This article presents a brief overview of respiratory muscle mechanics and the ... effects of muscle training on cardiopulmonary function, muscle strength, endur-.
Respiratory Muscle Function, Assessment, and Training THOMAS H. SHAFFER, PhD, MARLA R. WOLFSON, BS, and VINOD K. BHUTANI, MD
This article presents a brief overview of respiratory muscle mechanics and the effects of lung disease and neuromuscular disease on pulmonary function. A variety of current specific and general muscle training techniques are described and discussed. Also presented is a current review of training studies and the effects of muscle training on cardiopulmonary function, muscle strength, endurance and fatigue, and exercise tolerance. Key Words: Respiratory muscles, Respiratory disease, Neuromuscular disease, Pulmonary rehabilitation.
Exercise training programs have long been considered an integral component in rehabilitation of patients with pulmonary dysfunction.1 The efficacy of such health care programs on lung disease and neuromuscular disease has been studied in patients of various ages and with associated disabilities. Patient education, chest physical therapy, occupational therapy, and medical services have been incorporated in multidisciplinary programs in an attempt to maximize individual patient recovery. Among the many therapeutic procedures provided, exercise training is one of the most difficult to deliver and evaluate because of equipment and personnel logistics (for a predominantly outpatient population) and variable baseline ventilatory conditions. The purposes of this article are to provide a brief overview of respiratory muscle mechanics and the effects of lung disease and neuromuscular disease on pulmonary function; to describe and discuss current specific and general muscle training techniques; and to present a current review of training studies and the effects of muscle training on cardiopulmonary function, muscle strength, endurance and fatigue, and exercise tolerance. RESPIRATORY MECHANICS AND MUSCLE FUNCTION The mechanics of respiration concerns respiratory muscle forces required to overcome the elastic recoil Dr. Shaffer is Associate Professor of Physiology, Temple University School of Medicine, Department of Physiology, 3420 N Broad St, Philadelphia, PA 19140 (USA). Ms. Wolfson is a physical therapist and a graduate student, Temple University School of Medicine, Department of Physiology. Dr. Bhutani is Research Assistant Professor of Physiology, Temple University School of Medicine, Department of Physiology. The research leading to this paper was supported in part by Public Health Service Grant HL-22843.
Volume 61 / Number 12, December 1981
of the lungs and thorax as well as a functional resistance to airflow through hundreds of thousands of conducting pathways. The energy for ventilating the lungs is supplied by active contraction of the respiratory muscles. During quiet breathing, the primary muscles responsible for ventilation are the diaphragm and the external intercostal muscles. Although the diaphragm is not essential for breathing it is the principal muscle of inspiration. The diaphragm's contribution to tidal volume has been estimated to be two-thirds in the sitting and standing positions and three-fourths in the supine position.2 Expiration is a passive process during quiet breathing and occurs because of the elasticity of the lung and chest wall. As breathing becomes more vigorous, such as in exercise or respiratory disease, expiration is no longer a passive function. The internal intercostal and rectus abdominus muscles contract to increase intrapleural pressure during expiration. Normally the abdominal muscles are regarded as expiratory muscles; however, Grimby and associates have demonstrated their role in certain inspiratory maneuvers.3 In addition, other accessory muscles come into play during vigorous breathing including the sternocleidomastoid and scalene muscles in the neck, the muscles of the shoulder region, and the pectoral muscles.
Morphology and Properties The respiratory muscles are striated and microscopically classified into two muscle fiber groups. In general, fast muscle fibers are white and slow muscle fibers are red. The description of skeletal muscle fibers as slow-twitch or fast-twitch is a relative designation only applicable within a single species. For
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TABLE 1 Properties of Muscle Fibersa Microscopic
Histochemical
Contractile Properties
Red
High myoglobin content Rich in sarcoplasm Many mitochrondria
High oxidative activity Low phosphorylase
Slow
White
Lower myoglobin content Less sarcoplasm Fewer mitochrondria
Low oxidative activity High phosphorylase
Fast
Naked Eye
a
Modified from Campbell.2
example, muscles of smaller animals are usually faster than similar muscles of larger animals.2 Table 1 shows a simplified classification of muscle fiber properties, although precise correlation of microscopic, histochemical, and contractile characteristics has not been established. Recent studies of the histochemical properties of muscle fibers have demonstrated that the oxidative capacity of the ventilatory muscles increases markedly from midgestation to early childhood.4 Premature infants have less than 10 percent high oxidative, slow-twitch fibers in the diaphragm as compared to 55 percent found in the adult diaphragm. It has been suggested that the ventilatory muscles of newborns are more susceptible to fatigue than those of older subjects and may contribute to the respiratory problems of preterm neonates. 5
Electromyogram and Respiratory Muscle Function Although the EMG presents an exceedingly complicated signal of motor unit behavior during muscle contractions, the use of it has been recognized as a valuable predictor of muscle activity, timing, and fatigue.6 As shown in Figure 1, EMG activity of individual respiratory muscles can be associated with specific respiratory maneuvers and body positioning. Diaphragmatic (esophageal) and intercostal muscle EMG activity are only observable during inspiration as indicated by inspiratory flow and chest wall and abdominal displacement. Inasmuch as expiration is passive, there is no expiratory muscle EMG activity present. More recently, investigators have studied frequency analysis of respiratory muscle EMG activity.7 Of the available frequency domain methods, power density spectral analysis provides the most quantitative technique for expressing the power in a myoelectric signal as a function of its frequency components. Using esophageal electrodes, several studies have shown that the diaphragmatic EMG spectrum is concentrated in the band width 25 to 250 Hz and that electrode motion artifact was only significant at low frequencies.7 RESPIRATORY MUSCLE FUNCTION IN DISEASE
