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1 Department of Physiology and Pharmacology, Karolinska Institute, and 2 Stockholm University College of Physical Education and Sports, S-171 77 Stockholm, Sweden
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Microdialysis catheters (CMA-60 with a polyamide dialysis membrane; 20,000-molecular wt cutoff) were either immersed in an external medium or were inserted in the quadriceps femoris muscle of healthy subjects, using perfusate with or without dextran 70. Varying the position of the outflow tubing induced changes in hydrostatic pressure. The sample volumes were significantly smaller in catheters perfused without a colloid compared with those perfused with a colloid [11-50% (in vitro) and 8-59% (in vivo) lower than in colloid-perfused catheters with the same position of the outflow tubing]. The sample volumes were also significantly smaller when the dialysis membrane was influenced by maximal hydrostatic pressure (above position) compared with minimal hydrostatic pressure (below position) [7-38% (in vitro) and 3-46% (in vivo) lower than in catheters in the below position with the same perfusion fluid]. In vivo, glucose concentration at a perfusion flow rate of 0.33 µl/min was higher when the catheters were perfused without a colloid [18-28% higher than in colloid-perfused catheters with the same position of the outflow tubing (P < 0.001)] than with a colloid. A corresponding difference also tended to occur with lactate, glycerol, and urea. At 0.16 µl/min, the glucose concentration was the same irrespective of whether fluid loss had been counteracted by colloid inclusion or by lowering of outlet tubing. The mechanism behind the observed concentration difference is thought to be a higher effective perfusion flow rate when fluid loss is prevented at low-perfusion flows. This study shows that fluid imbalances can have important implications for microdialysis results at low-perfusion flow rates.
dextran; glucose; lactate; glycerol; urea
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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WITH MICRODIALYSIS, THE DEGREE of equilibration between the interstitial and perfusion fluids (recovery) is mainly dependent on the perfusion flow, the size of the dialysis membrane, and the diffusivity of substances in the tissue. Generally, most previous microdialysis experiments have been performed under conditions of incomplete equilibration; therefore, the concentrations measured in dialysate represent a fraction of the true interstitial concentration. To precisely determine the magnitude of this fraction, various calibration methods have been suggested, such as the "no net flux" method (8), the method of extrapolation to zero flow (4), or methods based on the inclusion of an internal standard (2, 8, 9, 11, 15). An alternative approach is to use a perfusion flow low enough to ensure complete equilibration between the interstitial and perfusion fluids (1, 2, 10). Because the recovery with this technique is 100%, the concentrations measured in the dialysate equal the concentrations in the interstitial fluid and no recalculation of the data is necessary. To make sampling at these low-perfusion flows possible, without a substantial loss of perfusate into the tissue, we have previously found that a colloid needs to be included in the perfusion fluid (13). In the referred study and in a subsequent study (12), it was shown that, when dextran 70 at 40 g/l is used, no net loss of perfusate occurs, even if the perfusion flow is as low as 0.075 µl/min. When we examined the effect of perfusate loss on metabolite concentrations in dialysate (12), no statistical difference was found between experiments with large perfusate loss and experiments in which the loss of perfusate was prevented by dextran 70. The statistical power in this comparison was, however, low because of a low number of subjects and because the experiments with and without dextran were performed on different days.
