Respiration
Physiology
(1976) 26; 55-64; North-Holland
Publishing
Company,
Amsterdam
INCREASED ELASTIC RECOIL AS A DETERMINANT OF PULMONARY BAROTRAUMA IN DIVERS’
H. J. H. COLEBATCH, School of Medicine,
University
M. M. SMITH2 and C. K. Y. NG of New South
Wales, Sydney,
Australia
Abstract. The elastic and conductive behaviour of the lungs were studied in sixteen divers during an interrupted deflation from total lung capacity (TLC). The results in six divers, who had suffered pulmonary barotrauma (PBT) during shallow water diving, were compared with the findings in a control group of divers. Conductive behaviour and mean lung volumes were similar in the two groups. Compared with the control group, the PBT group had higher maximum transpulmonary pressures and a lower static pulmonary compliance, and deflated their lungs earlier. In relatively stiff lungs, an even distribution of elastance may increase susceptibility to barotrauma, because the more compliant zones are subjected to a greater strain. Pulmonary barotrauma appears to select from the total population of healthy divers those with lungs of decreased distensibility. Diving Pulmonary compliance
Pulmonary conductance Static pressure-volume curve
The escape of gas into the interstitial tissue of the lungs and mediastinum (pulmonary barotrauma) occasionally causes respiratory distress during diving. It is thought to occur when an increased transpulmonary pressure, occasioned by a reduction of ambient pressure causes sufficient strain to rupture alveolar septae (Schaeffer et al., 1958). Divers are taught to exhale gas during ascent and therefore it has been suggested that rupture results from localized overinflation, associated with an abnormal distending pressure, in an area of the lung in which gas is trapped (Lanphier, 1965 ; Liebow et al., 1959). On this hypothesis, bronchial disease may increase the risk of rupture of the lung during diving. Individual variation in the elastic behaviour of the lungs has not been considered as a factor determining susceptibility to rupture of alveolar tissue: but the development of abnormal elastic forces, whether or not airways are obstructed, is the essential condition for pulmonary barotrauma. Acceptedfor
publication
4 October
1975.
’ This study was supported by a grant from the National Health and Medical Research Council of Australia. ’ Senior Research Officer, National Health and Medical Research Council of Australia. 55
56
H. J.H. COLEBATCH, M. M. SMITH
and C. K. Y. NC
Evidence of airway obstruction was found in one of two subjects with pulmonary barotrauma and air embolism reported by Liebow et al. (1959). In the second case a cyst developed in the left lower lobe, but no evidence was provided to show that it resulted from obstruction of a local airway. In two fatal cases, reported by Kinsey (1954), no local lesions, other than interstitial emphysema and air embolism, were found in the lungs. In the present study, the mechanical behaviour of the lungs of divers who had suffered pulmonary barotrauma was compared with a group of healthy divers. The findings show that the group who had suffered pulmonary barotrauma have less distensible lungs than the healthy divers. Methods The subjects were 16 qualified divers from the Naval Diving School, Balmoral, Sydney. They had spent not less than 100 hours underwater using rebreathing equipment. Six divers had suffered an episode of pulmonary barotrauma (PBT) during shallow water diving (less than 20 m below sea level), while using self contained breathing equipment, 9 days to 2 years prior to study. In each of these 6 divers, escape of gas into the mediastinal tissues had been established radiologically, and one subject had had a small apical pneumothorax ; none showed evidence of air embolism. The remaining ten divers had not experienced any diving accidents involving their lungs and served as a control group. The divers were studied over a period of six years from August 1966. MEASUREMENTS
The vital capacity (VC) and FEVr were measured with a 9-litre Collins spirometer, absolute lung volume by nitrogen washout, or by body plethysmography. The static pressure-volume (P-V) properties of the lung were measured with an oesophageal balloon using the technique of Milic-Emili et al., (1964); lung volume (VL) and static transpulmonary pressure, Pst(L), were recorded during an interrupted expiration from total lung capacity (TLC) after three maximal inspirations. Transpulmonary pressure (PL) was measured with a Statham differential strain gauge (PM 131 TC) and gas flow rate at the mouth (%‘) with a Fleisch pneumotachometer (No. 2) connected to a differential transducer (Elema Schonander, model EMT 32). Lung volume change was obtained by integration of the instantaneous flow rate; and PL, V and VL were recorded simultaneously (Elema Schonander, Mingograf 34). The pressure, flow and volume recording systems were calibrated prior to each study and were linear (within 2%) over the ranges used. All lung volumes were corrected to BTPS.The predicted values were obtained from the regression equations of Goldman and Becklake (1959). Details of the analysis of the P-V data have been published (Finucane and Colebatch, 1969). Pulmonary conductance (GL) was also obtained during an interrupted expiration from TLC by relating V at the time of interruption to the difference in transpulmonary pressure between the dynamic and static condition (fig. 1; Colebatch et al.,
57
PULMONARY BAROTRAUMA
PRESSURE cmH20
VOLUME Liir*s
GAS FLOW LJscc
Fig. 1. Recording from a healthy diver of transpulmonary pressure (PL), change in lung volume and gas flow at the mouth obtained during a maximum inspiratory effort and subsequently during an interrupted expiration. At the arrow the sensitivity of the pressure recording is doubled. Expiration is upwards. The increase in F’Lat each interruption represents the dynamic component of PL.
