Advertisement

Clinical Reviews in Allergy & Immunology

, Volume 25, Issue 1, pp 89–104 | Cite as

Immunopathogenesis of Sjögren's syndrome

  • Andrea T. Borchers
  • Stanley M. Naguwa
  • Carl L. Keen
  • M. Eric Gershwin
Article

Abstract

Sjögren's syndrome (SS) is an autoimmune disease characterized by the sicca symptoms of dry eyes and dry mouth. Glandular dysfunction is thought to arise from destruction associated with lymphocytic infiltration. The degree of glandular destruction, however, does not correlate with the severity of sicca symptoms, suggesting that other mechanisms are involved, including abnormalities in parasympathetic neurotransmission. Autoantibodies against the muscarinic acetylcholine receptor have been implicated in this process, but multiple other autoantibodies have been found. Cytokines elaborated in the inflammatory lesions also appear to be involved and dysregulation of apoptosis are also involved in the pathogenesis of SS. A new two-stage model of SS has been proposed. First, there is a lymphocyte-independent phase during which inappropriate apoptosis results in the generation of apoptotic autoantigens which then attract lymphocytes. Subsequently, in the second lymphocyte-dependent phase, an immune attack causes further cell death and salivary dysfunction. Although the disease generally takes a rather stable and benign course, patients with SS have a significant risk of developing B cell lymphoma.

