Diaphragmatic breathing training: further investigation needed.

To the Editor:

I commend the authors of the Perspective article "Evidence Underlying Breathing Retraining in People With Stable Chronic Obstructive Pulmonary Disease" (December 2004) on their observations, interpretations, and recommendations regarding pursed-lips breathing (PLB). As a person who has emphysema and as a clinical psychologist who has presented with physical therapists on yoga and chronic obstructive pulmonary disease (COPD), (1) and as someone who serves on the Board of Directors of the National Emphysema/ COPD Association and is a member of COPD-ALERT, I was particularly interested in this article. However, I believe the conclusions regarding diaphragmatic breathing (DB) training warrant further scientific investigation.

The following questions and suggestions can be used for testable hypotheses:

1. Pursed-lips breathing is a conscious and deliberate action and can be tiring after a short period. I believe, therefore, that diaphragmatic breathing stands a better chance of becoming an automatic habit or behavior. Should PLB or DB be the method of choice for cultivating slow breathing as a habitual pattern of breathing?

2. Should people with COPD, who are not likely to benefit from PLB, be taught DB instead in order to slow down their breathing?

3. Should PLB or DB be the method of choice for reaching a very slow rate of breathing, such as 6 breaths per minute? Recent studies showed that 6 breaths per minute improved the efficiency of gas exchange in people without known pathology or impairments (2) and improved 6-minute walk distance in people with COPD. (3)

4. Which of the 2 techniques has greater overall health benefit for people with COPD? Diaphragmatic breathing, according to the teachings of some yoga schools, gently stimulates and massages the heart and abdominal organ areas, aids peristaltic movement, increases cerebral blood flow, and promotes spinal flexibility and improvement in posture.

5. Many patients use secondary breathing muscles. Would PLB or DB be more effective for disengaging the upper chest and neck muscles during breathing?

6. Would PLB or DB be more effective for anxiety reduction and mental relaxation, which are so critical in COPD?

7. The authors expressed some reservations regarding DB training, because DB appeared to have increased paradoxical breathing movements. In patients who habitually do paradoxical breathing, would PLB or DB be the technique of choice to establish correct breathing pattern?

8. What should be the optimal length, curriculum, and techniques for teaching DB and related breathing and airway clearance techniques to a person with COPD before we regard DB as redundant, harmful, or too cost-prohibitive?

9. In the study by Breslin (4) cited by the authors, Breslin reported that, during PLB, decreased diaphragm activity during inspiration was accompanied by increased use of rib-cage muscles. We do not know whether Breslin was referring to the increase in the activity in the lower ribs or to the increase in activity in the upper ribs. In my experience, a decrease in diaphragm activity and an increase in activity in the lower ribs are incompatible. The role of horizontal expansion of the lower ribs during inspiration is not adequately recognized, and therefore is not specifically taught to the patients with COPD. I say this because the DB studies reviewed by authors seem to have relied on abdominal movement rather than movement of the lower ribs. In my opinion, pulmonary rehabilitation programs in the United States appear to equate abdominal expansion with diaphragm action. I believe we should emphasize movement of the lower ribs because the more powerful action of the diaphragm is in the lower ribs rather than in the front of the abdomen. Furthermore, unless the diaphragm and lower ribs are too rigid, the diaphragm is not recruited if PLB is continued for several minutes. As a yoga instructor, I teach people to "kick in" the diaphragm by doing PLB. Pursed-lips breathing and DB are not incompatible. Perhaps future studies should investigate breathing outcomes in people who do PLB and DB simultaneously.

10. Studies utilizing DB techniques cited by the authors appear to have relied on and measured only abdominal expansion. Were the participants really doing DB? Suppose they were simply focusing on expanding the abdomen with minimal involvement of the diaphragm? Such abdominal excursion can be totally out of sync with the actual diaphragm activity. Therefore, movement of the lower ribs also should be measured to ensure that DB was applied.