1973). To ensure that the measurements of GL were made at approximately the same ir in an individual at different lung volumes and from one individual to another, iT was controlled during deflation. The subject exhaled through a hole (5-11 mm diameter) in a rubber stopper, which provided an external resistance. In one diver in the barotrauma group GL during deflation was not obtained. In all other subjects, GL values from successive deflations were related to the corresponding Pst(L), and TABLE 1 Anthropometric data and lung volumes in divers
Measurement
Control
Barotrauma
Number of divers Age, years Height, cm FEV, ml FEVJVC% TLC ml ‘A predicted FRC ml % predicted VC ml % predicted RV ml 0/0predicted
10 22.8 k3.6 175 +5.2 4,310+530 80 +4 7,060+760 102 510 3,370 + 780 91 *22 5,360 + 700 104 *lo 1,680 f 370 97 +_24
6 21.0 k1.8 179 +2.5 4,610*420 81 k4 7,040 f 480 96 +8 3,140*490 81 +14 5,700+450 101 +8 1,340 f 220 74 +14
Values are mean +SD. Respective mean values in the two groups did not differ significantly from each other. Volumes given are at BTPS.
58
H. J. H. COLEBATCH, M. M. SMITH
and C. K. Y. NG
Fig. 2. Pressure-volume curves in 10 healthy divers (left panel) and 6 divers who had suffered pulmonary barotrauma (right panel). The curves are drawn from the transpulmonary pressure produced after a maximum inspiration when gas was held in the lungs against a closed valve. A wider range of lung volumes is found in the healthy subjects than in the barotrauma group.
the regression of GL on Pst(L) was obtained by the method of least squares. Conductance during tidal breathing was also obtained by interruption of inspiration and expiration ; a mean value from 4-6 measurements was calculated for each subject. Results LUNG VOLUMES
The group of divers were of similar age and height and had similar lung volumes and ventilatory capacity (table 1). P-v RELATIONSHIPS Individual pressure-volume curves for both groups are shown in fig. 2. When lung volume was expressed as a percentage of the predicted TLC, the variation in lung volume at fixed Pst(L) was greater in the control group. When volume was expressed as a percentage of the measured TLC (fig. 3), the lungs of the PBT group showed earlier deflation and a lower slope for the linear part of the deflation curve than did the lungs of the control divers. The pressures across the lung during a sustained maximum inspiration, and when the subject relaxed his respiratory muscles with the gas held in his lungs by a closed valve (at approximately 2% less than TLC), were significantly greater in the PBT group than in the control group (table 2). The volume of gas in the lungs at Pst(L)
59
PULMONARY BAROTRAUMA 100 -
90 -
90
-
m-
20
0
v
1, 0
PRESSURE 10
20
cm&O 30
40
60
Fig. 3. Mean pressure-volume curves in the same subjects as in fig. 2 with lung volume for each subject plotted as a percentage of his total lung capacity. The lungs of the barotrauma subjects deflate earlier and the slope of the linear part of the curve is lower than in the control group. The bars define one standard deviation of pressure or volume.
of 10.0 cm H,O was less and pulmonary compliance (CL) at FRC, whether expressed as an absolute value or as a percentage of TLC, was lower in the PBT group than in the control group. Lung volumes at Pst(L) of 15 cm HZ0 and 6 cm HZ0 were also less in the PBT group (P < 0.05). GL-Pst@) RELATIONSHIPS In all subjects studied the regression of GL on Pst(L) was significant (P < 0.01). In the barotrauma group the average slope of the regression was lower and the intercept on the Pst(L) axis at zero conductance had a lower value than was found in the control group of divers, but these differences did not reach statistical significance (table 3). Conductance measured during tidal breathing was also similar in the two groups. Discussion
The higher recoil pressures, earlier deflation of the lungs and lower static CL show that divers who have suffered barotrauma have less distensible lungs than a control group of divers. The elastic behaviour of the lungs of the control group was similar to that found in other healthy young adults (Colebatch, unpublished). Theoretically the increased elastic recoil in the PBT group might represent either an increase in surface or an increase in tissue forces. The following evidence suggests that an in-
60
H. J. H. COLEBATCH, M. M. SMITH
and
C. K. Y. NG
TABLE 2 Pressure-volume
measurements
Measurement
Control
Barotrauma
Number of divers
10
6
Static transpulmonary pressure Pst(L), cm H,O At maximum inspiration Relaxed at TLC
36.4k5.2 25.1 ,4.1
46.2kl.l 32.8k3.5
+
Lung volume at Pst(L) 10 cm H,O ml % TLC
5.48 +0.82 77.616.8
4.37 +0.59 61.8k4.6
* +
Static pulmonary compliance at FRC, litre/cm Hz0 % TLC/cm Hz0
0.392+0.075 5.54kO.90
0.253 kO.033 3.6OkO.42
+
+ +
Values are mean + SD. Abbreviations : TLC = total lung capacity; FRC = functional residual capacity. * statistical significance of difference, barotrauma from control group: P i 0.05, + P < 0.01.
crease in surface forces is an unlikely explanation. The earlier deflation of the lungs in the PBT group was found in the lower range of lung volumes, when surface forces are low (Bachofen et al., 1970). In those conditions in which abnormally early deflation of the lungs has been attributed to an increase in surface forces, alveoli are unstable, the maximum lung volume decreased and the function of the lungs is usually severely disturbed (Avery and Said, 1965 ; Finucane et al., 1970). In contrast the divers who had suffered barotrauma all appeared in normal health and as a group their TLC was not decreased. The effect on elastic behaviour of an increase in surface forces has been sfudied in animals poisoned with Paraquat. In cats, at a time when the alveolar surface lining was disrupted and the surface tension of lung extracts increased, the air deflation P-V curve of inflatable units was normal, but maximum lung volume was decreased (Ng, 1972). In what appears to have been a more severe depletion of surfactant in rats, Fisher et al. (1973) found abnormally early deflation of the lungs as well as alveolar oedema. Although these experiment do not provide a pure model of an increase in alveolar surface tension, they suggest that, when an increase in surface forces is responsible for early deflation of the lungs, there are associated abnormalities not compatible with otherwise normal lung function. Therefore for the purpose of the present discussion increased elastic recoil in the PBT group will be taken to represent an increase in tissue forces and the possibility of an increase in surface forces will not be further considered.
