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1 Department of Physiology and Pharmacology, James Cook University of North Queensland, Townsville, Queensland, Australia 4811; and 2 Department of Biochemistry, Chang Gung College of Medicine and Technology, Kwei-san, Tao-yuan, Taiwan, Republic of China
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ABSTRACT |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Tissue spaces were determined in rat heart, liver, and skeletal muscle in vivo using isotopically labeled [14C]inulin. Tracer was injected into the jugular vein of pentobarbital-anesthetized male Sprague-Dawley rats. After a 30-min equilibration period, a blood sample was taken, and heart, liver, and gastrocnemius muscle were excised and immediately freeze clamped at liquid nitrogen temperatures. The extracellular inulin space was 0.209 ± 0.006 (n = 13), 0.203 ± 0.080 (n = 7), and 0.124 ± 0.006 (SE) ml/g wet wt tissue (n = 8) for heart, liver, and skeletal muscle, respectively. Total tissue water was 0.791 ± 0.005 (n = 9), 0.732 ± 0.002 (n = 9), and 0.755 ± 0.005 ml/g wet wt tissue (n = 10) for heart, liver, and skeletal muscle, respectively. Expressed as a percentage of total tissue water, the intracellular space was 73.6, 72.2, and 83.7% for heart, liver, and skeletal muscle, respectively. With use of 2,3-diphospho-D-glyceric acid as a vascular marker, the interstitial space was calculated by subtracting the counts in tissue due to whole blood from total tissue counts and dividing by plasma counts. The interstitial space was 18.8, 22.4, and 14.5% of total tissue water, with accompanying plasma spaces of 7.7, 5.3, and 1.8% for heart, liver, and gastrocnemius muscle, respectively. The tracer method used in this study provides a quantitative assessment of water distribution in tissues of nonnephrectomized rats that has applications for calculation of tissue ion and metabolite concentrations, gradients, and fluxes under normal and pathophysiological conditions.
extracellular space; inulin; intracellular space; muscle interstitial space; plasma space; 2,3-diphospho-D-glyceric acid
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INTRODUCTION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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THE DETERMINATION of extracellular and intracellular tissue spaces by volume (or weight) in animal tissues has a long history (13). Among the earliest work is that of Hermann who, in 1888, with the assistance of Langendorff, estimated the extracellular tissue space on frozen cross sections of frog sartorius to be 14.5% (13). It was not until some four decades later that different methodologies were developed. In 1934, Fenn (13) claimed that if all the chloride of frog muscle was confined in 14.7% of the total muscle, it would have a concentration equal to that in plasma. This "chloride space" was taken as a measure of the extracellular space (ECS) on the assumption that all the chloride is contained in this compartment and not in the tissue cells
![ECS (%) = <FR><NU>[Cl<SUP>−</SUP>]<SUB>ti</SUB></NU><DE>[Cl<SUP>−</SUP>]<SUB>pl</SUB></DE></FR> × 100](/content/vol275/issue5/fulltext/R1530/img001.gif)
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(1) |
]ti
and
[Cl]pl
represent chloride concentration in tissue and plasma, respectively.
With use of similar criteria, the "sodium space" has also been
used by some investigators to estimate the ECS. Mannery and Hastings
(25), using chloride and sodium measurements, found that the magnitude
of the ECS in vivo varied from ~15 to 47% [percent total
tissue water (TTW) by volume] for heart, liver, skeletal muscle,
brain, and kidney of rat and rabbit. Shortly thereafter, it was
concluded (5, 12, 24, 40) that the fundamental assumption that all the chloride (or sodium) was extracellular was questionable and that alternative markers are required. Some of the markers subsequently tried included tracer amounts of uncharged, low-molecular-weight compounds such as inulin (18), mannitol (10), sorbitol (3, 27), sucrose
(6), and raffinose (19). In addition, thiocyanate, sulfate,
thiosulfate, EDTA, and polyethylene glycol have been found to be useful
(21, 22, 32). More recently, phenylphosphonic acid,
59Co (in vitro systems), and
N-methyl-D-alanine
have been used as extracellular markers in different magnetic resonance
imaging procedures (1, 4, 39). For ECS in brain, ionophoresis of
tetramethylammonium combined with ion-selective microelectrodes has
also been found useful (7).
