Original Article

Inhaled Nitric Oxide for the Adult Respiratory Distress Syndrome

Rolf Rossaint, Konrad J. Falke, Frank Lopez, Klaus Slama, Ulrich Pison, and Warren M. Zapol

N Engl J Med 1993; 328:399-405February 11, 1993

Abstract

Background

The adult respiratory distress syndrome is characterized by pulmonary hypertension and right-to-left shunting of venous blood. We investigated whether inhaling nitric oxide gas would cause selective vasodilation of ventilated lung regions, thereby reducing pulmonary hypertension and improving gas exchange.

Full Text of Background...

Methods

Nine of 10 consecutive patients with severe adult respiratory distress syndrome inhaled nitric oxide in two concentrations for 40 minutes each. Hemodynamic variables, gas exchange, and ventilation-perfusion distributions were measured by means of multiple inert-gas-elimination techniques during nitric oxide inhalation; the results were compared with those obtained during intravenous infusion of prostacyclin. Seven patients were treated with continuous inhalation of nitric oxide in a concentration of 5 to 20 parts per million (ppm) for 3 to 53 days.

Full Text of Methods...

Results

Inhalation of nitric oxide in a concentration of 18 ppm reduced the mean (±SE) pulmonary-artery pressure from 37 ±3 mm Hg to 30 ±2 mm Hg (P = 0.008) and decreased intrapulmonary shunting from 36 ±5 percent to 31 ±5 percent (P = 0.028). The ratio of the partial pressure of arterial oxygen to the fraction of inspired oxygen (PaO₂/FiO₂), an index of the efficiency of arterial oxygenation, increased during nitric oxide administration from 152 ±15 mm Hg to 199 ±23 mm Hg (P = 0.008), although the mean arterial pressure and cardiac output were unchanged. Infusion of prostacyclin reduced pulmonary-artery pressure but increased intrapulmonary shunting and reduced the PaO₂/FiO₂ and systemic arterial pressure. Continuous nitric oxide inhalation consistently lowered the pulmonary-artery pressure and augmented the PaO₂/FiO₂ for 3 to 53 days.

Full Text of Results...

Conclusions

Inhalation of nitric oxide by patients with severe adult respiratory distress syndrome reduces the pulmonary-artery pressure and increases arterial oxygenation by improving the matching of ventilation with perfusion, without producing systemic vasodilation. Randomized, blinded trials will be required to determine whether inhaled nitric oxide will improve outcome.

Full Text of Discussion...

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Media in This Article

Figure 1Mean Pulmonary-Artery Pressure (PAP), Arterial Oxygenation Efficiency (PaO₂/FiO₂), and Intrapulmonary Shunting (Q_S/Q_T) in Nine Patients with ARDS during Inhalation of Nitric Oxide.

Figure 2Hemodynamic Function and Gas Exchange before, during, and after Brief Interruptions (Arrows) of Nitric Oxide Inhalation (Bars) during the First Six Days of Treatment in Seven Patients with ARDS.

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Article

The adult respiratory distress syndrome (ARDS) is characterized by intrapulmonary shunting that results in arterial hypoxemia,1 and by acute pulmonary arterial hypertension due to vasoconstriction and widespread occlusion of the pulmonary microvasculature2,3. Pulmonary arterial hypertension contributes to pulmonary edema4 and can cause right ventricular dysfunction5. Reducing the abnormally elevated pulmonary vascular resistance by infusing vasodilators lowers pulmonary-artery pressure as well as the effective pulmonary-capillary pressure,6-9 thereby improving right ventricular function5,10 and possibly promoting the resolution of pulmonary edema6. However, the dose of a vasodilator agent is limited by concomitant dilation of the systemic vasculature, leading to systemic arterial hypotension, right ventricular ischemia, and consequent heart failure7-9,11. In addition, intravenously infused vasodilators produce diffuse dilation of the pulmonary vasculature that increases blood flow to areas of intrapulmonary shunting. This mismatch between ventilation and perfusion usually further reduces the already compromised partial pressure of arterial oxygen (PaO₂)7-9,12,13.