The purpose of the present study was to investigate the effect of changes in the colloid osmotic and hydrostatic pressures of the perfusion solution on net fluid transport across the dialysis membrane and on metabolite concentrations in dialysate. Changes in the hydrostatic pressure were induced by varying the vertical position of the outflow tubing, whereas changes in the osmotic pressure were induced by using perfusate with or without the inclusion of dextran 70.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In Vitro Experiments
Twelve microdialysis catheters (CMA-60, CMA Microdialysis, Stockholm, Sweden) with a 20,000-molecular wt cutoff polyamide dialysis membrane (length of 30 mm, 0.62 mm OD) were placed in a vial containing Krebs-Henseleit buffer (KHB) (13) with substance concentrations verified by analysis as follows: 5.1 mM glucose, 2.2 mM lactate, 36 µM glycerol, and 4.8 mM urea. The microdialysis catheters were connected to 1-ml plastic syringes that were placed in a microinfusion pump (CMA-100, CMA Microdialysis). The perfusion flow rate was 0.33 µl/min for the first 6 h, 1.33 µl/min during the subsequent 1.5 h, and 2.66 µl/min during the last 45 min of the experiment. The samples were collected in capped microvials (CMA Microdialysis) in 60-min fractions when the perfusion flow rate was 0.33 µl/min, 15-min fractions at 1.33 µl/min, and 7.5-min fractions at 2.66 µl/min.Effect of varying the position of outlet tubing. To evaluate the effect of varying the position of the outlet tubing on the sample volume collected and on the solute concentrations in dialysate, the microvial (and orifice of outlet tubing) was placed either maximally above or below the microdialysis catheter (the vertical distance between these positions was ~15 cm). The position of the microvial at the start of the experiment was randomized. In each position, three samples per catheter were collected. Before samples were obtained once the microvial position was changed, the system accommodated for 5 min to avoid influence of the previous position.
Effect of adding a colloid to the perfusion solution. The effect of colloid addition was investigated by performing all experiments in a randomized protocol with either KHB only or KHB with 40 g/l of dextran 70 as perfusate, where each individual catheter was perfused with one of the solutions.
By weighing all microvials before and after sample collection on a high-precision balance (Mettler AT 261 Delta Range), the sample volume in each microvial was determined (the density of the perfusate was taken as 1.00). The measured density was found to be 1.007 ± 0.0005 for KHB only and 1.018 ± 0.0007 for KHB supplemented with 40 g/l of dextran 70. The concentrations of glucose, lactate, glycerol, and urea in the microdialysis samples were analyzed by using ordinary enzymatic methods on a CMA-600 microdialysis analyzer as described previously (12). To verify that the analysis of glucose, lactate, glycerol, and urea was not influenced by the inclusion of dextran 70 in the medium, five different solutions with and without dextran 70 were analyzed in quadruplicate. Although metabolite concentrations averaged slightly higher with dextran 70, the results showed no statistically significant difference in concentration of these metabolites between the different medias (glucose: 4.28 ± 0.07 mM with dextran and 4.25 ± 0.07 mM without; lactate: 1.43 ± 0.06 mM with dextran and 1.37 ± 0.06 mM without; glycerol: 91 ± 1.3 µM with dextran and 90 ± 1.8 µM without; urea: 4.61 ± 0.08 mM with dextran and 4.49 ± 0.08 mM without).In Vivo Experiments
Thirteen healthy male subjects with mean age, height, and weight of 24 ± 0.8 yr, 182 ± 0.02 cm, and 77.7 ± 2.7 kg, respectively, participated in the study. Before the start of the investigation, a detailed description of the study was given to the subjects, who gave their informed consent. The ethics committee of the Karolinska Institute approved the study. All subjects arrived to the laboratory in the morning after a normal breakfast and were investigated in the supine position in a room kept at 24-25°C. Each subject had four microdialysis catheters inserted, as previously described (14), in the vastus lateralis of the quadriceps femoris muscle (two in the right and two in the left leg). One of the catheters in each leg was perfused with KHB only, whereas the other catheter was perfused with KHB containing 40 g/l of dextran 70. In subjects 11-13, the concentration of dextran 70 was reduced to 30-35 g/l to avoid the slight overcompensation of the perfusate fluid loss (shown in Fig. 4) when 40 g/l of dextran 70 was included in the perfusion medium.Subjects were divided into three groups with five subjects in groups 1 (subjects 1-5) and 2 (subjects 6-10) and three subjects in group 3 (subjects 11-13). In subjects 1-5, the perfusion flow rate was 0.33 µl/min for the entire 7-h experiment, and microdialysis samples were collected in 60-min fractions (same as in vitro). In subjects 6-10, the perfusion flow rate was 1.33 µl/min for the first 4 h of the experiment and 0.66 µl/min for the next (and last) 2 h. The samples were collected in 30-min fractions. In subjects 11-13, the perfusion flow rate was 0.16 µl/min for the entire 7.5-h experiment, and microdialysis samples were collected in 60-min fractions.
