scholarly journals The rate of O2 loss from mesenteric arterioles is not unusually high

2011 ◽  
Vol 301 (3) ◽  
pp. H737-H745 ◽  
Author(s):  
Aleksander S. Golub ◽  
Bjorn K. Song ◽  
Roland N. Pittman

The O2 disappearance curve (ODC) recorded in an arteriole after the rapid arrest of blood flow reflects the complex interaction among the dissociation of O2 from hemoglobin, O2 diffusivity, and rate of respiration in the vascular wall and surrounding tissue. In this study, the analysis of experimental ODCs allowed the estimation of parameters of O2 transport and O2 consumption in the microcirculation of the mesentery. We collected ODCs from rapidly arrested blood inside rat mesenteric arterioles using scanning phosphorescence quenching microscopy (PQM). The technique was used to prevent the artifact of accumulated O2 photoconsumption in stationary media. The observed ODC signatures were close to linear, in contrast to the reported exponential decline of intra-arteriolar Po2. The rate of Po2 decrease was 0.43 mmHg/s in 20-μm-diameter arterioles. The duration of the ODC was 290 s, much longer than the 12.8 s reported by other investigators. The arterioles associated with lymphatic microvessels had a higher O2 disappearance rate of 0.73 mmHg/s. The O2 flux from arterioles, calculated from the average O2 disappearance rate, was 0.21 nl O2·cm−2·s−1, two orders of magnitude lower than reported in the literature. The physical upper limit of the O2 consumption rate by the arteriolar wall, calculated from the condition that all O2 is consumed by the wall, was 452 nl O2·cm−3·s−1. From consideration of the microvascular tissue volume fraction in the rat mesentery of 6%, the estimated respiration rate of the vessel wall was ∼30 nl O2·cm−3·s−1. This result was three orders of magnitude lower than the respiration rate in rat mesenteric arterioles reported by other investigators. Our results demonstrate that O2 loss from mesenteric arterioles is small and that the O2 consumption by the arteriolar wall is not unusually large.

2005 ◽  
Vol 289 (1) ◽  
pp. H295-H300 ◽  
Author(s):  
Masahiro Shibata ◽  
Shigeru Ichioka ◽  
Akira Kamiya

To examine the effects of vascular tone reduction on O2 consumption of the vascular wall, we determined the O2 consumption rates of arteriolar walls under normal conditions and during vasodilation induced by topical application of papaverine. A phosphorescence quenching technique was used to quantify intra- and perivascular Po2 in rat cremaster arterioles with different branching orders. Then, the measured radial Po2 gradients and a theoretical model were used to estimate the O2 consumption rates of the arteriolar walls. The vascular O2 consumption rates of functional arterioles were >100 times greater than those observed in in vitro experiments. The vascular O2 consumption rate was highest in first-order (1A) arterioles, which are located upstream, and sequentially decreased downstream in 2A and 3A arterioles under normal conditions. During papaverine-induced vasodilation, on the other hand, the O2 consumption rates of the vascular walls decreased to similar levels, suggesting that the high O2 consumption rates of 1A arterioles under normal conditions depend in part on the workload of the vascular smooth muscle. These results strongly support the hypothesis that arteriolar walls consume a significant amount of O2 compared with the surrounding tissue. Furthermore, the reduction of vascular tone of arteriolar walls may facilitate an efficient supply of O2 to the surrounding tissue.


2004 ◽  
Vol 286 (3) ◽  
pp. H878-H883 ◽  
Author(s):  
Nanae Hangai-Hoger ◽  
Pedro Cabrales ◽  
Juan C. Briceño ◽  
Amy G. Tsai ◽  
Marcos Intaglietta

Oxygen phosphorescence quenching was used to measure tissue Po2 of lymphatic vessels of 43.6 ± 23.1 μm (mean ± SD) diameter in tissue locations of the rat mesentery classified according to anatomic location. Lymph and adipose tissue Po2 were 20.6 ± 9.1 and 34.1 ± 7.8 mmHg, respectively, with the difference being statistically significant. Rare microlymphatic vessels in connective tissue not surrounded by microvessels had a Po2 of 0.8 ± 0.2 mmHg, whereas the surrounding tissue Po2 was 3.0 ± 3.2 mmHg, with both values being significantly lower than those of adipose tissue. Lower of lymph fluid Po2 relative to the surrounding tissue was also evident in paired measurements of Po2 in the lymphatic vessels and perilymphatic adipose tissue, which was significantly lower than the Po2 in paired adipose tissue. The Po2 of the lymphatic fluid of the mesenteric microlymphatics is consistently lower than that of the surrounding adipose tissue by ∼11 mmHg; therefore, lymph fluid has the lowest Po2 of this tissue. The disparity between lymph and tissue Po2 is attributed to the microlymphatic vessel wall and lymphocyte oxygen consumption.


