Skip to main content
NCBI home page
Journal of Anatomy logoLink to Journal of Anatomy
. 2001 Nov;199(Pt 5):503–526. doi: 10.1046/j.1469-7580.2001.19950503.x

The anatomical basis for disease localisation in seronegative spondyloarthropathy at entheses and related sites

M BENJAMIN 1 ,✉, D McGONAGLE 2
PMCID: PMC1468363  PMID: 11760883

Abstract

The 2 major categories of idiopathic inflammatory arthritis are rheumatoid arthritis and the seronegative spondyloarthropathies. Whilst the synovium is the primary site of joint disease in the former, the primary site in the latter is less well defined. However, it has recently been proposed that enthesitis-associated changes in the spondyloarthropathies are primary and that all other joint manifestations are secondary. Nevertheless, some of the sites of disease localisation have not been adequately explained in terms of enthesitis. This article summarises current knowledge of the structure, function, blood supply, innervation, molecular composition and histopathology of the classic enthesis (i.e. the bony attachment of a tendon or ligament) and introduces the concept of ‘functional’ and articular ‘fibrocartilaginous’ entheses. The former are regions where tendons or ligaments wrap-around bony pulleys, but are not attached to them, and the latter are synovial joints that are lined by fibrocartilage rather than hyaline cartilage. We describe how these 3 types of entheses relate to other, and how all are prone to pathological changes in spondyloarthropathy. We propose that the inflammatory responses characteristic of spondyloarthropathies are triggered at these seemingly diverse sites, in genetically susceptible individuals, by a combination of anatomical factors which lead to higher levels of tissue microtrauma, and the deposition of microbes.

Keywords: Enthesis, fibrocartilage, tendons, ligaments, ankylosing spondylitis

Full Text

The Full Text of this article is available as a PDF (611.7 KB).

Selected References

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

  1. Ahlström H., Feltelius N., Nyman R., Hällgren R. Magnetic resonance imaging of sacroiliac joint inflammation. Arthritis Rheum. 1990 Dec;33(12):1763–1769. doi: 10.1002/art.1780331202. [DOI] [PubMed] [Google Scholar]
  2. BIERMANN H. Die Knochenbildung im Bereich periostaler-diaphysärer Sehnenund Bandanstäze. Z Zellforsch Mikrosk Anat. 1957;46(6):635–671. [PubMed] [Google Scholar]
  3. Ball J. Enthesopathy of rheumatoid and ankylosing spondylitis. Ann Rheum Dis. 1971 May;30(3):213–223. doi: 10.1136/ard.30.3.213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benjamin M., Evans E. J., Copp L. The histology of tendon attachments to bone in man. J Anat. 1986 Dec;149:89–100. [PMC free article] [PubMed] [Google Scholar]
  5. Benjamin M., Evans E. J. Fibrocartilage. J Anat. 1990 Aug;171:1–15. [PMC free article] [PubMed] [Google Scholar]
  6. Benjamin M., Evans E. J., Rao R. D., Findlay J. A., Pemberton D. J. Quantitative differences in the histology of the attachment zones of the meniscal horns in the knee joint of man. J Anat. 1991 Aug;177:127–134. [PMC free article] [PubMed] [Google Scholar]
  7. Benjamin M., Newell R. L., Evans E. J., Ralphs J. R., Pemberton D. J. The structure of the insertions of the tendons of biceps brachii, triceps and brachialis in elderly dissecting room cadavers. J Anat. 1992 Apr;180(Pt 2):327–332. [PMC free article] [PubMed] [Google Scholar]
  8. Benjamin M., Qin S., Ralphs J. R. Fibrocartilage associated with human tendons and their pulleys. J Anat. 1995 Dec;187(Pt 3):625–633. [PMC free article] [PubMed] [Google Scholar]
  9. Benjamin M., Ralphs J. R. Fibrocartilage in tendons and ligaments--an adaptation to compressive load. J Anat. 1998 Nov;193(Pt 4):481–494. doi: 10.1046/j.1469-7580.1998.19340481.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Benjamin M., Ralphs J. R., Newell R. L., Evans E. J. Loss of the fibrocartilaginous lining of the intertubercular sulcus associated with rupture of the tendon of the long head of biceps brachii. J Anat. 1993 Apr;182(Pt 2):281–285. [PMC free article] [PubMed] [Google Scholar]
