Malignant lymphoma in primary Sjögren's syndrome: An update on the pathogenesis and treatment

Seminars in Arthritis and Rheumatism

Volumn 43, Issue 2, 2013, Pages 178-186

  Routsias, John G ^a   Goules, John D ^a   Charalampakis, Georgios ^b   Tzima, Sotiria ^a   Papageorgiou, Aristea ^a   Voulgarelis, Michael ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Autoimmunity; Lymphoproliferation; Non Hodgkin lymphoma; Salivary glands; Sj gren's syndrome

Indexed keywords

B CELL ACTIVATING FACTOR; CYCLOPHOSPHAMIDE; DOXORUBICIN; PREDNISONE; RITUXIMAB; VINCRISTINE;

ARTICLE; B LYMPHOCYTE DIFFERENTIATION; CANCER COMBINATION CHEMOTHERAPY; CANCER GRADING; CANCER PROGNOSIS; CANCER RISK; DISEASE ASSOCIATION; DISEASE FREE SURVIVAL; EVENT FREE SURVIVAL; HISTOPATHOLOGY; HUMAN; IMMUNE DYSREGULATION; IMMUNOPATHOGENESIS; INTERNATIONAL PROGNOSTIC INDEX; LARGE CELL LYMPHOMA; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; LYMPHOMA; MARGINAL ZONE LYMPHOMA; MOLECULAR PATHOLOGY; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; SJOEGREN SYNDROME; TUMOR LOCALIZATION;

AUTOIMMUNITY; LYMPHOPROLIFERATION; NON-HODGKIN LYMPHOMA; SALIVARY GLANDS; SJÖGREN'S SYNDROME;

B-LYMPHOCYTES; HUMANS; LYMPHOMA; RISK FACTORS; SJOGREN'S SYNDROME;

EID: 84886088134     PISSN: 00490172     EISSN: 1532866X     Source Type: Journal    
DOI: 10.1016/j.semarthrit.2013.04.004     Document Type: Article

References (82)