2008 ◽  
Vol 294 (1) ◽  
pp. H21-H28 ◽  
Author(s):  
Aleksander S. Golub ◽  
Matthew C. Barker ◽  
Roland N. Pittman

Longitudinal Po2 profiles in the microvasculature of the rat mesentery were studied using a novel phosphorescence quenching microscopy technique that minimizes the accumulated photoconsumption of oxygen by the method. Intravascular oxygen tension (Po2, in mmHg) and vessel diameter ( d, in μm) were measured in mesenteric microvessels ( n = 204) of seven anesthetized rats (275 g). The excitation parameters were as follows: 7 × 7-μm spot size; 410 nm laser; and 100 curves at 11 pulses/s, with pulse parameters of 2-μs duration and 80-pJ/μm2 energy density. The mean Po2 (± SE) was 65.0 ± 1.4 mmHg ( n = 78) for arterioles ( d = 18.8 ± 0.7 μm), 62.1 ± 2.0 mmHg ( n = 38) at the arteriolar end of capillaries ( d = 7.8 ± 0.3 μm), and 52.0 ± 1.0 mmHg ( n = 88) for venules ( d = 22.5 ± 1.0 μm). There was no apparent dependence of Po2 on d in arterioles and venules. There were also no significant deviations in Po2 based on d (bin width, 5 μm) from the general mean for both of these types of vessels. Results indicate that the primary site of oxygen delivery to tissue is located between the smallest arterioles and venules (change of 16.3 mmHg, P = 0.001). In conclusion, oxygen losses from mesenteric arterioles and venules are negligible, indicating low metabolic rates for both the vascular wall and the mesenteric tissue. Capillaries appear to be the primary site of oxygen delivery to the tissue in the mesenteric microcirculation. In light of the present results, previously reported data concerning oxygen consumption in the mesenteric microcirculation can be explained as artifacts of accumulated oxygen consumption due to the application of instrumentation having a large excitation area for Po2 measurements in slow moving and stationary media.


2008 ◽  
Vol 294 (6) ◽  
pp. H2905-H2916 ◽  
Author(s):  
Aleksander S. Golub ◽  
Roland N. Pittman

In phosphorescence quenching microscopy (PQM), the multiple excitation of a reference volume produces the integration of oxygen consumption artifacts caused by individual flashes. We analyzed the performance of two types of PQM instruments to explain reported data on Po2 in the microcirculation. The combination of a large excitation area (LEA) and high flash rate produces a large oxygen photoconsumption artifact manifested differently in stationary and flowing fluids. A LEA instrument strongly depresses Po2 in a motionless tissue, but less in flowing blood, creating an apparent transmural Po2 drop in arterioles. The proposed model explains the mechanisms responsible for producing apparent transmural and longitudinal Po2 gradients in arterioles, a Po2 rise in venules, a hypothetical high respiration rate in the arteriolar wall and mesenteric tissue, a low Po2 in lymphatic microvessels, and both low and uniform tissue Po2. This alternative explanation for reported paradoxical results of Po2 distribution in the microcirculation obviates the need to revise the dominant role of capillaries in oxygen transport to tissue. Finding a way to eliminate the photoconsumption artifact is crucial for accurate microscopic oxygen measurements in microvascular networks and tissue. The PQM technique that employs a small excitation area (SEA) together with a low flash rate was specially designed to avoid accumulated oxygen photoconsumption in flowing blood and lymph. The related scanning SEA instrument provides artifact-free Po2 measurements in stationary tissue and motionless fluids. Thus the SEA technique significantly improves the accuracy of microscopic Po2 measurements in the microcirculation using the PQM.


2008 ◽  
Vol 28 (9) ◽  
pp. 1597-1604 ◽  
Author(s):  
Maithili Sharan ◽  
Eugene P Vovenko ◽  
Arjun Vadapalli ◽  
Aleksander S Popel ◽  
Roland N Pittman

Using modified oxygen needle microelectrodes and intravital videomicroscopy, measurements were made of tissue oxygen tension (PO2) profiles near cortical arterioles and transmural PO2 gradients in the pial arterioles of the rat. Under control conditions, the transmural PO2 gradient averaged 1.17 ± 0.06 mm Hg/μm (mean ± s.e., n = 40). Local arteriolar dilation resulted in a marked decrease in the transmural PO2 gradient to 0.68 ± 0.04 mm Hg/μm ( P < 0.001, n = 38). The major finding of this study is a dependence of the transmural PO2 gradient on the vascular tone of the pial arterioles. Using a model of oxygen transport in an arteriole and experimental PO2 profiles, values of radial perivascular and intravascular O2 fluxes were estimated. Our theoretical estimates show that oxygen flux values at the outer surface of the arteriolar wall are approximately 10−5mL O2/cm2 per sec, independent of the values of the arteriolar wall O2 consumption within a wide range of consumption values. This also means that PO2 transmural gradients for cerebral arterioles are within the limits of 1 to 2 mm Hg/μm. The data lead to the conclusion that O2 consumption of the arteriolar wall is within the range for the surrounding tissue and O2 consumption of the endothelial layer appears to have no substantial impact on the transmural PO2 gradient.


