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Am J Physiol Heart Circ Physiol 285: H1980-H1985, 2003. First published July 3, 2003; doi:10.1152/ajpheart.00322.2002
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Oxygen tension distribution in postcapillary venules in resting skeletal muscle

Darin J. Saltzman, Andras Toth, Amy G. Tsai, Marcos Intaglietta, and Paul C. Johnson

Department of Bioengineering, University of California-San Diego, La Jolla, California 92093-0412

Submitted 15 April 2002 ; accepted in final form 30 June 2003


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 REFERENCES
 
We tested the hypothesis that blood flow is distributed among capillary networks in resting skeletal muscle in such a manner as to maintain uniform end-capillary PO2. Oxygen tension in venules draining two to five capillaries was obtained by using the phosphorescence decay methodology in rat spinotrapezius muscle. For 64 postcapillary venules among 18 networks in 10 animals, the mean PO2 was 30.1 Torr (range, 9.7–43.5 Torr) with a coefficient of variation (CV; standard deviation/mean) of 0.26. Oxygen levels of postcapillary venules within a single network or single animal, however, displayed a much smaller CV (0.064 and 0.094, respectively). By comparison, the CV of blood flow in 57 postcapillary venules of 17 networks in 9 animals was 1.27 with a mean flow of 0.011 ± 0.014 nl/s and a range of 3.7 x 10–4 to 6.5 x 10–2 nl/s. Blood flow of postcapillary venules within single networks displayed a lower CV (mean, 0.51), whereas that in individual animals was 0.78. Results indicate that among venular networks, heterogeneity of oxygen tension is less than that of blood flow and within venular networks the heterogeneity of oxygen tension is much less than that of blood flow. In addition, postcapillary PO2 was independent of flow among venules in which both were measured. Results of this study may be attributable to three factors: 1) O2 diffusion between adjacent capillaries and venules, 2) structural remodeling in regions of lower PO2, and 3) O2-dependent local control mechanisms.

coefficient of variation

PREVIOUS INVESTIGATIONS HAVE revealed a substantial degree of spatial heterogeneity of blood flow indicated by a relatively large coefficient of variation (CV), defined as standard deviation/mean, among similar vessels in the microcirculation (6, 19). The spatial heterogeneity in capillary networks is typically in the range of 0.40 to 0.90 (19). In the cat sartorius muscle, the CV of volume flow was 0.63 in both fifth- and sixth-order venules (10), whereas in arterioles values of ~1.0 were seen (3). One possible explanation for this spatial variability in flow is that it relates to the oxygen requirements of the tissue region supplied. It is possible that local tissue regions with higher oxygen consumption are served by vessels with higher blood flow, thereby providing a balance between oxygen supply and oxygen demand. This concept has drawn support from evidence that flow heterogeneity in arterioles may be related, in part, to differences in local oxygen demand (21) and that flow heterogeneity within an isolated perfused muscle might also reflect local differences in oxygen consumption (32). If this is the case, then tissue and blood oxygen levels in the region of venous capillaries and postcapillary venules should be relatively uniform, despite differences in blood flow.

However, most of the data currently available do not support the suggestion that oxygen tension at the venous capillary and postcapillary level is relatively uniform. The CV of tissue PO2 in the vicinity of venous capillaries of cat sartorius muscle was 0.45 (3), and we calculate from data on rat intestinal muscle (4) that the CV in that tissue was 0.23. In studies on postcapillary venules of rat spinotrapezius muscle, values of 0.31 to 0.45 have been reported (20). Kerger et al. (14) obtained a value of 0.33 in larger venules in the hamster skinfold preparation of muscle. These CV values approach those cited above for blood flow. A possible explanation for this lack of uniformity in oxygen levels is that the studies pooled data from different animals and from different regions of the muscle in the same animal. In this case, the physiological state and experimental conditions may be sufficiently different among measurement sites so that local uniformity in PO2 was masked.

The purpose of this study was to examine, in localized vascular beds, the hypothesis that oxygen tension in postcapillary venules is significantly more uniform than blood flow. The study used the microvascular bed of rat spinotrapezius muscle for which considerable data on oxygen tension are already available for comparison and to aid in interpretation. The study also examined uniformity of oxygen tension and blood flow among different regions in the same muscle and among muscles of different animals.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 DISCLOSURES
 REFERENCES
 
Juvenile male Wistar rats (127 ± 13 g body wt) were prepared under pentobarbital sodium anesthesia (50 mg/kg) given intraperitoneally with additional booster doses given as needed. Animal use was in accord with guidelines of the National Institutes of Health and approved by the University of California San Diego Animal Subjects Committee. The femoral artery and vein were first cannulated, followed by cannulation of the trachea. The spinotrapezius muscle was prepared according to the procedure originally described by Gray (7). The muscle preparation was covered with Saran Wrap, and the animal preparation was placed on a heated platform with the muscle and the animal temperature held at 37°C and mounted on the stage of a special-purpose microscope as previously described (23, 29). The preparation was allowed to equilibrate for 30 min before microcirculatory measurements were obtained.

