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Departments of 1 Anaesthesiology and 2 Physiology, Academic Medical Center, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study
evaluates the effects of anesthesia and fluid support on
hemodynamic parameters of the mechanically ventilated mouse of four
different strains. All experiments were performed at a similar surgical
level of anesthesia, as indicated by the probing of the pedal
withdrawal reflex. Three anesthetic regimens [fentanyl-fluanisone-midazolam (FFM), ketamine-medetomidine-atropine (KMA), and isoflurane (ISO)], four commonly used mouse strains (Swiss,
CD-1, BalbC, and C57Bl6), and three different fluid support strategies
(no fluid, 0.2 ml · h
1 · 10 g1 of 6% polystarch solution, and 0.5 ml · h1 · 10 g1 saline)
were studied. Mean arterial pressure (MAP) or heart rate (HR)
was similar among the four strains of mice except a trend toward lower
HR for the BalbC mice. In terms of MAP, KMA is the preferred anesthetic
for the Swiss and CD-1 mice, whereas KMA or ISO are recommended for
BalbC or C57Bl6 mice. In terms of HR, ISO is the preferred anesthetic
for the Swiss, CD-1, and C57Bl6 strains. No differences in HR for the
three anesthetics were observed for the BalbC strain. Compared with
administration of no fluid, both saline and polystarch administration
similarly increased MAP by 7 ± 2, 10 ± 2, and 11 ± 2 mmHg at t = 1, 2, and 3 h, respectively, whereas
fluid administration was without effect on HR. Saline supplementation
resulted in an increased dry-to-wet ratio of the heart and both fluid
regimens decreased total hemoglobin in the blood from 12.6 ± 0.5 to 10.4 ± 0.5 g/100 ml. Saline administration was associated with
blood acidosis (pH 7.20 ± 0.03) compared with the Haes (pH
7.29 ± 0.02) or no-fluid group (pH 7.34 ± 0.03), whereas
PCO2 was ~30 mmHg for all groups. We conclude
that at similar surgical levels of anesthesia, the preferable type of anesthesia (ISO or KMA, but never FFM) depends on the strain used and
whether MAP or HR is the focus of study. Additional fluid support is
beneficial in terms of raising arterial blood pressure, although this
is at the cost of changes in organ water content and increased anemia.
blood pressure; heart rate; murine physiology
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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THE MOUSE HAS BECOME a model of choice in molecular medicine due to the knowledge concerning the mouse genome and the general availability of genetically modified mice. Current research is becoming increasingly focused on the relation between gene and function, and physiological genomics is a rapidly growing area in cardiovascular research. Although the issue of anesthetics and fluid support is often well described and validated in terms of hemodynamics and sedation in similar experiments in larger animals, such information is mostly lacking in mice.
In particular, heart rate (HR) and blood pressure are, when reported, frequently depressed in studies (17, 18). Furthermore, even when hemodynamic parameters are reported to fall into the "normal" range, it is often uncertain whether this is due to perceived pain or preserved hemodynamic regulation because no indication of depth of anesthesia is usually given. Thus it is imperative to have mouse models with hemodynamic parameters in the normal range that are not due to elevated pain levels if a proper interpretation of the physiological consequences of genetic manipulations is desired.
The present study focuses on the type of anesthesia and the use
of fluid support as important mediators in the optimization of
hemodynamics in mechanically ventilated mouse models. Although it is
very important, few studies have systematically looked at these aspects
for the mouse within one experimental design. In many
hemodynamic studies, the anesthetic regimen of choice has been urethane
and/or 
-chloralose, which was recently recommended for the mouse
(4, 17). However, in our study, the
urethane/-chloralose combination was inferior in terms of blood
pressure and HR when compared with a fentanyl-fluanisone-midazolam
(FFM) regimen (15). In addition, the analgesic properties
of the recommended dosage (4) were insufficient to prevent
animal responses to noxious stimuli. It should be noted that others
(14) have reported on the insufficient pain reduction with
the use of -chloralose, despite its widespread use in studies aimed
at preserving hemodynamic function. Therefore, continuous monitoring of
the depth of anesthesia is necessary in the development and
optimization of in vivo mouse models. In the present study, depth of
anesthesia was indicated by probing the pedal withdrawal reflex, as
recommended by Flecknell (6).
