Abstract
OBJECTIVES—The use of silicone implants in cosmetic and reconstructive surgery has been implicated in the development of autoimmune connective tissue diseases. Previous investigation of the influence of short-term silicone implantation using an experimental model of rheumatoid arthritis revealed no adverse influence upon disease despite the generation of autoantibodies against silicone bound proteins. This study was designed to examine the influence of long term implantation of different forms of silicone in collagen induced arthritis. METHODS—DBA/1 mice were surgically implanted with silicone elastomers, gel or oil nine months before immunisation with type II collagen emulsified in Freund's incomplete adjuvant. The incidence and severity of arthritis, antibodies to type II collagen, and serum cytokines were assessed and compared with sham implanted mice. Silicone implants were recovered, and autoantibodies to silicone bound proteins evaluated in arthritic and non-arthritic mice. RESULTS—Immunisation with CII/FIA resulted in a 30% arthritis incidence in sham implanted DBA/1 mice. Long term silicone implantation resulted in an increased incidence of arthritis, with a significant increase of 90% arthritis in animals implanted with silicone elastomers. Animals implanted with silicone elastomer also developed foreign body sarcomas during the study. Serum concentrations of interleukin 10 were increased in mice implanted with elastomers and immunised with CII/FIA, while interleukin 5 concentrations were significantly diminished in these mice. The production of autoantibodies to autologous silicone bound proteins, including anti-type I collagen antibody, was also attributed to the implantation of either silicone gel or silicone elastomer in type II collagen immunised animals. CONCLUSIONS—These data suggest that long term silicone implantation results in both the production of autoantibodies to connective tissue antigens and increased susceptibility to an experimental model of autoimmune disease.
Full Text
The Full Text of this article is available as a PDF (1.5 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bliven M. L., Wooley P. H., Pepys M. B., Otterness I. G. Murine type II collagen arthritis. Association of an acute-phase response with clinical course. Arthritis Rheum. 1986 Sep;29(9):1131–1138. doi: 10.1002/art.1780290911. [DOI] [PubMed] [Google Scholar]
- Brahn E., Peacock D. J., Banquerigo M. L., Liu D. Y. Effects of tumor necrosis factor alpha (TNF-alpha) on collagen arthritis. Lymphokine Cytokine Res. 1992 Oct;11(5):253–256. [PubMed] [Google Scholar]
- Brand I., Buoen L. C., Brand K. G. Foreign-body tumors of mice: strain and sex differences in latency and incidence. J Natl Cancer Inst. 1977 May;58(5):1443–1447. doi: 10.1093/jnci/58.5.1443. [DOI] [PubMed] [Google Scholar]
- Brand K. G., Brand I. Risk assessment of carcinogenesis at implantation sites. Plast Reconstr Surg. 1980 Oct;66(4):591–595. doi: 10.1097/00006534-198010000-00015. [DOI] [PubMed] [Google Scholar]
- Cooper S. M., Sriram S., Ranges G. E. Suppression of murine collagen-induced arthritis with monoclonal anti-Ia antibodies and augmentation with IFN-gamma. J Immunol. 1988 Sep 15;141(6):1958–1962. [PubMed] [Google Scholar]
- Cooper W. O., Fava R. A., Gates C. A., Cremer M. A., Townes A. S. Acceleration of onset of collagen-induced arthritis by intra-articular injection of tumour necrosis factor or transforming growth factor-beta. Clin Exp Immunol. 1992 Aug;89(2):244–250. doi: 10.1111/j.1365-2249.1992.tb06939.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cuéllar M. L., Scopelitis E., Tenenbaum S. A., Garry R. F., Silveira L. H., Cabrera G., Espinoza L. R. Serum antinuclear antibodies in women with silicone breast implants. J Rheumatol. 1995 Feb;22(2):236–240. [PubMed] [Google Scholar]
