Prior human studies have shown that halothane attenuates activity in the parasternal intercostal muscle and enhances phasic activity in respiratory muscles with expiratory actions. This expiratory muscle activity could contribute to reductions in the functional residual capacity produced by anesthesia. Termination of this activity could contribute to the maintenance of inspiratory rib cage expansion. The purpose of this study was to estimate in humans the mechanical significance of expiratory muscle activity during halothane anesthesia and to search for the presence of scalene muscle activity during halothane anesthesia that might contribute to inspiratory rib cage expansion.
Six subjects (3 males, 3 females) were studied while awake and during 1.2 MAC halothane anesthesia, both during quiet breathing and during carbon dioxide rebreathing. Respiratory muscle activity was measured using fine-wire electromyography electrodes. Chest wall configuration was determined using images of the thorax obtained by three-dimensional, fast computed tomography and respiratory impedance plethysmography. Functional residual capacity was measured by a nitrogen dilution technique. Measurements were obtained after paralysis with 0.1 mg/kg vecuronium and mechanical ventilation.
Phasic inspiratory activity was present in the scalene muscle of four anesthetized subjects during quiet breathing and all anesthetized subjects during rebreathing. Phasic inspiratory activity was present in the parasternal intercostal muscle during halothane anesthesia in only the three female subjects and was enhanced by rebreathing; parasternal intercostal muscle activity was never present in anesthetized males. During anesthesia with quiet breathing, phasic expiratory activity was observed in the transversus abdominis muscles of only the three male subjects. Despite these differences in the pattern of respiratory muscle use, the pattern of chest wall responses to rebreathing was similar between males and females. When expiratory muscle activity was present, paralysis increased the end-expiratory thoracic volume by expanding the rib cage, demonstrating that this activity reduced thoracic volume in these subjects. Changes in thoracic blood volume were significant determinants of the change in functional residual capacity produced by paralysis.
In humans anesthetized with 1.2 MAC end-tidal halothane, there are marked interindividual differences in respiratory muscle use during quiet breathing that may be related to sex; phasic inspiratory scalene muscle and parasternal intercostal muscle activity may contribute to inspiratory rib cage expansion in some subjects; and when present, expiratory muscle activity significantly constricts the rib cage and contributes to reductions in functional residual capacity caused by halothane anesthesia.
Key words: Anesthetics, volatile: halothane. Lung: breathing pattern; diaphragm; functional residual capacity; intrathoracic blood volume; rib cage. Measurement technique: dynamic spatial reconstructor; electromyography; fast computed tomography; respiratory impedance plethysmography. Muscle: diaphragm; parasternal intercostal; respiratory; scalene; transversus abdominis. Sex: female; male.
HALOTHANE anesthesia profoundly changes the pattern of respiratory muscle use. In humans, halothane attenuates electromyogram (EMG) activity in the parasternal intercostal muscles. [1-4]Because such activity is crucial to normal inspiratory rib cage expansion, [5-8]halothane anesthesia should impair this expansion. However, we found in a previous study that inspiratory rib cage expansion during both quiet and stimulated breathing was not markedly impaired in humans anesthetized with 1 MAC end-tidal halothane. [2,3]We posited two possible explanations for this finding.
First, other muscles that act to expand the rib cage, such as the scalene muscles, [9-11]may have been active during halothane anesthesia. Activity in the scalenes has not yet been sought during halothane anesthesia. Second, halothane anesthesia enhances EMG activity in muscles with expiratory actions such as the internal intercostal and transversus abdominis muscles. [2,3,12-14]This expiratory activity may contribute to rib cage expansion in the following manner. During expiration, this activity should reduce thoracic volume below its relaxed volume (i.e., the thoracic volume in the absence of any muscle activity). At the onset of inspiration, activity in these expiratory agonists ceases, and the chest wall (including the rib cage) passively expands to approach its relaxed volume. Inspiratory agonists such as the diaphragm are then activated to complete the inspiration. In this way, expiratory muscle activity can contribute to inspiratory rib cage expansion. This phenomenon is well-documented in quadrupeds such as the dog. [15-19]However, its possible significance in humans during halothane anesthesia is unknown; the mere presence of EMG activity in a muscle does not signify that the muscle actually has a mechanical effect (in this case to reduce end-expiratory thoracic volume).