Inhalation of nitric oxide gas in a concentration of 5 to 80 parts per million (ppm) dilated the pulmonary circulation of conscious, spontaneously breathing lambs in which acute vasoconstriction had been induced either by giving them an infusion of a stable thromboxane-endoperoxide analogue or by having them breathe a hypoxic gas mixture14. In patients with primary pulmonary hypertension, inhaling nitric oxide in a concentration of 40 ppm produced pulmonary vasodilation equivalent to that produced by prostacyclin15. Nitric oxide is synthesized by the vascular endothelium from the terminal guanidino nitrogen atom of the amino acid L-arginine16 and acts as a natural local vasodilator. It relaxes muscular arteries and veins by activating guanylate cyclase and increasing cyclic guanosine 3',5'-monophosphate17,18. Since nitric oxide binds rapidly to hemoglobin with a high affinity and is thereby inactivated,19-21 inhalation of the gas cannot dilate the systemic circulation. Thus, the vasodilatory effect of nitric oxide should be limited to the ventilated regions of the lung when it is given by inhalation. In contrast to intravenously administered vasodilators, inhaled nitric oxide should selectively improve the perfusion of ventilated regions, thus reducing intrapulmonary shunting and improving arterial oxygenation.

To test this hypothesis we first compared the effects of inhaled nitric oxide with those of an intravenously infused vasodilator, prostacyclin. We then treated the patients with inhalation of nitric oxide for up to 53 days.

Methods

This investigation was approved by the institutional ethics committee. Informed consent was obtained from each patient's family.

Patients

We studied 10 consecutive patients without a history of previous lung disease who had severe ARDS when referred to our hospital. Their clinical characteristics recorded immediately before inhalation of nitric oxide are shown in Table 1Table 1Clinical Characteristics of the Patients., including their ARDS-severity scores determined according to the technique of Murray et al.22 (range, 3.2 to 4). The pulmonary occlusion pressure (pulmonary-capillary wedge pressure) ranged from 8 to 18 mm Hg. Acute renal failure requiring hemodialysis or hemofiltration was present in six patients,23 and liver dysfunction in five23. All patients received mechanical ventilation in the pressure-controlled mode with the application of positive end-expiratory pressure (10 to 15 cm of water) (Servo 900C ventilator, Siemens Elema, Lund, Sweden). The inhalation of nitric oxide was begun 3 to 10 days after admission and before any signs of recovery. At that time, the patients had undergone ventilation for 14 to 41 days, and six of them were treated with venovenous extracorporeal membrane oxygenation at flow rates of 2 to 3 liters per minute as previously described,24 because of a persistent pulmonary venous admixture (Q_VA/Q_T) of more than 45 percent that was associated with severe arterial hypoxemia.

The patients were sedated and relaxed. The use of cardiotonic or vasoactive drugs was avoided during studies of gas exchange.

Measurements

Routine clinical monitoring of the patients included a thermodilution pulmonary-artery catheter and a thermistor femoral-artery catheter (Baxter Healthcare, Irvine, Calif.). The mean systemic arterial pressure, pulmonary arterial pressure, right atrial pressure, and pulmonary occlusion pressure were measured with disposable transducers (Abbott Laboratories, Chicago) and a monitoring system (Hewlett-Packard Model 66 S, Boblingen, Germany). The zero reference level for the supine position was the midaxilla; the vascular pressures were the average of values taken at end-expiration from three successive respiratory cycles. Cardiac output was measured with thermodilution techniques and expressed as the mean of the values recorded after each of four injections of saline (10 ml at 1 degrees to 5 °C)25. The systemic and pulmonary vascular resistances were calculated according to standard formulas. Measurements of extravascular lung water (Lung Water Computer 9310, Edwards Laboratories, Irvine, Calif.) were obtained daily with a double-indicator dilution technique26.

Arterial and mixed-venous-blood concentrations were measured with standard blood-gas electrodes (ABL 300, Radiometer, Copenhagen, Denmark), and the total hemoglobin concentration, hemoglobin oxygen saturation, and methemoglobin levels with spectrophotometry (OSM 3 Hemoximeter, Radiometer). Samples of inspired gas were obtained from the inspiratory tubing; samples of expired gas were drawn into a heated flow-through mixing box. The ratio of the partial pressure of arterial oxygen to the fraction of inspired oxygen (PaO₂/FiO₂) was used as an index of arterial oxygenation because inspiratory admixture of nitrogen, the carrier gas for nitric oxide, reduced the concentration of inspired oxygen. Concentrations of arterial, mixed venous, and capillary oxygen were calculated, and the Q_VA/Q_T was derived from the standard shunt equation, with the concentration of oxygen in the alveolar gas (FiO₂) set at 0.90 to 0.98.