- Duffy D. M. Silicone: a critical review. Adv Dermatol. 1990;5:93–109. [PubMed] [Google Scholar]
- Ellis J. S., Chain B. M., Cooke A., Ibrahim M. A., Katz D. R. Adjuvant composition determines the induction of type II collagen-induced arthritis. Scand J Immunol. 1992 Jul;36(1):49–56. doi: 10.1111/j.1365-3083.1992.tb02939.x. [DOI] [PubMed] [Google Scholar]
- Engel A., Lamm S. H., Lai S. H. Human breast sarcoma and human breast implantation: a time trend analysis based on SEER data (1973-1990). J Clin Epidemiol. 1995 Apr;48(4):539–544. doi: 10.1016/0895-4356(94)00210-h. [DOI] [PubMed] [Google Scholar]
- Finegold I. Allergy to silicone: is it real? Compr Ther. 1996 Jun;22(6):393–398. [PubMed] [Google Scholar]
- Fuss I. J., Strober W., Dale J. K., Fritz S., Pearlstein G. R., Puck J. M., Lenardo M. J., Straus S. E. Characteristic T helper 2 T cell cytokine abnormalities in autoimmune lymphoproliferative syndrome, a syndrome marked by defective apoptosis and humoral autoimmunity. J Immunol. 1997 Feb 15;158(4):1912–1918. [PubMed] [Google Scholar]
- Hennekens C. H., Lee I. M., Cook N. R., Hebert P. R., Karlson E. W., LaMotte F., Manson J. E., Buring J. E. Self-reported breast implants and connective-tissue diseases in female health professionals. A retrospective cohort study. JAMA. 1996 Feb 28;275(8):616–621. [PubMed] [Google Scholar]
- Holmdahl R., Jansson L., Andersson M., Jonsson R. Genetic, hormonal and behavioural influence on spontaneously developing arthritis in normal mice. Clin Exp Immunol. 1992 Jun;88(3):467–472. doi: 10.1111/j.1365-2249.1992.tb06473.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hom J. T., Bendele A. M., Carlson D. G. In vivo administration with IL-1 accelerates the development of collagen-induced arthritis in mice. J Immunol. 1988 Aug 1;141(3):834–841. [PubMed] [Google Scholar]
- James S. J., Pogribna M., Miller B. J., Bolon B., Muskhelishvili L. Characterization of cellular response to silicone implants in rats: implications for foreign-body carcinogenesis. Biomaterials. 1997 May;18(9):667–675. doi: 10.1016/s0142-9612(96)00189-5. [DOI] [PubMed] [Google Scholar]
- Kasama T., Strieter R. M., Lukacs N. W., Lincoln P. M., Burdick M. D., Kunkel S. L. Interleukin-10 expression and chemokine regulation during the evolution of murine type II collagen-induced arthritis. J Clin Invest. 1995 Jun;95(6):2868–2876. doi: 10.1172/JCI117993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kessler D. A. The basis of the FDA's decision on breast implants. N Engl J Med. 1992 Jun 18;326(25):1713–1715. doi: 10.1056/NEJM199206183262525. [DOI] [PubMed] [Google Scholar]
- Killar L. M., Dunn C. J. Interleukin-1 potentiates the development of collagen-induced arthritis in mice. Clin Sci (Lond) 1989 May;76(5):535–538. doi: 10.1042/cs0760535. [DOI] [PubMed] [Google Scholar]
- Kossovsky N., Stassi J. A pathophysiological examination of the biophysics and bioreactivity of silicone breast implants. Semin Arthritis Rheum. 1994 Aug;24(1 Suppl 1):18–21. doi: 10.1016/0049-0172(94)90105-8. [DOI] [PubMed] [Google Scholar]
- Krams S. M., Cao S., Hayashi M., Villanueva J. C., Martinez O. M. Elevations in IFN-gamma, IL-5, and IL-10 in patients with the autoimmune disease primary biliary cirrhosis: association with autoantibodies and soluble CD30. Clin Immunol Immunopathol. 1996 Sep;80(3 Pt 1):311–320. doi: 10.1006/clin.1996.0129. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Llorente L., Zou W., Levy Y., Richaud-Patin Y., Wijdenes J., Alcocer-Varela J., Morel-Fourrier B., Brouet J. C., Alarcon-Segovia D., Galanaud P. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J Exp Med. 1995 Mar 1;181(3):839–844. doi: 10.1084/jem.181.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noone R. B. A review of the possible health implications of silicone breast implants. Cancer. 1997 May 1;79(9):1747–1756. doi: 10.1002/(sici)1097-0142(19970501)79:9<1747::aid-cncr17>3.0.co;2-y. [DOI] [PubMed] [Google Scholar]
