to gender. Patients with the following
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conditions were excluded from the sample: uncontrolled hypertension, autonomic neuropathy, severe peripheral neuropathy, proliferative diabetic retinopathy, severe nonproliferative diabetic retinopathy, decompensated heart failure, limb amputations, chronic renal failure (MDRD-GFR < 30 ml/min) [16] or any muscle or joint impairments which prevented individuals from engaging in physical exercise. The presence of these conditions was confirmed by medical history as well as clinical and laboratory examinations. All patients had undergone electrocardiogram (ECG) stress testing in the six months
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preceding the study.
2.2 Anthropometric measurements
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Prior to the intervention, patients underwent anthropometric measurements at our exercise research laboratory. Body mass and height were assessed using a digital scale and a stadiometer
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(FILIZOLA; São Paulo, Brazil). These values were used to calculate patient body mass index (BMI) using the following formula: mass (kg)/height² (m). Waist circumference was measured at the midpoint between the iliac crest and the last rib.
2.3 Capillary glycemia
Capillary glycemia was assessed before and immediately after the first session of each training mesocycle using a clinical glucometer (Accu-Check Performa, Roche, São Paulo, Brazil), which
ACCEPTED MANUSCRIPT 4 assesses glycemic levels in approximately 5 seconds and an Accu-Chek – Multiclix lancet device (São Paulo, Brazil).
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2.4 Intervention
Patients underwent 9-week training programs involving deep-water walking or running with a life vest (WBE group) or walking or running on an athletic track (LBE group). Both groups underwent interval-training programs consisting of a three-week adaptation period followed by three mesocycles
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of three weeks each. Training was conducted three times per week (Monday, Wednesday and Friday), and each 45-minute session was divided into a warm-up period (5 min), followed by the main training program (35 min) and a cool down section (5 min). The intensity of the exercise prescribed was
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adjusted according to each subject heart rate deflection point, which was determined by progressive exercise tests conducted in the water [17] or on land [18] for the water- and land-based groups, respectively. This method was chosen due to its ease of application and association with the second ventilatory threshold in patients with type 2 diabetes [18], a precise indicator of the relative stress caused by exercise [19]. The HRDP was observed in the HR-by-intensity graph. The analysis were carried out by two independent, blinded, experienced exercise physiologists. Participants were asked to
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wear heart rate (HR) monitors (RSX 300, Polar) during exercise to control training intensity. Each individual was asked to read and report their HR to one of the three teachers who supervised the waterand land-based exercise sessions. Each teacher then used a table containing subjects' training HR ranges to provide feedback on the recommended exercise intensity for each patient. The 9-week
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training program prescribed to each participant is described in table 1.
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Table 1. Nine-week aerobic training program. Mesocycle
Week
Training sessions
1
1* - 3
7x (4 min 85 at 90% ATHR with/ 1min at <85% ATHR)
7x (4 min 90 at 95% ATHR with/ 1min at <85% ATHR) 2 4* - 6 7x (4 min 95 at 100% ATHR with/ 1min at <85% ATHR) 3 7* - 9 Note: ATHR: Anaerobic threshold heart rate; *weeks in which capillary glycemia was assessed.
Duration (main part) 35 min 35 min 35 min
2.5 Statistical analysis Patients’ characteristics data are presented as mean and standard deviation or median and interquartil range (P25-P75) for continuous variables and by number of patients (n) for categorical
ACCEPTED MANUSCRIPT 5 variables. Baseline comparisons were performed using Student’s t-test and U of Mann Whitney for continuous variables and by Fisher’s exact test for categorical variables. A generalized estimation equation (GEE) was used to assess reductions in glucose levels in different mesocycles and different environments of training; considering the three factors involved in
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the analysis (time, mesocycle, and group). As the model of training in both groups was identical, an analysis was also conducted without the group factor (time, mesocycle), aiming only to assess reductions in glucose levels in different mesocycles of the training periodization. The three factors (time, mesocycle, and group) and two factors (time and mesocycle) analysis were performed with all
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patients and excluding the insulin users. Multiple comparisons were performed with the Bonferroni correction. The level of significance was set at α < 0.05. All analyses were performed using the
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Statistical Package for the Social Sciences (SPSS) software, version 19.0.
3. Results
3.1. Patients’ characteristics
Patients’ characteristics regarding disease duration, age, anthropometric measurements and medications use are showed in table 2. Only BMI was higher in WBE group at baseline. For the other
profile.
Table 2. Patients’ characteristics.
