Effects of 2 Models of Aquatic Exercise Training on Cardiorespiratory Responses of Patients With Type 2 Diabetes: The Diabetes and Aquatic Training Study—A Randomized Controlled Trial

in Journal of Physical Activity and Health

Background: There are a lack of clinical trials with suitable methodological quality that compare aquatic exercise training types in type 2 diabetes (T2D) treatment. This study aimed to compare the effects of aerobic and combined aquatic training on cardiorespiratory outcomes in patients with T2D. Methods: Untrained patients with T2D were randomized to receive an aerobic aquatic training, a combined aquatic training, or a procedure control in 3 weekly sessions for 15 weeks. The sessions were 50 minutes long. The intensities were from 85% to 100% of heart rate of anaerobic threshold and at maximal velocity for aerobic and resistance parts, respectively. Resting heart rate, peak oxygen uptake (VO2peak), and oxygen uptake corresponding to second ventilatory threshold and its relation with VO2peak were evaluated. Results: Participants were 59.0 (8.2) years old and 51% women. Intervention groups increased in VO2peak (aerobic aquatic training group: 4.48 mL·kg−1·min−1, P = .004; combined aquatic training group: 5.27 mL·kg−1·min−1; P = .006) and oxygen uptake corresponding to second ventilatory threshold, whereas the control group presented an increase in oxygen uptake corresponding to second ventilatory threshold and minimal change in VO2peak. Conclusions: Aerobic and combined aquatic exercise interventions improve the cardiorespiratory fitness of patients with T2D.

Responses related to cardiorespiratory fitness (CRF) are strong mortality predictors.1 Especially in type 2 diabetes (T2D), a low CRF is an independent risk factor for cardiovascular diseases.2 In this sense, besides glycemic control and cardiometabolic outcomes usually considered in disease treatment, CRF should also be a therapeutic target in this population, which is highly responsive to structured physical training, a key tool for improving this outcome.

American Diabetes Association guidelines3 recommend that people with T2D should perform aerobic physical training and, when possible, also include resistance exercises in their routine, characterizing combined training. However, improvements in CRF have been found after both isolated aerobic training4 and combined training.5 Nevertheless, the vast majority of clinical trials found in the literature were performed in a dry-land environment with walking and running as aerobic training modalities. This made it difficult for some patients, particularly those who are overweight or obese, which are conditions highly associated with T2D, to perform the training.6

In this context, exercises performed in the aquatic environment have been highlighted as an alternative physical training for patients with T2D, especially for lower musculoskeletal stress and specific physiological alterations, such as the suppression of the renin–angiotensin system.710

However, there are still few studies evaluating water-based exercise training effects on CRF of patients with T2D.1116 In these studies, the results are still controversial, the intervention periods are no longer than 12 weeks, and the comparison between aerobic and combined training models has not been yet performed.

In addition, studies in the aquatic environment present little methodological information that could enable their reproduction in clinical practice, clubs, and gyms. Therefore, there is a lack of consistent information on different models of water-based exercise training and their benefits in the clinical aspects related to T2D, especially CRF outcomes. Due to the importance of CRF in diabetes context and the benefits resulting from water-based physical training, it is necessary to perform a randomized clinical trial with high methodological quality comparing the aerobic and combined training in the aquatic environment on CRF responses of patients with T2D.

Thus, the aim of the present study was to compare 2 models of upright water-based exercise training (aerobic and combined) on CRF outcomes in patients with T2D. Our hypothesis was that both models would promote improvements of similar magnitude.

Methods

Study Design

The Diabetes and Aquatic Training Study is a randomized, controlled, 3-arm parallel-group clinical trial and is reported according to the CONSORT Statement for Randomized Trials of Nonpharmacologic Treatments.17 The research protocol, which complies with the Declaration of Helsinki, was approved by the Universidade Federal do Rio Grande do Sul Ethics Committee (protocol no 1.083.589) and by the Hospital de Clínicas de Porto Alegre Ethics Committee (protocol no 1.175.958), and each participant provided written informed consent. The study protocol was registered in ClinicalTrials.gov (NCT02612805).

Subjects

The main entry criterion was known T2D (defined by the American Diabetes Association criteria), treated with an oral hypoglycemic and/or insulin. Additional requirements were age 30–75 years, not engaged in regular exercise (defined as not exercising 20 min or more in 3 or more days a week), and eligibility after an electrocardiogram stress test. Exclusion criteria were severe autonomic neuropathy, severe peripheral neuropathy or history of foot injuries, severe nonproliferative and proliferative diabetic retinopathy, decompensated heart failure, limb amputations, chronic kidney disease (MDRD-GFR < 30 mL·min−1),18 body mass index ≥45.0 kg·m−2, or any muscle or joint impairment that prevented individuals from engaging in physical exercise.

Care Providers

Three exercise specialists (professionals holding a degree in exercise science) with experience in aquatic training prescription and evaluation were responsible for standardizing the exercise training procedures.

Recruitment

Participants were recruited by advertisements in local (Porto Alegre/RS—Brazil) newspapers and contacted the authors by phone. All potentially eligible patients who made contact by phone were evaluated for eligibility based on medical history, clinical examination, and cardiologic evaluation.

Randomization and Blinding

Patients were randomized 1:1:1 to an aquatic aerobic training (AERO) group (n = 19), an aquatic combined training (COMBI) group (n = 19), or an active control (CON) group (n = 19), which performed an aquatic program of stretching and relaxation exercises.