  11. Benjamin M., Ralphs J. R., Shibu M., Irwin M. Capsular tissues of the proximal interphalangeal joint: normal composition and effects of Dupuytren's disease and rheumatoid arthritis. J Hand Surg Br. 1993 Jun;18(3):371–376. doi: 10.1016/0266-7681(93)90067-p. [DOI] [PubMed] [Google Scholar]
  12. Benjamin M., Ralphs J. R. Tendons and ligaments--an overview. Histol Histopathol. 1997 Oct;12(4):1135–1144. [PubMed] [Google Scholar]
  13. Benjamin M., Ralphs J. R. The cell and developmental biology of tendons and ligaments. Int Rev Cytol. 2000;196:85–130. doi: 10.1016/s0074-7696(00)96003-0. [DOI] [PubMed] [Google Scholar]
  14. Benjamin M., Rufai A., Ralphs J. R. The mechanism of formation of bony spurs (enthesophytes) in the achilles tendon. Arthritis Rheum. 2000 Mar;43(3):576–583. doi: 10.1002/1529-0131(200003)43:3<576::AID-ANR14>3.0.CO;2-A. [DOI] [PubMed] [Google Scholar]
  15. Bland Y. S., Ashhurst D. E. Fetal and postnatal development of the patella, patellar tendon and suprapatella in the rabbit; changes in the distribution of the fibrillar collagens. J Anat. 1997 Apr;190(Pt 3):327–342. doi: 10.1046/j.1469-7580.1997.19030327.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Bode-Lesniewska B., Dours-Zimmermann M. T., Odermatt B. F., Briner J., Heitz P. U., Zimmermann D. R. Distribution of the large aggregating proteoglycan versican in adult human tissues. J Histochem Cytochem. 1996 Apr;44(4):303–312. doi: 10.1177/44.4.8601689. [DOI] [PubMed] [Google Scholar]
  17. Boyde A., Jones S. J., Aerssens J., Dequeker J. Mineral density quantitation of the human cortical iliac crest by backscattered electron image analysis: variations with age, sex, and degree of osteoarthritis. Bone. 1995 Jun;16(6):619–627. doi: 10.1016/8756-3282(95)00119-x. [DOI] [PubMed] [Google Scholar]
  18. Braun J., Sieper J. Spondyloarthropathy. Lancet. 1999 May 1;353(9163):1526–1527. doi: 10.1016/S0140-6736(05)75137-0. [DOI] [PubMed] [Google Scholar]
  19. Braun J., Sieper J. The sacroiliac joint in the spondyloarthropathies. Curr Opin Rheumatol. 1996 Jul;8(4):275–287. doi: 10.1097/00002281-199607000-00003. [DOI] [PubMed] [Google Scholar]
  20. Burgos-Vargas R., Vázquez-Mellado J. The early clinical recognition of juvenile-onset ankylosing spondylitis and its differentiation from juvenile rheumatoid arthritis. Arthritis Rheum. 1995 Jun;38(6):835–844. doi: 10.1002/art.1780380618. [DOI] [PubMed] [Google Scholar]
  21. Canoso J. J. The premiere enthesis. J Rheumatol. 1998 Jul;25(7):1254–1256. [PubMed] [Google Scholar]
  22. Castelli W. A., Nasjleti C. E., Diaz-Perez R., Caffesse R. G. Histopathologic findings in temporomandibular joints of aged individuals. J Prosthet Dent. 1985 Mar;53(3):415–419. doi: 10.1016/0022-3913(85)90525-6. [DOI] [PubMed] [Google Scholar]
  23. Chiquet M. Regulation of extracellular matrix gene expression by mechanical stress. Matrix Biol. 1999 Oct;18(5):417–426. doi: 10.1016/s0945-053x(99)00039-6. [DOI] [PubMed] [Google Scholar]
  24. Clark J., Stechschulte D. J., Jr The interface between bone and tendon at an insertion site: a study of the quadriceps tendon insertion. J Anat. 1998 May;192(Pt 4):605–616. doi: 10.1046/j.1469-7580.1998.19240605.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. DiFrancesco L., Sokoloff L. Lipochondral degeneration of capsular tissue in osteoarthritic hips. Am J Surg Pathol. 1995 Mar;19(3):278–283. doi: 10.1097/00000478-199503000-00005. [DOI] [PubMed] [Google Scholar]
  26. Dougados M., van der Linden S., Juhlin R., Huitfeldt B., Amor B., Calin A., Cats A., Dijkmans B., Olivieri I., Pasero G. The European Spondylarthropathy Study Group preliminary criteria for the classification of spondylarthropathy. Arthritis Rheum. 1991 Oct;34(10):1218–1227. doi: 10.1002/art.1780341003. [DOI] [PubMed] [Google Scholar]
  27. Eulderink F., Ivanyi P., Weinreich S. Histopathology of murine ankylosing enthesopathy. Pathol Res Pract. 1998;194(11):797–803. doi: 10.1016/S0344-0338(98)80070-8. [DOI] [PubMed] [Google Scholar]
  28. Evans E. J., Benjamin M., Pemberton D. J. Fibrocartilage in the attachment zones of the quadriceps tendon and patellar ligament of man. J Anat. 1990 Aug;171:155–162. [PMC free article] [PubMed] [Google Scholar]
