Acute Effects of Different Intensities of Resistance Training on ...

Research in Sports Medicine, 22:75–87, 2014 Copyright © Taylor & Francis Group, LLC ISSN: 1543-8627 print/1543-8635 online DOI: 10.1080/15438627.2013.852096

Acute Effects of Different Intensities of Resistance Training on Glycemic Fluctuations in Patients With Type 1 Diabetes Mellitus ANA PAULA S. SILVEIRA Sport Sciences Departament, Trás os Montes e Alto Douro University, Vila Real, Portugal

CLAUDIO MELIBEU BENTES Physical Education, Graduate Program, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil

PABLO B. COSTA Human Performance Laboratory, Department of Kinesiology, California State University—San Bernardino, San Bernardino, California, USA

ROBERTO SIMÃO Physical Education, Graduate Program, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil

FRANCICARLOS C. SILVA Physical Education, Graduate Program, Montes Claros State University, Minas Gerais, Brazil

RODRIGO P. SILVA University Sports Center, Ouro Preto Federal University, Ouro Preto, Minas Gerais, Brazil

JEFFERSON S. NOVAES Physical Education, Graduate Program, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil

Six men and six women (24.4 ± 6.4 years) who had been diagnosed with T1D for 7.3 ± 6.8 years volunteered for the study. Three RT sessions were repeated with the same experimental approach with randomized load percentages. Blood glucose measurements

Received 14 January 2013; accepted 30 July 2013. Address correspondence to Claudio Melibeu Bentes, Federal University of Rio de Janeiro, Graduate Program, Avenida Pau Brasil 540, Ilha do Fundão, Rio de Janeiro, Brazil, 21941-590. E-mail: [email protected] 75

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were performed at rest, after warm-up, immediately after the last set of each exercise, and 10, 20, and 30 minutes after the exercise session. Significant decreases from rest for blood glucose concentration in each intensity vs. post warm-up, immediately post exercise session, and 10, 20 and 30 minutes after total training session were observed. Effect size (ES) results for the 60 and 80% of 1RM intensities demonstrated large magnitudes. The three intensities investigated promoted a reduction in blood glucose levels and therefore can be recommended for diabetic patients. In addition, the moderate and high intensities appear to lower blood glucose levels to a greater extent than the low intensity. KEYWORDS glucose control, glycemic control, weight training, strength training

INTRODUCTION Diabetes mellitus (DM) is a glucose metabolic disease caused by insulin resistance or no insulin production. The American College of Sports Medicine (ACSM) and the American Diabetes Association (ADA) endorse exercise as a treatment method for individuals with type 1 diabetes mellitus (T1D) and currently recommend expending a minimum cumulative total of 1000 kcal/week or 150 min per week of moderate intensity aerobic physical activity, 90 min per week of vigorous aerobic exercise, or both (Albright et al., 2000; Sigal, Kenny, Wasserman, Castaneda-Sceppa, & White, 2006). Accordingly, aerobic exercise has been the main focus of exercise-training studies due to consistent findings of improved glucose control. Although physical activity has been associated with a reduction in cardiovascular mortality in T1D subjects (Cheng et al., 2003), conflicting data have been reported regarding the benefits of physical activity on metabolic control in these individuals (Chimen et al., 2012). Nevertheless, including resistance training in a physical exercise program for subjects with T1D is recommended for minimizing cardiac risks and increasing muscle strength, and it appears to improve the body’s resistance to insulin (Albright et al., 2000). In addition, increasing muscle strength is generally deemed as an important consideration for training programs with the purpose of improving general health, physical fitness, and performance (Chaves et al., 2013). A considerable amount of research has analyzed the relationship between glycemic control and physical exercise (Marcus et al., 2013). For instance, D’Hooge et al. (2011) examined the effects of combined exercise training on metabolic control, physical fitness, and quality of life in adolescents with T1D. Sixteen children were randomly assigned to a control group or an intervention group. In the intervention group, subjects participated

