INTRODUCTION

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Previous investigators have found that muscular individuals have stronger inspiratory muscles and greater diaphragm mass than control subjects (1, 2). Possible explanations for this observation include an overall increase in muscle mass due to different intrinsic or extrinsic levels of anabolic steroids, or differences in nutrition or genetics. Alternatively, strenuous nonrespiratory activities involving the trunk or upper extremities, in themselves, may strength train the diaphragm. With vigorous use of the arms and torso, the abdominal and rib cage muscles are activated, thereby increasing abdominal pressure. To avoid expiration, the glottis can be closed or the diaphragm can be activated. Repeated engagement in such activities then may result in repeated contractions of the diaphragm. If the pressure generated with each contraction is of sufficient magnitude, the diaphragm and other muscles of inhalation may be strengthened. However, the degree to which the diaphragm is activated during robust activities involving the trunk is not known. The purpose of this study was to evaluate the effects of vigorous nonrespiratory activities involving the trunk and upper extremities on transdiaphragmatic pressure. We hypothesized that activities such as weight lifting and sit-ups increase transdiaphragmatic pressure to a degree sufficient to strength train the diaphragm.

	METHODS

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Six healthy subjects between the ages of 27 and 48 were recruited for the study. Anthropometric data for these subjects are shown in Table 1. None of these subjects was engaged in regular weight-lifting activities with the exception of subject no. 6 who trained 3 or 4 d/wk. The study was approved by the Institutional Review Committee and informed consent was obtained from all subjects.

Pressure Measurements

Esophageal and gastric catheters were positioned using standard techniques. Pressure was measured (Validyne mean pressure [MP] ± 400 cm H₂O) in the distal esophagus (Pes) and stomach (Pga). Pressures were recorded on a strip chart recorder (Gould Instruments). The transdiaphragmatic pressure difference (Pdi) was calculated as Pga  Pes.

Protocol

Prior to participation in the study, each subject was asked to perform three types of weight-lifting maneuvers: power lift, bench press, and biceps curl. During this session, we determined the maximum amount of weight that could be lifted for 10 repetitions with each maneuver. Knowing this maximum weight for each subject, we then prescribed 10 repetitions of approximately 33, 67, and 90% of the maximal weight (low-, moderate-, and high-intensity activities, respectively). The subjects occasionally needed verbal encouragement to complete the full 10 repetitions of the highest intensity tasks.

On the study day, we first determined the maximal transdiaphragmatic pressure (Pdi_max) that could be generated during a combined Mueller and expulsive maneuver for each subject (3). During this maneuver, esophageal and gastric pressures were displayed to the subject on an oscilloscope, with Pes located above Pga so that the distance between the two pressure signals would fall but the signals would not cross as the pressure difference (Pdi) increased. The subject was instructed to inhale against the occluded mouthpiece while simultaneously contracting the abdominal muscles in an attempt to make the two tracings converge as closely as possible. Each maneuver was sustained for at least 3 s. The maximal pressure was taken as the highest value sustained for 1 s.

Transdiaphragmatic pressure was then measured as subjects performed the following activities: power lift, bench press, biceps curl, and sit-ups. The power lift was performed with the subject standing upright, bent at the hips, and lifting a barbell from the floor to the chest. The bench press consisted of lying on a bench with the back and buttock supported by the bench. The barbell was lifted from the chest until the arms were fully extended. The biceps curl was performed with the subject standing upright and consisted of lifting a dumbbell starting with the arm fully extended and finishing with the arm fully flexed. Sit-ups were performed with the subject supine, the knees bent, and arms folded across the chest. The subject then raised the back to an angle of approximately 45°. With the exception of the sit-ups, each activity was repeated at three different task intensities. With low-intensity lifting, the subject could comfortably finish 10 repetitions; with moderate-intensity lifting, the subject finished the 10 repetitions with modest effort; and with high-intensity lifting, the subject strained to finish 10 repetitions. Each maneuver at each intensity was performed twice, once with the subject inhaling during the active phase of each maneuver and once with the subject exhaling during the active phase of each maneuver. The higher intensity activities were performed with and without the subject wearing an abdominal binder. The abdominal binder consisted of a standard weight-lifting belt, which was wrapped around the anterior abdominal wall and secured with straps. Control activities consisted of reproducing each maneuver but with no added weights or bar being lifted. The control for the sit-up consisted of lying supine with the knees flexed. The subject was allowed to rest for 3-5 min between maneuvers. The different activities were performed randomly and the entire protocol took between 2 and 3 h to complete. Each activity was initiated when the subject's lung volume was at functional residual capacity (FRC).