Index Entries

Sjögren's syndrome autoimmune disease autoantigens cytokines apoptosis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Kruize, A. A., Hené, R. J., van der Heide, A., Bodeutsch, C, de Wilde, P. C. M., van Bijsterveld, O. P., et al. (1996). Arthritis Rheum. 39, 297–303.PubMedGoogle Scholar
  2. 2.
    Soto-Rojas, A. E., Villa, A. R., Sifuentes-Osornio, J., Alarcon-Segovia, D., and Kraus, A. (1998), J. Rheumatol. 25, 906–910.PubMedGoogle Scholar
  3. 3.
    Soto-Rojas, A. E., Villa, A. R., Sifuentes-Osornio, J., Alarcon-Segovia, D., and Kraus, A. (1998), J. Rheumatol. 25, 906–910.PubMedGoogle Scholar
  4. 4.
    García-Carrasco, M., Ramos-Casals, M., Rosas, J., Pallarés, L., Calvo-Alen, J., Cervera, R., et al. (2002), Medicine (Baltimore) 81, 270–280.Google Scholar
  5. 5.
    Jonsson, R., Moen, K., Vestrheim, D., and Szodoray, P. (2002), Oral Dis. 8, 130–140.PubMedGoogle Scholar
  6. 6.
    Manthorpe, R., Jacobsson, L. T., Kirtava, Z., and Theander, E. (1998), Ann. Med. Interne (Paris) 149, 7–11.Google Scholar
  7. 7.
    Vitali, C., Bombardieri, S., Moutsopoulos, H. M., Balestrieri, G., Bencivelli, W., Bernstein, R. M., et al. (1993), Arthritis Rheum. 36, 340–347.PubMedGoogle Scholar
  8. 8.
    Vitali, C., Bombardieri, S., Moutsopoulos, H. M., Coll, J., Gerli, R., Hatron, P. Y., et al. (The European Study Group on Diagnostic Criteria for Sjögren's Syndrome). (1996), Ann. Rheum. Dis. 55, 116–121.PubMedGoogle Scholar
  9. 9.
    Fox, R. I., Robinson, C. A., Curd, J. G., Kozin, F., and Howell, F. (1986), Arthritis Rheum. 29, 577–585.PubMedGoogle Scholar
  10. 10.
    Manthorpe, R., Oxholm, P., Prause, J. U., and Schiodt, M. (1986), Scand. J. Rheumatol. Suppl. 61, 19–21.Google Scholar
  11. 11.
    Homma, M., Tojo, T., Akizuki, M., and Yamagata, H. (1986), Scand. J. Rheumatol. Suppl. 61, 26–27.PubMedGoogle Scholar
  12. 12.
    Skopouli, F. N., Drosos, A. A., Papaioannou, T., and Moutsopoulos, H. M. (1986), Scand. J. Rheumatol. Suppl. 61, 26–27.Google Scholar
  13. 13.
    Vitali, C., Bombardieri, S., Jonsson, R, Moutsopoulos, H. M., Alexander E. L., Carsons, S. E., et al. the European Study Group on Classification Criteria for Sjögren's Syndrome. (2002), Ann. Rheum. Dis. 61, 554–558.PubMedGoogle Scholar
  14. 14.
    The Japanese Medical Society for Sjögren's Syndrome. 1999, in Vol. 2002, http://www.fujitahuac.jp/~ktorikai/JapaneseCriterialE.html.Google Scholar
  15. 15.
    Manthorpe, R. (2002), Ann. Rheum. Dis. 61, 482–484.PubMedGoogle Scholar
  16. 16.
    Skopouli, F. N., Fox, P. C., Galanopoulou, V., Atkinson, J. C., Jaffe, E. S., and Moutsopoulos, H. M. (1991), J. Rheumatol. 18, 210–214.PubMedGoogle Scholar
  17. 17.
    Kizu, Y., Sakurai, H., Katagiri, S., Shinozaki, N., Ono, M., Tsubota, K., et al. (1996), J. Clin. Pathol. 49, 728–732.PubMedGoogle Scholar
  18. 18.
    Lee, M., Rutka, J. A., Slomovic, A. R., McComb, J., Bailey, D. J., and Bookman, A. A. M. (1998), J. Rheumatol. 25, 247–253PubMedGoogle Scholar
  19. 19.
    Manthorpe, R. (2002), Arthritis Rheum. 47, 114–115.PubMedGoogle Scholar
  20. 20.
    Zandbelt, M. M., Wentink, J. R. M., de Wilde, P. C. M., van Damme, P. A., van de Putte, L. B. A., and van den Hoogen, F. H. J. (2002), Rheumatology (Oxford) 41, 819–823.Google Scholar
  21. 21.
    Vivino, F. B., Gala, I., and Hermann, G. A. (2002), J. Rheumatol. 29, 938–944.PubMedGoogle Scholar
  22. 22.
    Izumi, M., Eguchi, K., Ohki, M., Uetani, M., Hayashi, K., Kita, M., et al. (1996), AJR Am. J. Roentgenol. 166, 1483–1487.PubMedGoogle Scholar