11. What is the effect of DB or PLB on dynamic hyperinflation? Studies cited in the article barely touched this subject. In my opinion, dynamic hyperinflation plays a critical role in management of COPD and should be included in therapeutic breathing strategies.

12. Control of shortness of breath and slowing the breathing rate are not the only issues for me, as a person with emphysema. Sometimes, my breath is "slow and short" rather than "slow and deep." Occasionally, I have to use PLB, but I do DB all the time. Diaphragmatic breathing has been extremely beneficial to my ability to function in daily life and to the quality of my personal, recreational, and professional life. Can DB optimize the gas exchange for a person with COPD (and, if so, up to what level of improvement), or is there another method to achieve a breathing pattern of slow, deeper, and fuller breath or end-inspiration breath holding?

I believe that, lest we deprive patients of important health benefits, a negative recommendation for DB training for patients with COPD should be deferred until direct evidence has been established under rigorous scientific standards. I am grateful to the authors for bringing up the issue of relative efficacy and economy of the breathing training techniques, in view of the scarce national health care resources and trained pulmonary staff.

Vijai Sharma, PhD

[e-mail]

References

(1) Yoga breathing therapy in COPD, exchange of East and West techniques. Workshop presented at: 23rd International Symposium on Respiratory Psychophysiology and 11th Annual Meeting of the International Society for the Advancement of Respiratory Psychophysiology; October 17-19, 2004; Princeton,

(2)Giardino ND, Glenny RW, Borson S, Chan L. Respiratory sinus arrhythmia is associated with the efficiency of pulmonary gas exchange in healthy humans. Am J Physiol Heart Circ Physiol. 2003;284:H1585-H1591.

(3) Giardino ND, Chan L, Borson S. Combined heart rate variability and pulse oximetry biofeedback for chronic obstructive pulmonary disease: a feasibility study. Appl Psychophysiol Biofeedback. 2004;29:121-133.

(4) Breslin EH. The pattern of respiratory muscle recruitment during pursed-lips breathing. Chest. 1992;101:75-78.

Author Response:

We thank Dr Sharma for his interest in our article and agree with his observation that questions remain regarding the role of breathing retraining in people with chronic obstructive pulmonary disease (COPD). Our goal in writing this article was to review the evidence on the effects of pursed-lips breathing (PLB) or diaphragmatic breathing (DB) retraining on physiological parameters that met specific inclusion criteria. We excluded descriptive studies because these studies cannot determine whether a cause-effect relationship exists between the specific breathing retraining technique and the measured result. The evidence we reviewed does not support the use of DB to improve ventilation, gas exchange, or the work of breathing in people with COPD. This is in contrast to some clinicians' experiences that suggest that DB is a useful intervention. As we strive to develop an evidence-based practice, personal experience can be a springboard for research hypotheses, but we caution against accepting these experiences as evidence.

Dr Sharma wonders which breathing retraining technique "would be more effective for disengaging the upper chest and neck muscles during breathing." We interpret this as meaning the elimination of accessory muscle use. Because activation of accessory muscles is a normal physiologic response to the increased work of breathing, elimination of this activity may not always be desirable. Nonetheless, we did not find any studies that measured the effect of PLB or DB on electromyographic (EMG) activity of these muscles in individuals with COPD.

When Dr Sharma states in point 9 that "a decrease in diaphragm activity and an increase in activity of the lower ribs are incompatible," we do not know if he is referring to EMG activity of the intercostal or other muscles attaching to the lower rib cage or to movement of the lower rib cage. However, it seems that he has misinterpreted the work of Breslin. (1) Breslin measured changes in abdominal and esophageal pressures in order to infer changes in diaphragm versus rib cage muscle EMG activity. With this measurement technique, rib cage muscle activity is not directly measured, and upper and lower rib cage muscle activity cannot be differentiated.

