ORIGINAL RESEARCH
Pranayam for Treatment of Chronic Obstructive Pulmonary Disease: Results From a Randomized, Controlled Trial Anupama Gupta, MD; Rajesh Gupta, MD; Sushma Sood, MD; Mohammad Arkham, BNYS
Abstract Context: Existing medications for chronic obstructive pulmonary disease (COPD) do not modify the longterm decline in lung functions. The increasing prevalence of COPD requires the development of interventions beyond the usual medical treatment, with a specific focus on rehabilitation. Controlled breathing (pranayam) is a specific set of respiratory exercises within yoga that has been shown to improve the resting respiratory rate, vital capacity, maximum voluntary ventilation, breath-holding time, and maximal inspiratory and expiratory pressures. Objective: In this study, pranayam was analyzed as an adjunct treatment for medically stable individuals with moderate to severe COPD. Design: The research team carried out a case control study. Setting: This study took place at a tertiary care institution, with the participation of the departments of Physiology, Yoga and Naturopathy, and Pulmonary Medicine at Pandit Bhagwat Dayal Sharma Postgraduate Institute of Medical Sciences in Rohtak, Haryana, India. Participants: Participants were 50 medically stable individuals with moderate to severe COPD. Intervention: Twenty-five participants in the intervention arm (IA) were trained to practice pranayam for 30 min 2 ×/d and also received the usual medical treatment. The control group also included 25 participants, and they received the usual medical treatment only, without pranayam.
Anupama Gupta, MD, is an associate professor and specializes in physiology. Rajesh Gupta, MD, practices respiratory medicine and is a professor in the Department of Respiratory Medicine. Sushma Sood, MD, specializes in physiology. Mohammad Arkham, BNYS, is a chief instructor in the Department of Yoga and Naturopathy. All are located at Pandit Bhagwat Dayal Sharma Postgraduate Institute of Medical Sciences in Rohtak, Haryana, India. 26
Integrative Medicine • Vol. 13, No. 1 • February 2014
IMCJ_13_1.indd 26
Outcome Measures: The COPD assessment test (CAT) score and the body-mass index, obstruction, dyspnea, exercise (BODE) capacity index were assessed at baseline and at 3 mo. The results were expressed using standard statistical methods. Results: For the IA, a significant improvement occurred in the CAT score (21.2 ± 2.6-17.4 ± 2.5, P < .001) and in the impact level, which moved from high (>20) to medium (10-20) after 3 mo of practicing pranayam. The control arm (CA) showed no significant improvement in the CAT score (21.6 ± 2.7-21.4 ± 2.7). Although the IA showed a significant improvement in a 6-min walk test (6MWT) when compared to the CA, (1) the IA’s forced expiratory volume in 1 sec (FEV1), which is a measure of airflow that is commonly impaired in COPD patients and which is associated with poor functional status, showed no significant improvements, and (2) the IA’s BODE capacity index showed no significant improvements. Conclusion: The current study shows that pranayam has been demonstrated as useful for individuals with moderate to severe COPD. Significant improvements in the IA’s CAT scores after 3 mo of practice suggests that pranayam can improve the subjective experience of health, disease severity, and functional status for COPD patients, without much improvement in FEV1 actually occurring and with airflow limitation not fully reversible but usually progressive. The research team concluded that pranayam is a useful adjunct treatment and can be an effective rehabilitation program for individuals with COPD.
Corresponding author: Rajesh Gupta, MD E-mail address: [email protected]
Gupta—Pranayam for COPD
1/16/14 2:58 PM
W
orldwide, chronic obstructive pulmonary disease (COPD) has emerged as a major health problem. It is the 12th-largest burden of disease and is likely to be the 5th-largest burden within the next 10 years, although it is preventable and treatable.1,2 Its pulmonary component is associated with an abnormal inflammatory response of the lung to noxious particles or gases. COPD is characterized by airflow limitation that is not fully reversible but is usually progressive.3,4 Airway inflammation in COPD passes to other systems, causing extrapulmonary effects like weight loss, cachexia, osteoporosis, chronic anemia, cardiovascular disorders, and derangement of cognitive function. All effects have an impact on the quality of life.5 Existing medications for COPD do not modify the long-term decline in lung function. Nonpharmacological intervention in the form of pulmonary rehabilitation reduces symptoms, improves the quality of life, and increases physical and emotional participation in everyday activities.3,4 In the last few decades, yoga has been incorporated into modern medicine.6 Relaxation, exercise (asanas), controlled breathing (pranayam), a nourishing diet (satvik), positive thinking, and meditation are its various constituents.7 Yogic breathing, or pranayam, is part of all yogas. This technique of controlled breathing (1) increases the capacity of the lungs, (2) helps to strengthen the internal organs, (3) improves mental control, and (4) strengthens the ability to relax.7 Pranayam has been shown to improve the resting respiratory rate, vital capacity, maximum voluntary ventilation, breath-holding time, and maximal inspiratory and expiratory pressures.6,7 It reduces the dead-space ventilation (the volume of air that is inhaled but does not take part in the gas exchange), and it aerates the whole lung, in contrast to regular shallow breathing that ventilates only the bases of the lung. This full aeration has beneficial effects on exercise performance and quality of life.6 When individuals with COPD have been specifically trained to perform pranayam, the strength of both the inspiratory and expiratory muscles increased.6,7
COPD3 of the study’s procedures and obtaining written consent, 50 medically stable individuals (mostly male) were divided into 2 arms of 25 participants each. The research team clinically ruled out certain disease states for participants using an electrocardiogram (ECG) or other specific investigations as required, including (1) asthma or any other pulmonary or major systemic diseases (eg, ischemic, rheumatic, or congenital heart disease or cor pulmonale [pulmonary heart disease]) and (2) any renal or hepatic diseases. All participants had been exsmokers for at least 6 months or were nonsmokers.