  29. Ferretti A., Ippolito E., Mariani P., Puddu G. Jumper's knee. Am J Sports Med. 1983 Mar-Apr;11(2):58–62. doi: 10.1177/036354658301100202. [DOI] [PubMed] [Google Scholar]
  30. François R. J., Gardner D. L., Degrave E. J., Bywaters E. G. Histopathologic evidence that sacroiliitis in ankylosing spondylitis is not merely enthesitis. Arthritis Rheum. 2000 Sep;43(9):2011–2024. doi: 10.1002/1529-0131(200009)43:9<2011::AID-ANR12>3.0.CO;2-Y. [DOI] [PubMed] [Google Scholar]
  31. François R. J. Ligament insertions into the human lumbar vertebral body. Acta Anat (Basel) 1975;91(3):467–480. [PubMed] [Google Scholar]
  32. Frowen P., Benjamin M. Variations in the quality of uncalcified fibrocartilage at the insertions of the extrinsic calf muscles in the foot. J Anat. 1995 Apr;186(Pt 2):417–421. [PMC free article] [PubMed] [Google Scholar]
  33. Fujii Y., Yoshida H., Sakou T. Immunohistochemical studies on tenascin in human yellow ligament. In Vivo. 1993 Mar-Apr;7(2):143–146. [PubMed] [Google Scholar]
  34. Fujioka H., Wang G. J., Mizuno K., Balian G., Hurwitz S. R. Changes in the expression of type-X collagen in the fibrocartilage of rat Achilles tendon attachment during development. J Orthop Res. 1997 Sep;15(5):675–681. doi: 10.1002/jor.1100150508. [DOI] [PubMed] [Google Scholar]
  35. Fujiwara K., Fujimoto M., Yonenobu K., Ochi T. A clinico-pathological study of cervical myelopathy in rheumatoid arthritis: post-mortem analysis of two cases. Eur Spine J. 1999;8(1):46–53. doi: 10.1007/s005860050126. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Fukuta S., Oyama M., Kavalkovich K., Fu F. H., Niyibizi C. Identification of types II, IX and X collagens at the insertion site of the bovine achilles tendon. Matrix Biol. 1998 Apr;17(1):65–73. doi: 10.1016/s0945-053x(98)90125-1. [DOI] [PubMed] [Google Scholar]
  37. Fukuyama S., Nakamura T., Ikeda T., Takagi K. The effect of mechanical stress on hypertrophy of the lumbar ligamentum flavum. J Spinal Disord. 1995 Apr;8(2):126–130. [PubMed] [Google Scholar]
  38. Gao J. Immunolocalization of types I, II, and X collagen in the tibial insertion sites of the medial meniscus. Knee Surg Sports Traumatol Arthrosc. 2000;8(1):61–65. doi: 10.1007/s001670050013. [DOI] [PubMed] [Google Scholar]
  39. Gao J., Messner K. Quantitative comparison of soft tissue-bone interface at chondral ligament insertions in the rabbit knee joint. J Anat. 1996 Apr;188(Pt 2):367–373. [PMC free article] [PubMed] [Google Scholar]
  40. Gao J., Räsänen T., Persliden J., Messner K. The morphology of ligament insertions after failure at low strain velocity: an evaluation of ligament entheses in the rabbit knee. J Anat. 1996 Aug;189(Pt 1):127–133. [PMC free article] [PubMed] [Google Scholar]
  41. Gillard G. C., Reilly H. C., Bell-Booth P. G., Flint M. H. The influence of mechanical forces on the glycosaminoglycan content of the rabbit flexor digitorum profundus tendon. Connect Tissue Res. 1979;7(1):37–46. doi: 10.3109/03008207909152351. [DOI] [PubMed] [Google Scholar]
  42. Giori N. J., Beaupré G. S., Carter D. R. Cellular shape and pressure may mediate mechanical control of tissue composition in tendons. J Orthop Res. 1993 Jul;11(4):581–591. doi: 10.1002/jor.1100110413. [DOI] [PubMed] [Google Scholar]
  43. Gotoh M., Hamada K., Yamakawa H., Tomonaga A., Inoue A., Fukuda H. Significance of granulation tissue in torn supraspinatus insertions: an immunohistochemical study with antibodies against interleukin-1 beta, cathepsin D, and matrix metalloprotease-1. J Orthop Res. 1997 Jan;15(1):33–39. doi: 10.1002/jor.1100150106. [DOI] [PubMed] [Google Scholar]
  44. Haines R. W., Mohuiddin A. Metaplastic bone. J Anat. 1968 Nov;103(Pt 3):527–538. [PMC free article] [PubMed] [Google Scholar]
  45. Hammer R. E., Maika S. D., Richardson J. A., Tang J. P., Taurog J. D. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human beta 2m: an animal model of HLA-B27-associated human disorders. Cell. 1990 Nov 30;63(5):1099–1112. doi: 10.1016/0092-8674(90)90512-d. [DOI] [PubMed] [Google Scholar]