This enhancement of expiratory muscle activity by halothane may also contribute to the reduction in the functional residual capacity (FRC) produced by halothane anesthesia. Activity in expiratory agonists of the abdomen may increase abdominal pressure and produce cephalad diaphragm displacement, and intrinsic expiratory agonists may constrict the rib cage. [20-22]Previous studies have suggested that FRC during halothane anesthesia is similar during anesthesia with spontaneous breathing and anesthesia-paralysis with mechanical ventilation. [23-25]Based on these findings, it has been concluded that any expiratory muscle activity during spontaneous breathing does not have significant mechanical effects to reduce FRC. However, it is now clear that mechanisms responsible for anesthetic-induced reductions in FRC are complex, [2,26-29]and that measurements of FRC alone are not sufficient to characterize anesthetic effects on a particular chest wall structure. For example, changes in FRC produced by anesthesia may in part be related to changes in the volume of blood in the thorax. .
The primary goal of this study was to explore mechanisms responsible for the findings of our previous work by estimating the mechanical significance of the expiratory muscle activity produced by halothane anesthesia in humans. We hypothesized that this activity reduces thoracic volume below its relaxation volume, thus contributing to inspiratory rib cage expansion and reductions in FRC. To test this, we compared chest wall configuration at end-expiration, measured with fast three-dimensional computed tomography, during three conditions: (1) wakefulness, (2) spontaneous breathing in subjects anesthetized with halothane, and (3) paralysis and mechanical ventilation in subjects anesthetized with halothane. We reasoned that the mechanical actions of expiratory muscles could be inferred by comparing chest wall configurations during spontaneous breathing with the configuration in the absence of muscle activity (i.e., paralysis and mechanical ventilation). To better interpret these results, we further checked for scalene muscle activity during halothane anesthesia that might also contribute to inspiratory rib cage expansion. This activity was sought both during quiet breathing and during hyperpnea induced by the rebreathing of expired gas.
Materials and Methods
This study was approved by the Institutional Review Board. Six healthy subjects (3 male, 3 female) were studied after informed consent was obtained (Table 1). Each subject had a complete physical examination, including pulmonary function tests, which were normal, and was brought to the laboratory the day before the actual experiment for familiarization with experimental procedures. Female subjects had a negative pregnancy test the day before the study. The subjects were not allowed oral fluids after midnight the day before the experiment.
All studies were performed with subjects supine. Respiratory impedance plethysmography (RIP) belts (Respitrace, Ardsley, NY) were placed around the upper rib cage and mid abdomen. An intravenous catheter was inserted, and the radial artery was cannulated to obtain samples for blood gas analysis (IL 1302, Instrumentation Laboratories, Lexington, MA) and for blood pressure monitoring.
Bipolar electromyogram electrodes were inserted into several respiratory muscles. [2,3]The electrodes were fashioned by removing 1 mm of insulation from the end of 0.002-inch polytetrafluorethylene-insulated wires. Two wires were passed through an insulated 30-G needle, then bent 1 mm from the end to form hooks. The electrodes were inserted under ultrasonic guidance [2,21]while monitoring electrical activity. After placement in the desired location, the needle was removed, leaving the wires in the desired muscle. Electrodes were placed in the transversus abdominis muscle at the anterior axillary line approximately 4 cm inferior to the costal margin, the parasternal intercostal muscle at the third right interspace, approximately 3 cm lateral to the midline, and the right anterior scalene muscle near the base of the neck. After removal of the introducing needles, the subjects noted no sensation from the electrodes. Electromyographic signals were amplified (Grass P511), band-pass filtered between 30 and 3000 Hz, and recorded both on a strip chart recorder (Astromed MT9500) and on digital audio tape (TEAC RT100) for later processing.
