INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

The force output of respiratory muscles generally depends on respiratory muscle mass, intrinsic contractility, mechanical advantage, operating length, and degree of neural activation of these muscles (1). In a recent study (2), we showed that certain maneuvers may significantly increase the pressure (force) output of the expiratory muscles. Specifically, the maximal dynamic expiratory pressure generated during a forced expiration at TLC can be significantly enhanced if expiratory muscle contraction is immediately preceded by a fast inspiratory muscle (IM) contraction, such as in rapid inspiration to TLC. In contrast, the maximal dynamic expiratory pressure at TLC is comparatively lower when the maneuver involves a slow inspiration to TLC and a breathhold prior to maximal expiration (2). Although not fully understood, the mechanism underlying the enhanced maximal dynamic expiratory pressure in the first of these situations appears to be an enhanced activation of the agonist muscles related to a specific inspiratory-expiratory interaction analogous to those described for a pair of agonist- antagonist skeletal muscles (3).

In the study reported here, we reversed the sequence of agonist-antagonist contraction and examined the extent to which IM pressure output is similarly augmented by maneuvers in which IM (agonist) contraction is preceded by a fast contraction of the expiratory (antagonist) muscles. To this end, we assessed the ability of normal subjects to generate maximal inspiratory pressures and maximal inspiratory flows against an occluded or unoccluded airway near RV following slow or fast expirations to RV.

	METHODS

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Twelve laboratory volunteers (all men, age 35 ± 6 yr) participated in the study. The subjects were familiar with respiratory maneuvers, and all but three were naive to the purpose of the study. No subject had a history of pulmonary disease; there were five smokers, but they all had normal spirometric results. The study was approved by the institutional review board.

All experiments were performed with the subjects in the seated position. Pressure at the airway opening (Pao) was measured with a pressure transducer (MP-45, ± 250 mm Hg; Validyne Corp., Northridge, CA) calibrated to 300 cm H₂O. Inspiratory flow was measured with a heated pneumotachograph (Hans-Rudolph, Kansas City, MO) and a differential pressure transducer (MP-45, ± 2 cm H₂O; Validyne). Inspired volume was obtained by integrating (Gould integrator; Gould Instrument, Cleveland, OH) the flow signal. The electromyograph (EMG) of parasternal muscles was recorded through a pair of surface electrodes placed over the second or third intercostal space near the right sternal margin. EMGs signals were amplified (Nihon-Koden Co., Tokyo, Japan) and filtered, using a bandpass between 20 Hz and 1 kHz. Raw EMG signals were rectified and integrated by a moving averager (MA-821 RSP; CWE Inc., Ardmore, PA), using a 200-ms averaging time. Pressure, flow, volume, and EMG signals were displayed on a monitor (Gould V1000 video display). All signals were digitized in real time, recorded on a strip chart recorder (Gould ES 1000), and stored in a computer (Wyse 486) for later analysis.

Maximal static inspiratory pressure (PI_max) against an occluded airway (Mueller maneuver), and maximal dynamic inspiratory pressure (PI_dyn) and maximal inspiratory flow (I_max) with no external resistance, were measured near RV in all subjects, using two different (fast [F] or slow [S]) maneuvers. With the F maneuver, the subject exhaled rapidly to RV and immediately performed a forceful inspiration, whereas in the S maneuver, the subject exhaled slowly to RV, held the breath at RV for about 4 to 6 s, and then inspired forcefully against the resistance. During Mueller maneuvers, a 14-gauge needle was inserted into the mouthpiece of the respirometer to prevent contraction of the buccal muscles. During efforts with an unoccluded airway, the lung volume at which measurements were made was assessed from inspiratory VC values, which were obtained by having the subject fully inspire to TLC. Prior to measurements, all subjects performed several practice runs for each maneuver. Both occluded and unoccluded maneuvers were initiated from TLC, and the two types of maneuver were interspersed randomly with one another. During these efforts, care was taken to maintain the subject's neck in a neutral position in order to decrease flow variability related to tracheal collapsibility (4). Each subject performed from five to seven repeats of each maneuver with and without resistance, with a frequency of one run every 2 to 3 min.

The digitized data were analyzed with the Labdat software program. Integrated EMG signals were analyzed for peak EMG activity; the rate of increase of Pao (dPao/dt) was analyzed by differentiating the pressure waveform. Efforts for a given maneuver were accepted if they were within 5% of maximum VC; of those that met this criterion, the three or four runs with the greatest Pao values were analyzed. Average values of three or four measurements were used for analysis. Grouped data were analyzed with Student's t test for paired variables, and were reported as Mean ± SE. A value of p  0.05 was considered significant.

	RESULTS

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Complete EMG data were available for nine subjects. Figure 1 shows typical maneuvers from which the data were obtained. With the F maneuver, duration of expiration was comparable (p > 0.05) for efforts with occluded airway and those with no added resistance (2.75 ± 0.25 s versus 2.53 ± 0.21 s, respectively); similarly, with the S maneuver, duration of expiration did not differ between efforts with an occluded airway and those with no added resistance (7.87 ± 0.57 s versus 8.54 ± 0.58 s, respectively).

View larger version (14K): [in this window] [in a new window]   Figure 1.   Representative tracings obtained with the F and S expiratory maneuvers during maximal inspiratory efforts with an occluded airway near RV in one subject. The solid vertical line marks the beginning of expiration and the dotted vertical line passes through the beginning of inspiration. Pao = pressure at the airway opening; EMGp = electromyograph of parasternal muscles.

During Mueller maneuvers, PI_max, dPI_max/dt, and peak EMG activity of the parasternal muscles were all greater (p < 0.05) with the F than with the S maneuver (Table 1). During efforts with no added resistance, PI_dyn, I_max, dPI_dyn/dt, and peak EMG activity of the parasternal muscles were similarly greater with the F (p < 0.05) than with the S maneuver (Table 1).