It has been suggested that to maintain isovolemia, and thereby blood pressure, fluid should be administered to ventilated animals undergoing surgery and experimentation (6, 11, 19). However, quantitative data on how fluid administration affects hemodynamics, blood anemia, and edema for the anesthetized, mechanically ventilated mouse are currently lacking.
Although in the field of genetic manipulations most research is restricted to a single species, i.e., the mouse, a large variety of mouse strains with different genetic backgrounds are in use. Although it is known that a large interstrain variability exists in the sensitivity toward anesthetic agents (1, 21), it is unknown whether hemodynamic parameters among strains vary when compared at a similar level of analgesia for different anesthesia regimens.
The purpose of this study is therefore to develop an in vivo mouse model for hemodynamic research with sufficient pain reduction such that surgical interventions may be performed, and to determine the following: 1) the optimal anesthetic regimen in terms of blood pressure and HR, 2) the quantitative effect of fluid support on important hymodynamic parameters, and 3) whether hemodynamic parameters in such anesthetized model differ among commonly used mice strains.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Mice Strains
Four different mouse strains (all male) were investigated: Swiss (33 ± 1 g; 7-8 wk), CD-1 (32 ± 1 g; 7-8 wk), BalbC (27 ± 1 g; 12-13 wk), and C57Bl6 (27 ± 1 g; 8-9 wk). All mice were obtained from Harlan. These strains were chosen due to their frequent use in current biomedical research. All animals were kept in cages in groups of 2-6 animals of similar strain subjected to a 12-h dark/12-h light cycle, with water and food given ad libitum.Anesthesia
Three different anesthetic regimens were studied: FFM, ketamine-medetomidine-atropine mixture (KMA), and isoflurane (ISO). The FFM mixture consisted of (in ml) 1 Hypnorm (0.315 mg/ml fentanyl + 10 mg/ml fluanison), 1 Dormicum (5 mg/ml midazolam), and 2 saline. This mixture was administered (0.1 ml/10 g body wt ip) for induction of anesthesia, whereas anesthesia was maintained throughout the experiment by continuous intraperitoneal infusion of this mixture at a rate of 0.1 ml · h1 · 10 g1.
Intraperitoneal induction of anesthesia for the KMA mixture was started
with 0.1 ml · h1 · 10 g1
(12.5 mg/ml ketamine + 20 µg/ml medetomidine), with anesthesia maintained by continuous infusion at a rate of 0.1 ml · h1 · 10 g1 (3.5 mg/ml
ketamine + 3.5 µg/ml medetomidine). The induction of anesthesia
with the gaseous ISO was started by placement of the animal in a
container with 4-5% ISO, whereas maintenance of anesthesia was
provided by continuous inhalation of 1.5-2% ISO.
Fluid Support
We examined the effects of intravascular fluid administration by comparing no fluid, 0.2 ml · h1 · 10 g1 Haes (Fresenius Kabi), and 0.5 ml · h1 · 10 g1 saline
administration throughout the experiment. The amount of saline is in
between infusion rates commonly used in mouse models (6, 11,
19). Fluid was given through the vena jugularis with the use of
polyethylene tubing [0.61 mm outer diameter (OD), 0.28 mm inner
diameter (ID)] and a syringe pump (Harvard Apparatus) (11). The Haes solution consisted of 6% polyhydroxyethyl
starch and 0.9% NaCl. The saline solution consisted of 0.9% NaCl.
