Complementary Therapies in Clinical Practice 18 (2012) 151e153

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Complementary Therapies in Clinical Practice

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Diaphragmatic breathing exercise as a therapeutic intervention for control of oxidative stress in type 2 diabetes mellitus
Shreelaxmi V. Hegde a, *, Prabha Adhikari b, N.K. Subbalakshmi c, M. Nandini d, Gayathri M. Rao d, Vivian DSouza d
a

Department of Biochemistry, Srinivas Institute of Medical Science and Research Centre, Mukka, Mangalore, Karnataka, India Department of Medicine, Kasturba Medical College and Hospital, Manipal University, Mangalore, India Department of Physiology, Kasturba Medical College, Manipal University, Mangalore, India d Department of Biochemistry, Kasturba Medical College, Manipal University, Mangalore, India
b c

a b s t r a c t
Keywords: Type 2 diabetes Oxidative stress Antioxidants Glycated hemoglobin Diaphragmatic breathing

Present study aims to evaluate the effect of diaphragmatic breathing on anthropometry, blood pressure, glycemic control and oxidative stress in patients with type 2 diabetes on standard care in comparison with standard care alone. Study involved 123 patients who were assigned to receive either standard care or with additional diaphragmatic breathing for 3 months. In comparison with the control group, diaphragmatic breathing resulted in signicant reduction in body mass index, waist-hip ratio, fasting and post prandial plasma glucose, glycated hemoglobin, malondialdehyde, superoxide dismutase and improvement in glutathione and vitamin C. There was no difference in waist circumference, blood pressure and vitamin E in intervention group at follow-up. It can be concluded that diaphragmatic breathing can be employed as an effective therapy in reducing the oxidative stress while it can be incorporated as an add-on therapy to standard care in improving the anthropometry and glycemic parameters in type 2 diabetes. 2012 Elsevier Ltd. All rights reserved.

1. Introduction Some biochemical pathways associated with hyperglycemia (non-enzymatic glycosylation, glucose auto-oxidation, polyol pathways) lead to oxidative stress (OST) in diabetes mellitus. OST is found to be the root cause in the pathogenesis of diabetes mellitus and its associated clinical conditions like atherosclerosis, microvascular complications and neuropathy.1e3 Therapies aimed at reducing OST would benet patients with type 2 diabetes and those at risk for developing diabetes. Studies on yoga and pranayama have shown to be benecial in reducing OST in type 2 diabetes.4,5 But promoting behavioral interventions like yoga for diabetes faces several challenges as it needs training by a yoga expert and a quiet place where yoga can be performed. Yogic asanas are strenuous requiring exibility and therefore are unsuitable for most of the elderly diabetic patients with complications.6 Motivation for yoga is less among young patients as they nd these classes in an inconvenient time (especially for those at work or studying). Overall, all these factors affect

the attendance at the yoga classes. Recent study by Skora-Kondza et al6 was limited by low attendance rate of 50% for yoga. The study failed to show any signicant improvement in glycemic control and blood pressure in type 2 diabetes. When yoga is delivered as home-based exercises, participants do not practice regularly at home due to practical constraints e.g. lack of time, noise, room size.6 Hence from public health perspective, there is need for newer strategies which will be effective in diabetes management. In the present study we have adopted a new technique which is user friendly and can be performed in a small place without the need of privacy. We took up diaphragmatic breathing exercise7 which is a form of chest physical therapy program. The essence of pranayama was incorporated in this breathing exercise to see its effect on OST. With this background the present study was framed to demonstrate the effect of diaphragmatic breathing exercise on anthropometry, BP control, glycemic control and OST in type 2 diabetes patients with or without complications when compared to controls on standard care. 2. Methods

* Corresponding author. Tel.: 91 9986668611 (mobile), 91 824 2425966; fax: 91 824 2442766. E-mail address: shreelaxmi.hegde@gmail.com (S.V. Hegde). 1744-3881/$ e see front matter 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.ctcp.2012.04.002

This study was conducted at the diabetes clinic of Kasturba Medical College (KMC) hospital, Mangalore, India and also at 4