The RIP bands were calibrated using the method of Mankikian et al. In this method, changes in dimensions of the rib cage and abdomen measured with the RIP bands are related to the volumes displaced by the rib cage and diaphragm-abdomen (referred to hereafter as abdominal) compartments during tidal breathing. These relationships are expressed as volume-motion coefficients of the rib cage and abdomen. These coefficients are calculated from data obtained by asking the subjects to alternate predominately abdominal and thoracic breathing (while awake) or after transient airway obstruction (while anesthetized). Calibrations were performed at the beginning and end of each experimental condition (awake and anesthetized), and average values were calculated for each condition.
Subjects breathed through a mouthpiece and nose clip during awake measurements. As in our previous study, this apparatus did not change the pattern of breathing (data not shown). Inspiratory and expiratory gas flows were measured using a pneumotachograph (Fleisch 3) connected to a differential pressure transducer (Validyne MP-45). Gas flows were integrated to obtain changes in lung volume, and were corrected to BTPS (body temperature, pressure standard) conditions. The electrocardiogram, blood pressure, and arterial oxygen saturation were monitored throughout the study.
After instrumentation, each subject breathed quietly for several minutes to establish a stable pattern of breathing. They were then quickly connected to a 7-l bag containing 7% CO2, 93% O2(awake measurements) or 8% CO2, 91% O2, and 1% halothane (anesthetized measurements). Carbon dioxide concentration in the bag was continuously monitored by an infrared analyzer and expressed as a PCO2(Nelcor N-2500). The different initial carbon dioxide concentrations were used to promote rapid equilibration between blood and bag PCO2and to standardized the rate of rise of PCO2in awake and anesthetized conditions. Rebreathing continued until PCO2in the bag increased by approximately 10-15 mmHg. Arterial blood gases were obtained before and at the conclusion of rebreathing.
Each subject was then placed in the dynamic spatial reconstructor (DSR), a high-speed X-ray scanner that uses the computed tomography principle to provide three-dimensional images of the thorax. This technique has been described in detail elsewhere. [2,16,28,29]The DSR has sufficient temporal resolution to image thoracic structures during quiet breathing and sufficient volume resolution to determine a known volume to within 2%.
Dynamic Spatial Reconstructor images were obtained while the awake subject breathed a gas mixture of 30% Oxygen2and balance nitrogen. Scans of 300 ms duration were triggered manually at end-expiration during three consecutive breaths and gated together during later analysis. Because the cephalocaudal height of the imaging field was not sufficient to include the entire thorax, these initial scans included only the superior half of the thorax. The subject was then shifted cephalad, and a similar sequence of scans was obtained to image the inferior portion of the thorax. Respiratory impedance plethysmography measurements, tidal volume, and EMGs were recorded simultaneously to ensure stability of the breathing pattern. During subsequent analysis, the superior and inferior images were joined to produce end-expiratory images of the entire thorax.
Immediately after scanning, the FRC was measured in duplicate using a nitrogen dilution technique. [2,19,32]Each subject performed six vital capacity maneuvers into a 4-l bag initially filled with 100% Oxygen2after the bag was connected to the mouthpiece at end-expiration. Nitrogen concentrations in the bag were determined before and after this maneuver by mass spectrometry (Perkin-Elmer MGA 1100, Buffalo Grove, IL).
Anesthesia was induced with inhalational halothane, using an oral airway to maintain airway patency as necessary. The trachea was intubated with a 9.0 mm ID endotracheal tube during deep halothane anesthesia, then the inspired halothane concentration was adjusted to maintain approximately 1 MAC end-tidal concentration in a 30% Oxygen2, balance nitrogen mixture. Esophageal and gastric balloons were placed in the mid-esophagus and stomach, respectively, and these measurements were validated by standard techniques. An additional EMG electrode was placed in the internal intercostal muscle at the 9th left interspace in the mid-axillary line. After the pattern of breathing had stabilized, measurements were repeated as performed while the subject was awake, including carbon dioxide rebreathing, DSR scans during quiet breathing, and FRC measurements (using passive inflation).