In the experiment with perfusion flow rate of 0.33 µl/min, the microvial was placed maximally below the catheter during the first 3 h as well as during the last 2 h of the experiment. During hours 4 and 5, the microvial was placed maximally above the microdialysis catheter (the vertical distance between these positions being ~15 cm). In the experiment with perfusion flow rates of 1.33 µl/min and 0.66 µl/min, the microvial was placed maximally below the catheter during the first 2 h and maximally above the microdialysis catheter during the next 1 h. Thereafter, the position of the microvial was changed every hour. After 4 h, the perfusion flow rate was changed from 1.33 to 0.66 µl/min. Before sample collection was started and after a change in microvial position (or a change in perfusion flow rate), the system accommodated for 10 min in the experiment with 0.33 µl/min perfusion flow rate and for 5 min in the experiment with the higher perfusion flow rates. In the experiments with a perfusion flow rate of 0.16 µl/min, the outflow tubing from the catheters perfused with KHB only was extended with a 35-cm-long plastic tubing (of the same size) to achieve complete fluid balance between dialysate inflow and outflow as in the catheters perfused with KHB-dextran 70 (30-35 g/l). The outflow tubings from the catheters perfused with KHB only were placed maximally below the catheter, and the outflow tubings from the catheter perfused with KHB-dextran 70 (30-35 g/l) were placed at the same level as the catheter (vertical distance between these positions of ~40 cm). Because of the low flow rate and the extension of the outflow tubing, sample collection started 1.5 h after insertion of the catheters to allow the perfusion fluid to be transported from the membrane to the microvial at the end of the outflow tubing (this volume was 9.1 µl compared with 2.9 µl when the outflow tubing was not extended). Venous blood samples were obtained from an antecubital vein before the start of the experiments and at different time points during the experiment for the different experimental groups. In the experiment with 0.33 µl/min perfusion flow rate, the time points were 2.5, 4.5, and 6.5 h; in the experiment with higher flow rates, the time points were 1.75, 2.75, 3.75, 4.75, and 5.75 h; and in the experiment with 0.16 µl/min as perfusion flow rate, the time points were 4 and 7 h.
The concentrations of glucose, lactate, glycerol, and urea in the
microdialysis samples were analyzed as described for the in vitro
samples. The blood samples were transferred to heparinized tubes and
centrifuged at 3,000 revolutions/min for 10 min, after which the
supernatant was stored at 
20°C until analyzed. The plasma glucose
concentration was determined with colorimetric methods on a Cobas
Mira-s clinical analyzer (Roche Diagnostics, Basel, Switzerland).
One of the catheters (in subjects 1-5) was excluded because it displayed a large continuous decrease in glucose concentration in the microdialysis samples combined with a continuous increase in the lactate concentration. Therefore, the corresponding catheter was also excluded due to a lack of comparable results.
Calculations and Statistics
Values are reported as means ± SE. Each sample in the in vitro experiments was analyzed twice. If the duplicate values differed more than 2% or if the average of the two values differed more than 1% from the median value of the three samples at that position, that sample was excluded (on the bases of these criteria, of the 216 samples analyzed for the in vitro experiment, 14 samples were excluded for glucose, 31 for lactate, 51 for glycerol, and 18 for urea). In the in vivo experiments, each sample was analyzed once. For statistical calculations, a two-way ANOVA was used with a repeated measures design followed by Sheffé's post hoc test. One separate ANOVA was used for each flow rate.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In Vitro Experiments: Comparison of the Different Positions of the Outlet Tubing
The sample volume achieved (Fig. 1) was significantly smaller when the microvials were placed in a position above the catheter compared with a position below the catheter (0.33 µl/min: 38 ± 3% KHB only and 18 ± 3% KHB-dextran 70, P < 0.001; 1.33 µl/min: 13 ± 2% KHB only and 9 ± 2% KHB-dextran 70, P < 0.001; and 2.66 µl/min: 7 ± 2% KHB only and 9 ± 3% KHB-dextran 70, P < 0.05). The concentrations of glucose, lactate, glycerol, and urea in dialysate did not differ significantly between the different positions of the microvial (n = 12 catheters) (Figs. 2 and 3A).