Calculations

Transdiaphragmatic pressure for each maneuver was reported as the mean of five measurements of the maximum pressures during the maneuver. This value was normalized by Pdi_max for each subject (Pdi/Pdi_max). Transdiaphragmatic pressure was partitioned into its gastric and esophageal components for each maneuver.

Statistics

Data are presented as mean ± standard deviation (SD). A one-factor repeated measures analysis of variance with a Fischer post hoc was used to determine level of significance for differences among the condition (control, inhalation, exhalation) and task intensity (light, intermediate, heavy, and heavy + belt) split for each task (bench press, curl, power lift, and sit-up). Significance was set at the 0.05 level.

	RESULTS

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The group mean value of Pdi_max obtained during the combined Mueller and expulsive maneuver was 197 ± 25 cm H₂O (mean ± SD). This is within the range of normal values for Pdi_max reported by us and others (2).

The diaphragm was recruited during sit-ups and all weight-lifting activities. Typical changes in Pes and Pga during a weight-lifting maneuver for one individual are shown in Figure 1. Pga increased during the active phase of the maneuver. Group mean values of Pdi, expressed either in absolute terms or as a fraction of its maximum (Pdi/Pdi_max), increased significantly during all maneuvers when compared to the control maneuver (57 ± 24 versus 18 ± 10 cm H₂O for Pdi [p < 0.001] and 0.30 ± 0.13 versus 0.10 ± 0.06 for Pdi/Pdi_max [p < 0.001]).

View larger version (16K): [in this window] [in a new window]   Figure 1.   Changes in esophageal (upper panel ) and gastric (lower panel ) pressures as weights are repeatedly lifted by a healthy individual. During the activity (vertical lines), transdiaphragmatic pressure is generated and the increase in gastric pressure associated with the activity is not transmitted to the thorax.

The magnitude of Pdi achieved differed among activities. Mean values of Pdi/Pdi_max for each activity are shown in Figure 2. When compared with the control maneuver, Pdi increased significantly during the active phase of each activity, irrespective of the timing of inspiration. The activities that were accompanied by the greatest changes in Pdi were the power lifts (Pdi/Pdi_max of 0.34 ± 0.07 and 0.38 ± 0.08 performed with the active phase during inhalation or exhalation, respectively) and sit-ups (Pdi/Pdi_max of 0.47 ± 0.16 and 0.41 ± 0.18 performed with the active phase during inhalation or exhalation, respectively). There were no significant differences in Pdi or Pdi/Pdi_max when the active phase of the maneuver occurred during inhalation or exhalation.

View larger version (23K): [in this window] [in a new window]   Figure 2.   Mean values of Pdi/Pdimax for each activity are shown during the control maneuver and when the subject was instructed either to inhale (inspiration) or exhale (expiration) during the active phase of the maneuver. Sit-ups and power lifts were accompanied by the greatest changes in Pdi. *p < 0.005 for control versus inhalation; p < 0.01 for control versus exhalation; §p < 0.001 for control versus inhalation or exhalation.

The Pdi achieved during the weight-lifting activities increased as the intensity of each activity increased. The relationship between Pdi/Pdi_max and task intensity for each of the weight-lifting activities is shown in Figure 3. Pdi/Pdi_max was greatest when each maneuver was performed at the highest intensity. When comparing heavy and light intensities, we found that Pdi/Pdi_max was 0.33 ± 0.09 versus 0.18 ± 0.09 for the curls (p < 0.0005), 0.35 ± 0.10 versus 0.15 ± 0.06 for the bench press (p < 0.005), and 0.40 ± 0.06 versus 0.32 ± 0.08 for the power lift (p < 0.05). The application of an abdominal binder during the most intense weight-lifting activities further increased Pdi/ Pdi_max for curls (0.33 ± 0.09 versus 0.44 ± 0.10 9) (p < 0.05) and bench press (0.24 ± 0.07 versus 0.35 ± 0.10) (p < 0.005) (Figure 3). Pooled values of Pdi for the highest intensity activities are shown in Table 2. During these activities, peak values of Pdi were 126 ± 11 cm H₂O or 0.65 ± 0.04 of Pdi_max.

