Effect of Acute Smoke Inhalation on Angiotensin Converting Enzyme, Plasminogen Activator, and Angiotensin-II in the Dog
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1 ANNALS OF CLINICAL AND LABORATORY SCIENCE, Vol. 19, No. 6 Copyright 1989, Institute for Clinical Science, Inc. Effect of Acute Smoke Inhalation on Angiotensin Converting Enzyme, Plasminogen Activator, and Angiotensin-II in the Dog W ILLIAM R. CLARK, M.D.t AGOSTINO M OLTENI, M.D., Ph.D.* GARY NIEM AN, B.S.f LOREDANA BRIZIO-M OLTENI, M.D 4 and NORMAN H. SOLLIDAY, M.D 4 fdepartment of Surgery, SUNY Health Science Center at Syracuse Syracuse, NY and fdepartment of Pathology, Northwestern University Medical School Chicago, 1L ABSTRACT Smoke inhalation injuries in hum ans are associated w ith m any uncontrolled variables which impact on the lung and make the cause of the pulmonary response difficult to assess. In this report, an established model of smoke inhalation injury in the dog was used to study the early responses of tissue and serum angiotensin-converting enzym e (ACE), tissue plasm inogen activator (PLA), and plasma angiotensin II. Animals were exposed to smoke from burning sawdust and kerosene for five minutes. The hem odynamic and pulmonary mechanical responses were typical with a rise in pulmonary artery pressure, pulmonary vascular resistance, and venous adm ixture (shunt fraction) while dynamic compliance fell. W ithin five m inutes of smoke exposure, lung ACE declined without any change in serum ACE. Lung PLA dropped one hour after injury. Plasma angiotensin II increased w ithin 30 m inutes w ithout evidence for systemic h y p erten sion. These early enzym atic changes substantiate the presence of pulm o nary endothelial damage known to occur in this form of chemical injury. These changes may condition the lung s physiologic response to the injury and to additional stresses which are m ultiple w hen smoke inhalation occurs in conjunction w ith a cutaneous burn. Introduction * Send reprint requests to: W. R. Clark, M.D. D epartm ent of Surgery, SUNY H ealth Science c i i i. i Center at Syracuse, 750 East Adams Street, Syra- Smoke inhalation Severe enough to cuse, NY injure the lung increases the m orbidity /89/ $01.50 Institute for Clinical Science, Inc.
2 ENZYMATIC RESPONSE TO ACUTE SMOKE INHALATION-DOG LUNG 45 3 and m o rtality of b u rn victim s significantly. 10,25,27 T he burn illness is fre quently prolonged, 12,23 and the clinical course is often complicated by episodes of hem odynam ic instability and sepsis, all of which affect the lung. 19 The lung is th e site of n um erous m etabolic p ro c e s s e s. T h is o rg a n r e g u la te s gas exchange; it also m odulates system ic homeostasis by controlling the secretion of substances such as angiotensin-1 -conv ertin g enzym e (ACE), plasm inogen activator (PLA), prostaglandins, and throm boxane. Any pulm onary parenchymal injury may result in major changes in pulmonary endocrine balance and also alter the systemic physiologic state of the injured subject. It has b een shown that exposure of one lung in dogs to wood smoke caused an increased ACE activity in the same lung while no changes were observed in the contralateral organ m aintained in an hypoxic condition.3 Preliminary findings in a d u lt b u rn v ictim s in d ic a te th a t p a tien ts w ith an inhalation injury in addition to a cutaneous burn had higher v alu es o f se ru m A CE a c tiv ity th an patients suffering from therm al injury alone.5,21 Serum ACE is secreted by pulm onary en d o th elial cells; it converts approximately 90 percent of the angiotensin-i e n te rin g th e pulm onary capillary b ed to angiotensin-ii.30 In addition, ACE inactivates 20 to 30 p e rc e n t o f b rad y k in in reach in g th e lung. 24 Changes in serum and lung ACE activity, PLA activity, as well as prostaglandins and thromboxane (also secreted by pulmonary endothelial cells) may be used as markers of the pulmonary parenchymal dam age caused by different injurious agents: exposure to chronic h y poxia, ra d ia tio n, a d m in istra tio n of m onocrotaline, bleom ycin, paraquat, th io u re a. 15,16,17,20,31,33 The enzym atic changes seen following these forms of injury play a significant role in the pathogenesis of pulm onary fibrosis. A m odel of smoke inhalation in the dog8,9,22 was used in this study to confirm and to define some of the consequences of smoke inhalation on enzymes secreted by the lung endothelium. Both ACE and PLA activity w ere m easured in lungs; serum ACE activity and plasm a angioten sin-ii concentration w ere also m easured to evaluate the response of the renin-angiotensin system to injury of the lung parenchym a. M aterials and M ethods M ongrel dogs, 13 to 25 kg, of both sexes w ere anesthetized w ith sodium pentobarbital, 30 mg per kg, intubated w ith a cuffed endotracheal tube, and ventilated with room air using a piston ventilator.