PULMONARY
61
BAROTRAUMA
TABLE 3 Relationship
between pulmonary conductance, GL, and static transpulmonary
pressure, Pst(L)
Barotrauma
Measurement
Control
Number of divers Slope dGL/dPst(L) Intercept Pst(L), axis cm Hz0 GL at Pst(L), 5 cm H,O GLtidal breathing expiration inspiration
10 0.0631 kO.0112 - 2.98 k4.79 0.379f0.121
5 0.0369+0.0176 -6.12 +6.97 0.349 kO.124
0.508+0.157 0.466) 0.075
0.397 kO.112 0.525 kO.156
Values are mean k SD. Respective mean values in the two groups did not differ significantly from each other.
In their ability to expel gas from their lungs rapidly and in the conductive behaviour of their lungs there were no significant differences between the PBT group and the healthy divers. While the present studies reveal no evidence that barotrauma was the result of airway obstruction, temporary airway obstruction at the time of injury would not have been detected. However, it would be remarkable if airway obstruction occurred only in divers whose lungs showed an increase in elastic recoil. The more plausible explanation is that the increased elastic recoil was causally related to the episode of pulmonary barotrauma. There are two possible relationships between stiff lungs and pulmonary barotrauma. It is possible that an episode of PBT makes the lungs stiffer, or that subjects with stiff lungs are more susceptible to PBT. On the following grounds the former explanation appears to be unlikely. Asthmatic subjects have an increased incidence of interstitial emphysema (Macklin and Macklin, 1944). If dissection of gas through tissues always made the lungs stiffer (which would have to be the case to explain the results in PBT subjects) then subjects with severe asthmatic episodes would tend to show an increase in elastic recoil. In fact elastic recoil is decreased in asthmatic subjects (Finucane and Colebatch, 1969). In addition, the present studies were made as long as 2 years after the episode of PBT when any acute changes should have resolved. There is thus no evidence that increased stiffness is the result of PBT. The final possibility, that subjects who happen to have relatively stiff lungs are more susceptible to PBT, will now be considered. As the diver ascends from depth, ambient pressure decreases and lung volume increases according to Boyle’s Law. At full inflation, intrapulmonary gas pressure is opposed by the combined elastic recoil of the lungs and chest wall. The inflating pressure is therefore distributed partly across the lung and partly across the chest wall. A continued decrease in ambient pressure produces a relative increase in intrapulmonary gas pressure; under these conditions rupture of the lungs will be determined, in part, by whether the lung
62
H. J. H. COLEBATCH,
M. M. SMITH
and
C. K. Y. NG
itself or the chest wall is the less distensible part of the system. If the chest wall (and abdomen) is made very stiff by the use of a binder, the incidence of PBT in animal experiments is decreased (Schaeffer et al., 1958; Malhotra and Wright, 1960). However, there is no simple relationship between these results and the findings in the present study. In normal men the stiffness of the lung at high lung volumes is many times the stiffness of the chest wall (Agostoni and Mead, 1964). Contraction of antagonistic abdominal muscles may limit lung expansion in some healthy subjects (Mead et al., 1963) but is uncommon and has no obvious relationship with the elastic behavior of the lungs. The larger transpulmonary pressure at TLC in the PBT group does not necessarily mean larger stresses in the parenchyma. Assuming that stiff and distensible lungs are made with the same material, then a decreased compliance over a similar range of lung volumes may be related to an increased density (number per unit cross section of tissue) of elastic tibres. In the model of Mead (1970) this means an increase in the number of fibres all of equal elastance and resting length. Both the normal and the less compliant models should rupture at the same strain and stress in the fibres, but the latter at higher PL’S than the former. The influence of lung stiffness on expansion of alveolar gas may be evaluated using Boyle’s Law. ~VL.
