Regional in intact
lung expansion at total lung capacity vs. excised canine lungs
PETER A. CHEVALIER, JOSEPH R. RODARTE, AND LOWELL D. HARRIS Departments of Physiology and Biophysics, and Medicine, Mayo Clinic and Mayo Foundation, Rochester, Minnesota 55901
CHEVALIER, PETER A., JOSEPHR. RODARTE, AND LOWELL Regional lung expansion at total lung capacity in intact vs. excised canine lungs. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 45(3): 363-369, 1978. -A computerbased biplane videoroentgenographic recording technique that determines the spatial coordinates of radiopaque lung parenchymal markers was used to compare regional lung expansion at total lung capacity (TLC) in the intact dog (prone and supine) and after removal from the chest. The reproducibility of the technique was examined by repeated determinations of intermarker distances at various static lung volumes during stepwise inflation and deflation of the lungs. Most of the variability in repeated determinations of intermarker distances at any lung volume was due to cardiogenic motion. When marker positions were determined repeatedly at the same phase of the cardiac cycle, the maximum coefficient of variation was ~3% for a marker pair separated by 16.5 mm* At TLC, distances between all intralobar marker pairs in the intact thorax (prone and supine) and excised were highly linearly related (r = 0.96-0.99), whereas distances between interlobar marker pairs did not correlate as well (r = 0.770.86). We conclude that at TLC 1) the intact thorax does not distort the shape of the individual lobes from the state of isotropic expansion, and 2) in different body positions, overall lung shape may be different due to displacement of lobes relative to each other, but individual lobes remain uniformly expanded. D.
HARRIS.
regional lung mechanics; radiopaque parenchymal markers; lung deformation; biplane videoroentgenographic recordings; pressure-volume curves; videometric analysis
WHENEVER THEREIs NONUNIFORM regional ventilation, there must be nonuniform deformation of the lung. Regional ventilation depends on the mechanical properties of the lung, rib cage, diaphragm, and abdomen and the coupling between these various components of the respiratory system. To understand the mechanical determinants of nonuniform regional ventilation, it is necessary to know the displacements and three-dimensional distortions of specific lung regions. Given a description of the properties of the lung parenchyma that determine its stress-strain relationships, it is possible to estimate the external force distributions required to produce an observed shape and volume distribution, To perform such an analysis, it is essential to relate an observed lung parenchymal shape to a state of uniform or isotropic expansion. At high inflation pressures, the isolated lobes should be too stiff to be de00%8987/78/0000-0000$01.25
Copyright
0 1978 the American
Physiological
formed by their own weight and thus should be uniformly expanded. Studies of canine lungs quick-frozen at high inflation pressures revealed no systematic regional difference in alveolar size (4, 5) suggesting that at total lung capacity (TLC) the lung is uniformly expanded. The purposes of this paper are 1) to compare regional expansion of the canine lung in the intact thorax (prone and supine) at TLC, and at the same inflation pressure after death and excision of the lungs, and 2) to provide additional data regarding the reproducibility of measurements obtained with the operator-interactive parenchymal marker technique (2) and the effect of cardiogenic motion on the variability of intermarker distance measurements. METHODS
Regional lung parenchymal expansion in the intact thorax can be determined by recording the displacements of radiopaque metallic markers by means of a computer-based biplane videoroentgenographic recording system that provides high spatial (-t 1.O mm) resolution measurements of the “tagged” lungs (2). Metallic markers, which consist of l-mm-diameter spheres (avg wt, 0.01 g/marker) and 2-mm-long (l-mmdiam) rods (avg wt, 0.02 g/marker), were implanted percutaneously under fluoroscopic control throughout the parenchyma of the right lung of anesthetized dogs. A three-dimensional gridlike array of up to 30-40 markers (Fig. 1) is obtained without causing physiologically significant pneumo- or hemothorax (2, 8). Postmortem studies have demonstrated that there is no significant pleural reaction following implantation of the markers and pulmonary parenchymal pathologic changes are limited to a region 100-200 pm surrounding each marker (8). A minimal recovery period of 2-3 wk is provided before the dogs are used in an experiment. Then, by means of the biplane videoroentgenographic system, it is possible to track the displacements, in three-dimensional space, of these radiopaque parenchyma1 markers throughout a complete respiratory cycle or maneuver (e.g., a static pressure-volume curve). Data acquisition. A schematic diagram of the biplane videoroentgenographic system and recording equipment is shown in Fig. 2. Each video roentgen imaging chain consists of an X-ray source, a 9-in.-diam fluoroscopic screen, and image intensifier, and a television (PlumSociety
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364
CHEVALIER,
RODARTE,
AND
FIG. 1. Dorsal-ventral and lateral dog’s thorax with metallic markers neously implanted in three-dimensional array throughout parenchyma of right
r-4
Corn,por,~
Vfdeo
,
1
V,deo
VRC
Keyboard
FIG. 2. Diagram of biplane videoroentgenographic system for generation and recording of data for dynamic measurements of regional lung strains and volumes. Axes of 2 X-ray-video recording systems can be selectively aligned for stereo (as shown) or orthogonal recordings. Video roentgen images and analog variables (pressures, flows, ECG) are simultaneously recorded on videotape or disc.
bicon) camera. The central axes of the two video roentgen imaging systems can be selectively aligned from approximately 25-30” (i.e., the angle of separation of the imaging chain central axes) for stereo recording to 90” for orthogonal recording. The central axes of the two imaging systems are aligned to lie in the same transverse plane relative to the cephalocaudal axis of the animal and the animal is positioned so that the lungs and thorax are centered at the intersection of the axes of the video roentgen imaging chains. Each fluoroscopic image, which is projected onto the target of the television camera, is recorded as a sequence of approximately 250 horizontal lines (1 video field; %o s) interlaced with a second field of as many lines to create a frame every l/30 s containing approximately 500 lines/image. Then by means of special switching circuitry (lo), the two video frames are positioned in the left and right halves of the video picture so that biplane videographic images are displayed and recorded simultaneously in the same video frame. The sequence of 30/s biplane images is recorded on videotape (Ampex VR 1100) in absolute temporal synchrony with up to 16 channels of analog information, such as vascular, pleural and airway pressures, velocity and volume of ventilation, and the electrocardiogram (ECG) at sampling rates up to approximately 1,000 samples/s per
HARRIS
X rays of percutagridlike lung.