Despite the increasing number of ECS markers available, problems of accuracy and precision with literature values remain; expressed as percent TTW in vivo, ECS ranges from 20 to 29% for rat heart (22, 31, 32), from 14 to 28% for liver (41), and from 6 to 19% for whole gastrocnemius skeletal muscle (21, 22, 35). The difficulty is deciding which value best represents the in vivo state. The aim of this study is to examine tissue water spaces in the heart, liver, and gastrocnemius muscle in vivo in nonnephrectomized rats using [14C]inulin as extracellular marker. Inulin was chosen in tracer amounts because of its demonstrated nontoxicity (6, 23), its large size (mol wt 5,000), which prevents penetration into cells to any appreciable extent (6, 23), and its slow excretion rate compared with the rate at which it distributes in the extracellular phase (6, 20, 21, 23). In addition to measuring ECS, we calculated the interstitial space using 2,3-diphospho-D-glyceric acid (2,3-DPG) as an intrinsic vascular marker, and the strengths and limitations of this method are discussed. It cannot be overemphasized that this study deals with in vivo spaces, not in vitro spaces of perfused organs.
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MATERIALS AND METHODS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Definitions
Extracellular water space. Extracellular water space is the space outside tissue cells and comprises plasma fluid, interstitial fluid (including lymph), and transcellular fluid spaces (secretions from epithelial cells, including cerebrospinal fluid in the brain and exocrine secretions in the gut) (8).
Plasma space. Plasma space is the volume occupied by the plasma in a given weight of tissue or expressed as percent TTW.
Interstitial water space. Interstitial fluid is thought to be an ultrafiltrate of plasma and is distributed around the exchange vessels and tissue cells. Part of the interstitial volume is occupied by a matrix of collagen and associated structures (8).
Intracellular space. Intracellular space (ICS) is TTW space minus the extracellular water space; it is expressed as a volume per given weight of tissue or as percent TTW.
Total tissue whole blood space. Total tissue whole blood space is the amount of whole blood in a given amount of tissue.
TTW space. TTW is total volume or weight of water measured in a given amount of tissue (usually expressed as a percent volume of wet weight tissue).
Enzymes and Chemicals
[Carboxyl-14C]inulin (mol wt 5,000, 4.36 µCi/mg) was purchased from ICN Pharmaceuticals as the crystalline solid prepared by the cyanohydrin synthesis method and stored at
20°C (purity 99% by HPLC). Radioactive inulin was
used between 1 wk and 2 mo of date of purchase to ensure no loss of
purity. On the day of experimentation, solid inulin was weighed and
dissolved in 1.0 ml of 0.9% saline. Triethanolamine buffer for the
2,3-DPG assay was purchased from Sigma Chemical. 3-Phosphoglycerate
kinase (EC 2.7.2.3) from yeast, triosephosphate isomerase (EC 5.3.1.1),
glyceraldehyde-3-phosphate dehydrogenase (EC 1.2.1.12), and
glycerol-3-phosphate dehydrogenase (EC 1.1.1.8) from rabbit muscle were
purchased as the crystalline suspension in 3.2 M ammonium sulfate
solution from Boehringer Mannheim. Phosphoglyceromutase (PGlyM, EC
5.4.2.1) from rabbit muscle was purchased as the 2.4 M ammonium sulfate
suspension from Sigma Chemical (1 U converts 1 µmol of
3-phosphoglyceric acid to 2-phosphoglyceric acid per minute at pH 7.6 at 25°C in the presence of 2,3-DPG). 2-Phosphoglycollate
(trimonocyclohexylammonium salt), an activator of phosphatase side
activity of PGlyM, was purchased from Sigma Chemical. NADH was
purchased as the amorphous disodium salt (grade 1) from Boehringer
Mannheim. 2,3-DPG was obtained from Sigma Chemical. All other chemicals
were reagent grade. Disposable borosilicate Kimble glass culture tubes
(10 × 75 mm) for fluorometry (Lab Supplies, Townsville) were used in the enzyme assay.