- Rowley M. J., Cook A. D., Teuber S. S., Gershwin M. E. Antibodies to collagen: comparative epitope mapping in women with silicone breast implants, systemic lupus erythematosus and rheumatoid arthritis. J Autoimmun. 1994 Dec;7(6):775–789. doi: 10.1006/jaut.1994.1061. [DOI] [PubMed] [Google Scholar]
- Schaefer C. J., Whalen J. D., Knapp T., Wooley P. H. The influence of silicone implantation on type II collagen-induced arthritis in mice. Arthritis Rheum. 1997 Jun;40(6):1064–1072. doi: 10.1002/art.1780400611. [DOI] [PubMed] [Google Scholar]
- Solomon G. A clinical and laboratory profile of symptomatic women with silicone breast implants. Semin Arthritis Rheum. 1994 Aug;24(1 Suppl 1):29–37. doi: 10.1016/0049-0172(94)90107-4. [DOI] [PubMed] [Google Scholar]
- Stein S. H., Hart T. E., Hoffman W. H., Hendrix C. L., Gustke C. J., Watson S. C. Interleukin-10 promotes anti-collagen antibody production in type I diabetic peripheral B lymphocytes. J Periodontal Res. 1997 Jan;32(1 Pt 2):189–195. doi: 10.1111/j.1600-0765.1997.tb01404.x. [DOI] [PubMed] [Google Scholar]
- Sánchez-Guerrero J., Colditz G. A., Karlson E. W., Hunter D. J., Speizer F. E., Liang M. H. Silicone breast implants and the risk of connective-tissue diseases and symptoms. N Engl J Med. 1995 Jun 22;332(25):1666–1670. doi: 10.1056/NEJM199506223322502. [DOI] [PubMed] [Google Scholar]
- Sánchez-Guerrero J., Schur P. H., Sergent J. S., Liang M. H. Silicone breast implants and rheumatic disease. Clinical, immunologic, and epidemiologic studies. Arthritis Rheum. 1994 Feb;37(2):158–168. doi: 10.1002/art.1780370203. [DOI] [PubMed] [Google Scholar]
- Tenenbaum S. A., Rice J. C., Espinoza L. R., Cuéllar M. L., Plymale D. R., Sander D. M., Williamson L. L., Haislip A. M., Gluck O. S., Tesser J. R. Use of antipolymer antibody assay in recipients of silicone breast implants. Lancet. 1997 Feb 15;349(9050):449–454. doi: 10.1016/s0140-6736(96)07131-0. [DOI] [PubMed] [Google Scholar]
- Teuber S. S., Rowley M. J., Yoshida S. H., Ansari A. A., Gershwin M. E. Anti-collagen autoantibodies are found in women with silicone breast implants. J Autoimmun. 1993 Jun;6(3):367–377. doi: 10.1006/jaut.1993.1031. [DOI] [PubMed] [Google Scholar]
- Thomassen M. J., Buoen L. C., Brand I., Brand K. G. Foreign-body tumorigenesis in mice: DNA synthesis in surface-attached cells during preneoplasia. J Natl Cancer Inst. 1978 Aug;61(2):359–363. [PubMed] [Google Scholar]
- Walmsley M., Katsikis P. D., Abney E., Parry S., Williams R. O., Maini R. N., Feldmann M. Interleukin-10 inhibition of the progression of established collagen-induced arthritis. Arthritis Rheum. 1996 Mar;39(3):495–503. doi: 10.1002/art.1780390318. [DOI] [PubMed] [Google Scholar]
- Wooley P. H. Collagen-induced arthritis in the mouse. Methods Enzymol. 1988;162:361–373. doi: 10.1016/0076-6879(88)62091-x. [DOI] [PubMed] [Google Scholar]
- Wooley P. H., Luthra H. S., Stuart J. M., David C. S. Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates. J Exp Med. 1981 Sep 1;154(3):688–700. doi: 10.1084/jem.154.3.688. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wooley P. H., Seibold J. R., Whalen J. D., Chapdelaine J. M. Pristane-induced arthritis. The immunologic and genetic features of an experimental murine model of autoimmune disease. Arthritis Rheum. 1989 Aug;32(8):1022–1030. doi: 10.1002/anr.1780320812. [DOI] [PubMed] [Google Scholar]