Systemic measurements. Arterial blood pressure and heart rate were monitored continuously from a catheter placed in the femoral artery by using a TNF-R Viggo pressure transducer and recorded on a four-channel strip-chart recorder (model 2600; Gould-Brush). A positive-pressure ventilation system was used when necessary to maintain stable arterial pressure and heart rate parameters.

In vivo microscope system. The system used in these experiments has been used previously in other studies (23, 29) and described in detail. In these studies, only that part of the system utilizing equipment to obtain oxygen measurements was used to obtain data. Matched Leitz objectives (magnification, x 20 and x 32; numerical aperture, 0.40) were used as an objective and as a condenser. Continuous video imaging and recording was implemented while the studies were being performed.

Oxygen measurement. Oxygen tension was determined by the phosphorescence decay technique (31) and described in detail by Shonat et al. (23) for microcirculatory studies. The method allowed for assessment of intravascular PO2 on the basis of oxygen-dependent quenching of phosphorescence emitted by albumin-bound metalloporphyrin complexes after pulsed light excitation. The method shows close agreement with the recessed microelectrode in vivo (5). The oxygen probe solution for injection consisted of 240 mg of palladium meso-tetra(4-carboxyphenyl)porphine (Porphyrin Products; Logan, UT) dissolved in 1 ml of DMSO (Sigma; St. Louis, MO) and added to 23 ml of physiological saline containing BSA (60 mg/ml, fraction V; ICN Biochemicals). It was buffered to a pH of 7.4 to provide a stock solution of 10 mg probe/ml. An amount sufficient to create a concentration of 15 mg/kg body wt was injected and allowed to equilibrate until a sufficient signal was present. The relationship between the rate of phosphorescence decay ({tau}) after excitation at an appropriate wavelength and oxygen tension is given by the Stern-Volmer equation: {tau}0/{tau} = 1 + kq ·{tau}0 · PO2, where kq is the quenching constant (325 Torr–l · s–l) and {tau}o and {tau} (µs) are the phosphorescence lifetimes in the absence of molecular oxygen and at a given PO2, respectively. The porphyrin complex was excited via a strobe light source at 50 Hz through an interference filter (532 ± 32 nm). The flash energy delivered to the tissue was 3.1 mJ/cm2. The emission wavelength (>560 nm), after being passed through a dichroic mirror and a long-pass collection filter (630 nm), was projected onto a red-sensitive photomultiplier tube. The photometric data were then collected by an acquisition system and fitted to the above equation using custom software (23). The area of excitation referred to the tissue was ~100 µm in diameter, whereas the area from which emission was collected was 8 µm in diameter. An average of 32 decay profiles was used to determine the oxygen tension. If the linear coefficient of determination (R2) was <0.85, the measurement was rejected. It was assumed that for coefficient values < 0.85, a low signal-to-noise ratio and/or an inhomogeneous PO2 sampling region existed.

Experimental protocol. In the first experimental series, data were obtained on PO2 in 64 venules among 18 networks in 10 animals. A microcirculatory region consisting of several collecting venules and their tributary postcapillary venules was selected for study on the basis of visibility of vessels of interest. The vascular network was recorded on videotape, and a preliminary map of the region was drawn by hand for reference during the experiment. A distal venular tree consisting of two to four postcapillary venules, each draining two to five capillaries in the region, was chosen for measurements. For each venular tree, oxygen tension was determined at each postcapillary venule in the manner described above. For the purpose of data analysis and comparisons, each venular tree was classified as an "individual network." In some instances, it was possible to study more than one venular tree in a single muscle preparation. Data obtained from two or more individual networks in one animal were classified as "individual animals." Measurements classified as "total population" consisted of all observations in all animals.

An example of an individual network is shown in Fig. 1 together with PO2 data obtained from this network. Because it was a concern that temporal variations in PO2 could occur, a preliminary data set such as that shown in Fig. 1 was taken at each site and repeated 5 min later. Data from sites that showed significant temporal changes were not retained. Measurements were taken at least 1 min apart. Approximately 1–2 min elapsed when moving to the next postcapillary venule to be measured. Approximately 20 min were required to obtain measurements within one network. It took ~40–60 min to complete measurements in two or more networks in one animal.