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twice a week for 20 weeks in the combined aerobic and resistance training group, while the control group continued their normal daily activities. The results showed no significant anthropometric, glycemia, or HbA1c changes. The daily doses of insulin injected were lowered significantly in the training group, however, from pre- to post-training (0.96 IU/kg·day vs. 0.90 IU/kg·day, respectively), whereas it increased in the control group. Jimenez, Santiago, Sitler, Boden, and Homko (2009) investigated the insulin-sensitivity response to a single bout of resistance training in T1D in active subjects. Their results showed no differences between the training group (1RM test) and a control group (without training). These results indicate a single bout of vigorous resistance training does not alter insulin sensitivity in people with T1D. In addition, no significant differences in blood glucose were reported. Similarly, Ramalho et al. (2006) examined the effects of aerobic training versus resistance training on metabolic control in nonactive T1D subjects, ranging in age from 13 to 30, who underwent a 12-week aerobic exercise or resistance training program. The aerobic training group (ATG) program consisted of a 40-min walk or run, and the resistance training group (RTG) program consisted of resistance exercises three times a week. Blood samples were obtained before and after the 12-week training period. The results demonstrated no changes in the ATG for glycated hemoglobin, lipid profile, fasting glucose level, or body mass index (BMI). There were reductions, however, in hip circumference and in average self-monitored blood glucose levels, measured after each exercise session. In the RTG, there were no changes in the parameters assessed. Further, the total insulin dosage was reduced in both groups. There is still conflicting evidence concerning the beneficial effects of exercise on glycemic control in T1D subjects. Nevertheless, the question remains regarding which type of activity is more appropriate. Several adaptations have been promoted with RT exercises in subjects with T1D, especially regarding glucose control. The literature on this topic, however, is still scarce. For instance, it is unclear what intensity should be prescribed for a resistance training program. Most of the evidence on the use of RT in patients with T1D is associated with aerobic exercise (Chimen et al., 2012; Kennedy et al., 2013). Moreover, the results in patients with type 2 diabetes show excellent acute results (Kennedy et al., 2013; Koivula, Tornberg, & Franks, 2013; Umpierre, Ribeiro, Schaan, & Ribeiro, 2013; Zanuso, Jimenez, Pugliese, Corigliano, & Balducci, 2010). The literature on exercise, however, requires more investigations with resistance training in isolation. In addition, this is a public health issue, since the population of T1D has been increasing worldwide (Egro, 2013). Little is known about the efficiency of resistance training intensity on glycemic control responses in individuals with T1D. Scarcity in the literature surrounding the use of this exercise type suggests the need to further examine its use and impact. Different intensities and percentage of

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workload in a resistance training program require further investigation in order for their benefits and proper applications to be elucidated. Therefore, the aim of this study was to compare the acute effects of different resistance training intensities (40%, 60%, and 80% of 1RM) on glycemic fluctuations in subjects with T1D.

METHODS Subjects Six men and six women with a mean age of 24.4 (± SD) ± 6.4 years, who had been diagnosed with T1D for 7.3 ± 6.8 years (Table 1), participated in the study. The subjects with T1D were recruited after a medical evaluation if they were considered able to perform physical activity without any physical exercise experience, and used Neutral Protamine Hagedorn (NPH) associated or nonassociated with the other rapid-acting insulin or ultrafast. The exclusion criteria for the study follow: subjects who had complications resulting from chronic hyperglycemia and were not treated with a daily insulin application or with the dosage adequately established by a physician. Subjects answered the Physical Activity Readiness Questionnaire and signed an informed consent form before participation. This study was approved by the Institutional Ethics Committee under study protocol 009/08.

One Repetition Maximum Testing (1RM) The 1RM test to measure muscle strength was performed to determine maximum strength (Kraemer & Ratamess, 2004). To determine reliability, a 1RM test and retest were conducted for all exercises (Ploutz-Snyder & Giamis, 2001). There were training protocols on nonconsecutive days, changing only the percentage of maximum load (i.e., 40%, 60%, and 80% of 1 RM). The TABLE 1 Physical Characteristics of the Participants (n = 6 Male and 6 Female) Variable Age (year) Diagnosis time (year) Body mass (kg) Height (m) BMI (kg/m2 ) % fat Resting blood glucose at 40%1RM (mg/dl) Resting blood glucose at 60%1RM (mg/dl) Resting blood glucose at 80%1RM (mg/dl) BMI = body mass index; SD = standard deviation. ∗ Significant difference in normality test (Shapiro-Wilk) p < 0.05.

