Chest wall and lung mechanics during acute hemorrhage in anesthetized dogs

Chest Wall and Lung Mechanics During Acute Hemorrhage in Anesthetized Dogs Juraj Sprung, MD, PhD, Colin F. Mackenzie, MD, Michael D. Green, MS, Joseph O'Dwyer, MD, and George M. Barnas, PhD

Objectives: In trauma and in surgical patient s, respiratory mechanics may change because of many factors, including the hypotension induced by hemorrhage. The effects of acute hemorrhage on elastic and resistive characteristics of the respiratory system were studied. Design: Prospective study. Setting: Anesthesia research laboratory. Interventions: Acute hemorrhagic shock was induced in 24 supine anesthetized/paralyzed, mechanica!ly ventilated dogs by blood withdrawal over a 12-minute period to decrease systolic arterial pressure to 50 mrnHg; additional blood was subsequently withdrawn to maintain this pressure for 2 hoursl Total respiratory system dynamic compliance and resistance and lung and chest wall compliances and resistances were measured. Measurements and Main Results: Total respiratory system dynamic compliance :decreased from control (0.03 -+ 0.002 L/cmH20) by the first 1 0 minutes of shock (p < 0.05) and was 9.8 -+ 2% lower than control 2 hours after the induction of shock because ofdecreases in both lung (9. 6 -+ 3%) and chest wall {7.7 _+ 3%)compliances. Total

respiratory resistance increased 12.8 _+ 3% from control (3108 _+ 0.19 cmHzO/L/s) after 2 hours of shock (p < 0.05) because of an increase in chest wall resistance (21.6 -+ 8%, p < 0.05). Pulmonary resistance was not significantly increased (p > 0.05), in six control dogs, prepared similarly but not hemorrhaged, chest wall compliance and resistance did not change, but lung compliance gradually decreased by 17.8% during 150 minutes Of anesthesia/paralysis. Lung resistance increased only after 100 minutes (p < 0.05). Conclusions: (1) Hemorrhagic shock caused slight changes in the chest wall, but effects on lung mechanics were a consequence of prolonged mechanical ventilation during anesthesia/paralysis, and (2) changes in respiratory mechanics caused by hemorrhagic shock are small and, unless other deleterious factors are present, would probably have little clinical significance.

HE ANESTHESIOLOGIST frequently treats patients with massive blood loss. such as occurs after trauma or an aortic aneurysm rupture. Respiratory distress after trauma and during hemorrhage in surgical patients is frequent, and contributing factors thai need to be considered are changes in respiratory system mechanical properties (ie, compliance and resistance) caused by severe blood loss. The effects of hemorrhagic shock on respiratory system mechanics have seldom been studied and are controversial. Total respiratory system compliance has been reported to either decrease 1 or not change 2 during hemorrhagic shock, and total respiratory system resistance during such shock has been measured in just one study and seems to decrease. 2 Studies of lung compliance during hemorrhagic shock have also led to contradictory results. 3,4 and there are no such studies of lung resistance or of chest wall resistance and compliance. Pulmonary blood vessels make an appreciable contribution to the stiffness of the lung, and pulmonary venous congestion is associated with reduced compliance. 5 It should be especially noted that changes in chest wall mechanics in different conditions have not been studied, even though chest wall properties determine intrathoracic pressure for a given inflating pressure and lung condition. It was hypothesized that large decreases in circulating volume of the visceral circulation and of the large central veins may have significant effects on lungs and chest wall properties; namely, increases in lung and total respiratory system compliances. The purpose of this study was to determine the isolated

effects of hemorrhagic shock on lung and chest wall mechanics. In this study, these effects were not influenced by the variability of breathing patterns that are usually present during spontaneous breathing in shock. The authors therefore determined lung, chest wall. and total respiratory system compliances and resistances at normal respiratory rate and tidal volume in supine anesthetized/paralyzed, mechanically ventilated dogs exposed to hemorrhage (series 1). Results were compared with control dogs, treated similarly, but not hemorrhaged (series 2).

