Flow-volume curves of excised right and left rabbit lungs EIJI YOKOYAMA Department of Industrial
Health,
Institute
of Public
Health,
Tokyo, Japan
YOKOYAMA, EIJI. Flow-volume curves of excised right and Left rabbit lungs. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 46(3): 463-466, 1979.-Static pressure-volume (PV) curves and flow-volume (VV) curves of excised right and left rabbit lungs obtained by forced and passive deflation were compared. Deflation PV curves in which the volume was expressed as either ml/lung weight or percent total lung capacity were nearly identical between right and left lungs. Descending limbs of the forced VV curves in which the flow divided by vital capacity (VC) was plotted against %VC generally agreed between right and left lungs, although peak flow tended to be higher in left lungs. However, the flow obtained during passive deflation was higher in left lungs over most of the deflation suggesting that the resistance of proximal airways per unit volume is lower in left than in right lungs.
respectively. Because the right main bronchus was usually shorter than the left one, there was the possibility that in the case of the right main bronchus the tip of cannula could block some openings of airways branching from the main bronchus, resulting in decreased volume or flow. The flanged tip of cannula minimized this risk. We had to discard a few lungs because the length of right main bronchus was not long enough for the cannula to be safely inserted. PV curve with air. Technique and equipment used were essentially the same as described by Frank et al. (4). Lungs are degassed in a vacuum jar, and static inflation and deflation were repeated three times in a plethysmograph. A mean deflation PV curve was constructed from the second and third runs. Total lung pressure-volume curve; peripheral airway resistance; proximal capacity (TLC) was defined as the gas volume at the airway resistance elastic recoil pressure of lung (PL) of 30 cmH20. The gas volume remaining in the lung at 0 cmHz0 of PL was calculated by subtracting the tissue volume from the total volume of lung estimated by saline displacement ALTHOUGH the differential gas exchange and CO diffusion between right and left lung has been extensively studied (specific gravity of the tissue was assumed to be 1). VV curve. The technique used to measure VV curve is (3, 5, lo), relatively little information is available concerning differences in mechanical properties between outlined in Fig. 1. The lung was suspended vertically in right and left lung. Frank et al. (4) reported that in a cylindrical plastic box, 2.4 liters in volume, after the rabbits there is virtually no difference in static pressure- measurement of PV curve was completed. The cannuvolume (PV) curves between excised right and left lungs. lated bronchus was connected to a pneumotachograph In the present report I compare the PV curves as well as (Fleisch no. 0) placed outside the box. The rate of airflow the flow-volume (VV) curves of excised right and left was measured with a differential transducer (Nihon-Korabbit lungs. Such information is needed for evaluating den, Tokyo), and the volume was obtained by electrical integration of the flow signal. Transpulmonary pressure effects of inhaled noxious agents on the flow-resistive p-roperties using a recently developed technique (1,4) by (Ptp), the difference in pressure between the box and the cannula, was measured with a differential inductance which only one lung is exposed to the agents. transducer (Sanborn, Waltham, MA, model 268BC). A tap in the box was connected via a wide-bore, manual METHODS valve to either a suction line of a cleaner attached with Eleven male white rabbits weighing 2.0-2.8 kg (mean a volt-regulator or to a source of positive pressure of 2.4 kg) were killed by exsanguination from the abdominal approximately 50 cmHa0. The box could also be made aorta following anesthesia with intravenous pentobarbiopen to ambient atmosphere by removing the pressure tal sodium (30-40 mg/kg). The lungs were excised, the source. After the lung was kept inflated at Ptp of 30 m.ain bronchi of the right and left lungs were radially cut cmHz0 for 30 s, the box was vented to the pressure just below the carina, and the weight of each lung was source (forced deflation) or to ambient atmosphere (pasmeasured. sive deflation) by rotating the valve. Flow, volume, and A straight glass cannula of 0.6-cm internal diameter, pressure signals were simultaneously recorded on an inknarrowing with a flange to approximately 0.3 cm at its writing oscillograph, and the VV curve was traced on a tip, was tied to the cut edge of the bronchus around the storage oscilloscope (Matsushita, Tokyo, model VP058V) and photographed with a Polaroid camera. Usually flanged tip. The internal diameter of the tip was slightly b.roader for the cannula used for the right lung than for three curves were traced for both types of deflation and the left lung to such an extent that flow resistance at an a mean curve drawn by eye through two curves showing a:lrflow of 100 ml/s was 0.20 and 0.25 cmHzO/ml per s, the highest and the next to highest flow. The volume 0 ~61-7567/79/oooO-oooO$01.~5
Copyright
0
1979
the
American Physiological Society
463
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
464
( “I’ . w
E. YOKOYAMA Integrator 7 An Transducer -1 -
: crrv
Pneumotachograph
l&k
Compressor
tank
Pressue.
