Sjögren Syndrome-associated lymphomas: An update on pathogenesis and management

British Journal of Haematology

Volumn 168, Issue 3, 2015, Pages 317-327

  Nocturne, Gaetane ^a   Mariette, Xavier ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Auto immunity; Lymphomagenesis; Mucosa associated lymphoid tissue lymphoma; NF kB; Sj gren syndrome

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; BENDAMUSTINE; CD135 ANTIGEN; CHEMOKINE RECEPTOR CXCR5; CHLORAMBUCIL; CXCL13 CHEMOKINE; CYCLOPHOSPHAMIDE; DOXORUBICIN; FLT3 LIGAND; FLUDARABINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 14; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; LA ANTIBODY; PREDNISONE; PROTEIN BCL 10; RHEUMATOID FACTOR; RITUXIMAB; RO ANTIBODY; VINCRISTINE;

AUTOIMMUNE DISEASE; B CELL LYMPHOMA; B LYMPHOCYTE; CANCER SURVIVAL; CELIAC DISEASE; CELL ACTIVATION; CRYOGLOBULINEMIA; DISEASE ACTIVITY; DISEASE DURATION; EVENT FREE SURVIVAL; GENETIC PREDISPOSITION; GERMINAL CENTER; HEPATITIS C; HISTOPATHOLOGY; HUMAN; IMMUNE COMPLEX DISEASE; LYMPHADENOPATHY; LYMPHOCYTOPENIA; LYMPHOMA; MARGINAL ZONE LYMPHOMA; NODAL MARGINAL ZONE LYMPHOMA; NONHODGKIN LYMPHOMA; NUCLEAR MAGNETIC RESONANCE IMAGING; OVERALL SURVIVAL; PATHOGENESIS; REVIEW; RHEUMATOID ARTHRITIS; SIALOADENITIS; SJOEGREN SYNDROME; SYSTEMIC LUPUS ERYTHEMATOSUS; CELL TRANSFORMATION; COMPLICATION; IMMUNOLOGY; LYMPHOMA, B-CELL, MARGINAL ZONE; RISK FACTOR; SJOGREN'S SYNDROME;

CELL TRANSFORMATION, NEOPLASTIC; HEPATITIS C, CHRONIC; HUMANS; LYMPHOMA, B-CELL, MARGINAL ZONE; RISK FACTORS; SJOGREN'S SYNDROME;

EID: 84921342740     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.13192     Document Type: Review

References (93)

1. Ahlin, E., Mathsson, L., Eloranta, M.L., Jonsdottir, T., Gunnarsson, I., Ronnblom, L. & Ronnelid, J. (2012) Autoantibodies associated with RNA are more enriched than anti-dsDNA antibodies in circulating immune complexes in SLE. Lupus, 21, 586-595.
2. Alamanos, Y., Tsifetaki, N., Voulgari, P.V., Venetsanopoulou, A.I., Siozos, C. & Drosos, A.A. (2006) Epidemiology of primary Sjogren's syndrome in north-west Greece, 1982-2003. Rheumatology (Oxford), 45, 187-191.
3. Ambrus, J.L. Jr & Fauci, A.S. (1985) Human B lymphoma cell line producing B cell growth factor. The Journal of Clinical Investigation, 75, 732-739.
4. Amft, N., Curnow, S.J., Scheel-Toellner, D., Devadas, A., Oates, J., Crocker, J., Hamburger, J., Ainsworth, J., Mathews, J., Salmon, M., Bowman, S.J. & Buckley, C.D. (2001) Ectopic expression of the B cell-attracting chemokine BCA-1 (CXCL13) on endothelial cells and within lymphoid follicles contributes to the establishment of germinal center-like structures in Sjogren's syndrome. Arthritis and Rheumatism, 44, 2633-2641.
5. Anaya, J.M., McGuff, H.S., Banks, P.M. & Talal, N. (1996) Clinicopathological factors relating malignant lymphoma with Sjogren's syndrome. Seminars in Arthritis and Rheumatism, 25, 337-346.
6. Bachy, E., Besson, C., Suarez, F. & Hermine, O. (2010) Hepatitis C virus infection and lymphoma. Mediterranean Journal of Hematology and Infectious Diseases, 2, e2010004.
7. Bende, R.J., Aarts, W.M., Riedl, R.G., de Jong, D., Pals, S.T. & van Noesel, C.J. (2005) Among B cell non-Hodgkin's lymphomas, MALT lymphomas express a unique antibody repertoire with frequent rheumatoid factor reactivity. Journal of Experimental Medicine, 201, 1229-1241.