We compared the effects of inhaled nitric oxide with those of infused prostacyclin, using the multiple inert-gas-elimination technique27,28. This technique characterizes pulmonary gas exchange by analyzing the exchange of inert gases across the blood-gas barrier. In brief, a solution of 5 percent glucose in water was equilibrated with a mixture of six inert gases (sulfur hexafluoride, ethane, cyclopropane, halothane, diethyl ether, and acetone) and infused continuously into a peripheral vein, beginning 30 minutes before blood sampling. Samples of arterial and mixed venous blood and mixed expired gas were collected during several respiratory cycles and analyzed by gas chromatography (Sichromat 1, Siemens, Cologne, Germany). Retention (the ratio of the concentration in arterial blood to that in mixed venous blood) and excretion (the ratio of the concentration in expired gas to that in mixed venous blood) were calculated for each gas. Ventilation-perfusion (V_A/Q) distributions were estimated from the retention-partition and excretion-partition coefficients by means of a computer program with a 50-compartment model of ventilation and blood flow, to estimate ventilation-perfusion ratios in the lungs27. The extent of intrapulmonary shunting (Q_S/Q_T) was derived from the sulfur hexafluoride measurements and was defined as the fraction of total blood flow perfusing unventilated lung units (V_A/Q ratio <0.005). Low V_A/Q, which indicates poor ventilation, was defined as the fraction of total blood flow perfusing areas with V_A/Q ratios of 0.005 to 0.10 (normal V_A/Q ratios range from 0.1 to 10). The fraction of gas entering unperfused lung units was defined as the inert-gas dead space. Log_SDQ, an index of V_A/Q inequality, was defined as the square root of the value for the second moment of the blood-flow distribution.

Administration of Nitric Oxide

During the inspiratory cycle, the nebulizer of the ventilator released nitric oxide from a tank of nitrogen with a nitric oxide concentration of 400 or 800 ppm (AGA, Bottrop, Germany). The resulting bolus of nitric oxide in nitrogen represented 2 to 4 percent of inspired volume. The level of nitric oxide was measured by chemiluminescence (CLD 700 AL, Tecan AG, Munich, Germany).

Short-Term Inhalation of Nitric Oxide as Compared with Prostacyclin Infusion

Nine consecutive patients (Table 1, Patients 1 through 9) inhaled nitric oxide in a concentration of 18 ppm and then in a concentration of 36 ppm, before or after they received an intravenous infusion of prostacyclin at a rate of 4 ng per kilogram of body weight per minute (Wellcome Laboratories, London). Systemic and pulmonary hemodynamic variables and V_A/Q distributions were measured before, during, and after each vasodilator was administered. To exclude the effects of sequential administration of vasodilators, the sequence of administration was randomized: in five patients the sequence was base-line study I, nitric oxide at 18 ppm, nitric oxide at 36 ppm, base-line study II, prostacyclin, and base-line study III; in four other patients, the sequence was base-line study I, prostacyclin, base-line study II, nitric oxide at 18 ppm, nitric oxide at 36 ppm, and base-line study III. Each step in each sequence lasted approximately 40 minutes, and measurements were performed toward the end of each period, when hemodynamic function was stable.

Prolonged Inhalation of Nitric Oxide

Seven patients (Patients 4 through 10) were treated with prolonged inhalation of nitric oxide at 5 to 20 ppm, begun when the PaO₂/FiO₂ was below 150 mm Hg. The administration of nitric oxide was discontinued daily for 30 minutes, with the ventilator settings kept constant and the FiO₂ set at 0.90 to 0.98, to determine the effect of withdrawal and resumption of treatment on hemodynamic function, blood gas pressures, and Q_VA/Q_T. Extravascular lung water was measured daily if the arterial thermistor remained in place or until the measurements decreased to levels slightly above normal (5.7 ±1.2 g per kilogram)26. Treatment with nitric oxide was terminated after weaning from extracorporeal membrane oxygenation was successful and when the PaO₂/FiO₂ rose above 250 mm Hg during daily tests without the inhalation of nitric oxide.

Statistical Analysis

Values are expressed as means ±SE. Treatment effects are reported as the difference between the mean of the base-line values (before and after treatment) and the value during the intervention. If a difference between base-line values was significant, the value recorded during the intervention was compared separately with the base-line values determined before and after the intervention. In addition, the effect of nitric oxide at 18 ppm was compared with its effect at 36 ppm, and the effects of both concentrations of nitric oxide were compared with the effects of prostacyclin infusion.