Materials and Methods The research team studied the effects of pranayam on medically stable individuals with moderate to severe COPD.3
Intervention Participants in the intervention arm (IA) performed pranayam for 30 minutes, twice per day, and received the usual medicines for COPD. The control arm (CA) took only the usual medicines for COPD. Participants in the IA could adopt any meditative or comfortable postures under the supervision of yoga instructors. Participants in the IA were trained to perform pranayam using 4 easy and effective asanas, including suryabhedana, nadishuddhi, bhramari, and kapalbharti,6,7 performing each for 5 to 7 minutes. This time decreases to a minimum of 20 minutes as one acclimates to the process. Suryabhedana. The practitioner closes his or her left nostril using the ring and little fingers on the right hand and inhales slowly and deeply through the right nostril. The practitioner then closes the right nostril with the right thumb and exhales slowly and deeply through the left nostril. The exhalation should be longer than the inhalation. The practitioner repeats the cycle. Nadishuddhi. The practitioner closes his or her right nostril with the right thumb, exhales completely with the left nostril, and then inhales deeply through the same nostril. The practitioner then closes his or her left nostril with the ring and little finger of the right hand and exhales slowly and completely through the right nostril. The practitioner repeats the rounds, alternating the nostrils. Bhramari. The practitioner inhales deeply and then exhales to produce a low-pitched sound resembling the humming of a bee, feeling the vibrations in his or her entire head. The practitioner repeats the process. Kapalbharti. The practitioner breathes rapidly through the nostrils, with active and forceful exhalation and passive inhalation.
Participants The current study was conducted at a tertiary care institution, Pandit Bhagwat Dayal Sharma Postgraduate Institute of Medical Sciences in Rohtak, Haryana, India, with the participation of 3 departments—Physiology, Yoga and Naturopathy, and Pulmonary Medicine—after approval by the Interdepartment Meeting (IDM). Participants/patients were shortlisted from those regularly attending Chest OPD, the school's respiratory clinic. After informing potential participants with moderate to severe
Outcome Measures The participants were drawn from our Chest OPD patients and advised to attend the physiologist. After the processes of excluding, including, explaining, and initial (baseline) recording on a separate card/sheet for the study (in addition to a Chest OPD card), the participants were referred to regularly follow-up at the Chest OPD (CA and IA) and yoga clinics (IA). For the IA, this occurred daily until each was confident in performing pranayam, at which time the IA participants switched to weekly follow-
Gupta—Pranayam for COPD
IMCJ_13_1.indd 27
Integrative Medicine • Vol. 13, No. 1 • February 2014
27
1/16/14 2:58 PM
Table 1. Comparison of IA and CA IA CA Mean ± SD (n = 25) (n = 25) 24/1b Gender: 24/1a Male/ Female, n Mean ± SD Age, y 52.5 ± 3.9 BMI 20.8 ± 1 51.1 ± 8.7 FEV1c 6MWT 257.1 ± 0.5 BODE Index 4.9 ± 0.7 CAT Score 21.2 ± 2.6
Mean ± SD 52 ± 4.1 20.78 ± 1.2 49.6 ± 8.6 251.1 ± 38.1 5 ± 0.7 21.6 ± 2.7
P Value
>.05 >.05 >.05 >.05 >.05 >.05
One participant was female. One participant was female. c FEV1 is measured by the percent of the predicted value taking all other variables into consideration. a
b
ups. IA could follow up with Chest OPD clinic at any time and with the physiologist after 3 months. Using a separate card, participants included in the study attended the Chest COPD clinic at baseline then followed up whenever required or monthly, without revealing their participation in the study. The research team did not reveal the results of the COPD consultation to the yoga (pranayam) instructor. To evaluate the benefits of pranayam, the research team used the BODE (body-mass index, obstruction, dyspnea, exercise) capacity index8 and the COPD assessment test (CAT) score.9 The BODE capacity index involves measuring forced expiratory volume in 1 second (FEV1), which is used for grading the disease, and the CAT is a concise, validated questionnaire based on the subjective feelings of the individual. All participants in the 2 arms were evaluated using the BODE capacity index8 and the CAT score9 at baseline and at 3 months. BODE Capacity Index.8 The index is a composite marker of the disease, taking into consideration its systemic nature as evaluated based on the measurement of the FEV1, the 6-minute walk test (6MWT) in meters, the modified Medical Research Council (MMRC) dyspnea scale,10 and the body mass index (BMI). CAT.9 The assessment is a concise and simple questionnaire about cough, phlegm, chest tightness, breathlessness, activity, confidence, and energy (power) of individuals. Using the CAT score, medical practitioners identify the CAT score impact level: 30 = very high.9 Data Analysis Calculations were carried out by standard statistical methods with SPSS version 11 (SPSS Inc, Chicago, IL, USA) using mean ± standard deviation (SD), paired, for comparing changes within same arm and unpaired t tests 28
Integrative Medicine • Vol. 13, No. 1 • February 2014
IMCJ_13_1.indd 28
for comparing changes between the 2 arms. The level of significance for results was expressed using P values, with P < .05 being statistically significant. Results In the span of 1 month, 100 individuals were considered for study. Of these, 50 individuals were enrolled. The IA and CA were similar with respect to age, gender, FEV1, and 6MWT scores. All participants had grade-2 dyspnea, as measured by the MMRC scale.10 Table 1 compares the ages, genders, and results of testing at baseline for the 2 groups. The research team recorded results for each participant, identified the differences between his or her baseline values and the values after 3 months, and calculated the mean differences and SDs from baseline to the end of the study for each group. The research team also compared the mean differences from baseline to the end of the study between groups, using an unpaired t test. The study’s most exciting results stem from the comparison of the change from baseline to the end of the study between the 2 groups. The calculations from the unpaired t test provided statistically significant results for both the CAT score and the 6MWT (borderline significant), as shown in Table 2. The IA’s CAT scores improved from 21.24 ± 2.69 to 17.4 ± 2.54 (ie, the impact level goes from high [>20] to medium [10-20]).9 The 6MWT, an alternative exercise test or a measure of generalized performance, improved significantly for the IA as compared to the CA (P < .05), but after 3 months, the FEV1, a measure of airflow that is commonly impaired in individuals with COPD and that is associated with poor functional status, and the BODE capacity index, failed to improve in a statistically significant manner for the IA. This result is relevant to the use of pranayam as an auxiliary measure for individuals with COPD. In the CA, after 3 months of typical medical treatment, no improvement was observed but, rather, a slight deterioration occurred. In the IA, no exacerbations of COPD symptoms in any one of the participants had occurred after 3 months. Overall, they were feeling better according to the CAT score. The IA had no increases in requirements for medical intervention, although the medical treatments were not considered in the study. In the CA, members experienced deteriorations in condition and increases in requirements for medicines, but no admissions occurred that would cause the research team to call the changes exacerbations. Discussion COPD is a multifaceted disorder with pulmonary and systemic components impairing the quality of life of the affected. It is irreversible and progressive. Regular medical treatment needs to be maintained at the same level for long periods unless significant side effects occur or the disease worsens. Progression of the disease can be delayed Gupta—Pranayam for COPD