Randomization was stratified by sex using the www.randomization.org software. The allocation sequence was generated by a researcher not directly involved with the study, and the allocation list was concealed from the outcome evaluators throughout the study and was concealed from the patients and aquatic exercise trainers until the beginning of the interventions.

Due to the specific features of each group, it was not possible to blind the patients and exercise trainers. However, all outcome evaluators were blinded during the study.

Aquatic Interventions (AERO and COMBI)

Both aerobic and combined aquatic training interventions lasted 15 weeks, with 3 weekly sessions. These sessions had a total duration of 56 minutes, divided into warm-up (3 min), main part (50 min), and cooldown (3 min). Aerobic training intensity was prescribed according to the heart rate (HR) corresponding to anaerobic threshold (HRAT), verified by HR deflection point,19 which was determined by an aquatic progressive stationary running test.20,21 This test started with an initial cadence of 85 beats per minute (bpm) for 3 minutes and was increased by 15 bpm every 2 minutes, wherein the amplitude of movement was controlled to 90° of hip and knee flexion. Participants trained wearing HR monitors (FT1; Polar, Kajaani, Finland) during exercise to control training intensity. In the COMBI group, resistance training intensity was prescribed by maximal effort (index 19 of Borg scale of perceived exertion) and amplitude to achieve the greatest possible velocity of motion and, consequently, greatest resistance. The modality of aquatic training adopted in both interventions was upright water-based exercises in a shallow pool.

Before the beginning of the interventions, participants from the AERO and COMBI groups were familiarized with the aquatic exercises (3 sessions) of the training program to ensure proper execution of movements.

Aquatic Aerobic Training

The AERO program consisted of a combination of lower and upper limb exercises. The 5 lower limb exercises used were stationary running, front kick, cross-country skiing, backward stationary running, and hip extension, all accompanied with upper limbs movements. Each 2 minutes of lower limb exercises were combined with 2 (1 min for each) upper limb exercises. The continuous method of aerobic training was adopted with the following periodization: weeks 1 to 5 (50 min 85%–90% HRAT), weeks 6 to 10 (50 min 90%–95% HRAT), and weeks 11 to 15 (50 min 95%–100% HRAT) (Table 1).

Table 1

Aquatic Aerobic Training Periodization

WeeksSetsExercisesDuration, minTotal duration, minIntensity
1–55Stationary running25085%–90% HRAT
Front kick2
Cross-country skiing2
Backward stationary running2
Hip hyperextension2
6–105Stationary running25090%–95% HRAT
Front kick2
Cross-country skiing2
Backward stationary running2
Hip hyperextension2
11–155Stationary running25095%–100% HRAT
Front kick2
Cross-country skiing2
Backward stationary running2
Hip hyperextension2

Abbreviations: HRAT, heart rate corresponding to anaerobic threshold.

Aquatic Combined Training

Aerobic Part

The aerobic part always preceded the resistance part with the periodization similar to that previously described and shown in Table 1. There was a difference in duration, with 4 sets of each lower limb exercise being performed until week 10, totaling 40 minutes, and finishing with 3 sets, totaling 30 minutes, in the third mesocycle.

Resistance Part

The resistance part was always performed at maximal velocity and lasted approximately 10 minutes in the first 2 mesocycles (weeks 1–10) and approximately 20 minutes in the last mesocycle (weeks 11–15) (Table 2). The aquatic resistance exercises were divided into 2 blocks, and each block had 1 exercise for upper limbs and 1 exercise for lower limbs. Block 1 consisted of elbow flexion and extension (bilateral) combined with right or left hip flexion and extension (unilateral). In addition, block 2 consisted of horizontal shoulder adduction and abduction (bilateral) combined with right or left knee flexion and extension (starting from hip flexion at 90°; unilateral). Participants performed 3 sets of each block with the following sequence: exercise for upper limbs, 10 seconds for switching the exercise; exercise for lower limb (right leg), 10 seconds for switching; and exercise for lower limb (left leg). This sequence was repeated according to the number of sets of each mesocycle with a passive interval between sets and between blocks. The structure of the sets (number and duration) was the following: weeks 1 to 5 (2 sets of 30 s; interval of 40 s), weeks 6 to 10 (3 sets of 20 s; interval of 60 s), and weeks 11 to 15 (5 sets of 15 s; interval of 80 s). Intervals between blocks were always 60 seconds.

Table 2

Aquatic Resistance Training Periodization

WeeksSetsExercise blocksDuration, sInterval between exercise, sInterval between sets, sIntensityTotal durationInterval between block, s
1–52Block 1

 Elbow flexion and extension
301040Maximal velocity9 min60
 Hip flexion and extension (right leg)3010
 Hip flexion and extension (left leg)30
2Block 2

 Horizontal shoulder adduction and abduction
3010
 Knee flexion and extension (right leg)3010
 Knee flexion and extension (left leg)30
6–103Block 1

 Elbow flexion and extension
201060Maximal velocity13 min60
 Hip flexion and extension (right leg)2010
 Hip flexion and extension (left leg)20
3Block 2

 Horizontal shoulder adduction and abduction
20

20
10
 Knee flexion and extension (right leg)2010
11–155Block 1

 Elbow flexion and extension
1580Maximum velocity22 min 10 s60
 Hip flexion and extension (right leg)1510
 Hip flexion and extension (left leg)1510
5Block 2

 Horizontal shoulder adduction and abduction
15

15
10
 Knee flexion and extension (right leg)1510

Water temperature was always kept between 30°C and 32°C. Participants of all groups performed the activities immersed to the height of the xiphoid process.