8. Bi, Y., Zeng, N., Chanudet, E., Huang, Y., Hamoudi, R.A., Liu, H., Dong, G., Watkins, A.J., Ley, S.C., Zou, L., Chen, R., Zhu, X. & Du, M.Q. (2011) A20 inactivation in ocular adnexal MALT lymphoma. Haematologica, 97, 926-930.
9. Bombardieri, M., Barone, F., Humby, F., Kelly, S., McGurk, M., Morgan, P., Challacombe, S., De Vita, S., Valesini, G., Spencer, J. & Pitzalis, C. (2007) Activation-induced cytidine deaminase expression in follicular dendritic cell networks and interfollicular large B cells supports functionality of ectopic lymphoid neogenesis in autoimmune sialoadenitis and MALT lymphoma in Sjogren's syndrome. Journal of Immunology, 179, 4929-4938.
10. Bombardieri, M., Barone, F., Lucchesi, D., Nayar, S., van den Berg, W.B., Proctor, G., Buckley, C.D. & Pitzalis, C. (2012) Inducible tertiary lymphoid structures, autoimmunity, and exocrine dysfunction in a novel model of salivary gland inflammation in C57BL/6 mice. Journal of Immunology, 189, 3767-3776.
11. Bowman, S.J., Ibrahim, G.H., Holmes, G., Hamburger, J. & Ainsworth, J.R. (2004) Estimating the prevalence among Caucasian women of primary Sjogren's syndrome in two general practices in Birmingham, UK. Scandinavian Journal of Rheumatology, 33, 39-43.
12. Brkic, Z., Maria, N.I., van Helden-Meeuwsen, C.G., van de Merwe, J.P., van Daele, P.L., Dalm, V.A., Wildenberg, M.E., Beumer, W., Drexhage, H.A. & Versnel, M.A. (2012) Prevalence of interferon type I signature in CD14 monocytes of patients with Sjogren's syndrome and association with disease activity and BAFF gene expression. Annals of the Rheumatic Diseases, 72, 728-735.
13. Chanudet, E., Ye, H., Ferry, J., Bacon, C.M., Adam, P., Muller-Hermelink, H.K., Radford, J., Pileri, S.A., Ichimura, K., Collins, V.P., Hamoudi, R.A., Nicholson, A.G., Wotherspoon, A.C., Isaacson, P.G. & Du, M.Q. (2009) A20 deletion is associated with copy number gain at the TNFA/B/C locus and occurs preferentially in translocation-negative MALT lymphoma of the ocular adnexa and salivary glands. The Journal of Pathology, 217, 420-430.
14. Coornaert, B., Baens, M., Heyninck, K., Bekaert, T., Haegman, M., Staal, J., Sun, L., Chen, Z.J., Marynen, P. & Beyaert, R. (2008) T cell antigen receptor stimulation induces MALT1 paracaspase-mediated cleavage of the NF-kappaB inhibitor A20. Nature Immunology, 9, 263-271.
15. Croia, C., Astorri, E., Murray-Brown, W., Willis, A., Brokstad, K.A., Sutcliffe, N., Piper, K., Jonsson, R., Tappuni, A.R., Pitzalis, C. & Bombardieri, M. (2014) Implication of Epstein-Barr virus infection in disease-specific autoreactive B cell activation in ectopic lymphoid structures of Sjogren's syndrome. Arthritis & Rheumatology, 66, 2545-2557.
16. Daridon, C., Devauchelle, V., Hutin, P., Le Berre, R., Martins-Carvalho, C., Bendaoud, B., Dueymes, M., Saraux, A., Youinou, P. & Pers, J.O. (2007) Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjogren's syndrome. Arthritis and Rheumatism, 56, 1134-1144.
17. De Re, V., De Vita, S., Marzotto, A., Gloghini, A., Pivetta, B., Gasparotto, D., Cannizzaro, R., Carbone, A. & Boiocchi, M. (2000) Pre-malignant and malignant lymphoproliferations in an HCV-infected type II mixed cryoglobulinemic patient are sequential phases of an antigen-driven pathological process. International Journal of Cancer, 87, 211-216.
18. Drexler, H.G. (1996) Expression of FLT3 receptor and response to FLT3 ligand by leukemic cells. Leukemia, 10, 588-599.
