1 Critical Care Research Program, Department of Anesthesiology and Intensive Care, and 2 Department of Surgery, Kuopio University Hospital, FIN-70210 Kuopio, Finland
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ABSTRACT |
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The hepatic
arterial buffer response (HABR) tends to maintain liver blood flow
under conditions of low mesenteric perfusion. We hypothesized
that systemic hypoperfusion impairs the HABR. In 12 pigs, aortic blood
flow was reduced by cardiac tamponade to 50 ml · kg1 · min
1 for 1 h (short-term tamponade) and further to 30 ml · kg
1 · min
1 for another
hour (prolonged tamponade). Twelve pigs without tamponade served as
controls. Portal venous blood flow decreased from 17 ± 3 (baseline) to 6 ± 4 ml · kg
1 · min
1 (prolonged
tamponade; P = 0.012) and did not change in controls, whereas hepatic arterial blood flow decreased from 2 ± 1 (baseline) to 1 ± 1 ml · kg
1 · min
1 (prolonged
tamponade; P = 0.050) and increased from 2 ± 1 to 4 ± 2 ml · kg
1 · min
1
in controls (P = 0.002). The change in hepatic arterial
conductance (
Cha) during acute portal vein
occlusion decreased from 0.1 ± 0.05 (baseline) to 0 ± 0.01 ml · kg
1 · min
1 · mmHg
1
(prolonged tamponade; P = 0.043). In controls,
Cha did not change. Hepatic lactate
extraction decreased, but hepatic release of glutathione S-transferase A did not change during cardiac tamponade. In
conclusion, during low systemic perfusion, the HABR is exhausted and
hepatic function is impaired without signs of cellular damage.
tonometry; lactate; glutathione S-transferase A
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INTRODUCTION |
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DURING LOW-BLOOD FLOW STATES, profound reductions in splanchnic blood flow and volume occur (3, 20, 23). Hypovolemia in healthy volunteers causes a sustained splanchnic hypoperfusion (5), and in patients with hemodialysis-induced hypovolemia, the splanchnic erythrocyte content decreases (24). In patients with low cardiac output, splanchnic perfusion is reduced in proportion to systemic perfusion (13, 19). The liver is partially protected from hypoperfusion by the hepatic arterial buffer response (HABR; Ref. 10). The HABR, the hydrodynamic interaction between the portal venous and hepatic arterial blood flow, tends to maintain liver blood flow under conditions of low mesenteric blood flow (8, 11). It is believed that constantly produced adenosine in the Mall space is washed out by the portal venous blood flow under normal conditions (12). Because branches of hepatic arteries and the portal vein are close together in the space of Mall, accumulation of adenosine during decreased portal venous blood flow causes dilatation of the hepatic arterial branches and thereby an increase in hepatic arterial blood flow (12). Because adenosine production is an energy-dependent process, prolonged and severe splanchnic hypoperfusion may impair or abolish the HABR. The HABR has not been measured in anatomically intact animals. It is not known whether the HABR is exhausted during prolonged and severe impairment of systemic perfusion. Exhaustion of the HABR during low systemic blood flow could explain the observed organ dysfunction associated with heart failure and other clinical conditions associated with low splanchnic blood flow. We hypothesized that under conditions of sustained low systemic perfusion, a relative increase in hepatic arterial perfusion cannot be maintained and the HABR is exhausted. We theorized further that under these conditions, liver function is impaired and signs of impaired cellular integrity may appear.
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MATERIALS AND METHODS |
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This study was approved by the Institutional Animal Care and Use Committee of the University of Kuopio.
Anesthesia and monitoring.
Twenty-four female pigs (27-40 kg) were deprived of food but not
water 12 h before the experiments. After premedication with atropine (0.05 mg/kg) and azaperone (8 mg/kg im), an ear vein was
cannulated and thiopental sodium (5-15 mg/kg) was administered intravenously for endotracheal intubation. Anesthesia was maintained with thiopental (5 mg · kg1 · h
1) and fentanyl
(30 µg · kg
1 · h
1) until
the end of the surgical procedure and afterward with thiopental (5 mg · kg
1 · h
1) and fentanyl
(5 µg · kg
1 · h
1) until
the end of the experiment. The animals were ventilated with a
volume-controlled ventilator without positive end-expiratory pressure.