One of the major problems associated with clinical management of patients with either respiratory or neuromuscular diseases is the maintenance of adequate alveolar ventilation. In patients with lung disease (Tab. 2), respiratory muscle strength (even if normal or stronger) is insufficient for overcoming increased respiratory loads. In patients with severe Fig. 1. Effect of body position on respiratory muscle neuromuscular diseases, inadequate respiration reEMGs (normal breathing). Esophageal EMG (diaphrag- sults from either muscle weakness or respiratory cenmatic activity); intercostal space (ICS); anterior axillary ter abnormalities. Some of these disorders are outline (AAL); posterior scapular (PS); posterior axillary line (PAL); rib cage displacement (MRC), abdominal displace- lined in Table 3. Although patients can usually be ment (M AB ), and inspiratory flow. (Photo through courtesy classified as having either respiratory or neuromusof Dr. Sanford Levine) cular dysfunction, frequently, mixed problems are 1712
PHYSICAL THERAPY
TABLE 2 Respiratory Diseases Affecting Respiratory Muscle Function in Different Age Groups Disease 1. Obstructive
Adult Asthma Bronchitis Emphysema Aspiration syndrome Bronchiolitis Tumor
II. Restrictive A. Alveolar
Pneumonia Pulmonary edema Adult respiratory disease syndrome B. Interstitial Interstitial fibrosis Connective tissue disorders
C. Vascular
D. Pleural
Child Asthma Meconium aspiration Amniotic fluid aspiration Bronchiolitis Cystic fibrosis Congenital disorders of larynx & trachea Hyaline membrane disease Atelectasis Pneumonia
Broncho-Pulmonary dysplasia Connective tissue disorders Cystic fibrosis Thrombo-Embolic Persistent pulmodisease nary hypertenPulmonary hypersion of newborn tension Pleural effusion Pleural effusion Chylothorax Mesothelioma
of fatigue provide sensitive indicators of respiratory muscle function.
Muscle Strength The performance of the respiratory muscles are dependent on 1) specific respiratory muscle strength and 2) general systemic muscle strength. Respiratory Muscle Strength Respiratory muscle strength has been defined as the maximum and minimum static pressures measured at the mouth and attributable to a sustained muscle effort.8, 9 Both maximum static inspiratory pressure (MSIP) and maximum static expiratory pressure (MSEP) are measured over the range of the vital capacity (Fig. 3). The subject inspires to his total lung capacity (TLC) and then expires at about 20 percent TLC intervals until he reaches his functional residual capacity (FRC). At each interval, a Dubois shutter is activated to occlude airways. Maximum inspiratory and expiratory maneuvers are performed against the closed shutter. The measurements of MSIP and
seen. Figure 2 illustrates the clinical course of both respiratory and neuromuscular disease processes.
EVALUATION AND DIAGNOSIS OF RESPIRATORY MUSCLE PERFORMANCE Muscle performance is best assessed by its strength, endurance, and inherent ability to resist fatigue. Measurements of muscle strength, endurance, and onset TABLE 3 Acute and Chronic Neuromuscular Problems Affecting Respiratory Muscle Function Problem 1. Neuromyopathic
II. Skeletal
Acute
Chronic
Cord transection Guillain-Barré syndrome Botulism Cholinergic poisoning Poliomyelitis Tetanus Diaphragmatic paralysis Congenital diaphragmatic paralysis Crush injury of chest Post-cardiothoracic surgery
Spastic quadriplegia Hemiplegia Cerebral palsy Parkinsonism Multiple sclerosis Spina bifida Myasthenia gravis Muscular dystrophy Diaphragmatic fatigue of prematurity Kyphoscoliosis Ankylosing spondylitis Pectus excavatum
Volume 61 / Number 12, December 1981
Fig. 2. The interrelationship between respiratory muscles and pulmonary function in the pathogenesis of respiratory failure.
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This quality is difficult to assess and little data are available in the literature. General muscle strength is increased with resistive loading, ergometry, and system exercises with or without supplemental oxygen. Improvement is gauged by measuring the oxygen consumption, carbon dioxide levels, and alveolar ventilation. Muscle Endurance Endurance is defined as the capacity of the muscle to resist fatigue and can be applied to 1) the ventilatory muscle groups and 2) the systemic muscle groups. Respiratory Muscle Endurance
Fig. 3. Maximum inspiratory and expiratory pressures a function of lung volumes (modified from Leith and Bradley10). MSEP are correlated to specific thoracic gas volumes.10 These pressures are reduced in the presence of respiratory muscle weakness or fatigue. Hypercapnic respiratory failure has been associated with a respiratory muscle strength of 30 percent or less of the predicted value.6 Systemic Muscle Strength Muscle strength of an individual is measured by muscle power and bulk as well as exercise tolerance.11
Respiratory muscle endurance has been defined and measured as the capacity to sustain high levels ol ventilation under isocapnic conditions.10, 12 Using a as partial rebreathing system, maximal ventilation (a predetermined fraction of maximum voluntary ventilation) is maintained, and the length of time to sustain isocapnia is measured. The endurance may also be measured by breathing against a known resistance.13 Endurance measurements can be standardized to 12 to 15 seconds of maximal voluntary ventilation,10 lung volume, and flow-resistive work.13 The endurance capacity of the ventilatory muscles is dependent on the interaction between the respiratory system impedance and the maximum available muscle power. Thus, the sustained ventilatory capacity is not only indicative of weakness or fatigue of the muscle, but may demonstrate a response to an increased respiratory load. An increased endurance capacity, in the presence of a chronic progressive respiratory disease, demonstrates the ability of the muscles to adapt to the changing functional demands.5 Systemic Muscle Endurance Endurance of systemic muscle groups is measured by the capacity of an individual to perform a specific physical activity at an aerobic level (estimated by the predicted maximal oxygen consumption method). Intensive physical activities that do not involve specific ventilatory muscles include canoeing, rowing, and swimming. Muscle Fatigue
Fig. 4. Factors associated with respiratory muscle fatigue. 1714
A muscle is fatigued when the rate of energy consumption is greater than the rate of energy supplied to the muscle. Depletion of the energy stores within the muscle subsequently leads to its failure as a force generator. The onset of muscle fatigue following a static maneuver determines its strength, and following a sustained effort, its endurance. PHYSICAL THERAPY
Fatigue of the respiratory muscles, both the diaphragm and the intercostal muscles, is an important potential clinical problem because this would be the final common pathway to respiratory failure. The psychological and physiological factors contributing to respiratory muscle fatigue are shown in Figure 4. Muscle fatigue also accounts for exercise intolerance in patients with lung disease and the difficulty in weaning patients off ventilators.