19. Drexler, H.G. & Quentmeier, H. (2004) FLT3: receptor and ligand. Growth Factors, 22, 71-73.
20. Dunn, P., Kuo, T.T., Shih, L.Y., Lin, T.L., Wang, P.N., Kuo, M.C. & Tang, C.C. (2004) Primary salivary gland lymphoma: a clinicopathologic study of 23 cases in Taiwan. Acta Haematologica, 112, 203-208.
21. Ekstrom Smedby, K., Vajdic, C.M., Falster, M., Engels, E.A., Martinez-Maza, O., Turner, J., Hjalgrim, H., Vineis, P., Seniori Costantini, A., Bracci, P.M., Holly, E.A., Willett, E., Spinelli, J.J., La Vecchia, C., Zheng, T., Becker, N., De Sanjose, S., Chiu, B.C., Dal Maso, L., Cocco, P., Maynadie, M., Foretova, L., Staines, A., Brennan, P., Davis, S., Severson, R., Cerhan, J.R., Breen, E.C., Birmann, B., Grulich, A.E. & Cozen, W. (2008) Autoimmune disorders and risk of non-Hodgkin lymphoma subtypes: a pooled analysis within the InterLymph Consortium. Blood, 111, 4029-4038.
22. Fallah, M., Liu, X., Ji, J., Forsti, A., Sundquist, K. & Hemminki, K. (2014) Autoimmune diseases associated with non-Hodgkin lymphoma: a nationwide cohort study. Annals of Oncology, pii, mdu365.
23. Ferreri, A.J. & Zucca, E. (2007) Marginal-zone lymphoma. Critical Reviews in Oncology Hematology, 63, 245-256.
24. Gottenberg, J.E., Sellam, J., Ittah, M., Lavie, F., Proust, A., Zouali, H., Sordet, C., Sibilia, J., Kimberly, R.P., Mariette, X. & Miceli-Richard, C. (2006) No evidence for an association between the -871 T/C promoter polymorphism in the B-cell-activating factor gene and primary Sjogren's syndrome. Arthritis Research & Therapy, 8, R30.
25. Gottenberg, J.E., Seror, R., Miceli-Richard, C., Benessiano, J., Devauchelle-Pensec, V., Dieude, P., Dubost, J.J., Fauchais, A.L., Goeb, V., Hachulla, E., Hatron, P.Y., Larroche, C., Le Guern, V., Morel, J., Perdriger, A., Puechal, X., Rist, S., Saraux, A., Sene, D., Sibilia, J., Vittecoq, O., Nocturne, G., Ravaud, P. & Mariette, X. (2013) Serum levels of beta2-microglobulin and free light chains of immunoglobulins are associated with systemic disease activity in primary Sjogren's syndrome. Data at enrollment in the prospective ASSESS cohort. PLoS ONE, 8, e59868.
26. Hermine, O., Lefrere, F., Bronowicki, J.P., Mariette, X., Jondeau, K., Eclache-Saudreau, V., Delmas, B., Valensi, F., Cacoub, P., Brechot, C., Varet, B. & Troussard, X. (2002) Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. New England Journal of Medicine, 347, 89-94.
27. Ioannidis, J.P., Vassiliou, V.A. & Moutsopoulos, H.M. (2002) Long-term risk of mortality and lymphoproliferative disease and predictive classification of primary Sjogren's syndrome. Arthritis and Rheumatism, 46, 741-747.
28. Ittah, M., Miceli-Richard, C., Eric Gottenberg, J., Lavie, F., Lazure, T., Ba, N., Sellam, J., Lepajolec, C. & Mariette, X. (2006) B cell-activating factor of the tumor necrosis factor family (BAFF) is expressed under stimulation by interferon in salivary gland epithelial cells in primary Sjogren's syndrome. Arthritis Research & Therapy, 8, R51.
29. Ittah, M., Miceli-Richard, C., Gottenberg, J.E., Sellam, J., Eid, P., Lebon, P., Pallier, C., Lepajolec, C. & Mariette, X. (2008) Viruses induce high expression of BAFF by salivary gland epithelial cells through TLR- and type-I IFN-dependent and -independent pathways. European Journal of Immunology, 38, 1058-1064.
30. Ittah, M., Miceli-Richard, C., Lebon, P., Pallier, C., Lepajolec, C. & Mariette, X. (2011) Induction of B cell-activating factor by viral infection is a general phenomenon, but the types of viruses and mechanisms depend on cell type. Journal of Innate Immunity, 3, 200-207.