1. Soliotis F.C., Moutsopoulos H.M. Sjogren's syndrome. Autoimmunity 2004, 37(4):305-307.
2. Smedby K.E., Hjalgrim H., Askling J., Chang E.T., Gregersen H., Porwit-MacDonald A., et al. Autoimmune and chronic inflammatory disorders and risk of non-Hodgkin lymphoma by subtype. J Nat Cancer Inst 2006, 98(1):51-60.
3. Zintzaras E., Voulgarelis M., Moutsopoulos H.M. The risk of lymphoma development in autoimmune diseases: a meta-analysis. Arch Intern Med 2005, 165(20):2337-2344.
4. Voulgarelis M., Moutsopoulos H.M. Lymphoproliferation in autoimmunity and Sjogren's syndrome. Curr Rheumatol Rep 2003, 5(4):317-323.
5. Ioannidis J.P.A., Vassiliou V.A., Moutsopoulos H.M. Long-term risk of mortality and lymphoproliferative disease and predictive classification of primary Sjogren's syndrome. Arthritis Rheum 2002, 46(3):741-747.
6. Skopouli F.N., Dafni U., Ioannidis J.P.A., Moutsopoulos H.M. Clinical evolution, and morbidity and mortality of primary Sjogren's syndrome. Semin Arthritis Rheum 2000, 29(5):296-304.
7. Bende R.J., van Maldegem F., van Noesel C.J. Chronic inflammatory disease, lymphoid tissue neogenesis and extranodal marginal zone B-cell lymphomas. Haematologica 2009, 94(8):1109-1123.
8. Lesley R., Xu Y., Kalled S.L., Hess D.M., Schwab S.R., Shu H.B., et al. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 2004, 20(4):441-453.
9. Martin F., Kearney J.F. Marginal-zone B cells. Nat Rev Immunol 2002, 2(5):323-335.
10. Saito T., Chiba S., Ichikawa M., Kunisato A., Asai T., Shimizu K., et al. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 2003, 18(5):675-685.
11. Dunn-Walters D.K., Isaacson P.G., Spencer J. Analysis of mutations in immunoglobulin heavy chain variable region genes of microdissected marginal zone (MGZ) B cells suggests that the MGZ of human spleen is a reservoir of memory B cells. J Exp Med 1995, 182(2):559-566.
12. Tsuiji M., Yurasov S., Velinzon K., Thomas S., Nussenzweig M.C., Wardemann H. A checkpoint for autoreactivity in human IgM+ memory B cell development. J Exp Med 2006, 203(2):393-400.
13. Routsias J.G., Tzioufas A.G. Autoimmune response and target autoantigens in Sjogren's syndrome. Eur J Clin Invest 2010, 40(11):1026-1036.
14. Tzioufas A.G., Voulgarelis M. Update on Sjögren's syndrome autoimmune epithelitis: from classification to increased neoplasias. Best Pract Res Clin Rheumatol 2007, 21(6):989-1010.
15. Mitsias D.I., Kapsogeorgou E.K., Moutsopoulos H.M. The role of epithelial cells in the initiation and perpetuation of autoimmune lesions: lessons from Sjogren's syndrome (autoimmune epithelitis). Lupus 2006, 15(5):255-261.
16. Dimitriou I.D., Kapsogeorgou E.K., Moutsopoulos H.M., Manoussakis M.N. CD40 on salivary gland epithelial cells: high constitutive expression by cultured cells from Sjogren's syndrome patients indicating their intrinsic activation. Clin Exp Immunol 2002, 127(2):386-392.
17. Daridon C., Pers J.O., Devauchelle V., Martins-Carvalho C., Hutin P., Pennec Y.L., et al. Identification of transitional type II B cells in the salivary glands of patients with Sjogren's syndrome. Arthritis Rheum 2006, 54(7):2280-2288.
18. Theander E., Vasaitis L., Baecklund E., Nordmark G., Warfvinge G., Liedholm R., et al. Lymphoid organisation in labial salivary gland biopsies is a possible predictor for the development of malignant lymphoma in primary Sjogren's syndrome. Ann Rheum Dis 2011, 70(8):1363-1368.
19. Bombardieri M., Barone F., Humby F., Kelly S., McGurk M., Morgan P., et al. 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. J Immunol 2007, 179(7):4929-4938.
20. Mackay F., Groom J.R., Tangye S.G. An important role for B-cell activation factor and B cells in the pathogenesis of Sjogren's syndrome. Curr Opin Rheumatol 2007, 19(5):406-413.
21. Le Pottier L., Devauchelle V., Fautrel A., Daridon C., Saraux A., Youinou P., et al. Ectopic germinal centers are rare in Sjogren's syndrome salivary glands and do not exclude autoreactive B cells. J Immunol 2009, 182(6):3540-3547.
22. Aloisi F., Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 2006, 6(3):205-217.
