The Maximum Expiratory Flow Rate and Volume Dependent Respiratory Resistance in Small Airway Obstruction
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1 Tohoku J. exp. Med., 1976, 120, The Maximum Expiratory Flow Rate and Volume Dependent Respiratory Resistance in Small Airway Obstruction HIDETADA SASAKI, WATARU HIDA and TAMOTSU TAKISHIMA The First Department of Internal Medicine, Tohoku University School of Medicine, Sendai SASAKI, H., HIDA, W. and TAKISHIMA, T. The Maximum Expiratory Flow Rate and Volume Dependent Respiratory Resistance in Small Airway Obstruction. Tohoku J. exp. Med., 1976, 120 (3), In 8 healthy subjects (group A) and 4 subjects with respiratory symptoms (group B), the lung pressure-volume curve (P-V curve), maximum expiratory flow-volume curve (MEFVC) and respiratory resistance (Rrs) at all vital capacities were measured. To avoid laryngeal artifact on a mouth pressure, an intratracheal catheter was used for measurement of Rrs which was obtained with 3 cycles/sec oscillatory forced pressure. Group B did not show a different elastic recoil from group A. In comparison of the maximum expiratory flow (vmax) at 80, 70, 60 and 50% of the total lung capacity (TLC),Vmax of group B showed lower values than that of group A. Rrs was almost the same in both groups from 70%TLC upwards, but Rrs of group B was higher than that of group A from 65%TLC downwards. Since the lung elastic recoil pressures (Pat (1) ) in the two groups were not different and Rrs's were different significantly only at low lung volumes, the decrease in Vmax of group B was supposed to be due to the increased Rrs which might reflect small airway obstruction. maximum expiratory flow; respiratory resistance; lung volume; pressure-volume curve It has been recognized that the conventional techniques such as the measure ment of airway resistance are not useful for detecting the early stage of small airway disease (Macklem and Mead 1967; Brown et al. 1969; Woolcock et al. 1969). On the other hand a decrease in Vmax has been supposed to be due to an increased upstream resistance, therefore, this can be used to detect the early stage of an airway obstruction (Mead et al. 1967). Macklem and Mead (1967) devided the airway resistance into central and peripheral airway resistances on the basis of results of examination with their retrograde catheter technique. They proved that a peripheral resistance was too small to be detected at high lung volumes, but it increased to 15% of a total airway resistance at low lung volumes. Their results suggest that the increase in the peripheral airway resistance which occurs at the early stage of airway obstruc tion may contribute significantly to total airway resistance at low lung volumes, while at high lung volumes it may not. If a decrease in Vmax is accompanied by a marked increase of Rrs at low lung volumes and other normal mechanical Received for publication, May 11,
2 260 H. Sasaki et al. factors of the lung, a major factor causing a decrease in Vmax may be an increase in the peripheral airway resistance. To investigate the above-mentioned problem, we analyzed P-V curve, MEFVC and respiratory resistance in 8 healthy subjects and 4 symptomatic subjects who might have the small airway obstruction. SUBJECTS AND METHODS The subjects were 8 normal volunteers (Subjects Nos. 1-8, group A) who had no history of lung or heart disease. Details of their physical characteristics are given in Table 1. The subjects Nos (Group B) were respiratory symptomatic out-patients of internal medicine of the Iwaki Kyoritsu Hospital. The chief complaints were described in Table 1. They showed no stridor symptoms, and their chest X-ray examinations and ECG's were normal. They were not treated with any bronchodilator drugs before the present examination. TABLE 1. Physical characteristics of subjects In parentheses are percentages of predicted normal values based on J.E. Cotes: Lung Function, 1968, p MEFVC was studied with the flow-volume curve recorder (CHEST, Japan) (Takishima et al. 1972) in the sitting position, and the examination was repeated several times in each subject to obtain reproducible results. The curve with maximal flow was selected for analysis. Forced expiratory vital capacity measurements were carried out with Collin's 13.5 liter respirometer of Benedict-Roth type. The lung volume was measured at least three times in each subject by a spirographic display of functional residual capacity and other lung volumes (Okubo et al. 1972). The concentration of He gas was measured with a He-analyzer (CHEST, Japan). Its accuracy was checked to be within 0.5%. Then the subject was seated in an air conditioned volume-displacement body plethysmo graph. The volume signal was obtained with a Krogh spirometer attached to the Sanborn linear transducer (535 DL, 1000 Bm). Transpulmonary pressure was measured as the difference between esophageal pressure and mo ith pressure using a differential pressure transducer (DLP1J 0.05 Nihon-Koden, Japan) with the same way of Milic-Emili et al. (1964). The subjects were breathed through a Fleish-type pneumotachograph coupled with a high sensitive transducer (RP-2, Nihon-Koden, Japan). The pressure, volume and flow curves were recorded on a pen writing four-channel recorder (8 S, Sanei, Japan). The static deflation pressure-volume curves were recorded during 2 sec interruption of expiratory flow from the full inflation to the residual volume (RV). This was repeated three times.