31. Johnsen, S.J., Brun, J.G., Goransson, L.G., Smastuen, M.C., Johannesen, T.B., Haldorsen, K., Harboe, E., Jonsson, R., Meyer, P.A. & Omdal, R. (2012) The risk of non-hodgkin lymphoma in primary sjogren's syndrome, a population-based study. Arthritis Care & Research, 65, 816-821.
32. Kassan, S.S., Thomas, T.L., Moutsopoulos, H.M., Hoover, R., Kimberly, R.P., Budman, D.R., Costa, J., Decker, J.L. & Chused, T.M. (1978) Increased risk of lymphoma in sicca syndrome. Annals of Internal Medicine, 89, 888-892.
33. Kato, M., Sanada, M., Kato, I., Sato, Y., Takita, J., Takeuchi, K., Niwa, A., Chen, Y., Nakazaki, K., Nomoto, J., Asakura, Y., Muto, S., Tamura, A., Iio, M., Akatsuka, Y., Hayashi, Y., Mori, H., Igarashi, T., Kurokawa, M., Chiba, S., Mori, S., Ishikawa, Y., Okamoto, K., Tobinai, K., Nakagama, H., Nakahata, T., Yoshino, T., Kobayashi, Y. & Ogawa, S. (2009) Frequent inactivation of A20 in B-cell lymphomas. Nature, 459, 712-716.
34. Kauppi, M., Pukkala, E. & Isomaki, H. (1997) Elevated incidence of hematologic malignancies in patients with Sjogren's syndrome compared with patients with rheumatoid arthritis (Finland). Cancer Causes and Control, 8, 201-204.
35. Lavie, F., Miceli-Richard, C., Ittah, M., Sellam, J., Gottenberg, J.E. & Mariette, X. (2008) B-cell activating factor of the tumour necrosis factor family expression in blood monocytes and T cells from patients with primary Sjogren's syndrome. Scandinavian Journal of Immunology, 67, 185-192.
36. Leadbetter, E.A., Rifkin, I.R., Hohlbaum, A.M., Beaudette, B.C., Shlomchik, M.J. & Marshak-Rothstein, A. (2002) Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature, 416, 603-607.
37. Lessard, C.J., Li, H., Adrianto, I., Ice, J.A., Rasmussen, A., Grundahl, K.M., Kelly, J.A., Dozmorov, M.G., Miceli-Richard, C., Bowman, S., Lester, S., Eriksson, P., Eloranta, M.L., Brun, J.G., Goransson, L.G., Harboe, E., Guthridge, J.M., Kaufman, K.M., Kvarnstrom, M., Jazebi, H., Cunninghame Graham, D.S., Grandits, M.E., Nazmul-Hossain, A.N., Patel, K., Adler, A.J., Maier-Moore, J.S., Farris, A.D., Brennan, M.T., Lessard, J.A., Chodosh, J., Gopalakrishnan, R., Hefner, K.S., Houston, G.D., Huang, A.J., Hughes, P.J., Lewis, D.M., Radfar, L., Rohrer, M.D., Stone, D.U., Wren, J.D., Vyse, T.J., Gaffney, P.M., James, J.A., Omdal, R., Wahren-Herlenius, M., Illei, G.G., Witte, T., Jonsson, R., Rischmueller, M., Ronnblom, L., Nordmark, G., Ng, W.F., Mariette, X., Anaya, J.M., Rhodus, N.L., Segal, B.M., Scofield, R.H., Montgomery, C.G., Harley, J.B. & Sivils, K.L. (2013) Variants at multiple loci implicated in both innate and adaptive immune responses are associated with Sjogren's syndrome. Nature Genetics, 45, 1284-1292.
38. Lichtenfeld, J.L., Kirschner, R.H. & Wiernik, P.H. (1976) Familial Sjogren's syndrome with associated primary salivary gland lymphoma. American Journal of Medicine, 60, 286-292.
39. Litinskiy, M.B., Nardelli, B., Hilbert, D.M., He, B., Schaffer, A., Casali, P. & Cerutti, A. (2002) DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nature Immunology, 3, 822-829.
40. Mackay, F., Woodcock, S.A., Lawton, P., Ambrose, C., Baetscher, M., Schneider, P., Tschopp, J. & Browning, J.L. (1999) Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. Journal of Experimental Medicine, 190, 1697-1710.
41. Makula, E., Pokorny, G., Kiss, M., Voros, E., Kovacs, L., Kovacs, A., Csernay, L. & Palko, A. (2000) The place of magnetic resonance and ultrasonographic examinations of the parotid gland in the diagnosis and follow-up of primary Sjogren's syndrome. Rheumatology (Oxford), 39, 97-104.