Fractional inspired O2 concentration was adjusted to reach
a target arterial PO2 of >100 mmHg. Tidal
volume was kept at 10 ml/kg, and the minute ventilation was adjusted to
maintain arterial PCO2 levels between 33 and 45 mmHg. A pulmonary artery catheter (via the right submandibular vein), a
femoral artery catheter, and a gastric air tonometer were inserted
(Tonometrics, Worcester, MA). During surgery, the animals received
saline at 5 ml · kg
1 · h
1.
Additional Ringer acetate and hydroxyethyl starch were administered in
equal amounts to keep the pulmonary artery occlusion pressure between 7 and 11 mmHg. The body temperature of the animals was kept at 38 ± 1°C using an operating table heater and warmed fluids.
Animal preparation. The abdominal cavity was exposed by a midline abdominal incision. Air tonometers (Tonometrics) were inserted into the urinary bladder and the jejunum through a small antimesenteric incision 80 cm distal to the ligament of Treitz. In the last 12 animals, microdialysis capillaries were attached to the jejunal tonometer as previously described (21). The abdominal aorta, celiac trunk, and superior mesenteric artery were exposed, and ultrasound transit time flow probes (Transonic Systems, Ithaca, NY) were placed around the vessels. An inflatable occluder was placed around the aorta proximal to the flow probe. Two fluid-filled catheters were inserted proximally and distally into a mesenteric vein, respectively. The tip of the first catheter was left in the mesenteric vein, whereas the tip of the second catheter was positioned within the portal vein. The hepatic arteries and the portal vein were exposed, and ultrasound transit time flow probes were placed around the vessels. An inflatable occluder was placed around the portal vein. A fluid-filled catheter was inserted into the celiac trunk, and the tip was positioned close to the bifurcation of the hepatic artery. At the end of the experiment, the catheter was pulled back while the hepatic arterial blood flow was still being recorded. This test confirmed that hepatic arterial blood flow was not impaired by the catheter. A hepatic vein catheter was inserted via the right internal jugular vein, and its position was checked by direct palpation. Thereafter, the catheter was withdrawn 0.5-1 cm from the wedged position to allow blood sampling. A catheter was inserted into the pericardial space through a small diaphragmatic and pericardial incision and fixed to the pericardium to prevent a leakage. When all surgical procedures were completed, the abdominal wall was reapproximated and towels were placed on the surface to minimize heat loss.
Experimental protocol.
The surgical preparation was followed by 90 min of stabilization. The
animals were randomized either to cardiac tamponade (n = 12) or controls without tamponade (n = 12; block
randomization, 12 animals in each block). Cardiac tamponade was induced
by instilling warmed hydroxyethyl starch into the pericardial space.
Once the target abdominal aortic blood flow of 50 ml · kg1 · min
1 was
reached, the abdominal aortic blood flow was kept constant by adjusting
the tamponade for 1 h (short-term tamponade). Thereafter, the
abdominal blood flow was further reduced to 30 ml · kg
1 · min
1 for another
hour (prolonged tamponade). For HABR assessment, the portal vein was
occluded rapidly by inflating the occluder until the portal venous
blood flow was zero and stable hemodynamics had been reached. For the
measurement of zero flow pressure in the hepatic artery, the aortic
occluder was briefly inflated. The maneuver was performed at baseline
and thereafter every 30 min in all 12 animals from the control group.
Twenty to thirty seconds of stable blood flows were recorded during
each occlusion. In the tamponade group, the HABR was tested similarly
at baseline and during short-term tamponade. During prolonged
tamponade, the portal vein was occluded in only 5 of the 12 animals,
because occlusion of the portal vein at very low systemic perfusion in pilot animals resulted in cardiovascular collapse and death. In the
tamponade group, four animals died between the second-to-last and the
last measurement.