Clinical Evaluation Inspection of the thoracic cage may indicate an out-of-phase and incoordinated chest wall movement in a combined, alternating, diaphragmatic and intercostal breathing pattern. An inward movement of the costal margins (Hoover's sign) is observed in fatiguing patients with chronic obstructive pulmonary disease (COPD). Inward inspiratory motions of the abdomen may often predict severe respiratory failure. Palpation of the chest wall and neck allows evaluation of increased activity of the accessory respiratory muscles. Though these are important clinical signs of an increased respiratory load, these signs are difficult to measure and are not specific or sensitive indications of fatigue.
Fig. 5. Changes in high/low frequency components of EMG activity during diaphragmatic muscle fatigue (modified from Macklem55).
Magnetometry The dimensional changes of the rib cage and abdomen are measured using a magnetometer and are useful for coordinating clinical observations.14 These data are of lung volume displacements rather than of any muscle group activity. The subtle, mechanical signs of fatigue include 1) rapid, shallow respiratory cycles, 2) paradoxical abdominal movements, and 3) alternating between predominantly abdominal movement and rib cage movement during inspiration. However, it would be erroneous to attribute abdominal motion solely to the diaphragm and rib cage motion solely to intercostal muscle activity.
Lung Volume A decrease in TLC and an increase in residual volume (RV) of a patient performing maximal effort is suggestive of respiratory muscle weakness. The values of TLC and RV are governed by two opposing forces—the elastic recoil of the lung and the muscle force. Thus, at TLC the inspiratory muscle forces are most active while at RV the expiratory muscle groups are predominant.
Electromyography Characteristic patterns of electrical activity have been observed on the EMG of a fatiguing skeletal Volume 61 / Number 12. December
1981
muscle. Similar shifts in the power spectrum of the EMG have been observed during diaphragmatic fatigue.15, 16 These observations (Fig. 5) document the onset of fatigue through 1) increased amplitude of low frequency (20-46.7Hz) components, 2) decreased amplitude of high frequency (150-350Hz) components, and 3) decreased ratio of high to low (H:L ratio) frequency components. The H:L ratio is independent of respiratory muscle force and begins to decrease long before the muscle reaches its limit of endurance.17 The other aspects of EMG power spectrum also need to be considered for the evaluation of fatigue. These include 1) the maximum amplitude of the power spectrum, 2) the area under the amplitudefrequency curve, 3) the first movement of inertia, and 4) the centroid frequency. The role of these factors as the best predictor of muscle fatigue needs yet to be evaluated. Diaphragmatic EMG is obtained at sites with minimal or poor intercostal activity during inspiration. These sites are 1) the 10th intercostal space in the midaxillary line by needle electrodes; 2) the 7th, 8th, and 9th intercostal spaces in the midclavicular line by surface electrodes; and 3) esophageal.15
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Similarly, P di max selectively assesses diaphragmatic endurance, and values of over 40 percent have been associated with fatigue (Fig. 6b). TRAINING PROGRAMS Exercise programs take on many forms, but for convenience they can be divided into two groups: general (systemic) and specific (localized training of respiratory muscles). General or systemic training programs include activities using extremity muscles in addition to respiratory musculature with or without supplemental oxygen.21-35 Almost any combination of exercise has been studied: general conditioning, including treadmill and bicycling, breathing exercises, and psychological support; bicycling and treadmill or treadmill alone21, 22, 27, 30, 35, 36; treadmill and breathing exercises; calisthenics-gymnastics-swimming and patient education for children28; jogging for adolescents33; and walking.31,32 These programs have been designed to improve the physiologic factors of pulmonary function, strength, endurance, cardiac function, and exercise tolerance as well as nonphysiologic factors such as cooperation and psychological wellbeing. Alternatively, specific or localized training refers to exercises primarily involving and emphasizing ventilatory muscle groups. Diaphragmatic training37 alone or in conjunction with incentive spirometry1 has been recommended in patients with COPD. In these patients, a flattened, depressed diaphragm was observed Fig. 6. Diagramatic representation of a) transdiaphrag- to have limited respiratory excursions, and consematic pressure (Pdi) expressed as a fraction of maximum quently, minimal contribution to ventilation. Use of inspiratory pressure at FRC (Pdi/Pdi max %) as a function a Gordon-Barach belt and diaphragmatic breathing of time; b) mouth pressure (Pm) as a percentage of with active abdominal contraction during expiration maximum inspiratory pressure at FRC (Pmax) plotted as a function of time (modified from Roussos and associates18). was recommended37,to38cause a cephalic displacement of the diaphragm. As the diaphragm lengthens, the abdominal and inspiratory rib cage musculature shortens. Length tension relationships are optimized Pressures providing increased contraction and pressure change 39 Pressures measured at the mouth (Pm), esophagus for improved diaphragmatic respiration. However, substantial data are scant and of questionable support (Pes), and stomach (Pg) provide an indirect assessment of respiratory muscle function. The mouth pressure of this modality as an independent means to enhance 24 (Pm) generated during ventilation can be fractionated respiration. Pursed lip breathing, the pattern of exhaling through the mouth against the pressure of by P max (the maximum inspiratory mouth pressure generated at FRC). Thus, P m /P m a x expressed