analog channel by means of a video amplitude modulator-demodulator system (9). At the end of an experiment, pressure, volume and flow calibrations, and the reference (x, y, z) axes used for spatial localization of the markers are recorded on videotape. The reference axes are obtained by placing precision-milled l-cm metal grids on the face of each image intensifier such that the centers of the two grids form a locus with spatial coordinates (0, 0,O) to serve as the center of the Cartesian reference system. Data processing and analysis. Analysis of the biplane video images and multichannel analog recordings is accomplished by transferring the images from videotape to a stop-action video disc recorder (Ampex DR-1OA) for frame-by-frame identification of parenchymal marker positions. A specially designed computer station (Fig. 2; lower right corner), consisting primarily of I) an alphanumeric keyboard to communicate with the computer, 2) an interactive video cursor that is “mixed” with the video image thereby eliminating parallax, 3) a video disc controller (VRC), and 4) a high-performance video monitor (Tektronix 632), is used by an operator to track all parenchymal markers that are identifiable on both images of a single biplane video frame. Once the geometric coordinates of all parenchymal markers have been entered into computer memory, the operator directs the computer via the keyboard to transfer the coordinates and the analog data (pressures, flows, ECG) recorded with that video image from core memory to digital magnetic tape. This regimen is then repeated on a frame-by-frame basis for any selected time interval (i.e., time between frames analyzed), over the duration of the respiratory maneuver. In this way, the dynamic displacements, in three-dimensional space, of the parenchymal markers during various respiratory maneuvers can be determined with sufficient temporal (30/s) and spatial (-+ 1.0 mm) resolution to permit quantitation of regional lung parenchymal displacements and volumes in the intact thorax. Experimental procedure. Six adult mongrel dogs, weighing 8-14 kg, with parenchymal markers implanted previously were used for these studies. The dogs were anesthetized with pentobarbital sodium (30 mg/kg iv) and a cuffed endotracheal tube was inserted into the airway. Intermittent positive-pressure breathing (end-
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REGIONAL
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TLC
inspiratory airway pressure, lo-15 cmH,O) was maintained, except during selected periods when the animals were allowed to breathe spontaneously, with a Bird respirator (Bird Oxygen Breathing Equipment, Palm Springs, Calif.). Esophageal pressure (Pes) was measured with a latex balloon positioned, under fluoroscopic control, in the middle third of the esophagus. Transpulmonary pressure (Ptp) was determined by subtracting airway (Pao), i.e., tracheal, pressure from Pes (3) by means of special electronic circuitry. The EGG was also recorded. An indwelling catheter was inserted into the cephalic vein of the foreleg so that additional anesthetic could be given intravenously without opening the plethysmograph and disrupting the measurements. The dog was then positioned in a radiolucent plethysmograph (Fig. 3), in either the prone or supine position, and all pressure and intravascular catheters, along with the ECG leads, were exteriorized through airtight ports. The plethysmograph was closed, sealed, and then aligned in the biplane video roentgen imaging system (Fig. 3). The animals breathed through a pneumotachograph. Pao, Ptp, lung volume, airflow, and ECG were recorded on video tape and, with the exception of the ECG, on a four-channel oscillographic recorder (model 7414A, Hewlett-Packard Co., Palo Alto, Calif.). The Validyne differential transducers (model DP-9), used to record airway and esophageal pressures, were each interfaced with the oscillographic recorder via carrier amplifiers (model CD-19, Validyne Engineering Corp., Northridge, Calif.). After two inflations to Ptp = 25 cm H,O to ensure a constant volume history, static pressure-volume (PV) curves were obtained for the intact lungs by manually inflating the lungs with a calibrated l,OOO-ml syringe in a stepwise manner (usually 100 ml/v01 step) from func-
tional residual capacity (FRC) to total lung capacity (TLC) (Ptp = 25 cmHzO) and then deflating in the same incremental manner back to FRC. TLC was defined as that volume obtained with a Ptp = 25 cmH,O since the PV curve was essentially flat at this transpulmonary pressure. After obtaining the in vivo PV curves, the animals were killed with an overdose of anesthetic agent and the heart and lungs were excised. No pleural adhesions were observed in any of the animals studied. After ligating the pulmonary arteries and veins and removing the heart, the entire excised lung was positioned in the sling in the open plethysmograph so that when fully inflated its shape approximated the in vivo shape as closely as possible. Biplane videoroentgenograms were recorded with the isolated lungs inflated to 25 cmHzO (Ptp). Anteroposterior and lateral roentgenograms of the entire excised lung were obtained then and after sequential removal of each lobe. These roentgenograms were subsequently used to determine the lobar location of the individual markers and to aid in identifying markers in the intact animals. RESULTS
AND
DISCUSSION
Reproducibility of intermarker distance measurements. It has previously been shown that the spatial loci of markers in a Lucite model can be determined to within * 1.0 mm by this technique (2). To examine the reproducibility of this technique in the living animal, an anesthetized dog was passively inflated in a stepwise manner from FRC to TLC and deflated back to FRC. From the same videotape recording of this PV maneuver, two trained operators, on three separate occasions each, determined the geometric positions of eight parenchymal markers at each of 15 lung volumes. The inter-
FIG. 3. Cylindrical, air-conditioned, radiolucent body plethysmograph positioned in biplane videoroentgenographic recording system. Plethysmograph permits quantitation of lung volumes and can be used with anesthetized spontaneously breathing or ventilated dogs in various positions (prone, supine, right and left lateral decubitus).