Palv = (VL+AVL) .(Palv+APs+dPL)
where VL = initial lung volume; Palv = initial alveolar pressure ; A PS = change in ambient pressure; APL = change in pulmonary elastic recoil pressure. Simplifying, rearranging and regarding decreases in pressure as negative, we obtain : APs- APL AvL = vL (Palv-APs+APL) from which it becomes evident that the greater the increase in PL the smaller is the change in lung volume. For a decrease in ambient pressure to half the initial value, the increase in lung volume (assuming an initial volume about half TLC) would be approximately 2% less for the PBT group than the control group. Thus the expansion of gas and therefore the strain on alveolar tissue appears to be somewhat smaller for subjects with stiffer lungs. Therefore, the overall increase of lung stiffness, of itself, does not account for an increased susceptibility to ‘pulmonary barotrauma. However, it is possible that the increased elastic recoil in the PBT group is associated with a non-uniform increase in stiffness throughout the lungs, that is, that the density of elastic tibres is not constant throughout the lungs. Areas with a normal density of tibres may be surrounded by areas with an increased density of fibres. If all airspaces communicate and gradients of transpulmonary pressure are disregarded, then PL is uniform throughout the lungs. According to the analysis of Mead et al., (1970) the transmission of PL to the outer surface of areas within the lung may be expressed :
PULMONARY
BAROTRAUMA
63
nFo PL = A where n = number of elements; Fo = normal force of a single element; A = area of the surface. If the number of elements (fibres) within a given area is decreased then the force transmitted by a single element will increase in proportion to the decrease. Thus the more compliant zones will be subjected to a larger strain. For a given decrease in ambient pressure PL is larger the stiffer the lung as a whole, but the overall strain is similar in the stiff and normal lungs. As a result normal lungs may be uniformly strained to a lesser extent than are zones with normal CL embedded in a stiffer lung. These zones may reach a strain at which rupture occurs even though the overall strain is the same in both the stiff and the more distensible lungs. During rapid ascent many divers notice feelings of faintness attributed to an increase in intrapulmonary pressure (Edmonds and Thomas, 1972), but pulmonary barotrauma is uncommon. It is therefore possible that the lungs of many divers are subjected to a strain somewhat greater than achieved during maximum inspiration. The findings in the present study suggest that in these circumstances the divers whose lungs have increased elastic recoil are more likely to develop pulmonary barotrauma. Theoretically it would be possible to measure elastic recoil and exclude from diving those subjects whose lungs are stiffer than average. But an estimate of subjects who may be at risk for this reason suggests that such an approach would not usually be worthwhile. Of approximately 500 divers at risk, only 6 suffered PBT. Review of studies of elastic recoil in 26 healthy male subjects less than 40 years of age (Colebatch, unpublished) showed that 3 had an increase in elastic recoil similar to that found in the PBT group. Given a similar proportion, the lungs of about 58 of 500 divers would have shown increased elastic recoil. Therefore, the majority with increased elastic recoil did not suffer PBT. The present findings identify mechanical properties of the lung that make individuals more susceptible to PBT. In special circumstances, an assessment of the mechanical properties of the lungs may be relevant to an attempt to minimize all the risks involved in diving. Acknowledgements
The authors are indebted to Dr Carl Edmonds and the School of Underwater Medicine, H. M. A. S. PENGUIN for the opportunity to study the divers concerned in this report, to the Department of Medical Illustration, University of New South Wales, for photographic work, and to the anonymous reviewer who suggested that healthy subjects with stiff lungs may have an uneven distribution of elastance. References Avery,
M. E. and S. Said (1965). Surface
phenomena
in lungs in health and disease. Medicine 44: 503-526.
H. J. 13.COLEBATCH,
64
M. ivi. SMITH
and c. K. Y. NG
Agostoni, E. and J. Mead (1964). Statics of the respiratory system. In: Handbook of Physiology Sect. 3. Respiration. Vol. 2, edited by W. 0. Fenn and H. Rahn. Washington, D.C., Am. Physiol. Sot., pp. 387-409. Bachofen, H., J. Hildebrandt and M. Bachofen (1970). Pressure-volume curves of air and liquid-filled excised lungs - surface tension in situ. J. Appl. Physiol. 29 : 42243 1. Colebatch, H. J. H., K. E. Finucane and M. M. Smith (1973). Pulmonary conductance and elastic recoil relationships in asthma and emphysema. J. Appl. Physiol. 34: 143-153. Edmonds, C. and R. L. Thomas (1972). Medical aspects ofdiving- part 5. Med. J. Aust. 2: 14161419. Fisher, H. K., J. A. Clements and R. R. Wright (1973). Pulmonary effects of the herbicide paraquat studied 3 days after injection in rats. J. Appl. Physiol. 35: 268-273. Finucane, K. E. and H. J. H. Colebatch (1969). Elastic behaviour of the lungs in patients with airway obstruction. J. Appl. Physiol. 26: 330-338. Finucane, K. E., H. J. H. Colebatch, M. R. Robertson and B. H. Gandevia (1970). The mechanism of respiratory failure in a patient with viral (varicella) pneumonia. Am. Rev. Respir. Dis. 101 : 949-958. Goldman, H. 1. and M. R. Becklake (1959). Respiratory function tests: Normal values at median altitudes and the prediction of normal results. Am. Rev. Tuberc. Pulm. Dis. 79: 457-467. Kinsey, J. L. (1954). Air embolism as a result of submarine escape training. U.S. Armed Forces Med. J. 5: 243-255.
Lanphier, E. H. (1965). Overinflation of the lungs. In: Handbook of Physiology. Sect. 3. Respiration. Vol. 2, edited by W. 0. Fenn and H. Rahn. Washington, D.C., Am. Physiol. Sot., pp. 118991193. Liebow, A. A., J. E. Stark, J. Vogel and K. E. Schaeffer (1959). Intrapulmonary air trapping in submarine escape training casualties. U.S. Armed Forces Med. J. 10: 265-289. Macklin, M. T. and C. C. Macklin (1944). Malignant interstitial emphysema of the lungs and mediastinum as an important occult complication in many respiratory diseases and other conditions: An interpretation of the clinical literature in the light of laboratory experiment. Medicine 23: 281-358. Malhotra, M. S. and H. C. Wright (1961). Arterial air embolism during decompression and its prevention. Proc. Roy. Sot. (London) Ser. B 154: 4188427. Mead, J., J. Milic-Emili and J. M. Turner (1963). Factors limiting depth of maximum inspiration in human subjects. J. Appl. Physiol. 18: 2955296. Mead, J., T. Takishma and D. Leith (1970). Stress distribution in the lungs; a model of pulmonary elasticity. J. Appl. Physiol. 28: 59G608. Milic-Emili, J., J. Mead, J. M. Turner and E. M. Glauser (1964). Improved technique for estimating pleural pressure from esophageal balloons. J. Appl. Physiol. 19 : 207-211. Ng, C. K. Y. (1972). Alveolar Surface Tension and the Elastic Behaviour of the Lung. M. SC. Thesis, University of New South Wales. Schaeffer, K. E., W. P. McNulty, C. Carey and A. A. Liebow (1958). Mechanisms in development of interstitial emphysema and air embolism on decompression from depth. .I. Appl. Physiol. 13: 15-29.