We agree with Dr Sharma that, in individuals without pulmonary problems, diaphragmatic contraction can cause expansion of the lower rib cage. The amount of lower rib cage motion that is generated by the diaphragm will largely be determined by the zone of apposition of the diaphragm, the angle of insertion of the costal fibers, the compliance of the abdominal compartment, the compliance of the chest wall, the length of the diaphragmatic fibers, and the magnitude of diaphragmatic EMG activity. Diaphragm flattening will influence rib cage and abdominal movement in people with COPD. In our experience, physical therapists may encourage patients to perform lower rib expansion in isolation or combined with abdominal excursion. None of the studies reviewed in our article, however, specifically included rib cage expansion as a criterion for diaphragmatic breathing. Therefore, we cannot report the effectiveness of this technique.

Dr Sharma is correct in noticing that few studies addressed the issue of hyperinflation. We discussed the work of Ingrain and Schilder, (2) who reported that expiratory resistive loading, a surrogate for PLB, increased end-expiratory lung volume, and we related this to work by O'Donnell et al, (3) who noted similar findings. We also explained why expiratory resistive loading may not be a good model of PLB. Studies directly examining the effects of PLB on end-expiratory lung volume, although technically very difficult, could, as Dr Sharma suggests, provide more insight on this important topic. There were no studies that assessed dynamic hyperinflation during DB.

Dr Sharma states that "the diaphragm is not recruited if PLB is continued for several minutes." There is no evidence demonstrating that PLB inhibits the EMG activity of the diaphragm. As far as we know, as long as the central respiratory control center and spinal cord are intact, diaphragm EMG activity will cease only if C[O.sub.2] levels fall below the apneic threshold, if the phrenic nerve is severed, or if oxygen levels rise above a critical level in an individual with chronically elevated C[O.sub.2] levels.

Dr Sharma raises several points that were beyond the scope of our article. We did not review evidence regarding the psychological effects of DB (eg, anxiety reduction), nor did we attempt to investigate people's ability to retrain a "habitual" paradoxical breathing pattern. Work by O'Donnell et als and Loveridge et al (4) may indirectly shed light on the second point. In our article, we cited work by O'Donnell et al, (3) who proposed that people with COPD develop a very fine, active control of expiratory flow and that this control develops with the disease. This suggests that habitual breathing patterns develop because they are in some way advantageous. Similarly, Loveridge et al (4) proposed that changes in breathing patterns in people with COPD reflect changes in neural control of breathing that occur as a result of changes in lung and chest wall mechanics.

In conclusion, Dr Sharma brings up numerous ideas about breathing retraining that were not within the scope of our article (eg, the effect of DB on anxiety) or for which no pertinent experimental studies were found during our review of the literature. We are pleased that our article generated questions about the use of breathing retraining, and we encourage individuals to design and conduct rigorous scientific studies that can further contribute to evidence-based practice.

Gail Dechman, PT, PhD

Associate Professor

Physical Therapy Department

Husson College 

1 College Cir

Bangor, ME 04411

[e-mail]

Christine R Wilson, PT, PhD

Assistant Professor

Department of Physical Therapy

Thomas J Long School of Pharmacy and

Health Sciences

University of the Pacific

Stockton, Calif

References

(1)Breslin EH. The pattern of respiratory muscle recruitment during pursed-lip breathing. Chest. 1992;101:75-78.

(2)Ingram RM, Schilder DE Effect of pursed lips expiration on the pulmonary pressureflow relationship in obstructive lung disease. Am Rev Respir Dis. 1967;96:381-388.

(3) O'Donnell DE, Sanii R, Anthonisen NR, Younes M. Expiratory resistive loading in patients with severe chronic air-flow limitation: an evaluation of ventilatory mechanics and compensatory responses. Am Rev Respir Dis. 1987;136:102-107.

(4) Loveridge B, West P, Anthonisen NR, et al. Breathing patterns in patients with chronic obstructive pulmonary disease. Am Rev Respir Dis. 1984;130:730-733.

