Measurement of Renal Tissue Oxygen Tension: Systematic Differences between Fluorescence Optode and Microelectrode Recordings in Anaesthetized Rabbits

American Journal of Physiology-Regulatory, Integrative and Comp

Goddard

Eppel

et al. 2011

Self Cite

Evans RG, Goddard D, Eppel GA, O'Connor PM. Factors that render the kidney susceptible to tissue hypoxia in hypoxemia. Am J Physiol Regul Integr Comp Physiol 300: R931-R940, 2011. First published January 19, 2011 doi:10.1152/ajpregu.00552.2010To better understand what makes the kidney susceptible to tissue hypoxia, we compared, in the rabbit kidney and hindlimb, the ability of feedback mechanisms governing oxygen consumption (V O2) and oxygen delivery (DO 2 ) to attenuate tissue hypoxia during hypoxemia. In the kidney (cortex and medulla) and hindlimb (biceps femoris muscle), we determined responses of whole organ blood flow and V O2, and local perfusion and tissue PO2, to reductions in DO2 mediated by graded systemic hypoxemia. Progressive hypoxemia reduced tissue PO2 similarly in the renal cortex, renal medulla, and biceps femoris. Falls in tissue PO2 could be detected when arterial oxygen content was reduced by as little as 4 -8%. V O2 remained stable during progressive hypoxemia, only tending to fall once arterial oxygen content was reduced by 55% for the kidney or 42% for the hindlimb. Even then, the fall in renal V O2 could be accounted for by reduced oxygen demand for sodium transport rather than limited oxygen availability. Hindlimb blood flow and local biceps femoris perfusion increased progressively during graded hypoxia. In contrast, neither total renal blood flow nor cortical or medullary perfusion was altered by hypoxemia. Our data suggest that the absence in the kidney of hyperemic responses to hypoxia, and the insensitivity of renal V O2 to limited oxygen availability, contribute to kidney hypoxia during hypoxemia. The susceptibility of the kidney to tissue hypoxia, even in relatively mild hypoxemia, may have important implications for the progression of kidney disease, particularly in patients at high altitude or with chronic obstructive pulmonary disease. hyperemia; hypoxia; ischemia; kidney circulation; oxygen tension; skeletal muscle ONE OF THE GREAT PARADOXES of physiology is the susceptibility of the kidney to tissue hypoxia. The kidneys are among the most highly perfused organs in the body, receiving approximately one-quarter of the cardiac output at rest yet comprise Ͻ1% of total body weight (14). Thus renal oxygen delivery (DO 2 ) greatly exceeds oxygen consumption (V O 2 ). Yet the kidney is extremely susceptible to hypoxic damage, which in turn appears to be a crucial event in the pathogenesis of chronic kidney disease (8,19,32,35) and acute kidney injury (7, 20, 24) of diverse etiology. Therefore, it is imperative that we improve our understanding of the structural and functional characteristics of the kidney that make it susceptible to development of hypoxia.Most organs respond to a reduction in oxygenation by increasing local blood flow and so DO 2 (14). The increased DO 2 then acts to increase tissue oxygenation and so attenuate development of hypoxia and tissue injury. In this regard, the control of blood flow to the kidney is unique in that it appears to be dominated by the func...

Section: Discussionmentioning

confidence: 82%

Section: Animalsmentioning

confidence: 99%

Factors that render the kidney susceptible to tissue hypoxia in hypoxemia

American Journal of Physiology-Regulatory, Integrative and Comp

Goddard

Eppel

et al. 2011

Self Cite

“…The positions of the probes were confirmed at postmortem. Each probe contained a dual-fiber laser Doppler probe [for estimation of tissue perfusion by measurement of laser Doppler flux (LDF)], a single-fiber fluorescence optode (for measurement of tPO 2), and a thermocouple (for measurement of tissue temperature) (3,20,24). The probes are precalibrated by the manufacturer.…”

Section: Methodsmentioning

confidence: 99%

Variable responses of regional renal oxygenation and perfusion to vasoactive agents in awake sheep

Calzavacca

American Journal of Physiology-Regulatory, Integrative and Comp

Bailey

et al. 2015

Self Cite

“…Custom-built fiber-optic probes (450 m outer diameter; CP-004-001 Oxford Optronix, Oxford, UK), with 20 mm of optical fiber extending from the outer sheath, were inserted into the renal cortex and medulla along tracks prepared by previous insertion of a 25-gauge needle (514-m outer diameter). Each combined probe contained a dual-fiber laser-Doppler probe (for estimation of tissue perfusion by measurement of laser-Doppler flux), a single-fiber fluorescence optode (for measurement of tPO 2), and a thermocouple (for measurement of tissue temperature) (22,26,31). Before insertion, the outer sheath of each probe was joined with PVC glue to a flexible sheet (2.0 ϫ 1.0 cm), made in-house from PVC glue spread thinly on a single layer of gauze, which was then allowed to dry.…”

