It is not only the diaphragm that helps move air in and out of the lungs; accessory muscles, too, play an important role. How do we train them? 

Pulmonary Rehab 2A

Lung failure involves either alterations in the gas exchange units—presenting as hypoxemia; or failure of the respiratory pump—presenting as hypercapnia. While the importance of the diaphragm for generating pressure swings in the thorax to move air in and out of the lung has been emphasized, the accessory muscles of respiration (intercostal, scaleni, sternomastoids, and others) assume a more prominent role as the work of breathing increases due to hyperinflation, as seen in chronic obstructive pulmonary disease (COPD).

The neural recruitment strategy used by the respiratory pump seeks to maintain alveolar ventilation while minimizing the work of breathing. Demand for nutrient delivery and blood flow to the active muscles continues to increase, and an energy supply/demand deficit presents. Changes in metabolic functioning of the respiratory muscle compromise strength and endurance, giving rise to muscle weakness and fatigue.

Many opportunities for intervening in respiratory pump failure exist: reducing respiratory muscle loading, resting the fatigued muscles, or enhancing myocyte contractility and muscle energetics offers opportunities to return to a meaningful quality of life. Respiratory muscle weakness is a powerful predictor for survival in COPD patients, thus emphasizing muscle function restoration as a primary focus.1 This paper will focus on one aspect of pump failure—respiratory muscle strength/fatigue—and review the various approaches to enhance muscle function through muscle training.

PRESENTATION OF RESPIRATORY MUSCLE WEAKNESS

During muscle fatigue, inspiratory muscles, rather than expiratory muscles, are stressed to the point of failure.2-4 Inspiratory muscle compromise is attributed to hyperinflation (muscle length/tension disadvantage), while expiratory muscle weakness is often attributed to a generalized myopathy in COPD patients,5 promoting a low lactate threshold6 and a reduction in muscle oxidative enzyme activity.7,8 Clinical signs suggestive of respiratory muscle weakness include unexplained reduction in vital capacity, CO2 retention (awake or sleeping), dyspnea, orthopnea (shortness of breath while supine), short sentences while conversing, tachypnea, paradoxical movement of the abdominal and thoracic wall, problems with cough (recurrent infections), and generalized muscle weakness.5 However, respiratory muscle weakness is often advanced, reflecting compensatory respiratory pump mechanisms, the low respiratory muscle forces required to overcome declining abilities, and the low correlation between symptoms and respiratory muscle strength and endurance measures. Thus, the overarching symptom of respiratory muscle weakness is dyspnea.9 This simple presentation suggests that all suspected patients should be evaluated during exercise for early detection and tracking of disease progression. For example, the 6-minute walk or shuttle test should be routinely administered in patients predisposed to respiratory muscle weakness and subjective dyspnea ratings evaluated.10-12 Even modest increases in dyspnea may be suggestive of disease progression and the need to intervene, while a reduction in dyspnea ratings may indicate a response to therapy.13

RESPIRATORY MUSCLE TRAINING

The most widely used forms of respiratory muscle training (RMT) focus on both inspiratory muscle training (IMT) and components of expiratory muscle training (EMT). Inspiratory muscle training has assumed a key role in reestablishing muscle function, while a definitive role for EMT remains to be established. Inspiratory muscle training reduces dyspnea in normal young individuals14,15 and in patients with COPD.16,17 Lotters et al16 noted a reduction in dyspnea and improved exercise ability using meta-analysis for respiratory muscle training.

Additionally, Beckerman et al18 documented that 1 year of IMT decreases utilization of health care services and suggested this may assist in reducing the overall economic costs. Ongoing debate regarding the mechanisms for enhancement of respiratory muscle strength following IMT remains. Some advocate that in COPD patients, the respiratory muscles are under chronic loading and, thus, have adapted to this chronic loading, eg, training. However, IMT has demonstrated an increase in type I fibers (38% increase) and an increase in the size of type II fibers (21%) of the external intercostal muscles.19 Further, indirect data demonstrates improved function following training suggestive of changes in the respiratory pump.16,20-22

EXERCISE PHYSIOLOGY AND TRAINING

The principles for training are now known and include training frequency, intensity, duration, and mode of training.23,24 What remains is how to design training programs for specific populations using the principles discussed above that elicit the desired predicted outcomes. Thus, there is ongoing research in many areas to address this concern and gap in our knowledge. Focusing on respiratory muscle dysfunction, the question arises as to how we might be able to enhance function beyond that provided by specific medical interventions aimed at removal of or limiting the underlying causative pathophysiology. Thus, a number of approaches have been used with varying levels of success in specific cohorts.