Physiology
(1976) 26; 55-64; North-Holland
Publishing
Company,
Amsterdam
INCREASED ELASTIC RECOIL AS A DETERMINANT OF PULMONARY BAROTRAUMA IN DIVERS’
H. J. H. COLEBATCH, School of Medicine,
University
M. M. SMITH2 and C. K. Y. NG of New South
Wales, Sydney,
Australia
Abstract. The elastic and conductive behaviour of the lungs were studied in sixteen divers during an interrupted deflation from total lung capacity (TLC). The results in six divers, who had suffered pulmonary barotrauma (PBT) during shallow water diving, were compared with the findings in a control group of divers. Conductive behaviour and mean lung volumes were similar in the two groups. Compared with the control group, the PBT group had higher maximum transpulmonary pressures and a lower static pulmonary compliance, and deflated their lungs earlier. In relatively stiff lungs, an even distribution of elastance may increase susceptibility to barotrauma, because the more compliant zones are subjected to a greater strain. Pulmonary barotrauma appears to select from the total population of healthy divers those with lungs of decreased distensibility. Diving Pulmonary compliance
Pulmonary conductance Static pressure-volume curve
The escape of gas into the interstitial tissue of the lungs and mediastinum (pulmonary barotrauma) occasionally causes respiratory distress during diving. It is thought to occur when an increased transpulmonary pressure, occasioned by a reduction of ambient pressure causes sufficient strain to rupture alveolar septae (Schaeffer et al., 1958). Divers are taught to exhale gas during ascent and therefore it has been suggested that rupture results from localized overinflation, associated with an abnormal distending pressure, in an area of the lung in which gas is trapped (Lanphier, 1965 ; Liebow et al., 1959). On this hypothesis, bronchial disease may increase the risk of rupture of the lung during diving. Individual variation in the elastic behaviour of the lungs has not been considered as a factor determining susceptibility to rupture of alveolar tissue: but the development of abnormal elastic forces, whether or not airways are obstructed, is the essential condition for pulmonary barotrauma. Acceptedfor
publication
4 October
1975.
’ This study was supported by a grant from the National Health and Medical Research Council of Australia. ’ Senior Research Officer, National Health and Medical Research Council of Australia. 55
56
H. J.H. COLEBATCH, M. M. SMITH
and C. K. Y. NC
Evidence of airway obstruction was found in one of two subjects with pulmonary barotrauma and air embolism reported by Liebow et al. (1959). In the second case a cyst developed in the left lower lobe, but no evidence was provided to show that it resulted from obstruction of a local airway. In two fatal cases, reported by Kinsey (1954), no local lesions, other than interstitial emphysema and air embolism, were found in the lungs. In the present study, the mechanical behaviour of the lungs of divers who had suffered pulmonary barotrauma was compared with a group of healthy divers. The findings show that the group who had suffered pulmonary barotrauma have less distensible lungs than the healthy divers. Methods The subjects were 16 qualified divers from the Naval Diving School, Balmoral, Sydney. They had spent not less than 100 hours underwater using rebreathing equipment. Six divers had suffered an episode of pulmonary barotrauma (PBT) during shallow water diving (less than 20 m below sea level), while using self contained breathing equipment, 9 days to 2 years prior to study. In each of these 6 divers, escape of gas into the mediastinal tissues had been established radiologically, and one subject had had a small apical pneumothorax ; none showed evidence of air embolism. The remaining ten divers had not experienced any diving accidents involving their lungs and served as a control group. The divers were studied over a period of six years from August 1966. MEASUREMENTS
The vital capacity (VC) and FEVr were measured with a 9-litre Collins spirometer, absolute lung volume by nitrogen washout, or by body plethysmography. The static pressure-volume (P-V) properties of the lung were measured with an oesophageal balloon using the technique of Milic-Emili et al., (1964); lung volume (VL) and static transpulmonary pressure, Pst(L), were recorded during an interrupted expiration from total lung capacity (TLC) after three maximal inspirations. Transpulmonary pressure (PL) was measured with a Statham differential strain gauge (PM 131 TC) and gas flow rate at the mouth (%‘) with a Fleisch pneumotachometer (No. 2) connected to a differential transducer (Elema Schonander, model EMT 32). Lung volume change was obtained by integration of the instantaneous flow rate; and PL, V and VL were recorded simultaneously (Elema Schonander, Mingograf 34). The pressure, flow and volume recording systems were calibrated prior to each study and were linear (within 2%) over the ranges used. All lung volumes were corrected to BTPS.The predicted values were obtained from the regression equations of Goldman and Becklake (1959). Details of the analysis of the P-V data have been published (Finucane and Colebatch, 1969). Pulmonary conductance (GL) was also obtained during an interrupted expiration from TLC by relating V at the time of interruption to the difference in transpulmonary pressure between the dynamic and static condition (fig. 1; Colebatch et al.,
57
PULMONARY BAROTRAUMA
PRESSURE cmH20
VOLUME Liir*s
GAS FLOW LJscc
Fig. 1. Recording from a healthy diver of transpulmonary pressure (PL), change in lung volume and gas flow at the mouth obtained during a maximum inspiratory effort and subsequently during an interrupted expiration. At the arrow the sensitivity of the pressure recording is doubled. Expiration is upwards. The increase in F’Lat each interruption represents the dynamic component of PL.