Section: Animal Preparationmentioning

confidence: 99%

“…Any fibrosis would be expected to lead to an under estimation of tPO 2 , so is unlikely to account for the relatively high tPO 2 that we observed in the renal medulla in the unanesthetized sheep. A major advantage of the fluorescence optode technique over polarographic electrodes is the ability of the former to capture tPO 2 over a larger volume of tissue, thus leading to better "averaging" of tPO 2 , particularly in the renal cortex where there is considerable spatial heterogeneity of tPO 2 (26). We have previously shown, at least after acute implantation in anesthetized rabbits, that the combination probe used here responds to changes in tissue oxygenation and perfusion in a manner indistinguishable from the response of individual fluorescence optodes and laser-Doppler flow probes (31).…”

Section: Strengths and Limitationsmentioning

confidence: 99%

Long-term measurement of renal cortical and medullary tissue oxygenation and perfusion in unanesthetized sheep

Calzavacca

American Journal of Physiology-Regulatory, Integrative and Comp

Bailey

et al. 2015

Self Cite

Calzavacca P, Evans RG, Bailey M, Lankadeva YR, Bellomo R, May CN. Long-term measurement of renal cortical and medullary tissue oxygenation and perfusion in unanesthetized sheep. Am J Physiol Regul Integr Comp Physiol 308: R832-R839, 2015. First published March 11, 2015 doi:10.1152/ajpregu.00515.2014.-The role of renal cortical and medullary hypoxia in the development of acute kidney injury is controversial, partly due to a lack of techniques for the long-term measurement of intrarenal oxygenation and perfusion in conscious animals. We have, therefore, developed a methodology to chronically implant combination probes to chronically measure renal cortical and medullary tissue perfusion and oxygen tension (tPO2) in conscious sheep and evaluated their responsiveness and reliability. A transit-time flow probe and a vascular occluder were surgically implanted on the left renal artery. At the same operation, dual fiber-optic probes, comprising a fluorescence optode to measure tPO2 and a laser-Doppler probe to assess tissue perfusion, were inserted into the renal cortex and medulla. In recovered conscious sheep (n ϭ 8) breathing room air, mean 24-h cortical and medullary tPO 2 were similar (31.4 Ϯ 0.6 and 29.7 Ϯ 0.7 mmHg, respectively). In the renal cortex and medulla, a 20% reduction in renal blood flow (RBF) decreased perfusion (14.6 Ϯ 8.6 and 41.2 Ϯ 8.5%, respectively) and oxygenation (48.1 Ϯ 8.5 and 72.4 Ϯ 8.5%, respectively), with greater decreases during a 50% reduction in RBF. At autopsy, minimal fibrosis was observed around the probes. In summary, we have developed a technique to chronically implant fiber-optic probes in the renal cortex and medulla for recording tissue perfusion and oxygenation over many days. In normal resting conscious sheep, cortical and medullary tPO 2 were similar. The responses to and recovery from renal artery occlusion, together with the consistent measurements over a 24-h period, demonstrate the responsiveness and stability of the probes. renal blood flow; kidney oxygenation; renal artery occlusion; perfusion; tissue oxygen tension.THE ETIOLOGY OF RENAL FAILURE is highly dependent on the setting in which it occurs. Nevertheless, considerable interest has focused on the potential for renal tissue hypoxia to provide a common pathway in multiple forms of acute and chronic kidney disease (18). Oxygen supply to the kidney via the renal artery far exceeds the kidney's metabolic requirements, yet the renal medulla, in particular, appears susceptible to the development of hypoxia (8).Many studies in which medullary tissue PO 2 (tPO 2 ) has been measured by polarographic electrodes in experimental animals and humans, breathing air or gas mixtures enriched in oxygen, have provided values of 10 -20 mmHg (4,8,9,11,25), close to the critical tPO 2 for isolated tubular cells (5 to 15 mmHg) (2, 3, 13, 14). These observations have led to the concept that the medulla normally operates on the brink of hypoxia and so is highly susceptible to factors that might reduce oxygen delivery or increase oxygen...