  23. 23.
    Makula, E., Pokorny, G., Kiss, M., Vörös, E., Kovács, L., Kovács, A., et al. (2000), Rheumatology (Oxford) 39, 97–104.Google Scholar
  24. 24.
    Niemelä, R. K., Pääkkö, E., Suramo, I., Takalo, R., and Hakala, M. (2001), Arthritis Rheum. 45, 512–518.PubMedGoogle Scholar
  25. 25.
    Mavragani, C. P., Tzioufas, A. G., and Moutsopoulos, H. M. (2000), Int. Arch. Allergy Immunol. 123, 46–57.PubMedGoogle Scholar
  26. 26.
    Kuwana, M., Okano, R., Ogawa, Y., Kaburaki, J., and Kawakami, Y. (2001), J. Immunol. 167, 5449–5456.PubMedGoogle Scholar
  27. 27.
    Watanabe, T., Tsuchida, T., Kanda, N., Mori, K., Hayashi, Y., and Tamaki, K. (1999), Arch. Dermatol. 135, 535–539.PubMedGoogle Scholar
  28. 28.
    Berra, A., Sterin-Borda, L., Bacman, S., and Borda, E. (2002), Clin. Immunol. 104, 49–57.PubMedGoogle Scholar
  29. 29.
    James, J. A., Herley, J. B., and Scofield, R. H. (2001), Curr. Opin. Rheumatol. 13, 370–376.PubMedGoogle Scholar
  30. 30.
    Reveille, J. D. (1992), Curr. Opin. Rheumatol. 4, 644–656PubMedGoogle Scholar
  31. 31.
    Kang, H. I., Fei, H. M., Saito, I., Sawada, S., Chen, S. L., Yi, D., et al. (1993), J. Immunol. 150, 3615–3623.PubMedGoogle Scholar
  32. 32.
    Guggenbuhl, P., Jean, S., Jego, P., Grosbois, B., Chalès, G., Semana, G., et al. (1998), J. Rheumatol. 25, 900–905.PubMedGoogle Scholar
  33. 33.
    Jean, S., Quelvennec, E., Alizadeh, M., Guggenbuhl, P. Birebent, B., Perdriger, A., et al. (1998), Clin. Exp. Rheumatol. 16, 725–728.PubMedGoogle Scholar
  34. 34.
    Bolstad, A. I., Wassmuth, R., Haga, H.-J., and Jonsson, R. (2001), J. Rheumatol. 28, 1554–1562.PubMedGoogle Scholar
  35. 35.
    Nakken, B., Johnsson, R., Brokstad, K. A., Omholt, K., Nerland, A. H., Haga, H. J., et al. (2001), Scand. J. Immunol. 54, 428–433.PubMedGoogle Scholar
  36. 36.
    Anaya, J. M., Correa, P. A., Mantilla, R. D., and Arcos-Burgos, M. (2002), Semin. Arthritis Rheum. 31, 396–405.PubMedGoogle Scholar
  37. 37.
    Tzioufas, A. G., Wassmuth, R., Dafni, U. G., Guialis, A., Haga, H. J., Isenberg, D. A., et al. (2002), Ann. Rheum. Dis. 61, 398–404.PubMedGoogle Scholar
  38. 38.
    Reveille, J. D., Macleod, M. J., Whittington, K., and Arnett, F. C. (1991), J. Immunol. 146, 3871–3876.PubMedGoogle Scholar
  39. 39.
    Rischmueller, M., Lester, S., Chen, Z., Champion, G., van den Berg, R., Beer, R., et al. (1998), Clin. Exp. Immunol. 111, 365–371.PubMedGoogle Scholar
  40. 40.
    Miyagawa, S., Shinohara, K., Nakajima, M., Kidoguchi K, Fujita, T., Fukumoto, T., et al. (1998), Arthritis Rheum. 41, 927–934.PubMedGoogle Scholar
  41. 41.
    Kumagai, S., Kanagawa, S., Morinobu, A., Takada, M., Nakamura, K., Sugai, S., et al. (1997), Arthritis Rheum. 40, 1685–1692.PubMedGoogle Scholar
  42. 42.
    Guggenbuhl, P., Veillard, É., Quelvenec, E., Jego, P., Semana, G., Jean, S., et al. (2000), Joint Bone Spine 67, 290–295.PubMedGoogle Scholar
  43. 43.
    Hadj Kacem, H., Kaddour, N., Adyel, F.-Z., Bahloul, Z., and Ayadi, H. (2001,), Rheumatology (Oxford) 40, 1370–1374.Google Scholar
  44. 44.
    Magnusson, V., Nakken, B., Bolstad, A. I., and Alrcón-Riquelme, M. E. (2001), Scand. J. Immunol. 54, 55–61.PubMedGoogle Scholar
  45. 45.
    Hulkkonen, J., Pertovaara, M., Antonen, J., Pasternack, A., and Hurme, M. (2001), Rheumatology (Oxford) 40, 656–661.Google Scholar
  46. 46.
    Hulkkonen, J., Pertovaara, M., Antonen, J., Lahdenpohja, N., Pasternack, A., and Hurme, M. (2001), Arthritis Rheuim. 44, 176–179.Google Scholar
