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. 1985 Mar;360:311–332. doi: 10.1113/jphysiol.1985.sp015619

Effect of fluid pressure on the hydraulic conductance of interstitium and fenestrated endothelium in the rabbit knee.

A D Knight, J R Levick
PMCID: PMC1193463  PMID: 3989719

Abstract

A synovial cavity is separated from plasma by synovial intima in series with capillary endothelium. Because 20% of the intimal surface is bare interstitium, the system is a convenient model for the study of passive transport through serial endothelial and interstitial layers. Here hydraulic flow across the composite barrier was investigated in forty-seven knees of isolated, blood-perfused rabbit hindquarters, at intra-articular pressures between 4 and 30 cmH2O. In order to measure barrier conductance at constant intra-articular pressure, pressure on the opposite side of the barrier was varied, i.e. capillary blood pressure (PC). Capillary pressure was changed by alteration of vascular perfusion pressures, and the resulting changes in rate of absorption of Krebs solution from the synovial cavity (QS) were recorded. Trans-synovial absorption was a negative linear function of PC at each joint pressure, in verification of the applicability of Starling's hypothesis to this system. The hydraulic conductance of the blood-joint barrier was calculated as dQS/dPC. Conductance was independent of intra-articular pressure below 9 cmH2O and was 0.12 +/- 0.015 microliter min-1 mmHg-1 (mean +/- S.E. of mean). Barrier conductance increased as a curvilinear function of intra-articular pressure above 9.4 cmH2O (yield pressure). At 30 cmH2O conductance averaged 0.60 +/- 0.06 microliter min-1 mmHg-1, a 5-fold increase. A hyperbolic curve relating net barrier conductance to joint pressure was predicted from the hypothesis that interstitial conductance increases as a monotonic function of intra-articular pressure above yield pressure (Appendix). The data were in reasonable agreement with the theoretical hyperbola. Interstitial conductivity (3 X 10(-7)-7 X 10(-7) cm4 s-1 N-1 below yield pressure) and mean endothelial conductance (1.1 X 10(-4)-1.4 X 10(-4) cm3 s-1 N-1) were evaluated and compared with values in other tissues. Synovial endothelium contains on average 0.25 fenestrae micron-1 circumference. The conductance of a single fenestra was calculated to be 2.3 X 10(-13) cm5 s-1 N-1. Interstitial resistance accounted for roughly half the total resistance below yield point: therefore dQS/dPC should not be equated with 'capillary filtration capacity' in tissues with dense or fenestrated capillary beds. Large inconsistencies between interstitial conductivity and glycosaminoglycan concentration are noted, and mechanistic explanations of increases in conductivity with joint pressure are offered.