Control Procedure (CON)

For the participants allocated into the CON group, stretching and relaxation sessions were provided in the aquatic environment with weekly duration and frequency identical to those proposed in the exercise training programs. The aim of this procedure was to control exercise intensity and volume while maintaining the same social (social relationships) and environmental exposure (water immersion) factors of the aerobic and combined aquatic training. Moreover, the aim was to maintain among the 3 arms of the study identical care of the research team, contact between participants, possible immersion effects, and the physical stimulus caused by the displacement of the patients to the intervention site.

Sample Characteristics Assessment

Before the outcome assessments, anthropometric variables were collected for sample characterization. Initially, height, body mass, waist circumference, and the sum of 6 skinfolds were measured. These data were used to calculate body mass index and waist/height ratio. The equations proposed by Petroski and Pires-Neto22 were used to estimate the body density of men and women, whereas body fat percentages were estimated using the Siri formula.23

Outcomes Assessments

Resting heart rate (HRrest), peak oxygen uptake (VO2peak), and oxygen uptake corresponding to second ventilatory threshold (VO2VT2) and its relation with VO2peak (%VO2VT2) were evaluated as outcomes, with the VO2peak being the primary outcome of this secondary analysis of the Diabetes and Aquatic Training Study.

The HRrest was considered as the lowest HR value found during the final 3 minutes of 10 minutes rest with the participant seated. A Polar HR monitor was used (model FT1TM; Polar, Shanghai, China). After that, the participants performed an incremental test using a treadmill (Inbramed, Porto Alegre, Brazil) to determine the VO2peak and VO2VT2. The test protocol started at 3 km·h−1 for 3 minutes, which was progressively increased by 1 km·h−1 every 2 minutes with fixed inclination (1%). This protocol was used in the study of Delevatti et al.15 The effort perception was recorded at the end of each stage. The test was interrupted when the participants signaled with a manual gesture, and the patients were instructed to only signal when they reached a state of exhaustion. Approximately 1 week before testing, all participants were familiarized with the protocol, the use of the gas collection mask, and the treadmill.

The VO2VT2 was determined using the ventilation curve corresponding to the point of exponential increase in the ventilation in relation to the velocity. In addition, to confirm the data, VO2VT2 was determined using the CO2 ventilatory equivalent.24 Two experienced, independent physiologists determined the corresponding points. The maximum oxygen uptake that was obtained close to exhaustion was considered the VO2peak. The maximum test was considered valid if at least one of the following 3 criteria was met: (1) the maximum HR predicted by age was reached (220 age), (2) rating of perceived exertion was >17 (very intense—6–20 Borg scale), and (3) respiratory exchange rate >1.1 was obtained.25 Participants were instructed not to eat for 3 hours before the tests, not to consume stimulants, and not to practice intense physical activities for 12 hours before the test.

Statistical Analysis

Descriptive data of participants are presented as mean and SD or median and interquartile interval (P25–P75) for continuous variables and as absolute frequency (n) for categorical variables. Baseline differences between groups were compared using chi-square test for categorical variables and 1-way analysis of variance with post hoc of Bonferroni for continuous variables.

Generalized estimation equations were used for evaluation of outcomes (time effect, group effect, and time × group interaction effect). Multiple comparisons were performed by Bonferroni post hoc test. The outcomes were analyzed using both per-protocol (PP) and intention-of-treat (ITT) principles. Patients who attended at least 70% of the 43 proposed sessions were included in the PP analysis. For ITT analysis, all available data of all patients were used. The authors used the maximum likelihood estimation approach for computing missing data in the generalized estimation equations model. Effect sizes representing differences of intervention (AERO and COMBI) groups versus the CON group were calculated using Cohen26 d test and lower and upper limits, with effect sizes considered small (0.20 ≤ d < 0.50), medium (0.50 ≤ d < 0.80), and great (d ≥ 0.80). Significance level was set at P < .05; however, for time × group interactions the authors considered P <.10 as marginally significant.27 Analyses were performed in the Statistical Package for the Social Sciences (SPSS) software (version 20, IBM, Armonk, NY). A priori sample size was calculated for the primary outcome of the major study (The Diabetes and Aquatic Training Study), which was HbA1c. This calculation demonstrated the need of 15 participants for each group, which also was used for the other outcomes of this study.

Results

Between July and August 2015, 367 participants were assessed for eligibility of which 219 were primarily excluded because they were not diagnosed with T2D. Of the 148 patients with T2D, 86 attended the initial meeting in which 57 were considered eligible for the study and randomized into the 3 intervention groups. Of these, 19 participants were allocated to the AERO group, 19 to the COMBI group, and 19 to the CON group. Thirteen participants (23%) dropped out from the study along the 15 weeks of intervention (AERO, n = 5; COMBI, n = 6; and CON, n = 2). With this, 44 patients completed the trial, of which 42 were included in the PP analysis (one participant of each intervention group was excluded due to training frequency lower than 70%). Flow of participants throughout the study is presented in Figure 1.

Figure 1
Figure 1

—Flow of participants throughout the study. AERO, aerobic aquatic training group; COMBI, combined aquatic training group; CON, control group; ITT, intention-of-treat; PP, per-protocol.

Citation: Journal of Physical Activity and Health 17, 11; 10.1123/jpah.2020-0236

At baseline, mean age, number of women, duration of T2D, anthropometric profile, and medication were not different between groups (Table 3).