3 Analysis of Maximum Expiratory Flow 261 A side-tracheal pressure was measured by the tracheal catheter in order to avoid the laryngeal resistance. The respiratory resistances (Rrs) were measured by the forced oscillatory method using a tracheal pressure. A tracheal catheter was introduced by the procedure of Vincent et al. (1970). The catheter was a device commercially available (Venula, Top, Japan) which consists of an inner steel 18-gauge needle and a closely fitted outer plastic cannula (16-guage). The inner needle was withdrawn after insertion. As an aseptic technique, the puncture site was scrubbed with alcohol and 3 ml 1% Xylocain was infiltrated from skin to trachea. The cannula was then inserted at the level of the second or third tracheal cartilage. At first, the subjects lay supine for insertion of the cannula. The cannula tip was inserted 1 cm at most into the tracheal lumen to obtain the laryngeal pressure and the outer cannula was kept at right angle to the trachea with glue bundle. Air was occasionally flushed through the cannula with a syringe to ensure freedom from obstruct ing fluid menisci. After the subject satin the body plethysmograph, aloud speaker-amplifier system provided with a variable frequency sine wave generator was used to impose the pressure waves of 3 cycles/sec. Fig. 1 shows an example of tracings which was obtained from the full inflati n to RV. The speed of expiration was liter/sec. The top tracing is the time signals of 1 sec interval. To calculate Rrs a faster paper speed than that of Fig. 1 was used, and effective resistance was calculated by the graphical method of Goldman et al. (1970). This procedure was also repeated several times. Fig. 1. Tracings obtained during measurement of respiratory resistance (Rrs) on deflation from TLC. Top tracing is a time line with marks indicating 1 sec intervals. The calculation of resistance was obtained with another suitable faster paper speed following the way of Goldman et al. (1970).
4 262 H. Sasaki et al. RESULTS Spirographic studies and lung volumes were shown in Table 1. These values were within normal limits for healthy subjects as reported by Cotes (1968). Fig. 2 shows the relation of static recoil pressure (Pst (1)) to lung volume, where dotted lines show the results from group A and continuous lines from group B. In every case the curves were reproducible and showed no significant shifts with repeated measurements. Each curve of all subjects lay within the same range of data of healthy subjects studied by Turner et al. (1968). Small horizontal bars at low lung volumes represent the functional residual capacity (FRC). We could not find a significant difference between the two groups. In Fig. 3, MEFV was represented by %TLC for lung volume and Vmax/TLC for Vmax (Zapletal et al. 1969). Marks of lines are the same as those in Fig. 2. Vmax of group B is considerably lower than that of group A except near RV. The mean values and standard deviations of Vmax/TLC at 80, 70, 60 and 50% TLC of both groups are shown in Table 2. The difference between them was statistically significant (un paired t test: p<0.01 at 80 and 70 %TLC, p<0.02 at 60 %TLC, p<0.05 at 50 %TLC). Fig. 4 shows the values of Rrs of subject No. 11 which were calculated at every 0.1 liter volume interval. In all subjects the values of Rrs at every 0.1 liter volume.interval were averaged at every 0.5 liter volume interval and mean values of Rrs calculated in this way were expressed as a specific resistance multiplying TLC to Rrs. Fig. 2. Pst (1) versus %TLC curves of all subjects. Dotted lines and continuous lines are for subjects Nos. 1-8 and Nos respectively. Horizontal small bars indicate their FRC.
5 Analysis of Maximum Expiratory Flow 263 Fig. 3. Maximum expiratory flows normalized with TLC versus %TLC curves of all subjects. Marks of both groups are the same as Fig. 2. The continuous lines are considerably low in every lung volume. TABLE 2. The mean values }S.D of v max/tlc (1/sec) Fig. 4. Graph of Rrs versus lung volume in subject No. 11. Rrs was calculated at every 0.1 liter volume interval.