After these measurements, 0.1 mg/kg vecuronium was administered, and complete neuromuscular blockade was confirmed by absence of a response to peripheral ulnar nerve stimulation. The lungs were mechanically ventilated using a tidal volume and breathing frequency matched to that observed while awake and breathing quietly. The thorax was then scanned at end-expiration, and measurements of FRC were performed.
After these measurements, the neuromuscular blockade was reversed and the subject was allowed to emerge from anesthesia. No untoward effects were observed.
Details of image processing to define chest wall boundaries and validation of the DSR in measuring chest wall motion have been previously described. [2,16,17,19,28]To summarize, each scan produced a three-dimensional volume image of the thorax composed of cubic volume elements (voxels) with edge lengths of 1.3 mm. Images were processed to define each voxel in the image as being in the thoracic cavity, the abdominal cavity, or the background. Thoracic volume (Vth) was determined by counting the number of voxels in the thoracic cavity above the diaphragm. Changes in thoracic liquid volume (Delta Vliq) at end-expiration, presumably representing changes in thoracic blood volume, were calculated as the difference between changes in Vthand changes in FRC measured by nitrogen dilution (Delta Vliq= Delta Vth- Delta FRC). Changes in Vthbetween any two scans were partitioned into volumes displaced by the motion of the diaphragmatic and rib cage surfaces as previously described. [2,16].
Changes in the volumes of the heart and major vessels were also estimated directly from these images. The heart and other mediastinal structures were isolated in each image using a combination of computer thresholding and operator interaction. The pulmonary vessels were truncated at approximately the same location in all scans from each subject. The total volume of these mediastinal structures was measured by counting the number of voxels within these structures and multiplying by the volume of one voxel.
Compartmental volume displacements of the rib cage and abdomen during inspiration, defined as the period of inspiratory gas flow, were computed from RIP measurements. [30,31]Comparable measurements were not performed using the DSR because of limitations of allowable radiation in these human subjects. We have previously shown that RIP measurements are sufficient to determine the pattern of anesthetic-induced changes in the relative contributions of these compartments to the tidal volume, even though they do not represent the actual volumes displaced by the rib cage and diaphragm. .
Statistical comparisons were made by paired t tests and a P < 0.05 was considered significant.
Consistent activity was noted in the scalene and parasternal intercostal muscles while awake (Figure 1and Table 2). This activity was phasic, occurring primarily during inspiration (with the exception of subject 3, who exhibited tonic activity in the scalene muscle during quiet breathing). No activity was observed in the transverse abdominis muscle during quiet breathing while awake (Figure 1), but rebreathing consistently produced phasic expiratory activity in this muscle (Table 2).
During quiet breathing while anesthetized with 0.9+/- 0.1% (M+/-SE, approximately 1.2 MAC) end-tidal concentration of halothane, phasic inspiratory activity was present in the scalene muscles of the three female subjects and one of the male subjects (Figure 1and Table 2). All anesthetized subjects exhibited phasic activity in the scalene muscles at the conclusion of rebreathing (Figure 2and Table 2). Phasic inspiratory activity in the parasternal intercostal muscle during quiet breathing persisted during anesthesia in the three female subjects (Figure 1), and was enhanced by rebreathing. Activity was never observed in the parasternal intercostal muscles of the three male subjects (Table 2).
During quiet breathing while anesthetized, phasic expiratory activity was observed in the transversus abdominis muscles of the three male subjects (Figure 2and Table 2). Transient phasic activity was noted in the transversus abdominis of the female subjects during induction; however, this activity did not persist once a stable level of anesthesia was achieved (Figure 1and Table 2). Rebreathing produced transversus abdominis expiratory activity in the female subjects (Table 2) and enhanced activity in the male subjects (Figure 2). The internal intercostal muscle was also monitored during anesthesia. Activity was never noted in the female subjects, but was present in two male subjects during quiet breathing, and all three male subjects during rebreathing (Figure 2and Table 2).
Chest Wall Motion
Quiet Breathing. Halothane anesthesia significantly increased breathing frequency and decreased tidal volume (Table 3). Halothane anesthesia significantly decreased the absolute volumes displaced by both rib cage and abdomen, but did not significantly change the relative contribution of the rib cage or abdominal compartments to tidal volume.