Table 3

Baseline Characteristics of Participants

CharacteristicsAERO (n = 19)COMBI (n = 19)CON (n = 19)P value
Demographics
 Age, y57.5 (7.4)60.9 (7.4)58.6 (9.7).425
 No of women, %9 (47)10 (53)10 (53).932
 T2D, y5 (2 to 10)6 (5 to 9.5)7 (4 to 9).496
Anthropometric profile
 Body mass, kg83.7 (15.4)85.2 (18.9)83.0 (19.1).925
 BMI, kg·m−231.6 (6.3)31.5 (4.6)30.6 (5.1).801
 Waist circumference, cm105.6 (14.6)108.1 (12.1)103.3 (16.1).590
 WHR0.65 (0.09)0.66 (0.05)0.62 (0.08).472
 ∑SF130.7 (54.1)129.6 (40.4)120.6 (44.0).472
 Fat percentage32.4 (6.0)31.1 (5.9)31.6 (6.2).736
Medication
 Glucose lowering medication, No (%)
  Metformin15 (79)18 (95)18 (95).187
  Sulfonylurea6 (32)6 (32)10 (53).306
  DPP-4 inhibitors2 (11)1 (5)3 (16).859
  Insulin2 (11)5 (26)5 (26).443
 Hypotensive medication, No (%)
  Diuretics8 (42)8 (42)10 (53).754
  Beta-blockers3 (16)8 (42)7 (37).201
  ACE-inhibitors6 (32)6 (32)5 (26).920
  ARA II5 (26)3 (16)5 (26).790
 Other chronic medications, No (%)
  Acetylsalicylic acid5 (26)5 (26)3 (16).192
  Statins10 (53)12 (63)12 (63).747

Abbreviations: ACE, angiotensin conversion enzyme; AERO, aerobic aquatic training group; ARA, angiotensin receptor antagonists; ANOVA, analysis of variance; BMI, body mass index; COMBI, combined aquatic training group; CON, control group; DPP-4, dipeptidyl peptidase-4; T2D, type 2 diabetes; WHR, waist-to-height ratio; ∑SF, sum of skinfolds. Note: Comparisons were performed by ANOVA 1-way with Bonferroni post hoc for continuous variables and by X2 for categorical variables. α = .05. Continuous data are expressed as mean (SD) or as median and interquartile range (P25–P75); categorical variables are presented as absolute and relative frequency.

Adherence to protocols was greater in the intervention groups (87% for AERO and 83% for COMBI) than in the CON (73%) group (P = .002). Also, weekly frequency and duration were higher in the intervention groups (2.5 sessions/wk 125 min for AERO; 2.4 sessions/wk 121 min for COMBI) than in the CON group (2.1 sessions/wk 103 min; P < .001).

Regarding the outcomes analyzed in the present study, the PP analysis of CRF, represented by VO2peak, demonstrated that the 3 groups had their values increased after the 15 weeks of intervention (P = .043) with no difference between groups (P = .151). On the other hand, in ITT analysis, there was a time × group interaction (P = .045) showing that only the AERO (P = .004) and COMBI (P = .006) groups increased their VO2peak values, which did not occur in the CON (P = .998) group. VO2VT2 increased in all groups, demonstrated in both PP (P = .006) and ITT analyses (P = .004) with no difference between them (P = .489 and P = .227 for PP and ITT, respectively). Differently, %VO2LV2 was not modified throughout the study in any group, regardless of the analysis performed (P = .496 and P = .460 for PP and ITT, respectively). Moreover, %VO2LV2 results showed a significant group effect in PP analysis (P = .023) in which the post hoc test showed that the COMBI group presented a tendency of difference when compared with AERO (P = .073) and with CON (P = .057). In addition, HRrest did not demonstrate any difference after the 15 weeks in PP analysis (P = .652), unlike the ITT analysis findings, which demonstrated reductions in all the groups (P = .004) with no difference between them (P = .703). The results of all CRF outcomes are presented in Table 4.

Table 4

Outcomes (VO2peak, VO2VT2, %VO2VT2, and HRrest) at Baseline and After 15 Weeks: Within- and Between-Group Changes Using PP and ITT Analyses

Outcomes (analyses)Group (n)Baseline15 wkMean differenceCohen d
VO2peakAERO (13)33.01 (1.62)36.25 (1.90)*3.240.63 (−0.12 to 1.38)
mL·kg−1·min−1COMBI (11)34.44 (1.53)35.83 (1.49)*1.390.66 (−0.13 to 1.45)
PPCON (16)31.47 (1.50)32.00 (1.41)*0.53
VO2peakAERO (18)32.24 (1.42)36.72 (1.56)*4.480.73 (0.06 to 1.41)
mL·kg−1·min−1COMBI (17)31.87 (1.26)37.14 (1.95)*5.270.71 (0.03 to 1.40)
ITTCON (18)31.98 (1.54)32.00 (1.41)0.02
VO2VT2AERO (13)23.68 (1.19)26.63 (1.39)*2.950.47 (−0.28 to 1.21)
mL·kg−1·min−1COMBI (11)22.67 (0.93)24.72 (1.15)*2.050.13 (−0.64 to 0.90)
PPCON (16)23.05 (1.14)24.05 (1.30)*1.00
VO2VT2AERO (18)24.05 (0.90)27.43 (1.50)*3.380.56 (−0.11 to 1.22)
mL·kg−1·min−1COMBI (17)22.74 (0.77)24.72 (1.15)*1.980.13 (−0.54 to 0.79)
ITTCON (18)23.08 (1.10)24.05 (1.30)*0.97
%VO2VT2AERO (13)71.90 (1.37)a73.93 (2.86)a2.030.02 (−0.71 to 0.75)
%COMBI (11)67.32 (2.43)b67.73 (2.56)b0.410.72 (−0.08 to 1.51)
PPCON (16)72.59 (2.56)a73.75 (1.81)a1.16
%VO2VT2AERO (18)76.09 (2.07)74.19 (2.65)−1.900.04 (−0.61 to 0.70)
%COMBI (17)71.84 (2.51)67.73 (2.56)−4.110.64 (−0.04 to 1.32)
ITTCON (18)71.68 (2.16)73.75 (1.81)2.07
HRrestAERO (13)75.16 (4.05)70.41 (3.95)−4.750.15 (−0.61 to 0.91)
bpmCOMBI (11)71.36 (2.87)67.63 (2.48)−3.730.41 (−0.39 to 1.21)
PPCON (14)71.92 (3.32)72.64 (3.54)0.72
HRrestAERO (18)77.21 (3.54)69.84 (3.68)*−7.370.18 (−0.48 to 0.83)
bpmCOMBI (17)74.47 (2.73)67.63 (2.48)*−6.840.38 (−0.29 to 1.05)
ITTCON (18)74.50 (3.07)72.64 (3.54)*−1.86