View larger version (25K): [in this window] [in a new window]   Figure 3.   Mean values of Pdi/Pdimax for each activity are shown for light, intermediate, and heavy tasks (pooled for inspiration and expiration) and for heavy tasks performed with an abdominal binder in place. Pdi/Pdimax significantly increases as task intensity increases and with the application of an abdominal binder. Curl: *p< 0.0005 for light versus heavy; p < 0.0001 for light versus heavy + belt; §p < 0.05 for intermediate versus heavy; p < 0.0001 for intermediate versus heavy + belt; °p < 0.05 for heavy versus heavy + belt. Bench press: *p < 0.005 for light versus heavy; p < 0.0001 for light versus heavy + belt; p < 0.0001 for intermediate versus heavy + belt; °p < 0.005 for heavy versus heavy + belt. Power lift: *p < 0.05 for light versus heavy; p < 0.01 for light versus heavy + belt.

The increase in Pdi during all activities was primarily due to an increase in gastric pressure. During the high intensity activities, Pga increased by 84 ± 11 cm H₂O and Pes decreased by 13 ± 7 cm H₂O (Table 2). Accordingly, the increase in Pga accounted for 85 ± 4% of the increase in Pdi during the weight-lifting activities and sit-ups. By contrast, the increase in Pdi during the control activities was more evenly distributed across the diaphragm. During these activities, Pga increased by 11 ± 4 cm H₂O and Pes decreased by 7 ± 3 cm H₂O (increases in Pga and Pes accounted for 58 ± 9 and 42 ± 9% of the rise in Pdi, respectively). Despite each individual developing very high gastric pressures during the activities (mean peak Pga of 112 ± 15 cm H₂O), esophageal pressure remained subatmospheric (14 ± 7 cm H₂O) (Table 2).

	DISCUSSION

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We found that the diaphragm is recruited during certain nonrespiratory activities involving the trunk and limb muscles. The greatest increases in transdiaphragmatic pressure were seen during sit-ups and power lifts, during the most strenuous maneuvers, and when an abdominal binder was in place. The magnitude of transdiaphragmatic pressures achieved during sit-ups and the high-intensity weight lifting was in the range that could potentially provide a strength-training stimulus to the diaphragm.

A number of studies have documented that respiratory muscle strength and endurance can be increased by training protocols specifically targeting the respiratory muscles (6). Whether the respiratory muscles adapt to nonspecific processes that increase the strength of other trunk muscles is not known. In support of this notion, Rinqvist (13) found a significant correlation between the strength of the trunk flexors and maximal static inspiratory pressure (PI_max) in a series of 200 healthy males and females. Subsequently, Arora and Rochester (1) measured diaphragm mass in an autopsy series of 33 subjects including 6 previously healthy muscular laborers. They found that the subjects who were formerly involved with manual labor had greater diaphragm mass. We extended these observations by using ultrasound to assess diaphragm mass in 31 subjects including 14 muscular weight lifters (2). We found that diaphragm mass was increased in the more muscular individuals. These observations suggested that the diaphragm may be recruited during nonrespiratory activities.

The abdominal muscles are often recruited during activities involving the upper extremities and trunk such as when lifting heavy objects. Contraction of these muscles increases abdominal pressure. A benefit of increasing abdominal pressure during weight-lifting activities is that it lessens the axially directed compressive forces on the spine that are associated with these maneuvers. However, if the glottis is closed and the diaphragm is passive during these activities, the elevated intraabdominal pressure is transmitted to the thorax. High intrathoracic pressures, in turn, may have adverse hemodynamic and central nervous system effects such as decreasing venous return from the extremities, increasing systemic blood pressure, and increasing central nervous system (CNS) pressure. To avert these complications, the diaphragm may be recruited during strenuous truncal activities. A tensed diaphragm will minimize or even avert the rise in intrathoracic pressure that occurs when the abdominal muscles are forcefully contracted. Thus, by recruiting the diaphragm, one can preserve the benefits of increasing abdominal pressure in minimizing the compressive forces on the spine while avoiding the complications related to high intrathoracic pressures. In our subjects, intrathoracic pressure remained subatmospheric even when gastric pressures were elevated to levels greater than 100 cm H₂O. In addition, activating the diaphragm not only maintained intrathoracic pressure at subatmospheric levels but also allowed the individual to breathe during the activity.

Unlike healthy individuals, ambulatory patients with bilateral diaphragm paralysis often complain of dyspnea when bending or lifting. These symptoms may be related to their inability to prevent a rise in intrathoracic pressure by contracting their diaphragm during postural activities. Such increases in intrathoracic pressures may interfere with their breathing. To evaluate this possibility we measured Pdi in one 36-yr-old patient with bilateral diaphragm paralysis (vital capacity [VC] 52% predicted, PI_max 30 cm H₂O) while he performed biceps curls. Similar to individuals with intact diaphragm function, we observed that intraabdominal pressure increased during these activities. However, there was no transdiaphragmatic pressure as intrathoracic pressure increased to the same magnitude as intraabdominal pressure. Consequently, he was able to inhale only between repetitions, and he quickly became dyspneic (Figure 4). This observation further supports the concept that diaphragm activation is needed to avert increases in intrathoracic pressure during truncal activities.