*
FIG. 1. Schematic diagram of method to measure forced VV curve. Pressure tank is a glass bottle, about 35 liters in volume. When measuring passive VV curve, pressure tank was removed from valve.
I Volt regulator
5
‘6
8
FIG. 2. Deflation PV curves of excised rab bit lungs. Volume is plotted as ml of gas per g of lu ng tissue. SoLid Lines: right lungs; dotted lines: left lungs.
10
20
30
K)
2030
lo
2030
PL
lo
2030
10
2030
.,mH20
measured during the forced deflation was defined as vital RESULTS AND DISCUSSION capacity (VC). The reproducibility of the curves was fairly good, the difference between the highest and the Ratio of wet to dry weight was nearly the same in the lowest flow at 30% VC being less than 10% in all cases of right and left lungs; means t SE are 4.70 t 0.07 and 4.67 passive deflation, and less than 15% in 14 cases of the t 0.09, respectively. forced deflation. Reproducible curves of similar degree Figure 2 shows the deflation PV curves of individual were obtained in the remaining six cases of the forced animals in which the volume is expressed as ml/g of the deflation by recording two or three more curves. Before lung weight. Interanimal variability was considerable, and after these measurements the volume of air remain- but-good agreement was observed in each rabbit between ing in the lungs at 0 Ptp was measured, and its change right and left lungs. As shown in Fig. 3, both lungs also was found to be negligible, ranging from 0 to 1 ml. After showed nearly identical curves when the same data were the experiment was completed, the lung was kept in an expressed as percent TLC. Thus the static mechanical properties of right and left lungs of rabbit can be regarded oven at 110°C for 38 h to obtain the dry weight. Only data from experiments in which both lungs as identical. showed no leaks during measurement of the PV curve Forced VV curves of individual animals are presented are presented. The paired difference between right and in Fig. 4 where flow expressed as VC per second is plotted left lungs was examined by Student’s t test. against %VC. Fairly large interanimal variability is again
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
VV
CURVES
OF
RIGHT-LEFT
80 60 7rrr 3
4
-
465
LUNG
6
-5
7
/
40
q
,/
f
20
.
co;;
10
20
30
-;-bnr
lo
20
30
I n
xl
30
FIG.
30
6
volume
lo2030
3. Same data as in Fig. expressed as %TLC.
2 with
a
6 6
>. B 10 e
\\ 9 50yx)
, 50
100
FIG. 4. Forced VV curves of same lungs shown in Fig. 2, except for I-ZO. 7 where measurement failed. Flow is plotted as VC/s, and volume as %VC. Curves obtained on right lungs and left lungs are represented as in Fig. 2.
