Respiratory muscle training for patients with chronic obstructive pulmonary disease.

Key Words: Diaphragm, Exercise tolerance, Inspiratory muscle training, Threshold training.

Chronic obstructive pulmonary disease (COPD) is a group of conditions characterized by airway obstruction. The term "chronic obstructive pulmonary disease" is usually used to refer to a combination of primarily chronic bronchitis and emphysema but can include other conditions such as asthma, bronchiectasis, and cystic fibrosis.[1] In this article, the term "chronic obstructive pulmonary disease" will be used to describe a combination of chronic bronchitis and emphysema, whereas other obstructive lung diseases will be identified with their specific term. Chronic obstructive pulmonary disease and cystic fibrosis are progressive, incurable conditions that incur large health care costs, result in loss of workdays, and eventually will lead to very limited mobility due to increased dyspnea and decreased exercise tolerance. Interventions that may improve and maintain mobility would be valuable to these patients.

Conditions characterized by chronic airflow limitations can result in impaired respiratory muscle function because of respiratory muscle weakness, increased work of breathing due to changes in the lungs, and inefficiency of the inspiratory muscles because of hyperinflation. Respiratory muscle weakness may occur because of systemic abnormalities such as poor nutrition, abnormal arterial blood gases, and disuse. Increased work of breathing results from airway obstruction, which contributes to dynamic airway compression and hyperinflation. Hyperinflation places all of the inspiratory muscles at shorter-than-normal lengths and at a mechanical disadvantage, with the diaphragm being affected to the greatest degree. (See article by Reid and Dechman in this issue for complete explanation, with figures.)

The etiology of poor respiratory muscle function in patients with COPD is not clear. Roussos[2] hypothesized several years ago that the respiratory muscles in individuals with COPD are susceptible to respiratory muscle fatigue. More recently, Rochester[3] postulated that weakness rather than fatigue is present in the respiratory muscles of some groups of patients with COPD. Discerning the difference between weakness and fatigue is often difficult. Regardless of whether weakness or fatigue is present, poor inspiratory muscle function is an important factor contributing to exertional dyspnea, exercise intolerance,[4] and, as diseases progress, to hypercapnic ventilatory failure in patients with COPD.[2,3] Respiratory muscles, similar to limb muscles, improve their function in response to training. This improved function, in turn, could potentially decrease dyspnea, improve exercise tolerance, and increase the ability to do daily activities, and may reverse hypercapnic ventilatory failure.

During the last 15 years, a plethora of studies have been performed examining the benefit of respiratory muscle training in patients with COPD. As with all clinical studies, difficulties were encountered, and often the clinical design and the training techniques were not optimal. These factors resulted in controversial results. More recently, however, improved training techniques have consistently demonstrated positive outcomes from respiratory muscle training in several different conditions involving airway obstruction.

This article will describe different respiratory muscle training techniques and the effectiveness of respiratory muscle training in patients with chronic airflow limitation. Finally, some recommendations will be given regarding the techniques to use for respiratory muscle training and which patient populations may benefit from these techniques.

Training Principles

The principle of specificity of training states that the effects of training are very specific to the neural and muscular elements overloaded. According to tits principle, respiratory muscle training will improve respiratory muscle function during day-to-day activities when the type of recruitment pattern during training is most similar to the recruitment pattern required during those activities. Of greater importance, respiratory muscle training will only be of benefit to the patient if respiratory muscle function is a major limiting factor during the performance of activities. The overload principle states that an overload must be applied to a muscle for a traffic response to occur. This overload may be applied by increasing the frequency of training, the duration of training, the intensity of the loading, or a combination of these factors. Many studies examining the benefit of respiratory muscle training have probably been unsuccessful because an inadequate overload was applied as a result of the type of training device used. Reversibility implies that the effects of training are transient. As soon as the individual stops training, the structural and functional changes within the body related to training will begin to return to baseline. The principle of individual differences states that all individuals are different, so their needs and abilities should be considered before designing an exercise program. We currently have no criteria to select which individuals may benefit most from respiratory muscle training.

Respiratory Muscle Strength

Training

Force production of the respiratory muscles can be improved through specific strength training in young asymptomatic individuals,[6] in elderly individuals,[7] and in those with COPD.[7] Inspiratory muscle force also improves in response to some inspiratory muscle endurance training protocols.[8-16] Respiratory muscle strength training can be defined as the performance of high, near-maximal inspiratory or expiratory maneuvers that are usually quasi-isometric.[6,7] The repetition rate is low (range=5[6]-20[7] repetitions). The primary goal of strength training is to improve force production of the respiratory muscles. Respiratory muscle strength training is probably not important clinically except in cases of neuromuscular weakness.[17] In these conditions, training of the expiratory muscles may be very important for the production of an effective cough.