* The initial tidal volume was 15 cc per kg, the respiratory rate 15 per m in; positive end expiratory pressure (PEEP) equal to five cm of w ater was used to compensate for the open-chested condition. Femoral arterial and venous cutdow ns w ere established using polyethylene tubes (two mm ID). All vascular and airway cannule were connected to pressure transducers leveled at the s p in e.t A th e r m is to r tip p e d, flo w directed 7 French, 110 cm catheter^ was inserted through the left external jugular vein and threaded into the pulm onary artery for pulm onary artery pressure (PAP), pulmonary artery wedge pressure (PAW), cardiac output (CO), and central tem perature m easurem ents. The animals w ere placed in the right lateral position, and a heating pad was placed over and under the caudal part of the body to maintain the body tem perature at 37 to 38. Blood gases were m easured on a Radiom eter, Acid-base Laboratory * Harvard Instrum ent Co., Cambridge, MA. t Sorenson, No. MK4-0400TNVF. $ Sorenson, CAT No Sorenson cardiac output computer, Cat. No
3 4 5 4 CLARK, MOLTENI, NIEMAN, BRIZIO-MOLTENI, AND SOLLIDAY IIC. 1 Intravenous N ah C 0 3, 1000 m Eq per liter, was used to correct any base deficit initially p resent using the equation BE X weight (kg) x 0.03 = ml of N a H C 0 3. T he re s p ira to ry ra te was adjusted to establish a control PaCOa of 35 ± 5 mm Hg. Airway pressure was m easured from a side port two cm from the end of the endotracheal tube. A left thoracotomy was done using the Bove cutting and coagulation c u rren t to provide access to the lung.h The lung was not touched during this part of the procedure, and blood loss was minimal. The pleural surface of the exposed lung was m oistened as necessary with one to two ml of normal saline at room tem perature. W hen no intrathoracic m anipulations w e re in p ro g re ss, th e th o raco to m y wound was covered with a layer of Saran W rap. The animals w ere allowed to stabilize for 40 to 60 m inutes after catheter placem ent prior to smoke exposure. All anim als w ere exposed to smoke generated from the ignition of a standard m ixture of kerosene and Douglass fir plyw ood sa w d u st. 22 T he com bustion cham ber was so placed in the inspiratory line of the ventilator circuit that smoke was delivered with each tidal respiration at a tem perature of 37 C. As developed in the initial study, sm oke exposure lasted for five m inutes at a respiratory rate of 15 breaths per m inute after which ventilation with room air resum ed.22 The respirator was occasionally adjusted to treat gross clinical deterioration usually by increasing the PEEP, and Ringer s lactate was adm inistered for the same purpose in a few animals. Occasionally an animal required small supplem ental doses of sodium pentobarbital (one to two ml, 50 mg per ml) and succinylcholine chloride (one ml, Sucostrine 20 mg per ml) in order to maintain m oderately d e e p an e sth e sia. Venous adm ix tu re I Radiometer, Copenhagen. 1 Surgi-Stat, Valley Lab, Boulder, CO. (shunt fraction) was calculated from stand a rd e q u a tio n s. P ulm onary vascular resistance (PVR) was calculated from the main pulmonary artery pressure, pulmonary wedge pressure, and the cardiac output using the equation: PVR = PAP PAW/CO. Dynamic compliance (liters per cm HaO) was calculated by dividing the airway pressure at peak inspiration minus the PEEP pressure into the tidal volume. A record of the volume of blood rem oved and the volume of fluid administered in the form of Ringer s lactate was kept. Tissue and blood specimens were collected at the en d of the baseline stabilization interval as the control samples, and at 5, 30, 60, 120, 180, and 240 m inutes follow ing smoke exposure. Physiologic data w ere acquired at the same tim e. No m ore than th re e lung specimens were taken from any one animal; pilot experiments had verified that three such lung samples could be taken w ithout changing the hem odynam ic m easurem ents or the airway pressure. Twenty-two dogs w ere used in this protocol. Because of the length of the study, the limit of three tissue specimens per animal, and the sudden death of two animals during smoke exposure, not all data points represent the same num ber of observations which vary from four to 18. Blood gas determ inations and carboxyhemoglobin levels* w ere done on blood from the pulm onary artery and aorta. Hem atocrits (arterial blood) were done on a microcapillary reader, t A clotted blood specim en (arterial) was sent to the clinical laboratory for determination of serum sodium and potassium concentrations:]: and total protein levels (Biuret method). Venous blood sufficient to provide three ml of serum was collected in a sep- * Co-oximeter, IL128. t Damen IEC. + IL Flame Photometer.