as a pursed lips, is used spontaneously by some patients function of duration would be a measurement of and often is taught to other patients as one facet of 40-42 Pursed lip breathing proendurance. Values of less than 60 percent have been breathing retraining. vides relief to some patients from unpleasant sensaassociated with delayed onset of fatigue and indefinite cyclical respiration (Fig. 6a).18 When correlated to tions associated with breathing. EMG, the P m at which the decrease in H:L ratio Ventilatory muscle strength training (VMST) has occurs is defined as a critical pressure (P crit ). Both P crit been shown to increase isometric pressures generated and P max may be used to measure endurance. by inspiratory and expiratory muscles.10 For example, Transdiaphragmatic pressure (Pdi), a differential of MSIP and MSEP are performed on the spirometer against the Dubois shutter at 20 percent intervals over Pg and Pes, can be fractionated by P di max (obtained either conventionally by performing expulsive ma- the range of vital capacity. Each maneuver is susneuvers,19 or by the maximal Mueller maneuver 20 ). tained for three to five seconds and the performance 1716
PHYSICAL THERAPY
TABLE 4 Training Effects on Static Pulmonary Function Training Group General
Specific
Study Group 30
Patients a
Paez Degre 26 Heimlich28
E COPD A
Woolf34 linger 32 Casciari 24 Sinclair31 Chester 25 Alpert21 Bass 22 Rothman 47 Gross 1 3
COPD COPD COPD CB COPD COPD COPD
Sharp 52
COPD
CP QUAD
Training Program b T B, BE GE, G, E, BE, P T W T, BE W T B B CTA VMET IFRL FL
Pulmonary Functionc Response d VC
FRC
0 0 +
TLC
RV/TLC
0
0
IC
P max
P crit
+
+
0 0
0 0 0 0 0
RV
0
0 0 0 0
0 0
0
+ +
+
+
+
+
a
Patients: A—asthma; CAO—chronic airway obstruction; CB—chronic bronchitis; COPD—chronic obstructive pulmonary disease; CF—cystic fibrosis; CP—cerebral palsy; CPT—chest physical therapy; E—emphysema QUAD—quadriplegia. b Program: B—bicycling; BE—breathing exercises; C—canoeing; CTA—collaborative therapeutic approach; E— education; FL—forward leaning; G—gymnastics; GE—general exercise; IFRL—inspiratory flow resistive load; P— psychological support; PLB—pursed lip breathing; S—swimming; T—treadmill; VMET—ventilatory muscle endurance training; W—walking. c Function: VC—vital capacity; FRC—functional residual capacity; RV—residual volume; TLC—total lung capacity; IC—inspiratory capacity; Pmax—maximum inspiratory mouth pressure; Pcrit—critical pressure. d Response: + = increase; - = decrease; 0 = no significant change.
is repeated so that the exercise lasts one-half hour a day. Ventilatory muscle endurance training (VMET) results in the capacity for sustaining higher levels of ventilation for relatively long periods of time (such as 15 minutes). Leith and Bradley describe VMET as sustained ventilation achieved three to five times until exhaustion that is interspersed with recovery intervals (duration unspecified).10 Each episode lasts 12 to 15 minutes; the duration of the session is 45 to 60 minutes, 5 days a week. Normocapnic hyperpnea is achieved with a partial rebreathing system. Use of the bag allows a visual biofeedback to the patient, and the CO 2 scrubber is adjusted to maintain a normal end tidal CO2.10 Both VMST and VMET are current approaches in exercise programs for pulmonary rehabilitation and have been investigated by Leith and Bradley in 1976,10 Keens and associates in 1977,43 and Belman and Mittman in 1980.44 Other unique collaborative therapeutic approaches to training may be required when respiratory problems are caused by or complicated by nonrespiratory disabilities. For example, children with cerebral palsy are extremely vulnerable to respiratory disease because of shallow, irregular respirations and reduced tussive effort.45 While respiratory functions are impaired in these children, concomitant decreased efficiency and poor coordination of the breathing mechanisms further jeopardize ventilatory capacity. In adVolume 61 / Number 12, December 1981
dition, impaired neuromotor control is often coupled with reduced physical activity, which is another respiratory disease risk factor. PHYSIOLOGICAL RESPONSES TO RESPIRATORY MUSCLE TRAINING PROGRAMS Effect of Training Programs on Pulmonary Function Pulmonary function response to a general training program for patients with COPD was reviewed in the literature. No significant change was seen in most pulmonary function variables.21, 24-29, 34 Decreased respiratory rate with a deeper breathing pattern was noted by Woolf,34 Unger and associates,32 and Moser and colleagues.36 Woolf suggested that a more efficient breathing pattern resulted,34 while Paez and colleagues described a task-specific improvement in ventilation.30 Sinclair and Ingram found an increase in forced vital capacity (FVC) that may have reflected reduction in air trapping.31 Bass and associates noted an intrasubject ventilatory equivalent change for oxygen (VEo2) from maximal oxygen consumption and minute ventilation; however, the change was not significant for the group.22 This finding was thought not to be a direct result of exercise training but rather an indication of ventilatory and perfusion abnormalities
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TABLE 5 Training Effects on Dynamic Pulmonary Function Study Group
General
Keens 5 Degre 26 Heimlich28
CF COPD A
Woolf34 linger 32 Casciari 24 Sinclair31 Chester 25 Alpert21 Bass 2 2 Keens 4 Sharp 5 2 Belman 44 Mueller42
Specific
Patients a
Training Program a
Pulmonary Function b Response a MSCV 0
COPD COPD COPD CB COPD COPD COPD
S, C B, BE GE, G, E, BE,P T W T, BE W T B B
CF COPD COPD CAO
VMET FL VMET PLB
0
FVC
FEV1
MVV
0 0
0
+
+
0
0
-
0
0
0 0
0
0 0 0 0
0
+
0
DLCO
MEFR
0
++
Training Group
0 0
0
0
0
+ 0
a
See Table 4 footnotes. b Function: MSVC—maximum sustainable ventilatory capacity; FVC—forced vital capacity; FEVi—forced expiratory volume in 1 second; MVV—maximum voluntary ventilation; DLC0—diffusion capacity for carbon monoxide; MEFR— maximum expiratory flow rate.