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community diabetes clinics offering primary care to diabetes patients (period 2006e2009). Total of 123 participants with type 2 diabetes, aged between 40 and 75 years, non-alcoholics and nonsmokers who gave a written informed consent were included. Those with acute macrovascular complications, cancer, pulmonary tuberculosis, rheumatoid arthritis or any serious systemic illness were excluded. Patients were grouped as 60 for diaphragmatic breathing exercise and 63 for control groups. Stratied sampling was employed at the time of allocation in order to maintain equal number of patients with uncomplicated diabetes mellitus and those with microvascular, macrovascular and peripheral neuropathy to these groups. The intervention group was given basic knowledge about the importance of diaphragmatic breathing exercise for the management of diabetes by the researcher herself. This method was adopted from Kisner et al7 with certain modications. The modication being, in addition to the breathing pattern relaxation of mind and concentration on the act of breathing was emphasized. In the beginning the patient was asked to rest for 5 min in the supine position. Next the patient was asked to place his/her right hand on the chest and left hand below the anterior costal margin. Patient was asked to breathe in slowly and deeply through the nose, with the shoulders relaxed and upper chest quiet allowing the abdomen to rise. The patient was told to slowly let all the air out using controlled expiration. Patients left hand would rise during inspiration and fall during expiration, whereas the right hand remained still. Precaution was taken to avoid hyperventilation. During the training the trainer constantly emphasized to relax and concentrate on the breathing pattern. After the breathing exercise the patient was asked to place both the hands down in resting pose and rest for 5 min. Although this breathing exercise can be performed in sitting position, the patients felt it comfortable to do it in supine position. Therefore supine position was standardized for this study. Patients practiced this breathing exercise in their homes once in the morning and again in the evening for 15e20 min daily for 3 months. The control group in their baseline visit was given general oral and written information about diet and exercise. Both the groups were allowed to continue any other physical activity that they were undertaking at baseline and follow the baseline diet. Drug dosages with regard to diabetes and hypertension were kept constant throughout the study period. Compliance to the intervention was dened as practice of diaphragmatic breathing for atleast 4 days/ week for 3 months. Participants were telephoned weekly to monitor adherence and to assist with any problems encountered with the program. Patients in the breathing group were checked for the breathing pattern every month when they visited the physician. Malondialdehyde (MDA), reduced glutathione (GSH), superoxide dismutase (SOD), vitamin C and E were measured to assess the oxidative stress and antioxidant status. Fasting plasma glucose (FPG), post prandial plasma glucose (PPPG), glycated hemoglobin (HbA1c), blood pressure (BP), waist circumference, waist-hip ratio (WHR) and body mass index (BMI) were the other outcome measures relevant to secondary objective. Twelve-hour fasting blood samples were collected and centrifuged at 3000 rpm to separate the plasma. Plasma glucose was measured by glucose oxidase method and HbA1c by particle enhanced immunoturbidimetric method using Dia Sys diagnostic kits, Holzheim, Germany. MDA and GSH in RBCs were measured according to Stocks and Dormandy8 and Beutler et al method.9 Plasma vitamin C and E were estimated by 2,4-dinitro phenyl hydrazine10 and Bieri et al method.11 SOD in RBCs was measured by Beauchamp and Fridovich method.12 Weight was measured while the subjects were minimally clothed without shoes using digital scales and recorded to the

nearest 0.1 kg. Height was measured in a standing position without shoes using a stadiometer. WHR was calculated as waist circumference in centimeters divided by hip circumference in centimeters. Waist circumference was measured using a non-stretchable inch tape kept midway between iliac crest and lower rib cage with the measurement taken at the end of expiration while the patient is breathing quietly. Blood pressure was recorded by taking mean of second and third readings of blood pressure taken 5 min apart in sitting position after the patient had completely relaxed. Data were analyzed by intention to treat. Paired t test was used to compare the continuous variables from baseline to follow-up. ManneWhitney U test, a non-parametric test was used to compare the differences in various parameters before and after intervention between the two groups. All parameters were analyzed using SPSS version 11.0. 3. Results Overall compliance with the intervention was 83%. Two participants withdrew from diaphragmatic breathing intervention during rst month of the study and were not included in the nal analysis. Both reported illness which was unrelated to the study. Mean SD age was 60.0 10.4 years in diaphragmatic breathing group and 57.5 8.9 years in control group. There was no signicant difference in sex, duration of diabetes and hypertension between the groups at baseline. Diaphragmatic breathing along with standard care signicantly improved BMI, WHR, FPG, PPPG, HbA1c, MDA, GSH and vitamin C at 3 months (Table 1). There was signicant increase in MDA and reduction in GSH and vitamin C status in the control group. Waist circumference, BP and vitamin E showed no signicant difference in the intervention group when compared to controls. However there was a signicant decrease in SOD activity in the breathing exercise group at follow-up. No adverse events were observed during the study. 4. Discussion The present study demonstrates the signicant effect of diaphragmatic breathing exercise on OST. There was 21% reduction in MDA which is clinically signicant. In diaphragmatic breathing exercise we incorporated the principle of pranayama with relaxation to see its role on OST. We found it superior to other lifestyle interventions like aerobic exercise and resistance training that are known to increase stress parameters.13,14 The results are in agreement with our previous ndings on yoga15: 3 months of yoga in type 2 diabetic subjects showed 20% reduction in oxidative stress. The results are in accordance with other reports on yoga.16,17 Reports in type 2 diabetes have shown increased SOD activity after performing yoga.5 With diaphragmatic breathing exercise we found a signicant reduction in SOD levels. Diaphragmatic breathing improves antioxidant potential in healthy volunteers.18 In the present study both GSH and vitamin C showed a signicant improvement by 37% and 45% respectively in diaphragmatic breathing group when compared to standard care. Increase in the levels of antioxidants can be directly related to the reduction of free radical production. Our data reveal that regular practice of diaphragmatic breathing exercise can prevent the effect of elevating OST in type 2 diabetes patients by improving the antioxidant status in them. The present data clearly shows that incorporation of diaphragmatic breathing exercise in addition to standard care bring about statistically signicant improvement in BMI, WHR, FPG, PPPG and HbA1c. When compared to aerobic exercise and resistance training we observed a marginal reduction in glycemic control, BMI and WHR. In the present study HbA1c levels decreased by 3% after 3