  47. 47.
    Davidson, B. K., Kelly, C. A., and Griffiths, I. D. (1999), Rehumatology (Oxford) 38, 245–253.Google Scholar
  48. 48.
    Halse, A., Harley, J. B., Kroneld, U., and Jonsson, R. (1999), Clin. Exp. Immunol. 115, 203–207.PubMedGoogle Scholar
  49. 49.
    Tengnér, P., Halse, A. K., Haga, H. J., Jonsson, R., and Wahren-Herlenius, M. (1998), Arthritis Rheum. 41, 2238–2248.PubMedGoogle Scholar
  50. 50.
    Fox, R. I., Michelson, P., Casiano, C. A., Hayashi, J., and Stern, M. (2000), Clinics Dermatol. 18, 589–600.Google Scholar
  51. 51.
    Hakala, M. and Niemela, R. K. (2000), Lancet 355, 1032–1033.PubMedGoogle Scholar
  52. 52.
    Bacman, S., Sterin-Borda, L., Camusso, J. J., Arana, R., Hubscher, O., and Borda, E. (1998), Clin. Exp. Immunol. 104, 454–459.Google Scholar
  53. 53.
    Bacman, S., Perez Leiros, C., Sterin-Borda, L., Hubscher, O., Arana, R., and Borda, E. (1998), Invest. Ophthalmol. Visc. Sci. 39, 151–156.Google Scholar
  54. 54.
    Waterman, S. A., Gordon, T. P., and Rischmueller, M. (2000), Arthritis Rheum. 43, 1647–1654.PubMedGoogle Scholar
  55. 55.
    Bacman, S., Berra, A., Sterin-Borda, L., and Borda, E. (2001), Invest. Ophthalmol. Vis. Sci. 42, 321–327.PubMedGoogle Scholar
  56. 56.
    Robinson, C. P., Brayer, J., Yamachika, S., Esch, T. R., Peck, A. B., Stewart, C. A., et al. (1998), Proc. natl. Acad. Sci. USA 95, 7538–7543.PubMedGoogle Scholar
  57. 57.
    Beroukas, D., Goofellow, R., Hiscock, J., Jonsson, R., Gordon, T. P., and Waterman, S. A. (2002), Lab. Investig. 82, 203–210.PubMedGoogle Scholar
  58. 58.
    Rosas, J., Ramos-Casals, M., Ena, J., García-Carrasco, M., Verdu, J., Cervera, R., et al. (2002). Rheumatology (Oxford) 41, 670–675.Google Scholar
  59. 59.
    Fox, R. I., Kang, H. I., Ando, D., Abrams, J., and Pisa, E. (1994), J. Immunol. 152, 5532–5539.PubMedGoogle Scholar
  60. 60.
    Boumba, D., Skopouli, F. N., and Moutsopoulos, H. M. (1995), Br. J. Rheumatol. 34, 326–333.PubMedGoogle Scholar
  61. 61.
    Ajjan, R. A., McIntosh, R. S., Waterman, E. A., Watson, P. F., Franklin, C. D., Yeoman, C. M., et al. (1998), Br. J. Rheumatol. 37, 179–185.PubMedGoogle Scholar
  62. 62.
    Ogawa, N., Dang, H., Lazaridis, K., McGuff, H. S., Aufdemorte, T. B., and Talal, N. (1995), J. Interferon Cytokine Res. 15, 759–767.PubMedGoogle Scholar
  63. 63.
    Pflugfelder, S. C., Jones, D., Ji, Z., Afonso, A. and Monroy, D. (1999), Curr. Eye Res. 19, 201–211.PubMedGoogle Scholar
  64. 64.
    Grisius, M. M., Bermudez, D. K., and Fox, P. C. (1997), J. Rheumatol. 24, 1089–1091.PubMedGoogle Scholar
  65. 65.
    Tishler, M., Yaron, I., Shirazi, I., Yossipov, Y., and Yaron, M. (1999), Rheumatol. Int. 18, 125–127.PubMedGoogle Scholar
  66. 66.
    Tishler, M., Yaron, I., Geyer, O., Shirazi, I., Naftaliev, E., and Yaron, M. (1998), Ophthalmology 105, 2327–2329.PubMedGoogle Scholar
  67. 67.
    Ohyama, Y., Nakamura, S., Matsuzaki, G., Shinohara, M., Hiroki, A., Fujimura, T., et al. (1996), Arthritis Rheum. 39, 1376–1384.PubMedGoogle Scholar
  68. 68.
    Mitsias, D. I., Tziofas, A. G., Veiopoulou, C., Zintzaras, E., Tassios, I. K., Kogopoulou, O., et al. (2002), Clin. Exp. Immunol. 128, 562–568.PubMedGoogle Scholar
  69. 69.
    Rowe, D., Griffiths, M., Stewart, J., Novick, D., Beverley, P. C. L., and Isenberg, D. A. (1987), Ann. Rheum. Dis. 46, 580–586.PubMedGoogle Scholar
  70. 70.
    Matsummura, R., Umemiya, K., Goto, T., Nakazawa, T., Kagami, M., Tomioka, H., et al. (2001), Ann. Rheum. Dis. 60, 473–482.Google Scholar