4 ENZYMATIC RESPONSE TO ACUTE SMOKE INHALATION-DOG LUNG arate tube and m aintained in an ice-slush bucket; enough blood to provide one ml of plasma was collected in a tube with disodium edetate as an anticoagulant and similarly held in an ice bath. The blood rem oved was replaced with four times its volume of Ringer s lactate. At the end of the experim ent, these tubes w ere processed in a refrigerated centrifuge at 5 C; 20 m inutes at 3500 rpm *; the serum and plasm a w ere transferred to plastic tu b es and sto red at 4 0 C.t Lung specim ens, two cm3, were secured after the atelectatic portions of lung had been expanded by tying off a portion of the lung with um bilical tape. T hree g specimens were transferred immediately to a pre-w eighed and labeled piece of aluminum foil and subm erged in liquid n itro g e n.t Periodically, as samples accum ulated, they w ere shipped in dry ice to Chicago for A CE, PLA, and angiotensin- II m easurem ents. Shipping tim e was approximately 16 hours. All specimens w ere received frozen. Activity of ACE in lung and serum was determ ined within one week of receipt in Chicago by the spectrophotom etric m ethod of Cushm an and Cheung11 using the synthetic substrate hippuryl-l-histidyl-l-leucinej Protein concentration in the lung hom ogenate was determ ined by the B iuret m ethod, and ACE activity was expressed as milliunits (mu) per g of w e t tis s u e o r p e r m g p r o te in as described previously. 3,31 Pooled normal hum an blood serum was analyzed simultaneously as an interassay standard. Lung PLA activity was m easured by the fibrin plate lysis m ethod of Astrup and A lbrechtsen2 and expressed as area (mu) lysed u n d er standard incubation conditions as described previously. 28 Plasma angiotensin II levels were m easured by a radioimmunoassay m ethod. 11 Data are presented as the mean and standard deviation of the mean. The students t-test was used to detect significant changes from baseline. Analysis of variance was used to d e te c t correlations betw een enzym atic changes following smoke exposure.34 Results P h y s io l o g ic R e s p o n s e (t a b l e I, FIGURE 1) The physiologic response of these animals to smoke exposure was consistent w ith our previous experience. 8,9,22 Qualitatively, th e physiologic p a ra m e te rs always change in the same direction; clinically, the severity of the insult varies enorm ously w ith some anim als dying during smoke exposure (not included in results) and some seem ing to recover over the course of the experiment. Most dogs dem onstrated a rapid loss of lung volum e (visible through the thoracotomy) after one or two breaths of smoke. D ense, non-segm ental atelectasis developed quickly; in general, these atelectatic areas did not change during the experim ent. T h ere was rarely any evidence for florid pulmonary edem a with fluid in the trachea. T he fem o ral a rte ry p re s s u re fell slightly from a mean control value of m m H g to th e 105 m m H g level. The pulse rate dropped transiently following smoke exposure but was otherwise maintained at 135 beats p e r m inute. Pulm o nary artery pressure rose from a mean control value of 11 mm Hg to 15 or 16 * Sorvall Superspeed RC2-B automatic refrigerated centrifuge. mm Hg. The PVR increased, and this t Harris deep freeze. increase was m aintained for th e whole $ Linde LR-40. Performed by A. Molteni, M.D., Ph.D. 1 Supplied by Sigma Chemical Corporation, St. Louis, MO. f Kit supplied by DuPont-New England Nuclear.