42. Mariette, X. (2001) Lymphomas complicating Sjogren's syndrome and hepatitis C virus infection may share a common pathogenesis: chronic stimulation of rheumatoid factor B cells. Annals of the Rheumatic Diseases, 60, 1007-1010.
43. Mariette, X., Roux, S., Zhang, J., Bengoufa, D., Lavie, F., Zhou, T. & Kimberly, R. (2003) The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjogren's syndrome. Annals of the Rheumatic Diseases, 62, 168-171.
44. Martin, T., Weber, J.C., Levallois, H., Labouret, N., Soley, A., Koenig, S., Korganow, A.S. & Pasquali, J.L. (2000) Salivary gland lymphomas in patients with Sjogren's syndrome may frequently develop from rheumatoid factor B cells. Arthritis and Rheumatism, 43, 908-916.
45. Mc Guire, C., Wieghofer, P., Elton, L., Muylaert, D., Prinz, M., Beyaert, R. & van Loo, G. (2013) Paracaspase MALT1 deficiency protects mice from autoimmune-mediated demyelination. Journal of Immunology, 190, 2896-2903.
46. Musone, S.L., Taylor, K.E., Nititham, J., Chu, C., Poon, A., Liao, W., Lam, E.T., Ma, A., Kwok, P.Y. & Criswell, L.A. (2011) Sequencing of TNFAIP3 and association of variants with multiple autoimmune diseases. Genes and Immunity, 12, 176-182.
47. Negri, E., Little, D., Boiocchi, M., La Vecchia, C. & Franceschi, S. (2004) B-cell non-Hodgkin's lymphoma and hepatitis C virus infection: a systematic review. International Journal of Cancer, 111, 1-8.
48. Nezos, A., Papageorgiou, A., Fragoulis, G., Ioakeimidis, D., Koutsilieris, M., Tzioufas, A.G., Moutsopoulos, H.M., Voulgarelis, M. & Mavragani, C.P. (2014) B-cell activating factor genetic variants in lymphomagenesis associated with primary Sjogren's syndrome. Journal of Autoimmunity, 51, 89-98.
49. Nishishinya, M.B., Pereda, C.A., Munoz-Fernandez, S., Pego-Reigosa, J.M., Rua-Figueroa, I., Andreu, J.L., Fernandez-Castro, M., Rosas, J. & Loza Santamaria, E. (2014) Identification of lymphoma predictors in patients with primary Sjogren's syndrome: a systematic literature review and meta-analysis. Rheumatology International, doi:10.1007/s00296-014-3051-x.
50. Nocturne, G., Boudaoud, S., Miceli-Richard, C., Viengchareun, S., Lazure, T., Nititham, J., Taylor, K.E., Ma, A., Busato, F., Melki, J., Lessard, C.J., Sivils, K.L., Dubost, J.J., Hachulla, E., Gottenberg, J.E., Lombes, M., Tost, J., Criswell, L.A. & Mariette, X. (2013) Germline and somatic genetic variations of TNFAIP3 in lymphoma complicating primary Sjogren's syndrome. Blood, 122, 4068-4076.
51. Nossent, J.C., Lester, S., Zahra, D., Mackay, C.R. & Rischmueller, M. (2008) Polymorphism in the 5' regulatory region of the B-lymphocyte activating factor gene is associated with the Ro/La autoantibody response and serum BAFF levels in primary Sjogren's syndrome. Rheumatology (Oxford), 47, 1311-1316.
52. Ono, M., Ono, M., Watanabe, K., Miyashita, Y., Inagaki, Y. & Ueki, H. (1999) A study of anti-carbonic anhydrase II antibodies in rheumatic autoimmune diseases. Journal of Dermatological Science, 21, 183-186.
53. Pertovaara, M., Pukkala, E., Laippala, P., Miettinen, A. & Pasternack, A. (2001) A longitudinal cohort study of Finnish patients with primary Sjogren's syndrome: clinical, immunological, and epidemiological aspects. Annals of the Rheumatic Diseases, 60, 467-472.
54. Pisa, E.K., Pisa, P., Kang, H.I. & Fox, R.I. (1991) High frequency of t(14;18) translocation in salivary gland lymphomas from Sjogren's syndrome patients. Journal of Experimental Medicine, 174, 1245-1250.
55. Pitzalis, C., Jones, G.W., Bombardieri, M. & Jones, S.A. (2014) Ectopic lymphoid-like structures in infection, cancer and autoimmunity. Nature Reviews Immunology, 14, 447-462.