  71. 71.
    Villarreal, G. M., Alcocer-Varela, J., and Llorente, L. (1996), Immunol. Lett. 49, 105–109.PubMedGoogle Scholar
  72. 72.
    Wahl, S. M. (1994), J. Exp. Med. 180, 1587–1590.PubMedGoogle Scholar
  73. 73.
    Lawrence, D. (1996), Eur. Cytok. Network 7, 363–374.Google Scholar
  74. 74.
    Cauli, A., Yanni, G., Pitzalis, C., Challacombe, S., and Parayi, G. S. (1995), Ann. Rheum. Dis. 54, 209–215.PubMedGoogle Scholar
  75. 75.
    Koski, H., Konttinen, Y. T., Gu, X. H., Hietanen, J., and Malmström, M. (1995), Ann. Rheum. Dis. 54, 744–747.PubMedGoogle Scholar
  76. 76.
    De Vita, S., Dolcetti, R., Ferraccioli, G., Pivetta, B., De Re, V., Gloghini, A., et al. (1995), J. Rheumatol. 22, 1674–1680.PubMedGoogle Scholar
  77. 77.
    Ferraccioli, G. F. and De Vita, S. (1997), Arthritis Rheum. 40, 987–990.PubMedGoogle Scholar
  78. 78.
    Amft, N. and Bowman, S. J. (2001), Scand. J. Immunol. 54, 62–69.PubMedGoogle Scholar
  79. 79.
    Cuello, C., Palladinetti, P., Tedla, N., Di Girolamo, N., Lloyd, A. R., McCluskey, P. J., et al. (1998), Br. J. Rheumatol. 37, 779–783.PubMedGoogle Scholar
  80. 80.
    Xanthou, G., Polihronis, M., Tzioufas, A. G., Paikos, S., Sideras, P., and Mautsopoulos, H. M. (2001), Arthritis Rheum. 44, 408–418.PubMedGoogle Scholar
  81. 81.
    Blink, E. J., Trapani, J. A., and Jans, D. A. (1999), Immunol. Cell Biol. 77, 206–215.PubMedGoogle Scholar
  82. 82.
    Humphreys-Beher, M. G., Peck, A. B., Dang, H. and Talal, N. (1999), Clin. Exp. Immunol. 116, 383–387.PubMedGoogle Scholar
  83. 83.
    Pollard, K. M. (2002), Arthritis Rheum. 46, 1699–1702.PubMedGoogle Scholar
  84. 84.
    Lorenz, H. M., Herrmann, M., Winkler, T., Gaipl, U., and Kalden, J. R. (2000), Apoptosis 5, 443–449.PubMedGoogle Scholar
  85. 85.
    Sumida, T., Matusmoto, I., Murata, H., Namekawa, T., Matsumura, R., Tomioka, H., et al. (1997), J. Immunol. 158, 1020–1025.PubMedGoogle Scholar
  86. 86.
    Kong, L., Ogawa, N., Nakabayashi, T., Liu, G. T., D'Souza, E., McGuff, H. S., et al. (1997), Arthritis Rheum. 40, 87–97.PubMedGoogle Scholar
  87. 87.
    Ohlsson, M., Skarstein, K., Bolstad, A. I., Johannessen, A. C., and Jonsson, R. (2001), Lab. Investig. 81, 95–105.PubMedGoogle Scholar
  88. 88.
    Polihronis, M., Tapinos, N. I., Theocharis, S. E., Economou, A., Kittas, C., and Moutsopoulos, H. M. (1998), Clin. Exp. Immunol. 114, 485–490.PubMedGoogle Scholar
  89. 89.
    Nakamura, H., Koji, Y., et al. (1998), Clin. Exp. Immunol. 114, 106–112.PubMedGoogle Scholar
  90. 90.
    Manganelli, P., Quaini, F., Andreoli, A. M., Lagrasta, C., Pilato, F. P., Zuccarelli, A., et al. (1997), J. Rheumatol. 24, 1552–1557.PubMedGoogle Scholar
  91. 91.
    Kong, L., Ogawa, N., McGuff, H. S., Nakabayashi, T., Sakata, K. M., Masago, R., et al., (1998), Clin. Immunol. Immunopathol. 88., 133–141.PubMedGoogle Scholar
  92. 92.
    Tsubota, K., Fujita, H., Tadano, K., Onoda, N., Tsuzaka, K., and Takeuchi, T. (2002), Clin. Exp. Immunol. 129, 177–182.PubMedGoogle Scholar
  93. 93.
    Casciola-Rosen, L. A., Anhalt, G., and Rosen, A. (1994), J. Exp. Med. 179, 1317–1330.PubMedGoogle Scholar
  94. 94.
    Miranda, M. E., Tseng, C. E., Rashbaum, W., Ochs, R. L., Casiano, C. A., Di Donato, F., et al. (1998), J. Immunol. 161, 5061–5069.PubMedGoogle Scholar
  95. 95.
    Jimenez, F., Aiba-Masago S, Al Hashim, I., Vela-Roch, N., Fernandes, G., Yeh, C. K., et al. (2002), Rheumatology (Oxford) 41, 338–342.Google Scholar
  96. 96.
