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. 1994 Mar;66(3 Pt 1):789–800. doi: 10.1016/s0006-3495(94)80855-0

Oxygen exchange in the isolated, arrested guinea pig heart: theoretical and experimental observations.

D A Mawson 1, P J Hunter 1, D N Kenwright 1, D S Loiselle 1
PMCID: PMC1275777  PMID: 8011911

Abstract

A model of oxygen transport in perfused myocardial tissue is presented. Steady-state conditions are assumed in order to mimic the metabolic rate of the arrested heart. The model incorporates Michaelis-Menten dependence of mitochondrial oxygen consumption, oxymyoglobin saturation and oxyhemoglobin saturation on oxygen partial pressure (PO2). The transport equations model both the advective supply of oxygen via the coronary circulation and the diffusive exchange of oxygen between tissues and environment across the epicardial and endocardial surfaces. The left ventricle is approximated by an axisymmetric prolate spheroid and the transport equations solved numerically using finite element techniques. Solution yields the PO2 profile across the heart wall. Integration of this profile yields the simulated rate of metabolic oxygen uptake determined according to the Fick principle. Correction for the diffusive flux of oxygen across the surfaces yields the simulated true metabolic rate of oxygen consumption. Simulated values of oxygen uptake are compared with those measured experimentally according to the Fick principle, using saline-perfused, Langendorff-circulated, K(+)-arrested, guinea pig hearts. Four perfusion variables were manipulated: arterial PO2, environmental PO2, coronary flow and perfusion pressure. In each case agreement between simulated and experimentally determined rates of oxygen consumption gives confidence that the model adequately describes the advective and diffusive transport of oxygen in the isolated, arrested, saline-perfused heart.

