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Effects of passive static stretching on blood glucose levels in patients with type 2 diabetes mellitus

[Purpose] This study determined the effects of passive static stretching on blood glucose levels in patients with type 2 diabetes. [Subjects] Fifteen patients (8 males and 7 females) with type 2 diabetes were recruited and randomly assigned to the control group or passive static stretching group. [Methods] Glycated hemoglobin was measured before and after the 8-week training period. [Results] Glycated hemoglobin levels decreased significantly in the passive static stretching group, and there were significant differences in blood glucose levels between the 2 groups. [Conclusion] Passive static stretching of the skeletal muscles may be an alternative to exercise to help regulate blood glucose levels in diabetes patients.


INTRODUCTION
The incidence of diabetes mellitus is increasing worldwide; this trend is particularly strong for type 2 diabetes mellitus (T2DM) 1) . T2DM is a chronic disease characterized by decreased insulin sensitivity and overall poor glucose control. Exercise is a generally accepted component of the nonpharmacologic treatment for T2DM 2) . The systematic review by Boule et al. indicates structured exercise programs have a statistically and clinically significant beneficial effect on glycemic control in patients with T2DM 3) . In addition, patients with T2DM who use insulin, low-intensity exercise significantly reduces the prevalence of hyperglycemia 4) .
Despite the benefits of physical activity, many people with T2DM do not exercise regularly. For some individuals, secondary diabetes-related complications such as lower-limb amputations, neuropathies, hypertension, nephropathies, and retinopathies can either contraindicate exercise or make it more difficult. In addition, many elderly people with T2DM do not have sufficient physical ability to perform aerobic exercise and thus have problems maintaining euglycemia 5) .
Passive static stretching occurs when sustained tension develops within a person's muscles through external forces. Several studies suggest passive stretching can increase cellular glucose uptake. Accordingly, blood glucose levels could decrease following a program of successive sustained muscle stretching. In addition, because passive stretching re-quires minimum effort by the person performing the stretch, people with T2DM who are reluctant or unable to exercise may be willing to follow a stretching protocol 6) . Therefore, this study determined the effect of passive static stretching on blood glucose levels in people with T2DM.

SUBJECTS AND METHODS
Fifteen in-patients with T2DM at a hospital in Busan, Korea participated in this study. Patients were eligible if they were sedentary (i.e., not participating in regular aerobic or strengthening exercises 6 months before the study) and willing to commit to an 8-week supervised exercise program 7) . All patients were diagnosed with T2DM confirmed by a glycated hemoglobin (HbA1c) level 6.5% or higher as a criterion for the diagnosis of diabetes 8) . All patients meeting the inclusion criteria were given verbal and written information about this study. The patients provided informed consent prior to participating. The study protocol was approved by the Ethics Committee of Daegu University.
Patients were randomized to the control group (n = 7) or passive static stretching group (PSS, n = 8). The control group was instructed to maintain their diet and medications for diabetes and not to perform any exercise during the experiment. Meanwhile, patients in the PSS group followed the same instructions as the control group but received a 40-minute intervention consisting of 6 lower-body and 4 upper-body static passive stretches. For each stretch, the muscle was held in the stretched position for 30 seconds and was repeated 4 times. Each repetition was separated by a 15-second relaxation period, and different stretches were separated by a minimum of 1 minute. A description of stretch is provided in Table 1 6) . The PSS group performed the stretches 3 times per week for 8 weeks.
For outcome measurements, a 10-mL blood sample was Original Article collected from each patient to determine blood glucose levels using an HbA1c analyzer (VARIANT™ α TURBO, Bio-Rad Laboratories, Inc., CA, USA). HbA1c values were obtained at baseline and after the 8-week intervention. Statistical analyses were performed using SPSS version 12.0. A paired t-test was used to determine whether there were significant changes in blood glucose levels before and after the intervention. Meanwhile, an independent t-test was used to analyze differences between the 2 groups. The level of significance was set at p < 0.05. The results are expressed as mean ± standard deviation (SD).

RESULTS
The baseline characteristics of the patients are shown in Table 2. There were no significant differences in the baseline characteristics between groups (p > 0.05). The results of outcome measures are summarized in Table 3. There was no significant difference in HbA1c level after the intervention in the control group (p > 0.05). However, HbA1c levels decreased significantly in the PSS group after the intervention  Values are means ± SD. CON: control group; PSS: passive static stretching group; BMI: body mass index (p < 0.05) and were significantly different between groups (p < 0.05).

DISCUSSION
As mentioned above, this study determined the effect of passive static stretching on blood glucose levels in patients with T2DM. The results showed HbA1c levels decreased significantly after an 8-week passive static stretching intervention. There are several possible mechanisms that could explain how passive stretching of skeletal muscles decreased blood glucose levels. According to a review by Dohm 9) , glucose transport into the skeletal muscles is primarily mediated by a glucose transport protein, GLUT-4; accordingly, exercise can increase GLUT-4 levels in the skeletal muscles. Furthermore, increased metabolic activity accompanying passive muscle stretching is related to the GLUT-4 activation pathway 9,10) . Therefore, passive muscle stretching could induce the incorporation of GLUT-4 into the stretched skeletal muscles.
Other studies also support the possibility of stretchinginduced incorporation of GLUT-4 into the skeletal muscles. First, the activity of protein kinase B controls GLUT-4 incorporation; accordingly, protein kinase B is activated by passive stretching of isolated muscles 11) . Second, Sun et al. report that ischemia induces the translocation of GLUT-4 to the plasma membrane of cardiac myocytes 12) ; accordingly, passive stretching of the skeletal muscles can cause ischemia 13) . Third, in an experimental study by Roberts et al., exercise-induced increases in nitric oxide levels resulted in increased glucose transport 14) ; accordingly, passive stretching can increase nitric oxide release from excised soleus muscles by 20% 15) . Finally, mitogen-activated protein kinase activity stimulates glucose uptake in muscle cells 16) ; Martineau et al. report that the activity of mitogen-activated protein kinase directly reflects the magnitude of mechanical stress (e.g., actively or passively generated tension) applied to the muscle 17) .
The results of this study are subject to several limitations. The sample size is insufficient to generalize the results to all patients with T2DM. In addition, as HbA1c reflects the average plasma glucose level over the preceding 2-3 months, the 8-week study period might have been too short to determine changes in blood glucose levels as a result of stretching 18) . Therefore, further studies are required to ascertain the longterm (i.e., more than 3 months) effects of passive static stretching on blood glucose levels in a larger population of patients with T2DM.