The Wilcoxon test for paired samples was used to compare values recorded during treatment with those recorded at base line for a single treatment and to compare differences between treatment values and base-line values for the two treatments29. All tests of significance were two-tailed. A P value below 0.05 was assumed to indicate significance. No adjustment was made for comparisons at multiple time points.

Results

Nitric Oxide as Compared with Prostacyclin

The inhalation of nitric oxide usually produced a prompt reduction in the pulmonary-artery pressure and a concomitant increase in the PaO₂/FiO₂ (Figure 1Figure 1Mean Pulmonary-Artery Pressure (PAP), Arterial Oxygenation Efficiency (PaO₂/FiO₂), and Intrapulmonary Shunting (Q_S/Q_T) in Nine Patients with ARDS during Inhalation of Nitric Oxide.). The hemodynamic responses to inhalation of nitric oxide and infusion of prostacyclin are summarized in Table 2Table 2Hemodynamic Responses of Nine Patients to Short-Term Nitric Oxide Inhalation and Prostacyclin Infusion (4 ng per Kilogram per Minute).. During inhalation of nitric oxide at 18 ppm, pulmonary-artery pressure decreased by 6 ±1 mm Hg from base line (P = 0.008). There was no significant difference between the effects of the two concentrations of nitric oxide on pulmonary-artery pressure. Intravenous prostacyclin infusions reduced the pulmonary-artery pressure by 6 ±2 mm Hg (P = 0.011). The mean systemic arterial pressure remained constant during inhalation of nitric oxide but decreased by 6 ±2 mm Hg (P = 0.018) during infusion of prostacyclin. Cardiac output remained unchanged from base-line values during inhalation of nitric oxide but increased by 1.3 ±0.4 liters per minute when prostacyclin was infused (P = 0.015). Pulmonary vascular resistance decreased during inhalation of nitric oxide at 18 ppm, by 71 ±17 dyn • sec • cm^-5 (P = 0.008), and did not change further during the inhalation of the gas at 36 ppm; during prostacyclin infusion, it decreased by 102 ±30 dyn • sec • cm^-5 (P = 0.011). Systemic vascular resistance was not altered by inhalation of nitric oxide but decreased during prostacyclin infusion by 152 ±34 dyn • sec • cm^-5 (P = 0.002). The heart rate, central venous pressure, and pulmonary occlusion pressure did not change during the administration of either vasodilator. The values for all variables shown in Table 2 returned to base line after the end of treatment with each vasodilator, with the exception of the pulmonary vascular resistance after cessation of nitric oxide treatment.

Data on pulmonary gas exchange are shown in Figure 1 and Table 3Table 3Data on Blood Gas Exchange and Inert-Gas Elimination in Nine Patients during Short-Term Nitric Oxide Inhalation and Prostacyclin Infusion (4 ng per Kilogram per Minute).. With inhalation of nitric oxide at 18 ppm, the PaO₂/FiO₂ increased by 51 ±11 mm Hg (P = 0.008) and the Q_VA/Q_T decreased by 6 ±1 percent (P = 0.008); nitric oxide at 36 ppm did not cause further changes in these variables. In contrast to inhalation of nitric oxide, prostacyclin infusion decreased the PaO₂/FiO₂ by 26 ±7 mm Hg (P = 0.005) and increased the Q_VA/Q_T by 8 ±2 percent (P = 0.011). The partial pressure of arterial carbon dioxide decreased by 2 ±1 mm Hg only during the inhalation of nitric oxide at 36 ppm (P = 0.038). The partial pressure of oxygen in mixed venous blood increased by 2 ±0.3 mm Hg only during the inhalation of nitric oxide at 18 ppm (P = 0.008). Arterial pH values did not differ throughout the study.

The results of the inert-gas studies are shown in Table 3. Inhalation of nitric oxide at 18 ppm decreased the Q_S/Q_T by 3 ±1 percent (P = 0.028); there was no further change during inhalation of 36 ppm. The fraction of blood flowing to lung regions with normal V_A/Q ratios increased by 5 ±1 percent (P = 0.011) during inhalation of nitric oxide at 18 ppm and was unchanged during inhalation of the gas at 36 ppm. A prostacyclin infusion, however, had the opposite effect on both measurements. The Q_S/Q_T was increased by 9 ±2 percent (P = 0.012), and blood flow to lung regions with normal V_A/Q ratios decreased by 9 ±2 percent (P = 0.012). Inhalation of nitric oxide at 18 ppm was associated with a trend of decreasing log_SDQ (P = 0.051) that became significant during the inhalation of 36 ppm (P = 0.011). Infusion of prostacyclin was associated with a trend of increasing log_SDQ, which rose by 0.1 ±0.01; this trend was not significant (P = 0.093). Blood flow to lung regions with low V_A/Q ratios was reduced by 2 ±1 percent only during the inhalation of nitric oxide at 36 ppm (P = 0.028). The inert-gas dead space did not change throughout the entire study. The delivered tidal volume at constant inspiratory and end-expiratory pressure did not change during inhalation of nitric oxide or infusion of prostacyclin.