  46. Harner C. D., Baek G. H., Vogrin T. M., Carlin G. J., Kashiwaguchi S., Woo S. L. Quantitative analysis of human cruciate ligament insertions. Arthroscopy. 1999 Oct;15(7):741–749. doi: 10.1016/s0749-8063(99)70006-x. [DOI] [PubMed] [Google Scholar]
  47. Hayashi K., Ishidou Y., Yonemori K., Nagamine T., Origuchi N., Maeda S., Imamura T., Kato M., Yoshida H., Sampath T. K. Expression and localization of bone morphogenetic proteins (BMPs) and BMP receptors in ossification of the ligamentum flavum. Bone. 1997 Jul;21(1):23–30. doi: 10.1016/s8756-3282(97)00080-x. [DOI] [PubMed] [Google Scholar]
  48. Hoshi K., Amizuka N., Sakou T., Kurokawa T., Ozawa H. Fibroblasts of spinal ligaments pathologically differentiate into chondrocytes induced by recombinant human bone morphogenetic protein-2: morphological examinations for ossification of spinal ligaments. Bone. 1997 Aug;21(2):155–162. doi: 10.1016/s8756-3282(97)00106-3. [DOI] [PubMed] [Google Scholar]
  49. Imai S., Hukuda S., Maeda T. Substance P-immunoreactive and protein gene product 9.5-immunoreactive nerve fibres in bone marrow of rat coccygeal vertebrae. J Orthop Res. 1994 Nov;12(6):853–859. doi: 10.1002/jor.1100120613. [DOI] [PubMed] [Google Scholar]
  50. Ippolito E., Postacchini F. Rupture and disinsertion of the proximal attachment of the adductor longus tendon. Case report with histochemical and ultrastructural study. Ital J Orthop Traumatol. 1981 Apr;7(1):79–85. [PubMed] [Google Scholar]
  51. Johnstone B., Yoo J. U. Autologous mesenchymal progenitor cells in articular cartilage repair. Clin Orthop Relat Res. 1999 Oct;(367 Suppl):S156–S162. doi: 10.1097/00003086-199910001-00017. [DOI] [PubMed] [Google Scholar]
  52. Järvinen T. A., Jozsa L., Kannus P., Järvinen T. L., Kvist M., Hurme T., Isola J., Kalimo H., Järvinen M. Mechanical loading regulates tenascin-C expression in the osteotendinous junction. J Cell Sci. 1999 Sep;112(Pt 18):3157–3166. doi: 10.1242/jcs.112.18.3157. [DOI] [PubMed] [Google Scholar]
  53. KNESE K. H., BIERMANN H. Die Knochenbildung an Sehnen- und Bandansătzen im Bereich ursprünglich chondraier Apophysen. Z Zellforsch Mikrosk Anat. 1958;49(2):142–187. [PubMed] [Google Scholar]
  54. Kampen W. U., Tillmann B. Age-related changes in the articular cartilage of human sacroiliac joint. Anat Embryol (Berl) 1998 Dec;198(6):505–513. doi: 10.1007/s004290050200. [DOI] [PubMed] [Google Scholar]
  55. Kannus P., Jozsa L., Järvinen T. A., Järvinen T. L., Kvist M., Natri A., Järvinen M. Location and distribution of non-collagenous matrix proteins in musculoskeletal tissues of rat. Histochem J. 1998 Nov;30(11):799–810. doi: 10.1023/a:1003448106673. [DOI] [PubMed] [Google Scholar]
  56. Kannus P., Jozsa L., Kvist M., Järvinen T. L., Maunu V. M., Hurme T., Järvinen M. Expression of osteocalcin in the patella of experimentally immobilized and remobilized rats. J Bone Miner Res. 1996 Jan;11(1):79–87. doi: 10.1002/jbmr.5650110112. [DOI] [PubMed] [Google Scholar]
  57. Katzman B. M., Klein D. M., Garven T. C., Caligiuri D. A., Kung J. Comparative histology of the annular and cruciform pulleys. J Hand Surg Br. 1999 Jun;24(3):272–274. doi: 10.1054/jhsb.1999.0069. [DOI] [PubMed] [Google Scholar]
  58. Kim W., Voloshin A. S. Role of plantar fascia in the load bearing capacity of the human foot. J Biomech. 1995 Sep;28(9):1025–1033. doi: 10.1016/0021-9290(94)00163-x. [DOI] [PubMed] [Google Scholar]
  59. Koch S., Tillmann B. The distal tendon of the biceps brachii. Structure and clinical correlations. Ann Anat. 1995 Jul;177(5):467–474. doi: 10.1016/S0940-9602(11)80155-X. [DOI] [PubMed] [Google Scholar]
  60. Koga H., Sakou T., Taketomi E., Hayashi K., Numasawa T., Harata S., Yone K., Matsunaga S., Otterud B., Inoue I. Genetic mapping of ossification of the posterior longitudinal ligament of the spine. Am J Hum Genet. 1998 Jun;62(6):1460–1467. doi: 10.1086/301868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Kolts I., Tillmann B., Lüllmann-Rauch R. The structure and vascularization of the biceps brachii long head tendon. Ann Anat. 1994 Jan;176(1):75–80. doi: 10.1016/s0940-9602(11)80420-6. [DOI] [PubMed] [Google Scholar]
  62. Koob T. J., Clark P. E., Hernandez D. J., Thurmond F. A., Vogel K. G. Compression loading in vitro regulates proteoglycan synthesis by tendon fibrocartilage. Arch Biochem Biophys. 1992 Oct;298(1):303–312. doi: 10.1016/0003-9861(92)90127-i. [DOI] [PubMed] [Google Scholar]
