mainly due to variability of the end-inspiratory point, although subjectively
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1 376 J. Physiol. (I950) III, I 6I2.2I7 THE NATURE OF THE LIMITATION OF MAXIMAL INSPIRATORY AND EXPIRATORY EFFORTS BY J. N. MILLS, Fellow of Jesus College, Cambridge From the Department of Physiology, University of Cambridge (Received 13 December 1949) The random variation in successive determinations of the vital capacity is mainly due to variability of the end-inspiratory point, although subjectively the limit of inspiratory seems much sharper than that of expiratory ability (Mills, 1949). The mode of limitation of maximal respiratory movements thus deserves study. This has been attempted by measuring the intra-abdominal pressure, by recording action potentials from muscles of the abdominal wall, and by observation of the glottis. METHODS AND SUBJECTS Fourteen healthy male subjects and one female subject were examined, supine on a level couch. Intra-abdominal pressure was recorded from a partly filled balloon in the stomach, connected to an optical manometer recording on photographic paper. Preliminary trials with the balloon in the rectum (Rushmer, 1946) were less successful as the balloon appeared to become kinked at times and failed to record known rises of pressure; on one occasion peristaltic waves of amplitude 30 mm. Hg were observed, at a frequency of about 2 per min. With the gastric balloon no such difficulty was encountered except when the subject was visibly retching. When rectal and gastric balloons were used simultaneously the pressures were the same to within 3 mm. Hg. The balloon was connected to Ryle's or pressure tubing as far as the mouth, thence by lead tubing to the manometer. All tubing was completely filled with water. The fidelity of the manometer was examined by enclosing the balloon in a jar of air at a pressure of mm. Hg above ambient, and suddenly releasing the pressure. The photographic pressure record fell to zero within 0 1 sec., but continued to oscillate detectably for 1-1I sec. at 2-3 cyc./sec. Calibration of the manometer against a mercury column was frequently performed. Deductions about the pressure exerted upon the balloon within the stomach depend upon its position, which was assumed to be 8 cm. above the surface of the couch. Errors of a few cm. in this height will have little effect. The balloon is thus presumed to be about 10 cm. below the anterior abdominal wall, and the hydrostatic pressure of overlying viscera will account for a considerable fraction of the resting pressure, of about 10 mm. Hg, leaving only a very small contribution for tone in the gastric and abdominal musculature. It is thus probable that the recorded pressure in the balloon was very close to the intra-abdominal pressure in this region. Rushmer (1946), using a rectal balloon in dogs and a direct record of intra-abdominal pressure, showed that the balloon gave an accurate reading. The gastric balloon has here been shown to give usually the same pressure as a rectal one, but to be more reliable owing to the absence of peristalsis, and the optical manometer will give a more accurate record of rapidly changing pressures than the liquid manometers used by Rushmer.
2 MAXIMAL INSPIRATION AND EXPIRATION 377 Pressure inside the trachea was recorded from a similar, but air-filled, manometer connected to a needle of internal diameter 1 mm. inserted in the trachea. When air in the manometer connexions was raised to pressures of 50, 100 and 150 mm. Hg above atmospheric and then allowed to escape to the room through the needle used in the trachea, the pressure record fell to zero within 0-10, 0413 and 0*15 sec., and showed no subsequent oscillation. Any delay in recording pressure changes is therefore trifling. Respiration was recorded with a Benedict type spirometer, whose movement caused a small light source to travel across the camera. Observations of the vocal cords were made by Mr K. F. Wilsdon by indirect laryngoscopy. Action potentials were recorded by Dr W. A. H. Rushton from the usual type of concentric electrodes inserted into the abdominal muscles. The subject was earthed through the mouth, and the hypodermic needle and central wire led to the input of a differential amplifier. A small coupling condenser was interposed between amplifier and cathode-ray output stage (CR =5 msec.) to pass the muscle spikes and restrain the swings of base-line due to electrode movement, etc. A simultaneous respiratory tracing was obtained from a Krogh spirometer connected to a light source. Abdominal pressure RESULTS Abdominal