Prolonged Inhalation of Nitric Oxide

Nitric oxide (5 to 20 ppm) was inhaled by seven patients for 3 to 53 days (Table 1 and Figure 2Figure 2Hemodynamic Function and Gas Exchange before, during, and after Brief Interruptions (Arrows) of Nitric Oxide Inhalation (Bars) during the First Six Days of Treatment in Seven Patients with ARDS.). The mean ARDS-severity score of these seven patients just before long-term inhalation of nitric oxide was 3.6 (range, 2.75 to 4)22. During brief daily interruptions of nitric oxide treatment, pulmonary-artery pressure and Q_VA/Q_T were consistently increased and the PaO₂/FiO₂ was consistently decreased. Representative changes during the first six days of nitric oxide treatment are shown in Figure 2. Values for extravascular lung water showed a declining trend (P>0.05). Methemoglobin levels, measured daily, always remained below 1.3 percent.

Discussion

In 1987, nitric oxide was reported to be an important endothelium-derived relaxing factor30,31. Although inhaling high concentrations of nitric oxide can be lethal because it causes severe acute pulmonary edema and methemoglobinemia,32 there is little evidence of toxicity when the concentration is below 50 ppm. Animals have breathed the gas in concentrations of 10 to 40 ppm for six days to six months without evidence of such toxicity33,34. The Occupational Safety and Health Administration has set the eight-hour maximal working-exposure level for nitric oxide at 25 ppm35.

Frostell et al. demonstrated that inhaling nitric oxide in a concentration of 5 to 80 ppm reversed hypoxic pulmonary vasoconstriction without affecting systemic hemodynamic function in conscious sheep14 and volunteers with induced hypoxia36. Fratacci et al. reported that inhalation of nitric oxide prevented thromboxane-induced pulmonary hypertension during the heparin-protamine reaction in lambs37. Recently, Dupuy et al. demonstrated in anesthetized guinea pigs that inhaling nitric oxide at 5 to 300 ppm reversed methacholine-induced bronchoconstriction38.

In our patients with ARDS, inhaled nitric oxide decreased intrapulmonary shunting and improved arterial oxygenation while reducing the pulmonary-artery pressure. Our inert-gas analyses revealed that this beneficial effect was due to a redistribution of pulmonary blood flow away from nonventilated regions of the lungs and toward ventilated regions, thereby improving the matching of ventilation and perfusion. Inhaled nitric oxide can decrease the regional pulmonary vascular resistance of ventilated lung areas, decreasing intrapulmonary shunting and selectively reducing the pulmonary-artery pressure without causing systemic vasodilation.

An increased pulmonary-artery pressure due to pulmonary vasoconstriction and vascular obstruction is a hallmark of severe ARDS2,9. Pulmonary-artery hypertension promotes the accumulation of extravascular lung water4 by increasing the microvascular filtration pressure39. Pulmonary hypertension can cause right ventricular dysfunction, reducing the right ventricular ejection fraction and cardiac output5. Intravenous infusion of nitroprusside reduces pulmonary-artery pressure and the accumulation of extravascular lung water in experimental pulmonary edema6,40. Reducing the pulmonary-artery pressure may improve right-sided cardiac performance5,10.

The clinical use of intravenously infused vasodilators to treat ARDS is limited because vasodilators reduce systemic arterial pressure. Intravenously infused vasodilators can markedly increase intrapulmonary shunting, leading to a severely reduced PaO₂,7-9,12,13 as we demonstrated with prostacyclin (Table 3).

We observed a consistent reduction in pulmonary hypertension and improvement in arterial oxygenation in patients with severe ARDS who inhaled low concentrations of nitric oxide. This is both surprising and therapeutically important. Although inhaling nitric oxide did not reduce the pulmonary-artery pressure to a normal level, probably because vascular occlusion or compression had occurred, it did lower pulmonary-artery pressure to the level achieved by infusing prostacyclin, and to the extent achieved by infusing nitroprusside in other patients with ARDS9. Unlike intravenously infused vasodilators, inhaled nitric oxide does not reduce systemic arterial pressure. We believe that this is because inhalation allowed nitric oxide to target and dilate lung vessels; thereafter, nitric oxide was inactivated rapidly by combination with hemoglobin in red cells and by oxidation19-21. Methemoglobin levels remained low because nitric oxide was reduced by methemoglobin reductase in red cells41.