Both IMT alone and in combination with general exercise condtioning yielded significant increases in inspiratory muscle strength and endurance.


INSPIRATORY MUSCLE TRAINING DEVICES AVAILABLE

Inspiratory muscle training devices can be categorized into three distinct types: nontargeted inspiratory resistance trainers (NIRT), targeted inspiratory muscle trainers (TIMT), and normocapnic hyperventilation trainers (NHT).

Nontargeted inspiratory resistance training requires the individual to perform inspiratory and expiratory efforts via a variable diameter orifice at a setting selected for that individual (eg, Pflex device, HealthScan Inc, Cedar Grove, NJ, [HealthScan Inc no longer markets the Pflex; it has been replaced by the Threshold IMT] and the Respirex 2 incentive spirometer with an inspiratory muscle trainer, Respirex, Canastota, NY). The smaller the orifice, the greater the flow resistance, thereby requiring greater effort to move air in and out through the device. Patients are allowed to manipulate their breathing strategies, and so the threshold differs from individual to individual at the same orifice setting.

Thus, the training load varies according to a power function and not just the orifice size.25 For those who choose this training method, careful attention to controlling the breathing strategy is required.17 When this and other issues are controlled through equipment modifications, some positive results are demonstrated. For example, improvement in respiratory muscle strength, dyspnea reduction, and improved exercise tolerance have been noted.20,21,26

Targeted inspiratory muscle training devices provide controlled exercise intensity by controlling inspiratory pressures. Briefly, the patient is required to generate negative pressure through inspiration sufficient to overcome the load the device is set to deliver. However, breathing strategies will allow the subject to alter the training intensity if not monitored. Typically, these devices provide visual feedback so that the subjects can maintain their breathing patterns at the prescribed level and thus their training intensity.

The simplest approach to TIMT is through incentive spirometry, which provides a target combined with a resistance trainer for adjusting the resistance orifice. The subject is instructed to maintain a specific flow at a prescribed orifice setting, thereby maintaining the intensity of training. Others have used various methods to control pressure for inspiratory muscle training. Weighted plungers,27 solenoid valves, a constant negative pressure system,28 and a spring-loaded poppet valve29,30 have all been used. Each relies on unimpeded expiratory flow through a valve system. Generally, these training devices have improved strength,16,31 maximal rate of muscle shortening,14 maximal power output,32 and muscle endurance.33,34

Normocapnic hyperventilation trainers. Belman and Mittman were perhaps the first to use NHT as a method for improving ventilatory muscle function.34,35 This work was followed by a paper by Levine et al,36 wherein the authors noted a significant increase in maximal sustained ventilatory capacity (MSVC) as compared to IPPB with no other significant changes noted between the groups. NHT requires subjects to maintain high target levels of ventilation for the prescribed time, while carbon dioxide is held fairly constant through rebreathing. The MSVC is the primary outcome and can be achieved by training 30 minutes/day 3 to 5 times/week at 70% to 90% of the measured MSVC. The major drawback to this form of training is that the required equipment is often expensive and complicated and not suited for ambulatory individuals at home.

Breathing Appartus

OUTCOMES

Since the pioneering work of Leith and Bradley in 1976,37 the question regarding the effectiveness of respiratory muscle training in selected populations has evolved. The early work was flawed by poor experimental designs and inadequate control of experimental variables. To assist the reader to better understand the potential for RMT, two meta-analyses were conducted. Smith et al17 and later Lotters et al16 established criteria for the inclusion of published papers and other aspects of the included research in the analysis.

The flaw in the study by Smith et al was that they included results derived from studies that failed to control training intensity during inspiratory resistive loading. Therefore, the calculated effect sizes were questioned; and, if a better analysis were performed, it might have demonstrated more consistent improvements following training. This was the focus of the analysis performed by Lotters et al.16 On the basis of an improved training intensity inclusion decision of at least 30% of the measured inspiratory pressure maximum (PImax), a clearer understanding regarding training of the respiratory muscles was obtained.

As noted, both IMT alone and in combination with general exercise conditioning yielded significant increases in inspiratory muscle strength and endurance, dyspnea was reduced both at rest and during exercise, and a trend for improved exercise was demonstrated for the combined IMT and exercise conditioning protocols. Other newer studies investigated IMT alone38 and in combination with general exercise conditioning.39 These recent updates reaffirm that IMT alone can improve inspiratory muscle strength and endurance and reduce dyspnea; and when it is used in combination with exercise training, additional benefits may exist.