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  		Fig. 1. Schematic of a typical postcapillary venular network individual network (not to scale) of the rat spinotrapezius muscle. Blood flow and PO2 measurements were taken at areas denoted by solid circles (8 µm diameter). Typically, 3–4 sites were measured. These values were then averaged to obtain the coefficient of variation (CV).

 

In a second experimental series, data were obtained from nine animals on diameters and red blood cell velocities of 57 postcapillary venules in 17 individual networks. Velocity was determined with the dual-slit velocity technique (1, 33). Specifically, in this application, we used the Fiber Optic Photo Diode Pickup System (IPM; San Diego, CA) and the cross-correlation technique (model 102 B Velocity Tracker; IPM) (11). In eight networks, PO2 measurements were taken before velocity readings in the same vessels. Volume flow of blood was calculated from vessel diameters and dual-slit red blood cell velocity readings by using a correction factor of 1.3 to convert to mean velocities at diameters <10 µm and increasing by 0.06 per micrometer in the diameter range of 10–15 µm (12).

Statistics. Measured values were expressed in terms of mean, standard deviation, range, and CV defined as standard deviation/mean. Statistical analysis was performed by using a statistical software package (StatView; SAS, Cary, NC). The Mann-Whitney U-test (for nonparametric data) was used to test significance of PO2 values among individual networks. To determine the statistical significance of the correlation coefficient, an ANOVA table for the specified regression was generated. Statistical significance was assumed for P < 0.05.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 DISCLOSURES
 REFERENCES
 
Venular PO2. Data were obtained from 64 postcapillary venules in 18 networks from 10 animals. Mean PO2 values for each network are presented in ascending order of PO2 in Fig. 2. As is apparent in this figure, the standard deviation in venules of the individual networks was small, averaging 2.0 Torr. The CV was small in individual networks, averaging 0.064, and was inversely related to mean network PO2, as shown in Fig. 3. The R2 value is 0.31, indicating that 31% of the variation in CV may be related to the mean PO2. The slope is significantly different from zero, (P < 0.05).



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  		Fig. 2. Mean PO2 in postcapillary venules in individual venular tree-type networks (individual networks).

 


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  		Fig. 3. Comparison of the PO2 CV and mean PO2 values in individual networks. Individual networks that had lower oxygen tensions tended to have a higher CV. Slope is significantly different from zero (P < 0.05).

 

In six animals, we obtained data from more than one network as shown in Fig. 4. In animals A and B, three networks were studied, whereas in the remaining animals, data were obtained from two networks. Mean oxygen tension in these networks ranged from 24.1 to 38.0 Torr. In three animals, a significant difference was seen when mean PO2 values among networks were compared. The CV within animals was greater than for individual networks, averaging 0.94. When data from all collecting venules were pooled (total population), the mean PO2 was 30.1 ± 7.7 Torr. The CV for the total population was 0.26, which is greater by a factor of four than for individual networks and almost three times greater than for individual animals (Table 1).



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  		Fig. 4. Networks within a single muscle preparation in 6 animals. Each letter (A–F) signifies data obtained within 1 muscle preparation of 1 animal (individual animals). *Significant difference (P < 0.05) compared with networks within the same muscle.

 

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  		Table 1. Postcapillary venule Po2 and coefficient of variation

 

Venular volume flow. Data on volume flow were obtained in 57 venules (mean diameter 8.68 ± 1.90 µm and mean red blood cell velocity 0.19 ± 0.27 mm/s) in 17 individual networks from nine animals as summarized in Table 2. As with the PO2 data, there was a progressive increase in CV from individual networks (0.51) to individual animals (0.78) to the total population (1.27). The CV for volume flow was much greater than that of PO2 at all levels, being eightfold greater than PO2 in individual networks and individual animals and six times that of PO2 for the total population.


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  		Table 2. Postcapillary venule flow and coefficient of variation

 

In nine individual networks, flow and PO2 were measured in the same vessels (n = 23). In this study, no correlation was evident between PO2 and volume flow of individual vessels (R = 0.04) as shown in Fig. 5. Thus it appears that variations in PO2 levels among the collecting venules are unrelated to differences in volume flow.



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  		Fig. 5. Comparison of volume flow and mean PO2 values in postcapillary venules. Note the low R value indicating a lack of relationship between flow and PO2. The slope is not significantly different from zero.