or cardiac dysfunction. Inspiratory capacity and maximal voluntary ventilation also improved. Alpert and associates reported high specific and static compliance values before training respiratory muscles.21 These values decreased (although not significantly) toward normal after training. Woolf and Suero reported a trend toward improved dynamic compliance and reduced respiratory work as a result of the training.35 Less information was available about the effects of specific training programs on pulmonary functions (Tabs. 4 and 5). Conflicting information was reported: Keens and associates43 and Merrick and Axen46 found no significant improvement in lung volumes after training respiratory muscles, while Leith and Bradley,10 Rothman,47 and Belman44 noted improvement in both lung volumes and maneuvers. Sharp and associates suggest that postural compensation—forward leaning upon respiratory stress—compresses the
abdomen, which stretches the diaphragm upward, thereby increasing the capacity to generate tension. Shannon suggests that costovertebral joint mobilization stimulates joint mechanoreceptors, which work through the medullary-pontine "rhythm generator" to influence the respiratory pattern.48 Effect of Training Programs on Cardiac Function
Physical exercise programs improve certain hemodynamic and cardiovascular functions in normal persons49 and patients with COPD (Tabs. 6 and 7).
21, 22, 25, 26, 30, 32, 35, 3 6
O x y g e n consumption (Vo 2 ) and
maximal oxygen consumption (Vo2max) are used to evaluate the effectiveness and intensity of training because they reflect a change in cardiac output and oxygen extraction (A-Vo2) by the tissues.
TABLE 6 Training Effects on Arterial Blood Chemistry Training Group General
Specific
Study Group 21
Alpert Bradley 23 Chester 25 Degre 26 Paez 3 0 Woolf35 Belman 44 Mueller42
Patients a COPD COPD COPD COPD E COPD COPD CAO
Training Program a B T T B, BE T T VMET PLB
Blood Chemistry b Response a Po 2
Pco 2
0 + 0 0
0 + 0 0 0
pH
A-ao 2
A-Vo2
Lactate
— 0 0 0
+ +
-
+
+
-
0
a b
See Table 4 footnotes. Chemistry: Po2—oxygen tension; Pco2—carbon dioxide tension; A-ao2—alveolar-arterial oxygen difference; AVo2—arterial-venous oxygen difference.
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PHYSICAL THERAPY
TABLE 7 Training Effects on Cardiopulmonary Function Training Group General
Specific
Study
Training Programa
Group
Patients a
Alpert21 Hale 27 Bass 2 2 Moser 36
COPD COPD COPD COPD
Bradley 23 Casciari 24 Sinclair31 Chester 25 Degre 26 Paez 3 0 linger 32 Woolf35
COPD COPD CB COPD COPD E COPD COPD
B T B T, CPT, P, E T T, BE W T B, BE T W T
Belman 44 Mueller42
COPD CAD
VMET PLB
Cardiopulmonary Functionb Responsea VO2
VO2max
sv
HR
CO
_
0
RR 0
_
+ —
0 0
-
0 0 0 0 0
0 0
-—
_
+
+
0
-
-
a
See Table 4 footnotes. b Function: Vo2—oxygen consumption; Vo2max—maximal oxygen consumption; SV—stroke volume; HR—heart rate CO—cardiac output; RR—respiratory rate.
Measures of Vo 2 increase linearly with escalating workloads and become stable with maximal work (Vo2max).11 After this point, the oxygen needs of the muscle are not met by the cardiovascular-respiratory system, and energy for increased work is derived from carbohydrate metabolism. Accumulation of lactic acid results.11 An objective indication of a training effect, therefore, is an increased Vo2max and a linear increase in work capacity. Scheuer and Tipton suggest that a higher Vo2max implies increased O2 use by peripheral musculature at maximal loads with associated A-Vo 2 difference increments and exercise blood lactate level decrements.49 The rate of Vo 2 at each level of exercise is not physiologically altered by mild training once the exercise is learned; whereas, Vo2max increases because maximal exercise performance is increased.49 Three notable studies showed a decrease in Vo 2 in patients with COPD. Unger and associates reported the greater the initial exercise load (higher Vo2), the greater the decrease in Vo 2 at a given exercise level after training.32 They suggest this relationship emphasizes the importance of beginning exercise at the highest safe level. Alpert and associates21 and Paez and associates30 also noted a decrease in Vo 2 after training, and both groups relate this decrease to improved coordination and exercise efficiency. Degre and colleagues demonstrated an improvement in Vo2max26 most probably related to more efficient oxygen extraction capacity of the muscles.49 Paez and associates also noted an increase in A-Vo2 values.30 Possible causes are elevated myoglobin concentrations and increased number of capillaries in each skeletal muscle fiber. Both factors are closely tied to oxygen diffusion and delivery as well as to redistribution of blood flow to skeletal muscles.49 Volume 61 / Number 12, December 1981
General physical training programs are known to produce slower heart rates regardless of the exercise employed. The reasons for this are unclear; however, it has been suggested that general muscle training may alter autonomic control, levels of circulating catecholamines, stroke volume, or the integrating ability of the CNS.49 After general muscle training, some studies showed that patients with COPD had a decreased heart rate,21, 22, 30, 32, 36 while other studies found no significant change in heart rate.24-26 Chester and associates relate this to the low level of peripheral activity caused by the high oxygen cost of breathing for patients with COPD.25 They suggest that severely disabled pulmonary patients may be unable to reach the level of activity needed to induce a training effect on the heart rate. Stroke volume increases are also found to be a result of general training. These increases are related to increased ventricular volume or bradycardia.49 However, increased stroke volumes were not demonstrated in the COPD general training programs.25'26 Chester and colleagues suggest that this may also be because of the inability of the individual with COPD to perform conditioning level activities.25 Cardiac output changes are often proportional to changes in Vo2. Maximal cardiac output, as well as Vo2max, increases in response to training. However, if the cardiac output does not increase significantly, as may be seen with coronary artery disease, enhanced oxygen extraction becomes the major factor in oxygen delivery.49 Paez and associates noted decreased cardiac output and increased A-Vo 2 and concluded that increased work tolerance was secondary to improved oxygen extraction by exercising muscles.30 Other studies found no significant improvement between cardiac output values before or after training.21, 25