Additional studies have now been accumulated to extend past efforts and address very specific issues. In animal models, the application of intermittent resistive loading resulted in type II fiber hypertrophy in diaphragm muscle40 and in the external intercostal muscles of COPD patients.19 These studies confirmed that structural remodeling was possible through inspiratory muscle training in normal animals and patients with COPD. More specifically, the present data suggest that IMT does improve function in those with weak inspiratory muscles and that improved force translates to improved outcomes.41

WHICH PATIENTS ARE MORE LIKELY TO SHOW A BENEFIT?

For individuals with COPD, the most likely candidate is the individual who presents with inspiratory muscle weakness (PImax <60 cm H2O) who has been medically optimized for a training intervention.42 Also, patients with a low Pao2 or high PaCO2 who trained using IMT showed improvement on several physiologic indices, with a universal finding of a reduction in dyspnea noted. Improvement in respiratory muscle strength and endurance and a reduction in nocturnal desaturations have been observed.29,43-45 These findings have been attributed to changes in PImax, which changes the PI/PImax ratio, an index of respiratory muscle work, promoting improved gas exchange (? PaCO2) and reducing dyspnea.29,33,46 When IMT is used in conjunction with general conditioning, there is greater improvement in performance noted for the IMT and general conditioning group. It should be noted that dyspnea scores (Borg and CRQ scores) did not demonstrate additional improvement by adding IMT, and while the trend was suggestive for additional improvement in general exercise capacity, statistical significance was not obtained using meta-analysis.47

HOW TO DESIGN THE TRAINING PROGRAM

Once optimal medical management has been established and suitable candidates exist, the next step is to design a program with specific objectives. Intensity, frequency, mode, and duration of training are all part of the training algorithm. The following recommendations were arrived at based on prior research. Intensity is perhaps the most difficult and should be based on an objective measure of strength or endurance or both. For example, multiple studies have used the PImax adjusted for lung volume to arrive at a training intensity. A range of 30% to 70% PImax has been used in prior studies with success. A lower intensity setting can be used for patients who are more debilitated. Progression for adjusting the intensity should be 5% per week or as tolerated, with ongoing monitoring of the changing PImax.

Frequency of training can refer to the number of training times per day and per week. At the onset of training, it might be advisable to break up the training into short bouts spaced throughout the day. What is important for training to ultimately succeed is that the volume of exercise be sufficient to elicit a response. To factor in the volume, you will need to also consider duration of training at the prescribed training intensity. A minimum of 30 minutes per day is recommended, but patients may need to start lower depending on their tolerance and response to training. Volume of exercise is the frequency times duration of exercise accomplished per day or week. Thus, duration and frequency of training can be varied to accommodate individual patients, with the total volume of exercise accomplished per day or per week used as the criterion outcome.

We recommend that once a training program has been selected, a trial training session should be attempted in front of the professional guiding the program. If tolerated by the patient, the at-home program can continue. If difficulties exist, however, the program may require modification.

SUMMARY

In general, outcomes can be described for changes in inspiratory muscle strength and endurance, dyspnea, health related quality of life (HRQL), and exercise tolerance. Changes in respiratory pressures are reflected by changes in maximal pressure obtained during incremental threshold loading, inspiratory and expiratory pressure maximum (PImax and PEmax at a controlled lung volume), and maximal sustained inspiratory pressure (SIPmax). Changes in dyspnea are documented through the use of various dyspnea scales, while HRQL changes reflect score improvements in the available HRQL instruments. Changes in exercise performance reflect changes in distance walked (6-minute walk test) or outcomes obtained from laboratory testing using a variety of protocols and devices to document work capacity.

The strength of the conclusions should be judged with the noted limitations for the specific training devices/approaches. Further, IMT is not just for COPD patients but for other patients who demonstrate respiratory muscle weakness such as those experiencing congestive heart failure and others with various muscle-specific issues. Additional data is needed to identify the best candidates for training and the best training regimen to optimize function and progression of training.


Rick Carter, PhD, MBA, is professor, exercise sciences; Brittnee Rodriguez is a fourth year premed student; Yunsuk Koh, PhD, is assistant professor, exercise sciences; Daniel R. Chilek, PhD, is associate professor, exercise sciences, Lamar University, Beaumont, Tex. Jim Williams, PhD, is associate professor, exercise physiology, Texas State University, San Marcos. For further information, contact [email protected].

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