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Selected References

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  1. Baylor S. M., Pape P. C. Measurement of myoglobin diffusivity in the myoplasm of frog skeletal muscle fibres. J Physiol. 1988 Dec;406:247–275. doi: 10.1113/jphysiol.1988.sp017379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brittain T., Simpson R. An analysis of the stopped-flow kinetics of gaseous ligand uptake and release by adult mouse erythrocytes. Biochem J. 1989 May 15;260(1):171–176. doi: 10.1042/bj2600171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Burkhoff D., Kalil-Filho R., Gerstenblith G. Oxygen consumption is less in rat hearts arrested by low calcium than by high potassium at fixed flow. Am J Physiol. 1990 Oct;259(4 Pt 2):H1142–H1147. doi: 10.1152/ajpheart.1990.259.4.H1142. [DOI] [PubMed] [Google Scholar]
  4. Buxton D. B., Kjaer-Pedersen K., Nguyen A. Metabolic effects of adenosine in the isolated perfused rat heart. J Mol Cell Cardiol. 1992 Feb;24(2):173–181. doi: 10.1016/0022-2828(92)93153-b. [DOI] [PubMed] [Google Scholar]
  5. Clark A., Jr, Federspiel W. J., Clark P. A., Cokelet G. R. Oxygen delivery from red cells. Biophys J. 1985 Feb;47(2 Pt 1):171–181. doi: 10.1016/s0006-3495(85)83890-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Duling B. R., Berne R. M. Longitudinal gradients in periarteriolar oxygen tension. A possible mechanism for the participation of oxygen in local regulation of blood flow. Circ Res. 1970 Nov;27(5):669–678. doi: 10.1161/01.res.27.5.669. [DOI] [PubMed] [Google Scholar]
  7. Ellsworth M. L., Pittman R. N. Arterioles supply oxygen to capillaries by diffusion as well as by convection. Am J Physiol. 1990 Apr;258(4 Pt 2):H1240–H1243. doi: 10.1152/ajpheart.1990.258.4.H1240. [DOI] [PubMed] [Google Scholar]
  8. Fletcher J. E. On facilitated oxygen diffusion in muscle tissues. Biophys J. 1980 Mar;29(3):437–458. doi: 10.1016/S0006-3495(80)85145-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Follert E. K. Significance of diffusion loss of oxygen in determining respiration of isolated, perfused organs. Pflugers Arch. 1971;323(1):80–85. doi: 10.1007/BF00586568. [DOI] [PubMed] [Google Scholar]
  10. Gibbs C. L., Kotsanas G. Factors regulating basal metabolism of the isolated perfused rabbit heart. Am J Physiol. 1986 Jun;250(6 Pt 2):H998–1007. doi: 10.1152/ajpheart.1986.250.6.H998. [DOI] [PubMed] [Google Scholar]
  11. Gonzalez-Fernandez J. M., Atta S. E. Facilitated transport of oxygen in the presence of membranes in the diffusion path. Biophys J. 1982 May;38(2):133–141. doi: 10.1016/S0006-3495(82)84540-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gorman M. W., Wangler R. D., Sparks H. V. Distribution of perfusate flow during vasodilation in isolated guinea pig heart. Am J Physiol. 1989 Jan;256(1 Pt 2):H297–H301. doi: 10.1152/ajpheart.1989.256.1.H297. [DOI] [PubMed] [Google Scholar]
  13. Groebe K. A versatile model of steady state O2 supply to tissue. Application to skeletal muscle. Biophys J. 1990 Mar;57(3):485–498. doi: 10.1016/S0006-3495(90)82565-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grunewald W. A., Sowa W. Distribution of the myocardial tissue PO2 in the rat and the inhomogeneity of the coronary bed. Pflugers Arch. 1978 Apr 25;374(1):57–66. doi: 10.1007/BF00585697. [DOI] [PubMed] [Google Scholar]
  15. Honig C. R., Gayeski T. E., Federspiel W., Clark A., Jr, Clark P. Muscle O2 gradients from hemoglobin to cytochrome: new concepts, new complexities. Adv Exp Med Biol. 1984;169:23–38. doi: 10.1007/978-1-4684-1188-1_2. [DOI] [PubMed] [Google Scholar]
  16. Hunter P. J., Smaill B. H. The analysis of cardiac function: a continuum approach. Prog Biophys Mol Biol. 1988;52(2):101–164. doi: 10.1016/0079-6107(88)90004-1. [DOI] [PubMed] [Google Scholar]
  17. Jöbsis F. F. Oxidative metabolism at low PO 2 . Fed Proc. 1972 Sep-Oct;31(5):1404–1413. [PubMed] [Google Scholar]
  18. Klitzman B., Popel A. S., Duling B. R. Oxygen transport in resting and contracting hamster cremaster muscles: experimental and theoretical microvascular studies. Microvasc Res. 1983 Jan;25(1):108–131. doi: 10.1016/0026-2862(83)90047-x. [DOI] [PubMed] [Google Scholar]
  19. Kreuzer F., Hoofd L. Facilitated diffusion of oxygen: possible significance in blood and muscle. Adv Exp Med Biol. 1984;169:3–21. doi: 10.1007/978-1-4684-1188-1_1. [DOI] [PubMed] [Google Scholar]
  20. Kreuzer F. Oxygen supply to tissues: the Krogh model and its assumptions. Experientia. 1982 Dec 15;38(12):1415–1426. doi: 10.1007/BF01955753. [DOI] [PubMed] [Google Scholar]
  21. Krogh A. The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J Physiol. 1919 May 20;52(6):409–415. doi: 10.1113/jphysiol.1919.sp001839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lagerlund T. D., Low P. A. A mathematical simulation of oxygen delivery in rat peripheral nerve. Microvasc Res. 1987 Sep;34(2):211–222. doi: 10.1016/0026-2862(87)90054-9. [DOI] [PubMed] [Google Scholar]
  23. Lochner W., Arnold G., Müller-Ruchholtz E. R. Metabolism of the artificially arrested heart and of the gas-perfused heart. Am J Cardiol. 1968 Sep;22(3):299–311. doi: 10.1016/0002-9149(68)90114-8. [DOI] [PubMed] [Google Scholar]