-80 l>
6
v .,OIOVC observed. Although the peak flows tended to be higher the flow divided by TLC showed a similar trend. in the left than in the right lung, the last parts of the It was possible that differences in weight between the curves were nearly superimposed in almost all animals. right and left lungs produced differing degrees of lung A striking contrast was presented by the passive VV distortion while hanging from the bronchus, and the curves of the same lungs, as shown in Fig. 5. In this observed result in flow during passive deflation was decircumstance the flow was in all but one rabbit much pendent to a certain extent on such differences in lung higher in the left than in the right lung over almost the distortion. To understand this effect, I tried to record VV entire range of the expired volume. Means t SE of paired curve in lungs kept horizontal on a smooth plate, but difference in the flow at 50,40, 30, and 20% VC were 0.97 found reproducible recording to be difficult because the t 0.16, 0.82 t 0.14, 0.72 t 0.14, and 0.48 t 0.13 VC/s, contact of lung surface with the plate interrupted to a respectively. These differences were significant (P < variable degree the movement of lungs. 0.01). Whether the correction of the flow by VC was If the effect of lung distortion is assumed to be identical physiologically appropriate remains to be elucidated, but for both the right and left lungs, the following specula-
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
466
E. YOKOYAMA 6
8
6
50
tions may be possible. a) According to the analysis described by Mead et al. (8), the determinants of the flow obtained in forced deflation are elastic recoil of lungs and airflow resistance upstream to the equal pressure point (EPP). Because the elastic recoil of lungs is shown to be equal between both lungs judge d from the present PV curve, the upstream resistance per un.i.t volume is assumed to be equal between them. Precise loGion of EPP in rabbit airways is uncertain, but because it-is expected to move peripherally at lower lung volume (7, 8), the result on forced deflation suggests that there are no significant difference in the flow resistance of peripheral airway per unit volume between the right and left lungs. b) By definition, flow during passive deflation is driven by lung recoil force. Therefore, if the analysis for dogs’ lungs reported by Macklem and Mead (6), namely that the resistance of proximal airways is a large part of total pulmonary resistance, can be applied to rabbits’ lungs, it is suggested by the observation on passive deflation that the flow resistance in proximal airways per unit volume of right lungs is higher than that of left lungs, as indicated by the trend of peak flow in the left lungs during forced
loo
FIG. 5. Passive VV curves of same lungs shown in Fig. 4. Flow and volume are plotted as in Fig. 4. Curves obtained on right and left lungs are shown as in Fig. 2.
VV curves. We have no explanation for the cause of this difference, but there may be dimensional or structural differences of proximal airways between right and left lungs. Let us regard intact lung as a simple system consisting of two parallel compartments (right and left lung). If time constant (R x C) of these compartments is different, overall dynamic compliance of the system is expected to be frequency dependent according to the analysis reported by Otis et al. (9). I found that whole lung, in vivo and in vitro, of rabbits had the slightly frequency-dependent compliance when artificially ventilated (unpublished data), and the dynamic compliance of healthy human subjects was occasionally shown to be frequency dependent. Therefore, it seems interesting to confirm whether the above speculation, namely that the flowresistive properties are different between right and left lungs, is valid in intact lungs. I am grateful Received
6 June
to Mrs.
H. Arakawa
1978; accepted
for careful
in final
form
technical
16 October
assistance. 1978.
REFERENCES 1. ALPERT, S. M., AND T. R. LEWIS. Ozone tolerance studies utilizing unilateral exposure. J. Appl. PhysioZ. 31: 243-246, 1971. 2. BROWN, R., A. J. WOOLCOCK, N. J. VINCENT, AND P. T. MACKLEM. Physiological effects of experimental airway obstruction with beads. J. AppZ. Physiol. 27: 328-335, 1969. 3. CARLENS, E., AND G. DAHLSTROM. The clinical evaluation of bronchospirometry. Am. Reu. Respir. Dis. 83: 202-207, 1961. 4. FRANK, R., J. D. BRAIN, AND E. YOKOYAMA. Compression atelectasis: a method for unilateral ventilation of the lung. J. Appl. Physiol. 34: 704-707, 1973. 5. KANAGAMI, H., K. SUZUKI, T. KATSURA, T. SHIROSHI, K. BABA, AND A. MORI. On measurement of the CO pulmonary diffusing capacity in each lung by a modified end-tidal sampling method. Respir. Circ. 9: 169-l 79, 1961. 6. MACKLEM, P. T., AND J. MEAD. Resistance of central and peripheral
7. 8.
9.
10.
airways measured by a retrograde catheter. J. AppZ. Physiol. 22: 395-401, 1967. MACKLEM, P. T., AND J. MEAD. Factors determining maximum expiratory flow in dogs. J. AppZ. PhysioZ. 25: 159-169, 1968. MEAD, J., J. M. TURNER, P. T. MACKLEM, AND J. B. LITTLE. Significance of the relationship between lung recoil and maximum expiratory flow. J. AppZ. Physiol. 22: 95-108, 1967. OTIS, A. B., C. B. MCKERROW, R. A. BARTLETT, J. MEAD, M. B. MCILLROY, N, J. SELVERSTONE, AND E. P. RADFORD. Mechanical factors in distribution of pulmonary ventilation. J. Appt. PhysioZ. 8: 427-443, 1956. SVANBERG, L. Influence of posture on the lung volumes, ventilation and circulation in normals. &and. J. CZin. Lab. Invest. SuppZ. 25: 1-195, 1957.