  63. Kumagai J., Sarkar K., Uhthoff H. K., Okawara Y., Ooshima A. Immunohistochemical distribution of type I, II and III collagens in the rabbit supraspinatus tendon insertion. J Anat. 1994 Oct;185(Pt 2):279–284. [PMC free article] [PubMed] [Google Scholar]
  64. Kumagai J., Sarkar K., Uhthoff H. K. The collagen types in the attachment zone of rotator cuff tendons in the elderly: an immunohistochemical study. J Rheumatol. 1994 Nov;21(11):2096–2100. [PubMed] [Google Scholar]
  65. Kumai T., Takakura Y., Akiyama K., Higashiyama I., Tamai S. Histopathological study of nonosseous tarsal coalition. Foot Ankle Int. 1998 Aug;19(8):525–531. doi: 10.1177/107110079801900804. [DOI] [PubMed] [Google Scholar]
  66. Lewis A. R., Ralphs J. R., Kneafsey B., Benjamin M. Distribution of collagens and glycosaminoglycans in the joint capsule of the proximal interphalangeal joint of the human finger. Anat Rec. 1998 Mar;250(3):281–291. doi: 10.1002/(SICI)1097-0185(199803)250:3<281::AID-AR3>3.0.CO;2-3. [DOI] [PubMed] [Google Scholar]
  67. Liu S. H., Panossian V., al-Shaikh R., Tomin E., Shepherd E., Finerman G. A., Lane J. M. Morphology and matrix composition during early tendon to bone healing. Clin Orthop Relat Res. 1997 Jun;(339):253–260. doi: 10.1097/00003086-199706000-00034. [DOI] [PubMed] [Google Scholar]
  68. Lorente Moltó F., Bonete Lluch D. J., Martí Perales V. Childhood periosteal chondroma. Arch Orthop Trauma Surg. 2000;120(10):605–608. doi: 10.1007/s004029900126. [DOI] [PubMed] [Google Scholar]
  69. Mackie E. J., Ramsey S. Expression of tenascin in joint-associated tissues during development and postnatal growth. J Anat. 1996 Feb;188(Pt 1):157–165. [PMC free article] [PubMed] [Google Scholar]
  70. Maksymowych W. P. Ankylosing spondylitis--at the interface of bone and cartilage. J Rheumatol. 2000 Oct;27(10):2295–2301. [PubMed] [Google Scholar]
  71. Malaviya P., Butler D. L., Boivin G. P., Smith F. N., Barry F. P., Murphy J. M., Vogel K. G. An in vivo model for load-modulated remodeling in the rabbit flexor tendon. J Orthop Res. 2000 Jan;18(1):116–125. doi: 10.1002/jor.1100180117. [DOI] [PubMed] [Google Scholar]
  72. Marsot-Dupuch K., Doyen J. E., Grauer W. O., de Givry S. C. SAPHO syndrome of the temporomandibular joint associated with sudden deafness. AJNR Am J Neuroradiol. 1999 May;20(5):902–905. [PMC free article] [PubMed] [Google Scholar]
  73. Martinod E., Zakine G., Fornes P., Zegdi R., d'Audiffret A., Aupecle B., Goussef N., Azorin J., Chachques J. C., Fabiani J. N. Métaplasie de tissu aortique en tissu trachéal. Perspectives chirurgicales. C R Acad Sci III. 2000 May;323(5):455–460. doi: 10.1016/s0764-4469(00)00150-5. [DOI] [PubMed] [Google Scholar]
  74. Maugars Y., Berthelot J. M., Ducloux J. M., Prost A. SAPHO syndrome: a followup study of 19 cases with special emphasis on enthesis involvement. J Rheumatol. 1995 Nov;22(11):2135–2141. [PubMed] [Google Scholar]
  75. McGonagle D., Emery P. Enthesitis, osteitis, microbes, biomechanics, and immune reactivity in ankylosing spondylitis. J Rheumatol. 2000 Oct;27(10):2302–2304. [PubMed] [Google Scholar]
  76. McGonagle D., Gibbon W., Emery P. Classification of inflammatory arthritis by enthesitis. Lancet. 1998 Oct 3;352(9134):1137–1140. doi: 10.1016/S0140-6736(97)12004-9. [DOI] [PubMed] [Google Scholar]
  77. McGonagle D., Gibbon W., O'Connor P., Green M., Pease C., Emery P. Characteristic magnetic resonance imaging entheseal changes of knee synovitis in spondylarthropathy. Arthritis Rheum. 1998 Apr;41(4):694–700. doi: 10.1002/1529-0131(199804)41:4<694::AID-ART17>3.0.CO;2-#. [DOI] [PubMed] [Google Scholar]
  78. McGonagle D., Khan M. A., Marzo-Ortega H., O'Connor P., Gibbon W., Emery P. Enthesitis in spondyloarthropathy. Curr Opin Rheumatol. 1999 Jul;11(4):244–250. doi: 10.1097/00002281-199907000-00004. [DOI] [PubMed] [Google Scholar]
  79. Meachim G., Allibone R. Topographical variation in the calcified zone of upper femoral articular cartilage. J Anat. 1984 Sep;139(Pt 2):341–352. [PMC free article] [PubMed] [Google Scholar]