23. Fauchais A.L., Martel C., Gondran G., Lambert M., Launay D., Jauberteau M.O., et al. Immunological profile in primary Sjogren syndrome: clinical significance, prognosis and long-term evolution to other auto-immune disease. Autoimmun Rev 2010, 9(9):595-599.
24. Barcellos K.S., Nonogaki S., Enokihara M.M., Teixeira M.S., Andrade L.E. Differential expression of Ro/SSA 60kDa and La/SSB, but not Ro/SSA 52kDa, mRNA and protein in minor salivary glands from patients with primary Sjogren's syndrome. J Rheumatol 2007, 34(6):1283-1292.
25. de Wilde P.C., Kater L., Bodeutsch C., van den Hoogen F.H., van de Putte L.B., van Venrooij W.J. Aberrant expression pattern of the SS-B/La antigen in the labial salivary glands of patients with Sjogren's syndrome. Arthritis Rheum 1996, 39(5):783-791.
26. Niewold T.B., Clark D.N., Salloum R., Poole B.D. Interferon alpha in systemic lupus erythematosus. J Biomed Biotechnol 2010, 2010:948364.
27. Farkas A., Tonel G., Nestle F.O. Interferon-alpha and viral triggers promote functional maturation of human monocyte-derived dendritic cells. Br J Dermatol 2008, 158(5):921-929.
28. Lavie F., Miceli-Richard C., Ittah M., Sellam J., Gottenberg J.E., Mariette X. B-cell activating factor of the tumour necrosis factor family expression in blood monocytes and T cells from patients with primary Sjogren's syndrome. Scand J Immunol 2008, 67(2):185-192.
29. Daridon C., Devauchelle V., Hutin P., Le Berre R., Martins-Carvalho C., Bendaoud B., et al. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjogren's syndrome. Arthritis Rheum 2007, 56(4):1134-1144.
30. Moisini I., Davidson A. BAFF: a local and systemic target in autoimmune diseases. Clin Exp Immunol 2009, 158(2):155-163.
31. Varin M.M., Le Pottier L., Youinou P., Saulep D., Mackay F., Pers J.O. B-cell tolerance breakdown in Sjogren's syndrome: focus on BAFF. Autoimmun Rev 2010, 9(9):604-608.
32. Batten M., Groom J., Cachero T.G., Qian F., Schneider P., Tschopp J., et al. BAFF mediates survival of peripheral immature B lymphocytes. J Exp Med 2000, 192(10):1453-1466.
33. Batten M., Fletcher C., Ng L.G., Groom J., Wheway J., Laabi Y., et al. TNF deficiency fails to protect BAFF transgenic mice against autoimmunity and reveals a predisposition to B cell lymphoma. J Immunol 2004, 172(2):812-822.
34. Wotherspoon A.C. Gastric MALT lymphoma and Helicobacter pylori. Yale J Biol Med 1996, 69(1):61-68.
35. Schollkopf C., Melbye M., Munksgaard L., Smedby K.E., Rostgaard K., Glimelius B., et al. Borrelia infection and risk of non-Hodgkin lymphoma. Blood 2008, 111(12):5524-5529.
36. Ponzoni M., Ferreri A.J., Guidoboni M., Lettini A.A., Cangi M.G., Pasini E., et al. Chlamydia infection and lymphomas: association beyond ocular adnexal lymphomas highlighted by multiple detection methods. Clin Cancer Res 2008, 14(18):5794-5800.
37. Lecuit M., Abachin E., Martin A., Poyart C., Pochart P., Suarez F., et al. Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med 2004, 350(3):239-248.
38. Luppi M., Longo G., Ferrari M.G., Ferrara L., Marasca R., Barozzi P., et al. Prevalence of HCV infection and second neoplasms in marginal zone lymphomas. Br J Haematol 1997, 96(4):873-874.
39. Ramos-Casals M., la Civita L., de Vita S., Solans R., Luppi M., Medina F., et al. Characterization of B cell lymphoma in patients with Sjogren's syndrome and hepatitis C virus infection. Arthritis and rheumatism 2007, 57(1):161-170.
40. Zucca E., Bertoni F., Roggero E., Cavalli F. The gastric marginal zone B-cell lymphoma of MALT type. Blood 2000, 96(2):410-419.
41. Manthorpe R., Bredberg A., Henriksson G., Larsson A. Progress and regression within primary Sjogren's syndrome. Scand J Rheumatol 2006, 35(1):1-6.
42. Guzman L.M., Castillo D., Aguilera S.O. Polymerase chain reaction (PCR) detection of B cell clonality in Sjogren's syndrome patients: a diagnostic tool of clonal expansion. Clin Exp Immunol 2011, 161(1):57-64.
43. Tokuno T., Takahashi H., Suzuki C., Yamamoto M., Naishiro Y., Sugaya A., et al. Analysis of B-cell clonality in the hepatic tissue of patients with Sjogren's syndrome. Scand J Rheumatol 2003, 32(5):268-272.
