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Continuous recording of pleural surface pressure at various sites
Respiration Physiology (1973) 19, 356-368; North-Holland
CONTINUOUS
Pt+blishing Company, Amsterdam
RECORDING OF PLEURAL SURFACE PRESSURE AT VARIOUS SITES1
EDGARDO Istituto di Fisiologia
D’ANGELO
and EMIL10
Umana (I cattedra),
AGOSTONI
Uniuersitci di Milano, Milano, Italy
A method has been developed that enables continuous recording of pleural surface pressure in dogs without producing a pneumothorax. The end-expiratory values agree with those obtained with the counterpressure technique. The tidal changes are not systematically different at various sites. As with the counterpressure technique, we found that the vertical gradient of transpulmonary pressure disappears when the respiratory system is passively expanded and that a crania-caudal gradient of transpulmonary pressure is produced in the supine posture when the abdominal pressure is lowered. The kinetics of pleural pressure during spontaneous breathing in some cases differed among sites and among dogs. During inspiratory efforts the kinetics tended to become similar. During artificial ventilation small differences in kinetics occurred. Cardiac oscillations were recorded in the 3rd, 4th and 5th intercostal spaces, seldom in the 6th.
Abstract.
Cardiac oscillations of pleural pressure Kinetics of pleural pressure
Pleural pressure Vertical gradient of transpulmonary
pressure
In a previous research we developed a technique for the measurement of the pressure on the pleural surface at FRC or higher lung volume in the apneic animal without introducing anything into the pleural space (D’Angelo et al., 1970). This technique involved only a small incision of the parietal pleura. It was then modified in such a way as to avoid the incision and thus allow measurements at end inspiration and expiration in the spontaneously breathing animal (Agostoni and Miserocchi, 1970). We then attempted to develop a technique for the continuous recording of pleural surface pressure: a small circular area of the parietal pleura was thinned and a cup was glued to the surrounding endothoracic fascia. The parietal pleura thus acted as the membrane of the cup connected to a pressure transducer. The system was calibrated at the end of the experiment when the cup with the attached membrane was removed. This approach, however, failed probably because of the changing effect of the adhesive (Eastman 910) on the membranes
Accepted
for publication
17 August 1973.
’ This research has been supported by the National Research Council of Italy. 356
PLEURAL
PRESSURE
357
RECORDING
throughout the experiment and because for a given transmural pressure the tension of the membrane in uiuo was different from that in vitro. We therefore decided to use a capsule with an unstretched rubber membrane, which was brought into contact with the surface ofthe lung through a small incision of the endothoracic fascia and parietal pleura without producing a pneumothorax. This paper describes this technique and the results obtained with it. Methods
The device used to measure pleural surface pressure is illustrated in fig. 1. It consisted of an internal part of perspex and an external one of brass. The perspex cylinder had a small concavity on one end: a polyvinyl tube ( 1 mm o.d.) connected it through a 3 way stopcock to a pressure transducer (Sanborn 268 or 267). The system was filled with saline solution and a rubber membrane was tied on the concave end of the perspex cylinder. The rubber membrane was obtained from standard esophageal balloon and its stiffness was negligible relative to that of the transducer membrane. The brass part of the device was made of a short tube and of an external ring. The tube had a flange at one end and its internal diameter was such as to fit tightly on the perspex cylinder. An external ring with a rubber washer was loosely screwed on the external part of the tube. The external ring was screwed by means of a forceps the
Fig.
I Sectional drawing
of the device used to record
pleural
surface
pressure.
See text.
358
E.
D’ANGELO
AND
F. AGOSTONI
teeth of which fitted a couple of four holes pierced into the ring. Before assembling the device the brass part was kept around the polyvinyl tube between the perspex cylinder and the transducer. After having tied the rubber membrane on the perspex cylinder the brass part was pushed until the flange was on the same plane of the rubber membrane. By pushing the brass part in this sense the rubber membrane was not tensed. A perspex box with 4 holes in which the flange of the device could be sealed enabled the simultaneous calibration of 4 capsules. The perspex box contained air and was connected through short. wide bore tubes to a water manometer and to a pressure transducer. The pressure in the box (up to + 16 cm H,O) was changed both by steps or sinusoidally. The frequency response curve of the capsules was flat at least up to 5 cps. The calibration was repeated at the end of the experiment. The experiments were performed on dogs (8827 kg b.w.) anesthetized with sodium pentobarbital (35 mg,‘kg b.w. initial dose). The animals were in the lateral or supine posture. Generally 3 intercostal spaces (i.c.s.) on the right side were cleared of tissues down to the endothoracic fascia over an area of about 2 cm2. The respiratory system was then inflated to about 20 cm H,O and an incision of the endothoracic fascia and parietal pleura was done. The incision was a little shorter than the diameter of the flange of the capsule. The flange of the capsule was then inserted into the pleural space and the external ring screwed until the endothoracic fascia with the parietal pleura was squeezed between the rubber washer and the flange providing an airtight seal. The pressure on the airways was released and the zero level of the transducer was placed at the height of the capsule. The height of the site of measurement relative to the total height in a given posture was also measured. The esophageal pressure was measured through a standard esophageal balloon. A flow-meter was connected to the tracheal cannula. When the airways were closed to make measurements during inspiratory efforts the side tube of the tracheal cannula was connected to a pressure transducer. All signals were recorded on a Sanborn oscillograph. In one experiment the caudal part of the abdomen and the hind limbs of the supine animal were placed in a plethysmograph in which the pressure was lowered in order to simulate the effect of gravity on the shape of the chest wall in the head-up posture (Agostoni and D’Angelo, 1971). In some experiments the supine animal was paralyzed with an injection of succinylcholine, which was preceded by 5-10 mg;kg b.w. of anesthetics. In these animals measurements of pleural surface pressure were made after having inflated the respiratory system up to 20 cm H,O. Comments on the techniques The rubber membrane of the device remained essentially flat because the system was filled with liquid and the compliance of the transducer was low. The introduction of the flange into the pleural space caused a small distortion of the lung at the border of the flange, but the rubber membrane was far enough from
PLEURAL
the border
of the
flange
PRESSURE
(D’Angelo
and
359
RECORDING
Michelini,
1973).