Abbreviations: AERO, aerobic group; bpm, beats per minute; COMBI, combined group; CON, control group; ITT, intention-of-treat; PP, per-protocol; VO2peak, peak oxygen consumption; VO2VT2, oxygen consumption in the second ventilatory threshold; %VO2VT2, percentage of peak oxygen consumption in the second ventilatory threshold; HRrest, resting heart rate. Note: Effect sizes are representing differences of intervention (AERO and COMBI) groups versus the CON group. Data are reported as mean and standard error. Effect sizes were calculated using Cohen d test and lower and upper limits.

*Significant difference between baseline versus 15 weeks. %VO2VT2–Different superscripts letters in the columns (a vs b) indicate significant difference between the AERO and the COMBI groups (P = .073) and between the COMBI and the CON groups (P = .057) in PP analysis. Generalized estimated equation; Bonferroni post hoc tests. α = .05.

In the AERO group, one patient’s CRF evaluation was not considered as a maximal test, and for this reason this value was not included in the analysis. Moreover, 4 patients (2 from COMBI, 1 from AERO, and 1 from CON) did not attend CRF assessments.

Discussion

The protocols adopted in the aquatic training groups and in the immersion procedure promoted beneficial effects on CRF in patients with T2D. In an analysis of the training variables in this scenario, we believe our proposal was innovative as it was performed with upright water-based exercises, utilized an acyclic activity that uses different muscle groups, favored a continuous training with progression of exercise intensity, and was well tolerated by the patients.

Regarding VO2peak, PP analysis demonstrated increases in the 3 groups, whereas ITT analysis demonstrated improvements only in the exercise training groups. Although the PP analysis demonstrated no difference between groups, the magnitude of difference was dramatically different between them: the AERO and COMBI groups had 3.24 and 1.39 mL·kg−1·min−1 of improvement, respectively, and the CON group only increased 0.53 mL·kg−1·min−1. These different magnitudes are well represented by the effect sizes of the intervention groups in relation to the CON group (AERO: 0.73; COMBI: 0.71).

In an aquatic environment, the effects of isolated aerobic training or combined training on VO2peak of T2D patients are still controversial. Delevatti et al15 did not find alterations in this outcome after 12 weeks of aerobic training, whereas a slight increase was demonstrated with the aerobic training protocols conducted by Nuttamonwarakul et al.11,12 More consistent findings, similar to those found in the AERO and COMBI groups of this study, were demonstrated after 12 weeks of water-based aerobic training16 and after 813,28 and 12 weeks14 of water-based combined training in this same population. It is important to highlight that, among the aforementioned studies investigating this population, our baseline VO2peak values (>30 mL·kg·min−1) are the highest ones, which may imply a lower amplitude for improvement and strengthens our findings in which both interventions (aerobic and combined) resulted in relevant improvement in this important outcome. In addition, our results are in accordance with a meta-analysis conducted by Yang et al,29 which analyzed 259 patients with T2D performing aerobic training and showed an increase of 3.10 mL·kg−1·min−1 in VO2peak, similar to that found by our study in the AERO group (PP analysis, 3.24 mL·kg−1·min−1).

An important discussion on VO2peak improvement found in a recent study28 can be carried out regarding the intervention period, because although our study showed cardiorespiratory improvements in 15 weeks, Scheer et al28 found important VO2peak (3 mL·kg−1·min−1) increase in only 8 weeks with weekly frequency and duration similar to our study.

Patients with T2D have an increased risk of cardiovascular and all-cause mortality and usually have low CRF.30,31 Faced with that, it is desirable that physical exercise interventions with this population strengthen the existing inverse relationship between CRF and mortality. Thus, our results have important clinical relevance, given that low CRF is an independent risk factor for cardiovascular disease in patients with T2D,2 and better CRF is associated with lower risk of all-cause mortality.1

Similarly to VO2peak, our results showed that VO2VT2 also increased in all groups, which was confirmed by both PP and ITT analyses. Although there was no statistical difference between the groups, both analyses presented magnitudes of effect favoring the AERO and COMBI groups in that the AERO group presented VO2VT2 increments of approximately 1 metabolic equivalent (MET) (3.5 mL·kg−1·min−1), the COMBI group presented increments of approximately 2.0 mL·kg−1·min−1, and CON of only 1.0 mL·kg−1·min−1. These results can be clinically confirmed by the effect sizes of the intervention groups in relation to the CON group (AERO, PP: 0.47 and ITT: 0.13; COMBI, PP: 0.56 and ITT: 0.13).