1/16/14 2:58 PM
Table 2. Change in IA and CA After Pranayam for 3 Months IA Parameters Mean ± SD BODE Index CAT Score FEV1d 6MWT
Baseline 4.9 ± 0.7 21.2 ± 2.8 51.2 ± 8.7 257.1 ± 40.5
After 3 Mo 4.8 ± 0.9 17.4 ± 2.5 53.3 ± 8.8 264 ± 4
CA
P Value Baseline 5.04 ± 0.7 >.05a .05a 49.6 ± 8.6 >.05a 251.1 ± 38
After 3 Mo 5.2 ± 1.1 21.4 ± 2.7 49.1 ± 8.7 249.2 ± 36.8
IA/CA After 3 Mo P Value P Value >.05 >.05a >.05 .05 >.05a >.05 20) to medium (10-20).9 The findings indicate that pranayam can improve the general condition of individuals with COPD, relieving their symptoms and making them feel better. Nonsignificant improvement in the BODE capacity index in the IA after 3 months of practice indicated that pranayam improved the performance status of individuals with COPD without much improvement in lung function. Borderline improvements seen in the 6MWT, one of the parameters of the BODE capacity index, led the research team to the same conclusion (ie, improvement in performance/activity). Gupta—Pranayam for COPD
IMCJ_13_1.indd 29
Researchers have suggested various mechanisms of efficiency of the lungs in individuals practicing pranayam. Pranayam causes nonfunctional or closed airways to work.6,7 It promotes abdominal respiration, providing relief to the main muscle of respiration, the diaphragm. This abdominal respiration not only improves respiration and oxygenation but also improves circulation. Researchers speculate that the movements or massage of the abdominal viscera during abdominal respiration, as per the maneuvers of pranayam, is the mechanism for improvement in the systemic manifestations of COPD. Clearance of airways with deep and slow breathing helps to combat secretions by keeping the weak and collapsed airways in the disease clear to expel the secretions by ciliary action and, therefore, inflammation of respiratory passages. Consequently, systemic inflammation is relieved, and so are its manifestations.7 Pranayam is easy to understand and requires little effort to perform, making it almost cost-free. Maintenance of it does not require much time (15-20 min) as a routine. The CAT score9 has recently been introduced as a test for regular assessment of COPD symptoms,4 which wax and wane in the course of disease. The test grades them on the basis of a concise, validated questionnaire without measuring any physical parameter, whereas the BODE capacity index involves physical parameters—FEV1, MMRC, 6MWT, and BMI—that are unlikely to improve upon each grading. The CAT gives better information regarding the worsening of COPD.8 This study provided observations at 3 months of practice of pranayam. Further practice could add to the improvement because inflammation might subside further and symptoms might be further relieved, thereby giving individuals with COPD more confidence. In the current study, the research team has studied the benefits of pranayam for individuals with moderate to severe COPD. If researchers studied the practice of pranayam for people at an earlier stage of the disease or for healthy individuals, it would likely be even more productive.
Integrative Medicine • Vol. 13, No. 1 • February 2014
29
1/16/14 2:58 PM
Table 3. Baseline and 3-month Outcome Measurements for IA Participant 2 Initial At 3 Mo 46 48 FEV1a 6MWT (m) 210 240 MMRC 2 2 >21 >21 BMI(kg/m2) BODE Index 5 5 CAT Score 22 18 a FEV1 is measured by the percent of the predicted value taking all other variables into consideration.
Table 4. Baseline and 3-month CAT Data for IA Participant 2a
Coughing: never/all the time Chest phlegm (mucous) level: none/completely full My chest feels tight: not at all/ very tight Walking up a hill or 1 flight of stairs leaves me: not breathless/ very breathless My activities at home are: not limited/very limited Despite my lung condition, when I leave home I am: confident/not at all confident The quality of my sleep with regard to my lung condition: I sleep soundly/I do not sleep soundly Energy: I have lots/I have none at all Totals
Baseline 2 3
3 Mo of Intervention Practice 2 2
3
2
4
3
3
2
2 2 Case Reports The following case examples from the trial illustrate how pranayam worked 3 3 as an adjunctive therapy to improve markers of activity for 2 participants. IA, Participant 2. The participant is a 55-year-old male with a known, 10-year 2 2 case of COPD with intermittent acute exacerbations. He has no history of 22 18 tuberculosis, diabetes mellitus, hypertension, allergy or asthma, cerebrovascular accident, a CAT scoring is based on a 6-point subjective scale from 0 to 5 with 0 or other disease and is nonalcoholic. describing symptoms as less severe and 5 describing symptoms as Although he has not smoked for 7 years, he more severe. maintained a habit of smoking 3 to 4 bundles (20 ea) per day for 10 years. At baseline, his SpO2 oximetry reading was 97% in his impairment impact from moderate to low (Table 4). IA, Participant 32. Participant is a 53-year-old male respiratory system exam. Auscultation revealed decreased whose COPD has been known for more than 7 years. He bilateral breath sound and no wheezing or rhonchi evident. has no history of antituberculosis treatment. In addition, The participant’s pulse rate was 102 beats per minute and, he has not been diagnosed with diabetes mellitus, upon cardiovascular exam, S1 and S2 were heard normally. Blood pressure was measured at 130/80 mm Hg. No hypertension, allergy or asthma, cerebrovascular accident abnormalities of the central nervous system were detected. or other disease, and is nonalcoholic. The participant Posteroanterior x-ray showed COPD-related changes with smoked cigarettes for 15 years at the rate of 6 to 7 bundles no infiltration. (20 ea) per day before quitting the habit 5 years ago. Following examination on March 9, 2011, the general At baseline, his SpO2 oximetry reading was 94% in his condition of the participant was stable with dyspnea respiratory system exam. Auscultation revealed decreased evaluated as minimal. Treatment at the time included bilateral breath sound and no wheezing or rhonchi evident. tiotropium inhaler, 2 puffs twice per day. In addition, the The participant’s pulse rate was 92 beats per minute and, following medications were initiated: (1) amoxiclav tablets upon cardiovascular exam, S1 and S2 were heard normally. (625 mg), three times daily and (2) Deriphylline (300 mg), No abnormalities of the central nervous system were twice daily for 10 days. He was asked to return for follow- detected. Posteroanterior x-ray showed COPD-related up after 10 days. At follow up on April 13, 2011, the changes with no infiltration. participant presented in better general condition and his Following examination on March 16, 2011, the medication was returned to just his tiotropium inhaler at general condition of the participant was stable with 2 puffs twice daily, as before, with multivitamin support dyspnea evaluated as absent. Treatment including (1) added. On November 5, 2011, the participant was advised azithromycin tablets (500 mg), once daily for 7 days, and to continue his current treatment protocol. (2) tiotropium inhaler, 2 puffs daily, was initiated. At Following 3 months of pranayam practice, participant follow-up on April 13, 2011, the tiotropium inhaler was 2 showed signs of improvement in 6MWT and CAT score continued at 2 puffs daily and a multivitamin was (Table 3), including subjective improvement in 4 categories recommended. On June 11, 2011, the participant was of the CAT scale resulting in a reclassification of his advised to continue his current treatment regimen. 30
Integrative Medicine • Vol. 13, No. 1 • February 2014
IMCJ_13_1.indd 30
Gupta—Pranayam for COPD
1/16/14 2:58 PM
Table 5. Baseline and 3-month Outcome Measurements for IA Participant 32 Initial At 3 Mo 47 48 FEV1a 6MWD (m) 230 237 MMRC 2 2 >21 >21 BMI(kg/m2) BODE Index 5 5 CAT Score 22 20 a FEV1 is measured by the percent of the predicted value taking all other variables into consideration.