Hemodynamic monitoring. Systemic, pulmonary and hepatic arterial, central, portal, and hepatic venous, and pulmonary artery occlusion pressures were recorded with quartz pressure transducers and displayed on a multimodular monitor and recorder (AS3, Datex-Ohmeda, Helsinki, Finland). All pressure transducers were zeroed to the level of the heart. Heart rate was measured from the electrocardiogram, which was also continuously monitored. Cardiac output was measured by thermodilution technique (mean value of 3 measurements). Central venous blood temperature (in °C) was recorded from the thermistor of the pulmonary artery catheter.
Blood flow measurements. Blood flows were measured with ultrasound transit time flow probes (Transonic Systems) placed around the abdominal aorta, celiac trunk, superior mesenteric artery, hepatic arteries, and portal vein. The transit time ultrasound volume flowmeter has been demonstrated to provide adequate measures of arterial and venous flows in experimental animals, if carefully positioned and aligned with respect to the vessel (4, 15). The perivascular ultrasound flow probes were calibrated in vivo. We checked the accuracy of the flow probes in our own laboratory using heated water (36°C) at three different nonpulsatile flow rates and latex tubing of the appropriate size.
Blood gas, lactate, and GSTA measurements.
Blood samples were analyzed immediately after withdrawal and were
temperature corrected in a blood gas analyzer (ABL 520, Radiometer, Copenhagen, Denmark). Plasma lactate was
measured by the amperometric enzyme-sensor method (YSI 2300 Stat Plus, YSI, Yellow Springs, OH). Serum GSTA concentration was measured by an
enzyme immunoassay designed for porcine blood (Hepkit-Alpha, BIO74Pg,
Biotrin International, Dublin, Ireland) after storage at 70°C. The
quantitation range of the assay was 0-100 µg/l.
Luminal microdialysis. Luminal microdialysis was used for the assessment of luminal lactate release as described previously (21). The length of the semipermeable polysulfone membrane (Fresenius, Bad Homburg, Germany) was 2 cm with a volume of 0.5 µl. The microdialysis fluid was Ringer acetate (Ringersteril), and the microdialysis flow rate was kept constant at 2 µl/min using a microdialysis pump (Carnagie Medicine, Stockholm, Sweden). The time delay from the capillary to the sampling tube was 7 min. Samples were collected every 15 min, and the samples were analyzed using the same analyzer as for the blood lactate.
Lactate and GSTA exchange.
We used the following equations for lactate and GSTA exchange:
1) mesenteric lactate (GSTA) exchange = mesenteric
blood flow × [mesenteric vein lactate (GSTA) arterial
lactate (GSTA) concentration]; 2) prehepatic lactate (GSTA)
exchange = portal vein blood flow × [portal vein lactate
(GSTA)
arterial lactate (GSTA) concentration]; 3)
hepatic lactate (GSTA) influx = portal vein blood flow × portal vein lactate (GSTA) concentration + hepatic arterial blood
flow × arterial lactate (GSTA) concentration; 4)
hepatic lactate (GSTA) efflux = (portal vein + hepatic
arterial blood flow) × hepatic vein lactate (GSTA) concentration;
5) hepatic lactate (GSTA) exchange = hepatic lactate
(GSTA) influx
hepatic lactate (GSTA) efflux; and 6)
pulmonary lactate exchange = cardiac output × (arterial lactate concentration
mixed venous lactate concentration).
Statistics. For statistical analysis, the SPSS software package (version 9.0) was used. Differences between groups were assessed by ANOVA for repeated measures using one dependent variable, one grouping factor (tamponade vs. control), and one within-subject factor (time). In this design, a significant group-time interaction is interpreted as an effect of tamponade. Levene's test was used for the assessment of equal variances. In case of unequal variances, logarithmic or inverse transformation was performed. Significant time effects were located post hoc by Wilcoxon's test. If transformation did not equalize the variances, nonparametric tests were used: the Mann-Whitney U-test for the assessment of between-group effects and Friedman's test for within-group effects. Within-group differences were located by Wilcoxon's test. When more than two measurements were compared, the Bonferroni correction was used. In the tamponade group, four animals died between the second-to-last and the last measurement. Three of the animals were in the group with mesenteric venous and jejunal luminal lactate measurements. The data from these four animals were excluded from the statistical analysis, except for mesenteric venous lactate, mesenteric lactate exchange, and jejunal luminal lactate in which the analysis included the data from five instead of six measurements (baseline, 30, 60, 90, and 120 min). During severe tamponade, portal vein occlusion for HABR assessment was performed in only 5 of the 12 animals in the tamponade group. The ANOVA therefore includes only the data from moderate tamponade. To assess whether there was a further change in hepatic arterial conductance during severe tamponade, Wilcoxon's signed-rank test was performed in these five animals. Statistical significance was considered at P < 0.05. All results are presented as means ± SD unless otherwise stated.