Experimental Procedure
Animal preparation. Adult male Sprague-Dawley rats (250 and 300 g; Animal Services Centre, Canning Vale, Western Australia) were given free access to food and water. At the time of experimentation, fed rats were anesthetized with pentobarbital sodium (60 mg/kg ip) and placed in a supine position on a heating pad (38°C) pending surgery. The right carotid artery and jugular vein were cannulated according to the procedures described in Dobson et al. (9). A sample (~300 µl) of arterial blood was removed, and the physiological status of the animal (blood gases, pH, monovalent electrolytes) was assessed using a Corning 368 analyzer. The remaining portion of blood was spun for the hematocrit, and an aliquot was kept (100 µl) for measuring whole blood 2,3-DPG concentration.
Tracer equilibration times. Tracer equilibration times were determined by a single injection of label (20 µCi in 0.5 ml saline) into the jugular vein of the rat and sampling from the artery every 5-10 min. A typical time course is shown in Fig. 1. Isotopic equilibrium was approached in blood within 30 min, indicating that the counts in plasma are in isotopic equilibrium with the extracellular fluid in tissue. All ECS measurements reported in this study were performed between 30 and 40 min.
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Single injection of label. A single bolus of [14C]inulin (20 µCi) in 0.5 ml of saline was injected into the jugular vein of the animal and washed with 0.2 ml of saline (~3% total blood volume). After 30-40 min of equilibration, 1.0 ml of whole blood was taken from the carotid artery into a heparinized syringe (100 U/ml), and heart (n = 5), liver (n = 6), and whole gastrocnemius muscle (n = 5) were immediately excised and freeze clamped at liquid nitrogen temperatures. For heart and liver, the chest and abdomen were opened and, first, the heart was excised and freeze clamped within 5 s and, then, the liver within 5 s. For the skeletal muscle study, separate animals were used, and the skin over the gastrocnemius muscle was shaved before tracer injection. After 30-40 min the muscle was exposed, excised, and freeze clamped within 7 s. In this group of rats the heart and liver were removed as described above. The inulin space measurements for heart and liver were not statistically different between the two protocols, and the data were combined.
After tissue sampling, the blood was mixed and an aliquot (100 µl) was kept for acid extraction and counting. The remainder was centrifuged at 11,500 rpm for 2 min (20°C), and 100 µl of plasma also were removed for acid extraction and counting (see below). The tissue samples were pulverized to a fine powder under liquid nitrogen, connective tissue was removed, and the powder was kept at80°C until use. The powdered tissue was used to determine total tissue counts of label, wet-to-dry weight ratio, and total tissue
2,3-DPG content. TTW (defined as g water/g wet wt) was determined by
the difference between wet and dry weight after tissue was dried for 48 h at 80°C. About 0.2 g wet wt of powdered tissue was added to a
previously weighed tube and dried in an oven to constant weight.
Radioactive counting.
Whole blood, plasma, and frozen powdered tissue (0.1 g of
each, 80°C) were added to separate tubes containing 1.0 ml
of ice-cold 3.6% perchloric acid (PCA). The tissues were homogenized
for 20 s (3 times) using a Heidldolf Diax 600 tissue homogenizer. The homogenates were centrifuged (11,500 rpm, 1 min), and the supernatant was removed and used directly for counting or stored overnight at
80°C. Whole blood, plasma, and tissue (0.2 ml of each) acid extracts were added to separate counting vials containing 10 ml of
Fluor (Organic Counting Scintillant, Amersham), thoroughly mixed, and
counted for beta activity in a Wallac 1410 liquid scintillation counter
(Pharmacia). The dilution factor for each tissue, blood, and plasma
sample was calculated using the following equation
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(2) |
Tissue and blood preparation for 2,3-DPG measurement. Frozen tissue (~200 mg) was homogenized in four volumes of ice-cold 3.6% PCA in the presence of glass beads using a Biospec mini-bead beater. The homogenate was centrifuged (11,500 rpm, 1.0 min), a known volume of supernatant was removed, and an aliquot of KHCO3 (0.3 M and 2.0 M stocks) was mixed with the supernatant to neutralize it (pH 6-7). To substantiate that 2,3-DPG does not exist in tissue cells, rat hearts (n = 4) were perfused with modified Krebs-Henseleit solution (9) for 2 h, and 2,3-DPG was measured on tissue extracts.