T

From the Departments of Anesthesiology, Cleveland Clinic Foundation. Cleveland. OH, and University of Maryland. Baltimore. MD. Address reprints requests ro Juraj Sprung, MD PhD, The Cleveland Clinic Foundation. Department of General Anesthesiology, E-31, 9500 Euclid Ave. Cleveland, 0H44195-9247. Copyright © 1997 by W.B. Saunders Company 1053-0770/97/1105-001453.00/0

608

Copyright© 1997by W.B. Saunders Company KEY WORDS: hemorrhage, shock, respiratory mechanics, compliance, resistance, respiratory system, chest wall, lung

MATERIALS AND METHODS The study was approved by the Institutional Animal Review Board, and the care and handling of the animals were in accord with National Institutes of Health guidelines. Animal Preparation and Measurements Series 1. Twenty-four beagles* (12.3 z 0.3 kg) were anesthetized with pentobarbital sodium (20 mg/kg intravenously), followed by continuous infusion of thiamylal (3 mg/kg/h). Pancuronium (0.08 mg/kg/h) was also infused to maintain complete muscle paralysis. Dogs' tracheas were intubated with an 8.0-mm ID cuffed endotracheal tube (Hi-Lo Jet, Mallinckrodt. Glens Falls. NY) and mechanically ventilated in supine posture with air at 12 breaths/rain (Engstrom ER 312. Medical AB, Stockholm. Swedem at a tidal volume (250 to 400 mLj sufficient to keep PaCO2 at 36 z 1 mmHg. Systolic and mean (MAP) arterial blood pressures were monitored through an indwelling catheter placed in the femoral artery Electronics for Medicine, M2103B. White Plains. NY). and heart rate by means of electrocardiograph ~Electronics for Medicine. Mll01C). Arterial oxyhemoglobin saturation (SaO2) was continuously monitored by a pulse oximeter (Nellcor. N-100. Nellcor Inc. Hayward. CA) attached to the tongue. A thermistor-tipped flow-directed catheter was floated through the femo-

*Same beagles reported in series 1 were used in another study, but the current results describing respiratory system mechanics in hemorrhagic shock have not been reported

Journal of Cardiothoracic and Vascular Anesthesia,

Vol 11, No 5 (August), 1997:pp 608-612

HEMORRHAGIC SHOCK A N D RESPIRATORY MECHANICS

ral vein into a pulmonary artery to measure pulmonary artery pressure, pulmonary capillary wedge pressure, and cardiac output by thermodilution (Baxter Edwards, Sat-2TM oximetric computer, Santa Ana, CA) and to sample mixed venous blood. Body temperature was also monitored by a pulmonary artery thermistor, and was kept between 36.5°C and 37.5°C with a heating blanket connected to a heat pump (T-Pump, Gaymar, Orchard Park, NY) and with a heat lamp. An additional arterial cannula was introduced into the femoral artery on the opposite side, and was used to withdraw the blood during the hemorrhage period. Blood gases were determined by a pH/blood gas analyzer (Instrumentation Laboratory Inc, Model IL 713, Lexington, MA) with temperature correction, and oxygen content in the blood was also measured (OSM2 Radiometer, Copenhagen, Denmark). Airway flow was measured with a pneumotachograph (Fleisch #1) attached to the end of the endotracheal tube and a differential pressure transducer (Celesco LCVR, Canoga Park, CA). Airway (Paw) and esophageal pressures (Pes) were measured with Gould Statham transducers (Oxnard, CA). Paw was measured through a sampling port in the endotracheal tube that opens at its tip. Pes was measured with a polyethylene catheter attached to a 10-cm thin-walled latex balloon (inflated with 0.5 mL) placed in the caudal third of the esophagus. The accuracy of the esophageal balloon-pressure transducer system was verified with a method modified from Baydur et al6 by comparing changes in Pes and Paw during abdomen compression against the closed airway. With optimum placement, the changes were equal and in phase. Series 2. Six additional dogs (10.2 _+ 0.3 kg) were similarly anesthetized, paralyzed, and ventilated as in series 1. In these dogs SaO2 (always between 95% and 97%), end-tidal CO2 (Hewlett Packard M14360 [Boblingen, Germany], maintained between 30 and 35 mmHg), and electrocardiogram were monitored and Paw, Pes, and airway flow were measured.