Following 3 months of pranayama practice, participant 32 showed signs of improvement in 6MWD and CAT score (Table 5), including subjective improvement in 2 categories of the CAT scale resulting in a reclassification of his impairment impact from moderate to low (Table 6).
Table 6. Baseline and 3-month CAT Data for IA Participant 32a 3 Mo of Intervention Baseline Practice Coughing: never/all the time 2 2 Chest phlegm (mucous) level: 1 1 none/completely full My chest feels tight: not at all/very 3 2 tight Walking up a hill or 1 flight of 4 3 stairs leaves me: not breathless/ very breathless My activities at home are: not 3 3 limited/very limited Despite my lung condition, when I 3 3 leave home I am: confident/not at all confident 3 3 The quality of my sleep with regard to my lung condition: I sleep soundly/I do not sleep soundly Energy: I have lots/I have none at 3 3 all Totals 22 20
a CAT scoring is based on a 6-point subjective scale from 0 to 5 with 0 Conclusions describing symptoms as less severe and 5 describing symptoms as more The current study demonstrated that severe. pranayam can be useful for individuals with moderate to severe COPD. 10. MRC dyspnoea scale. National Institute for Health and Care Excellence Web Significant improvements in the IA’s CAT scores after 3 site. http://www.nice.org.uk/usingguidance/commissioningguides/pulmonaryrehabilitationserviceforpatientswithcopd/mrc_dyspnoea_scale.jsp. months of practice suggests that pranayam can improve Updated December 13, 2007. Accessed May 10, 2012. the subjective experience of health, disease severity, and 11. COPD. American Lung Association Web site. www.lung.org/lung-disease/ copd. Accessed May 10, 2012. functional status for COPD patients, without much 12. Grove TP. Should patients with chronic obstructive pulmonary disease be improvement in FEV1 actually occurring and with airflow prescribed a resistance-training program? Br J Sports Med. 2010;44(6):396397. limitation not fully reversible but usually progressive. The 13. Kunik ME, Braun U, Stanley MA, et al. One session cognitive behavioral research team concluded that pranayam is a useful adjunct therapy for elderly patients with chronic obstructive pulmonary disease. Psychol Med. 2001;31(4):717-723. treatment and can be an effective rehabilitation program 14. Emery CF, Schein RL, Hauck ER, MacIntyre NR. Psychological and cognitive for individuals with COPD. outcomes of a randomized trial of exercise among patients with chronic
References
1. COPD statistics. COPD International Web site. http//www.copd-international.com/library/statistics/htm. Accessed January 23, 2010. 2. Halbert RJ, Natoli JL, Gano A, Badamgarav E, Buist AS, Mannino DM. Global burden of COPD: systematic review and meta-analysis. Eur Respir J. 2006;28(3):523-532. 3. Global Initiative for Chronic Obstructive Lung Disease. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease (2010 update). http://www.goldcopd.org/uploads/users/files/ GOLDReport_April112011.pdf. Accessed March 23, 2011. 4. MacNee W. ABC of chronic obstructive pulmonary disease: pathology, pathogenesis, and pathophysiology. BMJ. 2006;332(7551):1202-1204. 5. Agusti AG, Noguera A, Sauleda J, Sala E, Pons J, Busquets X. Systemic effects of chronic obstructive pulmonary disease. Eur Respir J. 2003;21(2):347-360. 6. Bijlani RL, Manjunatha S. Yoga. In: Bijlani RL, Manjunatha S. Understanding Medical Physiology: A Textbook for Medical Students. 4th ed. New Delhi, India: Jaypee Brothers Medical Publishers; 2011:743-775. 7. Katiyar SK, Bihari S. Role of pranayama in rehabilitation of COPD patients— a randomized controlled study. Indian J Allergy Asthma Immunol. 2006;20(2):98-104. 8. Celli BR, Cote CG, Marin JM, et al. The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(10):1005-1012. 9. GlaxoSmithKline. COPD Assessment Test Web site. www.CATestonline.org. Published September 2009. Accessed September 17, 2011.
Gupta—Pranayam for COPD
IMCJ_13_1.indd 31
obstructive pulmonary disease. Health Psychol. 1998;17(3):232-240. 15. Coulehan JL, Schulberg HC, Block MR, Madonia MJ, Rodriguez E. Treating depressed primary care patients improves their physical, mental, and social functioning. Arch Intern Med. 1997;157(10):1113-1120. 16. Coventry PA, Gellatly JL. Improving outcomes for COPD patients with mildto-moderate anxiety and depression: a systematic review of cognitive behavioral therapy. Br J Health Psychol. Sept 2008;13(pt 3):381-400. 17. Fernandes M, Cukier A, Feltrim MI. Efficacy of diaphragmatic breathing in patients with chronic obstructive pulmonary disease. Chron Respir Dis. 2011;8(4):237-244. 18. COPD: breathing techniques. Canadian Lung Association Web site. http:// lung.ca/diseases-maladies/copd-mpoc/breathing-respiration/index_e.php. Accessed May 12, 2012.