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RESULTS |
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Systemic hemodynamics and central temperature are shown in Table
1. Cardiac output (abdominal aortic blood
flow) decreased by 21% (35%) and 55% (64%) and systemic arterial
blood pressure by 40% and 64% during short-term and prolonged
tamponade, respectively.
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Effects of low cardiac output on regional blood flows.
Regional blood flows are given in Fig. 1.
During short-term tamponade, hepatic arterial blood flow increased
significantly in both groups (tamponade: from 2 ± 1 to 3 ± 1 ml · kg1 · min
1,
P = 0.032; controls: from 2 ± 1 to 3 ± 2 ml · kg
1 · min
1,
P = 0.004) and celiac trunk blood flow increased
significantly in controls (4 ± 2 vs. 5 ± 3 ml · kg
1 · min
1,
P = 0.024) but not in the tamponade group (3 ± 1 vs. 4 ± 1 ml · kg
1 · min
1,
P = 0.262). The other flows decreased in the
tamponade group and remained unchanged in controls. During prolonged
tamponade, celiac trunk and hepatic arterial blood flows decreased in
tamponade animals but increased further in controls.
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Effects of low cardiac output on adequacy of local mucosal
perfusion.
Arterial pH, PCO2, and mucosal-arterial
PCO2 gradients are shown in Table
3. Arterial pH decreased in the tamponade
group from 7.45 ± 0.03 to 7.26 ± 0.07 (P < 0.001). Whereas jejunal- and urinary bladder mucosal-arterial
PCO2 gradients increased in parallel during the
whole experiment, gastric mucosal-arterial PCO2
gradients demonstrated a wide variability and increased consistently only during prolonged tamponade.
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Effects of low systemic blood flow on HABR.
Responses to acute occlusion of portal vein are shown in Fig.
2. In control animals, the compensation
of the hepatic arterial blood flow for a decrease in portal venous
blood flow decreased from 16% at baseline to 6% at the end of the
experiment (P = 0.008; Fig. 2A). In
tamponade animals, the hepatic arterial blood flow compensation
disappeared during short-term tamponade (19% ± 12% vs. 0.02% ± 0.05%, P = 0.003) without significant further change during prolonged tamponade in the five animals tested (Fig.
2A). The change in hepatic arterial conduction during portal
vein occlusion remained constant in control animals but decreased in
the tamponade group (from 0.10 ± 0.05 at baseline to 0.01 ± 0.02 ml · kg
1 · min
1 · mmHg
1
during short-term tamponade, P = 0.003; Fig.
2B). The change in hepatic arterial conduction remained at
levels not significantly different from zero during prolonged
tamponade.
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Consequences of low cardiac output on regional metabolism and
cellular integrity.
Blood lactate concentrations and regional lactate exchange are
shown in Tables 4 and
5, respectively. Jejunal luminal,
mesenteric, portal, and hepatic venous and arterial lactate
concentrations increased in parallel in the tamponade group. Pulmonary
lactate exchange increased in the tamponade group from 0.8 ± 0.2 to 5.9 ± 2.2 µmol · kg1 · min
1
(P = 0.015), whereas the increase in mesenteric lactate
exchange from 1.3 ± 2 to 6.3 ± 5.6 µmol · kg
1 · min
1 was not
significant (P = 0.205). Prehepatic lactate exchange did not change (2.9 ± 1.9 vs. 3.2 ± 5.4 µmol · kg
1 · min
1,
P = 0.335). Hepatic lactate uptake decreased when
cardiac output was reduced (at 30 and 120 min, Table 5). It recovered
after 60 min but not after 150 min.