Protocol Series 1. Baseline measurements were performed before hemorrhage, approximately 30 minutes after the dog was connected to the mechanical ventilator. All dogs were then subjected to the same blood withdrawal protocol by aspiration of blood through the catheter placed in the femoral artery until the systolic blood pressure was reduced to 50 mmHg (over 10 to 15 minutes). The second set of measurements was performed about 10 to 15 minutes afterwards. Over the next 2-hour period, the dogs were kept hypotensive by withdrawal of additional blood to keep systolic blood pressure at the same low level. At the end of the 2-hour period, a third set of measurements was taken. In five of the dogs, respiratory system mechanics over the 10- to 15-minute period during hemorrhage were measured at 1-minute intervals. Series 2. Beginning approximately 30 minutes after the dog was placed on the mechanical ventilator, respiratory system mechanics were measured at 20-minute intervals up to 140 minutes, and once more at 150 minutes.

Data Analysis Total respiratory system, lung and chest wall resistances (Rrs, R1, Rcw, respectively), and dynamic compliances (Crs, C1, Ccw, respectively) were calculated from pressure and flow measurements from three respiratory cycles, analyzed with multiple linear regression by computer. 7,s All respiratory mechanics variables were expressed as a percent change from control. One-way analysis of variance for repeated measures and Fisher Paired Least Significance Difference Tests were used to judge differences among measurement periods for each variable; p < 0.05 was accepted as a significant level; values given are mean +_ SE.

609

RESULTS

Series 1 Cardiovascular parameters and blood gases. Hemorrhagic shock was acutely induced over 10 to 15 minutes. To achieve and maintain systolic blood pressure at 50 mmHg, on average, 617 -+ 20 mL of blood had to be withdrawn over 2 hours, representing 63 _+ 2% of the estimated dog's total blood volume. Table 1 shows cardiorespiratory variables before, 10 to 15 minutes after the shock was established (10-rain shock), and after 2 hours of hemorrhagic shock (2-hr shock). Cardiac output was reduced 68% at 10-rain shock. The percentage of pulmonary shunt (Qs/Qt%) increased by 135% at 2-hr shock. PaO2 decreased to 88 mmHg at 2-hr shock (p < 0.05). Pulmonary vascular resistance doubled at 10-min shock and remained unchanged after 2 hours of shock. At 2-hr shock, all dogs developed metabolic acidosis. Respiratory system mechanics. Average resistances of total respiratory system, chest wall, and lungs before hemorrhage were 3.08 -+ 0.19, 1.25 + 0.12 and 1.83 + 0.13 cmH20/L/s, respectively. Average dynamic compliances of total respiratory system, chest wall, and lungs before hemorrhage were 0.030 _+ 0.002, 0.090 -+ 0.007 and 0.050 _+ 0.004 L/cmH20, respectively (n = 24). Figure 1 shows average compliances and resistances in five dogs during the initial hemorrhage. There were no changes in chest wall and lung mechanics from the baseline during the initial 12-minute period of hemorrhage (p > 0.05). Figure 2 shows relative changes in compliances (left panel) and resistances (right panel) at 10-min shock and at 2-hr shock. Total respiratory system compliance decreased 9.8 + 2% at 10-min shock (p < 0.05) and remained low at 2-hr shock. This change in compliance at 2-hr shock was the result of concurrent decreases in both the chest wall (7.7 + 3%) and lung (9.6 +- 3%) components (p < 0.05). Respiratory system resistance increased 12.8 _+ 3% at 2-hr shock (p < 0.05) because of an increase in chest wall resistance (p < 0.05). Series 2 Respiratory system mechanics. Figure 3 shows relative changes in compliances (left panel) and resistances (right panel) Table 1. Cardiorespiratory Parameters Before Shock, at lO-Minutes' Shock, and at 2-Hour Shock Baseline MAP (mmHg)

