Chest wall and trunk muscle activity during inspiratory loading S. J. CALA,
J. EDYVEAN,?
Thorucic Medicine
AND
Unit, Westmeud
L. A. ENGEL?? Hospital,
Westmead,
New South Wales 2145, Austruliu
CALA, S. J., J. EDYVEAN, AND L. A. ENGEL. Chest wall and trunk muscle activity during inspiratory loading. J. Appl. Phys-
CWT electromyograms (EMGs) increased, in a manner similar to that of the Ps muscles, as the generated inspiraiol. 73(6): 2373-2381, 1992.-We measured the electromyotory muscle pressure (Pmus) increased. However, for a graphic (EMG) activity in four chest wall and trunk (CWT) given Pmus all EMG activity increased with increasing muscles,the erector spinae, latissimusdorsi, pectoralis major, and trapezius, together with the parasternal, in four normal lung volume. There was no difference in the Pmus-EMG between upright and supine positions for subjectsduring gradedinspiratory efforts against an occlusion relationship any of the muscles examined. This is evidence against in both upright and seatedpostures. We also measuredCWT that the CWT muscles are recruited EMGs in six seatedsubjectsduring inspiratory resistive load- the possibility ing at high and low tidal volumes [1,280? 80 (SE) and 920st 60 merely to maintain posture and/or preserve orientation ml, respectively]. With one exception, CWT EMG increasedas of the trunk with respect to the gravitational field in a function of inspiratory pressuregenerated (Pmus) at all lung upright subjects. Our findings are consistent with the hyvolumes in both postures,with no systematic difference in re- pothesis that the CWT muscles contribute actively to cruitment betweenCWT and parasternal musclesasa function inspiratory pressure generation.
of Pmus. At any given lung volume there was no consistent difference in CWT EMG at a given Pmus betweenthe two postures (P > 0.09). However, at a given Pmus during both graded inspiratory efforts and inspiratory resistive loading, EMGs of all musclesincreasedwith lung volume, with greater volume dependence in the upright posture (P < 0.02). The results suggest that during inspiratory efforts, CWT musclescontribute to the generation of inspiratory pressure. The CWT muscles may act asfixators opposingdeflationary forces transmitted to the vertebral column by rib cagearticulations, a function that may be lesseffective at high lung volumesif the direction of the muscularinsertions is altered disadvantageously.
METHODS Study A
Four normal subjects were studied in both the seated and supine postures. In the upright posture, subjects sat in a dental chair with the head supported, maintaining a fixed position of head, neck, and trunk. In the supine position, the subject’s trunk and extended arms rested on a firm board covered by foam rubber padding. The board overlay the backrest of the chair that had been rotated to respiratory muscles; electromyograms; accessory muscles; the horizontal plane. The head, neck, and shoulders were completely supported by a bean bag and pillow. The exloaded breathing perimental setup is shown in Fig. 1. First, maximal inspiratory efforts against an occluded airway were performed three times in a random seBREATHING EFFORTS against external inspiratory loads are associated with activity of inspiratory muscles, such quence, at 20% vital capacity (VC) increments, from reas the diaphragm and parasternal (Ps) and external in- sidual volume (RV) to total lung capacity (TLC) (Table I). Then, after inspiration to TLC, the subject expired to tercostals (18, 19). However, inspiratory effort-related a predetermined lung volume, relaxed, and made a subactivity has also been described in a variety of other musmaximal graded ramp like inspiratory effort against an cles that attach to the chest wall and trunk (CWT), occluded airway up to -500% maximal inspiratory presnamely the erector spinae (ES) (2, 12), latissimus dorsi sure at that lung volume (Fig. 2). The graded inspiratory (LD) (12), pectoralis major (PM) (12,16,17), and trapeefforts were also performed at increments of 20% of VC zius (Tr) (8, 22). These muscles have a wide range of functions, including the maintenance of posture and par- in random order and were repeated at least three times at ticipation in a variety of volitional motor tasks (11, 23) each lung volume in each subject. Both maximal and graded efforts were performed first in the upright and but are not conventionally regarded as having an importhen in the supine position. We used TLC as a common tant role in respiration. To examine the degree and pattern of participation of these muscles in respiratory acts, volume of reference for both postures. Flow was measured with a pneumotachograph, and the we studied the electrical activity in the CWT muscles, signal was integrated to obtain lung volume. Mouth prestogether with that of the Ps, an inspiratory muscle, in sure was measured by a pressure transducer (Validyne) normal subjects during graded inspiratory efforts against an occluded airway in both the upright and supine pos- connected to the mouthpiece by a side port. EMGs were ture. We found that at any given lung volume all the measured from the Ps in the second and third intercostal space, ES muscles from the region adjacent to the T,-T, t Deceased 27 October 1991. ttDeceased 7 February 1992. vertebral space, LD muscles 2-3 cm caudolateral to the 0161-7567/92 $2.00 Copyright 0 1992 the American Physiological Society
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MUSCLE
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INSPIRATORY
Mouth km
EFFORTS
Pressure Hz01
Erector
Spinao MTA
1
\
A B FIG. 1. Study A: D, 3-way tap, closed during graded inspiratory efforts; E, fine-wire bipolar electrodes. Study B: R, variable resistance; F, surface bipolar electrodes; Pm, differential transducer for pressure measurements at mouth; C, pneumotachograph; MTA-EMG, moving time-averaged electromyogram of chest wall and trunk (CWT) muscles.
tip of the scapula, PM muscles 3-4 cm craniolateral to the nipple, and Tr muscles midway between the spinous process of C, and the acromion. The bipolar EMG electrodes were made of 75ym insulated stainless steel wire (Cooner Wire) that was bared for -1 mm from the tip. They were inserted under sterile conditions using 25 gauge hypodermic needles. Once through the skin the electrode was connected to its amplifier, and the signal was monitored as the needle was advanced slowly to the required position. For Ps electrodes, the muscle was considered to be inspiratory when it recorded action potentials with characteristics of single motor units during natural or voluntary inspiration but not during maneuvers designed to activate nearby muscles. Ps intercostal muscles were sampled in the second or third interspace 2-3 cm lateral to the border of the sternum after penetrating the pectoral muscles, which were activated by adduction of the arm against a resistance. The Ps muscles are superficial to the transversus thoracis, which could be recruited by exhalation below functional residual capacity (FRC) (9). Electrodes that penetrated deeply enough to record motor unit potentials from this muscle were not used for the study. The ES was activated by asking the
LatlWmus MTA
Dorsl
Trapezius MTA
FIG. 2. Representative data obtained inspiratory effort at 80% vital capacity sistive breathing (B). MTA, moving-time
in subject JE during graded (A) and during inspiratory reaverage.
subject to extend the spine, the LD was activated by extension of the outstretched arm, the PM was activated by adduction of the arm, and the Tr was activated by elevation of the shoulders, all against resistance. Once the electrodes were in position, the needles were withdrawn, and wires were left in place. EMGs were band-pass filtered (loo-2,000 Hz), rectified, and smoothed with a leaky integrator (time constant of 200 ms). The raw signals were displayed on a storage oscilloscope (Tectronix). All signals were recorded on a Hewlett-Packard eight-channel strip chart recorder and stored on FM tape for analysis. Study B
TABLE
1. Anthropometric
data Pmax,cmH,O
Subj
Age, yr
AT JE
36 42
SC TB
32 29
HC
3’7
JW
33
Ht, cm
FRC,
VC,
Sex
liters
liters
F M M M M M
152 182 180 181 178 180
2.83 3.87 4.31 3.31 3.65 3.10
3.95 5.85 6.40 5.57 5.50 5.88
40% VC
60% VC
80% VC
100% VC
92 110 145 120
86 75 105 110
55 65 96 96
34 36 56 54
Subjects AT, JE, SC, and TB were common to studies A and B. FRC, functional residual capacity; VC, vital capacity; Pmax, maximum pressure generation by inspiratory muscles at different lung volumes; F, female; M, male.