56. Pollard, R.P., Pijpe, J., Bootsma, H., Spijkervet, F.K., Kluin, P.M., Roodenburg, J.L., Kallenberg, C.G., Vissink, A. & van Imhoff, G.W. (2011) Treatment of mucosa-associated lymphoid tissue lymphoma in Sjogren's syndrome: a retrospective clinical study. Journal of Rheumatology, 38, 2198-2208.
57. Qin, B., Wang, J., Yang, Z., Yang, M., Ma, N., Huang, F. & Zhong, R. (2014) Epidemiology of primary Sjogren's syndrome: a systematic review and meta-analysis. Annals of the Rheumatic Diseases, doi:10.1136/annrheumdis-2014-205375.
58. Quartuccio, L., Salvin, S., Fabris, M., Maset, M., Pontarini, E., Isola, M. & De Vita, S. (2012) BLyS upregulation in Sjogren's syndrome associated with lymphoproliferative disorders, higher ESSDAI score and B-cell clonal expansion in the salivary glands. Rheumatology (Oxford), 52, 276-281.
59. Ray, R.J., Paige, C.J., Furlonger, C., Lyman, S.D. & Rottapel, R. (1996) Flt3 ligand supports the differentiation of early B cell progenitors in the presence of interleukin-11 and interleukin-7. European Journal of Immunology, 26, 1504-1510.
60. Reksten, T.R., Johnsen, S.J., Jonsson, M.V., Omdal, R., Brun, J.G., Theander, E., Eriksson, P., Wahren-Herlenius, M., Jonsson, R. & Nordmark, G. (2014) Genetic associations to germinal centre formation in primary Sjogren's syndrome. Annals of the Rheumatic Diseases, 73, 1253-1258.
61. Risselada, A.P., Kruize, A.A., Goldschmeding, R., Lafeber, F.P., Bijlsma, J.W. & van Roon, J.A. (2014) The prognostic value of routinely performed minor salivary gland assessments in primary Sjogren's syndrome. Annals of the Rheumatic Diseases, 73, 1537-1540.
62. Royer, B., Cazals-Hatem, D., Sibilia, J., Agbalika, F., Cayuela, J.M., Soussi, T., Maloisel, F., Clauvel, J.P., Brouet, J.C. & Mariette, X. (1997) Lymphomas in patients with Sjogren's syndrome are marginal zone B-cell neoplasms, arise in diverse extranodal and nodal sites, and are not associated with viruses. Blood, 90, 766-775.
63. Rummel, M.J., Niederle, N., Maschmeyer, G., Banat, G.A., von Grunhagen, U., Losem, C., Kofahl-Krause, D., Heil, G., Welslau, M., Balser, C., Kaiser, U., Weidmann, E., Durk, H., Ballo, H., Stauch, M., Roller, F., Barth, J., Hoelzer, D., Hinke, A. & Brugger, W. (2013) Bendamustine plus rituximab versus CHOP plus rituximab as first-line treatment for patients with indolent and mantle-cell lymphomas: an open-label, multicentre, randomised, phase 3 non-inferiority trial. Lancet, 381, 1203-1210.
64. Saadoun, D., Pineton de Chambrun, M., Hermine, O., Karras, A., Choquet, S., Jego, P., Decaux, O. & Cacoub, P. (2013) Using rituximab plus fludarabine and cyclophosphamide as a treatment for refractory mixed cryoglobulinemia associated with lymphoma. Arthritis Care & Research, 65, 643-647.
65. Salomonsson, S., Jonsson, M.V., Skarstein, K., Brokstad, K.A., Hjelmstrom, P., Wahren-Herlenius, M. & Jonsson, R. (2003) Cellular basis of ectopic germinal center formation and autoantibody production in the target organ of patients with Sjogren's syndrome. Arthritis and Rheumatism, 48, 3187-3201.
66. Sang, A., Niu, H., Cullen, J., Choi, S.C., Zheng, Y.Y., Wang, H., Shlomchik, M.J. & Morel, L. (2014) Activation of rheumatoid factor-specific B cells is antigen dependent and occurs preferentially outside of germinal centers in the lupus-prone NZM2410 mouse model. Journal of Immunology, 193, 1609-1621.