S.V. Hegde et al. / Complementary Therapies in Clinical Practice 18 (2012) 151e153 Table 1 Changes in selected clinical and oxidative stress variables from baseline to the end of 3 month follow-up in the intervention and control groups. Variables Diaphragmatic breathing exercise group (n 60) Baseline Fasting plasma glucose (mmol/l) Post prandial plasma glucose (mmol/l) HbA1c (%) BMI (kg/m2) Waist circumference (cm) WHR Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Malondialdehyde (mmol/L) Glutathione (mmol/gmHb) Vitamin C (mmol/L) Vitamin E (mmol/L) Superoxide dismutase (unit/gmHb) 8.9 12.2 8.3 24.9 89.4 0.94 139.4 83.0 59.1 6.4 26.7 64.1 5962.6 2.7 4.4 1.7 3.1 9.9 0.06 15.8 9.7 13.0 2.4 13.6 25.3 1247.1 After 3 months 7.9 10.9 8.1 24.8 88.4 0.93 136.1 80.6 46.3 7.6 31.2 63.9 5353.7 2.2 3.3 1.5 3.4 9.8 0.06 18.3 9.3 11.0 2.8 19.3 25.3 1297.7 Change at 3 months 1.0 1.3 0.2 0.1 1.0 0.01 3.3 2.4 12.8 1.2 4.5 0.2 608.9 0.5 1.1 0.2 0.3 0.1 0.00 2.5 0.4 2.0 0.4 5.7 0.0 50.6 Control group (n 63) Baseline 8.6 12.3 8.0 25.3 90.5 0.93 139.6 84.1 50.7 7.1 30.0 59.7 5691.6 3.1 5.1 1.5 3.9 9.8 0.06 21.0 9.9 9.3 3.6 29.0 24.2 1641.4 After 3 months 9.0 12.6 8.5 25.5 90.0 0.93 138.0 83.9 52.3 6.3 23.8 58.0 5593.1 3.0 4.7 1.8 4.1 9.1 0.05 15.4 8.5 10.9 2.4 18.2 23.5 1768.0 Change at 3 months 0.4 0.3 0.5 0.3 0.5 0.0 1.6 0.2 1.6 0.8 6.2 1.7 98.5 0.1 0.4 0.3 0.2 0.7 0.01 5.6 1.4 1.6 1.2 10.8 0.7 126.6

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p value

<0.001 <0.007 <0.001 <0.003 0.200 <0.001 0.319 0.305 <0.001 <0.001 <0.001 0.583 <0.007

Data are mean SD. p values are signicance values in diaphragmatic breathing exercise group when compared to the control group.

months of diaphragmatic breathing exercise, while it increased by 6.25% in control group. By diaphragmatic breathing we observed a greater reduction in HbA1c when compared to our earlier nding on yoga which improved HbA1c levels by 1.4%. This may be due to the fact that in this breathing exercise there is a continuous movement of the abdomen which may exert a massaging effect on the internal organs, inducing insulin secretion from the pancreas. Yoga when combined with aerobic exercise has shown to reduce HbA1c upto 8% in controlled trials.19,20 Latest study by Skora-Kondza et al6 observed difculty with adherence of patients to yoga intervention resulting in no signicant improvement in glycemic control and blood pressure. The authors gave the following explanations for negative results recruitment challenges, practical and motivational barriers to class attendance, physical and motivational barriers to engaging in the exercises, inadequate intensity and/or duration of yoga intervention and insufcient personalization of yoga to individual needs. With this regard, diaphragmatic breathing may represent a useful technique for diabetes management as it is a fairly straight forward procedure. The only challenge is to stay focussed on the breath; therefore a short training would help to improve the concentration. Our study is limited by the fact that the allocation to groups was not randomized. The strength of our study was the stratication of sample according to complications. Since participants with various complications may have increased OST, stratication made the two groups identical. The present data reveal that diaphragmatic breathing is an important technique that can mimic the benets of yoga practice to control the burden of OST in type 2 diabetes. It is also a convenient therapy which can be adopted in health care settings. Additional studies whether diaphragmatic breathing can help in controlling the disease progression in diabetes remains warranted.

Acknowledgments This study was funded by grant from Manipal University (431/ 013/2007). The authors express appreciation to all the participants whose co-operation and dedication made this study possible.

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5. Conclusions The study shows that 3 month diaphragmatic breathing exercise can signicantly reduce the OST and improve the antioxidant status in type 2 diabetes. Diaphragmatic breathing exercise can be incorporated as an add-on therapy to standard care for improving the anthropometry and glycemic parameters. Its effect on waist circumference, BP and vitamin E was not evident in this short-term study. Conict of interest statement No potential conicts of interest relevant to this article were reported.