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610

SPRUNG ET AL

ment of chest wall properties would be difficult in nonrelaxed and spontaneously breathing animals. Thus, although clinical conditions may often differ in some ways from those in the current study on mechanically ventilated and anesthetized dogs, the results will aid in interpretation of such future measurements in spontaneously breathing patients. That is, this study provides fundamental information necessary for understanding the isolated effects of hemorrhage on chest wall and lung mechanics. Although controversial effects of hemolThage on lung mechanics were reported, vSJH3 nothing was known about how hemorrhage affects chest wall mechanics. An answer to this question may be important to the vascular anesthesiologist who manages massive blood loss such as occurs during a ruptured aortic aneurysm. As measured by computed tomography, acute hypovolemia results in a rapid decrease in lung density, which was attributed to the loss of the blood from the lung. u Others have postulated that a decrease in lung blood volume may increase lung compliance, presumably through reducing the splinting effect of the pulmonary vasculature. 5,12J3 It may also be expected that loss of blood from the large systemic veins and shock-induced reflex distribution of blood within the chest wall may have significant effects on chest wall mechanics. However, in this

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Elastance and resistance of the respiratory system depend importantly on respiratory frequency, tidal volume, waveform, and lung volume. 9J° Therefore, measurements of lung mechanics in patients during hemorrhage, or in a spontaneously breathing animal model, would be extremely difficult to interpret if the effects of hemorrhage alone were not known, because patients and animals will vary widely in their breathing patterns and functional residual capacities (FRC). In addition, measure-

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HEMORRHAGIC SHOCK AND RESPIRATORY MECHANICS

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study, during the 12 minutes of hemorrhage, there was no effect of blood loss on lung or chest wall mechanics. This also suggests that there was no immediate decrease in FRC, because a previous study has shown that the measured compliances should decrease and lung resistance should increase with even a small decrease in FRC, 9 About 20 minutes after the beginning of hemorrhage, decreases in lung compliance comparable to those seen in control dogs during monotonous mechanical ventilation (no sighs) for 20 minutes were found. Therefore, it is likely that small changes in lung mechanics seen during the shock period were not the result of hemorrhage, but rather the normal effects of prolonged mechanical ventilation. These effects are probably the result of gradually developing atelectasis 14 or changes in surface tension. ls,16 The increased shunt fraction by 2-hr shock (Table 1) probably also reflects the reduced lung volume and the atelectasis. In addition, it appears that when metabolic acidosis is present during hemorrhagic shock, as was the case in these dogs (Table 1), the amount of pulmonary shunt may be exaggerated, 17 The mechanisms causing the small alterations in chest wall mechanics are difficult to identify because the chest wall is a complex system including the rib cage, diaphragm, abdominal