Mean ± SD 24.4 ± 6.4 7.3 ± 6.8∗ 63.0 ± 13.3 1.7 ± 0.08 21.3 ± 2.9 17.9 ± 9.4 146.0 ± 10.8∗ 170.2 ± 11.9∗ 162.9 ± 11.3∗


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capillary blood glucose measurements were performed at rest, after warmup, immediately after the last set of each exercise, and 10, 20, and 30 minutes after the exercise session. To obtain reliable 1RM loads, data were assessed during two nonconsecutive days following the exercise sequence: chest fly exercises (CFE); leg curl (LC); lat pull down (LPD); leg extension (LE); and biceps curl (BC). During the 1RM test, each subject performed a maximum of three 1RM attempts for each exercise with 5-minute rest intervals between attempts. After the 1RM load in a specific exercise was determined, an interval of at least 10 minutes was allowed before the 1RM attempt of the next exercise. Standard exercise techniques were followed for each exercise. All subjects were asked not to exercise any of the muscle groups involved in the testing 48 hours prior to the strength assessments. The heaviest load achieved between both days was considered the 1RM. Capillary blood glucose measurements were performed before and after each test (Ploutz-Snyder & Giamis, 2001; Thompson, Gordon, & Pescatello, 2009).

Pre- and Post-Exercise Self-Monitored Blood Glucose Levels The self-monitored blood glucose levels were determined using a Johnson & Johnson One Touch Ultra 2, with disposable One Touch UltraSoft lancets and reagents strips One Touch Ultra (Lifescan, Milpitas, CA), before and after each exercise session, using blood drawn from a finger prick. Capillary blood glucose measurements were made by an experienced professional. After local cleansing, the side of the participant’s finger was lanced and the blood sample was collected at rest, after warmup, immediately after the last set of each exercise, and 10, 20, and 30 minutes after each exercise and intensity determined (Sacks et al., 2011).

Resistance Training Before the starts of each training session, a warm-up was performed in the major joints involved in the exercises. This warm-up consisted of 12 repetitions with 20% of the 1RM load of the first exercise performed. The training sessions occurred in three visits. Each visit repeated the same experimental approach with randomized load percentages (40%, 60%, and 80% of 1RM). The training sessions of individual subjects were performed at approximately the same time of the day, between 14:00 and 18:00 hrs, with the same experienced trainers. The exercises performed follow: FE, LC, PD, LE, and BC. The subjects performed three sets until muscular failure (Fleck & Kraemer, 2003). No pause was allowed between the eccentric and concentric phases or between repetitions, and the exercise sequence was the same as for

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the 1RM testing. During the execution of exercises, subjects were asked to avoid performing the valsalva maneuver. A 2 m rest interval was provided between exercises and a 48-hour rest interval was provided for each testing visit (Astorino, Martin, Schachtsiek, & Wong, 2013; Simao, Figueiredo, Leite, Jansen, & Willardson, 2012).

Statistical Analysis The statistical analysis was initially performed using the Shapiro–Wilk normality test and the homoscedasticity test (Bartlett criterion). The intraclass correlation coefficient (ICC) was used to assess the reliability of loads between test and retest of 1RM (Vincent, 1995; Weir, 2005). The serum glucose test did not demonstrate normal distribution or homoscedasticity (p < 0.05). To compare the variables (glucose at rest and after warm-up, immediately post training, 10 min, 20 min, and 30 min post training during RT sessions of 40%, 60%, and 80% of 1RM intensities), the Kruskal-Wallis nonparametric test was used, followed by the Mann–Whitney U post hoc test for the analysis of possible differences in post-exercise capillary blood glucose. Additionally, to determine the magnitude of the findings, effect sizes (the difference between pretest and posttest scores divided by the pretest SD) were calculated for the blood glucose levels for both rest intervals (Cohen, 1988; Vincent, 1995). The scale proposed by Rhea (2004) was used to classify the magnitude of the effect size (ES). The level of significance was set at p ≤ 0.05. All statistical analyses were carried out using SPSS statistical software package version 14.0 (SPSS Inc., Chicago, IL).