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366
CHEVALIER,
marker distances of four pairs of markers, where both markers of a given pair were located in the same lobe, were then computed from the spatial coordinates of the individual markers, The variability (i.e., standard deviations) of these six determinations is plotted against intermarker distance in Fig. 4, The data in the upper panel were obtained by determining marker positions at each lung volume without regard to the cardiac cycle. Note the small standard deviation (SD) of the intermarker distance measurements between markers close together (15-25 mm) in contrast to the relatively larger SD of the measurements of distances between markers further apart (35-60 mm). Because computation of intermarker distances from marker coordinates is mathematically exact and the determination of the coordinates of each marker independent of the other markers, there is no reason inherent in this technique why variability of intermarker distance measurements should be a function of intermarker distance. It was quite evident from viewing videotape recordings of these PV maneuvers that parenchymal markers located near the heart undergo additional (i.e., unrelated to changes in lung volume) oscillation and displacement due to the beating heart and that this effect of cardiogenic motion on marker position diminishes with increasing distance of the marker from the heart. For marker pairs that were near the heart, cardiogenic motion appeared to displace each marker approximately equally and thus the distance between this marker pair was little influenced by the beating heart. Similarly, for marker pairs that were close together but distant from the heart, intermarker distances did not appear to be influenced by cardiogenic motion due to the limited transmission of this motion Mar
A
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l
12,13
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AND
HARRIS
through the lung parenchyma. On the other hand, for markers further apart so that one is near the heart and one relatively distant from the heart, there was a greater effect of cardiac motion on intermarker distance measurements. Figure 4 (lower half) is a similar plot obtained when the positions of the same markers were determined in the same manner as described above, but at identical points in the cardiac cycle. Note the reduction in variability of the intermarker distance measurements. There is no longer any effect of intermarker distances on reproducibility. When cardiogenic motion is taken into account, the largest coeficient of variation observed was ~3% for a marker pair separated by 16.5 mm. Movement of the animal per se does not affect the measurements made with this technique since intermarker distances (i.e., distance between markers in three-dimensional space) are computed, rather than displacements of markers from some fixed coordinate origin. Figure 5 shows the frequency distribution of the maximum differences in intermarker distance measurements observed out of the six determinations for each of the four marker pairs at the 15 volumes examined. The maximum difference in computed intermarker distance was < 0.7 mm in 50% of the observations and was < 1.0 mm in 80% of the observations. Because these measurements can be made as frequently as 30 times/s, this biplane videoroentgenographic technique is capable of providing temporal and spatial resolutions that are manyfold greater than that obtainable with radioactive gas (e.g., xenon-133) techniques for measuring regional lung volumes. If the lung expanded in a uniform or isotropic manner, i.e., for a given change in stress (transpulmonary pressure), the fractional elongation of the lung parenchyma along the x, y, and z axes was equivalent, it
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4. Effect of cardiogenic motion on intermarker distance measurements. Top: SD of intermarker distance measurements as a function of mean intermarker distance. Data based on 6 determinations of intermarker distances of 4 marker pairs at each of 15 lung volumes (12 = 60) without regard to phase of cardiac cycle. Bottom: similar plot obtained when marker positions were determined for each volume at same point in cardiac cycle. FIG.
FIG. 5. Cumulative frequency distribution of maximum differences in intermarker distance measurements obtained by 2 operators (3 trials each) using an operator-interactive, computer-generated video cursor to identify spatial coordinates of 8 markers. Data based on 6 determinations of intermarker distances of 4 marker pairs at each of 15 lung volumes (n = 60) during static pressure-volume maneuver. Measurements at each lung volume made at same point in cardiac cycle.
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REGIONAL
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TLC
would be possible to calculate the spatial distribution of changes in regional lung volumes by considering the distance between any marker pair to be the diameter of a sphere of parenchyma. The cube of this intermarker distance would then be directly proportional to regional lung volume. However, it has been shown that lung expansion is not isotropic and the change in distance between two markers will depend on the spatial orientation of the marker pair within the lung parenchyma (1, 2). Hence, changes in intermarker distances are not direct measurements of dynamic changes in regional lung volume (i.e., ventilation). Regional lung expansion in the intact vs. excised cunine lung at TLC. To analyze the mechanical determinants of nonuniform ventilation it is important to know if at TLC the lung, in the intact thorax, is deformed from its shape under conditions of uniform or isotropic expansion. Figure 6 shows the comparisons obtained in four dogs of intermarker distances of all intralobar marker pairs at TLC for the intact prone animal and in the excised lung. If each lobe were uniformly expanded and at the same volume, intact and excised, there should be a linear relationship with a zero intercept and a slope of 1.0 for all parenchymal dimensions under both conditions, inasmuch as the intermarker distances represent a random sampling of linear dimensions of each lobe. If the lungs were uniformly expanded intact and excised, but had slightly different volumes, the intermarker distances would lie on a line passing through the origin but with a slope different from 1.0. As seen in Fig. 6, the relationship between intermarker distances of intralobar marker pairs in all three lobes of the right lung, intact and excised, is linear (linear correlation coefficient 0.960.99) with a negligible intercept and a slope of approximately 1.0 (range 0.94-1.01).
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FIG. 6. Comparison of distances in right lung of 4 dogs at TLC with and excised (abscissa).
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between intralobar marker pairs lungs in intact thorax (ordinate)
If individual lobes in the intact lung had the same volume as when excised but a deformed shape because of chest wall forces, an increased variability should be seen in the computed intermarker distances between marker pairs in the two conditions. However, the tight clustering of the data around the lines of identity (Fig. 6) suggests that at high inflation pressures changes in the shape of individual lobes between the intact and excised states must be, if any, quite small. Therefore, we conclude that at TLC in the prone dog, the lung is uniformly expanded and that individual lobes are not deformed by the thorax (i.e., chestwall and diaphragm) of the intact animal. We also compared regional lung expansion at TLC in the intact thorax in the prone and supine positions. Three dogs were used for this study, one of which (E123) was used in both studies. Figure 7 shows the relationship of intermarker distances for intralobar and interlobar marker pairs in the lungs of the three intact dogs at TLC in the supine and prone body positions. The data for intralobar marker pairs (i.e., marker pairs in which both markers are in the same lobe) are highly linear with correlation coefficients (r) of 0.96-0.99. The linear regressions had slopes close to 1.O with quite small intercepts. These data suggest that, at TLC, individual lobes are not only at the same volume, but are also expanded in a similar manner when the animal is in the supine and prone positions. Furthermore, by inference from the data presented in Fig. 6, the individual lobes in the intact thorax are uniformly expanded in the supine as well as the prone position. Therefore, we conclude that at TLC in the excised lung and in the prone and supine dog, the lung is uniformly expanded and that in the intact animal individual lobes are not deformed by the chest wall and diaphragm. At high inflation pressures, isolated lobes are too stiff to be deformed by their own weight (6). Our data indicate that regional volumes are uniform in intact lungs at TLC. This is consistent with morphometric studies of dog lungs frozen at high inflation pressures differ(RP = 30 cmH,O) that revealed no systematic ences in regional alveolar size (4) and the study by Hogg and Nepszy (5) that showed that regional lung tissue density was reasonably uniform at TLC except for extreme upper and lower regions of the lungs of headup dogs. Inasmuch as regional volumes are uniform at TLC, one can compute ventilation per alveolus as well as ventilation per unit volume by relating regional volume changes at any other volume (e.g., FRC) to TLC. It is possible to apply a nonuniform stress to a body producing a nonuniform strain without causing a nonuniform distribution of regional volumes (e.g., extending a cylinder axially and compressing it radially). Such a deformation would be difficult to identify by morphometric techniques. Our data that lobe shape is the same intact and excised suggest that by comparing lung shape to the shape at TLC nonuniform strains and thus nonuniform stresses can be identified. In contrast to the close correspondence of intermarker distances for intralobar marker pairs, comparisons of
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368
CHEVALIER, Right Intralobar
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FE. 7, Comparison of distances lobar marker pairs in intact lungs with each dog in supine (ordinate) scissa) body positions.