Respiratory Muscle Endurance

Training

Because the main function of the respiratory muscles is to perform low-intensity contractions about 10 to 20 times per minute throughout the life span, endurance training of the inspiratory muscles is much more important than strength training for individuals with COPD. In addition, endurance is decreased more than force production in patients with COPD compared with normal values.[18] Respiratory muscle endurance training can be defined as repetitive, shortening contractions that are in coordination with die breathing pattern. The duration is usually at least 15 minutes, and the endurance training may consist of a continuous or multiple-interval training period.

Three major types of respiratory muscle endurance training techniques have been developed: maximum sustained voluntary ventilation (MSVV),[6] inspiratory resistive breathing,[8] and threshold loading.[10] The advantages and disadvantages of each of these techniques will be outlined. In addition, the outcomes from each type of training in individuals with chronic airflow limitation will be discussed.

Maximum Sustained Voluntary

Ventilation

Maximum sustained voluntary ventilation, the least practical traffic technique, requires the individual to hyperventilate for 15 to 25 minutes. Because the person is hyperventilating, which decreases the partial pressure of carbon dioxide (arterial) level, equipment is necessary to maintain arterial blood gases within a physiologic range. An elaborate apparatus is used that consists of (1) equipment to monitor and adjust inspiratory oxygen and carbon dioxide levels, (2) a target such that the person can pace himself or herself at a defined minute ventilation, and (3) a measuring component to determine the amount ventilated. The combined cost of this equipment is likely in excess of $50,000 (Canadian), so MSVV is not a useful technique for large numbers of patients, and is not convenient as a home training technique. Home use of an MSW training apparatus, however, has been reported.[19] Although this training technique requires costly equipment, rendering it less practical than other training techniques, it is likely the best technique for purely improving endurance at high speeds of muscle contraction.

Maximum sustained voluntary ventilation training has been used in several studies of asymptomatic individuals,[6,20] those with cystic fibrosis,[20] those with COPD,[19,21,22] and those with COPD in respiratory failure[23] (Tab. 1). In these studies, the duration of training was usually 15 to 30 minutes per session, the frequency of training ranged from three to six times a week, and the time course of training was between 4 and 6 weeks. Several reports[6,20-22] showed an increase in the maximum sustained ventilatory capacity, although only nonsignificant trends toward improvement were shown in two studies.[19,23] Maximum sustained voluntary ventilation training increased exercise tolerance in patients with COPD in uncontrolled2l and controlled[19] studies, and showed a similar increase as an intermittent positive pressure breathing treatment group in another report.[22] Other researchers did not measure the effect of MSW training on exercise tolerance[6,23] or only estimated maximal oxygen consumption from submaximal exercise.[20,24] Maximum sustained voluntary ventilation training appears to improve inspiratory muscle endurance; however, the benefit of this technique on exercise tolerance is less clear. Further, the complexity of the training apparatus hinders the widespread use of MSVV as a home training technique.

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Inspiratory Resistance Training

Inspiratory resistance training is probably the most popular respiratory muscle training technique used to date. One inspiratory resistance trainer(*) consists of a mouthpiece attached to a T-piece with a one-way valve on one side and a nonlinear inspiratory resistance attached to the other side. A nonlinear resistance changes in intensity when flow rate is altered.[25] During inspiration, the one-way valve closes, so the person must breath against the nonlinear resistance, which is a colored disk with a small hole in the center. During expiration, the one valve opens, so expiration is unimpeded. The disks can be changed and vary in diameter from 2.0 to 7.1 mm. The P-flex[dagger] is another inspiratory resistance device, but rather than changing the disks in order to adjust hole size, dial can be adjusted to a larger or smaller hole (range in diameter=1.5-5.1 mm).

(*) Available from DHD Medical Products Diemolding Healthcare Division, Canastota, NY 13032. [dagger] Available from HealthScan Products Inc, Unit B-2, 908 Pompton Ave, Cedar Grove, NJ 07009-1292.

In several studies, the benefits of IRT have been examined in individuals with COPD[26-36] and those with cystic fibrosis[8] (Tab. 2). For the most part, the duration of training was 30 minutes (range = 15-50 min), the frequency of training was either five times per week or daily, and the time course of training sessions ranged from 4 weeks to 6 months.