Carbon Dioxide Rebreathing. Halothane anesthesia significantly reduced the slope of the response of expiratory minute ventilation to carbon dioxide (from 2.21+/-0.34 to 1.49+/-0.35 l *symbol* min sup -1 *symbol* mmHg). The expiratory minute ventilation at an expired PCO2of 55 mmHg was also significantly reduced by halothane anesthesia (from 40.4+/-7.5 to 6.7+/-3.7 l *symbol* min sup -1).
Minute ventilation of the rib cage and abdominal compartments was computed as the product of compartmental tidal volume (measured by RIP) and breathing frequency. Halothane anesthesia significantly decreased the rib cage response to carbon dioxide, quantified as the slope of the linear regression of this relationship between compartmental minute ventilation and PCO2measured in the rebreathing bag, but did not significantly change the abdominal response (Table 4). This analysis does not take into account that these responses were measured over different ranges of tidal volumes, tidal volumes being smaller during halothane anesthesia. To evaluate compartmental contributions at comparable tidal volumes, the compartmental volume displacements at a V sub T of 1.2 l were estimated using linear regression parameters of compartmental tidal volumes versus total tidal volume over the rebreathing period. Halothane anesthesia did not significantly change the estimated contribution of the rib cage at a VTof 1.2 l (Table 5).
Phase relationships between rib cage and abdominal motion were also analyzed. While awake, rib cage and abdominal movements were synchronous over the course of rebreathing, with both compartments expanding in concert (data not shown). During halothane anesthesia, paradoxical rib cage motion during quiet breathing developed in subjects 1 and 2; that is, the rib cage continued to expand during the first portion of expiratory gas flow (Figure 3). Rebreathing produced paradoxical rib cage motion in every subject except #3. Rebreathing also changed the phase relationship between rib cage and abdominal movements (as shown by the widened loops in Figure 3), especially in subjects 2 and 6.
Functional Residual Capacity
When compared with the awake condition, halothane anesthesia significantly decreased the FRC measured by nitrogen dilution (Table 6). The amount of this decrease did not differ between spontaneous breathing and mechanical ventilation with paralysis (-335+/-75 and -348 +/-67 ml, respectively). However, the mechanisms responsible for this decrease were dependent on the mode of ventilation.
The following comparisons concern subjects breathing spontaneously before and after the induction of halothane anesthesia (Table 6). Halothane anesthesia significantly decreased the end-expiratory intrathoracic volume (Vth), measured with the DSR. Most of this change was produced by a significant net inward motion of the rib cage at end expiration. The pattern of this motion was variable among subjects (Figure 4). In all subjects, the most dependent regions of the diaphragm moved cephalad and the most nondependent regions of the diaphragm moved caudad (Figure 5). However, these changes in end-expiratory diaphragm position did not significantly contribute to the reduction in Vthproduced by halothane during spontaneous breathing (Table 6). In five of the six subjects, halothane anesthesia increased both Vliqand mediastinal structures (Table 6). These findings suggest that halothane anesthesia increased intrathoracic blood volume in these subjects, a factor that would contribute to decreases in FRC.
The following comparisons concern anesthetized subjects breathing spontaneously and after the onset of paralysis and mechanical ventilation (i.e., the effects of abolishing all respiratory muscle activity in anesthetized subjects; Table 6). Paralysis did not significantly affect the mean FRC when all subjects were analyzed together. However, there were marked differences between sexes in the effects of paralysis. Paralysis increased the FRC in the three male subjects (1, 2, and 4) and decreased the FRC in the three female subjects (3, 5, and 6). This resulted from the interaction of the three factors controlling the FRC: rib cage position, diaphragm position, and intrathoracic blood volume.
