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. 1995 Oct;69(4):1429–1439. doi: 10.1016/S0006-3495(95)80012-3

Radial organization of interstitial exchange pathway and influence of collagen in synovium.

F M Price 1, R M Mason 1, J R Levick 1
PMCID: PMC1236373  PMID: 8534813

Abstract

The synovial intercellular space is the path by which water, nutrients, cytokines, and macromolecules enter and leave the joint cavity. In this study two structural factors influencing synovial permeability were quantified by morphometry (Delesse's principle) of synovial electronmicrographs (rabbit knee), namely interstitial volume fraction Vv.1 and the fraction of the interstitium obstructed by collagen fibrils. Mean Vv.1 across the full thickness was 0.66 +/- 0.03 SEM (n = 11); but Vv.1 actually varied systematically with depth normal to the surface, increasing nonlinearly from 0.40 +/- 0.04 (n = 5 joints) near the free surface to 0.92 +/- 0.02 near the subsynovial interface. Tending to offset this increase in transport space, however, the space "blocked" by collagen fibrils also increased nonlinearly with depth. Bundles of collagen fibrils occupied 13.6 +/- 2.4% of interstitial volume close to the free surface but 49 +/- 4.8% near the subsynovial surface (full-thickness average, 40.5 +/- 3.5%), with fibrils accounting for 48.6-57.1% of the bundle space. Because of the two counteracting compositional gradients, the space available for fibril-excluded transport (hydraulic flow and macromolecular diffusion) was relatively constant > 4 microns below the surface but constricted at the synovium-cavity interface. The space available to extracellular polymers was only 51-53% of tissue volume, raising their effective concentration and hence the lining's resistance to flow and ability to confine the synovial fluid.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashhurst D. E., Bland Y. S., Levick J. R. An immunohistochemical study of the collagens of rabbit synovial interstitium. J Rheumatol. 1991 Nov;18(11):1669–1672. [PubMed] [Google Scholar]
  2. Athanasou N. A., Quinn J. Immunocytochemical analysis of human synovial lining cells: phenotypic relation to other marrow derived cells. Ann Rheum Dis. 1991 May;50(5):311–315. doi: 10.1136/ard.50.5.311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aukland K., Reed R. K. Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol Rev. 1993 Jan;73(1):1–78. doi: 10.1152/physrev.1993.73.1.1. [DOI] [PubMed] [Google Scholar]
  4. Bone Q., Denton E. J. The osmotic effects of electron microscope fixatives. J Cell Biol. 1971 Jun;49(3):571–581. doi: 10.1083/jcb.49.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Comper W. D., Zamparo O. Hydraulic conductivity of polymer matrices. Biophys Chem. 1989 Oct;34(2):127–135. doi: 10.1016/0301-4622(89)80050-x. [DOI] [PubMed] [Google Scholar]
  6. Comper W. D., Zamparo O. Hydrodynamic properties of connective-tissue polysaccharides. Biochem J. 1990 Aug 1;269(3):561–564. doi: 10.1042/bj2690561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Davies D. V. The lymphatics of the synovial membrane. J Anat. 1946 Jan;80(Pt 1):21–23. [PMC free article] [PubMed] [Google Scholar]
  8. Elias H., Hennig A., Schwartz D. E. Stereology: applications to biomedicalresearch. Physiol Rev. 1971 Jan;51(1):158–200. doi: 10.1152/physrev.1971.51.1.158. [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. 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]
  11. 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]
  12. Levick J. R. A two-dimensional morphometry-based model of interstitial and transcapillary flow in rabbit synovium. Exp Physiol. 1991 Nov;76(6):905–921. doi: 10.1113/expphysiol.1991.sp003553. [DOI] [PubMed] [Google Scholar]
  13. Levick J. R. An analysis of the interaction between interstitial plasma protein, interstitial flow, and fenestral filtration and its application to synovium. Microvasc Res. 1994 Jan;47(1):90–125. doi: 10.1006/mvre.1994.1007. [DOI] [PubMed] [Google Scholar]
  14. Levick J. R. Flow through interstitium and other fibrous matrices. Q J Exp Physiol. 1987 Oct;72(4):409–437. doi: 10.1113/expphysiol.1987.sp003085. [DOI] [PubMed] [Google Scholar]