67. de Sanjose, S., Benavente, Y., Vajdic, C.M., Engels, E.A., Morton, L.M., Bracci, P.M., Spinelli, J.J., Zheng, T., Zhang, Y., Franceschi, S., Talamini, R., Holly, E.A., Grulich, A.E., Cerhan, J.R., Hartge, P., Cozen, W., Boffetta, P., Brennan, P., Maynadie, M., Cocco, P., Bosch, R., Foretova, L., Staines, A., Becker, N. & Nieters, A. (2008) Hepatitis C and non-Hodgkin lymphoma among 4784 cases and 6269 controls from the International Lymphoma Epidemiology Consortium. Clinical Gastroenterology and Hepatology, 6, 451-458.
68. Schollkopf, C., Smedby, K.E., Hjalgrim, H., Rostgaard, K., Panum, I., Vinner, L., Chang, E.T., Glimelius, B., Porwit, A., Sundstrom, C., Hansen, M., Adami, H.O. & Melbye, M. (2008) Hepatitis C infection and risk of malignant lymphoma. International Journal of Cancer, 122, 1885-1890.
69. Seror, R., Ravaud, P., Bowman, S.J., Baron, G., Tzioufas, A., Theander, E., Gottenberg, J.E., Bootsma, H., Mariette, X. & Vitali, C. (2010) EULAR Sjogren's syndrome disease activity index: development of a consensus systemic disease activity index for primary Sjogren's syndrome. Annals of the Rheumatic Diseases, 69, 1103-1109.
70. Shen, L., Zhang, C., Wang, T., Brooks, S., Ford, R.J., Lin-Lee, Y.C., Kasianowicz, A., Kumar, V., Martin, L., Liang, P., Cowell, J. & Ambrus, J.L. Jr (2006) Development of autoimmunity in IL-14alpha-transgenic mice. Journal of Immunology, 177, 5676-5686.
71. Shen, L., Suresh, L., Li, H., Zhang, C., Kumar, V., Pankewycz, O. & Ambrus, J.L. Jr (2009) IL-14 alpha, the nexus for primary Sjogren's disease in mice and humans. Clinical Immunology, 130, 304-312.
72. Sisto, M., Lisi, S., Lofrumento, D.D., Ingravallo, G., Maiorano, E. & D'Amore, M. (2011) A failure of TNFAIP3 negative regulation maintains sustained NF-kappaB activation in Sjogren's syndrome. Histochemistry and Cell Biology, 135, 615-625.
73. Smedby, K.E., Akerman, M., Hildebrand, H., Glimelius, B., Ekbom, A. & Askling, J. (2005) Malignant lymphomas in coeliac disease: evidence of increased risks for lymphoma types other than enteropathy-type T cell lymphoma. Gut, 54, 54-59.
74. Smedby, K.E., Hjalgrim, H., Askling, J., Chang, E.T., Gregersen, H., Porwit-MacDonald, A., Sundstrom, C., Akerman, M., Melbye, M., Glimelius, B. & Adami, H.O. (2006) Autoimmune and chronic inflammatory disorders and risk of non-Hodgkin lymphoma by subtype. Journal of the National Cancer Institute, 98, 51-60.
75. Solans-Laque, R., Lopez-Hernandez, A., Bosch-Gil, J.A., Palacios, A., Campillo, M. & Vilardell-Tarres, M. (2011) Risk, predictors, and clinical characteristics of lymphoma development in primary Sjogren's syndrome. Seminars in Arthritis and Rheumatism, 41, 415-423.
76. Song, H., Tong, D., Cha, Z. & Bai, J. (2012) C-X-C chemokine receptor type 5 gene polymorphisms are associated with non-Hodgkin lymphoma. Molecular Biology Reports, 39, 8629-8635.
77. Streubel, B., Huber, D., Wohrer, S., Chott, A. & Raderer, M. (2004) Frequency of chromosomal aberrations involving MALT1 in mucosa-associated lymphoid tissue lymphoma in patients with Sjogren's syndrome. Clinical Cancer Research, 10, 476-480.
78. Swerdlow, S.H., Campo, E., Harris, N.L., Jaffe, E.S., Pileri, S.A., Stein, H., Thiele, J. & Vardiman, J.W. (2008) WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues. IARC Press, Lyon.
79. Tapinos, N., Polihronis, M. & Moutsopoulos, H.M. (1999) Lymphoma development in primary Sjögren's Syndrome. Arthritis & Rheumatism, 7, 1466-1472.
80. Theander, E. & Mandl, T. (2014) Primary Sjogren's syndrome: the diagnostic and prognostic value of salivary gland ultrasonography using a simplified scoring system. Arthritis Care & Research, 66, 1102-1107.