44. Bahler D.W., Miklos J.A., Swerdlow S.H. Ongoing Ig gene hypermutation in salivary gland mucosa-associated lymphoid tissue-type lymphomas. Blood 1997, 89(9):3335-3344.
45. Bahler D.W., Swerdlow S.H. Clonal salivary gland infiltrates associated with myoepithelial sialadenitis (Sjogren's syndrome) begin as nonmalignant antigen-selected expansions. Blood 1998, 91(6):1864-1872.
46. Martin T., Weber J.C., Levallois H., Labouret N., Soley A., Koenig S., et al. Salivary gland lymphomas in patients with Sjogren's syndrome may frequently develop from rheumatoid factor B cells. Arthritis Rheum 2000, 43(4):908-916.
47. Roosnek E., Lanzavecchia A. Efficient and selective presentation of antigen-antibody complexes by rheumatoid factor B cells. J Exp Med 1991, 173(2):487-489.
48. Joao C., Farinha P., da Silva M.G., Martins C., Crespo M., Cabecadas J. Cytogenetic abnormalities in MALT lymphomas and their precursor lesions from different organs. A fluorescence in situ hybridization (FISH) study. Histopathology 2007, 50(2):217-224.
49. Chanudet E., Ye H., Ferry J., Bacon C.M., Adam P., Muller-Hermelink H.K., et al. 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. J Pathol 2009, 217(3):420-430.
50. Ivanovski M., Silvestri F., Pozzato G., Anand S., Mazzaro C., Burrone O.R., et al. Somatic hypermutation, clonal diversity, and preferential expression of the VH 51p1/VL kv325 immunoglobulin gene combination in hepatitis C virus-associated immunocytomas. Blood 1998, 91(7):2433-2442.
51. Dammacco F., Sansonno D., Piccoli C., Racanelli V., D'Amore F.P., Lauletta G. The lymphoid system in hepatitis C virus infection: autoimmunity, mixed cryoglobulinemia, and Overt B-cell malignancy. Semin Liver Dis 2000, 20(2):143-157.
52. De R.e.V., De Vita S., Marzotto A., Rupolo M., Gloghini A., Pivetta B., et al. Sequence analysis of the immunoglobulin antigen receptor of hepatitis C virus-associated non-Hodgkin lymphomas suggests that the malignant cells are derived from the rheumatoid factor-producing cells that occur mainly in type II cryoglobulinemia. Blood 2000, 96(10):3578-3584.
53. Miklos J.A., Swerdlow S.H., Bahler D.W. Salivary gland mucosa-associated lymphoid tissue lymphoma immunoglobulin V(H) genes show frequent use of V1-69 with distinctive CDR3 features. Blood 2000, 95(12):3878-3884.
54. Kuppers R., Klein U., Hansmann M.L., Rajewsky K. Cellular origin of human B-cell lymphomas. N Engl J Med 1999, 341(20):1520-1529.
55. Tapinos N.I., Polihronis M., Moutsopoulos H.M. Lymphoma development in Sjogren's syndrome: novel p53 mutations. Arthritis Rheum 1999, 42(7):1466-1472.
56. Rossi D., Gaidano G. Molecular heterogeneity of diffuse large B-cell lymphoma: implications for disease management and prognosis. Hematology 2002, 7(4):239-252.
57. Neumeister P., Hoefler G., Beham-Schmid C., Schmidt H., Apfelbeck U., Schaider H., et al. Deletion analysis of the p16 tumor suppressor gene in gastrointestinal mucosa-associated lymphoid tissue lymphomas. Gastroenterology 1997, 112(6):1871-1875.
58. Tzioufas A.G., Boumba D.S., Skopouli F.N., Moutsopoulos H.M. Mixed monoclonal cryoglobulinemia and monoclonal rheumatoid factor cross-reactive idiotypes as predictive factors for the development of lymphoma in primary Sjogren's syndrome. Arthritis Rheum 1996, 39(5):767-772.
59. Voulgarelis M., Tzioufas A.G. Pathogenetic mechanisms in the initiation and perpetuation of Sjogren's syndrome. Nat Rev Rheumatol 2010, 6(9):529-537.
60. Anderson L.G., Talal N. The spectrum of benign to malignant lymphoproliferation in Sjogren's syndrome. Clin Exp Immunol 1972, 10(2):199-221.
61. Kassan S.S., Thomas T.L., Moutsopoulos H.M., Hoover R., Kimberly R.P., Budman D.R., et al. Increased risk of lymphoma in sicca syndrome. Ann Intern Med 1978, 89(6):888-892.
62. Ramos-Casals M., Brito-Zeron P., Yague J., Akasbi M., Bautista R., Ruano M., et al. Hypocomplementaemia as an immunological marker of morbidity and mortality in patients with primary Sjogren's syndrome. Rheumatology 2005, 44(1):89-94.