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Several COPD exercise studies noted that arterial blood gases did not improve after training, implying that training does not affect gas transport.21, 25, 26, 30 Woolf and Suero, however, reported smaller alveolararterial oxygen gradients and improved venous admixtures, implying improved ventilation-perfusion relationships as well.35 Oxygen-assisted exercise produced increased arterial oxygen (Po2) and carbon dioxide (Pco 2 ) values without a change in pH. Bradley further suggests the pH stability was because oxygen ameliorated the lactic acidosis of exercise.23 Woolf and Suero also noted a decrease in exercise blood lactate levels.35 They suggest that training produced a more efficient capillary blood supply for bringing additional oxygen to the muscle and thereby reducing anaerobic metabolism. As seen in Tables 4 to 7, there are few recorded measurements of blood chemistry and cardiopulmonary function values for specific exercise programs. Keens and colleagues reported unchanged aerobic capacities.43 Belman and Mittman described increased Vo 2 associated with the higher exercise levels attained; increased blood lactate after exercise associated with recruitment of low oxidative, high glycolytic, fast-twitch muscle fibers at higher levels of exercise; and increased maximum exercise heart rate.44
Effects on Respiratory Muscle Strength, Endurance, and Exercise Tolerance The training response of respiratory muscle is similar to that of skeletal muscle. Muscles respond differently to exercises oriented to improving strength as compared to improving endurance. One striking difference is that strengthening exercises produce mostly a hypertrophy of muscle fibers whereas endurance exercises increase the vascularity of muscle fibers (number of capillaries in each fiber).50 The reason for this difference is not as yet fully understood. Respiratory muscle strength is defined as the maximum and minimum static pressures measured at the mouth attributable to the muscular effort needed to produce the change.10 Whereas, ventilatory muscle endurance may be defined and measured as the capacity for sustaining high levels of ventilation under isocapnic conditions for relatively long periods. Exercise tolerance is the ability to exercise without discomfort. Strength, endurance, fatigue, and dyspnea all play a role in determining an exercise tolerance level. Limited quantitative data are available on respiratory muscle strength and endurance response to a general exercise program. Some studies attribute an increase in exercise tolerance to psychological components of improved motivation, sense of well-being, and confidence.29, 30, 34, 36, 40, 51 Several studies allude
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to improved neuromuscular coordination as the causative factor.25, 30, 47 Stride length increased in some patients, perhaps improving the efficiency of walking. Paez and associates concluded that emphysematous patients improve the ability to perform the exercise used in their training programs.30 Again, this demonstrates improved neuromuscular coordination and efficiency of movement. Keens and colleagues demonstrated in children with cystic fibrosis that nonspecific upper body exercise, such as swimming and canoeing, was effective in improving endurance.43 Leith and Bradley trained normal volunteers according to the VMET and VMST methods previously described.10 They concluded that VMST improved strength while VMET improved endurance. Belman and Mittman trained patients with COPD according to the same VMET and VMST methods.44 Although spirometric indexes and lung volumes did not change, VMET did significantly increase endurance and exercise tolerance in these patients. Keens and associates used VMET in normal, young adults and in children with cystic fibrosis.43 Both groups increased their endurance measurements after four weeks. Other investigators have defined ventilatory muscle endurance as the amount of time the ventilatory muscles can perform work against a given inspiratory flow resistive load.13, 18, 52, 53 Anderson and associates used this definition to study the effects of training with inspiratory flow-resistive loads on ventilatory endurance in patients with COPD.54 After training, these patients could inspire through relatively high level flow-resistive loads without manifesting any signs of inspiratory muscle fatigue. Additionally, they were able to perform routine daily activities without dyspnea. Gross and colleagues designed a similar study for quadriplegic patients.13 Results indicated that ventilatory muscle strength and endurance improved independently and dyspnea disappeared. Merrick and Axen studied inspiratory muscle function following abdominal weight exercises in young, healthy adults.46 Weights were placed on the anterior abdominal wall to resist diaphragm descent during diaphragmatic breathing exercises. They concluded this commonly used isotonic exercise program did not increase maximal shortening, velocity of shortening, or strength of the diaphragm; however, these subjects increased the maximal weight tolerated, exercised more rapidly, and expressed less discomfort by the end of the program. Perhaps these observations suggest improved inspiratory muscle endurance through isotonic exercise. Whether true histochemical, biochemical, or anatomical changes resulted is unknown; improved exercise-specific coordination can probably be assumed. It remains unclear as to whether abdominal weight exercises actually enhance diaphragmatic performance. Sharp and associates demonstrated postural relief of dyspnea in patients with COPD through
PHYSICAL THERAPY
forward leaning.52 Perhaps the resultant improved diaphragmatic length-tension relationship was related to enhanced endurance by enabling full synergistic cooperation of the inspiratory muscles.