Depth of Anesthesia
The pedal withdrawal reflex was used as an index of surgical anesthesia, as recommended by Flecknell (6). Every 20 min throughout the experimental protocol, the right or left hind leg (intermittent) was stretched by pulling the fascia in between the toes and subsequently pinching it with a blunt tweezers as recommended. When a sharp withdrawal of the hind leg was observed after the fascia was pinched, it was assumed that surgical anesthesia was not present and an additional intraperitoneal bolus of the anesthetic mixture FFM or KMA or an increase in isoflurane inhalation concentration was applied. The additional bolus entailed 0.1 ml of the maintenance anesthetic mixture for FFM and KMA or a 0.5% increase in ISO inhalation concentration. As an index of anesthesia level, we used the number of times that the animal responded to the total of 10 times that the pedal withdrawal intervention was performed throughout each experiment.Preparation
Animals were treated according to the guidelines of the Declaration of Helsinki and all procedures were in accordance with the requirements of the Animal Ethics Commission of the University of Amsterdam.After anesthesia was induced, a tracheotomy was performed (trachea tube 1.0 mm OD, 0.6 mm ID) and mechanical ventilation was started. The animals were ventilated (model CIV-101; Columbus Instruments) with 50% O2-50% N2 at a rate of 100 breaths/min, an inspiratory-expiratory fraction of 0.25-0.35, and a tidal volume of 0.3 ml (23). The carotid artery was cannulated with polyethylene tubing (0.61 mm OD, 0.28 mm ID) and blood pressure and HR were recorded using a heparinized saline-filled catheter. The catheter was connected to a blood pressure transducer (Truwave PX-600F; Baxter), which was sampled at 1 kHz, and subsequently displayed and stored at 0.5 Hz using LabView version 5.1 (National Instruments) applications. Temperature was controlled at 37°C with the use of rectal temperature monitoring, a temperature-controlled heating pad, and an infrared lamp. The experiment started 10 min (designated t = 0 min) after the blood pressure transducer was connected, thus allowing 10-min stabilization of the preparation. Each experiment lasted for 180 min, after which a 0.2-ml blood sample was drawn from the carotid cannula for analysis of blood gases and hemoglobin (Hb) concentration (ABL550). Subsequently, a laparotomy was performed, followed by a 5-min blood pressure recording, after which the chest was opened, and blood pressure was recorded for an additional 5 min. Finally, the heart and the duodenum were taken out, blotted dry with a paper towel, and wet weight was determined. Dry weight was measured after 2 days of storage at 70°C.
Experimental Protocol
Effects of anesthesia on blood pressure and HR for four different mouse strains. The three different anesthetic regimens (n = 4 each regimen) were compared at a surgical level of anesthesia for their effects on hemodynamics. In addition, to examine whether strain significantly affected the relationship between anesthesia and hemodynamics, this relationship was compared among the four different mouse strains (n = 4 each strain).
Effects of fluid support on blood pressure, HR, total Hb, and edema of the intestine and heart for three different anesthetic regimens. To examine to what extent the hemodynamics of the mouse could be improved by the intravascular administration of fluid, two commonly used fluid supplementation protocols (large volume of crystalloid or smaller volume of isooncotic fluid) were compared with animals receiving no fluid (from protocol 1) for the three anesthetic regimens (n = 4 each). The comparison was facilitated by calculating the change in MAP or HR as result of fluid supplementation: the mean MAP or HR for each type of anesthesia of protocol 1 was subtracted from the individual MAP or HR value for that specific anesthesia regimen at t = 0, 60, 120, and 180 min. For comparison of total Hb (tHb) and edema, an extra group of animals was examined, where blood, and subsequently the heart and intestine, were immediately excised following induction of anesthesia ("direct" protocol). These fluid experiments were only performed for the C57Bl6 strain.