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Selected References

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  1. Aukland K., Nicolaysen G. Interstitial fluid volume: local regulatory mechanisms. Physiol Rev. 1981 Jul;61(3):556–643. doi: 10.1152/physrev.1981.61.3.556. [DOI] [PubMed] [Google Scholar]
  2. Casley-Smith J. R., Földi-Börcsök E., Földi M. A fine structural study of the tissue channels' numbers and dimensions in normal and lymphoedematous tissues. Z Lymphol. 1979 Jun;3(1):49–58. [PubMed] [Google Scholar]
  3. Casley-Smith J. R., O'Donoghue P. J., Crocker K. W. The quantitative relationships between fenestrae in jejunal capillaries and connective tissue channels: proof of "tunnel-capillaries". Microvasc Res. 1975 Jan;9(1):78–100. doi: 10.1016/0026-2862(75)90053-9. [DOI] [PubMed] [Google Scholar]
  4. Casley-Smith J. R., Vincent A. H. The quantitative morphology of interstitial tissue channels in some tissues of the rat and rabbit. Tissue Cell. 1978;10(3):571–584. doi: 10.1016/s0040-8166(16)30350-0. [DOI] [PubMed] [Google Scholar]
  5. Clough G., Smaje L. H. Exchange area and surface properties of the microvasculature of the rabbit submandibular gland following duct ligation. J Physiol. 1984 Sep;354:445–456. doi: 10.1113/jphysiol.1984.sp015387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Granger H. J., Taylor A. E. Permeability of connective tissue linings isolated from implanted capsules; implications for interstitial pressure measurements. Circ Res. 1975 Jan;36(1):222–228. doi: 10.1161/01.res.36.1.222. [DOI] [PubMed] [Google Scholar]
  7. Guyton A. C., Scheel K., Murphree D. Interstitial fluid pressure. 3. Its effect on resistance to tissue fluid mobility. Circ Res. 1966 Aug;19(2):412–419. doi: 10.1161/01.res.19.2.412. [DOI] [PubMed] [Google Scholar]
  8. HEDBYS B. O. Corneal resistance of the flow of water after enzymatic digestion. Exp Eye Res. 1963 Apr;2:112–121. doi: 10.1016/s0014-4835(63)80002-0. [DOI] [PubMed] [Google Scholar]
  9. Highton T. C., Myers D. B., Rayns D. G. The intercellular spaces of synovial tissue. N Z Med J. 1968 Mar;67(429):315–325. [PubMed] [Google Scholar]
  10. Intaglietta M., de Plomb E. P. Fluid exchange in tunnel and tube capillaries. Microvasc Res. 1973 Sep;6(2):153–168. doi: 10.1016/0026-2862(73)90017-4. [DOI] [PubMed] [Google Scholar]
  11. Jarvis S. M., Young J. D. Nucleoside translocation in sheep reticulocytes and fetal erythrocytes: a proposed model for the nucleoside transporter. J Physiol. 1982 Mar;324:47–66. doi: 10.1113/jphysiol.1982.sp014100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jayson MISt Dixon A. J. Intra-articular pressure in rheumatoid arthritis of the knee. II. Effect of intra-articular pressure on blood circulation to the synovium. Ann Rheum Dis. 1970 May;29(3):266–268. doi: 10.1136/ard.29.3.266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Knight A. D., Levick J. R. Morphometry of the ultrastructure of the blood-joint barrier in the rabbit knee. Q J Exp Physiol. 1984 Apr;69(2):271–288. doi: 10.1113/expphysiol.1984.sp002805. [DOI] [PubMed] [Google Scholar]
  14. Knight A. D., Levick J. R. Physiological compartmentation of fluid within the synovial cavity of the rabbit knee. J Physiol. 1982 Oct;331:1–15. doi: 10.1113/jphysiol.1982.sp014361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Knight A. D., Levick J. R. Pressure-volume relationships above and below atmospheric pressure in the synovial cavity of the rabbit knee. J Physiol. 1982 Jul;328:403–420. doi: 10.1113/jphysiol.1982.sp014273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Knight A. D., Levick J. R. The density and distribution of capillaries around a synovial cavity. Q J Exp Physiol. 1983 Oct;68(4):629–644. doi: 10.1113/expphysiol.1983.sp002753. [DOI] [PubMed] [Google Scholar]
  17. Knight A. D., Levick J. R. The influence of blood pressure on trans-synovial flow in the rabbit. J Physiol. 1984 Apr;349:27–42. doi: 10.1113/jphysiol.1984.sp015140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Levick J. R. An investigation into the validity of subatmospheric pressure recordings from synovial fluid and their dependence on joint angle. J Physiol. 1979 Apr;289:55–67. doi: 10.1113/jphysiol.1979.sp012724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Levick J. R. Contributions of the lymphatic and microvascular systems to fluid absorption from the synovial cavity of the rabbit knee. J Physiol. 1980 Sep;306:445–461. doi: 10.1113/jphysiol.1980.sp013406. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Michel C. C. Filtration coefficients and osmotic reflexion coefficients of the walls of single frog mesenteric capillaries. J Physiol. 1980 Dec;309:341–355. doi: 10.1113/jphysiol.1980.sp013512. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Murooka T. [A quantitative ultrastructural analysis of fenestrations and basal laminae of the blood capillaries in the knee joint synovial membrane (author's transl)]. Nihon Seikeigeka Gakkai Zasshi. 1979 Jan;53(1):43–51. [PubMed] [Google Scholar]
  22. Okada Y., Nakanishi I., Kajikawa K. Ultrastructure of the mouse synovial membrane. Development and organization of the extracellular matrix. Arthritis Rheum. 1981 Jun;24(6):835–843. doi: 10.1002/art.1780240611. [DOI] [PubMed] [Google Scholar]
  23. Preston B. N., Davies M., Ogston A. G. The composition and physicochemical properties of hyaluronic acids prepared from ox synovial fluid and from a case of mesothelioma. Biochem J. 1965 Aug;96(2):449–474. doi: 10.1042/bj0960449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Starling E. H. On the Absorption of Fluids from the Connective Tissue Spaces. J Physiol. 1896 May 5;19(4):312–326. doi: 10.1113/jphysiol.1896.sp000596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Swabb E. A., Wei J., Gullino P. M. Diffusion and convection in normal and neoplastic tissues. Cancer Res. 1974 Oct;34(10):2814–2822. [PubMed] [Google Scholar]
  26. Winters A. D., 3rd, Kruger S. Drug effects on bulk flow through mesenteric membrane. Arch Int Pharmacodyn Ther. 1968 May;173(1):213–225. [PubMed] [Google Scholar]
  27. Woodward D. H., Gryfe A., Gardner D. L. Comparative study by scanning electron microscopy of synovial surfaces of 4 mammalian species. Experientia. 1969 Dec 15;25(12):1301–1303. doi: 10.1007/BF01897513. [DOI] [PubMed] [Google Scholar]
  28. Wysocki G. P., Brinkhous K. M. Scanning electron microscopy of synovial membranes. Arch Pathol. 1972 Feb;93(2):172–177. [PubMed] [Google Scholar]

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