  15. Levick J. R., McDonald J. N. Fluid movement across synovium in healthy joints: role of synovial fluid macromolecules. Ann Rheum Dis. 1995 May;54(5):417–423. doi: 10.1136/ard.54.5.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Levick J. R., McDonald J. N. Microfibrillar meshwork of the synovial lining and associated broad banded collagen: a clue to identity. Ann Rheum Dis. 1990 Jan;49(1):31–36. doi: 10.1136/ard.49.1.31. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Levick J. R., McDonald J. N. Synovial capillary distribution in relation to altered pressure and permeability in knees of anaesthetized rabbits. J Physiol. 1989 Dec;419:477–492. doi: 10.1113/jphysiol.1989.sp017881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Levick J. R., McDonald J. N. Ultrastructure of transport pathways in stressed synovium of the knee in anaesthetized rabbits. J Physiol. 1989 Dec;419:493–508. doi: 10.1113/jphysiol.1989.sp017882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Maunsbach A. B. The influence of different fixatives and fixation methods on the ultrastructure of rat kidney proximal tubule cells. II. Effects of varying osmolality, ionic strength, buffer system and fixative concentration of glutaraldehyde solutions. J Ultrastruct Res. 1966 Jun;15(3):283–309. doi: 10.1016/s0022-5320(66)80110-7. [DOI] [PubMed] [Google Scholar]
  20. McDonald J. N., Levick J. R. Morphology of surface synoviocytes in situ at normal and raised joint pressure, studied by scanning electron microscopy. Ann Rheum Dis. 1988 Mar;47(3):232–240. doi: 10.1136/ard.47.3.232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Okada Y., Naka K., Minamoto T., Ueda Y., Oda Y., Nakanishi I., Timpl R. localization of type VI collagen in the lining cell layer of normal and rheumatoid synovium. Lab Invest. 1990 Nov;63(5):647–656. [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. Pitsillides A. A., Worrall J. G., Wilkinson L. S., Bayliss M. T., Edwards J. C. Hyaluronan concentration in non-inflamed and rheumatoid synovium. Br J Rheumatol. 1994 Jan;33(1):5–10. doi: 10.1093/rheumatology/33.1.5. [DOI] [PubMed] [Google Scholar]
  24. Pollock L. E., Lalor P., Revell P. A. Type IV collagen and laminin in the synovial intimal layer: an immunohistochemical study. Rheumatol Int. 1990;9(6):277–280. doi: 10.1007/BF00541324. [DOI] [PubMed] [Google Scholar]
  25. Revell P. A. Synovial lining cells. Rheumatol Int. 1989;9(2):49–51. doi: 10.1007/BF00270244. [DOI] [PubMed] [Google Scholar]
  26. Rittig M., Tittor F., Lütjen-Drecoll E., Mollenhauer J., Rauterberg J. Immunohistochemical study of extracellular material in the aged human synovial membrane. Mech Ageing Dev. 1992 Jul 15;64(3):219–234. doi: 10.1016/0047-6374(92)90080-w. [DOI] [PubMed] [Google Scholar]
  27. Scott J. E. Proteoglycan-fibrillar collagen interactions. Biochem J. 1988 Jun 1;252(2):313–323. doi: 10.1042/bj2520313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. WEIBEL E. R., KNIGHT B. W. A MORPHOMETRIC STUDY ON THE THICKNESS OF THE PULMONARY AIR-BLOOD BARRIER. J Cell Biol. 1964 Jun;21:367–396. doi: 10.1083/jcb.21.3.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wilkinson L. S., Pitsillides A. A., Worrall J. G., Edwards J. C. Light microscopic characterization of the fibroblast-like synovial intimal cell (synoviocyte). Arthritis Rheum. 1992 Oct;35(10):1179–1184. doi: 10.1002/art.1780351010. [DOI] [PubMed] [Google Scholar]
  30. Worrall J. G., Wilkinson L. S., Bayliss M. T., Edwards J. C. Zonal distribution of chondroitin-4-sulphate/dermatan sulphate and chondroitin-6-sulphate in normal and diseased human synovium. Ann Rheum Dis. 1994 Jan;53(1):35–38. doi: 10.1136/ard.53.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yamashita S., Ohkubo M. [Distribution and three-dimensional reconstruction of lymphatic vessels of the elbow joint capsule of rabbits]. Kaibogaku Zasshi. 1993 Oct;68(5):513–521. [PubMed] [Google Scholar]
  32. Zamparo O., Comper W. D. Hydraulic conductivity of chondroitin sulfate proteoglycan solutions. Arch Biochem Biophys. 1989 Oct;274(1):259–269. doi: 10.1016/0003-9861(89)90438-4. [DOI] [PubMed] [Google Scholar]

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