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between intraof 3 dogs at TLC and prone (ab-
-29.2
100
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100
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Prone INTERMARKER
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distances between interlobar marker pairs (Fig. 7), i.e., marker pairs that span fissures, do not show the same high degree of linear correlation (r = 0.77-0.86) that was observed with the intralobar marker pairs. In two animals (E-256 and E-281), the variability in the data is strikingly increased so that the linear regressions, although yielding positive correlations (r = 0.81 and 0.77, respectively), were quite different from the line of identity. In the third dog (E-123), even though the scatter in the data was somewhat increased, the differences are less pronounced. This comparison suggests that there are definite differences in the relationships of the lobes to each other in the two body positions. Lateral roentgenograms of the dog’s thorax at TLC in the supine and prone positions reveal that a change in curvature of the diaphragm and a shift in thoracic contents accompany the alteration in body posture (Fig. 8). Rutishauser and co-workers (7) have reported that the mean vertical lung diameter was 4 mm larger in supine than in prone dogs and that in supine dogs the ventral heart border was separated from the dorsal surface of the sternum by an average of 4 mm as compared to only 1 mm in prone dogs. In addition, the heart was more spherical in supine dogs and had a dorsal-ventral diameter 6 mm larger than in prone dogs in which the heart was more ovoid and partially supported by the sternum and the ventral rib cage. Although the lung volumes at which these measurements were made were not reported (7), these data demonstrate that a shift in mediastinal contents and a change in their position relative to the lung and thorax accompany the alteration in body position. Our data suggest that at high inflation pressures, when the lung parenchyma is relatively rigid and resists deformation, this change in thoracic cavity shape and shift in thoracic contents result in a reorganization of individual lung lobes within the thorax. Furthermore, the data indicate that this reorganization occurs with no detectable change in shape of the individual lung lobes. The direction and magnitude of movement of the lobes relative to each other have not been delineated. These data suggest that if a major determinant of nonuniform regional ventilation is the nonuniform parenchymal expansion necessary for the lung and thoracic cavity shapes to coincide, then the additional degrees of freedom of overall lung shape provided by interlobar fissures may be an important mechanism in
FIG. 8. Comparison of position of heart and curvature of diaphragm at TLC, obtained from lateral roentgenograms, in a dog in prone vs. supine body positions.
reducing the nonuniformity of ventilation, potentially injurious local stress concentrations, and the total energy required to expand the lung. Data to assess the magnitude of these effects are not available at present. In summary, the data presented here indicate that regional lung expansion at TLC appears to be identical in the intact thorax of dogs in the supine and prone body positions and in the individual lobes of the excised lung. If we assume that excised lungs are uniformly expanded at TLC because, at high inflation pressures and in the presence of a uniform pleural pressure, they are too stiff to be deformed by their own weight, then we can conclude that at TLC regional lung expansion is uniform or isotropic in the dog with an intact thorax. Therefore, in analyses of nonuniform regional ventilation, changes in regional lung parenchymal shape and volume from those pertaining at TLC represent changes from the state of uniform or isotropic expansion. This does not mean that overall lung shape intact and excised was the same or even that thoracic cavity shape at TLC in the supine vs. prone animal was necessarily the same. But the data do show that at TLC, while overall lung shape may be different in the different body positions, individual lobes remain uniformly expanded. Slippage of lobes along interlobar fissures could possibly aid the lung in conforming to different thoracic shapes and shift in thoracic contents without compromising regional expansion of the individual lung lobes. We thank Miss Pat Snider and Mrs. Donna Balow and their coworkers for secretarial assistance and illustrations, Messrs. Julijs Zarins, Don Erdman, Donald Hegland, Ron Roessler, Bill Sutterer,
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Merrill Wondrow, Eric Hoffman, Bruce Walters, and Dan Olson for their contributions to the engineering and experimentation aspects of this project, Mr. Al Wanek for computer programming assistance, and Dr. Robert E. Hyatt for critically reviewing the manuscript. This investigation was supported in part by Research Grants HL04664, HL-21584, HE-19025, and RR-00007 from the National Institutes of Health; F 49620-76-C-0001 from the US Air Force; and NGR24-003-001 from the National Aeronautics and Space Administration.
J. R. Rodarte is supported by a Public Health Service Academic Award (HL-70816). 1;. D. Harris is a Postdoctoral Fellow of the National Heart, Lung, and Blood Institute. Address for reprint requests: P. A. Chevalier, Mayo First St. SW, Rochester, Minn. 55901.
Pulmonary Research
Received
1978.
9 January
1978; accepted
in final
form
21 April
Clinic,
200
REFERENCES 1. CHEVALIER, P. A., L. D. HARRIS, J. F. GREENLEAF, AND R. A. ROBB. Dynamic regional lung strains in awake dogs (Abstract). Physiologist 18: 168, 1975. 2. CHEVALIER, P. A., J. F. GREENLEAF, R. A. ROBB, AND E. H. WOOD. Biplane videoroentgenographic analysis of dynamic regional lung strains in dogs. J. Apple. Physiol. 40: 118-122, 1976. 3. GILLESPIE, D. J,, Y. L. LAI, AND R. E. HYATT. Comparison of esophageal and pleural pressures in the anesthetized dog. J. Apple. Physiol. 35: 709-713, 1973. 4. GLAZIER, J. B., J. M. B, HUGHES, J. E. MALONEY, AND J. B. WEST* Vertical gradient of alveolar size in lungs frozen intact. J. AppZ. Physiol. 23: 694-705, 1967. 5. HOGG, J. C., AND S. NEPSZY. Regional lung volume and pleural pressure gradient estimated from lung density in dogs. J. Appl. Physiol. 27: 198-203, 1969, 6. KALLOK, Ma Gravitational Deformation and Ventilation Distri-
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bution in Excised Lobes of Dog Lungs. (PhD thesis). Minneapolis, Minn.: University of Minnesota, 1978. RUTISHAUSER, W. J., N. BANCHERO, A. G. TSAKIRIS, A. C. EDMUNDOWICZ, AND E, H. WOOD. Pleural pressures at dorsal and ventral sites in supine and prone body positions. J. Appl. Physiol. 21: 1500-1510, 1966. SMITH, H. C,, J, F. GREENLEAF, E. H. WOOD, D. J. SASS, AND A. A. BOVE. Measurement of regional pulmonary parenchymal movement in dogs. J. Appl. Physiol. 34: 544-547, 1973. STURM, R. E., E. L. RITMAN, R. J. HANSEN, AND E. H. WOOD. Recording of multichannel analog data and video images on the same videotape or disc. J. Appl. PhysioZ. 36: 761-764, 1974. WILLIAMS, J. C. P., R. E. STURM, A. G. TSAKIRIS, AND E. H. WOOD. Biplane videoangiography. J. Appl. PhysioL. 24: 724-727, 1968.