RESULTS The results of the test–retest reliability revealed high intraclass correlation coefficients (ICCs) for each exercise (FE = 0.976; LC =0.987; PD =0.956; LE = 0.987; and BC = 0.943) and the ICC results for resting glucose in different days for each intensity (40% of 1RM = 0.990; 60% of 1RM = 0.966; and 80% of 1RM = 0.970). In addition, paired t tests did not demonstrate significant differences between the 1RM tests for any of the exercises. Figure 1 displays the means and SD for all glucose values. There was a statistically significant difference among the different times of measurements for blood glucose for all intensities (40%, 60%, and 80% of 1RM intensity) at rest vs. 10, 20 and 30 minutes after total training session. Blood glucose decreased from rest after 10, 20, and 30 minutes post training session. The ES results for the 40% of 1RM intensity changes from rest to 10, 20, and 30 minutes after the training session showed small to moderate magnitudes. The ES results for the 60% and 80% of 1RM intensities changed from rest versus to 10, 30, and 30 minutes after the training session showed large magnitudes (Table 2).

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146.00 ± 37.65 170.25 ± 39.72 162.91 ± 37.64

ES

Immediately post training ES

10 min post training ES

20 min post training

ES

30 min post training

ES

140.16 ± 0.15 Trivial 121.25 ± 0.66 Small 113.20 ± 0.87 Moderate 108.00 ± 1.01 Moderate 104.20 ± 1.11 Moderate 35.65 28.83 24.50∗ 25.87∗ 24.59∗ 156.41 ± 0.35 Trivial 115.10 ± 1.38 Small 108.58 ± 1.55 Large 103.33 ± 1.68 Large 94.83 ± 1.85 Large 30.13 24.55 23.48∗ 24.44∗ 23.77∗ 158.25 ± 0.12 Trivial 112.91 ± 1.32 Moderate 106.00 ± 1.51 Large 100.83 ± 1.64 Large 93.50 ± 1.84 Large 34.14 27.16 24.67∗ 25.55∗ 24.70∗

Post warm-up

ES = Effect size between each moment versus resting glucose. ∗ Significant differences between each time period after session versus glucose at rest (p < 0.05).

40% of 1RM 60% of 1RM 80% of 1RM

Resistance training session Resting (%1RM) glucose

TABLE 2 Means and Standard Deviations of Blood Glucose Levels After Each Resistance Training Intensities and Effect Sizes

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DISCUSSION The present study investigated the acute effects of different resistance training intensities on glycemic fluctuations in subjects with T1D. Our results demonstrated a lower glucose concentration in all intensities until 30 minutes after training. The Kruskal-Wallis ANOVA results revealed no statistically significant differences in blood glucose levels among the three exercise intensities during each time period (rest, immediately, 10, 20, and 30 min post-exercise). The ES results, however, indicated that glycemic control in higher intensities of training (60% and 80% of 1RM) revealed large magnitudes within 30 minutes after the last exercise in resting blood glucose. In addition, the 40% of 1RM showed a moderate magnitude. Nevertheless, such results demonstrate low (40% of 1RM), moderate (60% of 1RM), and high intensities (80% of 1RM) caused a decrease in blood glucose concentration after 10 minutes. This behavior was evidenced by the constant and progressive decrease in blood glucose levels after 10 minutes of exercise in the three training intensities (Figure 1). The reduction in blood glucose might have occurred because of an acute effect of exercise. For example, an increased number of glucose transporters 4 (GLUT4) and its movement toward the plasma membrane of the muscle cell (Cauza et al., 2005; Schiavon, Gazola, Furlan, Barrena, & Bazotte, 2011), increased hexokinase activity (Murias, Kowalchuk, & Paterson, 2010), decreased free fatty acids release (Hansen, Landstad, Gundersen, Torjesen, & Svebak, 2012; Hazley, Ingle, Tsakirides, Carroll, & Nagi, 2010), and an increased blood flow causing greater glucose uptake (Behnke & Delp, 2010). Regarding GLUT4, Bienso et al. (2012) suggested the immediate biomarker for glucose transport in response to acute exercise is an AMP-activated protein kinase (AMPK), since its activation is made by changes in intracellular

FIGURE 1 Blood glucose across time in the three intensities (40, 60, and 80% of 1RM). ∗ Significant difference from rest.