The
weight
of the
capsule was 1.5 g and its center of gravity was 1.7 mm apart from the rubber membrane. Anyway small inclinations of the capsule with respect to its major axis did not modify the pressure measurements. Of more concern was the effect of the in-out movement of the intercostal space. We therefore determined in the apneic animal the change of pressure produced by small movement of the capsule in the direction normal to the surface of the lung. A rigid stick was fastened to the capsule and gently moved: its displacements were read on a scale fixed near the stick while the pressure changes were recorded. The results are shown in fig. 2. Moreover, in the breathing animal we measured the tidal in-out displacements of a point on a rib and of a point on the middle of the corresponding intercostal space or of the corresponding capsule by means of differential transformers (Lynearsin Sanborn 585DT). These were placed about 1 m apart from the rib cage: the thread coming from the core of the transformer was tied to a screw screwed into the rib, or to a hook placed in the intercostal muscles, or to the capsule. The weight of the core connected to the intercostal muscles or to the capsule was counterbalanced so that its pull was reduced to only 1 g. The outward disI
I
2-
I
:A kg
grd
ic.s. .
0 o-
_2_
qdog A 0 0
4 8, 6 II 7 ” 6
\
II
I
o-
\
-2-
in-,
-4
-2
8 I 0
displacement, Fig. 2. Changes
of pleural
surface
number
pressure
against
in each diagram
in-out
‘kl
out
I
‘6
-
2
4
mm artificial
displacement
refers to the intercostal
space.
of the capsule.
The
360
E. D’ANGELO
AND E. AGOSTONI
placement of the rib at end inspiration was greater than that of the intercostal space or of the capsule by less than 0.1 mm. During inspiratory efforts of about 20 cm H,O the inward displacement of the capsule was 0.2 mm greater than that of the corresponding rib. It appears from fig. 2 that the small difference between the tidal displacement of the capsule and of the corresponding rib does not affect the measurement. Only during strong inspiratory efforts the pressure on the intercostal space should have been barely affected by the inward movement of the capsule relative to the rib. But a difference of 0.24.3 cm H,O over a pressure change of about 20 cm H,O is negligible. Results and discussion Examples of tracing obtained by means of the capsule are shown in figs. 3, 4 and 5. The end-expiratory values of pleural surface pressure recorded at various heights are shown in fig. 6: they agree with the data previously obtained with the counterpressure techniques (D’Angelo et ul., 1970; Agostoni, D’Angelo and Bonanni, 1970; Agostoni and Miserocchi, 1970; Agostoni and D’Angelo, 1970) though in the supine posture the relationship tends to be a little more straight. The tidal changes of pleural surface pressure at various sites and of esophageal pressure are shown in table 1. In a given animal differences of about 1 cm H,O among sites occurred often (the maximum difference recorded was 1.9 cm H,O). These differences, however, are not systematic as shown by the following calculation. In each animal the tidal change at a given site was divided by the tidal change at the 5th intercostal space, the values so obtained for the various animals at a given site were averaged and each one multiplied by the average tidal change of the 5th i.c.s. The differences among sites so obtained were not significant. Hence, in line with the data obtained with the counterpressure techniques (Agostoni and Miserocchi. 1970). the tidal changes of pleural surface pressure over the intercostal surface may be considered similar. When an interlobar fissure was under the capsule the pressure measured was more negative by some cm H,O. Indeed in this case pleural liquid pressure instead of pleural surface pressure was measured (Agostoni, 1972). When the interlobar fissure moved under the capsule during inspiration the tidal change of pressure increased markedly because one shifted from end-expiratory surface pressure to end-inspiratory liquid pressure. The changes ofpressure occurring during the inspiratory efforts are illustrated in fig. 7 and summarized in table 1. Again there are no systematic differences of pressure changes among sites. The kinetics of pleural pressure during spontaneous breathing in some cases differed somewhat among sites and among dogs: most of the differences are illustrated by figs. 3, 4 and 5. These may be due to local differences in the resistance to the movement of the passive respiratory system and/or to local differences in the pattern of activity of the respiratory muscles. It can not be ruled out that the latter differences are a consequence of the experimental
PLEURAL PRESSURE RECORDING
a2
s -
0
.W -! -Q2
-1 f 0, I g-3
0
-
:: -b-
i -1 0, ;-3 e z-5 P -! G .
.
.
.._
:
:
.
..,
._,
I -1 9, = -3 : s-5
i
“f
Fig. 3. Tracings of lkm ~~xpii-~~ti~~il ncgawc).
csopha~c~~l prcssurc and pleural surtace pressure in the 3rd. 4th and 5th intercostal spaces. Time: 1 sec.Dog 2. latefal posture.
362
E. D’ANGELO
AND
E. AGOSTONI
-0.47
.> 0.4-
O0 I” E-4v cl!
0 I”
-8-O-
5 -4= L
0 r”
-8-
-2
E -6 ii p -10 I
-20 r I” 5 -6x L -lO-
Fig. 4. Tracings
negative). esophageal pressure and pleural surface of flow (expiration the 6th, 5th and 3rd intercostal spaces. Time: I sec. Dog 8. supine.