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lung expansion at total lung capacity vs. excised canine lungs
PETER A. CHEVALIER, JOSEPH R. RODARTE, AND LOWELL D. HARRIS Departments of Physiology and Biophysics, and Medicine, Mayo Clinic and Mayo Foundation, Rochester, Minnesota 55901
CHEVALIER, PETER A., JOSEPHR. RODARTE, AND LOWELL Regional lung expansion at total lung capacity in intact vs. excised canine lungs. J. Appl. Physiol.: Respirat. Environ. Exercise Physiol. 45(3): 363-369, 1978. -A computerbased biplane videoroentgenographic recording technique that determines the spatial coordinates of radiopaque lung parenchymal markers was used to compare regional lung expansion at total lung capacity (TLC) in the intact dog (prone and supine) and after removal from the chest. The reproducibility of the technique was examined by repeated determinations of intermarker distances at various static lung volumes during stepwise inflation and deflation of the lungs. Most of the variability in repeated determinations of intermarker distances at any lung volume was due to cardiogenic motion. When marker positions were determined repeatedly at the same phase of the cardiac cycle, the maximum coefficient of variation was ~3% for a marker pair separated by 16.5 mm* At TLC, distances between all intralobar marker pairs in the intact thorax (prone and supine) and excised were highly linearly related (r = 0.96-0.99), whereas distances between interlobar marker pairs did not correlate as well (r = 0.770.86). We conclude that at TLC 1) the intact thorax does not distort the shape of the individual lobes from the state of isotropic expansion, and 2) in different body positions, overall lung shape may be different due to displacement of lobes relative to each other, but individual lobes remain uniformly expanded. D.
HARRIS.
regional lung mechanics; radiopaque parenchymal markers; lung deformation; biplane videoroentgenographic recordings; pressure-volume curves; videometric analysis
WHENEVER THEREIs NONUNIFORM regional ventilation, there must be nonuniform deformation of the lung. Regional ventilation depends on the mechanical properties of the lung, rib cage, diaphragm, and abdomen and the coupling between these various components of the respiratory system. To understand the mechanical determinants of nonuniform regional ventilation, it is necessary to know the displacements and three-dimensional distortions of specific lung regions. Given a description of the properties of the lung parenchyma that determine its stress-strain relationships, it is possible to estimate the external force distributions required to produce an observed shape and volume distribution, To perform such an analysis, it is essential to relate an observed lung parenchymal shape to a state of uniform or isotropic expansion. At high inflation pressures, the isolated lobes should be too stiff to be de00%8987/78/0000-0000$01.25
Copyright
0 1978 the American
Physiological
formed by their own weight and thus should be uniformly expanded. Studies of canine lungs quick-frozen at high inflation pressures revealed no systematic regional difference in alveolar size (4, 5) suggesting that at total lung capacity (TLC) the lung is uniformly expanded. The purposes of this paper are 1) to compare regional expansion of the canine lung in the intact thorax (prone and supine) at TLC, and at the same inflation pressure after death and excision of the lungs, and 2) to provide additional data regarding the reproducibility of measurements obtained with the operator-interactive parenchymal marker technique (2) and the effect of cardiogenic motion on the variability of intermarker distance measurements. METHODS
Regional lung parenchymal expansion in the intact thorax can be determined by recording the displacements of radiopaque metallic markers by means of a computer-based biplane videoroentgenographic recording system that provides high spatial (-t 1.O mm) resolution measurements of the “tagged” lungs (2). Metallic markers, which consist of l-mm-diameter spheres (avg wt, 0.01 g/marker) and 2-mm-long (l-mmdiam) rods (avg wt, 0.02 g/marker), were implanted percutaneously under fluoroscopic control throughout the parenchyma of the right lung of anesthetized dogs. A three-dimensional gridlike array of up to 30-40 markers (Fig. 1) is obtained without causing physiologically significant pneumo- or hemothorax (2, 8). Postmortem studies have demonstrated that there is no significant pleural reaction following implantation of the markers and pulmonary parenchymal pathologic changes are limited to a region 100-200 pm surrounding each marker (8). A minimal recovery period of 2-3 wk is provided before the dogs are used in an experiment. Then, by means of the biplane videoroentgenographic system, it is possible to track the displacements, in three-dimensional space, of these radiopaque parenchyma1 markers throughout a complete respiratory cycle or maneuver (e.g., a static pressure-volume curve). Data acquisition. A schematic diagram of the biplane videoroentgenographic system and recording equipment is shown in Fig. 2. Each video roentgen imaging chain consists of an X-ray source, a 9-in.-diam fluoroscopic screen, and image intensifier, and a television (PlumSociety
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364
CHEVALIER,
RODARTE,
AND
FIG. 1. Dorsal-ventral and lateral dog’s thorax with metallic markers neously implanted in three-dimensional array throughout parenchyma of right
r-4
Corn,por,~
Vfdeo
,
1
V,deo
VRC
Keyboard
FIG. 2. Diagram of biplane videoroentgenographic system for generation and recording of data for dynamic measurements of regional lung strains and volumes. Axes of 2 X-ray-video recording systems can be selectively aligned for stereo (as shown) or orthogonal recordings. Video roentgen images and analog variables (pressures, flows, ECG) are simultaneously recorded on videotape or disc.
bicon) camera. The central axes of the two video roentgen imaging systems can be selectively aligned from approximately 25-30” (i.e., the angle of separation of the imaging chain central axes) for stereo recording to 90” for orthogonal recording. The central axes of the two imaging systems are aligned to lie in the same transverse plane relative to the cephalocaudal axis of the animal and the animal is positioned so that the lungs and thorax are centered at the intersection of the axes of the video roentgen imaging chains. Each fluoroscopic image, which is projected onto the target of the television camera, is recorded as a sequence of approximately 250 horizontal lines (1 video field; %o s) interlaced with a second field of as many lines to create a frame every l/30 s containing approximately 500 lines/image. Then by means of special switching circuitry (lo), the two video frames are positioned in the left and right halves of the video picture so that biplane videographic images are displayed and recorded simultaneously in the same video frame. The sequence of 30/s biplane images is recorded on videotape (Ampex VR 1100) in absolute temporal synchrony with up to 16 channels of analog information, such as vascular, pleural and airway pressures, velocity and volume of ventilation, and the electrocardiogram (ECG) at sampling rates up to approximately 1,000 samples/s per
HARRIS
X rays of percutagridlike lung.