6 264 H. Sasaki et al. Fig. 5. Rrs normalized with TLC versus %TLC curves of all subjects. Marks of lines are the same as in Fig. 2. Continuous lines show increased Rrs at low lung volumes, while Rrs at high lung volumes are almost the same as dotted lines. TABLE 3. The mean values±s.d. of Rrs ~TLC (cmh2o ~sec) The relationship between specific resistances and lung volumes were shown in Fig. 5 with the same marks of Fig. 2. All curves demonstrated the hyperbolic relation ship between Rrs and lung volumes. The increases of Rrs in group B were steeper at low lung volumes than in group A. The mean values at different lung volume from the curves of Fig. 5 were shown in Table 3 with the standard deviationṣ The difference in Rrs between two groups was not significant from 70 %TLC upwards, but highly significant from 65 %TLC downwards (un-paired t test p<0.01). DISCUSSION Concerning the determinants of Vmax, early theoretical considerations were based upon the Starling resistor and the equal pressure point (EPP) concept. The Starling resistor concept (Permutt and Pride 1964; Pride et al. 1967) states that during expiration the airways peripheral to those being compressed at Vmax acts as
7 Analysis of Maximum Expiratory Flow 265 a fixed resistor of the so-called Starling resistor system. The EPP concept (Mead et al. 1967) extended the Starling resistor concept of Vmax, so that the airways being compressed are in the downstream from the point where the intrabronchial pressure is equal to intrathroacic pressure (EPP). Furthermore, the EPP concept states the air flow resistance of the airways in the upstream from the EPP (Rup) and static recoil pressure (Pst (1) ) determine the Vmax according to the formula Pst(l) = [Vmax] ~ [Rup]. According to the EPP concept, Macklem and Mead (1968) concluded, from the dog experiments, that the most important determinants of Vmax at high lung volumes were the cross-sectional area at EPP and Pst (1), whereas at low lung volumes the frictional resistance of airways in the upstream from EPP and Pst (1). Recently Takishima and Sasaki (1972) have investigated from a two-dimensional flow model that the Vmax was inversely proportional to the products of the airway resistance in non-compressed state by the airway compliance. Also Takishima et al. (1975) have shown the airway compliance of dog lobes was inversely proportional to the Pst(1). These theoretical and experimental considerations have all emphasized that the determinants of Vmax are lung recoil pressure and airflow resistance. In the present study all subjects showed normal chest X-ray examinations and no differences in the Pst (1) between two groups. As there were no asthmatic subjects, we also might neglect the particular effects of smooth muscle contraction on the airway compliances, which was reported by Olsen et al. (1967). These condition may allow that the airway compliances were not different in both groups. Therefore it was suggested that the decrease in Vmax at low lung volumes in group B could be caused by an increase of airway resistance. This was supported by elevated respiratory resistance at low lung volumes. However, as investigated by Macklem and Mead (1967) and Hogg et al. (1968) with the retrograde catheter method, the peripheral airway resistance did not contribute to total airway resistance at high lung volumes, but 25% of total airway resistance in normal human lungs. This means that a respiratory resistance may not detect the slight increase of peripheral airway resistance. Furthermore, if the respiratory resistance was measured by the pressure and flow at mouth, changes in peripheral airway resistances were further masked, because, as reported by Spann and Hyatt (1971), the laryngeal resistance was as large as 37% of total airway resistance during quiet breathing. But this is not the case in the present study, because tracheal pressure was measured. On the other hand Hogg et al. (1968) reported that the peripheral airway resistance in chronic obstructive lung disease was increased extremely beyond the central airway resistance. Experimentally Brown et al. (1969) investigated the relationship of the airway resistance and the lung volume in the excised dog lobes which was insufflated with small beads in the peripheral bronchi, and found that the airway resistance was not increased at high lung volumes but increased at low lung volumes. This is also the case in the present study and it was assumed that considerable small airway obstruction had occurred in group B.