Fluorometric measurement of 2,3-DPG. Tissue and blood extracts were analyzed for 2,3-DPG by adapting the spectrophotometric assay of Michal (26) to fluorometry. 2,3-DPG was assayed in 32 mM triethanolamine buffer (pH 7.6), 0.015 mM NADH, 5.0 mM MgCl2, 0.65 mM Na-ATP, 2.5 mM mercaptoethanol, 3.5 mM Na-EDTA, and 0.01% BSA. This reagent contained PGlyM (0.13 U/ml), 3-phosphoglycerate kinase (11 U/ml), triosephosphate isomerase (11 U/ml), glyceraldehyde-3-phosphate dehydrogenase (0.2 U/ml), and glycerol-3-phosphate dehydrogenase (1.0 U/ml). Reagent (1.0 ml) was added to the fluorometric tubes and controls, and standards and samples were added. After 5-10 min the fluorometric readings became stable as the small quantity of PGlyM present converted interfering 2-phosphoglyceric acid to 3-phosphoglyceric acid. No loss of 2,3-DPG in standards occurred during this time. Fluorometric readings were then taken, and the 2,3-DPG assay commenced after the addition of a known volume of a mixture of PGlyM (9.0 U/ml) and phosphoglycollate (0.2 mM) in the final reaction soup. The reaction was complete in 20 min. NADH oxidation of blood and tissues was monitored using a Farrand Radio-2 filter fluorometer (Optical Technology Devices, Elmsford, NY) against known standards. 2,3-DPG standards were determined using a UV-VIS GBC spectrophotometer, where 2 mol of NADH were oxidized per mole of 2,3-DPG at 340-nm and 1.0-cm light path.
Calculations
ECS was calculated from the distribution of inulin after tracer equilibration as follows
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(3) |
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(4) |
The interstitial space (g/g wet wt tissue) was calculated by first measuring the whole blood contamination in each tissue (see below) subtracting these counts from the total tissue counts as follows
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(5) |
Plasma space was subsequently calculated by subtracting the interstitial space (Eq. 5) from the ECS (Eq. 3) as follows
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(6) |
Statistics
Values are means ± SE. Statistical comparisons are given by one- and two-way ANOVAs, with significance at P < 0.05.| |
RESULTS |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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Arterial blood gas, pH, and the monovalent electrolytes from anesthetized rats before the experiment are presented in Table 1. Animals were rejected from the experiment if hematocrit was <30%, arterial PO2 was <60 mmHg, and/or PCO2 was >50 mmHg.
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[14C]inulin counts in tissue and plasma (dpm/g wet wt) are presented in Table 2. With use of these data, the ECS was calculated from Eq. 3 and the ICS from Eq. 4. The results are expressed as grams per gram wet weight tissue or as percent TTW. Tissue and whole blood contents of 2,3-DPG (µmol/g wet wt), tissue whole blood space (g/g wet wt), and total inulin counts in whole blood (dpm/g wet wt) are presented in Table 3. Tissue whole blood spaces (g/g wet wt) were estimated from the tissue-to-whole blood ratio of 2,3-DPG. Expressed as a percentage per gram wet weight, tissue whole blood space was 10.6, 6.6, and 2.3% for heart, liver, and skeletal muscle in vivo. With knowledge of the amount of whole blood in each tissue and the counts of [14C]inulin in whole blood, the counts due to whole blood in each respective tissue were calculated. This value was then substituted into Eq. 5 to calculate interstitial spaces. From Eq. 6, the plasma space was then calculated for each of the three tissues (Table 4).
