Ocular adnexal marginal zone lymphoma of mucosa-associated lymphoid tissue

  • Dimitrios Kalogeropoulos
  • Alexandra Papoudou-Bai
  • Panagiotis Kanavaros
  • Chris Kalogeropoulos
Review Article
  • 132 Downloads

Abstract

Ocular adnexal lymphomas are a group of heterogeneous neoplasms representing approximately 1–2% of non-Hodgkin lymphomas and 8% of extranodal lymphomas. The incidence of primary ocular adnexal lymphoid tumors has raised over the last decades, and this could be probably attributed to the more sophisticated diagnostic techniques. Due to the wide spectrum of clinical manifestations, ocular tissue biopsy is important in order to set a precise diagnosis based on histological, immunophenotypical and, in some cases, molecular findings. The most common subtype, which may account for up to 80% of primary ocular adnexal lymphomas, is extranodal marginal zone lymphoma (EMZL) of mucosa-associated lymphoid tissue. This lymphoma is usually asymptomatic in the early phase of the disease causing a delay in the final diagnosis and prompt therapy. The pathogenesis of a proportion of these tumors has been linked to chronic inflammatory stimulation from specific infectious factors (e.g., Chlamydia psittaci) or to autoimmunity. The further improvement in diagnostic methods and the further understanding of the pathogenesis of ocular adnexal EMZL may contribute to the establishment of a more successful multidisciplinary therapeutic planning.

Keywords

Ocular adnexal lymphomas Immunohistochemistry Extranodal marginal zone lymphoma Mucosa-associated lymphoid tissue Chronic inflammatory stimulation 