In six seated normal subjects (4 from study A and 2 additional subjects), we also measured the EMG of the ES, LD, PM, and Tr muscles using bipolar surface electrodes during external inspiratory resistive loading. In each subject two runs were performed, generating identical inspiratory mouth pressures but with different tidal volumes, resulting in different end-inspiratory volumes. This study was performed to assessseparately the volume dependence of the EMG-Pmus relationship under dynamic conditions of inspiratory resistive breathing from FRC. With the use of the same surface landmarks as in study A, bipolar electrodes were placed on the skin overlying the CWT muscles. The subject inspired through the resis-
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2375
EFFORTS
resistive loading at the lower lung volume. The result for each muscle was averaged to obtain the change in mean EMG per 500 ml increase in lung volume. 60%VC
RESULTS
Study A
10
20
30
Pmus ( cm HzO) FIG. 3. Erector spinae muscle EMG activity plotted vs. pressure generated by inspiratory muscles (Pmus) in subject AT in upright posture during 3 graded inspiratory efforts at 2 lung volumes. Note reproducibility of Pmus-EMG relationships at each lung volume. VC, vital capacity; AU, arbitrary units.
tance (R in Fig. 1) via a three-way tap (D in Fig. 1). Expiration was unloaded. The target mouth pressure was attained quickly and maintained constant for the required time before relaxation, thereby achieving a square-wave pattern of breathing. This was facilitated by displaying mouth pressure to the subject on an oscilloscope screen (Fig. 1). The variable resistance was adjusted so that the predetermined pressure was associated with a given inspiratory flow rate. The inspiratory duration, expiratory duration, and frequency were controlled by the subject with the aid of a metronome. Hence, for a given inspiratory flow rate, tidal volume was determined by inspiratory duration. Each subject performed inspiratory resistive loaded runs with both a high and a low tidal volume (1,280 t 80 and 920 t 60 ml, respectively). Each run consisted of 10 reproducible breaths, and high and low runs were matched for breathing frequency, mean inspiratory mouth pressure (51 t 3% of maximum at FRC), and mean inspiratory flow rate. Hence, during high runs inspiratory time was slightly longer.
At each lung volume, in both postures, graded inspiratory efforts against an occluded airway resulted in a progressive increase in the electrical activity (MTA-EMG) of the Ps, as well as the ES, LD, PM, and, with the exception of one subject in the supine posture, the Tr muscles. The relationship between EMG and Pmus was curvilinear and concave upward in the majority of cases. The shape was reproducible at a given lung volume in the 40% VC to TLC range (Fig. 3). Direct comparisons of CWT muscle EMG with that of the Ps showed a consistently monotonic relationship (Fig. 4). Although in some cases at low Pmus, the rate of CWT muscle recruitment appeared relatively less than that of the parasternals (curvilinear relationship concave upward), this was not consistently so. In some cases a linear relationship was seen, and in others it was concave downward, i.e., relatively greater rate of recruitment of the CWT than Ps muscles at low Pmus. There was no difference in the Pmus-EMG relationships between upright and supine postures at any lung volume for any of the muscles examined. In both postures at a given Pmus, integrated activity of the muscle groups increased with increasing lung volume (Figs. 5-8) from 40% VC to TLC. The curves obtained at RV and 20% of VC were highly variable and did not demonstrate this relationship to lung volume. In some subjects the EMG-Pmus curve at one volume overlapped ES __t_ d -
AT JE SC 7-B
Data Analysis Study A. At each lung volume the integrated EMG was plotted vs. inspiratory Pmus, taken as the change in mouth pressure from that during relaxation. We compared the EMG at 40% VC to that at 80% VC at a level of Pmus corresponding to 50% of the maximum value obtained at 80% VC. This ratio constituted an index of volume dependence. Hence the smaller the value of the ratio, the greater the volume dependence. We also compared the EMG in the upright posture to that in the supine posture at both 40 and 80% VC at a level of Pmus corresponding to 40% of the maximum obtained at both lung volumes. Study B. The increase in peak EMG corresponding to an increase in end-inspiratory lung volume was exDressed as a percentage relative to that achieved during
1
0
10
20
30
40
50
60
0
10
20
30
40
50
Ps MTA-EMG (au) FIG. 4, CWT muscle MTA-EMG plotted vs. parasternal EMG (PsMTA-EMG) during graded inspiratory efforts in all subjects at 60% VC. Note increase in CWT MTA-EMG at relatively low values of PsMTA-EMG in most of 4 muscles in most subjects. ES, erector spinae; LD, latissimus dorsi; PM, pectoralis major; Tr, trapezius.
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2376
TRUNK
601AT
MUSCLE’, ACTIVITY
I JE
y
I
L
'I
20
0
40% 60% 80% 100%
-2 __b_ -
60
40
DURING
*
60
vc VC vc vc
INSPIRATORY
EFFORTS
1JE
80
1
0
80
100
1SC
20
3 ‘b v)
20
40
60
80
20
40
60
80
1 TB
w
0
20
40
do
0
60
20
40
60
Pmus (cm H20) 5. ES MTA-EMG plotted vs. Pmus during graded inspiratury efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume. FIG.
that at a volume 20% VC above or below, particularly at low levels of Pmus (Figs. 5-8). However, this overlap was not seen among curves corresponding to lung volumes that differed by 240% VC, except at very low levels of Pmus (45 cmH,O) and at the lowest lung volumes (RV and 20% VC) in some muscle groups. The ratio of EMG 80
JE
7
4oxvc 6OXVC BOXVC looxvc
-
60
0
80
Pmus (cm H20) FIG. 7. PM MTA-EMG plotted vs. Pmus during graded inspiratory efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume.
at 40% VC to that at 80% VC was no different for the Ps than any other muscle in either posture (P > 0.05). Thus lung volume had a comparable effect on the EMGs of the chest wall muscles and those of the Ps. This was true both in the upright and supine postures. However, the volume dependence, expressed as the ratio of EMG at 80
JE
-
4oxvc 608VC BOXVC
80 /”
/
40
20 o P
40
.-
30
zE
40
60
80
0
20
40
60
80
1TB 80
.-it
0 0
20
40
60
80
0
Pmus (cm H20) LD MTA-EMG plotted vs. Pmus during graded inspiratory efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume. FIG.
6.
20
40
60
Pmus (cm H20) 8. Tr MTA-EMG plotted vs. Pmus during graded inspiratory efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume. FIG.
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TABLE 2. Verttilatory parameters and ACWT during resistive breathing with low and high EIVL ACWT,
Subj
AEIVL,
liters
Pm (%Pmax)
%/500
ES
LD
PM
91 -28 57 66 67 46
90 45 464 351 64 28
61 60 182 514 322 10
50 17
174 76
192 79
ml Tr
>
$? 0.6
0
0.0
0.2
0.4
0.6
0.8
EMG40%VC/EMG8O%VC
1.0
Upright
FIG. 9. Ratio of CWT at 40% VC to that at 80% VC at a Pmus level corresponding to 50% of maximum at 80% VC in supine vs. upright posture. Note greater volume dependence of EMG (smaller ratio) in upright posture (P < 0.02).
40% VC to that at 80% VC at iso-Pmus (see METHODS) was greater in the upright posture (0.34 t 0.06) than in the supine posture (0.60 t 0.09; P < 0.02; Fig. 9). Study B
During resistive breathing, the EMG in all muscles sampled increased progressively during inspiration, reaching a peak near end inspiration, and then decreased rapidly during expiration (see Fig. 2). In addition, with the exception of one muscle in one subject (ES in subject HC, Fig. lo), the EMG increased with lung volume by 160 t 40 (SE) % 1500 ml (Table 2). 40
-
30 /
9 3
*O
(3 3
10
_t__ __c_ __t_ __t_
AT
HC JE JW SC TB
O 50
3 3 E
4o
Is 0
/
/
Tr
30 -
20 -
20 lo-
10
,’
/
0
3
4
6
3
End;nspirkwy
Mean +SE
0.390 0.060
54 3
370 363 90 46 217 71
AEIVL, difference in end-inspiratory lung volume between low and high tidal volume; Pm (%Pmax), mouth pressure as percentage of maximum at FRC; ACWT, electromyographic differences in chest wall and trunk muscles at end inspiration between high and low tidal volumes; ES, erector spinae; LD, latissimus dorsi; PM, pectoralis major; Tr, trapezius.
DISCUSSION
Our results indicate that 1) activation of four CWT muscles (Tr, LD, PM, and ES) increases as a function of inspiratory Pmus generated at a given lung volume in both the upright and supine postures; 2) there is no systematic difference in the pattern of recruitment between the CWT and Ps muscles as a function of Pmus; 3) at any lung volume there is no systematic difference in the magnitude of the EMG of the CWT muscle at a given Pmus between the two postures; 4) both during isovolumic inspiratory efforts and during inspiratory resistive breathing, activation of the CWT muscles increases with lung volume; and 5) the lung volume dependence of the PmusEMG relationship is greater for the upright than the supine posture.
of Methods
Volume of decompressionand volume matching between postures. During graded inspiratory efforts, intrathoracic
40
40-
3o
0.550 0.275 0.500 0.450
46 64 61 58 53 43
0.200
Before the findings are accepted, we need to examine several potential sources of error.