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In Vitro Experiments: Comparison of the Two Different Perfusion Fluids
The sample volumes (Fig. 1) were significantly smaller in the catheters perfused without dextran 70, compared with those with 40 g/l of dextran 70, at both positions of the microvial (0.33 µl/min: 50 ± 3% above and 34 ± 2% below, P < 0.001; 1.33 µl/min: 18 ± 2% above and 15 ± 1% below, P < 0.001; and 2.66 µl/min: 11 ± 1% above and 12 ± 3% below, P < 0.001).The concentration of glucose in dialysate was significantly higher in catheters perfused without a colloid, compared with catheters perfused with a colloid, when the perfusion flow rate was 0.33 µl/min (4.2 ± 0.8%, P < 0.05). At the other perfusion flow rates and as well as for lactate, glycerol and urea the concentrations did not differ significantly between the different perfusion fluids (Figs. 2 and 3B).
In Vivo Experiments: Comparison of the Different Positions of the Outlet Tubing
The volume achieved (Fig. 4) was significantly smaller when the microvial was placed above the microdialysis catheter compared with a position below the catheter (46 ± 5% KHB only and 8 ± 0.5% KHB-dextran 70 at 0.33 µl/min, P < 0.001; 17 ± 1% KHB only and 5 ± 1% KHB-dextran 70 at 0.66 µl/min, P < 0.001; and 9 ± 1% KHB only and 3 ± 0.5% KHB-dextran 70 at 1.33 µl/min, P < 0.001). This was accompanied by a significantly higher lactate concentration at the perfusion flow rate of 0.33 µl/min in the above position (9 ± 2%, P < 0.001), whereas the lactate concentration at the other flow rates did not differ. The other metabolites were unaffected by the changes in microvial position (Figs. 5 and 6A).
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In Vivo Experiments: Comparison of the Two Different Perfusion Fluids
At all perfusion flow rates and all positions, the volume achieved (Fig. 4) was significantly smaller from the catheter perfused without a colloid compared with the catheters perfused with a colloid (0.33 µl/min: 59 ± 4% above and 31 ± 2% below, P < 0.001; 0.66 µl/min: 24 ± 1% above and 13 ± 2% below, P < 0.001; and 1.33 µl/min: 14 ± 1% above and 8 ± 1% below, P < 0.001). There was a significant interaction at all perfusion flow rates (P < 0.05) between volume achieved and position of outflow tubing, indicating a larger difference between the perfusion fluids in the above position than in the below position (Fig. 4).The concentration of glucose in the catheters perfused without a colloid was found to be significantly higher than the catheters perfused with a colloid when the perfusion flow rate was 0.33 µl/min (28 ± 5% at 0.33 µl/min above, 18 ± 4% at 0.33 µl/min below, P < 0.001). The glucose concentration did not differ at the other perfusion flow rates or positions, although there was a tendency toward higher concentrations when the perfusion fluid contained no colloid at 1.33 µl/min (32 ± 8%, P = 0.1) (Figs. 5 and 6B).
There was no significant difference in lactate, glycerol, or urea concentrations between the different perfusion solutions. The lactate concentration at the perfusion flow rate of 1.33 µl/min had a tendency toward higher concentration when perfused without a colloid (24 ± 6%, P = 0.07) (Fig. 5).
When the perfusion flow rate was 0.33 µl/min, the glucose, glycerol, and urea concentrations were significantly reduced over time (Fig. 5).