1973). To ensure that the measurements of GL were made at approximately the same ir in an individual at different lung volumes and from one individual to another, iT was controlled during deflation. The subject exhaled through a hole (5-11 mm diameter) in a rubber stopper, which provided an external resistance. In one diver in the barotrauma group GL during deflation was not obtained. In all other subjects, GL values from successive deflations were related to the corresponding Pst(L), and TABLE 1 Anthropometric data and lung volumes in divers
Measurement
Control
Barotrauma
Number of divers Age, years Height, cm FEV, ml FEVJVC% TLC ml ‘A predicted FRC ml % predicted VC ml % predicted RV ml 0/0predicted
10 22.8 k3.6 175 +5.2 4,310+530 80 +4 7,060+760 102 510 3,370 + 780 91 *22 5,360 + 700 104 *lo 1,680 f 370 97 +_24
6 21.0 k1.8 179 +2.5 4,610*420 81 k4 7,040 f 480 96 +8 3,140*490 81 +14 5,700+450 101 +8 1,340 f 220 74 +14
Values are mean +SD. Respective mean values in the two groups did not differ significantly from each other. Volumes given are at BTPS.
58
H. J. H. COLEBATCH, M. M. SMITH
and C. K. Y. NG
Fig. 2. Pressure-volume curves in 10 healthy divers (left panel) and 6 divers who had suffered pulmonary barotrauma (right panel). The curves are drawn from the transpulmonary pressure produced after a maximum inspiration when gas was held in the lungs against a closed valve. A wider range of lung volumes is found in the healthy subjects than in the barotrauma group.
the regression of GL on Pst(L) was obtained by the method of least squares. Conductance during tidal breathing was also obtained by interruption of inspiration and expiration ; a mean value from 4-6 measurements was calculated for each subject. Results LUNG VOLUMES
The group of divers were of similar age and height and had similar lung volumes and ventilatory capacity (table 1). P-v RELATIONSHIPS Individual pressure-volume curves for both groups are shown in fig. 2. When lung volume was expressed as a percentage of the predicted TLC, the variation in lung volume at fixed Pst(L) was greater in the control group. When volume was expressed as a percentage of the measured TLC (fig. 3), the lungs of the PBT group showed earlier deflation and a lower slope for the linear part of the deflation curve than did the lungs of the control divers. The pressures across the lung during a sustained maximum inspiration, and when the subject relaxed his respiratory muscles with the gas held in his lungs by a closed valve (at approximately 2% less than TLC), were significantly greater in the PBT group than in the control group (table 2). The volume of gas in the lungs at Pst(L)
59
PULMONARY BAROTRAUMA 100 -
90 -
90
-
m-
20
0
v
1, 0
PRESSURE 10
20
cm&O 30
40
60
Fig. 3. Mean pressure-volume curves in the same subjects as in fig. 2 with lung volume for each subject plotted as a percentage of his total lung capacity. The lungs of the barotrauma subjects deflate earlier and the slope of the linear part of the curve is lower than in the control group. The bars define one standard deviation of pressure or volume.
of 10.0 cm H,O was less and pulmonary compliance (CL) at FRC, whether expressed as an absolute value or as a percentage of TLC, was lower in the PBT group than in the control group. Lung volumes at Pst(L) of 15 cm HZ0 and 6 cm HZ0 were also less in the PBT group (P < 0.05). GL-Pst@) RELATIONSHIPS In all subjects studied the regression of GL on Pst(L) was significant (P < 0.01). In the barotrauma group the average slope of the regression was lower and the intercept on the Pst(L) axis at zero conductance had a lower value than was found in the control group of divers, but these differences did not reach statistical significance (table 3). Conductance measured during tidal breathing was also similar in the two groups. Discussion
The higher recoil pressures, earlier deflation of the lungs and lower static CL show that divers who have suffered barotrauma have less distensible lungs than a control group of divers. The elastic behaviour of the lungs of the control group was similar to that found in other healthy young adults (Colebatch, unpublished). Theoretically the increased elastic recoil in the PBT group might represent either an increase in surface or an increase in tissue forces. The following evidence suggests that an in-
60
H. J. H. COLEBATCH, M. M. SMITH
and
C. K. Y. NG
TABLE 2 Pressure-volume
measurements
Measurement
Control
Barotrauma
Number of divers
10
6
Static transpulmonary pressure Pst(L), cm H,O At maximum inspiration Relaxed at TLC
36.4k5.2 25.1 ,4.1
46.2kl.l 32.8k3.5
+
Lung volume at Pst(L) 10 cm H,O ml % TLC
5.48 +0.82 77.616.8
4.37 +0.59 61.8k4.6
* +
Static pulmonary compliance at FRC, litre/cm Hz0 % TLC/cm Hz0
0.392+0.075 5.54kO.90
0.253 kO.033 3.6OkO.42
+
+ +
Values are mean + SD. Abbreviations : TLC = total lung capacity; FRC = functional residual capacity. * statistical significance of difference, barotrauma from control group: P i 0.05, + P < 0.01.
crease in surface forces is an unlikely explanation. The earlier deflation of the lungs in the PBT group was found in the lower range of lung volumes, when surface forces are low (Bachofen et al., 1970). In those conditions in which abnormally early deflation of the lungs has been attributed to an increase in surface forces, alveoli are unstable, the maximum lung volume decreased and the function of the lungs is usually severely disturbed (Avery and Said, 1965 ; Finucane et al., 1970). In contrast the divers who had suffered barotrauma all appeared in normal health and as a group their TLC was not decreased. The effect on elastic behaviour of an increase in surface forces has been sfudied in animals poisoned with Paraquat. In cats, at a time when the alveolar surface lining was disrupted and the surface tension of lung extracts increased, the air deflation P-V curve of inflatable units was normal, but maximum lung volume was decreased (Ng, 1972). In what appears to have been a more severe depletion of surfactant in rats, Fisher et al. (1973) found abnormally early deflation of the lungs as well as alveolar oedema. Although these experiment do not provide a pure model of an increase in alveolar surface tension, they suggest that, when an increase in surface forces is responsible for early deflation of the lungs, there are associated abnormalities not compatible with otherwise normal lung function. Therefore for the purpose of the present discussion increased elastic recoil in the PBT group will be taken to represent an increase in tissue forces and the possibility of an increase in surface forces will not be further considered.