 


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
DISCLOSURES
 REFERENCES
 
The principal finding in this study was the demonstration of a low heterogeneity of oxygen tension among postcapillary venules within individual networks. This heterogeneity was greater within individual animals and much greater for all animals. In addition, the degree of heterogeneity in venular PO2 was related to mean network PO2, being greater in networks with low PO2. Volume flow in venules was more heterogeneous than PO2 but showed the same trend of being lowest in individual networks and highest in the total population. Also, within a group of venules in which both oxygen tension and flow were measured, differences in PO2 were unrelated to differences in blood flow. Comparison of PO2 and volume flow data among individual networks, individual animals, and all animals suggests that pooling data from a group of animals may mask trends within individual networks and animals.

Previous studies of oxygen tension in venules. Mean values of PO2 ranging from 22.9 to 30.0 Torr have been reported for end-capillary values in hamster retractor muscle and collecting venules of hamster skinfold, respectively (25, 13, 14). A mean PO2 of 33 Torr in fourth-order venules (22 µm diameter) was obtained in the cremaster muscle of rats breathing 30% O2 in N2 (15). The mean value of PO2 we obtained in postcapillary (fifth order) venules (30.1 ± 7.7 Torr) is somewhat higher than previously reported from our laboratory, 17.7 ± 5.4 Torr by Richmond et al. (20) in 20-µm venules and 21 ± 9 Torr by Shonat et al. (22) for postcapillary venules in the same muscle but a different strain of rat (Sprague-Dawley) and maintenance anesthetic ({alpha}-choralose-urethane) than we used. The CV for all animals in those studies was 0.31 and 0.45, respectively, compared with our value of 0.26. However, whereas Shonat et al. (22) did not compare PO2 in fifth-order venules from the same network, they did examine consecutive orders of venules in the same network and found only small differences. Their finding is consistent with the present study and would not be expected if there were large differences in PO2 among postcapillary venules in the same network. They also observed substantial differences among networks in all orders of venules, which is consistent with our findings.

Heterogeneity of microcirculatory volume flow. Previous investigators have reported heterogeneity of volume flow and red blood cell flux at the microcirculatory level. The values we obtained for CV of volume flow in venules for all animals (1.27) is somewhat greater than that found by others for red blood cell velocity or flux in capillaries and volume flow in arterioles and venules (0.42–1.03) (3, 10, 19). There has not, to our knowledge, been a direct comparison previously of flow heterogeneity within and among networks and animals. In our study, the spatial variation in volume flow was lowest in individual networks, intermediate among venules in the same animal and highest in the total population (Table 2).

The lower variation in volume flow within individual networks could indicate that local flow regulatory mechanisms are involved. Sarelius (21) observed that local flow regulatory mechanisms tend to reduce the heterogeneity of flow among terminal arterioles. However, because, as discussed below, local metabolic requirements may vary, differences in flow rate are not unexpected in comparing venules in the same or different regions of one muscle. When comparing microcirculatory flow in muscles from different animals, a number of factors such as surgical preparation and anesthetic level could increase the variability and obscure underlying similarities.

Heterogeneity of venular PO2. Heterogeneity of venular PO2 was considerably less than that of volume flow, most strikingly within individual networks and individual animals, as is apparent from comparison of data in Tables 1 and 2. Within networks, this may be due, in part, to diffusion of oxygen among adjacent capillaries and venules. Because of the complexity of the venular network in the postcapillary region, it is not feasible to estimate this effect. However, the CV for individual animals was only 50% greater than that for individual networks, suggesting that factors other than diffusion must be involved. One such factor could be a matching of blood flow to oxygen consumption within localized regions. The spinotrapezius consists of different fiber types, which are reported in other muscles to have different oxygen consumption at rest (26) and differing degrees of capillary-fiber contact (27). Thus it is possible that some of the heterogeneity in flow within muscles is due to oxygen requirements of the different fiber types and would not be reflected in the PO2 of postcapillary venules. If the oxygen consumption in a region drained by a postcapillary venule is matched to volume flow in that region, then it would be expected that venular PO2 would not be a function of volume flow. This is, in fact, our finding as shown in Fig. 5, which adds support to this hypothesis. Our finding may not be representative of microcirculation in all muscles, because Swain and Pittman (28) found that oxyhemoglobin saturation in the hamster cremaster muscle was higher in venules with higher volume flow.