    Casciola-Rosen, L. A., Andrade, F., Ulanet, D., Bang Wong W., and Rosen, A. (1999), J. Exp. Med. 190, 815–825.PubMedGoogle Scholar
  97. 97.
    Alpert, S., Kang, H. I., Weissman, I., and Fox, R. I. (1994), Arthritis Rheum. 37, 1046–1054.PubMedGoogle Scholar
  98. 98.
    Tsubota, K., Saito, I., and Miyasaka, N. (1994), Am. J. Ophthalmol. 117, 120–121.PubMedGoogle Scholar
  99. 99.
    Haneji, N., Nakamaura, T., Takio, K., Yanagi, K., Higashiyama, H., Saito, I., et al. (1997), Science 276, 604–607.PubMedGoogle Scholar
  100. 100.
    Witte, T., Matthias, T., Arnett, F. C., Peter, H. H., Hartung, K., Sachse, C., et al. (2000), J. Rheumatol. 27, 2617–2620.PubMedGoogle Scholar
  101. 101.
    Saegusa, K., Ishimaru, N., Yanagi, K., Mishima, K., Arakaki, R., Suda, T., et al. (2002), J. Immunol. 169, 1050–1057.PubMedGoogle Scholar
  102. 102.
    Kassan, S. S., Thomas, T. L., Moutsopoulos, H. M., Hoover, R., Kimberly, R. P., Budman, D. R., et al. (1978), Ann. Intern. Med. 89, 888–892.PubMedGoogle Scholar
  103. 103.
    Valesini, G., Priori, R., Bavoillot, D., Osborn, J., Danieli, M. G., Del Papa, N., et al. (1997), J. Rheumatol. 24, 2376–2380.PubMedGoogle Scholar
  104. 104.
    Ioannidis, J. P., Vaassiliou, V. A., and Moutsopoulos, H. M. (2002), Arthritis Rheum. 46, 741–747.PubMedGoogle Scholar
  105. 105.
    Voulgarelis, M., Dafni, U. G., Isenberg, D. A., and Moutsopoulos, H. M., Members of the European Concerted Action on Sjögren's Syndrome. (1999), Arthritis Rheum. 42, 1765–1772.PubMedGoogle Scholar
  106. 106.
    De Vita, S., De Marchi, G., Sacco, S., Gremese, E., Fabrisv, M., and Ferraccioli, G. (2001), Blood Cells Mol. Dis. 27, 757–766.PubMedGoogle Scholar
  107. 107.
    Tzioufas, A. G., Boumba, D. S., Skopouli, F. N., and Moutsopoulos, H. M. (1996), Arthritis Rheum. 39, 767–772.PubMedGoogle Scholar
  108. 108.
    Pertovaara, M., Pukkala, E., Laippala, P., Miettinen, A., and Pasternack, A. (2001), Ann. Rheum. Dis. 560, 467–472.Google Scholar
  109. 109.
    Du, M., Diss, T. C., Xu, C., Peng, H., Isaacson, P. G., and Pan, L. (1996), Leukemia 10, 1190–1197.PubMedGoogle Scholar
  110. 110.
    Bahler, D. W. and Swerdlow, S. H. (1998), Blood 91, 1864–1872.PubMedGoogle Scholar
  111. 111.
    Stott, D. I., Hiepe, F., Hummel, M., Steinhauser, G., and Berek, C. (1998), J. Clin. Investig. 102, 938–946.PubMedGoogle Scholar
  112. 112.
    De Vita, S., Boiocchi, M., Sorrentino, D., Carbone, A., Avellini, C., Dolcetti, R., et al. (1997), Arthritis Rheum. 40, 318–331.PubMedGoogle Scholar
  113. 113.
    Gellrich, S., Rutz, S., Borkowski, A., Golembowski, S., Gromnica-Ihle, E., Sterry, W., et al. (1999), Arthritis Rheum. 42, 240–247.PubMedGoogle Scholar
  114. 114.
    Skopouli, F. N., Dafni, U., Ioannidis, J. P., and Moutsopoulos, H. M. (2000), Semin. Arthritis Rheum. 29, 296–304.PubMedGoogle Scholar
  115. 115.
    Lamour, A., Le Corre, R., Pennec, Y.-L., and Youinou, P. (1995), J. Rheumatol. 22,, 2241–2245.PubMedGoogle Scholar
  116. 116.
    Henriksson, G., Manthorpe, R., Bredberg, A. (2000), Rheumatology (Oxford) 39, 142–147.Google Scholar

Copyright information

© Humana Press Inc 2003

Authors and Affiliations

  • Andrea T. Borchers
    • 1
  • Stanley M. Naguwa
    • 1
  • Carl L. Keen
    • 2
  • M. Eric Gershwin
    • 1
  1. 1.Division of Rheumatology, Allergy and Clinical ImmunologyUniversity of California at Davis, TB 192, School of MedicineDavis
  2. 2.Department of NutritionUniversity of California at DavisDavis

Personalised recommendations