PULMONARY
61
BAROTRAUMA
TABLE 3 Relationship
between pulmonary conductance, GL, and static transpulmonary
pressure, Pst(L)
Barotrauma
Measurement
Control
Number of divers Slope dGL/dPst(L) Intercept Pst(L), axis cm Hz0 GL at Pst(L), 5 cm H,O GLtidal breathing expiration inspiration
10 0.0631 kO.0112 - 2.98 k4.79 0.379f0.121
5 0.0369+0.0176 -6.12 +6.97 0.349 kO.124
0.508+0.157 0.466) 0.075
0.397 kO.112 0.525 kO.156
Values are mean k SD. Respective mean values in the two groups did not differ significantly from each other.
In their ability to expel gas from their lungs rapidly and in the conductive behaviour of their lungs there were no significant differences between the PBT group and the healthy divers. While the present studies reveal no evidence that barotrauma was the result of airway obstruction, temporary airway obstruction at the time of injury would not have been detected. However, it would be remarkable if airway obstruction occurred only in divers whose lungs showed an increase in elastic recoil. The more plausible explanation is that the increased elastic recoil was causally related to the episode of pulmonary barotrauma. There are two possible relationships between stiff lungs and pulmonary barotrauma. It is possible that an episode of PBT makes the lungs stiffer, or that subjects with stiff lungs are more susceptible to PBT. On the following grounds the former explanation appears to be unlikely. Asthmatic subjects have an increased incidence of interstitial emphysema (Macklin and Macklin, 1944). If dissection of gas through tissues always made the lungs stiffer (which would have to be the case to explain the results in PBT subjects) then subjects with severe asthmatic episodes would tend to show an increase in elastic recoil. In fact elastic recoil is decreased in asthmatic subjects (Finucane and Colebatch, 1969). In addition, the present studies were made as long as 2 years after the episode of PBT when any acute changes should have resolved. There is thus no evidence that increased stiffness is the result of PBT. The final possibility, that subjects who happen to have relatively stiff lungs are more susceptible to PBT, will now be considered. As the diver ascends from depth, ambient pressure decreases and lung volume increases according to Boyle’s Law. At full inflation, intrapulmonary gas pressure is opposed by the combined elastic recoil of the lungs and chest wall. The inflating pressure is therefore distributed partly across the lung and partly across the chest wall. A continued decrease in ambient pressure produces a relative increase in intrapulmonary gas pressure; under these conditions rupture of the lungs will be determined, in part, by whether the lung
62
H. J. H. COLEBATCH,
M. M. SMITH
and
C. K. Y. NG
itself or the chest wall is the less distensible part of the system. If the chest wall (and abdomen) is made very stiff by the use of a binder, the incidence of PBT in animal experiments is decreased (Schaeffer et al., 1958; Malhotra and Wright, 1960). However, there is no simple relationship between these results and the findings in the present study. In normal men the stiffness of the lung at high lung volumes is many times the stiffness of the chest wall (Agostoni and Mead, 1964). Contraction of antagonistic abdominal muscles may limit lung expansion in some healthy subjects (Mead et al., 1963) but is uncommon and has no obvious relationship with the elastic behavior of the lungs. The larger transpulmonary pressure at TLC in the PBT group does not necessarily mean larger stresses in the parenchyma. Assuming that stiff and distensible lungs are made with the same material, then a decreased compliance over a similar range of lung volumes may be related to an increased density (number per unit cross section of tissue) of elastic tibres. In the model of Mead (1970) this means an increase in the number of fibres all of equal elastance and resting length. Both the normal and the less compliant models should rupture at the same strain and stress in the fibres, but the latter at higher PL’S than the former. The influence of lung stiffness on expansion of alveolar gas may be evaluated using Boyle’s Law. ~VL.