In each subject, paralysis caused an outward motion of the rib cage at end expiration, greatest in the three male subjects (Table 6and Figure 4). Paralysis also produced a small but significant cephalad motion of the diaphragm (Table 6and Figure 5). The interaction of these changes was such that paralysis increased total thoracic volume in all three male subjects (by 159+/-30 ml), whereas there was little change in thoracic volume in the female subjects (-9+/-13 ml). Paralysis significantly increased the intrathoracic blood volume, estimated by both Vliqand mediastinal structures. In the three male subjects, increases in Vthwere greater than increases in Vliq, and the FRC increased. In the three female subjects, increases in Vliqwere greater than increases in Vth, and the FRC decreased.
Because rib cage and diaphragm position depend on the positions of their attachments, the curvature of the thoracic spine in the sagittal plane was analyzed by tracing the anterior borders of the thoracic and upper lumbar vertebrae. This curvature consistently was increased by halothane anesthesia (Figure 6); paralysis had no additional effect.
The principal findings of this study are that, in subjects anesthetized with 1.2 MAC end-tidal halothane: (1) there were marked interindividual differences in respiratory muscle use during quiet breathing that may be related to sex, (2) phasic inspiratory scalene and parasternal intercostal muscle activity may contribute to inspiratory rib cage expansion in some subjects, and (3) when present, expiratory muscle significantly constricts the rib cage and contributes to reductions in FRC caused by halothane anesthesia.
Our approach was to infer the mechanical actions of expiratory muscle activity present during halothane anesthesia by comparing the end-expiratory chest wall configuration before and after the abolition of all muscle activity by pharmacologic paralysis. This approach assumes the absence of tonic activity in inspiratory muscles during anesthesia, which has not been observed in this or previous studies. [1-3,34]This information gives insight into the possible contribution of expiratory muscle activity to reductions in the FRC. It also allows estimation of the maximum possible contribution of this activity to inspiratory rib cage expansion as expiratory activity ceases at the onset of inspiration.
Respiratory Muscle Activation and Chest Wall Motion
In our previous study, we noted that inspiratory rib cage expansion was relatively well preserved during halothane anesthesia despite the virtual absence of activity in the parasternal intercostal muscles, which normally have an important inspiratory action on the rib cage. This finding was surprising, given that isolated diaphragm contraction constricts the upper rib cage by decreasing intrathoracic pressure. [11,20,35]In that study (and the current one), a 9.0-mm ID endotracheal tube was used to minimize any effects of increased upper airway resistance on chest wall motion. In clinical practice, increased resistance produced by smaller endotracheal tubes or partial upper airway obstruction in nonintubated patients may hinder rib cage expansion. We speculated that the release of expiratory muscle activity at the onset of a breath was important in maintaining inspiratory rib cage expansion. Indeed, if it could be demonstrated that no activity was present in other muscles that expand the rib cage, such as the scalene muscles, then this expiratory activity could be assigned a principal role in maintaining inspiratory rib cage expansion during halothane anesthesia.
However, contrary to expectations, we found differences in the patterns of respiratory muscle use during quiet breathing among anesthetized subjects, differences that were associated with the sex of the subject. Male subjects exhibited prominent phasic expiratory muscle use during quiet breathing, with no parasternal intercostal muscle activity and scalene muscle activity in only one of the three subjects. In contrast, expiratory muscle activity was absent in anesthetized female subjects during quiet breathing, whereas parasternal intercostal and scalene muscle activities were preserved. All subjects developed phasic expiratory activity in the transversus abdominis and phasic inspiratory activity in the scalene muscles during rebreathing, but parasternal intercostal activity remained absent in the male subjects. The numbers of subjects are insufficient to conclude that sex was causal, although we note that the pattern of results in the male subjects is consistent with the results in our previous study of six male subjects. [2,3]For the sake of subsequent discussion, we will classify these patterns according to sex, although we can only conclude now that there is substantial interindividual variability in the pattern of respiratory muscle use during halothane anesthesia that may be related to sex.