Statistics
All data are presented as means ± SE. ANOVA was performed using the general linear model repeated-measures procedure (SPSS version 10.1) for the between-subject factor (fluid) and within-subject factor (time). After an overall F-test showed significance, post hoc tests with Bonferroni corrections were performed to evaluate differences among means. One-way ANOVA was performed comparing dry-to-wet weight ratio for the heart and intestine and tHb (g%) between the three fluid protocols (no fluid, saline, or Haes) and the "direct" protocol.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Both the FFM and the KMA regimen resulted in similar levels of anesthesia, as indicated by the number of times that the animal responded to the pinching in between the toes throughout the experiment, i.e., 2.7 of 10 for FFM and 2.8 of 10 for KMA. For the ISO regimen this index was slightly, albeit significantly, smaller, i.e., 1.8 of 10.
MAP and HR for the four different strains and three different
anesthesia regimens are shown in Fig. 1.
For all four strains, at similar depths of anesthesia, FFM was always
associated with the lowest MAP during the 3 h of experimentation.
In contrast, KMA resulted in higher MAP for all four strains. Only the
efficacy of the ISO anesthesia in relation with MAP was dependent on
the strain used. For the BalbC and the C57Bl6 strain, both KMA and ISO
were equally superior compared with FFM in maintaining MAP at high
values. However, for the Swiss and CD-1 strain, KMA is the preferred
anesthetic regimen compared with both FFM and ISO in terms of MAP.
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When the MAP of the different strains is compared in the anesthetized condition by using the optimal anesthetic regimen KMA, no significant differences were observed. The MAP at 3-h experimentation is 68 ± 7, 79 ± 7, 66 ± 4, and 66 ± 3 mmHg for the Swiss, CD-1, BalbC, and C57Bl6 strains, respectively.
The HR measured with the three anesthetic regimens in the BalbC was superimposed, showing that the type of anesthetic did not influence HR in this strain. However, this did not apply to the other three strains. Especially for C57Bl6, a clear trend was observable for higher HR with ISO compared with KMA and FFM. The HR with KMA was superimposed with that of FFM in this strain. For both the Swiss and the CD-1 strain a similar trend for higher HR with ISO was present, although this was less clear and mainly became noticeable after 1 h of experimentation. The data indicate that ISO, at similar depth of anesthesia, is the preferred anesthetic in terms of HR when working with C57Bl7, CD-1 and Swiss, whereas for BalbC all three anesthetic regimens may be used.
When the HR of the different strains is compared in the anesthetized condition using the optimal anesthetic regimen ISO, no large differences were observed among the Swiss (477 ± 43), CD-1 (515 ± 30), and C57Bl6 (538 ± 27) strains. Only for the BalbC strain does a trend exists for a lower HR (434 ± 8) compared with the other strains.
Figure 2 demonstrates the effects
of intravenous fluid supplementation on MAP and HR for the different
anesthesia protocols. ANOVA showed that there was an overall effect of
fluid administration on MAP (P = 0.002), which was time
dependent (P < 0.001) but indiscernible (P = 0.741) between saline and Haes administration.
Fluid administration significantly improved blood pressure by 7 ± 2, 10 ± 2, and 11 ± 2 mmHg at t = 1, 2, and
3 h. Although Fig. 2 indicates that there is a trend for lower HR
with fluid administration, it did not reach statistical significance
(P = 0.052).
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Figure 3 depicts the effect of 3-h
experimentation with and without fluid administration on organ edema
and blood anemia. Saline administration during the 3-h experiment was
associated with a surprisingly increased dry-to-wet ratio of the heart,
whereas fluid (both saline and Haes) administration was without effect on the dry-to-wet ratio of the intestine. In addition, both fluid regimens significantly decreased tHb in the blood from 12.6 ± 0.5 to 10.4 ± 0.5 g/100 ml. Blood gases at the end of the 3-h experiment were similar for the no-fluid, Haes, and saline groups: PCO2 of 28.7 ± 4.5, 30.9 ± 2.8, and
31.1 ± 2.6 mmHg, and PO2 of 173 ± 16, 181 ± 19, and 183 ± 17 mmHg, respectively. However, saline administration was associated with increased acidosis of the
blood compared with no-fluid or Haes administration: pH of 7.20 ± 0.03 (saline group), 7. 29 ± 0.02 (Haes group), and 7.34 ± 0.03 (no-fluid group), respectively.