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anthropometric measurements, disease duration, age and medications used, the groups showed a similar
LBE (n = 11) 5/6
p 0.695
54.3 ± 9.1
60.1 ± 7.3
0.102
5.4 ± 3.7
8.4 ± 5.8
0.134
6.4 (6 – 9.8)
6.1 (6.0 – 7.8)
0.536
34.5 ± 3.9
29.9 ± 3.6
0.007
111.7 ± 10.7
104.0 ± 11.6
0.107
0.68 ± 0.1
0.64 ± 0.1
0.218
Metformin
11
11
1.000
Sulphonylurea
5
3
0.230
DPP-4 inhibitors
1
2
1.000
Pioglitazone
1
0
0.565
Diuretics
3
6
1.000
Age (years)
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WBE (n = 14) 8/6
Gender (F/M)
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Duration of diabetes (years) HbA1c (%)
2
BMI (kg/m )
Waist circumference (cm) WHR
Medical treatment
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2
0.661
ACE inhibitors
2
3
0.623
ARA II
4
3
1.000
Calcium channel blockers
1
1
1.000
Aspirin
4
3
1.000
Statins
6
6
0.695
Insulin
3
1
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Beta-blockers
0.604
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WBE: training program involving deep-water walking or running; LBE: training program involving walking or running on an athletic track; BMI: body mass index. WHR: WHR: waist to height ratio, DPP-4: dipeptidyl peptidase-4; ACE: angiotensin conversion enzyme; ARA: Angiotensin receptor antagonists; Data are expressed as mean ± SD, except glycated hemoglobin, which is expressed as median and interquartile range (P25–P75); categorical variables are presented as numbers of patients (n). Comparisons were performed using Student’s t-test and U of Mann Whitney for continuous variables and by Fisher’s exact test for categorical variables.
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3.2. Glycemic effect - Three factors analysis (time x mesocycle x group)
All sessions of training determined a reduction in glucose levels (time effect: p <0.001), with relative reductions of 19%, 29% and 24% for the WBE and 24%, 29% and 27% for the LBE in the mesocycles 1, 2 and 3, respectively, without differences between mesocycles (mesocycle effect: p = 0.383) and groups (group effect: p = 0.329) (Fig. 1).
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Considering that exogenous insulin use could potentiate exercise glucose-lowering effect, we performed an analysis excluding these patients using insulin, being 3 of the WBE and 1 of the LBE. The results, however, were very similar: exercise sessions determined reduction in glucose levels (time effect: p < 0,001), with relative reductions of 19%, 29% and 25% for the WBE and 21%, 27% and 27%
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for the LBE in the mesocycles 1, 2 and 3, respectively, without differences between mesocycles (mesocycle effect: p = 0.824) and groups (group effect: p = 0.595) (Fig. 2).
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3.3. Glycemic effect - Two factors analysis (time x mesocycle) As the model of training in both environments was identical, an analysis was conducted without the group factor (time x mesocycle), to increase the power of the analysis about the glycemic responses in different mesocycles of the training periodization. In this analysis, glycemic reductions (time effect: p<0.001) were similar between mesocycles (mesocycle effect: p = 0.278). As in the analysis involving different environments, we also conduct an overall analysis excluding patients taking exogenous insulin. In this analysis, glucose levels were reduced (effect time: p <0.001) in all mesocycles, without difference between these (mesocycle effect: p = 0.785). No hypoglycemic episodes or other adverse effects were reported over the course of the study.
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Figure 1 – Glucose levels before (black bars) and after (white bars) the exercise sessions in the three mesocycles of water- (WBE, n=14) and land- (LBE, n=11) based exercise in all patients. Time effect: p < 0.001; mesocycle effect: p = 0.383; group effect: p = 0.329; interaction effect: p < 0.001. Data are reported as mean and standard error. *p<0.05 vs. before session; Generalized estimated equation; Bonferroni correction.
Figure 2 – Glucose levels before (black bars) and after (white bars) the exercise sessions in the three mesocycles of water- (WBE, n=11) and land- (LBE, n=10) based exercise in patients excluding those
ACCEPTED MANUSCRIPT 8 using insulin. Time effect: p < 0.001; mesocycle effect: p = 0.824; group effect: p = 0.595; interaction effect: p = 0.001). Data are reported as mean and standard error. *p<0.05 vs. before; Generalized estimated equation; Bonferroni correction.
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Discussion
This study showed that acute exercise sessions performed in different training environments are equally effective in reducing glycemia, in water or on land. Each of the three mesocycles of both training programs resulted in similar glucose reductions, underscoring the importance of the
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progression of training variables, especially intensity, ensuring that exercise sessions continue to have a significant impact on the glycemic metabolism of patients with type 2 diabetes over time.