The mechanisms responsible for these apparent sex differences are unknown. Progesterone is known to affect ventilatory control, but there is little information about sex-related differences in specific patterns of respiratory muscle use. Subjects 5 and 6 were taking low-dose oral contraceptives, and subject 3 had undergone oophorectomy, so that significant increases of estrogen or progesterone concentrations are unlikely. The original study documenting consistent phasic expiratory muscle activity during nitrous oxide or halothane anesthesia was performed in males. A subsequent study of subjects anesthetized with thiopental and nitrous oxide that included females noted that expiratory activity did not develop in all subjects, but the presence of such activity did not seem to depend on sex. Activity persisted when halothane was added to the inspired gas. Previous studies of parasternal intercostal or scalene muscle activity during anesthesia are limited. Tusiewicz et al. found no parasternal intercostal muscle activity in three subjects (sex not specified) anesthetized with halothane during quiet breathing. Drummond found that enflurane administered for a brief period shortly after thiopental induction abolished parasternal and scalene muscle activity in five subjects (sex not specified).
Differences in the EMG pattern of respiratory muscle use among subjects often were not reflected in the patterns of chest wall motion measured using RIP. For example, during quiet breathing, no consistent differences between anesthetized males and females were observed in the relative contribution of the rib cage to tidal volume (Table 3). Scalene activity, which may have contributed to rib cage expansion, was present in one male subject (#4) during quiet breathing. Studies in quadriplegic subjects have demonstrated that scalene muscle activity can have an important inspiratory action on the upper rib cage. The lack of such activity in the other two male subjects (1 and 2), and the absence of parasternal intercostal activity, suggests that phasic expiratory activity in rib cage muscles such as the internal intercostals contributed significantly to inspiratory rib cage expansion in these two subjects. However, it appears that this activity was not sufficient to produce normal patterns of chest wall motion, because these two subjects exhibited paradoxical rib cage expansion during the early part of expiration (Figure 3). The maintenance of rib cage expansion during halothane anesthesia in the female subjects can be attributed to activity in the scalene and parasternal intercostal muscles.
Rebreathing promoted scalene and transversus abdominis activity in both males and females; parasternal intercostal activity remained absent in the males. The effect of halothane anesthesia on the response of minute ventilation and the compartmental responses of rib cage and abdomen were consistent with previous work. [1,3]No consistent sex-related differences in the rib cage ventilatory response, the rib cage contribution to tidal volume at a VTof 1.2 l, or phase differences between rib cage and abdominal motion were noted. This result suggests that the combination of expiratory muscle activity and scalene activity can maintain rib cage expansion during hyperpnea in anesthetized subjects, with or without parasternal intercostal activity. However, as noted in our previous study, rib cage motion during hyperpnea induced by rebreathing was not entirely normal, as most subjects (including two female subjects with parasternal intercostal muscle activity) developed paradoxical outward motion of the rib cage during early expiration.
Reductions in Functional Residual Capacity
Previous studies have noted little difference between reductions in the FRC produced by anesthesia with spontaneous breathing and anesthesia with paralysis and mechanical ventilation, and have concluded that expiratory muscle activity produced by anesthesia does not contribute to reductions in the FRC. [23-25]However, our results demonstrate that mechanisms producing reductions in FRC are complex, and that the mechanical effects of respiratory muscle activity cannot necessarily be inferred from changes in the FRC. We consider the three primary factors controlling the FRC: rib cage position, diaphragm position, and intrathoracic blood volume.
Rib Cage. Three mechanisms have been advanced to explain decreases in end-expiratory rib cage dimensions produced by anesthesia: abolition of tonic activity in inspiratory agonists, changes in the configuration of structures attached to the rib cage (e.g., the thoracic spine), and active constriction of the rib cage by expiratory muscle activity produced by anesthesia. Consistent with our previous study, no tonic activity was present in the parasternal intercostal muscles while subjects were awake. Tonic activity was noted in the scalene muscle of only one subject. Thus, although the existence and importance of tonic activity in inspiratory agonists has been controversial, [7,34]these results suggest that constriction of the rib cage caused by anesthesia does not result from abolition of this activity. Halothane anesthesia with spontaneous breathing increased the curvature of the thoracic spine in the sagittal plane, a finding that confirmed our previous results. The addition of paralysis did not further change thoracic curvature, making this an unlikely source of additional changes in rib cage configuration produced by paralysis. This increase in curvature may contribute to rib cage constriction (Figure 6). [2,37]Phasic expiratory activity was present in abdominal and rib cage muscles during quiet breathing in the male subjects. This activity had a clear expiratory effect on the rib cage, producing end-expiratory constriction of the rib cage, which was abolished by paralysis. The source of this action was most likely intrinsic rib cage muscles such as the internal intercostal or the triangularis sterni muscles. [8,14,20,22]Paralysis also produced a small amount of rib cage expansion in female subjects. This finding may imply the presence of some expiratory activity that was not measured in our EMG electrodes. Alternately, this expansion may have in part accommodated increases in intrathoracic blood volume produced by paralysis. .