PIressure
in
PLEURAL
Fig. 5. Tracings pressure
conditions.
of pleural
surface
and flow (expiration
In most
PRESSURE
pressure
in the 3rd.
negative).
of the cases
Time:
363
RECORDING
5th and
7th intercostal
spaces,
esophageal
I sec.Dog 9: left: lateral: right: supine.
the expiration
was
quick:
the
flow abruptly
reached a peak and decreased then exponentially. This indicates that the expiration was passive. In these cases therefore the local differences in the kinetics of pleural pressure during expiration should be due to local differences in the resistance to the movement of the lung and/or the chest wall. In some cases during the last part of expiration pleural pressure in the 5th and 6th intercostal spaces increased above the resting value indicating a contraction of the abdominal muscles. During inspiratory efforts the kinetics of pleural pressure tended to become similar at various sites in spite of the differences occurring during spontaneous breathing. During artificial respiration small differences in the kinetics of the pleural pressure at various sites occurred in the inspiratory and expiratory phase.
TABLE Changes Animal
Site
of pleural
“~._“_~_. AP
tidal
effort
- 2.2
- 7.0
63
-3.0
-2.5
_
11.0
- 2.2
- 7.6
93
- 5.6
-2.0
-
11.8
- 1.8
-2.0
3rd
57
- 2.7
- 2.7
- 15.2
75
- 2.7
- 2.6
- 16.2
4th
22
- 1.4
- 3.4
- 17.0
70
-3.0
- 3.0
- 19.0
5th
85
- 3.9
- 2.6
- 16.8
66
-2.3
-2.4
- 19.1
- 3.0
- 16.2
- 3.0
- 18.9
3rd
46
- 3.0
-5.3
- 28.0
76
-3.5
-4.7
- 30.4
4th
26
-2.0
-4.9
- 26.0
69
-3.1
5th
82
-4.3
- 5.5
- 25.0 - 24.5
60
-2.5
- 5.0 -4.8
-28.5
-4.7
27.0
69
-3.3 -4.5
-4.4 -4.7
- 19.0
68
- 2.7
-4.0
- 15.8
86
- 17.0
60
- 2.4
-3.8
- 16.2
6th
20
- 1.3
-4.1
- 17.3
86
-4.7
- 3.4
- 17.1
-3.6 -3.7
- 13.4 - 12.7
3rd 5th 6th
- 14.2
- 17.5 - 20.0
74
- 3.0
- 5.0
-23.5
- 20.0
57
- 2.0
-4.5
- 24.0
-4.3
- 19.5
83
-4.0
- 5.5
- 23.5
-4.7
- 19.8
56
- 3.2
-4.5
86
-4.0 - 2.0
- 5.2
20
- 4.8
3rd
47
-3.0
- 5.8
- 14.9
65
-2.5
5th 6th
90 27
- 4.8
- 5.0
- 15.8
73
- 3.0
- 3.9 - 4.8
- 2.4
- 4.0
- 14.5
93
- 5.0
-4.6
15.6 - 15.8
-4.5
- 14.2
- 5.0
- 13.0
28
- 2.3
- 4.0
73
- 3.3
-4.0
- 12.5
5th
87
- 4.3
- 4.0
57
- 2.5
- 3.0
6th esoph.
18
- 1.5
-3.8
93
- 5.3
- 3.3
- 12.0 - 12.6
- 3.0
- 11.8
- 4.0
- Il.8
3rd 5th
65
- 3.0
-3.7
- 17.7
74
-3.2
- 3.0
93
- 4.2
-3.7
- 18.3
63
-2.3
-4.0
6th
35
-2.2
-3.9
- 19.4
90
-4.3
-3.2
-3.8
- 16.6
- 3.1
- 18.0
3rd
69
- 3.2
- 5.4
- 18.7
72
-2.8
- 5.2
- 19.7
5th
89
-4.2
-3.5
- 17.8
70
-3.0
- 20.0
7th esoph.
37
-2.0
-3.9
- 18.0
93
-4.6
- 4.2 - 3.8
- 4.2
- 18.7 - 18.3
alv. Intercostal
-
4th
esoph. alv.
l
- 14.7
- 15.0
- 15.7
alv.
9
- 24.0 - 23.5
- 19.3
alv.
8
- 29.0
3rd 5th
esoph.
7
_~
AP
- 3.9
esoph. alv. 6
Lateral ~_
effort
PP’ end exp.
- 1.6
esoph. alv. 5
and inspiratory
height
84
esoph. 4
breathing
5; lung
24
esoph. 3
spontaneous
effort
AP tidal
esoph. 2
during
AP
PPI end exp.
height
6th
pressure
Supine
y/,lung
iilinHth*
surface
1
space.
-4.4
-20.5 - 19.5 - 20.0
PLEURAL
PRESSURE
-s
4
pkural Fig. 6. Percentage at end inspiration.
symbol
surbce
refers to an animal.
from all the data obtained
-2
-1
surface pressure,cm
of lung height against pleural Each
-3
-1
365
REfORDiNG
0
i-l@
pressure in right intercostal The
line represents
with the counterpressure
region
of dogs
the best fir relationship
technique (Agostoni.
1972).
Cardiac oscillations of pleural pressure were recorded in the 3rd. 4th and 5th i.c.s. and only in one case in the 6th i.c.s.: their values are summarized in table 2. In some instances they were probably masked by higher frequency vibrations of the rib cage produced by intercostal muscles tremor. Since cardiac oscillations appeared in the flow tracing, cardiac oscillations of alveolar pressure should occur. These are probably caused by the movements of the heart and are TABLE
-.
Cardiac _
.-_.
oscillations
3rd i.c.s. -.. Lateral
Supine
* SE.
-.
Mid-axillary -.. __
2
of pleural surface pressure (cm HZO) at various sites -. 4th i.c.s. Dorsal .._.
Sth i.c.s.
6th i.c.s.
Ventral
Dorsal .-.
-
-..