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Sampling of 0.2 ml of blood from the carotid artery resulted in a drop in mean blood pressure by 15.0 ± 1.0 mmHg. After the blood was withdrawn, a 5-min laparotomy was associated with no drop in blood pressure (0.4 ± 0.7 mmHg), in contrast with an additional significant fall in blood pressure (17.8 ± 1.8 mmHg) when blood pressure was recorded 5 min after the thorax was opened. However, no pedal withdrawal reflex was observed during both surgical interventions, indicating well-preserved surgical anesthesia following 3 h of experimentation.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The four major findings of the present study are 1) hemodynamic parameters are similar between different strains of mice at a surgical depth of anesthesia except that a trend toward lower HR was present for BalbC mice, 2) the preferred anesthetic regimen (ISO or KMA, but never FFM) depends on the strain used and whether MAP or HR is the focus of study, 3) fluid support improves arterial blood pressure, albeit at the cost of changes in organ water and blood Hb content, and 4) mild metabolic acidosis was present after 3 h of mechanical ventilation, and acidosis was exacerbated when saline was used for fluid support. It is important to note that body temperature was strictly controlled in all experiments, such that normal homeostasis for prolonged procedures could be achieved.
Strain Effects
In a previous study (5), it was reported that no differences were present in HR or blood pressure between C57Bl6, Swiss Webster, and CD-1 mice in the nonanesthetized, nonrestrained resting condition, whereas differences were observed comparing different strains. A MAP of 105 mmHg and a HR of 520 beats/min were reported as normal hemodynamic parameters for these three strains that were also used in the present study. A recent study showed similar results for the comparison of the nonanesthetized Swiss Webster and C57Bl6 strains (20). The present study extends these observations to the anesthetized, ventilated condition of the Swiss Webster, C57BL6, and CD-1 strains. It is known that strain differences in analgesic sensitivity toward opioid agents exist among the strains examined in the present study (21); however, such strain effect on sensitivity was not observed for ISO (24). In the present study, all strains received a similar dosage of the anesthetic agent, resulting in surgical anesthesia for all strains. That similar reductions in blood pressure and HR were observed for the different strains (except for the HR of the BalbC strain) with this similar dosage of the anesthetic agent indicates that for the anesthesia regimens used in the present study no large interstrain differences in sensitivity toward analgesia exist, as was also found previously for ISO (24). Alternatively, it may be argued that all strains were anesthetized to such extent (surgical level of anesthesia) that possible differences in sensitivity were mitigated.Anesthesia Effect on Blood Pressure and HR
Although the number of times the animal responded to pinching of the hind leg was slightly less for the ISO regimen than for the FFM and KMA regimen, the data indicates that the level of anesthesia was comparable among the three anesthetic regimens. Despite the frequent use of the anesthesia regimen of ketamine-xylazine in murine cardiovascular studies, several of these studies (8, 10, 12, 16, 25) have documented low HR associated with this type of anesthesia. We found low HR with our combination of ketamine-medetomidine, which low HR could be significantly improved by the use of atropine administration (C. J. Zuurbier, unpublished observations). These data indicate that even small amounts of2-adrenergic agonists (xylazine and medetomidine) in the
mice increase vagus activity to a large extent. However, even with
intermittent administration of atropine the associated HR is still
lower (400-450 beats/min) for the KMA regimen in three of the four
strains compared with ISO anesthesia (~500 beats/min) or with the
nonanesthetized condition (~500 beats/min) (3, 5). Only
for the BalbC strain was no difference in HR between KMA and ISO
observed. ISO is therefore a preferred anesthetic in terms of HR
compared with ketamine in Swiss, CD-1, and C57Bl5 mice. Other
beneficial aspects of the use of ISO are that it is easily titrated to
the desired level of anesthesia and that postoperative mortality is
negligible (26). Although mean arterial blood pressure was
best maintained by KMA for all four strains, or also by ISO for the
BalbC or C57Bl6 strain, its value (~70 mmHg) is still considerably
below values reported for the nonanesthetized animal (~90-110
mmHg) (3, 5). The most likely explanation for this difference is the well-known cardiac depressant effect of most anesthetics (2, 5). In addition, a surgical level of
anesthesia was deliberately chosen throughout the experiments for a
sufficient analgesia, such that this model allows interventions
associated with noxious stimuli for the animal. That this model allows
surgicical interventions was confirmed by the lack of the hind leg
withdrawal reflex during laparotomy or thoracotomy. This deep level of
anesthesia may explain why arterial blood pressure in our model can be
lower than blood pressure in anesthetized mice reported by some studies (4, 13).