50
4 ii 2
0.375
Critique
6oJLD
ES
AT HC JE JW SC TB
Lung “klle
;,
FIG. 10. CWT muscle MTA-EMC at end inspiration during inspiratory resistive loading with high and low tidal volumes plotted vs. endinspiratory lung volume. Different symbols are individual subjects and represent mean values of 10 consecutive breaths. Note increase in CWT MTA-EMG with lung volumes.
gas decompression will increase lung volume by an amount proportional to both the initial lung volume and the peak inspiratory pressure achieved. Because the latter was invariably lower at high lung volumes than at low lung volumes the effect of this correction would be to slightly narrow the family of Pmus-EMG curves corresponding to different lung volumes for a given muscle (Figs. 5-8) and to shift the curves to the left by -2.5%. Furthermore, both TLC and RV decrease by -5% on assumption of the supine posture (5, IO). Hence, absolute lung volumes in the supine posture may be (5% less than upright values. Therefore, when the errors related to matching of lung volume during postural changes and those due to volume decompression are combined, they would be smaller than the error of the method, and hence we neglected them. Nonstandardization of EMG. Because the EMGs were measured in arbitrary units, comparison of muscle activity between muscles (or between subjects) was not possible. We did not attempt to normalize the EMG measurements for two reasons. First, peak EMG values at maxi-
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ma1 inspiratory effort were not reproducible within individual subjects. This may be related to the use of different muscle recruitment strategies adopted when a rapid, maximum effort is required. Second, the peak activity of the CWT muscles during maximal inspiratory efforts is definitely submaximal. All subjects were able to exceed the values recorded during a maximal inspiratory maneuver by maximally activating the individual muscle against a resistance (See METHODS). Contamination of activity recorded during graded inspiratury efforts and inspiratory resistive breathing. Because
the fine-wire CWT electrodes were inserted close to the center of the muscle, most potentials sensed by the electrode are likely to have originated within a few millimeters of the tip. Each of the CWT muscles is larger than inspiratory rib cage muscles such as the Ps, external intercostals, and levator costae. Hence, during maximal activation, the capacity of the CWT muscles to influence EMG activity recorded in the Ps is expected to be at least as great, or greater than, that of the rib cage muscles to contaminate CWT EMGs. Yet during maximal static contractions of each CWT muscle in both study A and study B, no increase in activity was detected in the Ps nor the remaining CWT muscles. Therefore, although it is not possible to exclude a contribution by rib cage muscles to the increase in the CWT EMGs during inspiratory efforts, it is likely that any contamination by rib cage muscles of CWT EMGs during either graded inspiratory efforts or resistive breathing is minor. In study B, surface electrodes replaced the fine wires used during study A. Therefore, although large portions of the relevant muscle were sampled, the results could potentially be contaminated by other more superficial muscles. However, in most cases the electrodes were placed away from the edges of the CWT muscles, with no other muscles superficial to them. In the case of pectoralis major, the platysma could conceivably have contaminated the EMG signals. Variable Pmus during inspiratory resistive breathing.
Because inspiratory mouth pressure was kept constant during inspiratory resistive breathing, the magnitude of Pmus must have increased in the course of each inspiration. This would have been necessarily more marked when breathing with the larger tidal volumes. From the individual relaxation curves we calculated the increase in Pmus that would have occurred in each individual. The differences in Pmus between high and low tidal volumes constituted ~5% of the mean inspiratory mouth pressure during resistive breathing. Therefore this error was neglected. For all the above reasons we assumed that the measurements obtained were valid representations of the activation of the individual muscles sampled during both studies at the lung volumes stated. CWT Muscles and Generation
of Inspiratury
Pressure
Although CWT muscles are known to be activated during the performance of tasks specific to musculoskeletal acts, they have not been previously considered to make a major contribution to respiration in normal subjects. Yet we have demonstrated a positive, nonlinear
INSPIRATURY
EFFORTS
relationship between the generation of inspiratory pressure and muscle activity of the ES, LD, PM, and Tr muscles, as well as the Ps, the only conventionally accepted inspiratory muscle in this group. We examine the hypothesis that the CWT muscles are active participants in the generation of inspiratory pressure and therefore constitute an extended pool of skeletal muscles involved in respiration. However, before doing so we address the alternative hypothesis that the CWT muscle recruitment during inspiratory efforts serves merely to preserve posture and orientation of the trunk. The body mass of an upright subject is distributed over a small area centered at a substantial mean height above the ground. Consequently the center of gravity is inherently unstable. For an upright subject to preserve posture, any force vector other than that in the direction of gravity must be opposed by an appropriate antagonistic contraction of one or more such muscles. Therefore, it is possible that the configurational changes associated with inspiratory pressure generation result in gravitational vectors compensated for by CWT muscle recruitment. However, in the supine posture, body mass is distributed over a much larger surface and is centered at a lower elevation, thereby rendering the system more stable with minimal requirement for persisting truncal muscle activity. The fact that at a given Pmus the EMGs were not different in the supine and seated postures makes it most unlikely that the CWT muscles were recruited to preserve posture. An alternative hypothesis is that the CWT muscles actively participate in inspiratory pressure generation and the inspiratory process. Insofar that activation takes place even at relatively low values of Pmus, the muscle recruitment is not part of an overall nonspecific motor output at extremes of effort. Indeed, comparison with Ps muscles (Fig. 4) shows no systematic difference in the pattern of recruitment between the CWT and these conventionally regarded inspiratory muscles. To conclude that any particular muscle or group of muscles is instrumental in achieving a given motor function, several approaches may be taken. The first constitutes a demonstration of their activation whenever the particular motor function is being performed. This is the primary data base of our study. A second approach would be to demonstrate shortening of the relevant muscles during the performance of the motor act in question. Shortening would identify the muscle as an agonist for that motor act. However, absence of shortening or even lengthening during contraction would still be consistent with the muscle acting as a fixator or stabilizer. We did not measure changes in muscle length, and this clearly is an important area for future study. A third approach is a theoretical one, based on the anatomy of the muscles with predictions of their function based on their relationships to bony structures. This theoretical approach is now pursued with respect to the four CWT muscles examined during this study. We propose that as a consequence of the pressures generated during inspiration, forces are transmitted via the chest wall to the vertebral column. If unopposed, such forces lead to truncal-flexion deformation in proportion to the inspiratory pressure. The truncal-flexion
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deformation results in a decrease in ribcage cross-sectional area, thereby opposing inspiration. In this context, any muscular contraction that counteracts this deflationary effect may be regarded as assisting inspiration. In the absence of such activity, either the inspiratory task is not achieved or the truncal-flexion deformation requires an even greater activity of the primary inspiratory agonist muscles. The ES muscles (sacrospinalis) are the principal extensors of the vertebral column. The potential respiratory function of the muscle relates to the components that are inserted into the ribs and vertebrae (2). However, the relationship of these components to respiration and respiratory loading is unclear. Campbell (2) reported an increase in ES EMG activity during inspiration to high lung volumes and during graded inspiratory efforts against a pressure load. These observations have been extended by recent imaging studies of the human chest wall (13,21), which show that the spine moves during respiration. With the use of a model analysis of the human upper rib cage (20), a theoretical basis for the participation of the ES in respiration has been proposed. According to the model, during voluntary inspiratory efforts against a pressure load, forces are transmitted to the spine via the costovertebral and costotransverse articulations of the ribs. These forces promote spinal flexion and anterior rotation of the entire vertebral column on the pelvis. These actions are antagonized by the contraction of the ES, which tends to stiffen and extend the vertebral column, thereby opposing the forces induced by loading and counteracting the deflationary effect of spinal flexion on the rib cage. The contributions of the LD (12,22), PM (l&17), and Tr (22) muscles to respiration in normal subjects, as well as in patients with lung (12) and neuromuscular (6) diseases, have been previously reported. Because the LD contains fibers arising from the lower three or four ribs, contraction of these muscle bundles may result in elevation of the rib cage. The muscle would be assisted in this function by fixation of the humerus and the shoulder girdle by both the PM and Tr. Inspiratory activity within the LD has been reported during hyperpnea in normal subjects (12, 22) and in patients with either chronic asthma or emphysema (12). The PM has the potential to elevate the upper rib cage, particularly when the pectoral girdle and/or humerus are fixed by the Tr, rhomboids, and shoulder muscles (Z&11). Activity has been described at end inspiration in normal subjects (2, 17) and during tidal breathing in patients with asthma and emphysema (12). The PM and LD function as antagonists with reference to the humerus. However, when the latter is held fixed by these two muscles the mechanical advantage of their respiratory function may be magnified. The Tr has been described as an auxilliary muscle of respiration because the upper fibers extend the neck and facilitate the action of the sternomastoids and scalenes. The rest of the muscle stabilizes the shoulder girdle and facilitates the action of the pectoral, and potentially, LD muscles. In dyspnoeic patients, contraction can be felt within the occipitoclavicular portion of the muscle during inspiration (2). In high (C,-C,) quadriplegics, phasic inspiratory EMG activitv is associated with a disaroDortionate in-