analog channel by means of a video amplitude modulator-demodulator system (9). At the end of an experiment, pressure, volume and flow calibrations, and the reference (x, y, z) axes used for spatial localization of the markers are recorded on videotape. The reference axes are obtained by placing precision-milled l-cm metal grids on the face of each image intensifier such that the centers of the two grids form a locus with spatial coordinates (0, 0,O) to serve as the center of the Cartesian reference system. Data processing and analysis. Analysis of the biplane video images and multichannel analog recordings is accomplished by transferring the images from videotape to a stop-action video disc recorder (Ampex DR-1OA) for frame-by-frame identification of parenchymal marker positions. A specially designed computer station (Fig. 2; lower right corner), consisting primarily of I) an alphanumeric keyboard to communicate with the computer, 2) an interactive video cursor that is “mixed” with the video image thereby eliminating parallax, 3) a video disc controller (VRC), and 4) a high-performance video monitor (Tektronix 632), is used by an operator to track all parenchymal markers that are identifiable on both images of a single biplane video frame. Once the geometric coordinates of all parenchymal markers have been entered into computer memory, the operator directs the computer via the keyboard to transfer the coordinates and the analog data (pressures, flows, ECG) recorded with that video image from core memory to digital magnetic tape. This regimen is then repeated on a frame-by-frame basis for any selected time interval (i.e., time between frames analyzed), over the duration of the respiratory maneuver. In this way, the dynamic displacements, in three-dimensional space, of the parenchymal markers during various respiratory maneuvers can be determined with sufficient temporal (30/s) and spatial (-+ 1.0 mm) resolution to permit quantitation of regional lung parenchymal displacements and volumes in the intact thorax. Experimental procedure. Six adult mongrel dogs, weighing 8-14 kg, with parenchymal markers implanted previously were used for these studies. The dogs were anesthetized with pentobarbital sodium (30 mg/kg iv) and a cuffed endotracheal tube was inserted into the airway. Intermittent positive-pressure breathing (end-
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REGIONAL
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inspiratory airway pressure, lo-15 cmH,O) was maintained, except during selected periods when the animals were allowed to breathe spontaneously, with a Bird respirator (Bird Oxygen Breathing Equipment, Palm Springs, Calif.). Esophageal pressure (Pes) was measured with a latex balloon positioned, under fluoroscopic control, in the middle third of the esophagus. Transpulmonary pressure (Ptp) was determined by subtracting airway (Pao), i.e., tracheal, pressure from Pes (3) by means of special electronic circuitry. The EGG was also recorded. An indwelling catheter was inserted into the cephalic vein of the foreleg so that additional anesthetic could be given intravenously without opening the plethysmograph and disrupting the measurements. The dog was then positioned in a radiolucent plethysmograph (Fig. 3), in either the prone or supine position, and all pressure and intravascular catheters, along with the ECG leads, were exteriorized through airtight ports. The plethysmograph was closed, sealed, and then aligned in the biplane video roentgen imaging system (Fig. 3). The animals breathed through a pneumotachograph. Pao, Ptp, lung volume, airflow, and ECG were recorded on video tape and, with the exception of the ECG, on a four-channel oscillographic recorder (model 7414A, Hewlett-Packard Co., Palo Alto, Calif.). The Validyne differential transducers (model DP-9), used to record airway and esophageal pressures, were each interfaced with the oscillographic recorder via carrier amplifiers (model CD-19, Validyne Engineering Corp., Northridge, Calif.). After two inflations to Ptp = 25 cm H,O to ensure a constant volume history, static pressure-volume (PV) curves were obtained for the intact lungs by manually inflating the lungs with a calibrated l,OOO-ml syringe in a stepwise manner (usually 100 ml/v01 step) from func-
tional residual capacity (FRC) to total lung capacity (TLC) (Ptp = 25 cmHzO) and then deflating in the same incremental manner back to FRC. TLC was defined as that volume obtained with a Ptp = 25 cmH,O since the PV curve was essentially flat at this transpulmonary pressure. After obtaining the in vivo PV curves, the animals were killed with an overdose of anesthetic agent and the heart and lungs were excised. No pleural adhesions were observed in any of the animals studied. After ligating the pulmonary arteries and veins and removing the heart, the entire excised lung was positioned in the sling in the open plethysmograph so that when fully inflated its shape approximated the in vivo shape as closely as possible. Biplane videoroentgenograms were recorded with the isolated lungs inflated to 25 cmHzO (Ptp). Anteroposterior and lateral roentgenograms of the entire excised lung were obtained then and after sequential removal of each lobe. These roentgenograms were subsequently used to determine the lobar location of the individual markers and to aid in identifying markers in the intact animals. RESULTS
AND
DISCUSSION
Reproducibility of intermarker distance measurements. It has previously been shown that the spatial loci of markers in a Lucite model can be determined to within * 1.0 mm by this technique (2). To examine the reproducibility of this technique in the living animal, an anesthetized dog was passively inflated in a stepwise manner from FRC to TLC and deflated back to FRC. From the same videotape recording of this PV maneuver, two trained operators, on three separate occasions each, determined the geometric positions of eight parenchymal markers at each of 15 lung volumes. The inter-
FIG. 3. Cylindrical, air-conditioned, radiolucent body plethysmograph positioned in biplane videoroentgenographic recording system. Plethysmograph permits quantitation of lung volumes and can be used with anesthetized spontaneously breathing or ventilated dogs in various positions (prone, supine, right and left lateral decubitus).