Esophagus
-
-_
0.68 * 0.09*
0.80 + 0.20
1.10+0.16
0.31 +0.10
0.77+0.10
N=6
I%=3
N=8
K=6
N=U
1.cO+o.13
0.33 & 0.24
1.20~0.17
0. IO+ 0.0s
1.00~0.13
N=6
N=3
N=8
N=6
N=8
,-_
366
E. D’ANGELO
AND E. AGOSTONI
-0.4-
o-
f
-> 04-
O0 “-6 I
-
E t-12 I ‘L”-18-
9l =-6-
o-
-
E
u-12 -
t
-18 -
O0, I -65-12 *-I*
-
-3 c-9 I E U-151 z p-21_
O0 I” -6E “.-x2-E p -18-
Fig. 7. Tracings of flow (expiration negative), alveolar pressure, esophageal pressure. pressure in the 6th, 5th and 3rd intercostal spaces during an inspiratory effort against Time: I sec.Dog 8. supine.
pleural surface closed trachea.
PLEURAL
PRESSURE
367
RECORDING
transmitted to the pleural surface of the regions oscillations at one intercostal space were generally another space or with those of the esophagus. When the abdominal pressure of the supine dog decreased more in the cranial than in the caudal
close to the heart. Cardiac out of phase with those of was lowered pleural surface part. That is, by simulating
the effect of gravity on the chest wall shape occurring in the head-up posture. a crania-caudal gradient of transpulmonary pressure like that occurring in the head-up posture was produced in the supine posture. This finding in the breathing animal confirms our previous one obtained with the counterpressure technique in the apneic animal (Agostoni and D’Angelo, 1971). When the respiratory system of the supine dog was passively expanded the vertical gradient of transpulmonary pressure decreased and eventually disappeared (fig. 8). This confirms our previous data obtained with the counterpressure technique (Agostoni et al., 1970; Agostoni and Miserocchi, 1970). On the other hand, Lemelin et al. (1972) studying the distribution of regional lung volume from the dilution of 133Xe in seated man relaxing against positive air pressure found a crania-caudal difference of lung expansion similar to that occurring under normal conditions. They therefore concluded that the vertical pressure gradient of transpulmonary pressure did not decrease with passive inflation of the respiratory system. Since we confirmed our data with a different technique, and these data are in line with morphometric measurements in dogs (Glazier et al., 1967) and rabbits (D’Angelo, 1972). the discrepancy between our results and those of Lemelin et (11. may be due to a species difference. In this connection it must be considered that in the head-up man there are no marked differences of the shape of the rib cage between active and passive expansion above FRC (Agostoni.
._ 2 P 1
01 60
Ai,
0
4 V
i
Cl
s
0
x
1
x
V
0"s
0
a00
15
4
,
I
1
I
1
I
I
1
2
4
6
8
10
12
14
16
18
transpulmonary Fig. 8. Percentage values
of airway
v
0
10
01
V
I
of lung height pressure.
against
These values,
transpulmonary expressed
line. Each symbol
1
20
pressure, cmH@ pressure
in cm H,O,
in relaxed
are indicated
refers to an animal.
supine
dogs at various
at the bottom
of each
368
E. D’ANGELO
AND E. AGOSTONI
1970) whereas there are marked differences in dogs and rabbits (D’Angelo, Michelini and Miserocchi, 1973). The rib cage of man is relatively more stiff than thatcof dogs and rabbits; indeed when moving from the supine to the head-up posture the cross section of the rib cage of man decreases by about 16% of the change over the vital capacity (Agostoni, 1970), whereas that of dogs decreases by about 89”/;;,and that of rabbits even more (D’Angelo et al., 1973). A relatively stiffer rib cage implies likely a smaller range of regional compliance of the chest wall and this could in part explain the different behaviour of man. On the other hand one cannot neglect that the indirect approach used in man involves an error in translating the data from regional lung volume to pleural surface pressure particularly at high lung volume (Agostoni, 1972) and that this method might not be sensitive enough to this end. References Agostoni,
E. (1970).
Kinetics.
by E. J. M. Campbell, Agostoni,
E. and
E. LYAngelo (t970).
E., E. D’Angelo
above
resting
Agostoni,
and
lung expansion.
E. and
gravity
E. D’Angelo
E. (1972).
E., M. V. Bonanni.
pressure
features
and
Neural
Control,
edited
pressure.
Respir.
Lloyd-Luke.
of the transpulmo~ary
E. (1972).
(1971).
gradient
Topography
of the pleural S. Michelini
Topography
of pleural
Local
Physioi. 34: 80998 15. D’Angelo. E., S. Michelini and active expansion.
of transpulmonary
pressure
of pleural
surface
pressure
space. Physiol.
pressure
with active
and
during
simulation
of
Rec. 52: 57-128.
and E. Agostoni
(1970). Topography
alveolar
size and Alveolar
and G. Miserocchi Rrspir.
B. Hughes,
transpulmonary
pressure
of the pleural
morphology (1973).
under
Local
motion
in situ and
localized
surface
pressure
inflation
distorting
in isolated
lung.
forces. J. Appt.
of the chest wall during
passive
Phq’siol. 19: 47-59. J. E.
Maloney
and
J. B. West
(1967).
alveolar size in lungs of dogs frozen intact. J. Appl. Physiol. 23: 694-705. Lemelin, I., W. R. D. Ross, R. R. Martin and N. R. Anthonisen (1972). with positive
surface
29: 2977306.
and dogs. Respir. Physiol. 8: 204-229.
Rrspir. Physiol. 14: 25 l-266. D’Angelo, E. and S. Mi~helini (3973).
J. B., J. M.
(1970).
J. Appl. Ph#ol.
Respir. Ph~isioi. 12: 102109.
Mechanics
in rabbits
animals.
(1970). Vertical
effect on abdomen
D’Angelo,
Glazier,
Mechanics
Davis. London,
J. Appl. Physioi. 29: 705-7 12.
Agostoni.
D’Angelo.
Comparative
M. V. Bonanni
volume in relaxed
E. and G. Miserocchi
artificial Agostoni.
Muscles,
and J. Newsom
I1 : 76-83.
Physid. Agostoni,
In: The Respiratory
E. Agostoni
in erect humans.
Respiv. P~ysiuf.