5 45 6 CLARK, MOLTENI, NIEMAN, BRIZIO-MOLTENI, AND SOLLIDAY TABLE I Hemodynamics and Dynamic Compliance Following Smoke Exposure* Parameter Intervai ( minutes,) (units) Baseline Femoral artery pressure (mmhg) 117 ± ± ±19.8f 95 ±12.6f 108 ±16.6f 105 ±17.7f 108 ±26.4 Pulmonary artery pressure (mmhg) 11.2 ± ± 5.6f 14.0 ± 3.8f 13.8 ± 3.2f 12.2 ± ± 4.Of 15.0 ± 5.4f Cardiac index {liters/ M2/Min) 4.05 ± ± ± ± 1.24f 3.02 ± 0.9lf 2.39 ± ± 0.79 Pulmonary vascular resistance (Resistance units) 0.10 ± ± 0.08f 0.18 ± ± 0.09f 0.16 ± 0.09f 0.18 ± 0.07f 0.19 ± 0.13f Dynamic compliance (L/cm H20) 0.054± ± O.Ollf f 0.024± ± f *N = 18 fp < 0.05 from baseline experiment. The cardiac output fell from HzO and stayed low. There was a correa mean control value of 3.35 L per min to sponding increase in the airway pressure one L per min at four hours. The cardiac from 6.8 mm Hg to 12.8 mm Hg. index (L per m2) fell from a control value The venous admixture (shunt fraction) of 4.05 to 2.33 at four hours. There was increased from a control level of 17 to a no fall in the venous P 0 2 which suggests level of 70 and returned to a value of that in spite of the drop in cardiac output about 30 p e rc e n t one hour following all tissues w ere adequately perfused. smoke exposure. At four hours following O verall, th e dynam ic com pliance fell smoke, the shunt fraction was 25 percent from a value of to L per cm (figure 1). 100 Q. 40 F i g u r e 1. V en o u s a d m ix tu re. *p < 0.05 versus baseline. Baseline 5min 30m in 60min 120mm 180mm 240mm
6 ENZYMATIC RESPONSE TO ACUTE SMOKE INHALATION-DOG LUNG The arterial ph fell from a mean control value of 7.4 to 7.3. There was only a slight rise in the PCOa following smoke exposure which was not significant and did not fluctuate throughout the experim en t. T he P a 0 2 fell quickly d u rin g smoke exposure but improved gradually during the experim ent. The hematocrit rose from a m ean of 43 p ercen t to 49 percent following smoke exposure and did not change thereafter. There was no significant change in serum concentration of sodium, potassium or protein. There was a significant rise in the carboxyhemoglobin levels with an excretion curve which was consistent with our past experience. 7 P u l m o n a r y M e t a b o l ic R e s p o n s e (t a b l e II) There was a significant decline in lung ACE, expressed as units p e r gram of organ w eight, w ithin five m inutes of sm oke exposure. The decline of this enzym e activity p e rsiste d 30 m inutes after th e injury. It show ed a fu rth e r decline at one hour and then a gradual return to values close to those m easured at baseline by four hours post smoke exposure. No differences in ACE activity w ere observed betw een specim ens collected from areas with severe atelectasis versus those collected from areas m aintaining a norm al lung appearance. T here was a significant reduction in lung p ro te in (mg p e r g of organ w et weight) by 30 m inutes following exposure to smoke (p < 0.05). Lung protein concentration was slightly lower than the values m easured at baseline after one, two, and three hours from the injury, but these differences were not significant. A m ore m arked and significant decline (p < ) was observed in the sample collected at the fourth hour. A significant decline in tissue PLA was apparent after one and three hours from the injury. The lack of significant variations in the lung protein content while ACE and PLA activity declined significantly at th ese tim e intervals indicates TABLE II Angiotensin-Converting Enzyme, Plasminogen Activator, and Plasma Angiotensin-II Following Smoke Exposure Interval (minutes) Time Baseline Lung ACE mu/gm n=18 n=7 n=7 n=12 n=10 n=7 n=4 lung wet ± ± ± ± ± ±229 weight* p < 0.05 p < 0.01 p < 0.01 p < 0.05 p < 0.05 NS Lung plasminogen n=6 n=4 n=4 n=4 n=4 activator area 0.44± ± ± lysed mm^ NS NS p < 0.05 p < 0.05 o ï o o Lung protein n=18 n=7 n=7 n=12 n=10 n=7 n=4 mg/g wet 114 ± ± ± ± ± ± ± 10 weight NS p < 0.05 NS NS NS p < 0.01 Serum ACE n=18 n=8 n=12 n=12 n=10 n=10 n=5 mu/ml 3.55± ± ± ± ± ± ± 3.85 NS NS NS NS NS NS Plasma n=18 n=8 n=12 n=12 n=10 n=ll n=5 angiotensin-ii 567 ± ± ± ± ± ± ±134 pg/ml* NS p < 0.05 p < 0.05 p < 0.05 p < 0.05 NS n = number of samples studied. NS= not significant. p = significant difference from baseline. ACE= angiotensin-converting enzyme. Significant negative correlation between lung angiotensin-converting enzyme and plasma angiotensin-ii following smoke.