pressure records were obtained from six male and one female subjects. Upon maximal expiration the pattern of behaviour was remarkably uniform. The abdominal pressure rose very little until expiration was nearly complete, when it rose sharply as the last small volume of air was expired, as the records 2 A SpirometerI 21[ A _140 *- 1 _ Time=1 sec : E B Spirometer 80 E 0 1;00 W ~~~~~~~~~~~~~~~~~~~~~~~~~~~~ Manometer 40 0 a Fig. 1. Spirometer movement and abdominal pressure during maximal expiration. Subject A, J. N. M.; B, J. C. L. R. A gap of 4 sec. occurs in B. Inspiration downwards. Read from right to left. in Fig. 1 show. Over 5-10 sec. while the abdominal pressure was high an extra c.c. of air was expired. Only very rarely did the spirometer stop moving for a brief period. The peak pressures reached are shown in Table 1, and were very variable. The peak pressure on coughing was usually comparable, but varied even more with the vigour of the cough. Upon maximal inspiration the abdominal pressure also rose, and often to a high level; but the spirometer either stopped moving completely for up to 12 sec. except for oscillations of instrumental origin, as in Fig. 2 A, or it moved
3 378 J. N. MILLS in a series of irregular jerks separated by stationary periods, as in Fig. 2B. The subject appeared to be making either a sustained effort or a series of spasmodic ones. The highest abdominal pressures were always recorded when the spirometer was stationary. If the subject relaxed a little and then made a second attempt, the abdominal pressure fell and only rose again when the spirometer had once more come to rest. It appeared that high abdominal pressures were associated with unsuccessful attempts to increase inspiration. TABLE 1. Peak intra-abdominal pressures in mm. Hg during maximal respiratory movements Maximal expiration Maximal inspiration r No. of No. of No. of observa- Peak observa- Peak observa- Peak Subject tions pressures tions pressures tions pressures J. N. M * * J. H. W C. J. P over 133 J. C. L. R R. J. V W. H. C J. R. J. M * Perhaps higher, as peak pressure was often outside the recorded range. 11 A Coughing A 4) E._ E ManometertO Spirometer I E V a) M. Fig. 2. Spirometer movement and abdominal pressure during maximal inspiration. Subject A, J. N. M.; B, J. C. L. R. A gap of 4 sec. occurs in B. Inspiration downwards. Read from right to left. Four records were obtained upon J. N. M. of the tracheal pressure upon maximal inspiration. It was found that while the spirometer was stationary at the end of inspiration and the abdominal pressure exceeded 143 mm. Hg, the tracheal pressure was maintained at mm. with occasional brief rises to mm. The high pressures recorded for J. N. M. with all procedures were probably due to frequent practice and to familiarity with the discomforts involved.
4 MAXIMAL INSPIRATION AND EXPIRATION Abdominal electromyograms The needle electrode was inserted into either obliquus externus or rectus abdominis. A satisfactory position was confirmed by observing abundant action potentials when the subject strained. Sweeps lasting about 0416 sec. were photographed on moving paper at intervals of sec., with a continuous spirometer record. Records of maximal expiration, maximal inspiration and coughing were made on ten subjects. Discharge always occurred Volume in litres A Fig. 3. Electromyographic sweeps of 160 msec., at 600 msec. intervals, from obliquus externus abdominis, with continuous spirometer tracing. A, maximal expiration; B, maximal inspiration; C, coughing. Expiration to left. Read from top to bottom and left to right. during maximal expiration and coughing, as might be expected. In addition, seven subjects, including those three upon whom abdominal pressures had also been recorded, showed potentials during maximal inspiratory effort, when the movement of the spirometer had ceased. These were usually fewer than during maximal expiration, either in duration as in Fig. 3, or in frequency. In one