Vertical
Regional
16: 273-283.
gradient lung
of
volumes
CONTINUOUS
Pt+blishing Company, Amsterdam
RECORDING OF PLEURAL SURFACE PRESSURE AT VARIOUS SITES1
EDGARDO Istituto di Fisiologia
D’ANGELO
and EMIL10
Umana (I cattedra),
AGOSTONI
Uniuersitci di Milano, Milano, Italy
A method has been developed that enables continuous recording of pleural surface pressure in dogs without producing a pneumothorax. The end-expiratory values agree with those obtained with the counterpressure technique. The tidal changes are not systematically different at various sites. As with the counterpressure technique, we found that the vertical gradient of transpulmonary pressure disappears when the respiratory system is passively expanded and that a crania-caudal gradient of transpulmonary pressure is produced in the supine posture when the abdominal pressure is lowered. The kinetics of pleural pressure during spontaneous breathing in some cases differed among sites and among dogs. During inspiratory efforts the kinetics tended to become similar. During artificial ventilation small differences in kinetics occurred. Cardiac oscillations were recorded in the 3rd, 4th and 5th intercostal spaces, seldom in the 6th.
Abstract.
Cardiac oscillations of pleural pressure Kinetics of pleural pressure
Pleural pressure Vertical gradient of transpulmonary
pressure
In a previous research we developed a technique for the measurement of the pressure on the pleural surface at FRC or higher lung volume in the apneic animal without introducing anything into the pleural space (D’Angelo et al., 1970). This technique involved only a small incision of the parietal pleura. It was then modified in such a way as to avoid the incision and thus allow measurements at end inspiration and expiration in the spontaneously breathing animal (Agostoni and Miserocchi, 1970). We then attempted to develop a technique for the continuous recording of pleural surface pressure: a small circular area of the parietal pleura was thinned and a cup was glued to the surrounding endothoracic fascia. The parietal pleura thus acted as the membrane of the cup connected to a pressure transducer. The system was calibrated at the end of the experiment when the cup with the attached membrane was removed. This approach, however, failed probably because of the changing effect of the adhesive (Eastman 910) on the membranes
Accepted
for publication
17 August 1973.
’ This research has been supported by the National Research Council of Italy. 356
PLEURAL
PRESSURE
357
RECORDING
throughout the experiment and because for a given transmural pressure the tension of the membrane in uiuo was different from that in vitro. We therefore decided to use a capsule with an unstretched rubber membrane, which was brought into contact with the surface ofthe lung through a small incision of the endothoracic fascia and parietal pleura without producing a pneumothorax. This paper describes this technique and the results obtained with it. Methods
The device used to measure pleural surface pressure is illustrated in fig. 1. It consisted of an internal part of perspex and an external one of brass. The perspex cylinder had a small concavity on one end: a polyvinyl tube ( 1 mm o.d.) connected it through a 3 way stopcock to a pressure transducer (Sanborn 268 or 267). The system was filled with saline solution and a rubber membrane was tied on the concave end of the perspex cylinder. The rubber membrane was obtained from standard esophageal balloon and its stiffness was negligible relative to that of the transducer membrane. The brass part of the device was made of a short tube and of an external ring. The tube had a flange at one end and its internal diameter was such as to fit tightly on the perspex cylinder. An external ring with a rubber washer was loosely screwed on the external part of the tube. The external ring was screwed by means of a forceps the
Fig.
I Sectional drawing
of the device used to record
pleural
surface
pressure.
See text.
358
E.
D’ANGELO
AND
F. AGOSTONI
teeth of which fitted a couple of four holes pierced into the ring. Before assembling the device the brass part was kept around the polyvinyl tube between the perspex cylinder and the transducer. After having tied the rubber membrane on the perspex cylinder the brass part was pushed until the flange was on the same plane of the rubber membrane. By pushing the brass part in this sense the rubber membrane was not tensed. A perspex box with 4 holes in which the flange of the device could be sealed enabled the simultaneous calibration of 4 capsules. The perspex box contained air and was connected through short. wide bore tubes to a water manometer and to a pressure transducer. The pressure in the box (up to + 16 cm H,O) was changed both by steps or sinusoidally. The frequency response curve of the capsules was flat at least up to 5 cps. The calibration was repeated at the end of the experiment. The experiments were performed on dogs (8827 kg b.w.) anesthetized with sodium pentobarbital (35 mg,‘kg b.w. initial dose). The animals were in the lateral or supine posture. Generally 3 intercostal spaces (i.c.s.) on the right side were cleared of tissues down to the endothoracic fascia over an area of about 2 cm2. The respiratory system was then inflated to about 20 cm H,O and an incision of the endothoracic fascia and parietal pleura was done. The incision was a little shorter than the diameter of the flange of the capsule. The flange of the capsule was then inserted into the pleural space and the external ring screwed until the endothoracic fascia with the parietal pleura was squeezed between the rubber washer and the flange providing an airtight seal. The pressure on the airways was released and the zero level of the transducer was placed at the height of the capsule. The height of the site of measurement relative to the total height in a given posture was also measured. The esophageal pressure was measured through a standard esophageal balloon. A flow-meter was connected to the tracheal cannula. When the airways were closed to make measurements during inspiratory efforts the side tube of the tracheal cannula was connected to a pressure transducer. All signals were recorded on a Sanborn oscillograph. In one experiment the caudal part of the abdomen and the hind limbs of the supine animal were placed in a plethysmograph in which the pressure was lowered in order to simulate the effect of gravity on the shape of the chest wall in the head-up posture (Agostoni and D’Angelo, 1971). In some experiments the supine animal was paralyzed with an injection of succinylcholine, which was preceded by 5-10 mg;kg b.w. of anesthetics. In these animals measurements of pleural surface pressure were made after having inflated the respiratory system up to 20 cm H,O. Comments on the techniques The rubber membrane of the device remained essentially flat because the system was filled with liquid and the compliance of the transducer was low. The introduction of the flange into the pleural space caused a small distortion of the lung at the border of the flange, but the rubber membrane was far enough from
PLEURAL
the border
of the
flange
PRESSURE
(D’Angelo
and
359
RECORDING
Michelini,
1973).