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
Health,
Institute
of Public
Health,
Tokyo, Japan
YOKOYAMA, EIJI. Flow-volume curves of excised right and Left rabbit lungs. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 46(3): 463-466, 1979.-Static pressure-volume (PV) curves and flow-volume (VV) curves of excised right and left rabbit lungs obtained by forced and passive deflation were compared. Deflation PV curves in which the volume was expressed as either ml/lung weight or percent total lung capacity were nearly identical between right and left lungs. Descending limbs of the forced VV curves in which the flow divided by vital capacity (VC) was plotted against %VC generally agreed between right and left lungs, although peak flow tended to be higher in left lungs. However, the flow obtained during passive deflation was higher in left lungs over most of the deflation suggesting that the resistance of proximal airways per unit volume is lower in left than in right lungs.
respectively. Because the right main bronchus was usually shorter than the left one, there was the possibility that in the case of the right main bronchus the tip of cannula could block some openings of airways branching from the main bronchus, resulting in decreased volume or flow. The flanged tip of cannula minimized this risk. We had to discard a few lungs because the length of right main bronchus was not long enough for the cannula to be safely inserted. PV curve with air. Technique and equipment used were essentially the same as described by Frank et al. (4). Lungs are degassed in a vacuum jar, and static inflation and deflation were repeated three times in a plethysmograph. A mean deflation PV curve was constructed from the second and third runs. Total lung pressure-volume curve; peripheral airway resistance; proximal capacity (TLC) was defined as the gas volume at the airway resistance elastic recoil pressure of lung (PL) of 30 cmH20. The gas volume remaining in the lung at 0 cmHz0 of PL was calculated by subtracting the tissue volume from the total volume of lung estimated by saline displacement ALTHOUGH the differential gas exchange and CO diffusion between right and left lung has been extensively studied (specific gravity of the tissue was assumed to be 1). VV curve. The technique used to measure VV curve is (3, 5, lo), relatively little information is available concerning differences in mechanical properties between outlined in Fig. 1. The lung was suspended vertically in right and left lung. Frank et al. (4) reported that in a cylindrical plastic box, 2.4 liters in volume, after the rabbits there is virtually no difference in static pressure- measurement of PV curve was completed. The cannuvolume (PV) curves between excised right and left lungs. lated bronchus was connected to a pneumotachograph In the present report I compare the PV curves as well as (Fleisch no. 0) placed outside the box. The rate of airflow the flow-volume (VV) curves of excised right and left was measured with a differential transducer (Nihon-Korabbit lungs. Such information is needed for evaluating den, Tokyo), and the volume was obtained by electrical integration of the flow signal. Transpulmonary pressure effects of inhaled noxious agents on the flow-resistive p-roperties using a recently developed technique (1,4) by (Ptp), the difference in pressure between the box and the cannula, was measured with a differential inductance which only one lung is exposed to the agents. transducer (Sanborn, Waltham, MA, model 268BC). A tap in the box was connected via a wide-bore, manual METHODS valve to either a suction line of a cleaner attached with Eleven male white rabbits weighing 2.0-2.8 kg (mean a volt-regulator or to a source of positive pressure of 2.4 kg) were killed by exsanguination from the abdominal approximately 50 cmHa0. The box could also be made aorta following anesthesia with intravenous pentobarbiopen to ambient atmosphere by removing the pressure tal sodium (30-40 mg/kg). The lungs were excised, the source. After the lung was kept inflated at Ptp of 30 m.ain bronchi of the right and left lungs were radially cut cmHz0 for 30 s, the box was vented to the pressure just below the carina, and the weight of each lung was source (forced deflation) or to ambient atmosphere (pasmeasured. sive deflation) by rotating the valve. Flow, volume, and A straight glass cannula of 0.6-cm internal diameter, pressure signals were simultaneously recorded on an inknarrowing with a flange to approximately 0.3 cm at its writing oscillograph, and the VV curve was traced on a tip, was tied to the cut edge of the bronchus around the storage oscilloscope (Matsushita, Tokyo, model VP058V) and photographed with a Polaroid camera. Usually flanged tip. The internal diameter of the tip was slightly b.roader for the cannula used for the right lung than for three curves were traced for both types of deflation and the left lung to such an extent that flow resistance at an a mean curve drawn by eye through two curves showing a:lrflow of 100 ml/s was 0.20 and 0.25 cmHzO/ml per s, the highest and the next to highest flow. The volume 0 ~61-7567/79/oooO-oooO$01.~5
Copyright
0
1979
the
American Physiological Society
463
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
464
( “I’ . w
E. YOKOYAMA Integrator 7 An Transducer -1 -
: crrv
Pneumotachograph
l&k
Compressor
tank
Pressue.