5 380 J. N. MILlS record spikes were observed during the brief inspiratory phase of a cough. It was not easy to pick out recognizable units firing at a steady frequency, so no further analysis of the records was attempted. Behaviour of vocal cords Mr K. F. Wilsdon examined the glottis of J. N. M., upon whom a rise of pressure in the abdomen and action potentials in the abdominal wall had been recorded regularly during maximal inspiration, and observed that, after the wide abduction of the vocal cords during inspiration, the cords were closely approximated and remained so during sustained and repeated inspiratory efforts. With the help of his Registrar he also examined twenty-three hospital out-patients, of whom nine showed the same closure of the glottis at the end of a sustained effort to inspire. DISCUSSION It seems clear from these experiments that the limit to maximal expiration is reached when the muscles of chest and abdominal wall are bringing their maximum force to bear in collapsing the chest and forcing the diaphragm upwards. At the end a very large rise in abdominal pressure only forces a small amount of extra air out of the lungs, and despite considerable variations in the pressure developed in the abdomen a fairly constant end-expiratory level is reached, with a variation of + 40 c.c. (Mills, 1949). The only point of interest is the very high pressures that can be developed, and it is not surprising that such powerful respiratory movements can profoundly affect the circulation (Woodbury & Abreu, 1944). It appears that maximal inspiration is, commonly at least, terminated by closure of the glottis, accompanied by contraction of the muscles of the abdominal wall which raises both intra-abdominal and intrapulmonary pressures. No attempt has been made to find out whether this response is universal, and the three components were observed, for the most part, upon different subjects. All the subjects examined showed a high intra-abdominal pressure during maximal inspiratory effort, and although the pressure reached was often considerably less than that attained on maximal expiration the lowest pressures were still mm. Hg above the pressure recorded during quiet breathing. The absence of recorded action potentials in the abdominal musculature in three subjects might indicate either absence of muscular activity in those subjects, or activity of relatively few units, none of which was picked up by the electrodes. The failure of the vocal cords to approximate in some subjects might likewise be due to a different behaviour by those subjects, or to an inability to make maximal inspiratory movements when subjected to the moderate discomfort of traction on the tongue.
6 MAXIMAL INSPIRATION AND EXPIRATION 381 This involuntary closure of the glottis accounts simply for the variability of volume of maximal inspirations together with the subjective feeling of a very definite end-point (Mills, 1949). It also accords well with the very usual form of tracing of a vital capacity determination on a moving drum, when expiration appears to approach a final volume asymptotically whilst inspiration reaches a definite end-point or ends with a series of irregular jerky movements. When the glottis has once closed it seems that more air can only be inspired by relaxing, usually letting a little air out, and trying again. This paradoxical end-inspiratory phenomenon might be a reflex consequence of pulmonary inflation, or it might be a direct consequence of excessive discharge by the inspiratory centre. The latter possibility is supported by observations on two subjects of electromyographic activity in the abdominal wall on attempting to inspire against closed mouth and nose from the normal endexpiratory position. If one subscribes to the belief that all physiological phenomena have functional significance, this might be sought in protection of the lungs from over-distension, or in the promotion of increased venous return to the right side of the heart. SUMMARY 1. A high intra-abdominal pressure is developed at the end of maximal inspiratory as well as of maximal expiratory efforts. Intratracheal pressure also rises at the end of a maximal inspiratory effort. 2. The vocal cords are often closely approximated during final efforts at inspiration. 3. Action potentials can often be recorded from muscles of the abdominal wall in maximal inspiration, as well as in maximal expiration and coughing. 4. It is concluded that maximal inspiration is usually terminated by closure of the glottis and contraction of the muscles of the abdominal wall. My thanks are due to Mr K. F. Wilsdon for laryngeal observations and for the insertion of a needle in the trachea, to Dr W. A. H. Rushton for recording the electromyograms, to all those who have acted as subjects, and to Mr S. Langford for technical assistance. Note added in proof. Moritz (1895) recorded upon himself a rise of 51 cm. H20 in the intra-abdominal (intragastric) pressure on maximal inspiration. REFERENCES Mills, J. N. (1949). J. Phy8iol. 110, 76. Moritz (1895). Z. Biol. 32, 336. Rushmer, R. F. (1946). Amer. J. Phy8iol. 147, 242. Woodbury, R. A. & Abreu, B. E. (1944). Amer. J. Phy8iol. 142, 721.
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