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DISCUSSION |
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The main findings were as follows. 1) The HABR is exhausted during low systemic perfusion, and the capability of the liver to increase lactate uptake is abolished. 2) The fractional splanchnic blood flow is preserved, and the contribution of the splanchnic organs to whole body lactate production is small. 3) Low splanchnic perfusion does not cause GSTA release from hepatocytes but from other splanchnic tissue. 4) In this experiment, jejunal and urinary bladder mucosal-arterial PCO2 gradients better reflect decreasing organ perfusion than gastric mucosal-arterial PCO2 gradients.
The HABR has not been explored in intact animals. The most detailed work has been carried out in splenectomized animals, in which all venous branches of the portal vein and all branches from the celiac trunk but the hepatic arteries have been ligated (2, 11). Although this approach helps to establish the theoretical maximal increase of the hepatic arterial blood flow in response to a reduction of portal venous blood flow, it has several limitations. First, splenectomy and ligation of portal venous branches per se evoke the HABR by decreasing portal venous inflow. Second, ligation of celiac trunk branches increases the perfusion pressure along the hepatic arterial axis. Potential adaptive effects in other arterial beds are therefore neglected. In these experiments, the HABR is tested by occluding the superior mesenteric artery (2, 11). This procedure induces an increase in the peripheral vascular resistance and thereby in the perfusion pressure in the celiac trunk axis, which will result by itself in an increased hepatic arterial blood flow. This can be compensated for by keeping the hepatic arterial pressure constant, e.g., by using a celiac trunk occluder. Portal flow restriction by direct portal vein occlusion of up to 50% does not result in changes in systemic blood pressure, and therefore the perfusion pressure along the celiac trunk axis is maintained (7). However, most of the clinically relevant diseases leading to an impaired portal venous blood flow are associated with a low systemic blood pressure. Examples are hemorrhage, hypovolemia, and cardiac failure. A low systemic blood pressure may decrease the efficiency of the HABR.
Low systemic perfusion and HABR. The increase in hepatic arterial blood flow during the first stage of the experiment (short-term tamponade) was small in relation to the decrease in portal vein blood flow, compensating for only 7% of the flow changes, and it disappeared during the second stage (prolonged tamponade). During low systemic perfusion, the HABR is therefore much less important than previously thought (11). From animal experiments (1, 11, 16), it has been concluded that the increase in hepatic arterial blood flow compensates for roughly 25% of the reduction in portal vein blood flow, and in patients (7) after liver transplantation, values of ~10% have been reported during 50% reduction of portal vein blood flow. In response to acute reduction of portal vein blood flow, we found a somewhat lower fraction (18%) at baseline that also decreased in control animals during the first 90 min of the experiment. The smaller buffer response in our experiment can be explained by the fact that we did not removed the spleen, in contrast to others (2, 11). Preserved spleen perfusion is associated with a lower fraction of the hepatic arterial blood flow from celiac trunk blood flow. This could result in a decreased efficacy of the buffer response.
We hypothesize that the repeated hypoperfusion/reperfusion events induced by testing the HABR exceeded the capacity of the liver to produce adenosine. This could explain the decreasing efficacy of the HABR in controls and, partly, also in tamponade animals. Alternatively, surgery and anesthesia might have caused these effects (9). Our results also demonstrate that the same absolute change in hepatic arterial conductance can have very different effects on absolute flow changes. Hepatic arterial conductance is therefore not very useful for the estimation of the efficacy of the HABR. In our experiment, the efficacy of the HABR in terms of O2 delivery was much more important that the blood flow changes: after 90 min of low cardiac output, the O2 saturation, and therefore the O2 content, was roughly four times higher in the hepatic artery compared with the portal vein (86% vs. 22%; baseline: 95% vs. 56%). This ratio increased to 6.5 after 150 min (85% vs. 13%). Each unit increase in hepatic arterial blood flow can therefore compensate for a four- to six-unit decrease in portal vein blood flow. It has been shown (17) that the hepatic O2 delivery originating from the arterial perfusion may increase from 32% of total hepatic O2 delivery at baseline to 67% during hemorrhage.Low systemic perfusion and regional blood flow changes. Hypovolemia causes splanchnic hypoperfusion (20, 23), and several studies (3, 23) have shown a preferential reduction in splanchnic blood flow during low systemic perfusion. In contrast, we found a proportional reduction in mesenteric, portal, and total splanchnic blood flow even during severe reduction of cardiac output with signs of global hypoperfusion and anaerobic metabolism. Similar results have been shown (17) during hemorrhage. These differences can be explained by different sites of splanchnic blood flow measurements and by the fact that, in most of the experiments, the spleen has been removed, which interferes with the normal physiology.