Integrative Medicine • Vol. 13, No. 1 • February 2014
31
1/16/14 2:58 PM
Pranayam for Treatment of Chronic Obstructive Pulmonary Disease: Results From a Randomized, Controlled Trial Anupama Gupta, MD; Rajesh Gupta, MD; Sushma Sood, MD; Mohammad Arkham, BNYS
Abstract Context: Existing medications for chronic obstructive pulmonary disease (COPD) do not modify the longterm decline in lung functions. The increasing prevalence of COPD requires the development of interventions beyond the usual medical treatment, with a specific focus on rehabilitation. Controlled breathing (pranayam) is a specific set of respiratory exercises within yoga that has been shown to improve the resting respiratory rate, vital capacity, maximum voluntary ventilation, breath-holding time, and maximal inspiratory and expiratory pressures. Objective: In this study, pranayam was analyzed as an adjunct treatment for medically stable individuals with moderate to severe COPD. Design: The research team carried out a case control study. Setting: This study took place at a tertiary care institution, with the participation of the departments of Physiology, Yoga and Naturopathy, and Pulmonary Medicine at Pandit Bhagwat Dayal Sharma Postgraduate Institute of Medical Sciences in Rohtak, Haryana, India. Participants: Participants were 50 medically stable individuals with moderate to severe COPD. Intervention: Twenty-five participants in the intervention arm (IA) were trained to practice pranayam for 30 min 2 ×/d and also received the usual medical treatment. The control group also included 25 participants, and they received the usual medical treatment only, without pranayam.
Anupama Gupta, MD, is an associate professor and specializes in physiology. Rajesh Gupta, MD, practices respiratory medicine and is a professor in the Department of Respiratory Medicine. Sushma Sood, MD, specializes in physiology. Mohammad Arkham, BNYS, is a chief instructor in the Department of Yoga and Naturopathy. All are located at Pandit Bhagwat Dayal Sharma Postgraduate Institute of Medical Sciences in Rohtak, Haryana, India. 26
Integrative Medicine • Vol. 13, No. 1 • February 2014
IMCJ_13_1.indd 26
Outcome Measures: The COPD assessment test (CAT) score and the body-mass index, obstruction, dyspnea, exercise (BODE) capacity index were assessed at baseline and at 3 mo. The results were expressed using standard statistical methods. Results: For the IA, a significant improvement occurred in the CAT score (21.2 ± 2.6-17.4 ± 2.5, P < .001) and in the impact level, which moved from high (>20) to medium (10-20) after 3 mo of practicing pranayam. The control arm (CA) showed no significant improvement in the CAT score (21.6 ± 2.7-21.4 ± 2.7). Although the IA showed a significant improvement in a 6-min walk test (6MWT) when compared to the CA, (1) the IA’s forced expiratory volume in 1 sec (FEV1), which is a measure of airflow that is commonly impaired in COPD patients and which is associated with poor functional status, showed no significant improvements, and (2) the IA’s BODE capacity index showed no significant improvements. Conclusion: The current study shows that pranayam has been demonstrated as useful for individuals with moderate to severe COPD. Significant improvements in the IA’s CAT scores after 3 mo of practice suggests that pranayam can improve the subjective experience of health, disease severity, and functional status for COPD patients, without much improvement in FEV1 actually occurring and with airflow limitation not fully reversible but usually progressive. The research team concluded that pranayam is a useful adjunct treatment and can be an effective rehabilitation program for individuals with COPD.
Corresponding author: Rajesh Gupta, MD E-mail address: [email protected]
Gupta—Pranayam for COPD
1/16/14 2:58 PM
W
orldwide, chronic obstructive pulmonary disease (COPD) has emerged as a major health problem. It is the 12th-largest burden of disease and is likely to be the 5th-largest burden within the next 10 years, although it is preventable and treatable.1,2 Its pulmonary component is associated with an abnormal inflammatory response of the lung to noxious particles or gases. COPD is characterized by airflow limitation that is not fully reversible but is usually progressive.3,4 Airway inflammation in COPD passes to other systems, causing extrapulmonary effects like weight loss, cachexia, osteoporosis, chronic anemia, cardiovascular disorders, and derangement of cognitive function. All effects have an impact on the quality of life.5 Existing medications for COPD do not modify the long-term decline in lung function. Nonpharmacological intervention in the form of pulmonary rehabilitation reduces symptoms, improves the quality of life, and increases physical and emotional participation in everyday activities.3,4 In the last few decades, yoga has been incorporated into modern medicine.6 Relaxation, exercise (asanas), controlled breathing (pranayam), a nourishing diet (satvik), positive thinking, and meditation are its various constituents.7 Yogic breathing, or pranayam, is part of all yogas. This technique of controlled breathing (1) increases the capacity of the lungs, (2) helps to strengthen the internal organs, (3) improves mental control, and (4) strengthens the ability to relax.7 Pranayam has been shown to improve the resting respiratory rate, vital capacity, maximum voluntary ventilation, breath-holding time, and maximal inspiratory and expiratory pressures.6,7 It reduces the dead-space ventilation (the volume of air that is inhaled but does not take part in the gas exchange), and it aerates the whole lung, in contrast to regular shallow breathing that ventilates only the bases of the lung. This full aeration has beneficial effects on exercise performance and quality of life.6 When individuals with COPD have been specifically trained to perform pranayam, the strength of both the inspiratory and expiratory muscles increased.6,7
COPD3 of the study’s procedures and obtaining written consent, 50 medically stable individuals (mostly male) were divided into 2 arms of 25 participants each. The research team clinically ruled out certain disease states for participants using an electrocardiogram (ECG) or other specific investigations as required, including (1) asthma or any other pulmonary or major systemic diseases (eg, ischemic, rheumatic, or congenital heart disease or cor pulmonale [pulmonary heart disease]) and (2) any renal or hepatic diseases. All participants had been exsmokers for at least 6 months or were nonsmokers.