To the Editor:

We are writing to discuss several issues related to the Perspective article by Dechman and Wilson. We agree with the authors that the literature supporting diaphragmatic breathing (DB) is relatively weak, but from the available literature and a comprehensive review article that we published in the Journal of Cardiopulmonary Rehabilitation in 2002, (1) it appears that some patients do respond favorably to DB, and it is the role of the physical therapist to examine and determine whether a patient is likely or not to respond to DB. Therefore, the purpose of this letter is to challenge Dechman and Wilson's concluding statement that "there is no rationale for teaching DB to this patient population." We believe that this is very important because of the increasing prevalence and incidence of pulmonary disease. (2,3)

Ten studies of DB were reviewed in the article by Dechman and Wilson. We examined studies of DB published in English, Spanish, and Japanese and therefore were able to review 25 studies of DB (40% more studies than reviewed by Dechman and Wilson). (1) Four of the 25 studies we reviewed were true experimental studies, 3 were quasi-experimental studies, and 18 were pre-experimental studies. We found that 7 of the these studies did not describe the methods of DB, 4 studies poorly described the techniques of DB, and very few of the remaining studies prescribed DB in a similar manner. We therefore question whether there is adequate standardization of DB instruction to permit comparison of studies from multiple institutions.

In our review, a we focused on several specific outcomes of DB, including: (1) methods and competency of DB, (2) the severity of COPD on the effects of DB and the efficiency of breathing and symptoms of COPD after DB, (3) effects of DB on ventilation, (4) chest wall motion and changes after DB, (5) the effects of DB on pulmonary function, respiratory rate, and arterial blood gases, and (6) considering the above outcomes and available literature, methods to perform and prescribe DB to people with COPD. One reason for our focus was to attempt to standardize DB instruction using the available literature in people with COPD. (1)

Some of the areas that we addressed in our article (1) and several issues that were not addressed by Dechman and Wilson can be appreciated using the 2003 article by Jones et al. (4) * The article by Jones et al was published in Physical Therapy after we published our review article. (1) Their article was included in the article by Dechman and Wilson, but no significant discussion was provided about their study. Several major strengths and weaknesses were inherent in the article by Jones et al that should be noted. The

primary strengths of this article were that it was one of only several articles that have examined the effects of DB on oxygen consumption, it provided one of the best descriptions of DB instruction, and it showed that DB decreased oxygen consumption to a level that was similar to that of pursed-lips breathing (PLB) and slightly lower than that of combined PLB and DB. However, it lacked several important measurements (eg, some measure of the degree of hyperinflation such as residual volume or total lung capacity as well as measurement of the breathing pattern via inductive plethysmography), utilized several questionable methods of study (eg, supine body position and plexiglass-ventilated hood/canopy to measure oxygen consumption), and provided an incomplete discussion without full use of the available literature to support or refute the study findings.

The major strengths of studies on DB in people with COPD ([dagger]) include: (1) almost all studies that examined symptoms during DB showed an improvement in symptoms, (2) approximately one third of the studies showed an improvement in pulmonary function or ventilation, and (3) people with moderate to severe COPD demonstrated diaphragmatic motion and change in diaphragmatic length (despite the diaphragm being shorter at functional residual capacity) that were similar to those of people without COPD. (1,5,6) The major weaknesses of studies on DB in people with COPD include: (1) a relatively small number of subjects with COPD who had been studied performing DB, (2) poor methods of DB instruction and examination of competency in DB, and (3) the majority of the studies did not examine symptoms. (1) In view of these aspects, the literature does not suggest that "there is no rationale for teaching DB to this patient population," as suggested by Dechman and Wilson, but it strongly identifies the need for more properly controlled studies of DB.