In Vivo Experiments: Comparison of the Two Different Perfusion Fluids at Perfusion Flow Rate of 0.16 µl/min Under Conditions of Fluid Balance Achieved Either by a Colloid or by Minimal Hydrostatic Back Pressure, Respectively
Although the volume achieved (Fig. 7) tended to be lower in the catheters perfused without a colloid compared with the catheters perfused with a colloid, the ANOVA detected no significant difference. The metabolite concentrations did not differ significantly between the different perfusion fluids (Figs. 6C and 8). The glycerol and urea concentrations were significantly reduced over time (Fig. 8).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The effects of net fluid transport across a microdialysis membrane have only received attention in a few previous investigations. It is caused by an imbalance between the hydrostatic and/or osmotic pressures over the membrane, occurring preferentially with a large membrane area and when low perfusion flows are used, since the collection times of samples are extended compared with at higher perfusion flows. In previous investigations, no significant perfusate loss was observed when microdialysis catheters with small (3-10 mm long) dialysis membranes were used in vitro (7) or in experimental animals (3) at perfusion flows of 1-10 µl/min. However, when larger (20-30 mm long) dialysis membranes were used in muscle of experimental animals (3) or in humans (12, 14), the loss of perfusate was significant at perfusion flows of 1-4 µl/min but small relative to the perfused volume. With very low perfusion flows and a 30-mm-long dialysis membrane in skeletal muscle, we found that the loss of perfusate was markedly increased (13). With no colloid added to the perfusate, 50% of the perfused volume was lost at 0.33 µl/min and 80% was lost at 0.16 µl/min.
In this study, we describe the influence of variations in both colloid osmotic and hydrostatic pressures on the net fluid transport across a microdialysis catheter with a 30-mm-long dialysis membrane. Loss of perfusate was counteracted by the addition of dextran 70 to the microdialysis perfusate, as previously used in several microdialysis experiments (6, 12, 13), or, alternatively, by minimizing hydrostatic back pressure on the dialysis membrane by lowering the outlet tubing. With the commercially available microdialysis catheters used, the outflow tubing was not long enough to completely prevent the fluid loss in vivo at the perfusion flow rate of 0.33 µl/min when the outlet tubing was maximally lowered. This was rectified, however, in an additional experiment with a perfusion flow rate of 0.16 µl/min in which the outflow tubing from the catheters perfused with KHB only was extended with a 35-cm-long plastic tubing.
To our knowledge, there are no published data on how fluid shifts across a microdialysis membrane affect concentrations of metabolites in dialysate. We found that, in vivo, at 0.33 µl/min flow rate, glucose concentrations were substantially lower when 40 g/l of dextran 70 was included in the perfusate. There was a tendency in the same direction also at the other perfusion flow rates. This difference in glucose concentration, although smaller in magnitude, was also observed during microdialysis in vitro at 0.33 µl/min flow rate. In vivo, lactate, glycerol, and urea concentrations were not significantly affected by the inclusion of dextran 70 in the perfusion medium, although there was a tendency to a corresponding difference also in these metabolites, especially for lactate at perfusion flow rate of 1.33 µl/min (24%, P < 0.07). On the contrary, fluid shifts caused by changing hydrostatic pressure did not result in consistent changes in dialysate concentrations of the metabolites measured, and only the lactate concentration (at 0.33 µl/min flow rate) was significantly increased when fluid loss occurred.