Materials and Methods The research team studied the effects of pranayam on medically stable individuals with moderate to severe COPD.3
Intervention Participants in the intervention arm (IA) performed pranayam for 30 minutes, twice per day, and received the usual medicines for COPD. The control arm (CA) took only the usual medicines for COPD. Participants in the IA could adopt any meditative or comfortable postures under the supervision of yoga instructors. Participants in the IA were trained to perform pranayam using 4 easy and effective asanas, including suryabhedana, nadishuddhi, bhramari, and kapalbharti,6,7 performing each for 5 to 7 minutes. This time decreases to a minimum of 20 minutes as one acclimates to the process. Suryabhedana. The practitioner closes his or her left nostril using the ring and little fingers on the right hand and inhales slowly and deeply through the right nostril. The practitioner then closes the right nostril with the right thumb and exhales slowly and deeply through the left nostril. The exhalation should be longer than the inhalation. The practitioner repeats the cycle. Nadishuddhi. The practitioner closes his or her right nostril with the right thumb, exhales completely with the left nostril, and then inhales deeply through the same nostril. The practitioner then closes his or her left nostril with the ring and little finger of the right hand and exhales slowly and completely through the right nostril. The practitioner repeats the rounds, alternating the nostrils. Bhramari. The practitioner inhales deeply and then exhales to produce a low-pitched sound resembling the humming of a bee, feeling the vibrations in his or her entire head. The practitioner repeats the process. Kapalbharti. The practitioner breathes rapidly through the nostrils, with active and forceful exhalation and passive inhalation.
Participants The current study was conducted at a tertiary care institution, Pandit Bhagwat Dayal Sharma Postgraduate Institute of Medical Sciences in Rohtak, Haryana, India, with the participation of 3 departments—Physiology, Yoga and Naturopathy, and Pulmonary Medicine—after approval by the Interdepartment Meeting (IDM). Participants/patients were shortlisted from those regularly attending Chest OPD, the school's respiratory clinic. After informing potential participants with moderate to severe
Outcome Measures The participants were drawn from our Chest OPD patients and advised to attend the physiologist. After the processes of excluding, including, explaining, and initial (baseline) recording on a separate card/sheet for the study (in addition to a Chest OPD card), the participants were referred to regularly follow-up at the Chest OPD (CA and IA) and yoga clinics (IA). For the IA, this occurred daily until each was confident in performing pranayam, at which time the IA participants switched to weekly follow-
Gupta—Pranayam for COPD
IMCJ_13_1.indd 27
Integrative Medicine • Vol. 13, No. 1 • February 2014
27
1/16/14 2:58 PM
Table 1. Comparison of IA and CA IA CA Mean ± SD (n = 25) (n = 25) 24/1b Gender: 24/1a Male/ Female, n Mean ± SD Age, y 52.5 ± 3.9 BMI 20.8 ± 1 51.1 ± 8.7 FEV1c 6MWT 257.1 ± 0.5 BODE Index 4.9 ± 0.7 CAT Score 21.2 ± 2.6
Mean ± SD 52 ± 4.1 20.78 ± 1.2 49.6 ± 8.6 251.1 ± 38.1 5 ± 0.7 21.6 ± 2.7
P Value
>.05 >.05 >.05 >.05 >.05 >.05
One participant was female. One participant was female. c FEV1 is measured by the percent of the predicted value taking all other variables into consideration. a
b
ups. IA could follow up with Chest OPD clinic at any time and with the physiologist after 3 months. Using a separate card, participants included in the study attended the Chest COPD clinic at baseline then followed up whenever required or monthly, without revealing their participation in the study. The research team did not reveal the results of the COPD consultation to the yoga (pranayam) instructor. To evaluate the benefits of pranayam, the research team used the BODE (body-mass index, obstruction, dyspnea, exercise) capacity index8 and the COPD assessment test (CAT) score.9 The BODE capacity index involves measuring forced expiratory volume in 1 second (FEV1), which is used for grading the disease, and the CAT is a concise, validated questionnaire based on the subjective feelings of the individual. All participants in the 2 arms were evaluated using the BODE capacity index8 and the CAT score9 at baseline and at 3 months. BODE Capacity Index.8 The index is a composite marker of the disease, taking into consideration its systemic nature as evaluated based on the measurement of the FEV1, the 6-minute walk test (6MWT) in meters, the modified Medical Research Council (MMRC) dyspnea scale,10 and the body mass index (BMI). CAT.9 The assessment is a concise and simple questionnaire about cough, phlegm, chest tightness, breathlessness, activity, confidence, and energy (power) of individuals. Using the CAT score, medical practitioners identify the CAT score impact level: 30 = very high.9 Data Analysis Calculations were carried out by standard statistical methods with SPSS version 11 (SPSS Inc, Chicago, IL, USA) using mean ± standard deviation (SD), paired, for comparing changes within same arm and unpaired t tests 28
Integrative Medicine • Vol. 13, No. 1 • February 2014
IMCJ_13_1.indd 28
for comparing changes between the 2 arms. The level of significance for results was expressed using P values, with P < .05 being statistically significant. Results In the span of 1 month, 100 individuals were considered for study. Of these, 50 individuals were enrolled. The IA and CA were similar with respect to age, gender, FEV1, and 6MWT scores. All participants had grade-2 dyspnea, as measured by the MMRC scale.10 Table 1 compares the ages, genders, and results of testing at baseline for the 2 groups. The research team recorded results for each participant, identified the differences between his or her baseline values and the values after 3 months, and calculated the mean differences and SDs from baseline to the end of the study for each group. The research team also compared the mean differences from baseline to the end of the study between groups, using an unpaired t test. The study’s most exciting results stem from the comparison of the change from baseline to the end of the study between the 2 groups. The calculations from the unpaired t test provided statistically significant results for both the CAT score and the 6MWT (borderline significant), as shown in Table 2. The IA’s CAT scores improved from 21.24 ± 2.69 to 17.4 ± 2.54 (ie, the impact level goes from high [>20] to medium [10-20]).9 The 6MWT, an alternative exercise test or a measure of generalized performance, improved significantly for the IA as compared to the CA (P < .05), but after 3 months, the FEV1, a measure of airflow that is commonly impaired in individuals with COPD and that is associated with poor functional status, and the BODE capacity index, failed to improve in a statistically significant manner for the IA. This result is relevant to the use of pranayam as an auxiliary measure for individuals with COPD. In the CA, after 3 months of typical medical treatment, no improvement was observed but, rather, a slight deterioration occurred. In the IA, no exacerbations of COPD symptoms in any one of the participants had occurred after 3 months. Overall, they were feeling better according to the CAT score. The IA had no increases in requirements for medical intervention, although the medical treatments were not considered in the study. In the CA, members experienced deteriorations in condition and increases in requirements for medicines, but no admissions occurred that would cause the research team to call the changes exacerbations. Discussion COPD is a multifaceted disorder with pulmonary and systemic components impairing the quality of life of the affected. It is irreversible and progressive. Regular medical treatment needs to be maintained at the same level for long periods unless significant side effects occur or the disease worsens. Progression of the disease can be delayed Gupta—Pranayam for COPD