INSPIRATORY
EFFORTS
2379
crease in the anteroposterior diameter of the upper rib cage relative to the lower rib cage (8). In addition, in C, quadriplegics, isolated contraction of the Tr and sternomastoid muscles increases the anteroposterior rib cage diameter but decreases other rib cage diameters (6). On the basis of the above it appears likely that the ES muscles contribute to inspiration by preventing flexion of the spine, whereas a common feature of the other three CWT muscles is that their contraction may contribute to the extension of the vertebral column, elevation of the ribs, and stabilization of the sternum, especially when the nonthoracic point of attachment is fixed. Volume Dependence of Chest Wall Muscles
In both supine and upright postures there was a volume-dependent increase in EMGs of both Ps and CWT muscles at a given Pmus (Figs. 5-8). This was also evident during inspiratory resistive breathing (Fig. 10). The basis for this is unclear. No data are available regarding CWT muscle length as a function of lung volume. If muscle shortening had occurred, the increase in EMG with lung volume could reflect the length-tension relationship applying to all skeletal muscles. As mean muscle length decreases below the resting length, the capacity of the muscle to generate tension decreases, and therefore greater activation is required to achieve a given level of tension. However, we think it unlikely that the CWT muscles act as agonists and shorten during inspiration. More likely, CWT contraction occurs quasi-isometrically, in which case the reason for volume dependence is less clear. One possibility is that an increase in lung volume displaces structures into which the muscles insert so that the force vector is rotated away from the normal. Therefore, to generate the same force as at a lower lung volume and to counteract the effect of changing the direction of the vector, greater activation of the muscle may be required. When lung volume increases, the proportion of the rib cage exposed to pleural pressure increases progressively. Hence, for a constant force expanding the rib cage, the mechanical advantage of the rib cage muscles in lowering pleural pressure should systematically decrease with increasing lung volume. Conversely, generation of a constant inspiratory pleural pressure necessitates increasing rib cage muscle recruitment (in addition to that due to muscle shortening) as lung volume increases and in turn a progressive increase in the antagonistic CWT activity directed toward maintaining extension of the spine and preventing deformation. We also found that the volume dependence in the upright posture was almost twice that in the supine posture (P < 0.02; Fig. 9). However, we were unable to detect a difference between the upright and supine EMG for the Ps or any CWT muscle at either high or low lung volume (P > 0.09). Presumably, this was due to the difference in the variability between the two sets of comparisons. The coefficient of variation for the differences in EMG between postures at a given lung volume was much greater than that for the volume-dependent difference in EMG in either the upright or supine posture. For a given
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2380
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change in lung volume, the change in rib cage volume is considerably less in the supine compared with the upright posture (14). Consequently, between 40 and 80% VC the change in the rib cage volume in the supine posture is systematically less than that in the upright posture. Because all of the CWT muscles insert into the rib cage, we speculate that the mechanical linkage and geometric relationships change less in the supine than in the upright posture for a given change in lung volume. Therefore, at iso-Pmus, an increase in lung volume from 40 to 80% VC may require less CWT muscle activation in the supine than in the upright posture. Implications of CWT Recruitment to Energetics
An unexplained and consistent observation in respiratory muscle energetics is the relatively low inspiratory muscle efficiency (4, 15). One possible explanation for this discrepancy is that whereas total energy consumption can be determined relatively accurately, the work of breathing as represented by the pressure-volume diagram is underestimated. This is quite likely, as the work of deformation at high inspiratory pressures could be substantial and is not recorded. However, the results of the present study suggest another basis for the low values of respiratory muscle efficiency during loaded breathing. The generalized recruitment of CWT muscles acting as fixators and contracting isometrically must contribute substantially to the total 0, costs. Furthermore, because of their greater recruitment as a function of Pmus, the greater 0, cost (and hence lesser efficiency) as the pressure increases even at a constant work rate could be accounted for. A third implication of this study relates to the volume dependence of inspiratory muscle efficiency under conditions of identical work rate and pressure-time products (3). Because of the volume dependence of recruitment of the CWT muscles, a greater 0, cost and hence a lesser efficiency at higher lung volumes is predictable. The fourth implication of this work relates to our findings comparing the sensitivity of the 0, cost of breathing to changes in the pressure-time product at iso-work rates between ventilatory and pressure loads (1). We found that when breathing against high ventilatory loads (and hence at high lung volumes) the 0, cost of breathing at a given work rate is very sensitive to changes in pressuretime product. In contrast, when breathing against high pressure loads (at a volume close to FRC) efficiency was relatively uninfluenced by large changes in pressure-time product. To the extent that 0, cost correlates with EMG activity, the steeper relationship between EMG of the CWT muscle and Pmus at high lung volumes (Figs. 5-8) predicts a much greater change in energy cost as a function of inspiratory pressure than at low lung volumes. In summary, we found that the EMG of the four CWT muscles increases as a function of the inspiratory muscle pressure generated at a given lung volume. We hypothesize that the CWT muscles actively participate in the generation of inspiratory pressure by extending the spine (ES), elevating the ribs (LD and PM), stabilizing the sternum, and fixing the shoulder girdle (LD, PM and Tr). The volume-dependent increase of the Ps and CWT
INSPIRATORY
EFFORTS
EMGs at a given Pmus in both postures may be related to a decreased mechanical advantage of these muscles as volume increases. The greater volume dependence of the CWT EMGs in the upright posture may reflect greater changes in the mechanical linkage between the CWT muscles and the rib cage because of the systematically greater changes in rib cage volume in the upright compared with the supine posture for equivalent differences in lung volume. The authors are grateful to Jeanette Walker for typing this manuscript. Present address and address for reprint requests: S. J. Cala, Meakins-Christie Laboratories, 3626 St. Urbain St., Montreal, Quebec H2X 2P2, Canada. Received 15 November 1991; accepted in final form 23 June 1992. REFERENCES S. J., J. EDYVEAN, M. RYNN, AND L. A. ENGEL. Oxygen cost of breathing; ventilatory vs. pressure loads (Abstract). Aust. N. 2. J. Med. 21, Suppl. 4: A666, 1991. 2. CAMPBELL, E. J. M. Accessory muscles. In: The Respiratory Muscles: Mechanics and Neural Control, edited by E. J. M. Campbell, E. Agostoni, and J. Newsom Davis. Philadelphia, PA: Saunders, 1970, p* 181-193. 3. COLLETT, P. W., AND L. A. ENGEL. Influence of lung volume on oxygen cost of resistive breathing. J. Appl. Physiol. 61: 16-24,1986. 4. COLLETT, P. W., C. PERRY, AND L. A. ENGEL. Pressure-time product, flow, and oxygen cost of resistive breathing in humans. J. Appl, 1. CALA,
Physiol. 5. CRAIG,
58: 1263-1272,
Physiol. 6. DANON,
15: 59-61,
1985.
A. B., JR. Effects of position on expiratory reserve volume and vital capacity of the lungs during immersion in water. J. Appl. 1960.
J., W. S. DRUZ, N. B. GOLDBERG, AND J. T. SHARP. Function of the isolated paced diaphragm and the cervical accessory muscles in Cl quadriplegics. Am. Rev. Respir. Dis. 119: 909-919,
1979. 7* DELHEZ,
L., AND J. M. PETIT. Donnees actuelles de l’Electromyographie respiratoire chez 1’Homme normal. Electromyogruphy 6:
101-146, 1966, 8. DETROYER, A.,
M. ESTENNE, AND W. VINCKEN. Rib cage motion and muscle use in high tetraplegics. Am. Rev. Respir. Dis. 133:
1115-1119,1986. 9. DETROYER, A., V. NINANE, J. J. GILMARTIN, C. LEMERE, AND M. E~TENNE. Triangularis sterni muscle use in supine humans. J. Appl. Physiol. 62: 919-925, 1987. 10. DITTMER, D. S., AND R. M. GREBE (Editors). Handbook of Respiration. Philadelphia, PA: Saunders, 1958, p. 28-40. 11. GARDNER, E., D. J. GRAY, AND R. ~‘RAHILLY. Anatomy: A Regional Study of Human Structure. Philadelphia, PA: Saunders, 1975. 12. GRONBAEK, P., AND A. P. SKWBY. The activity of the diaphragm
13.
14.
15.
16.
17.