When fluid is lost from the microdialysis catheter into the tissue, this results in a lowered effective perfusion flow through the catheter. Conversely, by overcompensating the fluid loss across the microdialysis catheter, e.g., by the addition of a colloid to the perfusate, the effective perfusion flow through the catheter will be increased. The resulting differences in perfusion flow rate will, with everything else equal, change the recovery and therefore the concentrations of metabolites in the collected microdialysis samples. An increased perfusion flow rate will result in decreased substance concentrations as long as flow rate is not low enough to ensure complete equilibration between the interstitial and perfusion fluids. The equilibration flow rate is lower for glucose than for lactate, glycerol, and urea, due to the larger molecular size of glucose. It has previously been shown that, with the presently used microdialysis catheters, the glucose concentration in microdialysis samples from skeletal muscle does not equilibrate completely until the perfusion flow rate is as low as 0.16 µl/min, whereas lactate, glycerol, and urea concentrations equilibrate with a perfusion flow rate of 0.33 µl/min (12). The lower diffusivity of glucose is the likely reason why differences in fluid balance were shown to have a greater impact on the concentration of glucose than on the other metabolites. The recovery of glucose would be expected to change also with changes in hydrostatic pressure. That this was not detected in the present study could, however, be partly explained by the fact that the differences in effective flow rate were smaller.
With this background, we believe that the decreased substance concentrations in microdialysate samples, where a colloid had been included to counteract fluid loss, are due to effects on the effective perfusion flow and not to an influence of dextran 70 itself. This notion is supported by the experiments with a low perfusion flow rate, 0.16 µl/min, for which it is known that full substance equilibration between interstitial and perfusion fluids is obtained (12). At 0.16 µl/min, the glucose concentration was the same irrespective of whether the fluid loss had been counteracted by colloid inclusion or by lowering of outlet tubing. In these experiments, a dextran 70 concentration of 30 g/l (one subject) or 35 g/l (two subjects) was used. The reason for lowering the dextran concentration in the experiment at 0.16 µl/min was to avoid the slight gain of fluid seen in the previous part of this study when a dextran 70 concentration of 40 g/l was used. A very small net gain of fluid was seen even though the concentration of dextran 70 was 30 g/l. Therefore, under the present conditions, the concentration of dextran 70 should be clearly lower than 40 g/l (as used in the main part of this study) and probably also lower than 36.8 g/l [as was concluded in a previous study (13)] to achieve fluid balance with microdialysis at low perfusion flow rates. We do not, however, believe that the slightly higher volume achieved, and therefore also effective perfusion flow, in the dextran 70 catheters vs. in the catheters with KHB only at 0.16 µl/min would have influenced substance concentrations. The reason is that small differences in the flow rate would not be important at flow rates that enable full equilibrium between interstitial and perfusion fluids (see previous page).
In conclusion, the present data show that both hydrostatic and osmotic pressures determine the net fluid transport across the dialysis membrane of a microdialysis catheter, both in vitro and in vivo in human skeletal muscle. Fluid balance could be achieved in the present study by adding a colloid (dextran 70) to the perfusate or by maximally lowering an extended outflow tubing. With 40 g/l of dextran 70 in the perfusion solution at a perfusion flow rate of 0.33 µl/min, substance concentrations tended to be lower than without dextran 70, a difference that was especially marked for glucose. The mechanism behind this difference is thought to be a higher effective perfusion flow rate when dextran 70 is added and that the recovery of glucose is lower than for the other metabolites. Glucose is therefore more affected by changes in flow rate at flow rates in which concentrations in the interstitial and perfusion fluids are not equilibrated. This study shows that fluid imbalances can have important implications for microdialysis results at low perfusion flow rates.
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ACKNOWLEDGEMENTS |
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We thank CMA-Microdialysis (Stockholm, Sweden) for collaboration and generous support.
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FOOTNOTES |
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This work was supported by grants from Swedish Medical Research Council (project 07917) and the Swedish National Center for Research in Sports. Financial support was also given by the Swedish Society for Medical Research and the Research Foundations of Karolinska Institute, Novo Nordisk, Magn. Bergvall, Clas Groschinskys Minnesfond, Lars Hiertas Minne, and Fredrik and Ingrid Thuring.
Address for reprint requests and other correspondence: J. Henriksson, Dept. of Physiology and Pharmacology, Karolinska Institute, S-171 77 Stockholm, Sweden (E-mail Jan.Henriksson{at}fyfa.ki.se).
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 28 September 2000; accepted in final form 6 September 2001.
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RESULTS
DISCUSSION
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