1/16/14 2:58 PM
Table 2. Change in IA and CA After Pranayam for 3 Months IA Parameters Mean ± SD BODE Index CAT Score FEV1d 6MWT
Baseline 4.9 ± 0.7 21.2 ± 2.8 51.2 ± 8.7 257.1 ± 40.5
After 3 Mo 4.8 ± 0.9 17.4 ± 2.5 53.3 ± 8.8 264 ± 4
CA
P Value Baseline 5.04 ± 0.7 >.05a .05a 49.6 ± 8.6 >.05a 251.1 ± 38
After 3 Mo 5.2 ± 1.1 21.4 ± 2.7 49.1 ± 8.7 249.2 ± 36.8
IA/CA After 3 Mo P Value P Value >.05 >.05a >.05 .05 >.05a >.05 20) to medium (10-20).9 The findings indicate that pranayam can improve the general condition of individuals with COPD, relieving their symptoms and making them feel better. Nonsignificant improvement in the BODE capacity index in the IA after 3 months of practice indicated that pranayam improved the performance status of individuals with COPD without much improvement in lung function. Borderline improvements seen in the 6MWT, one of the parameters of the BODE capacity index, led the research team to the same conclusion (ie, improvement in performance/activity). Gupta—Pranayam for COPD
IMCJ_13_1.indd 29
Researchers have suggested various mechanisms of efficiency of the lungs in individuals practicing pranayam. Pranayam causes nonfunctional or closed airways to work.6,7 It promotes abdominal respiration, providing relief to the main muscle of respiration, the diaphragm. This abdominal respiration not only improves respiration and oxygenation but also improves circulation. Researchers speculate that the movements or massage of the abdominal viscera during abdominal respiration, as per the maneuvers of pranayam, is the mechanism for improvement in the systemic manifestations of COPD. Clearance of airways with deep and slow breathing helps to combat secretions by keeping the weak and collapsed airways in the disease clear to expel the secretions by ciliary action and, therefore, inflammation of respiratory passages. Consequently, systemic inflammation is relieved, and so are its manifestations.7 Pranayam is easy to understand and requires little effort to perform, making it almost cost-free. Maintenance of it does not require much time (15-20 min) as a routine. The CAT score9 has recently been introduced as a test for regular assessment of COPD symptoms,4 which wax and wane in the course of disease. The test grades them on the basis of a concise, validated questionnaire without measuring any physical parameter, whereas the BODE capacity index involves physical parameters—FEV1, MMRC, 6MWT, and BMI—that are unlikely to improve upon each grading. The CAT gives better information regarding the worsening of COPD.8 This study provided observations at 3 months of practice of pranayam. Further practice could add to the improvement because inflammation might subside further and symptoms might be further relieved, thereby giving individuals with COPD more confidence. In the current study, the research team has studied the benefits of pranayam for individuals with moderate to severe COPD. If researchers studied the practice of pranayam for people at an earlier stage of the disease or for healthy individuals, it would likely be even more productive.
Integrative Medicine • Vol. 13, No. 1 • February 2014
29
1/16/14 2:58 PM
Table 3. Baseline and 3-month Outcome Measurements for IA Participant 2 Initial At 3 Mo 46 48 FEV1a 6MWT (m) 210 240 MMRC 2 2 >21 >21 BMI(kg/m2) BODE Index 5 5 CAT Score 22 18 a FEV1 is measured by the percent of the predicted value taking all other variables into consideration.
Table 4. Baseline and 3-month CAT Data for IA Participant 2a
Coughing: never/all the time Chest phlegm (mucous) level: none/completely full My chest feels tight: not at all/ very tight Walking up a hill or 1 flight of stairs leaves me: not breathless/ very breathless My activities at home are: not limited/very limited Despite my lung condition, when I leave home I am: confident/not at all confident The quality of my sleep with regard to my lung condition: I sleep soundly/I do not sleep soundly Energy: I have lots/I have none at all Totals
Baseline 2 3
3 Mo of Intervention Practice 2 2
3
2
4
3
3
2
2 2 Case Reports The following case examples from the trial illustrate how pranayam worked 3 3 as an adjunctive therapy to improve markers of activity for 2 participants. IA, Participant 2. The participant is a 55-year-old male with a known, 10-year 2 2 case of COPD with intermittent acute exacerbations. He has no history of 22 18 tuberculosis, diabetes mellitus, hypertension, allergy or asthma, cerebrovascular accident, a CAT scoring is based on a 6-point subjective scale from 0 to 5 with 0 or other disease and is nonalcoholic. describing symptoms as less severe and 5 describing symptoms as Although he has not smoked for 7 years, he more severe. maintained a habit of smoking 3 to 4 bundles (20 ea) per day for 10 years. At baseline, his SpO2 oximetry reading was 97% in his impairment impact from moderate to low (Table 4). IA, Participant 32. Participant is a 53-year-old male respiratory system exam. Auscultation revealed decreased whose COPD has been known for more than 7 years. He bilateral breath sound and no wheezing or rhonchi evident. has no history of antituberculosis treatment. In addition, The participant’s pulse rate was 102 beats per minute and, he has not been diagnosed with diabetes mellitus, upon cardiovascular exam, S1 and S2 were heard normally. Blood pressure was measured at 130/80 mm Hg. No hypertension, allergy or asthma, cerebrovascular accident abnormalities of the central nervous system were detected. or other disease, and is nonalcoholic. The participant Posteroanterior x-ray showed COPD-related changes with smoked cigarettes for 15 years at the rate of 6 to 7 bundles no infiltration. (20 ea) per day before quitting the habit 5 years ago. Following examination on March 9, 2011, the general At baseline, his SpO2 oximetry reading was 94% in his condition of the participant was stable with dyspnea respiratory system exam. Auscultation revealed decreased evaluated as minimal. Treatment at the time included bilateral breath sound and no wheezing or rhonchi evident. tiotropium inhaler, 2 puffs twice per day. In addition, the The participant’s pulse rate was 92 beats per minute and, following medications were initiated: (1) amoxiclav tablets upon cardiovascular exam, S1 and S2 were heard normally. (625 mg), three times daily and (2) Deriphylline (300 mg), No abnormalities of the central nervous system were twice daily for 10 days. He was asked to return for follow- detected. Posteroanterior x-ray showed COPD-related up after 10 days. At follow up on April 13, 2011, the changes with no infiltration. participant presented in better general condition and his Following examination on March 16, 2011, the medication was returned to just his tiotropium inhaler at general condition of the participant was stable with 2 puffs twice daily, as before, with multivitamin support dyspnea evaluated as absent. Treatment including (1) added. On November 5, 2011, the participant was advised azithromycin tablets (500 mg), once daily for 7 days, and to continue his current treatment protocol. (2) tiotropium inhaler, 2 puffs daily, was initiated. At Following 3 months of pranayam practice, participant follow-up on April 13, 2011, the tiotropium inhaler was 2 showed signs of improvement in 6MWT and CAT score continued at 2 puffs daily and a multivitamin was (Table 3), including subjective improvement in 4 categories recommended. On June 11, 2011, the participant was of the CAT scale resulting in a reclassification of his advised to continue his current treatment regimen. 30
Integrative Medicine • Vol. 13, No. 1 • February 2014
IMCJ_13_1.indd 30
Gupta—Pranayam for COPD
1/16/14 2:58 PM
Table 5. Baseline and 3-month Outcome Measurements for IA Participant 32 Initial At 3 Mo 47 48 FEV1a 6MWD (m) 230 237 MMRC 2 2 >21 >21 BMI(kg/m2) BODE Index 5 5 CAT Score 22 20 a FEV1 is measured by the percent of the predicted value taking all other variables into consideration.