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DISCUSSION |
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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The primary aim of the present study was to examine the tissue spaces in heart, liver, and skeletal muscle of the rat in vivo using a single injection of [14C]inulin, with particular attention to equilibration times, injection sites, and freeze-clamp sampling procedures. Expressed as TTW, the in vivo ECS for rat heart, liver, and gastrocnemius skeletal muscle was 26.4, 27.8, and 16.3%, respectively, with ICS of 73.6, 72.2, and 83.7% (Table 2). For comparative purposes we have tabulated extracellular values in the literature for the rat, rabbit, and dog heart, liver, and skeletal muscle in vivo (expressed as %TTW, Table 5).
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It is apparent from Table 5 that there is wide variability for any given tissue using four common tracers (inulin, mannitol, sucrose, and sulfate). As mentioned in the introduction, the extracellular values range from 20 to 29% for heart, from 14 to 28% for liver, and from 6 to 19% for gastrocnemius muscle (4, 7, 15, 21, 22, 28, 31, 32, 36, 42). What are the possible reasons for this variability in ECS values in vivo? Part of the diversity appears to relate to whether the animal was nephrectomized or intact. In general, there has been a trend toward lower tissue ECS values with renal ligation, and these values should not be used to represent the intact animal. For example, Williams and Woodbury (42) found a decrease from 25.7 to 14.3% in the inulin space in rat liver as a result of nephrectomy. Glasby (15) also reported a lower value of 22.4% in dog liver accompanying nephrectomy but, unfortunately, did not report control values. With respect to the heart, Polimeni (31) calculated lower values for ECS as a result of nephrectomy (21.7% for sucrose and 24.7% for sulfate). More recently, Clarke et al. (4) reported a mannitol space of 22.9% in rat heart from nephrectomized animals (Table 5). A similar trend has been observed in skeletal muscle; Sreter and Woo (36) reported an inulin space of 10% for rat gastrocnemius, Nichols et al. (28) an inulin space of 14.1% in rabbit quadriceps muscle, and, more recently, Poole-Wilson and Cameron (32) an inulin value of 11.2% for rabbit quadriceps muscle. We conclude, therefore, that part of the reason for our higher inulin spaces for heart, liver, and skeletal muscle may be our experiments on renally intact rats.
Other possible reasons for the literature variability may relate to animal health and hydration status (hematocrit, blood gases, and blood electrolytes), animal preparation (intact or nephrectomized), tracer type (inulin, mannitol, sucrose, and sulfate), injection site (intravenous, intraperitoneal, or tail vein), tracer equilibration times (minutes up to 12 h), and blood sampling (indwelling cannulas, heart puncture, or tail bleeding) and tissue sampling procedures (blot tissue, slow freezing, biopsy, and rapid freeze clamping at liquid nitrogen temperatures). Addressing these issues experimentally was beyond the scope of the present study; however, we employed the following steps to ensure that our values were most representative of the in vivo state: 1) physiological status of intact rats was monitored, 2) a single bolus intravenous tracer injection was followed by a 0.3-ml saline wash, then the cannula was sealed and no longer used, 3) isotopic equilibrium of tracer in blood plasma and sampled blood and tissue was determined after 30 min, 4) all tissues were rapidly excised and freeze clamped (within seconds) to prevent major ischemic, hypoxia-induced water and ion shifts (17, 34), and 5) all freeze-clamped tissue was ground to a fine powder under liquid nitrogen, and, where necessary, connective tissue was removed.