The percent intermaneuver increase in variables at each resistance is shown in Figure 2. The percent increase in dPao/dt with F was significantly greater for efforts with no added resistance (p < 0.05) than for those with an occluded airway.

View larger version (24K): [in this window] [in a new window]   Figure 2.   Percent increase in parameters obtained with the F maneuver during maximal inspiratory efforts with an occluded or unoccluded airway in all subjects. The ordinate represents the percent increase with the F maneuver in comparison with the S maneuver. Data are in mean ± SE. (*p < 0.05). Pao = pressure at the airway opening, EMGp = electromyograph of parasternal muscles.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

We found that the ability of normal volunteers to generate pressure and flow at RV was significantly enhanced with maneuvers in which forceful inspiration was immediately preceded by a fast expiration. This enhanced capacity appears to be related to greater IM activation, as shown by the EMG activity of parasternal muscles.

In a recent study (2), we showed that the activation and force output of expiratory muscles at TLC was substantially enhanced when forced expiration was immediately preceded by fast inspirations without an end-inspiratory pause, as compared with slow inspiration and a breathhold lasting a few seconds at TLC. Identical maneuvers have also been found to be associated with significantly greater peak expiratory flows in both normal subjects (5, 6) and patients with respiratory disease (7, 8). This enhanced capacity was attributed to a specific inspiratory-expiratory muscle interaction analogous to those described in skeletal muscle for a pair of agonist-antagonist muscles. The present findings extend our previous work (2) to include a similar interaction near RV, thus establishing the bidirectional character of the inspiratory-expiratory muscle interaction. In fact, the intermaneuver differences in PI_dyn (19%) and I_max (9%) attained near RV are roughly in the same range as respective values for maximal dynamic expiratory pressure (17%) and expiratory flow (7%) obtained at TLC.

We paid special attention to conducting the measurements in the present study at similar lung volumes for both the F and S maneuvers. However, VC values measured during efforts with an unoccluded airway showed that the operating lung volume was greater (by approximately 300 ml) with the F than that with the S maneuver. Likewise, for efforts with an occluded airway, we estimate that the lung volume with the F maneuver was also greater than that with the S maneuver and by a similar amount, as shown by expiratory VC values (corrected for gas compression) and the comparable expiratory times. Given the shape of the volume-pressure relationship near RV, such differences in lung volume probably do not have any substantial effect on generated pressures and, if anything, would tend to underestimate pressures obtained with the F maneuver.

Our dPao/dt and EMG data clearly show that the greater IM pressure generation with forceful inspiration immediately preceded by fast expiration is related to increased muscle activation with this F maneuver. The precise mechanism underlying this enhancement is not quite known, and has previously been discussed (2). Briefly, the enhanced activation may be related to the conditioning contraction of the antagonist (expiratory) muscles, which immediately precedes agonist (inspiratory) muscle contraction. This interaction has recently been described in peripheral muscles, and studies suggest that the intensity of conditioning contraction is likely to influence agonist motor-unit activation (3). Alternatively, the intensity of contraction may be related to a pliometric (lengthening) contraction of the IM during expiration, which was followed immediately by a concentric contraction. IM pressure output under these conditions is expected to be greater than that occurring during pure concentric contraction (9). Evidence for an active contraction of the diaphragm during forced expiration was previously provided by Melissinos and coworkers in normal subjects (12). However, in the absence of measurements of transdiaphragmatic pressure and diaphragmatic EMG, our present design does not allow us either to elucidate the precise mechanism for the increased muscle activation that we found with the F maneuver or to partition increments of IM pressure between the diaphragm and rib cage muscles. Recent studies with normal volunteers showed that the diaphragm is poorly activated near RV (13, 14). The extent to which fast expiratory maneuvers actually augment voluntary diaphragmatic activation in this region awaits further study.

Figure 2 shows intermaneuver differences in the degree of IM activation and pressure generation between efforts against an occluded airway and those with no added resistance. With the F maneuver, there was a trend toward greater muscle activation and pressure generation (about twofold) for efforts with no added resistance than for those against an occluded airway. Although the mechanism underlying this difference has yet to be defined, it may be due to differences in reflex inhibition (15).

Our data may have implications for accurately measuring IM muscle strength and I_max in clinical and epidemiologic studies. PI_max, a widely used indicator of IM strength (16), is usually measured at RV, since patients find the maneuver much easier at RV than at FRC. Likewise, I_max is an important component of the flow-volume loop and is frequently used (in conjunction with maximum expiratory flow) in screening patients for upper airway obstruction. Given that expiratory speed influences both measurements, a standardization of the maneuver in which they are measured may decrease the variability of both PI_max and I_max obtained at RV (17, 18). Furthermore, the enhanced activation of IM with the F maneuver as used in our study could in theory be used in training protocols to increase IM strength (19). In our previous study (20) of IM training at various lung volumes, the greater posttraining increase in IM strength at RV than at FRC or at high lung volumes may have been related to a similar agonist-antagonist interaction. However, the clinical application of this training technique may be limited by a greater likelihood of muscle injury with the F maneuver (19).

In conclusion, the present study indicates that the ability of normal subjects to generate maximal inspiratory pressures and flows near RV can be significantly enhanced by maneuvers in which forceful inspiration is immediately preceded by a fast expiration. In contrast, slow expirations to RV, with a pause of a few seconds at RV, generate comparatively lower pressure and flows. These data suggest an expiratory-inspiratory muscle interaction similar to those described for pairs of agonist-antagonist skeletal muscles, and in conjunction with analogous data obtained previously at TLC, establish the bidirectional character of this respiratory muscle interaction.