18.
and some mu&es of the neck and trunk in chronic asthmatics and normal controls. Actcz Med. Stand. 168: 413-425, 1960. KENYON, C. M., T. J. PEDLEY, AND T. W. HIGENBOTTAM. Adaptive modeling of the human rib cage in median sternotomy. J. Appl. Physiol. 70: 2287-2302, 1991. KONNO, K., AND J. MEAD. Measurement of t;he separate volume changes of rib cage and abdomen during breathing. J. AppZ. Physiol. 22: 407-422, 1967. MCGREGOR, M., AND M. BECKLAKE. The relationship of oxygen cost of breathing to respiratory mechanical work and respiratory force. J. Clin. 1rcuest. 40: 971-980, 1961. MUZA, S. R., G. J. CRINER, AND S. G. KELSEN. Pectoralis muscle recruitment during weaning in patients with chronic respiratory failure (Abstract). Am. Rev. Respir. Dis. 143, Suppl. 4: A163, 1991. MUZA, S. R., G. J. CRINER, AND S. G. KELSEN. Pectoralis muscle recruitment during breathing in normal humans (Abstract). Am. Rev. Respir. Dis. 143, Suppl. 4: A366, 1991. ROBERTSON, C. H., G. H. FOSTER, AND R. L. JOHNSON. The relationship of respiratory failure to the oxygen consumption of lactic acid by, and distribution of blood flow among respiratory muscles
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MUSCLF,
ACTIVITY
DURING
during increasing inspiratory resistance. J. Clin. Invest. 59: 31-42, 19.
1977. ROCHESTER,
D. F., AND G. BETTINI. Diaphragmatic bloodflow and energy expenditure in the dog. J. Clin. 1nuest. 57: 661-672,1976. 20. SAUMAREZ, R. C. An analysis of action of intercostal muscles in human upper rib cage. J. Appl. Physiol. 60: 690-701,1986. 21. SAUMAREZ, R. C. Automated optical measurements of human
INSPIRATORY
EFFORTS
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torso surface movements during breathing. J. Appl. Physiol. 60: 702-709,1986,
22. TOKIZANE, T., K. KAWAMATA, AND H. TUKIZANE. Electromyographic studies on the human respiratory muscles. Jpn. J. Physiol. 2: 232-247, 1952. 23. WILLIAMS, P. L., AND R. WARWICK (Editors). Gray’s Anatomy. London: Churchill-Livingstone, 1989, p. 575-618.
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J. EDYVEAN,?
Thorucic Medicine
AND
Unit, Westmeud
L. A. ENGEL?? Hospital,
Westmead,
New South Wales 2145, Austruliu
CALA, S. J., J. EDYVEAN, AND L. A. ENGEL. Chest wall and trunk muscle activity during inspiratory loading. J. Appl. Phys-
CWT electromyograms (EMGs) increased, in a manner similar to that of the Ps muscles, as the generated inspiraiol. 73(6): 2373-2381, 1992.-We measured the electromyotory muscle pressure (Pmus) increased. However, for a graphic (EMG) activity in four chest wall and trunk (CWT) given Pmus all EMG activity increased with increasing muscles,the erector spinae, latissimusdorsi, pectoralis major, and trapezius, together with the parasternal, in four normal lung volume. There was no difference in the Pmus-EMG between upright and supine positions for subjectsduring gradedinspiratory efforts against an occlusion relationship any of the muscles examined. This is evidence against in both upright and seatedpostures. We also measuredCWT that the CWT muscles are recruited EMGs in six seatedsubjectsduring inspiratory resistive load- the possibility ing at high and low tidal volumes [1,280? 80 (SE) and 920st 60 merely to maintain posture and/or preserve orientation ml, respectively]. With one exception, CWT EMG increasedas of the trunk with respect to the gravitational field in a function of inspiratory pressuregenerated (Pmus) at all lung upright subjects. Our findings are consistent with the hyvolumes in both postures,with no systematic difference in re- pothesis that the CWT muscles contribute actively to cruitment betweenCWT and parasternal musclesasa function inspiratory pressure generation.
of Pmus. At any given lung volume there was no consistent difference in CWT EMG at a given Pmus betweenthe two postures (P > 0.09). However, at a given Pmus during both graded inspiratory efforts and inspiratory resistive loading, EMGs of all musclesincreasedwith lung volume, with greater volume dependence in the upright posture (P < 0.02). The results suggest that during inspiratory efforts, CWT musclescontribute to the generation of inspiratory pressure. The CWT muscles may act asfixators opposingdeflationary forces transmitted to the vertebral column by rib cagearticulations, a function that may be lesseffective at high lung volumesif the direction of the muscularinsertions is altered disadvantageously.
METHODS Study A
Four normal subjects were studied in both the seated and supine postures. In the upright posture, subjects sat in a dental chair with the head supported, maintaining a fixed position of head, neck, and trunk. In the supine position, the subject’s trunk and extended arms rested on a firm board covered by foam rubber padding. The board overlay the backrest of the chair that had been rotated to respiratory muscles; electromyograms; accessory muscles; the horizontal plane. The head, neck, and shoulders were completely supported by a bean bag and pillow. The exloaded breathing perimental setup is shown in Fig. 1. First, maximal inspiratory efforts against an occluded airway were performed three times in a random seBREATHING EFFORTS against external inspiratory loads are associated with activity of inspiratory muscles, such quence, at 20% vital capacity (VC) increments, from reas the diaphragm and parasternal (Ps) and external in- sidual volume (RV) to total lung capacity (TLC) (Table I). Then, after inspiration to TLC, the subject expired to tercostals (18, 19). However, inspiratory effort-related a predetermined lung volume, relaxed, and made a subactivity has also been described in a variety of other musmaximal graded ramp like inspiratory effort against an cles that attach to the chest wall and trunk (CWT), occluded airway up to -500% maximal inspiratory presnamely the erector spinae (ES) (2, 12), latissimus dorsi sure at that lung volume (Fig. 2). The graded inspiratory (LD) (12), pectoralis major (PM) (12,16,17), and trapeefforts were also performed at increments of 20% of VC zius (Tr) (8, 22). These muscles have a wide range of functions, including the maintenance of posture and par- in random order and were repeated at least three times at ticipation in a variety of volitional motor tasks (11, 23) each lung volume in each subject. Both maximal and graded efforts were performed first in the upright and but are not conventionally regarded as having an importhen in the supine position. We used TLC as a common tant role in respiration. To examine the degree and pattern of participation of these muscles in respiratory acts, volume of reference for both postures. Flow was measured with a pneumotachograph, and the we studied the electrical activity in the CWT muscles, signal was integrated to obtain lung volume. Mouth prestogether with that of the Ps, an inspiratory muscle, in sure was measured by a pressure transducer (Validyne) normal subjects during graded inspiratory efforts against an occluded airway in both the upright and supine pos- connected to the mouthpiece by a side port. EMGs were ture. We found that at any given lung volume all the measured from the Ps in the second and third intercostal space, ES muscles from the region adjacent to the T,-T, t Deceased 27 October 1991. ttDeceased 7 February 1992. vertebral space, LD muscles 2-3 cm caudolateral to the 0161-7567/92 $2.00 Copyright 0 1992 the American Physiological Society
2373
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2374
TRUNK
MUSCLE
ACTIVITY
DURING
INSPIRATORY
Mouth km
EFFORTS
Pressure Hz01
Erector
Spinao MTA
1
\
A B FIG. 1. Study A: D, 3-way tap, closed during graded inspiratory efforts; E, fine-wire bipolar electrodes. Study B: R, variable resistance; F, surface bipolar electrodes; Pm, differential transducer for pressure measurements at mouth; C, pneumotachograph; MTA-EMG, moving time-averaged electromyogram of chest wall and trunk (CWT) muscles.
tip of the scapula, PM muscles 3-4 cm craniolateral to the nipple, and Tr muscles midway between the spinous process of C, and the acromion. The bipolar EMG electrodes were made of 75ym insulated stainless steel wire (Cooner Wire) that was bared for -1 mm from the tip. They were inserted under sterile conditions using 25 gauge hypodermic needles. Once through the skin the electrode was connected to its amplifier, and the signal was monitored as the needle was advanced slowly to the required position. For Ps electrodes, the muscle was considered to be inspiratory when it recorded action potentials with characteristics of single motor units during natural or voluntary inspiration but not during maneuvers designed to activate nearby muscles. Ps intercostal muscles were sampled in the second or third interspace 2-3 cm lateral to the border of the sternum after penetrating the pectoral muscles, which were activated by adduction of the arm against a resistance. The Ps muscles are superficial to the transversus thoracis, which could be recruited by exhalation below functional residual capacity (FRC) (9). Electrodes that penetrated deeply enough to record motor unit potentials from this muscle were not used for the study. The ES was activated by asking the
LatlWmus MTA
Dorsl
Trapezius MTA
FIG. 2. Representative data obtained inspiratory effort at 80% vital capacity sistive breathing (B). MTA, moving-time
in subject JE during graded (A) and during inspiratory reaverage.
subject to extend the spine, the LD was activated by extension of the outstretched arm, the PM was activated by adduction of the arm, and the Tr was activated by elevation of the shoulders, all against resistance. Once the electrodes were in position, the needles were withdrawn, and wires were left in place. EMGs were band-pass filtered (loo-2,000 Hz), rectified, and smoothed with a leaky integrator (time constant of 200 ms). The raw signals were displayed on a storage oscilloscope (Tectronix). All signals were recorded on a Hewlett-Packard eight-channel strip chart recorder and stored on FM tape for analysis. Study B
TABLE
1. Anthropometric
data Pmax,cmH,O
Subj
Age, yr
AT JE
36 42
SC TB
32 29
HC
3’7
JW
33
Ht, cm
FRC,
VC,
Sex
liters
liters
F M M M M M
152 182 180 181 178 180
2.83 3.87 4.31 3.31 3.65 3.10
3.95 5.85 6.40 5.57 5.50 5.88
40% VC
60% VC
80% VC
100% VC
92 110 145 120
86 75 105 110
55 65 96 96
34 36 56 54
Subjects AT, JE, SC, and TB were common to studies A and B. FRC, functional residual capacity; VC, vital capacity; Pmax, maximum pressure generation by inspiratory muscles at different lung volumes; F, female; M, male.