The
weight
of the
capsule was 1.5 g and its center of gravity was 1.7 mm apart from the rubber membrane. Anyway small inclinations of the capsule with respect to its major axis did not modify the pressure measurements. Of more concern was the effect of the in-out movement of the intercostal space. We therefore determined in the apneic animal the change of pressure produced by small movement of the capsule in the direction normal to the surface of the lung. A rigid stick was fastened to the capsule and gently moved: its displacements were read on a scale fixed near the stick while the pressure changes were recorded. The results are shown in fig. 2. Moreover, in the breathing animal we measured the tidal in-out displacements of a point on a rib and of a point on the middle of the corresponding intercostal space or of the corresponding capsule by means of differential transformers (Lynearsin Sanborn 585DT). These were placed about 1 m apart from the rib cage: the thread coming from the core of the transformer was tied to a screw screwed into the rib, or to a hook placed in the intercostal muscles, or to the capsule. The weight of the core connected to the intercostal muscles or to the capsule was counterbalanced so that its pull was reduced to only 1 g. The outward disI
I
2-
I
:A kg
grd
ic.s. .
0 o-
_2_
qdog A 0 0
4 8, 6 II 7 ” 6
\
II
I
o-
\
-2-
in-,
-4
-2
8 I 0
displacement, Fig. 2. Changes
of pleural
surface
number
pressure
against
in each diagram
in-out
‘kl
out
I
‘6
-
2
4
mm artificial
displacement
refers to the intercostal
space.
of the capsule.
The
360
E. D’ANGELO
AND E. AGOSTONI
placement of the rib at end inspiration was greater than that of the intercostal space or of the capsule by less than 0.1 mm. During inspiratory efforts of about 20 cm H,O the inward displacement of the capsule was 0.2 mm greater than that of the corresponding rib. It appears from fig. 2 that the small difference between the tidal displacement of the capsule and of the corresponding rib does not affect the measurement. Only during strong inspiratory efforts the pressure on the intercostal space should have been barely affected by the inward movement of the capsule relative to the rib. But a difference of 0.24.3 cm H,O over a pressure change of about 20 cm H,O is negligible. Results and discussion Examples of tracing obtained by means of the capsule are shown in figs. 3, 4 and 5. The end-expiratory values of pleural surface pressure recorded at various heights are shown in fig. 6: they agree with the data previously obtained with the counterpressure techniques (D’Angelo et ul., 1970; Agostoni, D’Angelo and Bonanni, 1970; Agostoni and Miserocchi, 1970; Agostoni and D’Angelo, 1970) though in the supine posture the relationship tends to be a little more straight. The tidal changes of pleural surface pressure at various sites and of esophageal pressure are shown in table 1. In a given animal differences of about 1 cm H,O among sites occurred often (the maximum difference recorded was 1.9 cm H,O). These differences, however, are not systematic as shown by the following calculation. In each animal the tidal change at a given site was divided by the tidal change at the 5th intercostal space, the values so obtained for the various animals at a given site were averaged and each one multiplied by the average tidal change of the 5th i.c.s. The differences among sites so obtained were not significant. Hence, in line with the data obtained with the counterpressure techniques (Agostoni and Miserocchi. 1970). the tidal changes of pleural surface pressure over the intercostal surface may be considered similar. When an interlobar fissure was under the capsule the pressure measured was more negative by some cm H,O. Indeed in this case pleural liquid pressure instead of pleural surface pressure was measured (Agostoni, 1972). When the interlobar fissure moved under the capsule during inspiration the tidal change of pressure increased markedly because one shifted from end-expiratory surface pressure to end-inspiratory liquid pressure. The changes ofpressure occurring during the inspiratory efforts are illustrated in fig. 7 and summarized in table 1. Again there are no systematic differences of pressure changes among sites. The kinetics of pleural pressure during spontaneous breathing in some cases differed somewhat among sites and among dogs: most of the differences are illustrated by figs. 3, 4 and 5. These may be due to local differences in the resistance to the movement of the passive respiratory system and/or to local differences in the pattern of activity of the respiratory muscles. It can not be ruled out that the latter differences are a consequence of the experimental
PLEURAL PRESSURE RECORDING
a2
s -
0
.W -! -Q2
-1 f 0, I g-3
0
-
:: -b-
i -1 0, ;-3 e z-5 P -! G .
.
.
.._
:
:
.
..,
._,
I -1 9, = -3 : s-5
i
“f
Fig. 3. Tracings of lkm ~~xpii-~~ti~~il ncgawc).
csopha~c~~l prcssurc and pleural surtace pressure in the 3rd. 4th and 5th intercostal spaces. Time: 1 sec.Dog 2. latefal posture.
362
E. D’ANGELO
AND
E. AGOSTONI
-0.47
.> 0.4-
O0 I” E-4v cl!
0 I”
-8-O-
5 -4= L
0 r”
-8-
-2
E -6 ii p -10 I
-20 r I” 5 -6x L -lO-
Fig. 4. Tracings
negative). esophageal pressure and pleural surface of flow (expiration the 6th, 5th and 3rd intercostal spaces. Time: I sec. Dog 8. supine.
PIressure
in
PLEURAL
Fig. 5. Tracings pressure
conditions.
of pleural
surface
and flow (expiration
In most
PRESSURE
pressure
in the 3rd.
negative).
of the cases
Time:
363
RECORDING
5th and
7th intercostal
spaces,
esophageal
I sec.Dog 9: left: lateral: right: supine.
the expiration
was
quick:
the
flow abruptly
reached a peak and decreased then exponentially. This indicates that the expiration was passive. In these cases therefore the local differences in the kinetics of pleural pressure during expiration should be due to local differences in the resistance to the movement of the lung and/or the chest wall. In some cases during the last part of expiration pleural pressure in the 5th and 6th intercostal spaces increased above the resting value indicating a contraction of the abdominal muscles. During inspiratory efforts the kinetics of pleural pressure tended to become similar at various sites in spite of the differences occurring during spontaneous breathing. During artificial respiration small differences in the kinetics of the pleural pressure at various sites occurred in the inspiratory and expiratory phase.