Inhalation of nitric oxide decreased the Q_VA/Q_T and the Q_S/Q_T, thereby improving arterial oxygenation. Our analysis of V_A/Q distributions demonstrated that the increase in PaO₂ during inhalation of nitric oxide was due to a redistribution of blood flow away from regions with low V_A/Q ratios and toward regions with normal ratios, thus decreasing the inequality in V_A/Q among regions. This redistribution of pulmonary blood flow during nitric oxide inhalation occurred without any important variation in the two major determinants of intrapulmonary shunting: cardiac output did not change, and the partial pressure of oxygen in mixed venous blood increased only during inhalation of nitric oxide at 18 ppm.42-44 Therefore, we believe that the redistribution of pulmonary flow was due to a reversal of regional vasoconstriction in ventilated lung, supporting the hypothesis that nitric oxide selectively dilates blood vessels in ventilated lung regions. During inhalation of nitric oxide, we noted no change in the tidal volume delivered by constant inspiratory airway pressures. Thus, these effects of nitric oxide were probably not produced by bronchodilation. In contrast to inhaled nitric oxide, prostacyclin increased the Q_VA/Q_T and the Q_S/Q_T, thereby reducing the PaO₂ by increasing the fraction of blood flowing to nonventilated lung regions and thus enhancing V_A/Q mismatching. Our data did not determine whether the inhalation of nitric oxide is preferable to intravenous prostacyclin as therapy for ARDS, since the effects of prostacyclin on hemodynamic function and gas exchange were measured for only brief periods.

Long-term inhalation of nitric oxide, for 3 to 53 days, did not cause tachyphylaxis: prolonged inhalation remained effective in reducing pulmonary-artery hypertension and improving oxygen exchange. The increase of approximately 15 percent in the base-line Q_VA/Q_T and pulmonary-artery pressure during the brief daily periods when inhalation of nitric oxide was discontinued was similar at both the beginning and the end of the study. Adding nitric oxide to the inhaled gas allowed us to reduce the FiO₂ by about 15 percent. This minimizes exposure to high concentrations of inhaled oxygen and may reduce its pulmonary toxicity45,46. Since we have treated only a small group of patients with ARDS, we are uncertain whether nitric oxide therapy will improve the survival rate. Nevertheless, six of seven patients admitted with high ARDS-severity scores survived and were discharged from the hospital. This preliminary and uncontrolled study in patients with a high expected mortality rate is encouraging, but the findings must be confirmed by a prospective controlled trial to determine whether nitric oxide can improve the outcome in patients with ARDS. Future studies should evaluate any potential systemic effects of nitric oxide, such as interference with endogenous production of nitric oxide, platelet function,47 or leukocyte adhesion48.

Supported by a grant (Fa 139/1-3/2-3) from the Deutsche Forschungsgemeinschaft and a grant (HL-42397) from the National Heart, Lung, and Blood Institute.

The Massachusetts General Hospital has filed for a patent (pending) on the respiratory uses of nitric oxide.

We are indebted to R. Monhaupt, G. Merker, O. Weber, and R. Simon for technical assistance; to Dr. A. Zaslavsky (Harvard University Department of Statistics) and W. Steudel for statistical advice; to the nurses and staff of the intensive care unit (Universitatsklinikum Rudolf Virchow/Wedding, Freie Universitat Berlin) for their devoted care of our patients; and to Christine Heidelmeyer and Margaret Flynn for assistance in the preparation of the manuscript.

Source Information

From the Klinik fur Anaesthesiologie und operative Intensivmedizin, Universitatsklinikum Rudolf Virchow, Freie Universitat Berlin, Berlin (R.R., K.J.F., F.L., K.S., U.P.), and the Department of Anaesthesia, Harvard Medical School at Massachusetts General Hospital, Boston (W.M.Z.).

Address reprint requests to Dr. Falke at Klinik fur Anaesthesiologie und operative Intensivmedizin, Universitatsklinikum Rudolf Virchow/Wedding, Freie Universitat Berlin, Augustenburger Platz 1, 1000 Berlin 65, Germany.

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