In six seated normal subjects (4 from study A and 2 additional subjects), we also measured the EMG of the ES, LD, PM, and Tr muscles using bipolar surface electrodes during external inspiratory resistive loading. In each subject two runs were performed, generating identical inspiratory mouth pressures but with different tidal volumes, resulting in different end-inspiratory volumes. This study was performed to assessseparately the volume dependence of the EMG-Pmus relationship under dynamic conditions of inspiratory resistive breathing from FRC. With the use of the same surface landmarks as in study A, bipolar electrodes were placed on the skin overlying the CWT muscles. The subject inspired through the resis-
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EFFORTS
resistive loading at the lower lung volume. The result for each muscle was averaged to obtain the change in mean EMG per 500 ml increase in lung volume. 60%VC
RESULTS
Study A
10
20
30
Pmus ( cm HzO) FIG. 3. Erector spinae muscle EMG activity plotted vs. pressure generated by inspiratory muscles (Pmus) in subject AT in upright posture during 3 graded inspiratory efforts at 2 lung volumes. Note reproducibility of Pmus-EMG relationships at each lung volume. VC, vital capacity; AU, arbitrary units.
tance (R in Fig. 1) via a three-way tap (D in Fig. 1). Expiration was unloaded. The target mouth pressure was attained quickly and maintained constant for the required time before relaxation, thereby achieving a square-wave pattern of breathing. This was facilitated by displaying mouth pressure to the subject on an oscilloscope screen (Fig. 1). The variable resistance was adjusted so that the predetermined pressure was associated with a given inspiratory flow rate. The inspiratory duration, expiratory duration, and frequency were controlled by the subject with the aid of a metronome. Hence, for a given inspiratory flow rate, tidal volume was determined by inspiratory duration. Each subject performed inspiratory resistive loaded runs with both a high and a low tidal volume (1,280 t 80 and 920 t 60 ml, respectively). Each run consisted of 10 reproducible breaths, and high and low runs were matched for breathing frequency, mean inspiratory mouth pressure (51 t 3% of maximum at FRC), and mean inspiratory flow rate. Hence, during high runs inspiratory time was slightly longer.
At each lung volume, in both postures, graded inspiratory efforts against an occluded airway resulted in a progressive increase in the electrical activity (MTA-EMG) of the Ps, as well as the ES, LD, PM, and, with the exception of one subject in the supine posture, the Tr muscles. The relationship between EMG and Pmus was curvilinear and concave upward in the majority of cases. The shape was reproducible at a given lung volume in the 40% VC to TLC range (Fig. 3). Direct comparisons of CWT muscle EMG with that of the Ps showed a consistently monotonic relationship (Fig. 4). Although in some cases at low Pmus, the rate of CWT muscle recruitment appeared relatively less than that of the parasternals (curvilinear relationship concave upward), this was not consistently so. In some cases a linear relationship was seen, and in others it was concave downward, i.e., relatively greater rate of recruitment of the CWT than Ps muscles at low Pmus. There was no difference in the Pmus-EMG relationships between upright and supine postures at any lung volume for any of the muscles examined. In both postures at a given Pmus, integrated activity of the muscle groups increased with increasing lung volume (Figs. 5-8) from 40% VC to TLC. The curves obtained at RV and 20% of VC were highly variable and did not demonstrate this relationship to lung volume. In some subjects the EMG-Pmus curve at one volume overlapped ES __t_ d -
AT JE SC 7-B
Data Analysis Study A. At each lung volume the integrated EMG was plotted vs. inspiratory Pmus, taken as the change in mouth pressure from that during relaxation. We compared the EMG at 40% VC to that at 80% VC at a level of Pmus corresponding to 50% of the maximum value obtained at 80% VC. This ratio constituted an index of volume dependence. Hence the smaller the value of the ratio, the greater the volume dependence. We also compared the EMG in the upright posture to that in the supine posture at both 40 and 80% VC at a level of Pmus corresponding to 40% of the maximum obtained at both lung volumes. Study B. The increase in peak EMG corresponding to an increase in end-inspiratory lung volume was exDressed as a percentage relative to that achieved during
1
0
10
20
30
40
50
60
0
10
20
30
40
50
Ps MTA-EMG (au) FIG. 4, CWT muscle MTA-EMG plotted vs. parasternal EMG (PsMTA-EMG) during graded inspiratory efforts in all subjects at 60% VC. Note increase in CWT MTA-EMG at relatively low values of PsMTA-EMG in most of 4 muscles in most subjects. ES, erector spinae; LD, latissimus dorsi; PM, pectoralis major; Tr, trapezius.
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2376
TRUNK
601AT
MUSCLE’, ACTIVITY
I JE
y
I
L
'I
20
0
40% 60% 80% 100%
-2 __b_ -
60
40
DURING
*
60
vc VC vc vc
INSPIRATORY
EFFORTS
1JE
80
1
0
80
100
1SC
20
3 ‘b v)
20
40
60
80
20
40
60
80
1 TB
w
0
20
40
do
0
60
20
40
60
Pmus (cm H20) 5. ES MTA-EMG plotted vs. Pmus during graded inspiratury efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume. FIG.
that at a volume 20% VC above or below, particularly at low levels of Pmus (Figs. 5-8). However, this overlap was not seen among curves corresponding to lung volumes that differed by 240% VC, except at very low levels of Pmus (45 cmH,O) and at the lowest lung volumes (RV and 20% VC) in some muscle groups. The ratio of EMG 80
JE
7
4oxvc 6OXVC BOXVC looxvc
-
60
0
80
Pmus (cm H20) FIG. 7. PM MTA-EMG plotted vs. Pmus during graded inspiratory efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume.
at 40% VC to that at 80% VC was no different for the Ps than any other muscle in either posture (P > 0.05). Thus lung volume had a comparable effect on the EMGs of the chest wall muscles and those of the Ps. This was true both in the upright and supine postures. However, the volume dependence, expressed as the ratio of EMG at 80
JE
-
4oxvc 608VC BOXVC
80 /”
/
40
20 o P
40
.-
30
zE
40
60
80
0
20
40
60
80
1TB 80
.-it
0 0
20
40
60
80
0
Pmus (cm H20) LD MTA-EMG plotted vs. Pmus during graded inspiratory efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume. FIG.
6.
20
40
60
Pmus (cm H20) 8. Tr MTA-EMG plotted vs. Pmus during graded inspiratory efforts in upright posture at each lung volume in all subjects. Each curve is mean of 3 efforts performed in random order. Note consistent increase in MTA-EMG with increasing Pmus and, for a given value of Pmus, increase in MTA-EMG with lung volume. FIG.
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DURING
INSPIRATORY
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EFFORTS
TABLE 2. Verttilatory parameters and ACWT during resistive breathing with low and high EIVL ACWT,
Subj
AEIVL,
liters
Pm (%Pmax)
%/500
ES
LD
PM
91 -28 57 66 67 46
90 45 464 351 64 28
61 60 182 514 322 10
50 17
174 76
192 79
ml Tr
>
$? 0.6
0
0.0
0.2
0.4
0.6
0.8
EMG40%VC/EMG8O%VC
1.0
Upright
FIG. 9. Ratio of CWT at 40% VC to that at 80% VC at a Pmus level corresponding to 50% of maximum at 80% VC in supine vs. upright posture. Note greater volume dependence of EMG (smaller ratio) in upright posture (P < 0.02).