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adenosine triphosphate (ATP) and adenosine monophosphate (AMP) ratio, creatine phosphate, and pH, resulting in a GLUT4 cycle increase. In addition to this mechanism, nitric oxide can also be considered an exercise biomarker for muscle glucose uptake. This mechanism, however, lacks more evidence. Another mechanism that could help explain the decrease in serum glucose is the insulin counter-regulatory hormones disturbances (catecholamines, glucagon, cortisol, and growth hormone). In diabetics, the insulinemia during exercise does not decrease, a result of insulin counter-regulatory hormones disturbances, leading to increase in blood glucose uptake by active muscle. In contrast, the inhibition in liver glucose production results in a rapid decrease in glucose concentration (Kilpatrick, Rigby, & Atkin, 2007). The glucose muscle uptake continued for 2 hours after exercise, regardless of insulin action. Only a single set, however, improved insulin sensibility for 16 hours post-exercise (Schiavon et al., 2011). The last analysis in the current study was performed using the difference between blood glucose at rest and after 30 minutes of training (Table 2). According to our results, all the intensities would be recommended for glucose control (40%, 60% and 80% of 1RM). Nevertheless, the 60% and 80% of 1RM intensities showed larger magnitudes of ES at 30 minutes after the total training session. Nonetheless, no significant differences among intensities after 30 minutes post total session were observed. Therefore, after exercise, more recovery is necessary to restore muscle and liver glycogen used during the resistance training session, leading to more glucose inflow to restore muscle and liver glycogen reserves. For instance, Dunstan et al. (2002) reported high intensity resistance training, with 3 sets of 8–10 repetitions and 8 exercises, was effective in glucose control, muscular strength gains, glycated hemoglobin control, and decrease in abdominal fat. The present study demonstrated higher intensities of resistance training sessions (60% and 80% of 1RM) could be more efficient in glucose control based in ES results. Although these findings are an acute effect of a resistance training session, they corroborate with resistance training chronic responses, where adaptations can improve the health and modify the lifestyle in subjects with T1D. The blood glucose is controlled by the autonomic nervous system activity and metabolic hormone action (insulin, glucagon, catecholamines, and growth hormone). Therefore, it is controlled by the neuroendocrine system (Coker & Kjaer, 2005; Hackney, 2006). The neuroendocrine control, specifically the nervous system, may also help explain the higher percentage decrease in glucose with the moderate and high intensities in this study. As a preventive measure for hypoglycemia during or after resistance exercise, it was determined that if a participant tested with a pre-exercise blood glucose level of less than 100mg/dl, the participant would ingest 15 grams of simple carbohydrates. This procedure was performed four times throughout the data collection period. Hence, the participant started the exercise session with blood glucose levels between 100mg/dl and 250mg/dl,

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aiming to avoid hypoglycemia (Colberg, 2000). Thus, the supervision received by participants to maintain dietary patterns appeared to have been sufficient to ensure the pre-exercise blood glucose control. The small sample size and the variability in resting blood glucose levels among participants could be a potential limitation in the method of measuring blood glucose level. In addition, the glycemic collection in the present study was made by One Touch Ultra 2 glucometer test and One Touch Ultra reagent strips (Lifescan, Milpitas, CA, USA), which may have caused measurement errors. Although this instrument is not considered the gold standard, according to the World Health Organization (Alberti & Zimmet, 1998), it is a quite accurate glucose meter featuring a coefficient of variation of 5%. Accordingly, the result of the reliability of the glucose measurement reported was high. Resistance training sessions with different training manipulations (muscle actions, loading, volume, exercise selection and orders, rest periods, repitition velocity, and frequency) need further examination. It is suggested that future research investigate the different training variations on blood pressure responses and hormonal responses to further assist in the identification of the value and proper implementation of these training methods.

CONCLUSIONS In conclusion, the three intensities investigated promoted a reduction of blood glucose levels and therefore can be recommended for diabetic subjects. The moderate and high intensities had a greater magnitude in ES (large) when compared with the low intensity, which were small to moderate. Moreover, the reduction between the intensities of 60% and 80% of 1RM did not differ significantly. Such information is useful for a practical exercise prescription of resistance training for subjects with diabetes (Colberg, 2000). It is important to assess the individual’s fitness level to select the most appropriate intensity for exercise prescription. Thus, sedentary individuals may use a lower intensity (40% of a 1RM). Subjects with T1D without any contraindication, however, might be prescribed higher intensities (60% and 80%1RM) for glucose control.

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