  80. Mehr D., Pardubsky P. D., Martin J. A., Buckwalter J. A. Tenascin-C in tendon regions subjected to compression. J Orthop Res. 2000 Jul;18(4):537–545. doi: 10.1002/jor.1100180405. [DOI] [PubMed] [Google Scholar]
  81. Merrilees M. J., Flint M. H. Ultrastructural study of tension and pressure zones in a rabbit flexor tendon. Am J Anat. 1980 Jan;157(1):87–106. doi: 10.1002/aja.1001570109. [DOI] [PubMed] [Google Scholar]
  82. Messner K. Postnatal development of the cruciate ligament insertions in the rat knee. morphological evaluation and immunohistochemical study of collagens types I and II. Acta Anat (Basel) 1997;160(4):261–268. doi: 10.1159/000148020. [DOI] [PubMed] [Google Scholar]
  83. Milz S., McNeilly C., Putz R., Ralphs J. R., Benjamin M. Fibrocartilages in the extensor tendons of the interphalangeal joints of human toes. Anat Rec. 1998 Oct;252(2):264–270. doi: 10.1002/(SICI)1097-0185(199810)252:2<264::AID-AR11>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
  84. Milz S., Putz R., Ralphs J. R., Benjamin M. Fibrocartilage in the extensor tendons of the human metacarpophalangeal joints. Anat Rec. 1999 Oct 1;256(2):139–145. doi: 10.1002/(SICI)1097-0185(19991001)256:2<139::AID-AR4>3.0.CO;2-B. [DOI] [PubMed] [Google Scholar]
  85. Milz S., Valassis G., Büttner A., Maier M., Putz R., Ralphs J. R., Benjamin M. Fibrocartilage in the transverse ligament of the human acetabulum. J Anat. 2001 Feb;198(Pt 2):223–228. doi: 10.1046/j.1469-7580.2001.19820223.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Moss M. L. The functional matrix concept and its relationship to temporomandibular joint dysfunction and treatment. Dent Clin North Am. 1983 Jul;27(3):445–455. [PubMed] [Google Scholar]
  87. Murphy G. A., Pneumaticos S. G., Kamaric E., Noble P. C., Trevino S. G., Baxter D. E. Biomechanical consequences of sequential plantar fascia release. Foot Ankle Int. 1998 Mar;19(3):149–152. doi: 10.1177/107110079801900306. [DOI] [PubMed] [Google Scholar]
  88. Myerson M., Solomon G., Shereff M. Posterior tibial tendon dysfunction: its association with seronegative inflammatory disease. Foot Ankle. 1989 Apr;9(5):219–225. doi: 10.1177/107110078900900503. [DOI] [PubMed] [Google Scholar]
  89. Nakamura T., Hashimoto N., Maeda Y., Ikeda T., Nakagawa H., Takagi K. Degeneration and ossification of the yellow ligament in unstable spine. J Spinal Disord. 1990 Dec;3(4):288–292. [PubMed] [Google Scholar]
  90. Niyibizi C., Sagarrigo Visconti C., Gibson G., Kavalkovich K. Identification and immunolocalization of type X collagen at the ligament-bone interface. Biochem Biophys Res Commun. 1996 May 15;222(2):584–589. doi: 10.1006/bbrc.1996.0787. [DOI] [PubMed] [Google Scholar]
  91. Ogata S., Uhthoff H. K. Acromial enthesopathy and rotator cuff tear. A radiologic and histologic postmortem investigation of the coracoacromial arch. Clin Orthop Relat Res. 1990 May;(254):39–48. [PubMed] [Google Scholar]
  92. Okada K., Oka S., Tohge K., Ono K., Yonenobu K., Hosoya T. Thoracic myelopathy caused by ossification of the ligamentum flavum. Clinicopathologic study and surgical treatment. Spine (Phila Pa 1976) 1991 Mar;16(3):280–287. doi: 10.1097/00007632-199103000-00005. [DOI] [PubMed] [Google Scholar]
  93. Olivieri I., Barozzi L., Favaro L., Pierro A., de Matteis M., Borghi C., Padula A., Ferri S., Pavlica P. Dactylitis in patients with seronegative spondylarthropathy. Assessment by ultrasonography and magnetic resonance imaging. Arthritis Rheum. 1996 Sep;39(9):1524–1528. doi: 10.1002/art.1780390912. [DOI] [PubMed] [Google Scholar]
  94. Palesy P. D. Tendon and ligament insertions--a possible source of musculoskeletal pain. Cranio. 1997 Jul;15(3):194–202. doi: 10.1080/08869634.1997.11746012. [DOI] [PubMed] [Google Scholar]
  95. Petersen W., Bobka T., Stein V., Tillmann B. Blood supply of the peroneal tendons: injection and immunohistochemical studies of cadaver tendons. Acta Orthop Scand. 2000 Apr;71(2):168–174. doi: 10.1080/000164700317413148. [DOI] [PubMed] [Google Scholar]
  96. Petersen W., Laprell H. Insertion of autologous tendon grafts to the bone: a histological and immunohistochemical study of hamstring and patellar tendon grafts. Knee Surg Sports Traumatol Arthrosc. 2000;8(1):26–31. doi: 10.1007/s001670050006. [DOI] [PubMed] [Google Scholar]