Also, the extrahepatic fraction of the celiac trunk increased during low cardiac output. This has not previously been described, and the mechanism is speculative. Both local humoral factors or nervous system-mediated effects may play a role. The different, additive effects on systemic blood pressure when either the celiac trunk or superior mesenteric artery is occluded and the regional metabolic consequences have been shown previously (18). The extrahepatic fraction of the celiac trunk blood flow was the only flow that did not decrease significantly after 150 min of cardiac tamponade.Low systemic perfusion and mucosal-arterial PCO2 gradient. The pattern of gastric and jejunal mucosal-arterial PCO2 gradients in tamponade animals paralleled the respective changes in regional blood flows. During short-term tamponade, celiac trunk blood flow and gastric mucosal PCO2 gradients did not change significantly. At the same time, superior mesenteric arterial blood flow decreased and jejunal-arterial PCO2 gradients increased. During prolonged tamponade, both regional flows decreased whereas both mucosal-arterial PCO2 gradients increased. We assume therefore that tonometry reflected the regional blood flow changes. The variability in gastric mucosal PCO2 gradients was higher compared with jejunal mucosal-arterial PCO2 gradients, and the high gradients observed in some of the animals could indicate that the stomach is more vulnerable to surgical stress than the small bowel. Our results indicate that urinary bladder mucosal-arterial PCO2 gradients more consistently reflect decreasing systemic perfusion than gastric mucosal-arterial PCO2 gradients. In patients with circulatory failure (14), urinary PCO2 values were higher than in hemodynamically stable patients, and urinary PCO2 values correlate with the rate of dopamine infusion. Because there is an easy access to the urinary bladder and confounding factors such as mucosal acid production and bicarbonate reflux do not exist, the urinary bladder has the potential to complement or even replace the stomach as a measurement site in tonometry.
Low systemic perfusion and lactate and GSTA exchange.
Pulmonary but neither mesenteric nor prehepatic lactate exchange
increased significantly during tamponade, suggesting that the gut and
other intra-abdominal organs do not contribute much to systemic
hyperlactatemia during low-flow states. An acute decrease in cardiac
output caused a decreased hepatic lactate uptake, followed by a
recovery during short-term tamponade but not during prolonged tamponade. This suggests a mechanism of metabolic compensation or
adaptation within the liver that is exhausted once the perfusion has
decreased to a certain level. Hence, the observed hyperlactatemia during low systemic perfusion was caused both by an increased lactate
production and an inability to increase the hepatic lactate uptake.
Failure of hepatic lactate uptake to increase despite increased hepatic
lactate delivery during low cardiac output (hepatic O2
delivery 1-2
ml · kg1 · min
1) was
also reported by Fahey et al. (6).
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ACKNOWLEDGEMENTS |
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Present address of S. M. Jakob and J. Takala: Dept. of Intensive Care Medicine, Univ. Hospital Bern, Freiburgstrasse, CH-3010 Bern, Switzerland.
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FOOTNOTES |
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Address for reprint requests and other correspondence: S. M. Jakob, Dept. of Intensive Care Medicine, Univ. Hospital Bern, Freiburgstrasse, CH-3010 Bern, Switzerland (E-mail: stephan.jakob{at}insel.ch).
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 22 August 2000; accepted in final form 29 November 2000.
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