A number of clinically relevant findings with important clinical implications are present in the available literature on DB in people with COPD. (1) These findings include: (1) movement of the diaphragm, (2) body position used to perform DB and to examine the test-retest the effects of DB, (3) optimal instruction in DB without the possibility of forward protrusion of the abdominal area via abdominal muscle activity (with DB, the abdominal area is protruded forward as a result of the forward displacement of the abdominal contents by the descending diaphragm), (4) measurement of competency with DB, (5) duration, frequency, intensity, and progression of DB training, rind (6) a variety of clinical tests such as the change in symptoms, respiratory rate, tidal volume, and oxygen saturation or arterial blood gases before, during, and after DB. (1) Examining these variables in previous published studies--and including them in physical therapy provided to people with COPD in whom DB may be applicable--are necessary. For example, a patient with marked hyperinflation and a flattened diaphragm who demonstrates little to no diaphragmatic movement is unlikely to benefit from DB.

Pulmonary physical therapy education and care in the United States are in need of greater attention in view of the increasing prevalence and incidence of pulmonary disease. (2,3) Because of this and because some people with COPD may benefit from DB, we believe that the conclusion of Dechman and Wilson is incorrect and that, for appropriate patients, DB may be a valuable therapeutic option. However, it is the role of the physical therapist to examine and determine whether a patient is likely or not to respond to DB. Based on the available literature, people who respond to DB are likely to have elevated respiratory rates, low tidal volumes that increase during DB, and abnormal arterial blood gases with evidence of adequate diaphragmatic movement. (1) Finally, because of the increasing prevalence and incidence of lung disease, there is a need for standardized DB instruction and for more properly controlled studies of DB in people with COPD and other lung diseases.

Lawrence P Cahalin, PT, MA, CCS 

Clinical Professor

Department of Physical Therapy

Northeastern University 

Boston, MA 02115-5000

([e-mail])

Edgar D Hernandez, PT

Clinical Professor

Department of Physical Therapy

National University

Bogota, Colombia

Yoshimi Matsuo, PT, PhD

Department of Physical Therapy

Osaka University Hospital

Osaka, Japan

([dagger]) A summary of major strengths and weaknesses of studies on DB in people with COPD is presented in Table 2 on the Physical Therapy Web site.

References

(1) Cahalin LP, Braga M, Matsuo Y, Hernandez ED. Efficacy of diaphragmatic breathing in persons with chronic obstructive pulmonary disease: a review of the literature. J Cardiopulm Rehabil. 2002;22:7-21.

(2) Lung Disease Data 2003. American Lung Association Web site. Available at: www.lungusa.org. Accessed January 28, 2005.

(3) America's Children and the Environment: A First View of Available Measures. Washington, DC: US Environmental Protection Agency, Office of Children's Health Protection, Office of Policy, Economics, and Innovation, National Center for Environmental Economics; December 2000. EPA 240-R-00-006.

(4)Jones AYM, Dean E, Chow CCS. Comparison of the oxygen cost of breathing exercises and spontaneous breathing in patients with stable chronic obstructive pulmonary disease. Phys Ther. 2003;83:424-431.

(5) Gorman RB, McKenzie DK, Pride NB, et al. Diaphragm length during tidal breathing in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2002; 166:1461-1469.

(6)Kleinman BS, Frey K, VanDrunen M, et al. Motion of the diaphragm in patients with chronic obstructive pulmonary disease while spontaneously breathing versus during positive pressure breathing after anesthesia and neuromuscular blockade. Anesthesiology. 2002;97:298-305.

Author Response:

Clearly, Cahalin and colleagues are concerned about the lack of a standardized diaphragmatic breathing (DB) technique and the omission of competency standards in the current research on breathing retraining. The goal of our article was to review the available evidence on the effects of pursed-lips breathing (PLB) or DB on physiological outcome measures. Although we assessed only studies that were written in English, we reviewed 397 studies, and we discussed 10 studies on DB. We used a clinical definition of DB (increased abdominal motion) and included studies that described subjects performing this motion. Undoubtedly, there were differences in the breathing technique between studies, but this is not uncommon in literature reviews or meta-analyses. For instance, aerobic exercise intensity and duration vary among studies, but it is generally accepted that valuable information can be gleaned from studies that use similar exercise prescriptions.