Effects on Respiratory Muscle Fatigue Simonson defined skeletal muscle fatigue as the inability to maintain a predetermined load.55 Diaphragmatic fatigue, as defined by Roussos and Macklem, is the point at which the diaphragm is observed to be unable to sustain a predetermined level of transdiaphragmatic pressure.20 Gross and associates subsequently applied frequency spectrum analysis of the EMG to detect diaphragmatic fatigue before the diaphragm failed to maintain a predetermined load (generate pressure).15 Their study showed a decrease in amplitude of the high frequency components of myoelectric potentials and an increase in low frequency components when performing fatiguing work (decreased H:L ratio). Roussos and associates investigated what role the recruitment of other inspiratory muscles plays in preventing fatigue when breathing against resistive loads.18 By monitoring the abdominal pressure, the investigators noted the diaphragm and intercostal accessory muscles contributed alternately in time. They suggested that recovery may occur during the alternate rest periods possibly postponing the onset of fatigue. Additionally, hyperinflation was found to compromise the length-tension relationship of the inspiratory muscles; therefore, at larger lung volumes, lower maximum pressures are generated. Larger lung volumes also flatten the diaphragm, thus inhibiting the pressure generating capabilities. Hence, the indications for hyperinflation with airway obstruction (improved inspired gas distribution and gas exchange by opening narrowed airways) may be outweighed by placing the inspiratory muscles at a mechanical disadvantage, thus increasing the work of breathing and increasing energy consumption, which consequently lead to fatigue. As mentioned earlier, histochemical, biochemical, and anatomical changes are seen in respiratory muscles in response to training. Keens and colleagues demonstrated cellular adaptations of the respiratory muscles produced by a chronic increased respiratory load.5 Increase in oxidative capacity, in mitochondrial enzymes, and in capacity for fatty acid oxidation suggest that the increased load produced the same changes as seen in endurance training of guinea pigs, therefore, making the muscle fiber more resistant to fatigue.56 Keens and associates suggested that these same adaptations might occur with hyperinflation as experienced in patients with COPD.5 In this case, the diaphragm is at a mechanical disadvantage and the intercostals and accessory muscles experience greater
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loads. Therefore, these cellular adaptations could be associated with increased resistance to fatigue. Muscle fatigue was not measured as an independent variable in any of the reviewed general exercise programs for patients with COPD. However, endurance and exercise tolerance have been reported and described in previous sections. Several studies suggested that dyspnea curtails activity levels of patients with COPD before muscle fatigue occurs. Whether the physiological or psychological components of dyspnea limit activity is unclear. As mentioned earlier, Keens and colleagues suggested that endurance training against an increased respiratory load might increase the respiratory muscle fiber resistance to fatigue.5 This may occur during VMET. Sharp and associates have investigated the EMG patterns of ventilatory muscles while studying postural relief of dyspnea.52 Although the EMG activity of the accessory inspiratory muscles was greater in standing and erect sitting than in forward leaning, one group of patients experienced considerable relief of dyspnea in the forward leaning position. It seems that the force generated by these muscles was more efficiently applied to the rib cage in the forward leaning position. Perhaps by stabilizing the upper extremities and using the reverse action of the muscles, synergy of the inspiratory muscles was enhanced, thereby reducing fatigue. Gross and associates suggested that quadriplegia predisposes a patient to inspiratory muscle fatigue due to reduced strength, endurance, and compliance, and increased work of breathing.13 In their study the H:L ratio was used as a criterion to assess if the diaphragm was performing fatiguing work. No EMG activity was found in the intercostal or pectoral muscles after inspiratory training. These patients experienced increased strength and endurance and therefore gained protection against fatigue, without needing an "alternate recovery period" to enhance synergistic respiratory muscle function.
SUMMARY Although exercise programs have long been advocated as a therapeutic procedure for patients with respiratory or neuromuscular disease, there are few quantitative physiological data on the efficacy of these modalities. Studies have typically reported on changes in spirometric variables of lung function or on psychological advantages of rehabilitation training programs. Using these criteria, most investigators have failed to demonstrate improvement in lung function in patients with respiratory or neuromuscular disease. The information presented here describes some of the most current and promising methods for physio-
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logical evaluation of respiratory muscle performance. Correlation of clinical signs with magnetometry, transdiaphragmatic pressures, and electrical activity of EMG provides the earliest notice of the onset of fatigue as well as assessment of strength and quantification of endurance. Of the many rehabilitation programs for pulmonary insufficiency, exercise program formats can be considered either general (systemic exercise) or specific (localized training of ventilatory muscles). Although general programs have demonstrated positive motivational benefits, there is little evidence of improvement in either lung function or respiratory muscle function. In contrast, Leith and Bradley have demonstrated a promising new direction of training respiratory muscles.10 Application of such programs
to healthy individuals,10 patients with cystic fibrosis,43 and to patients with quadriplegia13 has yielded encouraging results with respect to respiratory muscle strength and endurance. The presented material and opinions should be considered commentary on and documentation of various respiratory rehabilitation programs. Based on the current literature, it appears that the design and assessment of a comprehensive pulmonary rehabilitation program for a patient should focus on the following points: 1) increasing ventilatory endurance, 2) increasing respiratory muscle strength, 3) reducing respiratory muscle fatigue, 4) improving cardiopulmonary function, and 5) demonstrating positive motivational benefits.