Diaphragm. Although earlier indirect studies suggested that a cephalad motion of the end-expiratory position of the diaphragm contributed to reductions in the FRC produced by anesthesia, [27,39]studies examining the entire diaphragm have consistently failed to find a significant contribution. [2,28,29,40]Rather, anesthesia consistently changes the shape of the diaphragm in subjects lying supine, with cephalad motion of the most dependent regions and a caudad motion of the most nondependent regions. The current study confirmed this pattern. Phasic expiratory activity in the transversus abdominis muscle should increase end-expiratory abdominal pressure and tend to produce cephalad diaphragm displacement. Abolition of this activity should decrease abdominal pressure and promote caudad motion of the end-expiratory position of the diaphragm. However, the opposite result was observed, with paralysis producing a small but significant cephalad motion of the diaphragm. Thus, it appears that phasic activity by the transversus abdominis muscle during halothane anesthesia does not have a significant mechanical effect on diaphragm position. The mechanism of this small cephalad motion of the diaphragm produced by paralysis is unclear. Changes in end-expiratory muscle tone of the diaphragm are unlikely, as there is little evidence for the existence of such tone either while awake or anesthetized. [2,7,41]Diaphragm position would be affected by changes in intrathoracic or abdominal pressures; however, paralysis did not produce significant changes in either esophageal or gastric pressures measured at end expiration (changes of -0.3+/-1.0 and 0.2+/-0.3 mmHg, respectively).
Intrathoracic Blood Volume. Previous studies have suggested that anesthesia may change the end-expiratory intrathoracic blood volume, although the magnitude and direction of this change have been controversial. [2,27,29]We previously reported that halothane anesthesia with spontaneous breathing did not significantly increase Vliq, a finding consistent with the current results. Krayer et al. reported that thiopental-narcotic anesthesia with paralysis and mechanical ventilation significantly increased intrathoracic blood volume compared with wakefulness, which is also consistent with our findings during paralysis. Thus, significant increases in Vliqdo not appear to be associated with anesthesia per se, but with the addition of paralysis and mechanical ventilation. Such increases contribute to reductions in the FRC. The mechanism responsible for this finding is unclear, but may be related either to pharmacologic effects of paralysis on the cardiovascular system (although such effects are thought to be minimal for vecuronium) or to differences in heart-lung interaction related to differences in the pattern of intrathoracic pressure changes between spontaneous breathing and mechanical ventilation.
In summary, we found significant interindividual variability in the pattern of respiratory muscle activity during spontaneous breathing of 1.2 MAC end-tidal halothane that may be related to sex. When present, expiratory muscle activity in anesthetized subjects significantly constricts the rib cage, contributing both to reductions in FRC and to subsequent inspiratory rib cage expansion. Rib cage expansion during anesthesia may also be aided by phasic inspiratory activity in other extradiaphragmatic muscles. Reductions in the FRC produced by halothane result from the complex interaction of several factors that differ depending on the presence and pattern of respiratory muscle activity.
The authors thank Kathy Street and Darrell Loeffler, for technical assistance; Janet Beckman, for secretarial support; Dr. Brad Narr, for performing preanesthetic medical evaluations; Don Erdman and Mike Rhyner, for operating the dynamic spatial reconstructor; Dr. Bill Lichty and Dr. Michael Joyner, for assistance with electromyogram techniques; and Dr. Jamil Tajik, for assistance with ultrasonography.