40% VC to that at 80% VC at iso-Pmus (see METHODS) was greater in the upright posture (0.34 t 0.06) than in the supine posture (0.60 t 0.09; P < 0.02; Fig. 9). Study B
During resistive breathing, the EMG in all muscles sampled increased progressively during inspiration, reaching a peak near end inspiration, and then decreased rapidly during expiration (see Fig. 2). In addition, with the exception of one muscle in one subject (ES in subject HC, Fig. lo), the EMG increased with lung volume by 160 t 40 (SE) % 1500 ml (Table 2). 40
-
30 /
9 3
*O
(3 3
10
_t__ __c_ __t_ __t_
AT
HC JE JW SC TB
O 50
3 3 E
4o
Is 0
/
/
Tr
30 -
20 -
20 lo-
10
,’
/
0
3
4
6
3
End;nspirkwy
Mean +SE
0.390 0.060
54 3
370 363 90 46 217 71
AEIVL, difference in end-inspiratory lung volume between low and high tidal volume; Pm (%Pmax), mouth pressure as percentage of maximum at FRC; ACWT, electromyographic differences in chest wall and trunk muscles at end inspiration between high and low tidal volumes; ES, erector spinae; LD, latissimus dorsi; PM, pectoralis major; Tr, trapezius.
DISCUSSION
Our results indicate that 1) activation of four CWT muscles (Tr, LD, PM, and ES) increases as a function of inspiratory Pmus generated at a given lung volume in both the upright and supine postures; 2) there is no systematic difference in the pattern of recruitment between the CWT and Ps muscles as a function of Pmus; 3) at any lung volume there is no systematic difference in the magnitude of the EMG of the CWT muscle at a given Pmus between the two postures; 4) both during isovolumic inspiratory efforts and during inspiratory resistive breathing, activation of the CWT muscles increases with lung volume; and 5) the lung volume dependence of the PmusEMG relationship is greater for the upright than the supine posture.
of Methods
Volume of decompressionand volume matching between postures. During graded inspiratory efforts, intrathoracic
40
40-
3o
0.550 0.275 0.500 0.450
46 64 61 58 53 43
0.200
Before the findings are accepted, we need to examine several potential sources of error.
50
4 ii 2
0.375
Critique
6oJLD
ES
AT HC JE JW SC TB
Lung “klle
;,
FIG. 10. CWT muscle MTA-EMC at end inspiration during inspiratory resistive loading with high and low tidal volumes plotted vs. endinspiratory lung volume. Different symbols are individual subjects and represent mean values of 10 consecutive breaths. Note increase in CWT MTA-EMG with lung volumes.
gas decompression will increase lung volume by an amount proportional to both the initial lung volume and the peak inspiratory pressure achieved. Because the latter was invariably lower at high lung volumes than at low lung volumes the effect of this correction would be to slightly narrow the family of Pmus-EMG curves corresponding to different lung volumes for a given muscle (Figs. 5-8) and to shift the curves to the left by -2.5%. Furthermore, both TLC and RV decrease by -5% on assumption of the supine posture (5, IO). Hence, absolute lung volumes in the supine posture may be (5% less than upright values. Therefore, when the errors related to matching of lung volume during postural changes and those due to volume decompression are combined, they would be smaller than the error of the method, and hence we neglected them. Nonstandardization of EMG. Because the EMGs were measured in arbitrary units, comparison of muscle activity between muscles (or between subjects) was not possible. We did not attempt to normalize the EMG measurements for two reasons. First, peak EMG values at maxi-
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ma1 inspiratory effort were not reproducible within individual subjects. This may be related to the use of different muscle recruitment strategies adopted when a rapid, maximum effort is required. Second, the peak activity of the CWT muscles during maximal inspiratory efforts is definitely submaximal. All subjects were able to exceed the values recorded during a maximal inspiratory maneuver by maximally activating the individual muscle against a resistance (See METHODS). Contamination of activity recorded during graded inspiratury efforts and inspiratory resistive breathing. Because
the fine-wire CWT electrodes were inserted close to the center of the muscle, most potentials sensed by the electrode are likely to have originated within a few millimeters of the tip. Each of the CWT muscles is larger than inspiratory rib cage muscles such as the Ps, external intercostals, and levator costae. Hence, during maximal activation, the capacity of the CWT muscles to influence EMG activity recorded in the Ps is expected to be at least as great, or greater than, that of the rib cage muscles to contaminate CWT EMGs. Yet during maximal static contractions of each CWT muscle in both study A and study B, no increase in activity was detected in the Ps nor the remaining CWT muscles. Therefore, although it is not possible to exclude a contribution by rib cage muscles to the increase in the CWT EMGs during inspiratory efforts, it is likely that any contamination by rib cage muscles of CWT EMGs during either graded inspiratory efforts or resistive breathing is minor. In study B, surface electrodes replaced the fine wires used during study A. Therefore, although large portions of the relevant muscle were sampled, the results could potentially be contaminated by other more superficial muscles. However, in most cases the electrodes were placed away from the edges of the CWT muscles, with no other muscles superficial to them. In the case of pectoralis major, the platysma could conceivably have contaminated the EMG signals. Variable Pmus during inspiratory resistive breathing.
Because inspiratory mouth pressure was kept constant during inspiratory resistive breathing, the magnitude of Pmus must have increased in the course of each inspiration. This would have been necessarily more marked when breathing with the larger tidal volumes. From the individual relaxation curves we calculated the increase in Pmus that would have occurred in each individual. The differences in Pmus between high and low tidal volumes constituted ~5% of the mean inspiratory mouth pressure during resistive breathing. Therefore this error was neglected. For all the above reasons we assumed that the measurements obtained were valid representations of the activation of the individual muscles sampled during both studies at the lung volumes stated. CWT Muscles and Generation
of Inspiratury
Pressure
Although CWT muscles are known to be activated during the performance of tasks specific to musculoskeletal acts, they have not been previously considered to make a major contribution to respiration in normal subjects. Yet we have demonstrated a positive, nonlinear
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relationship between the generation of inspiratory pressure and muscle activity of the ES, LD, PM, and Tr muscles, as well as the Ps, the only conventionally accepted inspiratory muscle in this group. We examine the hypothesis that the CWT muscles are active participants in the generation of inspiratory pressure and therefore constitute an extended pool of skeletal muscles involved in respiration. However, before doing so we address the alternative hypothesis that the CWT muscle recruitment during inspiratory efforts serves merely to preserve posture and orientation of the trunk. The body mass of an upright subject is distributed over a small area centered at a substantial mean height above the ground. Consequently the center of gravity is inherently unstable. For an upright subject to preserve posture, any force vector other than that in the direction of gravity must be opposed by an appropriate antagonistic contraction of one or more such muscles. Therefore, it is possible that the configurational changes associated with inspiratory pressure generation result in gravitational vectors compensated for by CWT muscle recruitment. However, in the supine posture, body mass is distributed over a much larger surface and is centered at a lower elevation, thereby rendering the system more stable with minimal requirement for persisting truncal muscle activity. The fact that at a given Pmus the EMGs were not different in the supine and seated postures makes it most unlikely that the CWT muscles were recruited to preserve posture. An alternative hypothesis is that the CWT muscles actively participate in inspiratory pressure generation and the inspiratory process. Insofar that activation takes place even at relatively low values of Pmus, the muscle recruitment is not part of an overall nonspecific motor output at extremes of effort. Indeed, comparison with Ps muscles (Fig. 4) shows no systematic difference in the pattern of recruitment between the CWT and these conventionally regarded inspiratory muscles. To conclude that any particular muscle or group of muscles is instrumental in achieving a given motor function, several approaches may be taken. The first constitutes a demonstration of their activation whenever the particular motor function is being performed. This is the primary data base of our study. A second approach would be to demonstrate shortening of the relevant muscles during the performance of the motor act in question. Shortening would identify the muscle as an agonist for that motor act. However, absence of shortening or even lengthening during contraction would still be consistent with the muscle acting as a fixator or stabilizer. We did not measure changes in muscle length, and this clearly is an important area for future study. A third approach is a theoretical one, based on the anatomy of the muscles with predictions of their function based on their relationships to bony structures. This theoretical approach is now pursued with respect to the four CWT muscles examined during this study. We propose that as a consequence of the pressures generated during inspiration, forces are transmitted via the chest wall to the vertebral column. If unopposed, such forces lead to truncal-flexion deformation in proportion to the inspiratory pressure. The truncal-flexion