We did not include studies where DB was performed with modification (such as maximal inspirations or abdominal weights) or when a combination of breathing retraining techniques was used. Using such studies would have clouded our ability to determine whether a cause-effect relationship existed between DB and the measured result. For example, DB performed with maximal inspirations will surely decrease arterial carbon dioxide levels, but this effect is due to the maximal inspirations rather than to the DB. We believe that we achieved our goal and that the result will be helpful to clinicians. A study to assess whether different ways of teaching or performing DB yield different results may be needed to address the issues cited by Cahalin and colleagues.

Other concerns expressed by Cahalin and colleagues include the small numbers of subjects in the available research, the lack of information regarding how disease severity affects DB, and a need to discriminate between those people who will respond to DB and those who do not obtain benefit from the technique. We addressed the issue of small numbers of subjects in our article. The small sample sizes certainly make it impossible to examine how disease severity affects the outcomes of breathing retraining or to distinguish responders from nonresponders. This is simply the state of knowledge regarding DB at this time.

Cahalin and colleagues are particularly concerned about the study by Jones et al. (1) Specifically, they mention that the authors should have included a measure of hyperinflation and that the supine position was not appropriate. We believe that the use of the supine position for testing was reasonable, because DB is frequently taught to patients in this position. Certainly, the changes in diaphragmatic length, zone of apposition, and chest wall configuration that occur when an individual moves from a supine position to a sitting position mean that the results obtained in a supine position may not be generalized to the sitting position. A measure of hyperinflation would be helpful, but its absence does not negate the value of the study. Indeed, many of the studies cited in the review by Cahalin and colleagues did not use a measure of hyperinflation and assessed DB in the supine position.

Cahalin and colleagues cite 2 studies on diaphragmatic motion (Gorman et al (2) and Kleinman et al (3)). These studies present interesting findings about spontaneous breathing in people with chronic obstructive pulmonary disease (COPD), but they do not provide information about what occurs when these individuals are asked to change their breathing patterns and perform DB. Like Sharma, Cahalin and colleagues are concerned about whether the abdominal protrusion that occurs when a patient performs DB is caused by increased diaphragmatic motion or merely abdominal muscle contraction. This is an important question that will require examination with sophisticated imaging techniques before performing any further studies regarding the outcomes of DB.

Cahalin and colleagues present a list of positive clinical effects, which they believe can be attributed to DB. We must emphasize that these positive outcomes must be judged vis-a-vis the rigor of the research design. Many of the studies cited by these authors assessed DB combined with other techniques or modifications. After examining experimental studies that satisfied our inclusion criteria, we were not able to recommend DB as an intervention for people with stable COPD. This is because the positive effect (increased ventilation) that sometimes occurs with DB is related to a slower breathing rate rather than to the abdominal motion per se. A slower breathing rate can be accomplished with simpler techniques such as PLB that do not cause the paradoxical and asynchronous motions of the chest wall and abdomen, which can occur during diaphragmatic breathing. Therefore, we support our original assessment of the technique and, based on the available literature, do not recommend teaching DB to people with COPD.

* A summary of important issues in DB is contained in Table 1 on the Physical Therapy Web site (www.ptjournal.org/info/Letters.cfm).

Gail Dechman, PT, PhD

Christine R Wilson, PT, PhD

References

(1) Jones AYM, Dean E, Chow CCS. Comparison of the oxygen cost of breathing exercises and spontaneous breathing in patients with stable chronic obstructive pulmonary disease. Phys Ther. 2003;83:424-431.

(2) Gorman RB, McKenzie DK, Pride NB, et al. Diaphragm length during tidal breathing in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2002; 166:1461-1469.

(3) Kleinman BS, Frey K, VanDrunen M, et al. Motion of the diaphragm in patients with chronic obstructive pulmonary disease while spontaneously breathing versus during positive pressure breathing after anesthesia and neuromuscular blockade. Anesthesiology. 2002;97:298-305.