contents, and abdominal wall, 1° and little is known about how changes in the chest wall tissues affect its mechanical properties. As mentioned earlier, it has been assumed, but not tested, that blood loss from the lungs should directly increase lung compliance by reducing the splinting effect of pulmonary vasculature, t3 and an analogous change could be postulated for the chest wall. However, such a simple mechanism did not occur because hemorrhagic hypovolemia in this study resulted in a decrease in chest wall compliance. The slight decrease in chest wall compliance and increase in resistance that were observed did not occur until about 12 minutes after the blood withdrawal period. It can only be speculated that redistribution of blood within the chest wall or regional vasoconstriction may change its global mechanical properties. There are few available comparisons to other studies, and of those available, each contains differences in protocol compared with the current study. In addition, no study separated lung and chest wall properties, and only one measured resistance. 2Fulton and Fischer1found a 20% drop in static total respiratory system compliance in mechanically ventilated dogs after 2.5 hours of acute bleeding, roughly similar to the current study. Martins et al2 found no change in static respiratory system compliance in mechanically ventilated anesthetized/paralyzed guinea pigs after a hemorrhage of 20 mL/kg over 10 minutes, which is consistent with this study's finding in Fig 1. They also found a decrease in respiratory system resistance, Rrsmax, measured by the flow-interruption technique. Because this type of measurement is based on a complex model and corresponds to an unknown combination of frequencies and tidal volumes, comparisons with this study's measurements made under a physiological breathing pattern are not clear. Kakvan et al4 found that in spontaneously breathing, anesthetized dogs, dynamic lung compliance decreased approximately 37%, 54%, and 59% after 30, 60, and 120 minutes, respectively, of hemorrhagic shock (MAP = 30 mmHg). The variability inherent in measurements of compliance made during spontaneous breathing makes comparisons with this study difficult, For example, respiratory frequency doubled during the shock: this alone would tend to decrease lung complianceJ 8 Buckberg and DowelP found no change in static compliance in lungs excised from baboons immediately after 2 hours of hemorrhagic shock unless the animals were killed by aortic occlusion, which may induce lung congestion. This suggests that hemorrhage decreases compliance only if lung congestion is present, which is not expected in hemorrhagic shock} 9,a° In conclusion, the mechanical properties of the respiratory system are only slightly changed during hemorrhagic shock in dogs. Initial blood loss does not affect respiratory system compliance and resistance, whereas subsequent shock induced only moderate changes. The changes in the lungs are consistent with the effect of prolonged mechanical ventilation, but the effects on the chest wall cannot be explained because little is known about how chest wall properties are affected by changes in its tissue constituents. Although the changes found in respiratory system mechanics have statistical significance, it is unlikely that they are large enough to be clinically important during acute hemorrhage in otherwise healthy patients.

612

SPRUNG ET AL

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11. Hendlund LW, Jones DR Effman EL, et al: A computed tomographic study of the dog lung during hemorrhagic shock and after resuscitation. Invest Radiol 16:466-472, 1981 12. Abel FL, Waldhansen JA, Daly WJ: Pulmonary blood volume in hemorrhagic shock in the dog and primate. Am J Physiol 213:10721079, 1967 13. Cahill JM, Byrne JS: Ventilatory mechanics in hypovolemic shock. J Appl Physiol 19:679-682, 1964 14. Mead J, Collier C: Relation of volume history of lung to respiratory mechanics in anesthetized dogs. J Appl Physiol 14:669-678, 1959 15. Huang YC, Weinmann GG, Mitzner W: Effect of tidal volume and frequency on the temporal fall in lung compliance. J Appl Physiol 65:2040-2045, 1988 16. Oyarun MJ, Clements JA: Ventilatory and cholinergic control of pulmonary surfactant in the rabbit. J Appl Physio143:39-45, 1977 17. Wahrenbrock EA, Carrico CJ, Amundsen DA, et al: Increased atelectatic pulmonary shunt during hemorrhagic shock in dogs. J Appl Physio129:615-621, 1970 18. Barnas GM, Stamenovic D, Lutchen KR: Lung and chest wall impedances in dog: Effects of frequency and tidal volume. J Appl Physio172:87-93, 1992 19. Magilligan DJ, Oleksyn TW, Yu PN: Pulmonary blood volume and pulmonary extravascular water in hemorrhagic shock. Surg Forum 22:32-33, 1971 20. Gump FE, Mashima Y, Ferenczy A: Pre- and postmortem studies of lung fluids and electrolytes. J Trauma 11:474-481, 1971