8 266 H. Sasaki et al. According to Macklem and Wilson (1965), the EPP moves further into peripheral airway in a condition of increased peripheral airway resistance, and an increase of peripheral airway resistance may be caused by increased airway compression. Also there is the evidence that some part of peripheral airway may be under dyna mic compression in severe chronic obstructive lung disease (Silvers et al. 1974). In this case we may not conclude an increase of respiratory resistance at low lung volumes is the primary factor of decreased Vmax at low lung volumes. However, the present subjects were all normal in forced expiratory volume. Therefore, for an explanation of the present results it nay not be necessary to introduce the concept of peripheral dynamic compression which was suggested in severe obstructive lung disease by Silvers et al. (1974). Finally, though we have shown the Vmax and Rrs normalized by TLC, the results of absolute values of Vmax and Rrs were almost the same as normalized ones. The normalization with TLC was thought to be a reasonable way in respect of the results of Zapletal et al. (1969) who reported that TLC, Vmax and airway conductance increased proportionately between ages 6 and 18 years. In conclusion our symptomatic subjects were assumed to have an early small airway disease on the basis of an increased respiratory resistance at low lung volumes but not at FRC as compared with healthy subjects. This was thought to be a result in a decrease of Vmax at low lung volumes. Therefore a decrease of Vmax at low lung volumes was proved to be a useful index for the detection of early small airway obstruction as has been suggested from the theoretical background. References 1) Brown, R., Woolcock, A.J., Vincent, N.J. & Macklem P.T. (1969) Physiologic effects of experimental airway obstruction with beads. J. appl. Physiol., 27, , 2) Cotes, J.E. (1968) Lung Function. 2nd ed., Blackwell Scientific Publications, Oxford and Edinburgh, p ) Goldman, M., Knudson, R.J., Mead, J., Peterson, N., Schwaber, J.R. & Wohl, M.F.. (1970) A simplified measurement J. appl. Physiol., 28, of respiratory resistance by forced oscillation. 4) Hogg, J.C., Macklem, P.T. & Thurlbeck, W.M. (1968) Site and nature of airway obstruction in chronic obstructive lung disease. New Engl. J. Med., 278, ) Maclem, P.T. & Mead, J. (1967) Resistance of central and peripheral airway measured by a retrograde catheter. J. appl. Physiol., 22, ) Macklem, P.T. & Mead, J. (1968) Factors determining maximum expiratory flow in dogs. J. appl. Physiol., 25, ) Macklem, P.T. & Wilson, N.J. (1965) Measurement of intrabronchial pressure in man. J. appl. Physiol., 20, ) Mead, J., Turner, J.M., Macklem, P.T. & Little, J.B. (1967) Significance of the relationship between lung recoil and maximum expiratory flow. J. appl. Physiol., 22, ) Milic-Emili, J., Mead, J., Turner, J.M. & Glauser, E.M. (1964) Improved technique for estimating pleural pressure from esophageal balloons. J. appl. Physiol., 19, ) Okubo, T., Teichmann, J. & Piiper, J. (1972) A method for spirographic display of functional residual capacity and other lung volumes. J. appl. Physiol., 33, ) Olsen, C.R., Stevcns, A.E. & Mellroy, M.B. (1967) Rigidity of tracheae and bronchi during muscular constriction. J. appl. Physiol., 23,
9 Analysis of Maximum Expiratory Flow ) Permutt, S. & Pride, N.B. (1964) The lung as a Starling resistor. Fed. Proc., 23, ) Pride, N.B., Permutt, S., Riley, R.L. & Bromberger-Barnea, B. (1967) Determinants of maximal expiratory flow from the lungs. J. appl. Physiol., 23, ) Silvers, G.W., Maisel, J.C., Petty, T.L., Filley, G.F. & Mitchell, R.S. (1974) From limitation during forced expiration in excised human lungs. J. appl. Physiol., 36, ) Spann, R.W. & Hyatt, R.E. (1971) Factors affecting upper airway resistance in conscious man. J. appl. Physiol., 31, ) Takishima, T. & Sasaki, H. (1972) Two-dimensional flow model for analysis of expiratory check valve. Bull. Physio-path. Resp., 8, ) Takishima, T., Sasaki, T., Takahashi, K., Sasaki, H. & Nakamura, T. (1972) Direct writing recorder of the flow-volume curve and its clinical application. Chest, 61, ) Takishima, T., Sasaki, H. & Sasaki, T. (1975) Influence of lung parenchyma on collapsibility of dog bronchi. J. appl. Physiol., 38, ) Turner, J.M., Mea, J. & Vhohl, M.E. (1968) Elasticity of human lungs in relation to age. J. appl. Physiol., 25, ) Vincent, N.J., Knudson, R., Leith, D.E., Macklem, P.T. & Mead, J. (1970) Factors influencing pulmonary resistance. J. appl. Physiol., 29, ) Wooleock, A.J., Vincent, N.J. & Macklem, P.T. (1969) Frequency dependence of compliance as a test for obstruction in the small airways. J. clip. Invest., 48, ) Zapletal, A., Motoyama, E.K., van de Woestijne, K.P., Hunt, V.R. & Bouhuys, A. (1969) Maximum expiratory flow-volume curves and airway conductance in children and adolescents. J. appl. Physiol., 26,
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