A clinical discussion regarding VO2VT2 improvement is still difficult because this outcome is poorly investigated in studies with exercise training in patients with diabetes. However, as CRF, represented by METs or VO2peak, has been constantly valued as protection for mortality in the cardiometabolic context,32,33 we believe that oxygen uptake in ventilatory thresholds will also be investigated in future cohort and clinical studies. Indeed, the improvement in this outcome may reflect an increased ability to perform daily living activities, because until they reach the second ventilatory threshold patients do not require a high anaerobic contribution, which implies glucose consumption by the muscles without significant glycemic counter regulation.34,35 Still, this improvement represents a higher tolerance to exercise, favoring the maintenance of a certain energetic contribution for longer periods.

In an aquatic environment, only Delevatti et al15 investigated this outcome and did not find alterations after 12 weeks of aerobic training. We believe that the longer intervention period (15 wk), longer sessions (50 min), and weekly duration (150 min) associated with the time spent training near the VT (5 vs 3 wk) may explain the different results. In a dry-land environment, a great clinical trial (Health Benefits of Aerobic and Resistance Training in Individuals with T2D—HART-D)36 performed structured aerobic and combined training interventions similar to the present study, with 150 weekly minutes for the aerobic training group and 110 minutes of aerobic training and 35 minutes of resistance training for the combined group. A supplementary manuscript of this trial demonstrated that both the aerobic and combined training groups increased their time (in seconds) to reach the VT.37 The authors called this outcome exercise efficiency.

When analyzing %VO2VT2, our study only demonstrated a group effect in PP analysis; however, the post hoc only showed marginally significant differences, representing lower values in COMBI in comparison with the other groups. The lack of difference after the 15 weeks may be understood by the similar behavior in VO2peak and VO2VT2 because when both are similarly altered, a change in %VO2VT2 is not expected. These results differ from the %VO2VT2 increase demonstrated by Delevatti et al,15 possibly because significant differences in VO2peak and VO2VT2 were not found in this study, only a slight transition of VO2VT2 in relation to %VO2peak, which determined the %VO2VT2 increase.

Regarding the HRrest results, the present study found a reduction in HRrest resulting from the interventions proposed only in ITT analysis with no difference between groups. This result may have occurred because of the higher pretraining values found and the greater sample size in ITT analysis. Although the efficacy was not confirmed by PP analysis, the behavior of the HRrest mean values differs between the 2 structured exercise groups and the CON group, because although the CON group presented an increase of 0.73 bpm in PP analysis and a reduction of −1.86 bpm in ITT analysis, the intervention groups demonstrated reductions between −3.73 and −7.37 bpm, considering both analyses. Recently, Cugusi et al14 also did not find significant results in this outcome with water-based combined training in patients with T2D, even with preintervention values well above those found in the present study (89 bpm). On the other hand, Nuttamonwarakul et al11,12 demonstrated reductions around 9 bpm in the HRrest of this population after water-based aerobic training. In this study,11 HR after intervention was 73 bpm, which was very similar to values in our study in the preintervention moment. In addition, Delevatti et al,15 Suntraluck et al,16 and Conners et al38 had similar preintervention values to those of the present study and also demonstrated significant reductions in the HRrest (reductions of −5.30 and – 6.50 in PP and ITT analyses, respectively),15 −7 bpm16 and −8 bpm.38

When analyzing all studies evaluating this outcome after water-based exercise training in patients with diabetes, aerobic training seems to be the most suitable, with more evident changes in those with higher HRrest (eg, a decrease in HRrest values to close to 67 bpm, at which point a stabilization is perceived). This behavior was also recently demonstrated with dyslipidemic women after water-based exercise training39 wherein the aerobic training group showed a behavior similar to that found in the AERO and COMBI groups of the present study, beginning the intervention with an HRrest of 72 bpm and ending with 68bpm, corroborating the supposed “limit” of improvement observed in studies with T2D.

This study has some limitations, such as the lack of a systematic record of the exercise intensities reached during the aerobic component of the sessions, the number of sample losses, and the low adherence of some patients from the AERO and COMBI groups, which promoted a lower sample size than that previously calculated, especially in PP analysis. Some strengths should also be emphasized, such as methodological aspects regarding the presentation of results by PP and ITT analyses as well as the randomization description and the control procedure with immersion for a similar time to the exercise groups. Regarding the interventions, we highlight the control of training variables, with linear progression of the intensity throughout the mesocycles in which the aerobic training intensity was determined by an easy application and low-cost method (heart rate deflection point). Future research should, with similar methodological design, evaluate other important health outcomes, such as metabolic, neuromuscular, and psychosocial outcomes as well as other training protocols with different periodization designs.

Conclusions

Our results allow us to conclude that aquatic aerobic and combined training in an upright position improves CRF, especially the VO2peak, of patients with T2D, which has important clinical relevance.

Acknowledgments

The authors would like to acknowledge the collaboration of all participants of this study. The authors also would like to acknowledge the support that was given by the organizations CAPES and CNPq. ClinicalTrials.gov (NCT02612805).

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    Almada BP, Kanitz AC, Alberton CL, Zaffari P, Pinto SS, Kruel LFM. Respostas cardiorrespiratórias de seis exercícios de hidroginástica realizados por mulheres pós-menopáusicas. Rev Bras Ativ Fis Saúde. 2014;19(3):333341.

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    Earnest CP, Johannsen NM, Swift DL, et al. Aerobic and strength training in concomitant metabolic syndrome and type 2 diabetes. Med Sci Sports Exerc. 2014;46(7):12931301. PubMed ID: 24389523 doi:10.1249/MSS.0000000000000242

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If the inline PDF is not rendering correctly, you can download the PDF file here.