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deformation results in a decrease in ribcage cross-sectional area, thereby opposing inspiration. In this context, any muscular contraction that counteracts this deflationary effect may be regarded as assisting inspiration. In the absence of such activity, either the inspiratory task is not achieved or the truncal-flexion deformation requires an even greater activity of the primary inspiratory agonist muscles. The ES muscles (sacrospinalis) are the principal extensors of the vertebral column. The potential respiratory function of the muscle relates to the components that are inserted into the ribs and vertebrae (2). However, the relationship of these components to respiration and respiratory loading is unclear. Campbell (2) reported an increase in ES EMG activity during inspiration to high lung volumes and during graded inspiratory efforts against a pressure load. These observations have been extended by recent imaging studies of the human chest wall (13,21), which show that the spine moves during respiration. With the use of a model analysis of the human upper rib cage (20), a theoretical basis for the participation of the ES in respiration has been proposed. According to the model, during voluntary inspiratory efforts against a pressure load, forces are transmitted to the spine via the costovertebral and costotransverse articulations of the ribs. These forces promote spinal flexion and anterior rotation of the entire vertebral column on the pelvis. These actions are antagonized by the contraction of the ES, which tends to stiffen and extend the vertebral column, thereby opposing the forces induced by loading and counteracting the deflationary effect of spinal flexion on the rib cage. The contributions of the LD (12,22), PM (l&17), and Tr (22) muscles to respiration in normal subjects, as well as in patients with lung (12) and neuromuscular (6) diseases, have been previously reported. Because the LD contains fibers arising from the lower three or four ribs, contraction of these muscle bundles may result in elevation of the rib cage. The muscle would be assisted in this function by fixation of the humerus and the shoulder girdle by both the PM and Tr. Inspiratory activity within the LD has been reported during hyperpnea in normal subjects (12, 22) and in patients with either chronic asthma or emphysema (12). The PM has the potential to elevate the upper rib cage, particularly when the pectoral girdle and/or humerus are fixed by the Tr, rhomboids, and shoulder muscles (Z&11). Activity has been described at end inspiration in normal subjects (2, 17) and during tidal breathing in patients with asthma and emphysema (12). The PM and LD function as antagonists with reference to the humerus. However, when the latter is held fixed by these two muscles the mechanical advantage of their respiratory function may be magnified. The Tr has been described as an auxilliary muscle of respiration because the upper fibers extend the neck and facilitate the action of the sternomastoids and scalenes. The rest of the muscle stabilizes the shoulder girdle and facilitates the action of the pectoral, and potentially, LD muscles. In dyspnoeic patients, contraction can be felt within the occipitoclavicular portion of the muscle during inspiration (2). In high (C,-C,) quadriplegics, phasic inspiratory EMG activitv is associated with a disaroDortionate in-
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crease in the anteroposterior diameter of the upper rib cage relative to the lower rib cage (8). In addition, in C, quadriplegics, isolated contraction of the Tr and sternomastoid muscles increases the anteroposterior rib cage diameter but decreases other rib cage diameters (6). On the basis of the above it appears likely that the ES muscles contribute to inspiration by preventing flexion of the spine, whereas a common feature of the other three CWT muscles is that their contraction may contribute to the extension of the vertebral column, elevation of the ribs, and stabilization of the sternum, especially when the nonthoracic point of attachment is fixed. Volume Dependence of Chest Wall Muscles
In both supine and upright postures there was a volume-dependent increase in EMGs of both Ps and CWT muscles at a given Pmus (Figs. 5-8). This was also evident during inspiratory resistive breathing (Fig. 10). The basis for this is unclear. No data are available regarding CWT muscle length as a function of lung volume. If muscle shortening had occurred, the increase in EMG with lung volume could reflect the length-tension relationship applying to all skeletal muscles. As mean muscle length decreases below the resting length, the capacity of the muscle to generate tension decreases, and therefore greater activation is required to achieve a given level of tension. However, we think it unlikely that the CWT muscles act as agonists and shorten during inspiration. More likely, CWT contraction occurs quasi-isometrically, in which case the reason for volume dependence is less clear. One possibility is that an increase in lung volume displaces structures into which the muscles insert so that the force vector is rotated away from the normal. Therefore, to generate the same force as at a lower lung volume and to counteract the effect of changing the direction of the vector, greater activation of the muscle may be required. When lung volume increases, the proportion of the rib cage exposed to pleural pressure increases progressively. Hence, for a constant force expanding the rib cage, the mechanical advantage of the rib cage muscles in lowering pleural pressure should systematically decrease with increasing lung volume. Conversely, generation of a constant inspiratory pleural pressure necessitates increasing rib cage muscle recruitment (in addition to that due to muscle shortening) as lung volume increases and in turn a progressive increase in the antagonistic CWT activity directed toward maintaining extension of the spine and preventing deformation. We also found that the volume dependence in the upright posture was almost twice that in the supine posture (P < 0.02; Fig. 9). However, we were unable to detect a difference between the upright and supine EMG for the Ps or any CWT muscle at either high or low lung volume (P > 0.09). Presumably, this was due to the difference in the variability between the two sets of comparisons. The coefficient of variation for the differences in EMG between postures at a given lung volume was much greater than that for the volume-dependent difference in EMG in either the upright or supine posture. For a given
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change in lung volume, the change in rib cage volume is considerably less in the supine compared with the upright posture (14). Consequently, between 40 and 80% VC the change in the rib cage volume in the supine posture is systematically less than that in the upright posture. Because all of the CWT muscles insert into the rib cage, we speculate that the mechanical linkage and geometric relationships change less in the supine than in the upright posture for a given change in lung volume. Therefore, at iso-Pmus, an increase in lung volume from 40 to 80% VC may require less CWT muscle activation in the supine than in the upright posture. Implications of CWT Recruitment to Energetics
An unexplained and consistent observation in respiratory muscle energetics is the relatively low inspiratory muscle efficiency (4, 15). One possible explanation for this discrepancy is that whereas total energy consumption can be determined relatively accurately, the work of breathing as represented by the pressure-volume diagram is underestimated. This is quite likely, as the work of deformation at high inspiratory pressures could be substantial and is not recorded. However, the results of the present study suggest another basis for the low values of respiratory muscle efficiency during loaded breathing. The generalized recruitment of CWT muscles acting as fixators and contracting isometrically must contribute substantially to the total 0, costs. Furthermore, because of their greater recruitment as a function of Pmus, the greater 0, cost (and hence lesser efficiency) as the pressure increases even at a constant work rate could be accounted for. A third implication of this study relates to the volume dependence of inspiratory muscle efficiency under conditions of identical work rate and pressure-time products (3). Because of the volume dependence of recruitment of the CWT muscles, a greater 0, cost and hence a lesser efficiency at higher lung volumes is predictable. The fourth implication of this work relates to our findings comparing the sensitivity of the 0, cost of breathing to changes in the pressure-time product at iso-work rates between ventilatory and pressure loads (1). We found that when breathing against high ventilatory loads (and hence at high lung volumes) the 0, cost of breathing at a given work rate is very sensitive to changes in pressuretime product. In contrast, when breathing against high pressure loads (at a volume close to FRC) efficiency was relatively uninfluenced by large changes in pressure-time product. To the extent that 0, cost correlates with EMG activity, the steeper relationship between EMG of the CWT muscle and Pmus at high lung volumes (Figs. 5-8) predicts a much greater change in energy cost as a function of inspiratory pressure than at low lung volumes. In summary, we found that the EMG of the four CWT muscles increases as a function of the inspiratory muscle pressure generated at a given lung volume. We hypothesize that the CWT muscles actively participate in the generation of inspiratory pressure by extending the spine (ES), elevating the ribs (LD and PM), stabilizing the sternum, and fixing the shoulder girdle (LD, PM and Tr). The volume-dependent increase of the Ps and CWT
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EMGs at a given Pmus in both postures may be related to a decreased mechanical advantage of these muscles as volume increases. The greater volume dependence of the CWT EMGs in the upright posture may reflect greater changes in the mechanical linkage between the CWT muscles and the rib cage because of the systematically greater changes in rib cage volume in the upright compared with the supine posture for equivalent differences in lung volume. The authors are grateful to Jeanette Walker for typing this manuscript. Present address and address for reprint requests: S. J. Cala, Meakins-Christie Laboratories, 3626 St. Urbain St., Montreal, Quebec H2X 2P2, Canada. Received 15 November 1991; accepted in final form 23 June 1992. REFERENCES S. J., J. EDYVEAN, M. RYNN, AND L. A. ENGEL. Oxygen cost of breathing; ventilatory vs. pressure loads (Abstract). Aust. N. 2. J. Med. 21, Suppl. 4: A666, 1991. 2. CAMPBELL, E. J. M. Accessory muscles. In: The Respiratory Muscles: Mechanics and Neural Control, edited by E. J. M. Campbell, E. Agostoni, and J. Newsom Davis. Philadelphia, PA: Saunders, 1970, p* 181-193. 3. COLLETT, P. W., AND L. A. ENGEL. Influence of lung volume on oxygen cost of resistive breathing. J. Appl. Physiol. 61: 16-24,1986. 4. COLLETT, P. W., C. PERRY, AND L. A. ENGEL. Pressure-time product, flow, and oxygen cost of resistive breathing in humans. J. Appl, 1. CALA,
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