  24. Loiselle D. S. Exchange of oxygen across the epicardial surface distorts estimates of myocardial oxygen consumption. J Gen Physiol. 1989 Sep;94(3):567–590. doi: 10.1085/jgp.94.3.567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Loiselle D. S. Stretch-induced increase in resting metabolism of isolated papillary muscle. Biophys J. 1982 May;38(2):185–194. doi: 10.1016/S0006-3495(82)84545-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Loiselle D. S. The effect of myoglobin-facilitated oxygen transport on the basal metabolism of papillary muscle. Biophys J. 1987 Jun;51(6):905–913. doi: 10.1016/S0006-3495(87)83418-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mainwood G. W., Rakusan K. A model for intracellular energy transport. Can J Physiol Pharmacol. 1982 Jan;60(1):98–102. doi: 10.1139/y82-016. [DOI] [PubMed] [Google Scholar]
  28. Moll W. The diffusion coefficient of myoglobin in muscle homogenate. Pflugers Arch Gesamte Physiol Menschen Tiere. 1968;299(3):247–251. doi: 10.1007/BF00362587. [DOI] [PubMed] [Google Scholar]
  29. Murray J. D. On the role of myoglobin in muscle respiration. J Theor Biol. 1974 Sep;47(1):115–126. doi: 10.1016/0022-5193(74)90102-7. [DOI] [PubMed] [Google Scholar]
  30. Nichols J. W., Weber L. J. Comparative oxygen affinity of fish and mammalian myoglobins. J Comp Physiol B. 1989;159(2):205–209. doi: 10.1007/BF00691741. [DOI] [PubMed] [Google Scholar]
  31. PENNES H. H. Analysis of tissue and arterial blood temperatures in the resting human forearm. J Appl Physiol. 1948 Aug;1(2):93–122. doi: 10.1152/jappl.1948.1.2.93. [DOI] [PubMed] [Google Scholar]
  32. Piiper J., Meyer M., Scheid P. Dual role of diffusion in tissue gas exchange: blood-tissue equilibration and diffusion shunt. Respir Physiol. 1984 May;56(2):131–144. doi: 10.1016/0034-5687(84)90099-9. [DOI] [PubMed] [Google Scholar]
  33. Piiper J., Scheid P. Cross-sectional PO2 distributions in Krogh cylinder and solid cylinder models. Respir Physiol. 1986 Jun;64(3):241–251. doi: 10.1016/0034-5687(86)90118-0. [DOI] [PubMed] [Google Scholar]
  34. Popel A. S., Gross J. F. Analysis of oxygen diffusion from arteriolar networks. Am J Physiol. 1979 Dec;237(6):H681–H689. doi: 10.1152/ajpheart.1979.237.6.H681. [DOI] [PubMed] [Google Scholar]
  35. Popel A. S., Pittman R. N., Ellsworth M. L. Rate of oxygen loss from arterioles is an order of magnitude higher than expected. Am J Physiol. 1989 Mar;256(3 Pt 2):H921–H924. doi: 10.1152/ajpheart.1989.256.3.H921. [DOI] [PubMed] [Google Scholar]
  36. ROSSI-FANELLI A., ANTONINI E. Studies on the oxygen and carbon monoxide equilibria of human myoglobin. Arch Biochem Biophys. 1958 Oct;77(2):478–492. doi: 10.1016/0003-9861(58)90094-8. [DOI] [PubMed] [Google Scholar]
  37. Salathé E. P., Kolkka R. W. Reduction of anoxia through myoglobin-facilitated diffusion of oxygen. Biophys J. 1986 Nov;50(5):885–894. doi: 10.1016/S0006-3495(86)83529-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schouten V. J., Allaart C. P., Westerhof N. Effect of perfusion pressure on force of contraction in thin papillary muscles and trabeculae from rat heart. J Physiol. 1992;451:585–604. doi: 10.1113/jphysiol.1992.sp019180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stroeve P. Myoglobin-facilitated oxygen transport in heterogeneous red muscle tissue. Ann Biomed Eng. 1982;10(2):49–70. doi: 10.1007/BF02366998. [DOI] [PubMed] [Google Scholar]
  40. Swain D. P., Pittman R. N. Oxygen exchange in the microcirculation of hamster retractor muscle. Am J Physiol. 1989 Jan;256(1 Pt 2):H247–H255. doi: 10.1152/ajpheart.1989.256.1.H247. [DOI] [PubMed] [Google Scholar]
  41. Tateishi N., Maeda N., Shiga T. A method for measuring the rate of oxygen release from single microvessels. Circ Res. 1992 Apr;70(4):812–819. doi: 10.1161/01.res.70.4.812. [DOI] [PubMed] [Google Scholar]
  42. Taylor B. A., Murray J. D. Effect of the rate of oxygen consumption on muscle respiration. J Math Biol. 1977 Feb 28;4(1):1–20. doi: 10.1007/BF00276348. [DOI] [PubMed] [Google Scholar]
  43. Tota B., Cimini V., Salvatore G., Zummo G. Comparative study of the arterial and lacunary systems of the ventricular myocardium of elasmobranch and teleost fishes. Am J Anat. 1983 May;167(1):15–32. doi: 10.1002/aja.1001670103. [DOI] [PubMed] [Google Scholar]
  44. Van Beek J. H., Loiselle D. S., Westerhof N. Calculation of oxygen diffusion across the surface of isolated perfused hearts. Am J Physiol. 1992 Oct;263(4 Pt 2):H1003–H1010. doi: 10.1152/ajpheart.1992.263.4.H1003. [DOI] [PubMed] [Google Scholar]
  45. Wilson D. F., Erecińska M., Drown C., Silver I. A. Effect of oxygen tension on cellular energetics. Am J Physiol. 1977 Nov;233(5):C135–C140. doi: 10.1152/ajpcell.1977.233.5.C135. [DOI] [PubMed] [Google Scholar]
  46. de Koning J., Hoofd L. J., Kreuzer F. Oxygen transport and the function of myoglobin. Theoretical model and experiments in chicken gizzard smooth muscle. Pflugers Arch. 1981 Mar;389(3):211–217. doi: 10.1007/BF00584781. [DOI] [PubMed] [Google Scholar]
  47. van Ouwerkerk H. J. Facilitated diffusion in a tissue cylinder with an anoxic region. Pflugers Arch. 1977;372(3):221–230. doi: 10.1007/BF01063856. [DOI] [PubMed] [Google Scholar]

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