Palv = (VL+AVL) .(Palv+APs+dPL)
where VL = initial lung volume; Palv = initial alveolar pressure ; A PS = change in ambient pressure; APL = change in pulmonary elastic recoil pressure. Simplifying, rearranging and regarding decreases in pressure as negative, we obtain : APs- APL AvL = vL (Palv-APs+APL) from which it becomes evident that the greater the increase in PL the smaller is the change in lung volume. For a decrease in ambient pressure to half the initial value, the increase in lung volume (assuming an initial volume about half TLC) would be approximately 2% less for the PBT group than the control group. Thus the expansion of gas and therefore the strain on alveolar tissue appears to be somewhat smaller for subjects with stiffer lungs. Therefore, the overall increase of lung stiffness, of itself, does not account for an increased susceptibility to ‘pulmonary barotrauma. However, it is possible that the increased elastic recoil in the PBT group is associated with a non-uniform increase in stiffness throughout the lungs, that is, that the density of elastic tibres is not constant throughout the lungs. Areas with a normal density of tibres may be surrounded by areas with an increased density of fibres. If all airspaces communicate and gradients of transpulmonary pressure are disregarded, then PL is uniform throughout the lungs. According to the analysis of Mead et al., (1970) the transmission of PL to the outer surface of areas within the lung may be expressed :
PULMONARY
BAROTRAUMA
63
nFo PL = A where n = number of elements; Fo = normal force of a single element; A = area of the surface. If the number of elements (fibres) within a given area is decreased then the force transmitted by a single element will increase in proportion to the decrease. Thus the more compliant zones will be subjected to a larger strain. For a given decrease in ambient pressure PL is larger the stiffer the lung as a whole, but the overall strain is similar in the stiff and normal lungs. As a result normal lungs may be uniformly strained to a lesser extent than are zones with normal CL embedded in a stiffer lung. These zones may reach a strain at which rupture occurs even though the overall strain is the same in both the stiff and the more distensible lungs. During rapid ascent many divers notice feelings of faintness attributed to an increase in intrapulmonary pressure (Edmonds and Thomas, 1972), but pulmonary barotrauma is uncommon. It is therefore possible that the lungs of many divers are subjected to a strain somewhat greater than achieved during maximum inspiration. The findings in the present study suggest that in these circumstances the divers whose lungs have increased elastic recoil are more likely to develop pulmonary barotrauma. Theoretically it would be possible to measure elastic recoil and exclude from diving those subjects whose lungs are stiffer than average. But an estimate of subjects who may be at risk for this reason suggests that such an approach would not usually be worthwhile. Of approximately 500 divers at risk, only 6 suffered PBT. Review of studies of elastic recoil in 26 healthy male subjects less than 40 years of age (Colebatch, unpublished) showed that 3 had an increase in elastic recoil similar to that found in the PBT group. Given a similar proportion, the lungs of about 58 of 500 divers would have shown increased elastic recoil. Therefore, the majority with increased elastic recoil did not suffer PBT. The present findings identify mechanical properties of the lung that make individuals more susceptible to PBT. In special circumstances, an assessment of the mechanical properties of the lungs may be relevant to an attempt to minimize all the risks involved in diving. Acknowledgements
The authors are indebted to Dr Carl Edmonds and the School of Underwater Medicine, H. M. A. S. PENGUIN for the opportunity to study the divers concerned in this report, to the Department of Medical Illustration, University of New South Wales, for photographic work, and to the anonymous reviewer who suggested that healthy subjects with stiff lungs may have an uneven distribution of elastance. References Avery,
M. E. and S. Said (1965). Surface
phenomena
in lungs in health and disease. Medicine 44: 503-526.
H. J. 13.COLEBATCH,
64
M. ivi. SMITH
and c. K. Y. NG
Agostoni, E. and J. Mead (1964). Statics of the respiratory system. In: Handbook of Physiology Sect. 3. Respiration. Vol. 2, edited by W. 0. Fenn and H. Rahn. Washington, D.C., Am. Physiol. Sot., pp. 387-409. Bachofen, H., J. Hildebrandt and M. Bachofen (1970). Pressure-volume curves of air and liquid-filled excised lungs - surface tension in situ. J. Appl. Physiol. 29 : 42243 1. Colebatch, H. J. H., K. E. Finucane and M. M. Smith (1973). Pulmonary conductance and elastic recoil relationships in asthma and emphysema. J. Appl. Physiol. 34: 143-153. Edmonds, C. and R. L. Thomas (1972). Medical aspects ofdiving- part 5. Med. J. Aust. 2: 14161419. Fisher, H. K., J. A. Clements and R. R. Wright (1973). Pulmonary effects of the herbicide paraquat studied 3 days after injection in rats. J. Appl. Physiol. 35: 268-273. Finucane, K. E. and H. J. H. Colebatch (1969). Elastic behaviour of the lungs in patients with airway obstruction. J. Appl. Physiol. 26: 330-338. Finucane, K. E., H. J. H. Colebatch, M. R. Robertson and B. H. Gandevia (1970). The mechanism of respiratory failure in a patient with viral (varicella) pneumonia. Am. Rev. Respir. Dis. 101 : 949-958. Goldman, H. 1. and M. R. Becklake (1959). Respiratory function tests: Normal values at median altitudes and the prediction of normal results. Am. Rev. Tuberc. Pulm. Dis. 79: 457-467. Kinsey, J. L. (1954). Air embolism as a result of submarine escape training. U.S. Armed Forces Med. J. 5: 243-255.
Lanphier, E. H. (1965). Overinflation of the lungs. In: Handbook of Physiology. Sect. 3. Respiration. Vol. 2, edited by W. 0. Fenn and H. Rahn. Washington, D.C., Am. Physiol. Sot., pp. 118991193. Liebow, A. A., J. E. Stark, J. Vogel and K. E. Schaeffer (1959). Intrapulmonary air trapping in submarine escape training casualties. U.S. Armed Forces Med. J. 10: 265-289. Macklin, M. T. and C. C. Macklin (1944). Malignant interstitial emphysema of the lungs and mediastinum as an important occult complication in many respiratory diseases and other conditions: An interpretation of the clinical literature in the light of laboratory experiment. Medicine 23: 281-358. Malhotra, M. S. and H. C. Wright (1961). Arterial air embolism during decompression and its prevention. Proc. Roy. Sot. (London) Ser. B 154: 4188427. Mead, J., J. Milic-Emili and J. M. Turner (1963). Factors limiting depth of maximum inspiration in human subjects. J. Appl. Physiol. 18: 2955296. Mead, J., T. Takishma and D. Leith (1970). Stress distribution in the lungs; a model of pulmonary elasticity. J. Appl. Physiol. 28: 59G608. Milic-Emili, J., J. Mead, J. M. Turner and E. M. Glauser (1964). Improved technique for estimating pleural pressure from esophageal balloons. J. Appl. Physiol. 19 : 207-211. Ng, C. K. Y. (1972). Alveolar Surface Tension and the Elastic Behaviour of the Lung. M. SC. Thesis, University of New South Wales. Schaeffer, K. E., W. P. McNulty, C. Carey and A. A. Liebow (1958). Mechanisms in development of interstitial emphysema and air embolism on decompression from depth. .I. Appl. Physiol. 13: 15-29.