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It is especially relevant to point out the glycemic reduction benefit of water-based exercise, since water aerobics have reduced impact compared to land-based exercises and deep-water walking and running is performed without contact between the feet and the bottom of the pool, decreasing the likelihood of lesions [9,11]. As such, water-based activities may be ideal for principle of continuity, with progression of physiological stimuli, such as those proposed in the periodization adopted in the present study. This finding is especially relevant in the case of type 2 diabetes due to the frequent
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association of this condition with functional disability [18], which may have difficulties from engaging on land-based walking or running. Moreover, no other clinical trial has investigated acutely the glycemic response to water-based exercises as compared to land-based sessions. Additionally to training environment, the design of the present study enabled us to discuss the
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association between training progression and glucose reduction, that has not been sufficiently studied in patients with type 2 diabetes. By keeping the duration of sessions stable, but increasing its intensity of
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exercises every three weeks, we could progress in volume and intensity of training over the course of periodization. A glycemic reduction of approximately 26% was shown in both types of exercise (average of 46 and 47 mg/dl absolute reduction in the WBE and LBE, respectively), which is similar to previous data of land-based exercise training for 12 weeks [6]. It is important to highlight that in that report, only exercise volume was increased, by increasing the duration over the course of the intervention, maintaining a mean intensity of 40% of oxygen uptake reserve over the mesocycles. Analyzing simultaneously this progression of training and the one used in the present study, we have two models that focus on different variables, but with similar magnitude of glycemic reduction. While Terada et al. (2013) [6] worked with a progression focused on the duration of the training sessions, the present study worked with a progression based especially in intensity. Both strategies of periodization
ACCEPTED MANUSCRIPT 9 seem appropriate, and can be used as needed. The different progressions can be adapted to the profile of patients: while subjects with limited training at high intensities (ie. land-based exercise, leading to higher joint impact), can progress in training duration, subjects with few available time for training may fix the duration of sessions and increase the intensity.
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The importance of exercise programs with progressively increasing intensity was also evidenced by the present findings. The similar glycemic response observed between mesocycles suggests that the adaptation to a specific treatment intensity may lead to an attenuation in glycemic responses. The exercise intensity (85-90% of anaerobic threshold heart rate) which initially caused
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glycemic reduction in 35 minutes may not be a sufficient physiological stress to maintain the same magnitude of reduction over the course of 9 weeks, when patients would likely have adapted to this level of effort, and would have had to expend less energy during the session, if the duration was
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maintained. However, further analyses of acute glucose responses to different training programs are required to confirm this hypothesis. Additionally, it is of great importance to know the acute metabolic effects of aerobic training at different intensities related to the anaerobic threshold, as this has been little studied in patients with type 2 diabetes, and the results yet are inconclusive. A strength of the present study is the determination of the anaerobic threshold through heart rate deflection method, which has low cost and easy application [18], expanding the application
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possibilities of exercise sessions. Besides, a special concern has been given to intensity precription in water-based exercise, being recommended to perform a progressive test in water environment, as in present study, due to several physiological alterations that occur in water-test when compared to landtest, as lower oxygen uptake and heart rate [17]. For this reason, the parameters of land-based tests are
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not suitable for intensity determination in water environment, which generally overestimates the intensity of water-based exercise.
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Another important issue to discuss is the effect of using or not exogenous insulin on glycemic responses and possible causing hypoglycemia of exercise. In a study [19] analyzing the effect of a single session of aerobic exercise performed on a cycle ergometer, with moderate intensity (35-50% of maximal power), a similar glycemic reduction effect was shown between insulin users and nonusers, differing only with respect to glycemic variability and the prevalence of hypoglycemia, higher in the insulin users. Regarding glycemic reduction effect of exercise, results of Van Djik et al. [19] are similar to results of the present study, that showed magnitude of reduction very similar when analyzing all patients or only those not using exogenous insulin.
ACCEPTED MANUSCRIPT 10 Conclusions
In conclusion, exercise performed on land or in water determine effective and similar acute glycemic responses. The progression of training variables, especially intensity, is important in ensuring
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this glucose reduction. It is tempting to speculate that long-term glycemic control, whether on land or in water would be improved.
List of abbreviations
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WBE: Water-based exercise; LBE: Land-based exercise; MDRD-GFR: Glomerular filtration rate using the Modification of Diet in Renal Disease formula;
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ECG: Electrocardiogram; HR: Heart rate. Conflict of interest: None'. Authors' contributions
R.S.D, B.D.S and L.F.M.K designed the study, obtained the funding, researched and analyzed
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data, wrote the manuscript, contributed to the discussion, reviewed and edited the manuscript. A.C.K and C.L.A researched and analyzed data, contributed to the discussion, reviewed and edited the manuscript. E.C.M, C.D.F.P, S.C.L and L.P.B participated in the collection and tabulation of data.
Acknowledgements
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All authors approve the final version of manuscript.
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The authors would like to thank the FIPE/HCPA, CAPES, CNPq and FAPERGS for their research support.
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ACCEPTED MANUSCRIPT HIGHLIGHTS
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Water- and land-based aerobic exercise sessions reduce equally glycemia.
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Mesocycles with different intensities result in similar glucose reductions.
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Progression of intensity is important for maintenance of glucose reductions.
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