Microcirculatory flow and tissue oxygen levels. If local flow is matched to local metabolic requirements in our preparation, one underlying mechanism could be structural modification according to local oxygen levels, because there is evidence that angiogenesis is stimulated by low oxygen tension (8). This could set a lower limit on the PO2 in the capillary and venular network. A more precise adjustment of flow may be affected by arteriolar tone, which has been shown to be dependent on tissue oxygen levels in the vicinity of the arterioles and the capillary network (21). It has been reported that hemoglobin deoxygenation leads to release of ATP from the red blood cell (24), and it has been shown that ATP causes release from the venular endothelium of prostanoids that could diffuse to adjacent arterioles (10). Finally, there is evidence that a conducted vasodilator response from the capillary network to the arterioles is involved in the hyperemia of exercising muscle (2). Thus available data from other vascular beds suggest that there may be localized feedback mechanisms that would tend to maintain a constant PO2 among postcapillary venules despite wide differences in volume flow as shown in Fig. 5.

Possible contribution of nonmetabolic factors to heterogeneity. Despite the ample evidence cited above of oxygen-related mechanisms for flow regulation in the skeletal muscle microcirculation, we found a small but significantly greater heterogeneity of PO2 in networks having lower PO2 levels (Fig. 3). This appears to be inconsistent with a preeminent role for oxygen in local flow regulation, because, intuitively, one would expect lower, rather than greater, heterogeneity at low PO2 in this instance. However, other mechanisms of flow regulation unrelated to oxygen are also present in the microcirculation and may contribute to regulation of flow, especially in resting muscle. These mechanisms include neural regulation (17) and the myogenic response (18) as well as shear-stress-dependent release of endothelium-derived relaxing factor from the endothelium (16). It is possible that blood flow in regions in which PO2 is low is under greater influence of nonmetabolic factors. Consistent with this is the evidence that flow in capillary networks is more heterogeneous at low flow rates in resting muscle than when metabolic rate is increased during muscle contraction (30).

Heterogeneity in total population compared with individual networks and animals. As seen in Tables 1 and 2, heterogeneity was greater in the total population than in individual networks and animals especially with respect to oxygen tension. Whether this increased heterogeneity is due to day-to-day differences in muscle surgical preparation, variability in conditions of the study, or intrinsic differences among the animals themselves is not clear. Because the pH of venular blood is lower than systemic levels (15), the relationship between PO2 and hemoglobin oxygen saturation may be subject to local metabolic conditions. Whatever the reason for the differences among animals, this finding suggests that pooled data from a number of animals tend to overestimate the variability of oxygen tension and volume flow in a local venular network.

In conclusion, this study demonstrates that heterogeneity of venular PO2 in the rat spinotrapezius muscle is lower in localized networks than in individual animals and considerably lower than in the total population of animals. Heterogeneity of venular PO2 is also considerably less than that of blood flow at all levels. The lower heterogeneity of PO2 compared with volume flow may reflect the effects of diffusion among adjacent vessels as well as mechanisms that would match blood flow to oxygen demand of the tissues in the short term and in the long term. Our finding that PO2 is unrelated to volume flow among venules in which both are measured is consistent with this interpretation. Finally, our findings show that the pooled data from different animals overestimate the variability of venular PO2 and volume flow likely to be found in a local network or an individual animal.


   DISCLOSURES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
REFERENCES
 
This work was supported by National Heart, Lung, and Blood Institute Grants HL-62318, HL-52684, and HL-66318.


   ACKNOWLEDGMENTS
 
Current address of A. Toth: Dept. of Pharmacology and Pharmacotherapy, Univ of Szeged, H-6701 Szeged, Hungary.


   FOOTNOTES
 

Address for reprint requests and other correspondence: P. C. Johnson, Dept. of Bioengineering, Univ. of California-San Diego, 9500 Gilman Dr., La Jolla, CA 92093-0412 (E-mail: pjohnson{at}bioeng.ucsd.edu).

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.


   REFERENCES
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 REFERENCES
 

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 Am. J. Physiol. Heart Circ. Physiol.Home page
A. S. Golub and R. N. Pittman
Erythrocyte-associated transients in PO2 revealed in capillaries of rat mesentery
Am J Physiol Heart Circ Physiol, June 1, 2005; 288(6): H2735 - H2743.
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 SEMIN CARDIOTHORAC VASC ANESTHHome page
B. D. Spiess
Transfusion of Blood Products Affects Outcome in Cardiac Surgery
Seminars in Cardiothoracic and Vascular Anesthesia, December 1, 2004; 8(4): 267 - 281.
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