  97. Petersen W., Tillmann B. Age-related blood and lymph supply of the knee menisci. A cadaver study. Acta Orthop Scand. 1995 Aug;66(4):308–312. doi: 10.3109/17453679508995550. [DOI] [PubMed] [Google Scholar]
  98. Petersen W., Tillmann B. Blood and lymph supply of the posterior cruciate ligament: a cadaver study. Knee Surg Sports Traumatol Arthrosc. 1999;7(1):42–50. doi: 10.1007/s001670050119. [DOI] [PubMed] [Google Scholar]
  99. Petersen W., Tillmann B. Structure and vascularization of the cruciate ligaments of the human knee joint. Anat Embryol (Berl) 1999 Sep;200(3):325–334. doi: 10.1007/s004290050283. [DOI] [PubMed] [Google Scholar]
  100. Pinczewski L. A., Clingeleffer A. J., Otto D. D., Bonar S. F., Corry I. S. Integration of hamstring tendon graft with bone in reconstruction of the anterior cruciate ligament. Arthroscopy. 1997 Oct;13(5):641–643. doi: 10.1016/s0749-8063(97)90194-8. [DOI] [PubMed] [Google Scholar]
  101. Poole A. R. The histopathology of ankylosing spondylitis: are there unifying hypotheses? Am J Med Sci. 1998 Oct;316(4):228–233. doi: 10.1097/00000441-199810000-00002. [DOI] [PubMed] [Google Scholar]
  102. Prockop D. J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science. 1997 Apr 4;276(5309):71–74. doi: 10.1126/science.276.5309.71. [DOI] [PubMed] [Google Scholar]
  103. Regan M. H., Case D. T., Brundige J. C. Articular surface defects in the third metatarsal and third cuneiform: nonosseous tarsal coalition. Am J Phys Anthropol. 1999 May;109(1):53–65. doi: 10.1002/(SICI)1096-8644(199905)109:1<53::AID-AJPA6>3.0.CO;2-P. [DOI] [PubMed] [Google Scholar]
  104. Reháková Z., Capková J., Stepánková R., Sinkora J., Louzecká A., Ivanyi P., Weinreich S. Germ-free mice do not develop ankylosing enthesopathy, a spontaneous joint disease. Hum Immunol. 2000 Jun;61(6):555–558. doi: 10.1016/s0198-8859(00)00122-1. [DOI] [PubMed] [Google Scholar]
  105. Roberts S., Bains M. A., Kwan A., Menage J., Eisenstein S. M. Type X collagen in the human invertebral disc: an indication of repair or remodelling? Histochem J. 1998 Feb;30(2):89–95. doi: 10.1023/a:1003278915981. [DOI] [PubMed] [Google Scholar]
  106. Rudnicki M. A., Schnegelsberg P. N., Stead R. H., Braun T., Arnold H. H., Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 1993 Dec 31;75(7):1351–1359. doi: 10.1016/0092-8674(93)90621-v. [DOI] [PubMed] [Google Scholar]
  107. Rufai A., Ralphs J. R., Benjamin M. Structure and histopathology of the insertional region of the human Achilles tendon. J Orthop Res. 1995 Jul;13(4):585–593. doi: 10.1002/jor.1100130414. [DOI] [PubMed] [Google Scholar]
  108. SCHNEIDER H. Zur Struktur der Sehnenansatzzonen. Z Anat Entwicklungsgesch. 1956;119(5):431–456. [PubMed] [Google Scholar]
  109. Sagarriga Visconti C., Kavalkovich K., Wu J., Niyibizi C. Biochemical analysis of collagens at the ligament-bone interface reveals presence of cartilage-specific collagens. Arch Biochem Biophys. 1996 Apr 1;328(1):135–142. doi: 10.1006/abbi.1996.0153. [DOI] [PubMed] [Google Scholar]
  110. Sakou T., Taketomi E., Matsunaga S., Yamaguchi M., Sonoda S., Yashiki S. Genetic study of ossification of the posterior longitudinal ligament in the cervical spine with human leukocyte antigen haplotype. Spine (Phila Pa 1976) 1991 Nov;16(11):1249–1252. doi: 10.1097/00007632-199111000-00001. [DOI] [PubMed] [Google Scholar]
  111. Sampson S. P., Badalamente M. A., Hurst L. C., Seidman J. Pathobiology of the human A1 pulley in trigger finger. J Hand Surg Am. 1991 Jul;16(4):714–721. doi: 10.1016/0363-5023(91)90200-u. [DOI] [PubMed] [Google Scholar]
  112. Sano H., Ishii H., Trudel G., Uhthoff H. K. Histologic evidence of degeneration at the insertion of 3 rotator cuff tendons: a comparative study with human cadaveric shoulders. J Shoulder Elbow Surg. 1999 Nov-Dec;8(6):574–579. doi: 10.1016/s1058-2746(99)90092-7. [DOI] [PubMed] [Google Scholar]
  113. Scapinelli R. Morphological and functional changes of the lumbar spinous processes in the elderly. Surg Radiol Anat. 1989;11(2):129–133. doi: 10.1007/BF02096469. [DOI] [PubMed] [Google Scholar]