*
FIG. 1. Schematic diagram of method to measure forced VV curve. Pressure tank is a glass bottle, about 35 liters in volume. When measuring passive VV curve, pressure tank was removed from valve.
I Volt regulator
5
‘6
8
FIG. 2. Deflation PV curves of excised rab bit lungs. Volume is plotted as ml of gas per g of lu ng tissue. SoLid Lines: right lungs; dotted lines: left lungs.
10
20
30
K)
2030
lo
2030
PL
lo
2030
10
2030
.,mH20
measured during the forced deflation was defined as vital RESULTS AND DISCUSSION capacity (VC). The reproducibility of the curves was fairly good, the difference between the highest and the Ratio of wet to dry weight was nearly the same in the lowest flow at 30% VC being less than 10% in all cases of right and left lungs; means t SE are 4.70 t 0.07 and 4.67 passive deflation, and less than 15% in 14 cases of the t 0.09, respectively. forced deflation. Reproducible curves of similar degree Figure 2 shows the deflation PV curves of individual were obtained in the remaining six cases of the forced animals in which the volume is expressed as ml/g of the deflation by recording two or three more curves. Before lung weight. Interanimal variability was considerable, and after these measurements the volume of air remain- but-good agreement was observed in each rabbit between ing in the lungs at 0 Ptp was measured, and its change right and left lungs. As shown in Fig. 3, both lungs also was found to be negligible, ranging from 0 to 1 ml. After showed nearly identical curves when the same data were the experiment was completed, the lung was kept in an expressed as percent TLC. Thus the static mechanical properties of right and left lungs of rabbit can be regarded oven at 110°C for 38 h to obtain the dry weight. Only data from experiments in which both lungs as identical. showed no leaks during measurement of the PV curve Forced VV curves of individual animals are presented are presented. The paired difference between right and in Fig. 4 where flow expressed as VC per second is plotted left lungs was examined by Student’s t test. against %VC. Fairly large interanimal variability is again
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
VV
CURVES
OF
RIGHT-LEFT
80 60 7rrr 3
4
-
465
LUNG
6
-5
7
/
40
q
,/
f
20
.
co;;
10
20
30
-;-bnr
lo
20
30
I n
xl
30
FIG.
30
6
volume
lo2030
3. Same data as in Fig. expressed as %TLC.
2 with
a
6 6
>. B 10 e
\\ 9 50yx)
, 50
100
FIG. 4. Forced VV curves of same lungs shown in Fig. 2, except for I-ZO. 7 where measurement failed. Flow is plotted as VC/s, and volume as %VC. Curves obtained on right lungs and left lungs are represented as in Fig. 2.
-80 l>
6
v .,OIOVC observed. Although the peak flows tended to be higher the flow divided by TLC showed a similar trend. in the left than in the right lung, the last parts of the It was possible that differences in weight between the curves were nearly superimposed in almost all animals. right and left lungs produced differing degrees of lung A striking contrast was presented by the passive VV distortion while hanging from the bronchus, and the curves of the same lungs, as shown in Fig. 5. In this observed result in flow during passive deflation was decircumstance the flow was in all but one rabbit much pendent to a certain extent on such differences in lung higher in the left than in the right lung over almost the distortion. To understand this effect, I tried to record VV entire range of the expired volume. Means t SE of paired curve in lungs kept horizontal on a smooth plate, but difference in the flow at 50,40, 30, and 20% VC were 0.97 found reproducible recording to be difficult because the t 0.16, 0.82 t 0.14, 0.72 t 0.14, and 0.48 t 0.13 VC/s, contact of lung surface with the plate interrupted to a respectively. These differences were significant (P < variable degree the movement of lungs. 0.01). Whether the correction of the flow by VC was If the effect of lung distortion is assumed to be identical physiologically appropriate remains to be elucidated, but for both the right and left lungs, the following specula-
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
466
E. YOKOYAMA 6
8
6
50
tions may be possible. a) According to the analysis described by Mead et al. (8), the determinants of the flow obtained in forced deflation are elastic recoil of lungs and airflow resistance upstream to the equal pressure point (EPP). Because the elastic recoil of lungs is shown to be equal between both lungs judge d from the present PV curve, the upstream resistance per un.i.t volume is assumed to be equal between them. Precise loGion of EPP in rabbit airways is uncertain, but because it-is expected to move peripherally at lower lung volume (7, 8), the result on forced deflation suggests that there are no significant difference in the flow resistance of peripheral airway per unit volume between the right and left lungs. b) By definition, flow during passive deflation is driven by lung recoil force. Therefore, if the analysis for dogs’ lungs reported by Macklem and Mead (6), namely that the resistance of proximal airways is a large part of total pulmonary resistance, can be applied to rabbits’ lungs, it is suggested by the observation on passive deflation that the flow resistance in proximal airways per unit volume of right lungs is higher than that of left lungs, as indicated by the trend of peak flow in the left lungs during forced
loo
FIG. 5. Passive VV curves of same lungs shown in Fig. 4. Flow and volume are plotted as in Fig. 4. Curves obtained on right and left lungs are shown as in Fig. 2.