2006 ◽  
Vol 291 (6) ◽  
pp. H2950-H2964 ◽  
Author(s):  
Xiaobing Zhang ◽  
Roger H. Adamson ◽  
Fitz-Roy E. Curry ◽  
Sheldon Weinbaum

The recent experiments in Hu et al. ( Am J Physiol Heart Circ Physiol 279: H1724–H1736, 2000) and Adamson et al. ( J Physiol 557: 889–907, 2004) in frog and rat mesentery microvessels have provided strong evidence supporting the Michel-Weinbaum hypothesis for a revised asymmetric Starling principle in which the Starling force balance is applied locally across the endothelial glycocalyx layer rather than between lumen and tissue. These experiments were interpreted by a three-dimensional (3-D) mathematical model (Hu et al.; Microvasc Res 58: 281–304, 1999) to describe the coupled water and albumin fluxes in the glycocalyx layer, the cleft with its tight junction strand, and the surrounding tissue. This numerical 3-D model converges if the tissue is at uniform concentration or has significant tissue gradients due to tissue loading. However, for most physiological conditions, tissue gradients are two to three orders of magnitude smaller than the albumin gradients in the cleft, and the numerical model does not converge. A simpler multilayer one-dimensional (1-D) analytical model has been developed to describe these conditions. This model is used to extend Michel and Phillips’s original 1-D analysis of the matrix layer ( J Physiol 388: 421–435, 1987) to include a cleft with a tight junction strand, to explain the observation of Levick ( Exp Physiol 76: 825–857, 1991) that most tissues have an equilibrium tissue concentration that is close to 0.4 lumen concentration, and to explore the role of vesicular transport in achieving this equilibrium. The model predicts the surprising finding that one can have steady-state reabsorption at low pressures, in contrast to the experiments in Michel and Phillips, if a backward-standing gradient is established in the cleft that prevents the concentration from rising behind the glycocalyx.


Circulation ◽  
2007 ◽  
Vol 116 (suppl_16) ◽  
Author(s):  
Xiaoping Liu ◽  
Parthasarathy Srinivasan ◽  
Eric Collard ◽  
Paula Grajdeanu ◽  
Jay L Zweier ◽  
...  

Endothelium-derived nitric oxide (NO) plays an important role in maintaining vascular tone. It is known that NO may be consumed by heme proteins, superoxide and oxygen during diffusion from the endothelium to smooth muscle cells in the vascular wall. Due to the limitation of available techniques, it is unclear to what extent these consumptions can affect the diffusion distance of NO, and if the vascular NO consumption could serve as a “sensor” of oxygen concentrations in the blood vessels. In this study, rat aortas were used as an experimental model for studying NO diffusion process in the vascular system. A Clark-type NO electrode was used to directly measure the flux of NO diffusion across the vascular wall at 37 °C. A segment of aorta was isolated from a 12-week old WKY rat. After the aorta was cleaned and surrounding tissue was removed, it was longitudinally opened. A specifically-designed aorta holder was attached on the tip of the Clark-type NO electrode. The aorta holder surface and the electrode tip surface were aligned in the same plane so that the opened aorta segment could be placed flat on the electrode tip surface and pinned to the aorta holder. Using this technique, we measured the flux of NO diffusion across the aortic wall at different oxygen concentration. It was observed that the NO flux increased 6 to 10 fold when oxygen concentrations dropped from 200 μM to zero. A mathematical model describing the steady-state diffusion-reaction was used in analyzing the experimental data. It was found that the rate of NO decay is first order with respect to [O 2 ] and first order with respect to [NO], and hence of the form k[O 2 ][NO]. The rate constant k was determined as (3.8±0.4)x10 −3 μM −1 s −1 (n=6). With this rate constant, the half-life of NO in the aortic wall in the presence of 200 μM O 2 (equilibrium with room air) will be 0.9 seconds. Our results show that the flux and diffusion distance of NO in the aortic wall is largely regulated by oxygen concentration. When oxygen concentrations drop, NO diffusion distance will significantly increase. As a result, the blood vessel will dilate to a larger extent to allow more blood to be delivered to the hypoxic tissues. Therefore this vascular NO consumption appears to play the role of an oxygen sensor in the regulation of blood flow in the body.