TABLE Changes Animal
Site
of pleural
“~._“_~_. AP
tidal
effort
- 2.2
- 7.0
63
-3.0
-2.5
_
11.0
- 2.2
- 7.6
93
- 5.6
-2.0
-
11.8
- 1.8
-2.0
3rd
57
- 2.7
- 2.7
- 15.2
75
- 2.7
- 2.6
- 16.2
4th
22
- 1.4
- 3.4
- 17.0
70
-3.0
- 3.0
- 19.0
5th
85
- 3.9
- 2.6
- 16.8
66
-2.3
-2.4
- 19.1
- 3.0
- 16.2
- 3.0
- 18.9
3rd
46
- 3.0
-5.3
- 28.0
76
-3.5
-4.7
- 30.4
4th
26
-2.0
-4.9
- 26.0
69
-3.1
5th
82
-4.3
- 5.5
- 25.0 - 24.5
60
-2.5
- 5.0 -4.8
-28.5
-4.7
27.0
69
-3.3 -4.5
-4.4 -4.7
- 19.0
68
- 2.7
-4.0
- 15.8
86
- 17.0
60
- 2.4
-3.8
- 16.2
6th
20
- 1.3
-4.1
- 17.3
86
-4.7
- 3.4
- 17.1
-3.6 -3.7
- 13.4 - 12.7
3rd 5th 6th
- 14.2
- 17.5 - 20.0
74
- 3.0
- 5.0
-23.5
- 20.0
57
- 2.0
-4.5
- 24.0
-4.3
- 19.5
83
-4.0
- 5.5
- 23.5
-4.7
- 19.8
56
- 3.2
-4.5
86
-4.0 - 2.0
- 5.2
20
- 4.8
3rd
47
-3.0
- 5.8
- 14.9
65
-2.5
5th 6th
90 27
- 4.8
- 5.0
- 15.8
73
- 3.0
- 3.9 - 4.8
- 2.4
- 4.0
- 14.5
93
- 5.0
-4.6
15.6 - 15.8
-4.5
- 14.2
- 5.0
- 13.0
28
- 2.3
- 4.0
73
- 3.3
-4.0
- 12.5
5th
87
- 4.3
- 4.0
57
- 2.5
- 3.0
6th esoph.
18
- 1.5
-3.8
93
- 5.3
- 3.3
- 12.0 - 12.6
- 3.0
- 11.8
- 4.0
- Il.8
3rd 5th
65
- 3.0
-3.7
- 17.7
74
-3.2
- 3.0
93
- 4.2
-3.7
- 18.3
63
-2.3
-4.0
6th
35
-2.2
-3.9
- 19.4
90
-4.3
-3.2
-3.8
- 16.6
- 3.1
- 18.0
3rd
69
- 3.2
- 5.4
- 18.7
72
-2.8
- 5.2
- 19.7
5th
89
-4.2
-3.5
- 17.8
70
-3.0
- 20.0
7th esoph.
37
-2.0
-3.9
- 18.0
93
-4.6
- 4.2 - 3.8
- 4.2
- 18.7 - 18.3
alv. Intercostal
-
4th
esoph. alv.
l
- 14.7
- 15.0
- 15.7
alv.
9
- 24.0 - 23.5
- 19.3
alv.
8
- 29.0
3rd 5th
esoph.
7
_~
AP
- 3.9
esoph. alv. 6
Lateral ~_
effort
PP’ end exp.
- 1.6
esoph. alv. 5
and inspiratory
height
84
esoph. 4
breathing
5; lung
24
esoph. 3
spontaneous
effort
AP tidal
esoph. 2
during
AP
PPI end exp.
height
6th
pressure
Supine
y/,lung
iilinHth*
surface
1
space.
-4.4
-20.5 - 19.5 - 20.0
PLEURAL
PRESSURE
-s
4
pkural Fig. 6. Percentage at end inspiration.
symbol
surbce
refers to an animal.
from all the data obtained
-2
-1
surface pressure,cm
of lung height against pleural Each
-3
-1
365
REfORDiNG
0
i-l@
pressure in right intercostal The
line represents
with the counterpressure
region
of dogs
the best fir relationship
technique (Agostoni.
1972).
Cardiac oscillations of pleural pressure were recorded in the 3rd. 4th and 5th i.c.s. and only in one case in the 6th i.c.s.: their values are summarized in table 2. In some instances they were probably masked by higher frequency vibrations of the rib cage produced by intercostal muscles tremor. Since cardiac oscillations appeared in the flow tracing, cardiac oscillations of alveolar pressure should occur. These are probably caused by the movements of the heart and are TABLE
-.
Cardiac _
.-_.
oscillations
3rd i.c.s. -.. Lateral
Supine
* SE.
-.
Mid-axillary -.. __
2
of pleural surface pressure (cm HZO) at various sites -. 4th i.c.s. Dorsal .._.
Sth i.c.s.
6th i.c.s.
Ventral
Dorsal .-.
-
-..