Delevatti is with the Department of Physical Education, Universidade Federal de Santa Catarina (UFSC), Florianópolis, Brazil. Kanitz, Bracht, Lisboa, Marson, Reichert, Bones, and Kruel are with the Department of Physical Education, Physiotherapy and Dance, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, Brazil.

Bracht (claudiagbracht@gmail.com) is corresponding author.
  • View in gallery

    —Flow of participants throughout the study. AERO, aerobic aquatic training group; COMBI, combined aquatic training group; CON, control group; ITT, intention-of-treat; PP, per-protocol.

  • 1.

    Kodama S, Saito K, Tanaka S, et al. Cardiorespiratory fitness as a quantitative predictor of all-cause mortality and cardiovascular events in healthy men and women: a meta-analysis. JAMA. 2009;301(19):20242035. PubMed ID: 19454641 doi:10.1001/jama.2009.681

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Johannsen NM, Swift DL, Lavie CJ, Earnest CP, Blair SN, Church TS. Categorical analysis of the impact of aerobic and resistance exercise training, alone and in combination, on cardiorespiratory fitness levels in patients with type 2 diabetes: results from the HART-D study. Diabetes Care. 2013;36(10):33053312. PubMed ID: 23877979 doi:10.2337/dc12-2194

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    American Diabetes Association Guidelines. Standards of medical care in diabetes. Diabetes Care. 2020;43(suppl 1):S1S212.

  • 4.

    Boulé NG, Kenny GP, Haddad E, Wells GA, Sigal RJ. Meta-analysis of the effect of structured exercise training on cardiorespiratory fitness in Type 2 diabetes mellitus. Diabetologia. 2003;46(8):10711081. PubMed ID: 12856082

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Larose J, Sigal RJ, Khandwala F, Prud’homme D, Boulé NG, Kenny GP. Associations between physical fitness and HbA1c in type 2 diabetes mellitus. Diabetologia. 2011;54(1):93102. PubMed ID: 20953579 doi:10.1007/s00125-010-1941-3

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Farag YMK, Gaballa MR. Diabesity: an overview of a rising epidemic. Nephrol Dial Transplant. 2011;26(1):2835. PubMed ID: 21045078 doi:10.1093/ndt/gfq576

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Delevatti RS, Alberton CL, Kanitz AC, Marson EC, Kruel LFM. Vertical ground reaction force during land- and water-based exercise performed by patients with type 2 diabetes. Med Sportiva. 2015;11(1):25012508.

    • Search Google Scholar
    • Export Citation
  • 8.

    Delevatti RS, Pinho CDF, Kanitz AC, et al. Glycemic reductions following water- and land-based exercise in patients with type 2 diabetes mellitus. Complement Ther Clin Pract. 2016;24:7377. PubMed ID: 27502804 doi:10.1016/j.ctcp.2016.05.008

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Epstein M. Renal effects of head-out water immersion in humans: a 15-year update. Physiol Rev. 1992;72(3):563621. PubMed ID: 1626032 doi:10.1152/physrev.1992.72.3.563

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Pendergast DR, Moon RE, Krasney JJ, Held HE, Zamparo P. Human physiology in an aquatic environment. Compr Physiol. 2015;5:17051750. PubMed ID: 26426465

    • Search Google Scholar
    • Export Citation
  • 11.

    Nuttamonwarakul A, Amatyakul S, Suksom D. Twelve weeks of aqua-aerobic exercise improve physiological adaptations and glycemic control in elderly patients with type 2 diabetes. J Exerc Physiol Online. 2012;15(2):6470.

    • Search Google Scholar
    • Export Citation
  • 12.

    Nuttamonwarakul A, Amatyakul S, Suksom D. Effects of water-based versus land-based exercise training on cutaneous microvascular reactivity and C-reactive protein in older women with type 2 diabetes mellitus. J Exerc Physiol Online. 2014;17(4):2733.

    • Search Google Scholar
    • Export Citation
  • 13.

    Asa C, Maria S, Katharina SS, Bert A. Aquatic exercise is effective in improving exercise performance in patients with heart failure and type 2 diabetes mellitus. Evid Based Complement Alternat Med. 2012;2012:349209. PubMed ID: 22593770

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Cugusi L, Cadeddu C, Nocco S, et al. Effects of an aquatic-based exercise program to improve cardiometabolic profile, quality of life, and physical activity levels in men with type 2 diabetes mellitus. PM R. 2015;7(2):141148. PubMed ID: 25217820 doi:10.1016/j.pmrj.2014.09.004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Delevatti RS, Kanitz AC, Alberton CL, et al. Glucose control can be similarly improved after aquatic or dry-land aerobic training in patients with type 2 diabetes: a randomized clinical Trial. J Sci Med Sport. 2016;19(8):688693. PubMed ID: 26777722 doi:10.1016/j.jsams.2015.10.008

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Suntraluck S, Tanaka H, Suksom D. The relative efficacy of land-based and water-based exercise training on macro- and micro-vascular functions in older patients with type 2 diabetes. J Aging Phys Act. 2017;25(3):446452. doi:10.1123/japa.2016-0193

    • Search Google Scholar
    • Export Citation
  • 17.

    Boutron I, Altman DG, Moher D, Schulz KF, Ravaud P, CONSORT NPT Group. CONSORT statement for randomized trials of nonpharmacologic treatments: a 2017 update and a CONSORT extension for nonpharmacologic trial abstracts. Ann Intern Med. 2017;167(1):4047. PubMed ID: 28630973 doi:10.7326/M17-0046

    • Search Google Scholar
    • Export Citation
  • 18.