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366
CHEVALIER,
marker distances of four pairs of markers, where both markers of a given pair were located in the same lobe, were then computed from the spatial coordinates of the individual markers, The variability (i.e., standard deviations) of these six determinations is plotted against intermarker distance in Fig. 4, The data in the upper panel were obtained by determining marker positions at each lung volume without regard to the cardiac cycle. Note the small standard deviation (SD) of the intermarker distance measurements between markers close together (15-25 mm) in contrast to the relatively larger SD of the measurements of distances between markers further apart (35-60 mm). Because computation of intermarker distances from marker coordinates is mathematically exact and the determination of the coordinates of each marker independent of the other markers, there is no reason inherent in this technique why variability of intermarker distance measurements should be a function of intermarker distance. It was quite evident from viewing videotape recordings of these PV maneuvers that parenchymal markers located near the heart undergo additional (i.e., unrelated to changes in lung volume) oscillation and displacement due to the beating heart and that this effect of cardiogenic motion on marker position diminishes with increasing distance of the marker from the heart. For marker pairs that were near the heart, cardiogenic motion appeared to displace each marker approximately equally and thus the distance between this marker pair was little influenced by the beating heart. Similarly, for marker pairs that were close together but distant from the heart, intermarker distances did not appear to be influenced by cardiogenic motion due to the limited transmission of this motion Mar
A
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l
12,13
0
AND
HARRIS
through the lung parenchyma. On the other hand, for markers further apart so that one is near the heart and one relatively distant from the heart, there was a greater effect of cardiac motion on intermarker distance measurements. Figure 4 (lower half) is a similar plot obtained when the positions of the same markers were determined in the same manner as described above, but at identical points in the cardiac cycle. Note the reduction in variability of the intermarker distance measurements. There is no longer any effect of intermarker distances on reproducibility. When cardiogenic motion is taken into account, the largest coeficient of variation observed was ~3% for a marker pair separated by 16.5 mm. Movement of the animal per se does not affect the measurements made with this technique since intermarker distances (i.e., distance between markers in three-dimensional space) are computed, rather than displacements of markers from some fixed coordinate origin. Figure 5 shows the frequency distribution of the maximum differences in intermarker distance measurements observed out of the six determinations for each of the four marker pairs at the 15 volumes examined. The maximum difference in computed intermarker distance was < 0.7 mm in 50% of the observations and was < 1.0 mm in 80% of the observations. Because these measurements can be made as frequently as 30 times/s, this biplane videoroentgenographic technique is capable of providing temporal and spatial resolutions that are manyfold greater than that obtainable with radioactive gas (e.g., xenon-133) techniques for measuring regional lung volumes. If the lung expanded in a uniform or isotropic manner, i.e., for a given change in stress (transpulmonary pressure), the fractional elongation of the lung parenchyma along the x, y, and z axes was equivalent, it
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4. Effect of cardiogenic motion on intermarker distance measurements. Top: SD of intermarker distance measurements as a function of mean intermarker distance. Data based on 6 determinations of intermarker distances of 4 marker pairs at each of 15 lung volumes (12 = 60) without regard to phase of cardiac cycle. Bottom: similar plot obtained when marker positions were determined for each volume at same point in cardiac cycle. FIG.
FIG. 5. Cumulative frequency distribution of maximum differences in intermarker distance measurements obtained by 2 operators (3 trials each) using an operator-interactive, computer-generated video cursor to identify spatial coordinates of 8 markers. Data based on 6 determinations of intermarker distances of 4 marker pairs at each of 15 lung volumes (n = 60) during static pressure-volume maneuver. Measurements at each lung volume made at same point in cardiac cycle.
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would be possible to calculate the spatial distribution of changes in regional lung volumes by considering the distance between any marker pair to be the diameter of a sphere of parenchyma. The cube of this intermarker distance would then be directly proportional to regional lung volume. However, it has been shown that lung expansion is not isotropic and the change in distance between two markers will depend on the spatial orientation of the marker pair within the lung parenchyma (1, 2). Hence, changes in intermarker distances are not direct measurements of dynamic changes in regional lung volume (i.e., ventilation). Regional lung expansion in the intact vs. excised cunine lung at TLC. To analyze the mechanical determinants of nonuniform ventilation it is important to know if at TLC the lung, in the intact thorax, is deformed from its shape under conditions of uniform or isotropic expansion. Figure 6 shows the comparisons obtained in four dogs of intermarker distances of all intralobar marker pairs at TLC for the intact prone animal and in the excised lung. If each lobe were uniformly expanded and at the same volume, intact and excised, there should be a linear relationship with a zero intercept and a slope of 1.0 for all parenchymal dimensions under both conditions, inasmuch as the intermarker distances represent a random sampling of linear dimensions of each lobe. If the lungs were uniformly expanded intact and excised, but had slightly different volumes, the intermarker distances would lie on a line passing through the origin but with a slope different from 1.0. As seen in Fig. 6, the relationship between intermarker distances of intralobar marker pairs in all three lobes of the right lung, intact and excised, is linear (linear correlation coefficient 0.960.99) with a negligible intercept and a slope of approximately 1.0 (range 0.94-1.01).
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FIG. 6. Comparison of distances in right lung of 4 dogs at TLC with and excised (abscissa).
0 at
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between intralobar marker pairs lungs in intact thorax (ordinate)
If individual lobes in the intact lung had the same volume as when excised but a deformed shape because of chest wall forces, an increased variability should be seen in the computed intermarker distances between marker pairs in the two conditions. However, the tight clustering of the data around the lines of identity (Fig. 6) suggests that at high inflation pressures changes in the shape of individual lobes between the intact and excised states must be, if any, quite small. Therefore, we conclude that at TLC in the prone dog, the lung is uniformly expanded and that individual lobes are not deformed by the thorax (i.e., chestwall and diaphragm) of the intact animal. We also compared regional lung expansion at TLC in the intact thorax in the prone and supine positions. Three dogs were used for this study, one of which (E123) was used in both studies. Figure 7 shows the relationship of intermarker distances for intralobar and interlobar marker pairs in the lungs of the three intact dogs at TLC in the supine and prone body positions. The data for intralobar marker pairs (i.e., marker pairs in which both markers are in the same lobe) are highly linear with correlation coefficients (r) of 0.96-0.99. The linear regressions had slopes close to 1.O with quite small intercepts. These data suggest that, at TLC, individual lobes are not only at the same volume, but are also expanded in a similar manner when the animal is in the supine and prone positions. Furthermore, by inference from the data presented in Fig. 6, the individual lobes in the intact thorax are uniformly expanded in the supine as well as the prone position. Therefore, we conclude that at TLC in the excised lung and in the prone and supine dog, the lung is uniformly expanded and that in the intact animal individual lobes are not deformed by the chest wall and diaphragm. At high inflation pressures, isolated lobes are too stiff to be deformed by their own weight (6). Our data indicate that regional volumes are uniform in intact lungs at TLC. This is consistent with morphometric studies of dog lungs frozen at high inflation pressures differ(RP = 30 cmH,O) that revealed no systematic ences in regional alveolar size (4) and the study by Hogg and Nepszy (5) that showed that regional lung tissue density was reasonably uniform at TLC except for extreme upper and lower regions of the lungs of headup dogs. Inasmuch as regional volumes are uniform at TLC, one can compute ventilation per alveolus as well as ventilation per unit volume by relating regional volume changes at any other volume (e.g., FRC) to TLC. It is possible to apply a nonuniform stress to a body producing a nonuniform strain without causing a nonuniform distribution of regional volumes (e.g., extending a cylinder axially and compressing it radially). Such a deformation would be difficult to identify by morphometric techniques. Our data that lobe shape is the same intact and excised suggest that by comparing lung shape to the shape at TLC nonuniform strains and thus nonuniform stresses can be identified. In contrast to the close correspondence of intermarker distances for intralobar marker pairs, comparisons of
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368
CHEVALIER, Right Intralobar
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(E-281)
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FE. 7, Comparison of distances lobar marker pairs in intact lungs with each dog in supine (ordinate) scissa) body positions.