Success from IRT in individuals with COPD has been variable. In many of the studies, there were no control groups[26,29,34] or functional indexes such as exercise tolerance or functional abilities were not used.[27,32] Not all the studies demonstrated an improved respiratory muscle endurance results obtained in a similar group of patients when an uncoached breathing pattern using the inspiratory resistance device had no effect.

The problem with the inspiratory resistance devices is that the resistance is nonlinear. If the person breathes in slowly, only a small effort is required to create a low pressure to produce flow, whereas if the person breathes in more quickly, a larger effort is required to produce the larger pressure to achieve the higher flow rate[25] (Figure). The lack of beneficial effects in some studies may have been due to patients changing their breathing patterns in order to make the load easier rather than working against the inspiratory resistance.[27,32] Further, the demonstration of an increase in the maximal inspiratory resistance (MIR) sustained during testing in some studies (Tab. 2) may have been due to an altered breathing pattern rather than improved inspiratory muscle endurance. Therefore, the breathing pattern and flow rate must be monitored carefully and controlled throughout every testing and training session when using inspiratory resistance devices.

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Inspiratory Resistance Training

Using Targeted Techniques

Recently, efforts have been made to control breathing patterns during IRT by using targeted techniques. The targeted device used by Dekhuijzen et al[13] is probably the simplest and most practical to use. They attached an inspiratory resistance to an incentive spirometer. The physical therapist modified the flow adjustment on the incentive spirometer such that patients had to exert 70% of their maximal inspiratory pressure (MIP) to keep the ball at the top of the incentive spirometer during training. The device used by Harver et al[11] was a modified P-flex device with a latex sleeve between the mouthpiece and the inspiratory resistance. The sleeve was connected to a needle, and subjects had to inspire with sufficient force to deflect the needle a significant amount. The feedback device used by Belman and Shadmehr[9,37] appears to be the most complex compared with other targeted devices, but these investigators demonstrated that patients were able to learn how to use the device. The inspiratory resistance breather was attached to a little box. On the box, a green light went on and off in order to time inspiration and expiration, respectively. The patient was instructed to breath in during the time that the green light was on. A scale at the top of the device gave an indication of the magnitude of pressure generated, and a red light went on when the maximum pressure was generated.

Recent studies using IRT with targeted devices have consistently shown positive results (Tab. 3) in contrast to the inconsistent benefits shown with the use of a nonlinear resistance trainer alone (Tab. 2). In addition, the experimental design of all three studies included another treatment for the control group, either low-intensity training[9,11] or pulmonary rehabilitation.[13] All three studies showed improvement in indexes of respiratory muscle force (MIP) or endurance (reduced electromyographic signs of diaphragm fatigue,[13] higher training pressures,[9,11] or higher maximum sustained ventilatory capacity[9]). In addition, greater improvement in exercise tolerance[9,13] and less dyspnea[11] were shown than in the other treatment group. From the data presented in Tables 2 and 3, it would appear that the use of a targeted device is essential to optimize benefits from IRT.

Threshold Loading

Threshold loading is probably the most practical approach to inspiratory muscle training to date. This technique uses an apparatus that consists of a mouthpiece connected to a one- or two-way valve, which in turn is attached to some sort of inspiratory threshold loading device. The subject breathes in against the threshold load (usually a weighted plunger or spring-loaded valve) and breathes out unimpeded. Earlier versions of the training device consisted of a weighted plunger for the threshold load,[12,38] but a one-way spring-loaded valve has recently been developed.[10] Using the spring-loaded threshold trainer,[dagger] expiration is unloaded. During inspiration, however, a person has to breathe in hard enough to open the valve against a tightened spring. The inspiratory load is calibrated in centimeters of water and can be increased by removing the mouthpiece and tightening the spring. Greater success is apparently achieved when training at a higher threshold load.[10]

Threshold loading training has been performed in asymptomatic individuals,[12] those with COPD,[10,16,38,39] those with asthma,[15] and those with cystic fibrosis [14] (Tab. 4). All studies demonstrated improved indexes of respiratory muscle endurance (increased endurance time at submaximal threshold load or increased submaximal threshold load sustained for a determined time),[10,12,15,16,38] except for one study that did not measure endurance.[14] Exercise tolerance was shown to improve in several studies,[10,14-16,38,39] although it was not measured in one Study.[12] The improvement in exercise tolerance in response to threshold training is a critical finding. Earlier reports examining the effects of IRT and MSVV did not consistently show an impact on exercise tolerance, compared with the exercise tolerance shown by a control group or another treatment group.