    Meara E, Chong K, Gardner R, Jardine AG, Neill JB, McDonagh TA. The Modification of Diet in Renal Disease (MDRD) equations provide valid estimations of glomerular filtration rates in patients with advanced heart failure. Eur J Heart Fail. 2006;8(1):6367. doi:10.1016/j.ejheart.2005.04.013

    • Search Google Scholar
    • Export Citation
  • 19.

    Delevatti RS, Kanitz AC, Alberton CL, et al. Heart rate deflection point as an alternative method to identify the anaerobic threshold in patients with type 2 diabetes. Apunts Med Sport. 2015;50(188):123128.

    • Search Google Scholar
    • Export Citation
  • 20.

    Almada BP, Kanitz AC, Alberton CL, Zaffari P, Pinto SS, Kruel LFM. Respostas cardiorrespiratórias de seis exercícios de hidroginástica realizados por mulheres pós-menopáusicas. Rev Bras Ativ Fis Saúde. 2014;19(3):333341.

    • Search Google Scholar
    • Export Citation
  • 21.

    Alberton CL, Kanitz AC, Pinto SS, et al. Determining the anaerobic threshold in water aerobic exercises: a comparison between the heart rate deflection point and the ventilatory method. J Sports Med Phys Fitness. 2013;53(4):358367. PubMed ID: 23828283

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Petroski EL, Pires-Neto CS. Validação de equações antropométricas para a estimativa da densidade corporal em mulheres. Rev Bras Ativ Fis Saúde. 1995;1(2):6573.

    • Search Google Scholar
    • Export Citation
  • 23.

    Siri WE. Body composition from fluid spaces and density: analysis of methods. Nutrition. 1993;9(5):480491. PubMed ID: 8286893

  • 24.

    Wasserman K, Whipp BJ, Koyal SN, Beaver WL. Anaerobic threshold and respiratory gas exchange during exercise. J Appl Physiol. 1973;35(2):236243. PubMed ID: 4723033 doi:10.1152/jappl.1973.35.2.236

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Howley ET, Basset DR Jr, Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc. 1995;27(9):12921301. PubMed ID: 8531628 doi:10.1249/00005768-199509000-00009

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Cohen J. Statistical Power Analysis for the Behavioral Sciences. New York, NY: Lawrence Erlbaum Associates; 1988.

  • 27.

    Montgomery DC. Design and Analysis of Experiments. New York, NY: Wiley; 1991.

  • 28.

    Scheer AS, Naylor LH, Gan SK, et al. The effects of water-based exercise training in people with type 2 diabetes. Med Sci Sports Exerc. 2020;52(2):417424. PubMed ID: 31469709 doi:10.1249/MSS.0000000000002133

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Yang Z, Scott CA, Mao C, Tang J, Farmer AJ. Resistance exercise versus aerobic exercise for type 2 diabetes: a systematic review and meta-analysis. Sports Med. 2014;44(4):487499. PubMed ID: 24297743 doi:10.1007/s40279-013-0128-8

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Sui X, Lamonte MJ, Blair SN. Cardiorespiratory fitness as a predictor of nonfatal cardiovascular events in asymptomatic women and men. Am J Epidemiol. 2007;165(12):14131423. PubMed ID: 17406007 doi:10.1093/aje/kwm031

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Katzmarzyk PT, Church TS, Janssen I, Ross R, Blair SN. Metabolic syndrome, obesity, and mortality: impact of cardiorespiratory fitness. Diabetes Care. 2005;28(2):391397. PubMed ID: 15677798 doi:10.2337/diacare.28.2.391

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Wei M, Kampert JB, Barlow CE, et al. Relationship between low cardiorespiratory fitness and mortality in normal-weight, overweight, and obese men. JAMA. 1999;282(16):15471553. PubMed ID: 10546694 doi:10.1001/jama.282.16.1547

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Pavón DJ, Artero EG, Lee DC, et al. Cardiorespiratory fitness and risk of sudden cardiac death in men and women in the United States: a prospective evaluation from the aerobics center longitudinal study. Mayo Clin Proc. 2016;91(7):849857. doi:10.1016/j.mayocp.2016.04.025

    • Search Google Scholar
    • Export Citation
  • 34.

    Simões HG, Campbell CS, Kokubun E, Denadai BS, Baldissera V. Blood glucose responses in humans mirror lactate responses for individual anaerobic threshold and for lactate minimum in track tests. Eur J Appl Physiol. 1999;80(1):3440. doi:10.1007/s004210050555

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Simões HG, Campbell CS, Kushnick MR, et al. Blood glucose threshold and the metabolic responses to incremental exercise tests with and without prior lactic acidosis induction. Eur J Appl Physiol. 2003;89(6):60311. PubMed ID: 12759761

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Church TS, Blair SN, Cocreham S, et al. Effects of aerobic and resistance training on hemoglobin A1c levels in patients with type 2 diabetes. JAMA. 2010;304(20):22532262. PubMed ID: 21098771 doi:10.1001/jama.2010.1710

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Earnest CP, Johannsen NM, Swift DL, et al. Aerobic and strength training in concomitant metabolic syndrome and type 2 diabetes. Med Sci Sports Exerc. 2014;46(7):12931301. PubMed ID: 24389523 doi:10.1249/MSS.0000000000000242

    • PubMed
    • Search Google Scholar
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  • 38.

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