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20. Roussos CS, Macklem PT: Diaphragmatic fatigue in man. J Appl Physiol 43:189-197, 1977 21. Alpert JS, Bass H, Szucs MM, et al: Effects of physical training on hemodynamics and pulmonary function at rest and during exercise in patients with chronic obstructive pulmonary disease. Chest 6 6 : 6 4 7 - 6 5 1 , 1974 22. Bass H, Whitcomb JF, Forman R: Exercise training: Therapy for patients with chronic obstructive pulmonary disease. Chest 5 7 : 1 1 6 - 1 2 1 , 1970 23. Bradley BL, Garner AE, Billiu D, et al: Oxygen-assisted exercise in chronic obstructive lung disease. Am Rev Respir Dis 118:239-243, 1978 24. Casciari RJ, Fairshter RD, Morrison JT: Effects of breathing retraining Jn patients with chronic obstructive pulmonary disease. Chest 79:393-398, 1981 25. Chester EH, Belman MJ, Bahler RC, et al: Multidisciplinary treatment of chronic insufficiency. 3: The effect of physical training on cardiopulmonary performance in patients with chronic obstructive pulmonary disease. Chest 72:695-702, 1977 26. Degre S, Sergysels S, Mession R, et al: Hemodynamic responses to physical training in patients with chronic lung disease. Am Rev Respir Dis 110:395-402, 1974 27. Hale T, Spriggs J, Hamley EJ: The effects of an exercise regimen on patients with lung malfunction. Br J Sports Med 11:181, 1977 28. Heimlich D: Evaluation of a breathing program for children. Respiratory Care 20:64-68, 1975 29. Kimbel P, Kaplan AS, Alkalay I, et al: An in-hospital program for rehabilitation of patients with chronic obstructive pulmonary disease. Bulletin of The American College of Chest Physicians 60:96-105, 1971 30. Paez PN, Philipain EA, Masangkay M, et al: The physiologic basis of training patients with emphysema. Am Rev Respir Dis 9 5 : 9 4 4 - 9 5 3 , 1967 31. Sinclair DJM, Ingram CG: Controlled trial of supervised exercise training in chronic bronchitis. Br Med J 280:519, 1980 32. Unger KM, Moser KM, Glansen P: Selection of an exercise program for patients with chronic obstructive pulmonary disease. Heart Lung 9:68-76, 1980 33. Wilbourn K: The long distance runners. Runner's World, August: 6 2 - 6 5 , 1978 34. Woolf CR: A rehabilitation program for improving exercise tolerance of patients with chronic lung disease. Can Med Assoc J 106:1289-1292, 1972 35. Woolf CR, Suero JT: Alterations in lung mechanics and gas exchange following training in chronic obstructive lung disease. Diseases of the Chest 55:37-44, 1969
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36. Moser KM, Bokinsky GE, Savage RT, et al: Results of a comprehensive rehabilitation program. Arch Intern Med 140: 1 5 9 7 - 1 6 0 1 , 1980 37. Barach AL, Seaman W: Role of diaphragm in chronic pulmonary emphysema. NY State J Med 63:415-417, 1963 38. Barach AL: Physiotherapy of advanced disease states. In Petty TL (ed): Chronic Obstructive Pulmonary Disease. New York, NY, Marcel Dekker Inc. 1978, pp 107-149 39. Goldman M, Mead J: Mechanical interaction between diaphragm and rib cage: Mechanics of the diaphragm. J Appl Physiol 35:197-204, 1973 40. Agle DP, Baum GL, Chester EH, et al: Multidiscipline treatment of chronic pulmonary insufficiency. 1: Psychologic aspects of rehabilitation. Psychosom Med 35:41-49, 1973 4 1 . Ingram RH, Schilder DP: Effect of pursed lips expiration on the pulmonary pressure-blow relationship in obstructive lung disease. Am Rev Respir Dis 96:381-388, 1967 42. Mueller RE, Petty TL, Filley GF: Ventilation and arterial blood gas changes induced by pursed lips breathing. J Appl Physiol 28:784-789, 1970 43. Keens TG, Krastins IRB, Wamamaker EM, et al: Ventilatory muscle endurance training in normal subjects and patients with cystic fibrosis. Am Rev Respir Dis 116:853-860, 1977 44. Belman MJ, Mittman C: Ventilatory muscle training improves exercise capacity in chronic obstructive pulmonary disease patients. Am Rev Respir Dis 121:273-280, 1980 45. Blumberg M: Respiration and speech in the cerebral palsied child. Am J Dis Child 89: 4 8 - 5 3 , 1955
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46. Merrick J, Axen K: Inspiratory muscle function following abdominal weight exercises in healthy subjects. Phys Ther 61:651-656, 1981 47. Rothman JG: Effects of respiratory exercises on the vital capacity and forced expiratory volume in children with cerebral palsy. Phys Ther 58:421 - 4 2 5 , 1978 48. Shannon R: Respiratory pattern changes during costovertebral joint movement. J Appl Physiol 48:862-867, 1980 49. Scheuer J, Tipton CM: Cardiovascular adaptations to physical training. Am Rev Physiol 3 9 : 2 2 1 - 2 5 1 , 1977 50. Johnson WR, Buskirk ER: Science and Medicine of Exercise and Sports, ed 2. New York, NY, Harper & Row, Publishers Inc. 1974 5 1 . Lustig FM, Haas A, Castillo R: Clinical and rehabilitation regimen in patients with chronic obstructive pulmonary disease. Arch Phys Med Rehabil 53:315-322, 1972 52. Sharp JT, Drutz WS, Moisan T, et al: Postural relief of dyspnea in severe chronic obstructive pulmonary disease. Am Rev Respir Dis 122:201 - 2 1 1 , 1 9 8 0 53. Macklem PT: Respiratory muscles: The vital pump. Chest 28: 7 5 3 - 7 5 8 , 1980 54. Anderson JB, Dragted L, Kann S, et al: Resistive breathing in severe chronic obstructive pulmonary disease: A pilot study. Scand J Respir Dis 60:151-156, 1979 55. Simonson E: Physiology of Work Capacity and Fatigue. Springfield, IL, Charles C Thomas, Publisher, 1971, p 97 56. Lieberman DA, Maxwell LC, Faulkner JA: Adaptation of guinea pig diaphragm muscle to aging and endurance training. Am J Physiol 22:556-560, 1972
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