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Threshold training has also been demonstrated to benefit other groups of patients not usually considered in respiratory muscle training studies. Weiner et al[15] found that this type of respiratory muscle training improved inspiratory muscle force and endurance and decreased symptoms irk patients with asthma. Threshold training prevented the loss of respiratory muscle force and endurance associated with high-dose steroids in patients with autoimmune diseases in one study.[40] Patients with COPD or patients with asthma receiving high-dose steroids, even delivered over repeated short courses, may be susceptible to steroid myopathy of the respiratory muscles.[41] Threshold training may prevent loss of respiratory muscle function and promote improvement during and following steroid administration in individuals with chronic respiratory disease.

Respiratory Muscle Training as

an Adjunct to Weaning

Respiratory muscle endurance training may also be used as an adjunct to assist weaning patients from a mechanical ventilator. Investigations have used IRT and MSVV to train individuals on mechanical ventilators. A few poorly controlled studies with small numbers of patients have demonstrated positive results[23,42,43] (Tab. 5). Aldrich et al[44] (Tab. 5) examined a larger number of patients in a chronic care institution who were more stable but who were still unable to wean. After 10 to 46 days, most of the patients were either weaned totally or to nocturnal ventilation.[44]

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Respiratory muscle training may better prepare the inspiratory muscles for the work of spontaneous breathing than traditional weaning techniques for a couple of reasons. Similar to what occurs in limb muscles, a higher-intensity training load may recruit a larger pool of muscle fibers and, hence, a larger pool of fibers are trained for subsequent lower, but potentially fatiguing, loads.[45] A training load may also facilitate intracellular changes in the diaphragm characteristic of endurance training such as increased mitochondrial density, increased substrate stores of lipid and glycogen, and increased capillary density.[5]

Respiratory muscle training may facilitate weaning in those patients who fail conventional T-piece weaning, but a better understanding of the specific etiology of respiratory muscle dysfunction contributing to failed weaning is needed. Unfortunately, there are no criteria for selecting those patients who are best suited for respiratory muscle training and which training protocol to use. If the overload is too severe, there is the potential for respiratory muscle injury to occur. Respiratory muscle injury has been shown in both animal models of respiratory overload[46,47] and in people with COPD.[48,49]

Endurance Exercise Involving

the Extremities

Some researchers have examined the benefit of endurance exercise involving the extremities such as running, swimming, or cycle ergometry on respiratory muscle endurance (Tab. 6). These types of exercise were effective techniques of training for the respiratory muscles in younger asymptomatic individuals[50] and those with cystic fibrosis,[20,51] but they were ineffective in two studies on older patients with COPD[19,52] (Tab. 6). At least in older patients with COPD, specific respiratory muscle training is required to improve respiratory muscle endurance.

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The benefits of exercise on other body systems (Tab. 7)[53] should be considered when weighing the relative benefit of endurance exercise involving the extremities versus respiratory muscle training in patients with chronic respiratory disease. Most studies demonstrate an increased maximal work load following a general exercise program in patients with COPD[53] and those with cystic fibrosis.[51,54-57] Several researchers have shown improved maximal oxygen consumption in patients with COPD[53] and those with cystic fibrosis.[51,54,55,57] In addition, several other effects have been shown (Tab. 7),[53] one of the most important being the facilitation of sputum expectoration in patients with cystic fibrosis.[54,58] For the time spent training, it may be of greater benefit to patients to perform endurance exercise involving the extremities rather than specific inspiratory muscle training in spite of the lack of benefit to the respiratory muscles from a general exercise training program in older patients with COPD.

Table 7. Effects of Endurance Exercise Involving the Extremities on Chronic Obstructive Pulmonary [Disease.sup.a]

Type of
Exercise           Effect

Cardiovascular    Increased [VO.sub.2] max
Respiratory       Increased tolerance of
                  dyspnea
                  Decrease in minute
                  ventilation at similar work
                  loads
                  Increased mucociliary
                  clearance
Skeletal muscle   Improved oxygen extraction
Maximal work      Increased
load

                  Improved efficiency - lower
                  HR, [VO.sub.2], or increased
                  anaerobic threshold
Psychological     Increased sense of
                  well-being
Activities of     Improved
daily living

(a)Modified from Reid and Pardy.[53] See this reference for complete citation of references supporting factors shown. HR = heart rate, [VO.sub.2] = oxygen consumption, [VO.sub.2]max = maximal oxygen consumption.