7 45 8 CLARK, MOLTENI, NIEMAN, BRIZIO-MOLTENI, AND SOLLIDAY that these changes do not reflect tissue edem a b u t indicate a decreased synthesis of these substances by the endothelial cells of the lung. S y s t e m ic M e t a b o l ic R e s p o n s e (t a b l e II) In contrast to what was observed for lung ACE, th e activity of the serum enzyme rem ained unchanged during the whole experim ent. T here was no difference in ACE activity in sam ples collected from the pulm onary artery cathe te r v e rsu s th o s e c o lle c te d in th e proximal aortic arch. Plasma angiotensin-ii concentrations w ere significantly increased from the values m easured at baseline, at 30 m inu tes post th e injury. This horm one rem ained significantly elevated up to three hours, when the highest level was observed. Four hours after the injury, the angiotensin-ii concentrations w ere still higher than those m easured at baseline but the difference was no longer statistically significant. Discussion This experim ent has confirm ed the reproducibility of the effects of smoke inhalation in this m odel. 8,9 22 It is here com bined for the first tim e w ith m etabolic studies which have the potential for indicating acute lung damage in advance of histologic changes. 15,16,18,20,31 In this acute study, the activity of ACE and PLA in lung tissue was significantly reduced w ithin 30 m inutes of smoke exposure (table II). In this respect, smoke inhalation shows some similarity with chronic and acute m odels of lung injury (administration of m onocrotaline, 20 bleom y cin, 17 phorbol m yristate acetate,18) in which significant changes in the enzym a tic activ ity of th e lung paren ch y m a occurred before there was histological or ultrastructural evidence for injury. The observation that pulm onary ACE levels w ere the same in atelectatic and nonatelectatic portions of the lung suggests the chem ical injury or response is u niformly d istributed w hereas th e inhom o geneity of the appearance of the lung are the m echanical consequences of surfactant inactivation. 22 The observations in this experim ent are at variance with an earlier report of the effect of smoke inhalation on the dog lung in w hich th e lung ACE activity rose. 3 In the prior experiments, only one lung was exposed to smoke while the opposite lung was not ventilated during the eight m inute interval of smoke exposure. T he m eth o d o lo g ic d ifferences betw een the two experiments are great; at this date there is no attem pt to reconcile the results.3,7 Another study in unrestrained rats showed a significant reduction in ACE activity in the lung at one and 24 hours after smoke exposure. 4 In the rat m odel of inhalation injury, the PLA re sp o n se was diphasic w ith an increase 30 m inutes after exposure to smoke and w ith a m arked decline 24 hours post injury. 29 A lthough the rats w ere not in tu b a te d and th e fuel was household m aterial, these experim ental conditions more closely correspond to those in this report, and the results are similar with the exception that no early rise in PLA was seen (table II). T h e A C E a c tiv ity in se ru m ro se slightly b u t not significantly over the four hours of the experim ent (table II). The observation that there was no difference in ACE activity in blood from both sides of the pulmonary vascular bed suggests there is no net efflux of ACE from the lung into th e systemic circulation following this form of trauma. These results are consistent with the previous study in dogs. 3 In experim ents in rats, serum ACE was elev ated th re e hours after smoke exposure, while in our study this increase did not reach statistical significance (table II). C hronic experim ents based on other forms of traum a have also
8 ENZYMATIC RESPONSE TO ACUTE SMOKE INHALATION-DOG LUNG 459 failed to dem onstrate changes in serum ACE activity. 