View larger version (8K): [in this window] [in a new window]   Figure 4.   Changes in esophageal (upper panel ) and gastric (lower panel ) pressures as weights are repeatedly lifted in an individual with bilateral diaphragm paralysis. During the activity (vertical lines), there is no transdiaphragmatic pressure and the increase in gastric pressure associated with the activity is transmitted to the thorax.

Diaphragm activation may also be associated with rapid movements of the upper extremities. When using a visual stimulus to initiate rapid movements of the arms, Hodges and coworkers (14) found an increase in electromyogram (EMG) activity of the diaphragm and the transversus abdominous prior to that of the deltoid. Diaphragm activation associated with upper extremity movements was accompanied by a rise in Pdi irrespective of whether the limb movement was initiated during inspiration or expiration. Since the transversus abdominous and diaphragm were coactivated and are usually thought of as antagonists, Hodges and coworkers (14) speculated that the diaphragm and abdominal muscles modulate changes in abdominal and pleural pressures for postural control. They concluded that diaphragm contraction prior to the onset of rapid limb movements may constitute a preparatory action that aids in truncal stabilization. Our observation that Pdi increases with weight-lifting activities supports the idea that the diaphragm is an important postural muscle.

We found that the increase in transdiaphragmatic pressure that occurs during intense truncal activities such as weight lifting is of a magnitude that may provide a strength-training stimulus to the diaphragm. Based on data from previous inspiratory muscle training studies (11) and on the established principles developed for isometric strength training of peripheral muscles (15), maximal contractions of long duration are the most effective strength-training regimens. Maximal rather than submaximal contractions are more likely to activate the high threshold units and thus evoke the training response. In our study, peak values of Pdi were 0.65 of Pdi_max during sit-ups and the most intense weight-lifting maneuvers. This range of Pdi would, in theory, be of sufficient magnitude to strength train the diaphragm and may be the mechanism underlying the previously noted increase in diaphragm muscle mass in weight lifters and laborers (1, 2).

Typical inspiratory muscle strength-training protocols consist of performing repetitive maximum inspiratory or expiratory efforts against a resistive load. With this type of training maneuver, increases in inspiratory muscle strength as great as 50% can be anticipated (6, 16). Other benefits include a reduction in dyspnea (10) and improved exercise capacity in some patients with chronic obstructive pulmonary disease (COPD) (6, 17, 18). However, the resistive loads imposed by such training protocols may be overcome primarily by recruiting the inspiratory muscles of the rib cage rather than the diaphragm (19). If the primary goal is to train the diaphragm, resistive loaded breathing may not be a useful training stimulus in individuals who adopt the former strategy. Differences in breathing strategies employed to overcome resistive loads, then, may account for some of the discrepancies among studies of inspiratory muscle training.

Activities that can specifically increase transdiaphragmatic pressure such as weight lifting, sit-ups, or combined inspiratory and expulsive maneuvers may also be used to strength train the diaphragm. In contrast to the combined inspiratory and expulsive maneuver, the activities that were evaluated in the present study were simple to perform and easy to teach. These activities also have other associated benefits. Maneuvers such as power lifts and biceps curls may not only potentially train the diaphragm, but also strengthen the muscles of the rib cage and upper extremities. Both of these muscle groups are often recruited during breathing in patients with COPD. Furthermore, weight training in these individuals may improve bone density. Finally, compliance with inspiratory muscle training protocols may be improved as these activities are simple to perform and provide positive feedback by increasing the mass of visible muscle groups. However, a number of differences between healthy individuals and patients with COPD may limit the degree to which our results can be extrapolated to these patients. Factors such as poor nutrition, age, and lack of motivation may limit the degree of any improvement in inspiratory muscle function with training. Nonetheless, inspiratory muscle performance has been improved using standard techniques in patients with COPD (6, 17, 18). However, the effects of weight lifting in a comprehensive pulmonary rehabilitation program remain to be studied.

We conclude that nonrespiratory maneuvers such as weight lifting can increase transdiaphragmatic pressure. The transdiaphragmatic pressure attained during nonrespiratory maneuvers is dependent on (1) the type of maneuver performed, (2) the intensity of the maneuver, and (3) abdominal compliance. The level of transdiaphragmatic pressure achieved in the most intense maneuvers reaches a magnitude that can potentially provide a strength-training stimulus for the diaphragm.