81. Theander, E., Henriksson, G., Ljungberg, O., Mandl, T., Manthorpe, R. & Jacobsson, L.T. (2006) Lymphoma and other malignancies in primary Sjogren's syndrome: a cohort study on cancer incidence and lymphoma predictors. Annals of the Rheumatic Diseases, 65, 796-803.
82. Theander, E., Vasaitis, L., Baecklund, E., Nordmark, G., Warfvinge, G., Liedholm, R., Brokstad, K., Jonsson, R. & Jonsson, M.V. (2011) Lymphoid organisation in labial salivary gland biopsies is a possible predictor for the development of malignant lymphoma in primary Sjogren's syndrome. Annals of the Rheumatic Diseases, 70, 1363-1368.
83. Tobon, G.J., Renaudineau, Y., Hillion, S., Cornec, D., Devauchelle-Pensec, V., Youinou, P. & Pers, J.O. (2010) The Fms-like tyrosine kinase 3 ligand, a mediator of B cell survival, is also a marker of lymphoma in primary Sjogren's syndrome. Arthritis and Rheumatism, 62, 3447-3456.
84. Tomsic, M., Logar, D., Grmek, M., Perkovic, T. & Kveder, T. (1999) Prevalence of Sjogren's syndrome in Slovenia. Rheumatology (Oxford), 38, 164-170.
85. Tzioufas, A.G., Boumba, D.S., Skopouli, F.N. & Moutsopoulos, H.M. (1996) Mixed monoclonal cryoglobulinemia and monoclonal rheumatoid factor cross-reactive idiotypes as predictive factors for the devolopment of lymphoma in primary Sjögren's syndrome. Arthritis & Rheumatism, 39, 767-772.
86. Valesini, G., Priori, R., Bavoillot, D., Osborn, J., Danieli, M.G., Del Papa, N., Gerli, R., Pietrogrande, M., Sabbadini, M.G., Silvestris, F. & Valsecchi, L. (1997) Differential risk of non-Hodgkin's lymphoma in Italian patients with primary Sjogren's syndrome. Journal of Rheumatology, 24, 2376-2380.
87. Voulgarelis, M., Dafni, U.G., Isenberg, D.A. & Moutsopoulos, H.M. (1999) Malignant lymphoma in primary Sjogren's syndrome: a multicenter, retrospective, clinical study by the European Concerted Action on Sjogren's Syndrome. Arthritis and Rheumatism, 42, 1765-1772.
88. Voulgarelis, M., Giannouli, S., Tzioufas, A.G. & Moutsopoulos, H.M. (2006) Long term remission of Sjogren's syndrome associated aggressive B cell non-Hodgkin's lymphomas following combined B cell depletion therapy and CHOP (cyclophosphamide, doxorubicin, vincristine, prednisone). Annals of the Rheumatic Diseases, 65, 1033-1037.
89. Voulgarelis, M., Ziakas, P.D., Papageorgiou, A., Baimpa, E., Tzioufas, A.G. & Moutsopoulos, H.M. (2012) Prognosis and outcome of non-Hodgkin lymphoma in primary Sjogren syndrome. Medicine, 91, 1-9.
90. Waterman, S.A., Gordon, T.P. & Rischmueller, M. (2000) Inhibitory effects of muscarinic receptor autoantibodies on parasympathetic neurotransmission in Sjogren's syndrome. Arthritis and Rheumatism, 43, 1647-1654.
91. Weng, M.Y., Huang, Y.T., Liu, M.F. & Lu, T.H. (2012) Incidence of cancer in a nationwide population cohort of 7852 patients with primary Sjogren's syndrome in Taiwan. Annals of the Rheumatic Diseases, 71, 524-527.
92. Zintzaras, E., Voulgarelis, M. & Moutsopoulos, H.M. (2005) The risk of lymphoma development in autoimmune diseases: a meta-analysis. Archives of Internal Medicine, 165, 2337-2344.
93. Zucca, E., Conconi, A., Laszlo, D., Lopez-Guillermo, A., Bouabdallah, R., Coiffier, B., Sebban, C., Jardin, F., Vitolo, U., Morschhauser, F., Pileri, S.A., Copie-Bergman, C., Campo, E., Jack, A., Floriani, I., Johnson, P., Martelli, M., Cavalli, F., Martinelli, G. & Thieblemont, C. (2013) Addition of rituximab to chlorambucil produces superior event-free survival in the treatment of patients with extranodal marginal-zone B-cell lymphoma: 5-year analysis of the IELSG-19 Randomized Study. Journal of Clinical Oncology, 31, 565-572.