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0.96 I
between intraof 3 dogs at TLC and prone (ab-
-29.2
100
-0
50
100
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Prone INTERMARKER
DISTANCE,
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distances between interlobar marker pairs (Fig. 7), i.e., marker pairs that span fissures, do not show the same high degree of linear correlation (r = 0.77-0.86) that was observed with the intralobar marker pairs. In two animals (E-256 and E-281), the variability in the data is strikingly increased so that the linear regressions, although yielding positive correlations (r = 0.81 and 0.77, respectively), were quite different from the line of identity. In the third dog (E-123), even though the scatter in the data was somewhat increased, the differences are less pronounced. This comparison suggests that there are definite differences in the relationships of the lobes to each other in the two body positions. Lateral roentgenograms of the dog’s thorax at TLC in the supine and prone positions reveal that a change in curvature of the diaphragm and a shift in thoracic contents accompany the alteration in body posture (Fig. 8). Rutishauser and co-workers (7) have reported that the mean vertical lung diameter was 4 mm larger in supine than in prone dogs and that in supine dogs the ventral heart border was separated from the dorsal surface of the sternum by an average of 4 mm as compared to only 1 mm in prone dogs. In addition, the heart was more spherical in supine dogs and had a dorsal-ventral diameter 6 mm larger than in prone dogs in which the heart was more ovoid and partially supported by the sternum and the ventral rib cage. Although the lung volumes at which these measurements were made were not reported (7), these data demonstrate that a shift in mediastinal contents and a change in their position relative to the lung and thorax accompany the alteration in body position. Our data suggest that at high inflation pressures, when the lung parenchyma is relatively rigid and resists deformation, this change in thoracic cavity shape and shift in thoracic contents result in a reorganization of individual lung lobes within the thorax. Furthermore, the data indicate that this reorganization occurs with no detectable change in shape of the individual lung lobes. The direction and magnitude of movement of the lobes relative to each other have not been delineated. These data suggest that if a major determinant of nonuniform regional ventilation is the nonuniform parenchymal expansion necessary for the lung and thoracic cavity shapes to coincide, then the additional degrees of freedom of overall lung shape provided by interlobar fissures may be an important mechanism in
FIG. 8. Comparison of position of heart and curvature of diaphragm at TLC, obtained from lateral roentgenograms, in a dog in prone vs. supine body positions.
reducing the nonuniformity of ventilation, potentially injurious local stress concentrations, and the total energy required to expand the lung. Data to assess the magnitude of these effects are not available at present. In summary, the data presented here indicate that regional lung expansion at TLC appears to be identical in the intact thorax of dogs in the supine and prone body positions and in the individual lobes of the excised lung. If we assume that excised lungs are uniformly expanded at TLC because, at high inflation pressures and in the presence of a uniform pleural pressure, they are too stiff to be deformed by their own weight, then we can conclude that at TLC regional lung expansion is uniform or isotropic in the dog with an intact thorax. Therefore, in analyses of nonuniform regional ventilation, changes in regional lung parenchymal shape and volume from those pertaining at TLC represent changes from the state of uniform or isotropic expansion. This does not mean that overall lung shape intact and excised was the same or even that thoracic cavity shape at TLC in the supine vs. prone animal was necessarily the same. But the data do show that at TLC, while overall lung shape may be different in the different body positions, individual lobes remain uniformly expanded. Slippage of lobes along interlobar fissures could possibly aid the lung in conforming to different thoracic shapes and shift in thoracic contents without compromising regional expansion of the individual lung lobes. We thank Miss Pat Snider and Mrs. Donna Balow and their coworkers for secretarial assistance and illustrations, Messrs. Julijs Zarins, Don Erdman, Donald Hegland, Ron Roessler, Bill Sutterer,
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Merrill Wondrow, Eric Hoffman, Bruce Walters, and Dan Olson for their contributions to the engineering and experimentation aspects of this project, Mr. Al Wanek for computer programming assistance, and Dr. Robert E. Hyatt for critically reviewing the manuscript. This investigation was supported in part by Research Grants HL04664, HL-21584, HE-19025, and RR-00007 from the National Institutes of Health; F 49620-76-C-0001 from the US Air Force; and NGR24-003-001 from the National Aeronautics and Space Administration.
J. R. Rodarte is supported by a Public Health Service Academic Award (HL-70816). 1;. D. Harris is a Postdoctoral Fellow of the National Heart, Lung, and Blood Institute. Address for reprint requests: P. A. Chevalier, Mayo First St. SW, Rochester, Minn. 55901.
Pulmonary Research
Received
1978.
9 January
1978; accepted
in final
form
21 April
Clinic,
200
REFERENCES 1. CHEVALIER, P. A., L. D. HARRIS, J. F. GREENLEAF, AND R. A. ROBB. Dynamic regional lung strains in awake dogs (Abstract). Physiologist 18: 168, 1975. 2. CHEVALIER, P. A., J. F. GREENLEAF, R. A. ROBB, AND E. H. WOOD. Biplane videoroentgenographic analysis of dynamic regional lung strains in dogs. J. Apple. Physiol. 40: 118-122, 1976. 3. GILLESPIE, D. J,, Y. L. LAI, AND R. E. HYATT. Comparison of esophageal and pleural pressures in the anesthetized dog. J. Apple. Physiol. 35: 709-713, 1973. 4. GLAZIER, J. B., J. M. B, HUGHES, J. E. MALONEY, AND J. B. WEST* Vertical gradient of alveolar size in lungs frozen intact. J. AppZ. Physiol. 23: 694-705, 1967. 5. HOGG, J. C., AND S. NEPSZY. Regional lung volume and pleural pressure gradient estimated from lung density in dogs. J. Appl. Physiol. 27: 198-203, 1969, 6. KALLOK, Ma Gravitational Deformation and Ventilation Distri-
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8.
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bution in Excised Lobes of Dog Lungs. (PhD thesis). Minneapolis, Minn.: University of Minnesota, 1978. RUTISHAUSER, W. J., N. BANCHERO, A. G. TSAKIRIS, A. C. EDMUNDOWICZ, AND E, H. WOOD. Pleural pressures at dorsal and ventral sites in supine and prone body positions. J. Appl. Physiol. 21: 1500-1510, 1966. SMITH, H. C,, J, F. GREENLEAF, E. H. WOOD, D. J. SASS, AND A. A. BOVE. Measurement of regional pulmonary parenchymal movement in dogs. J. Appl. Physiol. 34: 544-547, 1973. STURM, R. E., E. L. RITMAN, R. J. HANSEN, AND E. H. WOOD. Recording of multichannel analog data and video images on the same videotape or disc. J. Appl. PhysioZ. 36: 761-764, 1974. WILLIAMS, J. C. P., R. E. STURM, A. G. TSAKIRIS, AND E. H. WOOD. Biplane videoangiography. J. Appl. PhysioL. 24: 724-727, 1968.
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