In Vivo Interstitial and Plasma Spaces
To our knowledge, no study has employed 2,3-DPG as an intrinsic vascular marker to calculate the interstitial space in vivo (Eq. 4). By subtracting the interstitial space from the inulin space (ECS), the plasma space was calculated. With use of this method, the interstitial space was found to be 18.8, 22.4, and 14.5% TTW for heart, liver, and gastrocnemius muscle, respectively, with accompanying vascular spaces of 7.7, 5.3, and 1.8%. Our survey of the literature shows our in vivo values for the interstitial and plasma spaces to be in close agreement with those in heart using other methods (2, 30, 37). The interstitial space for in vivo cat heart was 21.4% (30). In contrast, we could find no data in mammalian liver or skeletal muscle in vivo. With respect to plasma spaces, the albumin space (extravascular ECS) ranges from 6 to 12% for heart (2) and from 3 to 7% for skeletal muscle for other animals (2, 29, 37).Strengths and Limitations of Using 2,3-DPG as Blood Space Marker
2,3-DPG was used to calculate the interstitial space on the basis of the following assumptions: 1) the metabolite is a constituent of red blood cells only and is not present in heart, liver, or skeletal muscle cells, and 2) the tissue hematocrit is equal to the hematocrit measured in arterial blood. Assumption 1, that 2,3-DPG is not present in the tissue cells, has been demonstrated earlier by Reddy and Burns (33) and Tauler and colleagues (38). Both studies report negligible 2,3-DPG in rat heart myocytes (2 nmol/g tissue), liver hepatocytes (29 nmol/g tissue), and skeletal muscle cells (3.3 nmol/g tissue) compared with 3,800 nmol/g in whole blood. We confirmed this finding in the isolated perfused heart. The 2,3-DPG on freeze-clamped heart after 2 h of blood washout using Krebs-Henseleit buffer (pH 7.4) containing 10 mM glucose was <1.0 nmol/g wet wt (n = 4), which is below the detection limits of our fluorometric procedure. This value is over three orders of magnitude lower than 2,3-DPG in whole blood (Table 3).With regard to assumption 2, because we are freeze clamping whole tissue (including blood in the large vessels, chambers, sinusoids, and microvessels), we believe this method is valid on the basis of conservation of mass. Because the entire perfusion field of our tissues is served by an artery, the phenomenon of plasma skimming and tissue hematocrit becomes less important. Blood that enters a tissue might well be partitioned at the level of the microcirculation, but at the level of whole tissue there is no effect, and organ hematocrit equals arterial hematocrit. By contrast, and not relevant to our study, in those tissues where large vessels and blood spaces have been excluded, the ratio of the tissue hematocrit to arterial blood hematocrit using radioactive iron and iodine has been shown to be 0.55, 1.02, and 0.53 for dog heart, liver, and skeletal muscle (14). More recently, a tissue-to-arterial blood hematocrit of 0.65 was calculated using the same markers in the microvasculature of the rat heart (11, 43). It must be emphasized that in our study all the large vessels and blood spaces in heart, liver, and skeletal muscle were intact.
Perspectives
This study measured in vivo ECS for rat heart, liver, and skeletal muscle of 26.4, 27.8, and 16.3% TTW, respectively. We showed from a literature survey that our values were higher than most published values, and we concluded that they are more representative of the in vivo state for the intact rat. Part of the reason for the higher values was the nonnephrectomized state of the animal and other methodological considerations. With use of 2,3-DPG as a marker of blood volume, the interstitial space was calculated to be 18.8, 22.4, and 14.5% TTW for heart, liver, and gastrocnemius muscle, with accompanying plasma spaces of 7.7, 5.3, and 1.8%, respectively. We further concluded from our study that using one extracellular tracer and tissue and whole blood 2,3-DPG contents provides a simple and comprehensive way to estimate extracellular, interstitial, and plasma spaces in vivo, which could be used to determine the relative water shifts in the various compartments during pathophysiological states such as hypoxia, ischemia, hypertrophy, reperfusion injury, and aging.| |
ACKNOWLEDGEMENTS |
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The authors thank Prof. Ray Olsson for commenting on the use of 2,3-DPG as a blood marker.
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FOOTNOTES |
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This study was supported by National Heart Foundation Grant G96B4547 and Australian Research Large Council Grants AO9701053 (large) and 93242.2827 (small).
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. §1734 solely to indicate this fact.
Address for reprint requests: G. P. Dobson, Dept. of Physiology and Pharmacology, James Cook University of North Queensland, Townsville, Queensland, Australia 4811.
Received 31 March 1998; accepted in final form 19 June 1998.
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Top
Abstract
Introduction
Materials & Methods
Results
Discussion
References
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