  114. Scapinelli R. Vascular anatomy of the human cruciate ligaments and surrounding structures. Clin Anat. 1997;10(3):151–162. doi: 10.1002/(SICI)1098-2353(1997)10:3<151::AID-CA1>3.0.CO;2-X. [DOI] [PubMed] [Google Scholar]
  115. Senga K., Kobayashi M., Hattori H., Yasue K., Mizutani H., Ueda M., Hoshino T. Type VI collagen in mouse masseter tendon, from osseous attachment to myotendinous junction. Anat Rec. 1995 Nov;243(3):294–302. doi: 10.1002/ar.1092430303. [DOI] [PubMed] [Google Scholar]
  116. Shaibani A., Workman R., Rothschild B. M. The significance of enthesopathy as a skeletal phenomenon. Clin Exp Rheumatol. 1993 Jul-Aug;11(4):399–403. [PubMed] [Google Scholar]
  117. Sieper J., Braun J., Kingsley G. H. Report on the Fourth International Workshop on Reactive Arthritis. Arthritis Rheum. 2000 Apr;43(4):720–734. doi: 10.1002/1529-0131(200004)43:4<720::AID-ANR2>3.0.CO;2-8. [DOI] [PubMed] [Google Scholar]
  118. Soma C. A., Mandelbaum B. R. Achilles tendon disorders. Clin Sports Med. 1994 Oct;13(4):811–823. [PubMed] [Google Scholar]
  119. Takae R., Matsunaga S., Origuchi N., Yamamoto T., Morimoto N., Suzuki S., Sakou T. Immunolocalization of bone morphogenetic protein and its receptors in degeneration of intervertebral disc. Spine (Phila Pa 1976) 1999 Jul 15;24(14):1397–1401. doi: 10.1097/00007632-199907150-00002. [DOI] [PubMed] [Google Scholar]
  120. Taurog J. D., Richardson J. A., Croft J. T., Simmons W. A., Zhou M., Fernández-Sueiro J. L., Balish E., Hammer R. E. The germfree state prevents development of gut and joint inflammatory disease in HLA-B27 transgenic rats. J Exp Med. 1994 Dec 1;180(6):2359–2364. doi: 10.1084/jem.180.6.2359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. URIST M. R., MAZET R., Jr, McLEAN F. C. The pathogenesis and treatment of delayed union and non-union; a survey of eighty-five ununited fractures of the shaft of the tibia and one hundred control cases with similar injuries. J Bone Joint Surg Am. 1954 Oct;36-A(5):931–passim. [PubMed] [Google Scholar]
  122. Vajda E. G., Bloebaum R. D. Age-related hypermineralization in the female proximal human femur. Anat Rec. 1999 Jun 1;255(2):202–211. doi: 10.1002/(SICI)1097-0185(19990601)255:2<202::AID-AR10>3.0.CO;2-0. [DOI] [PubMed] [Google Scholar]
  123. Waggett A. D., Ralphs J. R., Kwan A. P., Woodnutt D., Benjamin M. Characterization of collagens and proteoglycans at the insertion of the human Achilles tendon. Matrix Biol. 1998 Mar;16(8):457–470. doi: 10.1016/s0945-053x(98)90017-8. [DOI] [PubMed] [Google Scholar]
  124. Yonemori K., Imamura T., Ishidou Y., Okano T., Matsunaga S., Yoshida H., Kato M., Sampath T. K., Miyazono K., ten Dijke P. Bone morphogenetic protein receptors and activin receptors are highly expressed in ossified ligament tissues of patients with ossification of the posterior longitudinal ligament. Am J Pathol. 1997 Apr;150(4):1335–1347. [PMC free article] [PubMed] [Google Scholar]
  125. Yoshida M., Shima K., Taniguchi Y., Tamaki T., Tanaka T. Hypertrophied ligamentum flavum in lumbar spinal canal stenosis. Pathogenesis and morphologic and immunohistochemical observation. Spine (Phila Pa 1976) 1992 Nov;17(11):1353–1360. doi: 10.1097/00007632-199211000-00015. [DOI] [PubMed] [Google Scholar]
  126. Yutani Y., Yano Y., Ohashi H., Takigawa M., Yamano Y. Cartilaginous differentiation in the joint capsule. J Bone Miner Metab. 1999;17(1):7–10. doi: 10.1007/s007740050056. [DOI] [PubMed] [Google Scholar]
  127. Zeidman S. M., Ducker T. B. Rheumatoid arthritis. Neuroanatomy, compression, and grading of deficits. Spine (Phila Pa 1976) 1994 Oct 15;19(20):2259–2266. doi: 10.1097/00007632-199410150-00003. [DOI] [PubMed] [Google Scholar]
  128. de Bosset P., Gordon D. A., Smythe H. A., Urowitz M. B., Koehler B. E., Singal D. P. Comparison of osteitis condensans ilii and ankylosing spondylitis in female patients: clinical, radiological and HLA typing characteristics. J Chronic Dis. 1978 Mar;31(3):171–181. doi: 10.1016/0021-9681(78)90032-2. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Anatomy are provided here courtesy of Anatomical Society of Great Britain and Ireland

RESOURCES