20,31 Angiotensin converting enzym e is p ro d u ced in m any organs besides the lung. 1 These other sources of ACE may dom inate in control of serum levels, or, alternatively, the tissue concentrations which are physiologically c o n tro llin g m ay n o t be re fle c te d in serum co n c en tra tio n s. 13 Serum ACE activity in smoke exposed humans, many of whom had therm al skin injuries, was below normal from postbum day three to seven; after this, levels rose to the normal range and becam e abnormally high by postburn day 29.19,21 In contrast to th e decline of pulm o nary ACE and PLA follow ing sm oke exposure, th e plasm a angiotensin -II levels rose significantly w ithin 30 m inu te s (ta b le II). T h is r is e w as n o t re fle c te d in a rise in system ic blood pressure. A m arked increase in plasma renin activity and angiotensin-ii concentrations w ere also observed in experim ental models of burned rats with or w ithout smoke inhalation w here lung ACE concentrations w ere also low4 as well as in humans suffering from cutaneous b u rn s. 5 The decline of lung ACE activity could be interpreted as a negative feedback in response to an increased production of angiotensin-ii reflected in its elevated plasma levels. The apparent contradiction of finding low lung ACE activity in association with high plasma angiotensin II concentrations may be explained by increased synthesis of ACE in other organs or by the presence of an alternative pathw ay for angiotensin-ii synthesis through the beta-convertingenzym e (i.e., tonin ). 6 This alternative pathway may become more active when lung ACE synthesis is dim inished. The endocrine and metabolic changes in the smoke damaged lung are difficult to study except in the laboratory because of the extraordinary num ber of overlapping variables in m ost clinical situ a tions. 9,19 It is evident from this study and previous ones that im portant metabolic events take place in the injured lung im m ediately after exposure to smoke. These events interact in a complex m etabolic response in which the renin-angiotensin-aldosterone system is significantly involved. This o b serv atio n assum es increased importance in view of recent reports suggesting a correlation betw een angiotensin-ii levels and respiratory failu re follow ing sm oke exposu re w ith im provem ent following infusion of an angiotensin analogue26,32 and the m ultifaceted effects of ACE inhibitors in congestive h e a rt failu re. 14 A cute ex p erim e n ts d o c u m e n tin g th e e x te n s iv e m etabolic changes in th e lung a few hours after injury suggest the im portance of profiling this metabolic response d u rin g a m uch larg er tim e interval. Clues to the processes by which the lung recovers functionally or becom es dam aged perm anently m ight becom e apparent in such studies. References 1. A i k e n, J. W. and V a n e, J. R. : The renin angiotensin system: Inhibition of converting enzyme in isolated tissue. Nature (London) 228:30-34, A s t r u p, T. and A l b r e c h t s e n, O. K.: Estimation of the plasminogen activator and the trypsin inhibitor in animal and human tissue. Scand. J. Clin. Lab. Invest. 9: , B r i z i o - M o l t e n i, L., P i a n o, G., R i c e, P. L., W a r p e h a, R., F r e s c o, R., S o l l i d a y, N. H., and M o l t e n i, A.: Effect of wood combustion smoke inhalation on angiotensin-i-ce in the dog. Ann. Clin. Lab. Sci. 74: , B r i z i o - M o l t e n i, L., P i a n o, G., W a r p e h a, R., S o l l i d a y, N., P a t c j a k - R a d v a r i s k a, M., and M o l t e n i, A.: Effect of different types of trauma on angiotensin-i converting enzyme (ACE) in rats. Fed. Proc. 44:915, B r i z i o - M o l t e n i, L., P i a n o, G., W a r p e h a, R. L., S o l l i d a y, N. H., e t a l. : Angiotensinconverting-enzyme-activity (A-I-CE) as m etabolic index of pulm onary damage in thermal injury with or without smoke inhalation. Ann. Clin. Lab. Sci., 1989 (in press). 6. B oucher, R., Demassieux, S., G arcia, R., and G enest, J.: Tonin-angiotensin II system. Hypertension. Genest, J., Koiw, E., and Duchel, O., eds. N ew York, M cg raw -H ill, 1977, pp
9 460 CLARK, MOLTENI, NIEMAN, BRIZIO-MOLTENI, AND SOLLIDAY 7. C l a r k, W. R.: Smoke inhalation: models for research. Respiratory Trauma, Smoke Inhalation and Burns. Haponik, E. F. and Munster, A. M., eds. New York, McGraw-Hill, 1989, in press. 8. C l a r k, W. R., N i e m a n, G. F., G o y e t t e, D., and G r y z b o s k i, D. : Effects of crystalloid on lung fluid balance after smoke inhalation. Ann. Surg. 208:56-64, C l a r k, W. R. and N i e m a n, G. F. : Smoke inhalation. Bums 14: , C l a r k, W. R., B o n a v e n t u r a, M., and M y e r s, W.: Smoke inhalation and airway management at a regional burn unit: , Part I: Diagnosis and consequences of smoke inhalation. J. Bum Care Rehabil. 10:5 2-62, C u s h m a n, D. W. and C h e u n g, H. S.: Spectrophotometric assay and properties of the angiotensin-converting enzyme of rabbit lung. Biochem. Pharmacol. 20: , D E M L I N G, R. H.: Bums (medical progress). New Engl. J. Med. 373: , D z a u, V. 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