Fluid Support
Because of the perceived increased sensitivity of the mouse as a research animal to surgery and ventilation, many researchers have used fluid administration to compensate for possible fluid losses (10, 11, 13, 19). However, to our knowledge there has been no study that have examined in a quantitative manner to what extent fluid support actually supports hemodynamics in the anesthetized, ventilated mice and whether fluid support may also be associated with negative effects. This is the rationale as to why fluid support was examined in the present study. The results indicate that fluid support does raise blood pressure. Administration of 0.5 ml · h1 · 10 g1 saline
increased blood pressure by ~10 mmHg at 1-2 h of
experimentation, resulting in a MAP of 80-85 mmHg, in accordance
with blood pressure recordings at similar time intervals of 82-89
mmHg in a mouse model anesthetized by 1.5-2% ISO receiving 0.5 ml/10 g Ringer lactate solution (19). Blood pressure was
similarly increased using either 0.5 ml · h1 · 10 g1 saline or
0.2 ml · h1 · 10 g1 6%
Haes solution, which is in accordance with the observation that only
30-40% of the infused volume remains intravascular for saline
(7) compared with high molecular weight solutions. No changes in hematocrit were observed for the no-fluid group, indicating that possible water loss by evaporation through expiration or from open
wounds were of no consequence for the intravascular volume in our
model. In contrast, both saline and Haes administration were associated
with a similar degree of hemodilution. Other studies (7,
9) have also shown diminished hematocrit values following the
administration of saline or high molecular weight compound solution in
normovolumic animals. The observed pH of 7.34, together with the
arterial PCO2 of 28.7 mmHg, is similar to
values reported in the literature for mice (4, 10). The
arterial PCO2 is somewhat at the low side,
indicating that mice are sensitive to the development of mild metabolic
acidosis during prolonged mechanical ventilation in the anesthetized
condition. Interestingly, the fluid administration resulted in
increased acidosis, especially for the saline administration. This
increased acidosis may be due to a hyperchloremic metabolic state as a
result of large quantities of normal saline (22).
Therefore, our data indicate that for obtaining equal effects on blood
pressure, the use of Haes solution is recommended due to the smaller
changes observed in tissue water content and blood acidity.
In conclusion, the current study provided comparative data on three commonly used anesthetic regimens in mechanically ventilated mice for four commonly used strains, anesthetized at such levels that surgical interventions may be performed with minimal pain perception for the animal, and reported their disparate effects on hemodynamic parameters. The development of this mouse model demonstrated that the preferred anesthetic regimen (ISO or KMA, but never FFM) depends on the strain used and whether MAP or HR is the focus of study. Additional fluid is beneficial in terms of raising arterial blood pressure, although this is at the cost of changes in organ water content and increased anemia.
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FOOTNOTES |
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Address for reprint requests and other correspondence: C. J. Zuurbier, Dept. of Anaesthesiology, Academic Medical Centre, Univ. of Amsterdam, Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands (E-mail: c.j.zuurbier{at}amc.uva.nl).
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.
First published February 14, 2002;10.1152/ajpheart.01002.2001
Received 15 November 2001; accepted in final form 2 February 2002.
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DISCUSSION
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