A Practical Guide for

Respiratory Muscle Training

Although many of the specific details have not been worked out regarding the optimal respiratory muscle training program, there are a few guidelines that can be given to the physical therapist who wants to implement this type of training. Many patients with chronic respiratory disease may benefit from inspiratory muscle training (Tab. 8); however, it is still not known in which subgroups of patients arc optimal benefits achieved. Because many other aspects of respiratory rehabilitation such as a general exercise training program have more widespread benefits,[53] it would appear that inspiratory muscle training should be recommended to more motivated patients who would have time to commit to an endurance exercise program involving the extremities and an inspiratory muscle training program. An exception to this general guideline might be individuals who are at high-risk for an endurance exercise program involving the extremities, such as those with significant cardiovascular disease. For example, we received a referral for a 65-year-old man with a long-standing history of COPD combined with a more recent history of a 3-month stay in intensive care following coronary artery bypass surgery. This patient was discharged home to a rural community but continued to complain of extreme dyspnea on exertion. Because he was experiencing some cardiac arrhythmias, an unsupervised exercise program was not instituted, but instead he began threshold inspiratory muscle training. Respiratory muscle training decreased complaints of dyspnea and improved patient-reported exercise tolerance. In such an individual with a high cardiovascular risk, inspiratory muscle training may reduce dyspnea and improve exercise tolerance while imposing much less stress on the cardiovascular system (Reid WD, unpublished data, 1992).

Before beginning any kind of training program including respiratory muscle training, patients should be medically stable and properly managed. Medications should be optimal, and the patient should be using oxygen if prescribed. In addition, the therapist should ensure that nutrition is optimal. Exercising an individual with poor nutrition can result in muscle catabolism(59,60) and loss of function 61 rather than improved performance.

In order to determine the benefit of respiratory muscle training, the patient should be evaluated before and after a 6- to 8-week course of training. This evaluation should include an inspiratory muscle endurance test, an exercise tolerance test such as a 12-minute walk test or treadmill test, a measure of dyspnea,62,63 and a measure of functional activities.(,4,65 The minimum equipment required would include a respiratory muscle trainer, oximeter, stopwatch, blood pressure cuff, and electrocardiographic monitor (the latter two items would be required for the walk or treadmill test). More sophisticated respiratory muscle testing systems are described elsewhere (see article by Clanton and Diaz in this issue).

The most practical, effective training device appears to be the threshold trainer.[10] Although the optimal training program has not been determined, most studies have used a training duration of between 15 and 30 minutes. From what is known about endurance training of climb muscles, the frequency of training should probably be no fewer than three times per week.[5] If prescribing higher frequencies of training, it might be of benefit to have patients take the weekend off to give them some variety m activities and to maximize recovery from training. Training intensity should be at an inspiratory pressure equal to or greater than 30% of the MT.[9,10,13-16] Recent reports have described successful outcomes at much higher training intensities of about 60% to 70% of the MIP for a 10-week[13] or 4-month[16] training period or up to 800/o of the MIP during the last 2 months of a 6-Month training period.[15,16] Training at higher intensities, however, increases the risk of respiratory muscle fatigue and even respiratory muscle injury. Progression of training should be slow, and allowances should be made for any exacerbation of disease or social event so that training may be resumed at a lower level following any prolonged lapse in training.

Conclusion

Inspiratory muscle training is of benefit for some patient groups. The mechanism of respiratory muscle fatigue is poorly understood, and it is difficult to discern the difference between weak and fatigued respiratory muscles. It is therefore very difficult in some cases, such as weaning from a mechanical ventilator, to decide when to rest or train the respiratory muscles. The best protocols of respiratory muscle training are yet to be defined. Although many training studies have been performed, the optimal intensity, contraction speed, repetition rate, and frequency still need to be determined. Further, the specific subgroups that may benefit from these techniques need to be determined. Recent studies using targeted inspiratory resistive and threshold training in patients with COPD seem to indicate that this technique is helpful in addition to pulmonary rehabilitation. In patients with COPD, an endurance exercise program involving the extremities should be the first treatment of choice, and, in special circumstances, inspiratory muscle training may have an added benefit. Other patient groups such as those with steroid-induced myopathy, cystic fibrosis, or asthma may also benefit from inspiratory muscle training.

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