VV curves. We have no explanation for the cause of this difference, but there may be dimensional or structural differences of proximal airways between right and left lungs. Let us regard intact lung as a simple system consisting of two parallel compartments (right and left lung). If time constant (R x C) of these compartments is different, overall dynamic compliance of the system is expected to be frequency dependent according to the analysis reported by Otis et al. (9). I found that whole lung, in vivo and in vitro, of rabbits had the slightly frequency-dependent compliance when artificially ventilated (unpublished data), and the dynamic compliance of healthy human subjects was occasionally shown to be frequency dependent. Therefore, it seems interesting to confirm whether the above speculation, namely that the flowresistive properties are different between right and left lungs, is valid in intact lungs. I am grateful Received
6 June
to Mrs.
H. Arakawa
1978; accepted
for careful
in final
form
technical
16 October
assistance. 1978.
REFERENCES 1. ALPERT, S. M., AND T. R. LEWIS. Ozone tolerance studies utilizing unilateral exposure. J. Appl. PhysioZ. 31: 243-246, 1971. 2. BROWN, R., A. J. WOOLCOCK, N. J. VINCENT, AND P. T. MACKLEM. Physiological effects of experimental airway obstruction with beads. J. AppZ. Physiol. 27: 328-335, 1969. 3. CARLENS, E., AND G. DAHLSTROM. The clinical evaluation of bronchospirometry. Am. Reu. Respir. Dis. 83: 202-207, 1961. 4. FRANK, R., J. D. BRAIN, AND E. YOKOYAMA. Compression atelectasis: a method for unilateral ventilation of the lung. J. Appl. Physiol. 34: 704-707, 1973. 5. KANAGAMI, H., K. SUZUKI, T. KATSURA, T. SHIROSHI, K. BABA, AND A. MORI. On measurement of the CO pulmonary diffusing capacity in each lung by a modified end-tidal sampling method. Respir. Circ. 9: 169-l 79, 1961. 6. MACKLEM, P. T., AND J. MEAD. Resistance of central and peripheral
7. 8.
9.
10.
airways measured by a retrograde catheter. J. AppZ. Physiol. 22: 395-401, 1967. MACKLEM, P. T., AND J. MEAD. Factors determining maximum expiratory flow in dogs. J. AppZ. PhysioZ. 25: 159-169, 1968. MEAD, J., J. M. TURNER, P. T. MACKLEM, AND J. B. LITTLE. Significance of the relationship between lung recoil and maximum expiratory flow. J. AppZ. Physiol. 22: 95-108, 1967. OTIS, A. B., C. B. MCKERROW, R. A. BARTLETT, J. MEAD, M. B. MCILLROY, N, J. SELVERSTONE, AND E. P. RADFORD. Mechanical factors in distribution of pulmonary ventilation. J. Appt. PhysioZ. 8: 427-443, 1956. SVANBERG, L. Influence of posture on the lung volumes, ventilation and circulation in normals. &and. J. CZin. Lab. Invest. SuppZ. 25: 1-195, 1957.
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (196.011.235.237) on August 13, 2018. Copyright © 1979 American Physiological Society. All rights reserved.