Esophagus
-
-_
0.68 * 0.09*
0.80 + 0.20
1.10+0.16
0.31 +0.10
0.77+0.10
N=6
I%=3
N=8
K=6
N=U
1.cO+o.13
0.33 & 0.24
1.20~0.17
0. IO+ 0.0s
1.00~0.13
N=6
N=3
N=8
N=6
N=8
,-_
366
E. D’ANGELO
AND E. AGOSTONI
-0.4-
o-
f
-> 04-
O0 “-6 I
-
E t-12 I ‘L”-18-
9l =-6-
o-
-
E
u-12 -
t
-18 -
O0, I -65-12 *-I*
-
-3 c-9 I E U-151 z p-21_
O0 I” -6E “.-x2-E p -18-
Fig. 7. Tracings of flow (expiration negative), alveolar pressure, esophageal pressure. pressure in the 6th, 5th and 3rd intercostal spaces during an inspiratory effort against Time: I sec.Dog 8. supine.
pleural surface closed trachea.
PLEURAL
PRESSURE
367
RECORDING
transmitted to the pleural surface of the regions oscillations at one intercostal space were generally another space or with those of the esophagus. When the abdominal pressure of the supine dog decreased more in the cranial than in the caudal
close to the heart. Cardiac out of phase with those of was lowered pleural surface part. That is, by simulating
the effect of gravity on the chest wall shape occurring in the head-up posture. a crania-caudal gradient of transpulmonary pressure like that occurring in the head-up posture was produced in the supine posture. This finding in the breathing animal confirms our previous one obtained with the counterpressure technique in the apneic animal (Agostoni and D’Angelo, 1971). When the respiratory system of the supine dog was passively expanded the vertical gradient of transpulmonary pressure decreased and eventually disappeared (fig. 8). This confirms our previous data obtained with the counterpressure technique (Agostoni et al., 1970; Agostoni and Miserocchi, 1970). On the other hand, Lemelin et al. (1972) studying the distribution of regional lung volume from the dilution of 133Xe in seated man relaxing against positive air pressure found a crania-caudal difference of lung expansion similar to that occurring under normal conditions. They therefore concluded that the vertical pressure gradient of transpulmonary pressure did not decrease with passive inflation of the respiratory system. Since we confirmed our data with a different technique, and these data are in line with morphometric measurements in dogs (Glazier et al., 1967) and rabbits (D’Angelo, 1972). the discrepancy between our results and those of Lemelin et (11. may be due to a species difference. In this connection it must be considered that in the head-up man there are no marked differences of the shape of the rib cage between active and passive expansion above FRC (Agostoni.
._ 2 P 1
01 60
Ai,
0
4 V
i
Cl
s
0
x
1
x
V
0"s
0
a00
15
4
,
I
1
I
1
I
I
1
2
4
6
8
10
12
14
16
18
transpulmonary Fig. 8. Percentage values
of airway
v
0
10
01
V
I
of lung height pressure.
against
These values,
transpulmonary expressed
line. Each symbol
1
20
pressure, cmH@ pressure
in cm H,O,
in relaxed
are indicated
refers to an animal.
supine
dogs at various
at the bottom
of each
368
E. D’ANGELO
AND E. AGOSTONI
1970) whereas there are marked differences in dogs and rabbits (D’Angelo, Michelini and Miserocchi, 1973). The rib cage of man is relatively more stiff than thatcof dogs and rabbits; indeed when moving from the supine to the head-up posture the cross section of the rib cage of man decreases by about 16% of the change over the vital capacity (Agostoni, 1970), whereas that of dogs decreases by about 89”/;;,and that of rabbits even more (D’Angelo et al., 1973). A relatively stiffer rib cage implies likely a smaller range of regional compliance of the chest wall and this could in part explain the different behaviour of man. On the other hand one cannot neglect that the indirect approach used in man involves an error in translating the data from regional lung volume to pleural surface pressure particularly at high lung volume (Agostoni, 1972) and that this method might not be sensitive enough to this end. References Agostoni,
E. (1970).
Kinetics.
by E. J. M. Campbell, Agostoni,
E. and
E. LYAngelo (t970).
E., E. D’Angelo
above
resting
Agostoni,
and
lung expansion.
E. and
gravity
E. D’Angelo
E. (1972).
E., M. V. Bonanni.
pressure
features
and
Neural
Control,
edited
pressure.
Respir.
Lloyd-Luke.
of the transpulmo~ary
E. (1972).
(1971).
gradient
Topography
of the pleural S. Michelini
Topography
of pleural
Local
Physioi. 34: 80998 15. D’Angelo. E., S. Michelini and active expansion.
of transpulmonary
pressure
of pleural
surface
pressure
space. Physiol.
pressure
with active
and
during
simulation
of
Rec. 52: 57-128.
and E. Agostoni
(1970). Topography
alveolar
size and Alveolar
and G. Miserocchi Rrspir.
B. Hughes,
transpulmonary
pressure
of the pleural
morphology (1973).
under
Local
motion
in situ and
localized
surface
pressure
inflation
distorting
in isolated
lung.
forces. J. Appt.
of the chest wall during
passive
Phq’siol. 19: 47-59. J. E.
Maloney
and
J. B. West
(1967).
alveolar size in lungs of dogs frozen intact. J. Appl. Physiol. 23: 694-705. Lemelin, I., W. R. D. Ross, R. R. Martin and N. R. Anthonisen (1972). with positive
surface
29: 2977306.
and dogs. Respir. Physiol. 8: 204-229.
Rrspir. Physiol. 14: 25 l-266. D’Angelo, E. and S. Mi~helini (3973).
J. B., J. M.
(1970).
J. Appl. Ph#ol.
Respir. Ph~isioi. 12: 102109.
Mechanics
in rabbits
animals.
(1970). Vertical
effect on abdomen
D’Angelo,
Glazier,
Mechanics
Davis. London,
J. Appl. Physioi. 29: 705-7 12.
Agostoni.
D’Angelo.
Comparative
M. V. Bonanni
volume in relaxed
E. and G. Miserocchi
artificial Agostoni.
Muscles,
and J. Newsom
I1 : 76-83.
Physid. Agostoni,
In: The Respiratory
E. Agostoni
in erect humans.
Respiv. P~ysiuf.
Vertical
Regional
16: 273-283.
gradient lung
of
volumes