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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, Indiab Department of Medicine, Kasturba Medical College and Hospital, Manipal University, Mangalore, Indiac Department of Physiology, Kasturba Medical College, Manipal University, Mangalore, Indiad Department of Biochemistry, Kasturba Medical College, Manipal University, Mangalore, India

Keywords:

Type 2 diabetes

Oxidative stress

Antioxidants

Glycated hemoglobin

Diaphragmatic breathing

a b s t r a c t

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, dia-

phragmatic breathing resulted in significant 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, micro-

vascular complications and neuropathy.1e3 Therapies aimed at

reducing OSTwouldbenefit patients with type 2 diabetes and those

at risk for developing diabetes.

Studies on yoga and pranayama have shown to be beneficial in

reducing OST in type 2 diabetes.

4,5

But promoting behavioralinterventions like yoga for diabetes faces several challenges as it

needs training bya yoga expert and a quiet place where yoga can be

performed. Yogic asanas are strenuous requiring flexibility and

therefore are unsuitable for most of the elderly diabetic patients

with complications.6 Motivation for yoga is less among young

patients as they find these classes in an inconvenient time (espe-

cially 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 significant 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 perspec-

tive, 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 exercise

7

which is a form of chest physical therapyprogram. The essence of pranayama was incorporated in this

breathing exercise to see its effecton OST. With this background the

present study was framed to demonstrate the effect of diaphrag-

matic 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

This study was conducted at the diabetes clinic of Kasturba

Medical College (KMC) hospital, Mangalore, India and also at 4

* Corresponding author. Tel.: 91 9986668611 (mobile), 91 824 2425966;

fax: 91 824 2442766.

E-mail address: shreelaxmi.hegde@gmail.com (S.V. Hegde).

Contents lists available at SciVerse ScienceDirect

Complementary Therapies in Clinical Practice

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / c t c p

1744-3881/$ e see front matter 2012 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ctcp.2012.04.002

Complementary Therapies in Clinical Practice 18 (2012) 151e153

mailto:shreelaxmi.hegde@gmail.comhttp://www.sciencedirect.com/science/journal/17443881http://www.elsevier.com/locate/ctcphttp://dx.doi.org/10.1016/j.ctcp.2012.04.002http://dx.doi.org/10.1016/j.ctcp.2012.04.002http://dx.doi.org/10.1016/j.ctcp.2012.04.002http://dx.doi.org/10.1016/j.ctcp.2012.04.002http://dx.doi.org/10.1016/j.ctcp.2012.04.002http://dx.doi.org/10.1016/j.ctcp.2012.04.002http://www.elsevier.com/locate/ctcphttp://www.sciencedirect.com/science/journal/17443881mailto:shreelaxmi.hegde@gmail.com

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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 non-

smokers 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 exer-

cise and 63 for control groups. Stratified sampling was employed at

the time of allocation in order to maintain equal number of patients

with uncomplicated diabetes mellitus and those with microvas-

cular, macrovascular and peripheral neuropathy to these groups.

The intervention group was given basic knowledge about the

importance of diaphragmatic breathing exercise for the manage-

ment of diabetes by the researcher herself. This method was

adopted from Kisner et al7 with certain modifications. The modi-

fication 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 abdomento rise. The patient was told to slowly let all the air out using

controlled expiration. Patients left hand would rise during inspi-

ration 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 oraland 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

defined 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), super-

oxide 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 immunoturbidi-

metric 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 Plasmavitamin C and E were

estimated by 2,4-dinitro phenyl hydrazine10 and Bieri et al

method.11 SOD in RBCs was measuredby 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 circum-

ference 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 partic-

ipants withdrew from diaphragmatic breathing intervention

during first month of the study and were not included in the final

analysis. Both reported illness which was unrelated to the study.

Mean SD age was 60.0 10.4 years in diaphragmatic breathinggroup and 57.5 8.9 years in control group. There was no signifi-

cant difference in sex, duration of diabetes and hypertension

between the groups at baseline. Diaphragmatic breathing along

with standard care significantly improved BMI, WHR, FPG, PPPG,

HbA1c, MDA, GSH and vitamin C at 3 months (Table 1). There was

significant increase in MDA and reduction in GSH and vitamin C

status in the control group. Waist circumference, BP and vitamin E

showed no significant difference in the intervention group when

compared to controls. However there was a significant 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 significant effect of dia-

phragmatic breathing exercise on OST. There was 21% reduction in

MDA which is clinically significant. In diaphragmatic breathing

exercise we incorporated the principle of pranayama with relaxa-

tion 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 agree-

ment with our previous findings 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 significant reduction in SOD levels. Diaphragmatic

breathing improves antioxidant potential in healthy volunteers.18

In the present study both GSH and vitamin C showed a signifi-

cant 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 dia-

phragmatic 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 diaphrag-

matic breathing exercise in addition to standard care bring about

statistically significant 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) 151e153152

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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 finding

on yoga which improved HbA1

c 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 difficulty with

adherence of patients to yoga intervention resulting in no signifi-

cant 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 interven-

tion and insufficient 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 forwardprocedure. 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 stratification of

sample according to complications. Since participants with various

complications may have increased OST, stratification made the two

groups identical. The present data reveal that diaphragmatic

breathing is an important technique that can mimic the benefits 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.

5. Conclusions

The study shows that 3 month diaphragmatic breathing exercise

can significantly reduce the OSTand 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.

Conflict of interest statement

No potential conflicts of interest relevant to this article were

reported.

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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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) Control group (n 63) p value

Basel ine After 3 mon ths Change at 3 mon ths Basel ine After 3 mon ths Change at 3 mon ths

Fasting plasma glucose (mmol/l) 8.9 2.7 7.9 2.2 1.0 0.5 8.6 3.1 9.0 3.0 0.4 0.1