2007 ◽  
Vol 293 (2) ◽  
pp. H1097-H1106 ◽  
Author(s):  
Aleksander S. Golub ◽  
Matthew C. Barker ◽  
Roland N. Pittman

A scanning phosphorescence quenching microscopy technique, designed to prevent accumulated O2 consumption by the method, was applied to Po2 measurements in mesenteric tissue. In an attempt to further increase the accuracy of the measurements, albumin-bound probe was topically applied to the tissue and an objective-mounted pressurized bag was used to reduce the oxygen transport bypass through the thin layer of fluid over the mesentery. Po2 was measured at multiple sites perpendicular to the blood/wall interface in the vicinity of 84 mesenteric arterioles (7–39 μm in diameter) at distances of 5, 15, 30, 60, 120, and 180 μm in seven anesthetized Sprague-Dawley rats, thereby creating Po2 profiles. Interstitial Po2 above and immediately beside arterioles was found to agree with known intravascular values. No significant difference in Po2 profiles was found between small and large arterioles, indicating a small longitudinal Po2 gradient in the precapillary mesenteric microvasculature. In addition, the Po2 profiles were used to calculate oxygen consumption in the mesenteric tissue (56–65 nl O2·cm−3·s−1). Correction of these values for contamination with ambient oxygen yielded an oxygen consumption rate of 60–68 nl O2·cm−3·s−1, the maximal limit for consumption in the mesentery. The results were compared with measurements made by other workers in regard to the employed techniques.


1997 ◽  
Vol 82 (6) ◽  
pp. 1939-1945 ◽  
Author(s):  
George J. Cerniglia ◽  
David F. Wilson ◽  
Marek Pawlowski ◽  
Sergei Vinogradov ◽  
John Biaglow

Cerniglia, George J., David F. Wilson, Marek Pawlowski, Sergei Vinogradov, and John Biaglow. Intravascular oxygen distribution in subcutaneous 9L tumors and radiation sensitivity. J. Appl. Physiol. 82(6): 1939–1945, 1997.—Phosphorescence quenching was evaluated as a technique for measuring [Formula: see text] in tumors and for determining the effect of increased[Formula: see text] on sensitivity of the tumors to radiation. Suspensions of cultured 9L cells or small pieces of solid tumors from 9L cells were injected subcutaneously on the hindquarter of rats, and tumors were grown to between 0.2 and 1.0 cm in diameter. Oxygen-dependent quenching of the phosphorescence of intravenously injected Pd-meso-tetra-(4-carboxyphenyl) porphine was used to image the in vivo distribution of [Formula: see text] in the vasculature of small tumors and surrounding tissue. Maps (512 × 480 pixels) of tissue oxygen distribution showed that the[Formula: see text] within 9L tumors was low (2–12 Torr) relative to the surrounding muscle tissue (20–40 Torr). When the rats were given 100% oxygen or carbogen (95% O2-5% CO2) to breathe, the[Formula: see text] in the tumors increased significantly. This increase was variable among tumors and was greater with carbogen compared with 100% oxygen. Based on irradiation and regrowth studies, carbogen breathing increased the sensitivity of the tumors to radiation. This is consistent with the measured increase in[Formula: see text] in the tumor vasculature. It is concluded that phosphorescence quenching can be used for noninvasive determination of the oxygenation of tumors. This method for oxygen measurements has great potential for clinical application in tumor identification and therapy.


1991 ◽  
Vol 261 (6) ◽  
pp. H2031-H2043 ◽  
Author(s):  
C. R. Honig ◽  
T. E. Gayeski ◽  
A. Clark ◽  
P. A. Clark

Distribution of O2 within and among arterioles and venules was determined in dog and rat gracilis muscles with a cryospectrophotometric method. Saturation in 40-microns arterioles was not demonstrably different from saturation in the aorta even when flow was abnormally low. Arterioles greater than 40 microns ran parallel to venules. Measurements and a mathematical model indicate that diffusive shunting is negligible for typical separation distances between arterioles and venules. Most separation distances were greater than 30 microns. In some venule segments less than 15 microns from an arteriole, saturation within 10 microns of the wall facing the arteriole was higher than at other locations within the venule. However, saturation in the population of venules did not increase with venule diameter, and mean venular saturation was not different from saturation in effluent blood. We make the following conclusions: 1) a small arteriovenous diffusive O2 flux exists in postural muscles; 2) contribution of this flux to O2 mass balance is negligible; 3) O2 diffusivity of the arteriolar wall and surrounding tissue in vivo cannot be much higher than O2 diffusivity determined in vitro; and 4) effluent PO2 closely approximates mean end-capillary PO2.


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