63. Theander E., Henriksson G., Ljungberg O., Mandl T., Manthorpe R., Jacobsson L.T.H. Lymphoma and other malignancies in primary Sjogren's syndrome: a cohort study on cancer incidence and lymphoma predictors. Ann Rheum Dis 2006, 65(6):796-803.
64. Anaya J.M., McGuff H.S., Banks P.M., Talal N. Clinicopathological factors relating malignant lymphoma with Sjogren's syndrome. Semin Arthritis Rheum 1996, 25(5):337-346.
65. Sutcliffe N., Inanc M., Speight P., Isenberg D. Predictors of lymphoma development in primary Sjogren's syndrome. Semin Arthritis Rheum 1998, 28(2):80-87.
66. Leandro M.J., Isenberg D.A. Rheumatic diseases and malignancy-is there an association?. Scand J Rheumatol 2001, 30(4):185-188.
67. Voulgarelis M., Moutsopoulos H.M. Malignant lymphoma in primary Sjogren's syndrome. Israel Med Assoc J 2001, 3(10):761-766.
68. Voulgarelis M., Dafni U.G., Isenberg D.A., Moutsopoulos H.M. Malignant lymphoma in primary Sjogren's syndrome: a multicenter, retrospective, clinical study by the European concerted action on Sjogren's syndrome. Arthritis Rheum 1999, 42(8):1765-1772.
69. Voulgarelis M., Ziakas P.D., Papageorgiou A., Baimpa E., Tzioufas A.G., Moutsopoulos H.M. Prognosis and outcome of non-Hodgkin lymphoma in primary Sjogren syndrome. Medicine 2012, 91(1):1-9.
70. Inamdar K.V., Medeiros L.J., Jorgensen J.L., Amin H.M., Schlette E.J. Bone marrow involvement by marginal zone B-cell lymphomas of different types. Am J Clin Pathol 2008, 129(5):714-722.
71. Voulgarelis M., Moutsopoulos H.M. Mucosa-associated lymphoid tissue lymphoma in Sjogren's syndrome: risks, management, and prognosis. Rheum Dis Clin North Am 2008, 34(4):921-933. [viii].
72. Castrillo J.M., Montalban C., Abraira V., Carrion R., Cruz M.A., Larana J.G., et al. Evaluation of the international index in the prognosis of high grade gastric malt lymphoma. Leuk Lymphoma 1996, 24(1-2):159-163.
73. Gill H., Chim C.S., Au W.Y., Loong F., Tse E., Leung A.Y., et al. Non-gastric marginal zone B cell lymphoma: clinicopathologic features and treatment results. Ann Hematol 2011.
74. Pollard R.P., Pijpe J., Bootsma H., Spijkervet F.K., Kluin P.M., Roodenburg J.L., et al. Treatment of mucosa-associated lymphoid tissue lymphoma in Sjogren's syndrome: a retrospective clinical study. J Rheumatol 2011, 38(10):2198-2208.
75. Saraux A. The point on the ongoing B-cell depleting trials currently in progress over the world in primary Sjogren's syndrome. Autoimmun Rev 2010, 9(9):609-614.
76. Christodoulou M.I., Kapsogeorgou E.K., Moutsopoulos H.M. Characteristics of the minor salivary gland infiltrates in Sjogren's syndrome. J Autoimmun 2010, 34(4):400-407.
77. Conconi A., Martinelli G., Thiéblemont C., Ferreri A.J.M., Devizzi L., Peccatori F., et al. Clinical activity of rituximab in extranodal marginal zone B-cell lymphoma of MALT type. Blood 2003, 102(8):2741-2745.
78. Hammel P., Haioun C., Chaumette M.T., Gaulard P., Divine M., Reyes F., et al. Efficacy of single-agent chemotherapy in low-grade B-cell mucosa-associated lymphoid tissue lymphoma with prominent gastric expression. J Clin Oncol 1995, 13(10):2524-2529.
79. Jager G., Neumeister P., Brezinschek R., Hinterleitner T., Fiebiger W., Penz M., et al. Treatment of extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue type with cladribine: a phase II study. J Clin Oncol 2002, 20(18):3872-3877.
80. Voulgarelis M., Giannouli S., Anagnostou D., Tzioufas A.G. Combined therapy with rituximab plus cyclophosphamide/doxorubicin/vincristine/prednisone (CHOP) for Sjogren's syndrome-associated B-cell aggressive non-Hodgkin's lymphomas. Rheumatology 2004, 43(8):1050-1053.
81. Voulgarelis M., Giannouli S., Tzioufas A.G., Moutsopoulos H.M. 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). Ann Rheum Dis 2006, 65(8):1033-1037.
82. Voulgarelis M., Petroutsos G., Moutsopoulos H.M., Skopouli F.N. 2-Chloro-2'-deoxyadenosine in the treatment of Sjogren's syndrome-associated B cell lymphoproliferation. Arthritis Rheum 2002, 46(8):2248-2249.