Following 3 months of pranayama practice, participant 32 showed signs of improvement in 6MWD and CAT score (Table 5), including subjective improvement in 2 categories of the CAT scale resulting in a reclassification of his impairment impact from moderate to low (Table 6).
Table 6. Baseline and 3-month CAT Data for IA Participant 32a 3 Mo of Intervention Baseline Practice Coughing: never/all the time 2 2 Chest phlegm (mucous) level: 1 1 none/completely full My chest feels tight: not at all/very 3 2 tight Walking up a hill or 1 flight of 4 3 stairs leaves me: not breathless/ very breathless My activities at home are: not 3 3 limited/very limited Despite my lung condition, when I 3 3 leave home I am: confident/not at all confident 3 3 The quality of my sleep with regard to my lung condition: I sleep soundly/I do not sleep soundly Energy: I have lots/I have none at 3 3 all Totals 22 20
a CAT scoring is based on a 6-point subjective scale from 0 to 5 with 0 Conclusions describing symptoms as less severe and 5 describing symptoms as more The current study demonstrated that severe. pranayam can be useful for individuals with moderate to severe COPD. 10. MRC dyspnoea scale. National Institute for Health and Care Excellence Web Significant improvements in the IA’s CAT scores after 3 site. http://www.nice.org.uk/usingguidance/commissioningguides/pulmonaryrehabilitationserviceforpatientswithcopd/mrc_dyspnoea_scale.jsp. months of practice suggests that pranayam can improve Updated December 13, 2007. Accessed May 10, 2012. the subjective experience of health, disease severity, and 11. COPD. American Lung Association Web site. www.lung.org/lung-disease/ copd. Accessed May 10, 2012. functional status for COPD patients, without much 12. Grove TP. Should patients with chronic obstructive pulmonary disease be improvement in FEV1 actually occurring and with airflow prescribed a resistance-training program? Br J Sports Med. 2010;44(6):396397. limitation not fully reversible but usually progressive. The 13. Kunik ME, Braun U, Stanley MA, et al. One session cognitive behavioral research team concluded that pranayam is a useful adjunct therapy for elderly patients with chronic obstructive pulmonary disease. Psychol Med. 2001;31(4):717-723. treatment and can be an effective rehabilitation program 14. Emery CF, Schein RL, Hauck ER, MacIntyre NR. Psychological and cognitive for individuals with COPD. outcomes of a randomized trial of exercise among patients with chronic
References
1. COPD statistics. COPD International Web site. http//www.copd-international.com/library/statistics/htm. Accessed January 23, 2010. 2. Halbert RJ, Natoli JL, Gano A, Badamgarav E, Buist AS, Mannino DM. Global burden of COPD: systematic review and meta-analysis. Eur Respir J. 2006;28(3):523-532. 3. Global Initiative for Chronic Obstructive Lung Disease. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease (2010 update). http://www.goldcopd.org/uploads/users/files/ GOLDReport_April112011.pdf. Accessed March 23, 2011. 4. MacNee W. ABC of chronic obstructive pulmonary disease: pathology, pathogenesis, and pathophysiology. BMJ. 2006;332(7551):1202-1204. 5. Agusti AG, Noguera A, Sauleda J, Sala E, Pons J, Busquets X. Systemic effects of chronic obstructive pulmonary disease. Eur Respir J. 2003;21(2):347-360. 6. Bijlani RL, Manjunatha S. Yoga. In: Bijlani RL, Manjunatha S. Understanding Medical Physiology: A Textbook for Medical Students. 4th ed. New Delhi, India: Jaypee Brothers Medical Publishers; 2011:743-775. 7. Katiyar SK, Bihari S. Role of pranayama in rehabilitation of COPD patients— a randomized controlled study. Indian J Allergy Asthma Immunol. 2006;20(2):98-104. 8. Celli BR, Cote CG, Marin JM, et al. The body-mass index, airflow obstruction, dyspnea, and exercise capacity index in chronic obstructive pulmonary disease. N Engl J Med. 2004;350(10):1005-1012. 9. GlaxoSmithKline. COPD Assessment Test Web site. www.CATestonline.org. Published September 2009. Accessed September 17, 2011.
Gupta—Pranayam for COPD
IMCJ_13_1.indd 31
obstructive pulmonary disease. Health Psychol. 1998;17(3):232-240. 15. Coulehan JL, Schulberg HC, Block MR, Madonia MJ, Rodriguez E. Treating depressed primary care patients improves their physical, mental, and social functioning. Arch Intern Med. 1997;157(10):1113-1120. 16. Coventry PA, Gellatly JL. Improving outcomes for COPD patients with mildto-moderate anxiety and depression: a systematic review of cognitive behavioral therapy. Br J Health Psychol. Sept 2008;13(pt 3):381-400. 17. Fernandes M, Cukier A, Feltrim MI. Efficacy of diaphragmatic breathing in patients with chronic obstructive pulmonary disease. Chron Respir Dis. 2011;8(4):237-244. 18. COPD: breathing techniques. Canadian Lung Association Web site. http:// lung.ca/diseases-maladies/copd-mpoc/breathing-respiration/index_e.php. Accessed May 12, 2012.
Integrative Medicine • Vol. 13, No. 1 • February 2014
31
1/16/14 2:58 PM