Notes

Compliance with ethical standards

Conflicts of interest

All authors declare that there is no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. 1.
    Swerdlow SH, Campo E, Pileri SA, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood. 2016;127(20):2375–90. doi: 10.1182/blood-2016-01-643569.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Campo E, Swerdlow SH, Harris NL, Pileri S, Stein H, Jaffe ES. The 2008 WHO classification of lymphoid neoplasms and beyond: evolving concepts and practical applications. Blood. 2011;117(19):5019–32. doi: 10.1182/blood-2011-01-293050.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Chan CC. Primary intraocular lymphoma: clinical features, diagnosis, and treatment. Clin Lymphoma. 2003;4(1):30–1.PubMedCrossRefGoogle Scholar
  4. 4.
    Coupland SE, Damato B. Understanding intraocular lymphomas. Clin Exp Ophthalmol. 2008;36(6):564–78.PubMedCrossRefGoogle Scholar
  5. 5.
    Davis JL. Diagnosis of intraocular lymphoma. Ocul Immunol Inflamm. 2004;12(1):7–16.PubMedCrossRefGoogle Scholar
  6. 6.
    White WL, Ferry JA, Harris NL, Grove AS Jr. Ocular adnexal lymphoma. A clinicopathologic study with identification of lymphomas of mucosa-associated lymphoid tissue type. Ophthalmology. 1995;102(12):1994–2006.PubMedCrossRefGoogle Scholar
  7. 7.
    Coupland SE, Krause L, Delecluse HJ, et al. Lymphoproliferative lesions of the ocular adnexa. Analysis of 112 cases. Ophthalmology. 1998;105(8):1430–41.PubMedCrossRefGoogle Scholar
  8. 8.
    Cho EY, Han JJ, Ree HJ, et al. Clinicopathologic analysis of ocular adnexal lymphomas: extranodal marginal zone b-cell lymphoma constitutes the vast majority of ocular lymphomas among Koreans and affects younger patients. Am J Hematol. 2003;73(2):87–96.PubMedCrossRefGoogle Scholar
  9. 9.
    Ferry JA, Fung CY, Zukerberg L, et al. Lymphoma of the ocular adnexa: a study of 353 cases. Am J Surg Pathol. 2007;31(2):170–84.PubMedCrossRefGoogle Scholar
  10. 10.
    Stefanovic A, Lossos IS. Extranodal marginal zone lymphoma of the ocular adnexa. Blood. 2009;114(3):501–10.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Knowles DM, Jakobiec FA, McNally L, Burke JS. Lymphoid hyperplasia and malignant lymphoma occurring in the ocular adnexa (orbit, conjunctiva, and eyelids): a prospective multiparametric analysis of 108 cases during 1977–1987. Hum Pathol. 1990;21:959–73.PubMedCrossRefGoogle Scholar
  12. 12.
    Mannami T, Yoshino T, Oshima K, et al. Clinical, histopathological, and immunogenetic analysis of ocular adnexal lymphoproliferative disorders: characterization of malt lymphoma and reactive lymphoid hyperplasia. Mod Pathol. 2001;14:641–9.PubMedCrossRefGoogle Scholar
  13. 13.
    Auw-Haedrich C, Coupland SE, Kapp A, et al. Long term outcome of ocular adnexal lymphoma subtyped according to the REAL classification. Revised European and American Lymphoma. Br J Ophthalmol. 2001;85:63–9.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Ferreri AJ, Dolcetti R, Du M, et al. Ocular adnexal MALT lymphoma: an intriguing model for antigen-driven lymphoma-genesis and microbial-targeted therapy. Ann Oncol. 2008;19:835–46.PubMedCrossRefGoogle Scholar
  15. 15.
    Andrew NH, Coupland SE, Pirbhai A, Selva D. Lymphoid hyperplasia of the orbit and ocular adnexa: a clinical pathologic review. Surv Ophthalmol. 2016;61(6):778–90. doi: 10.1016/j.survophthal.2016.04.004.PubMedCrossRefGoogle Scholar
  16. 16.
    Woo JM, Tang CK, Rho MS, Lee JH, Kwon HC, Ahn HB. The clinical characteristics and treatment results of ocular adnexal lymphoma. Korean J Ophthalmol. 2006;20:7–12.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Nakata M, Matsuno Y, Katsumata N, et al. Histology according to the revised European-American lymphoma classification significantly predicts the prognosis of ocular adnexal lymphoma. Leuk Lymphoma. 1999;32:533–43.PubMedCrossRefGoogle Scholar
  18. 18.
    Tanimoto K, Kaneko A, Suzuki S, et al. Primary ocular adnexal MALT lymphoma: a long-term follow- up study of 114 patients. Jpn J Clin Oncol. 2007;37:337–44.PubMedCrossRefGoogle Scholar
  19. 19.
    Decaudin D, de Cremoux P, Vincent-Salomon A, et al. Ocular adnexal lymphoma: a review of clinicopathologic features and treatment options. Blood. 2006;108:1451–60.PubMedCrossRefGoogle Scholar
  20. 20.
    Shields CL, Shields JA, Carvalho C, et al. Conjunctival lymphoid tumors: clinical analysis of 117 cases and relationship to systemic lymphoma. Ophthalmology. 2001;108:979–84.PubMedCrossRefGoogle Scholar
  21. 21.
    Johnson TE, Tse DT, Byrne GE Jr, et al. Ocular-adnexal lymphoid tumors: a clinicopathologic and molecular genetic study of 77 patients. Ophthal Plast Reconstr Surg. 1999;15:171–9.PubMedCrossRefGoogle Scholar
  22. 22.
    Lagoo AS, Haggerty C, Kim Y, et al. Morphologic features of 115 lymphomas of the orbit and ocular adnexa categorized according to the World Health Organization classification. Are marginal zone lymphomas in the orbit mucosa-associated lymphoid tissue-type lymphomas? Arch Pathol Lab Med. 2008;132:1405–15.PubMedGoogle Scholar
  23. 23.
    Coupland SE, Damato B. Lymphomas involving the eye and the ocular adnexa. Curr Opin Ophthalmol. 2006;17:523–31.PubMedGoogle Scholar
  24. 24.
    Coupland SE, Hellmich M, Auw-Haedrich C, Lee WR, Stein H. Prognostic value of cell-cycle markers in ocular adnexal lymphoma: an assessment of 230 cases. Graefes Arch Clin Exp Ophthalmol. 2004;242:130–45.PubMedCrossRefGoogle Scholar
  25. 25.
    Annibali O, Sabatino F, Mantelli F, Olimpieri O, Bonini S, Avvisati G. Review article: mucosa-associated lymphoid tissue (MALT)-type lymphoma of ocular adnexa. Biology and treatment. Crit Rev Oncol Hematol. 2016;100:37–45.PubMedCrossRefGoogle Scholar
  26. 26.
    Middle Stephen, Coupland Sarah E, Taktak Azzam, et al. Immunohistochemical analysis indicates that the anatomical location of B-cell non-Hodgkin’s lymphoma is determined by differentially expressed chemokine receptors, sphingosine-1-phosphate receptors and integrins. Exp Hematol Oncol. 2015;4:10. doi: 10.1186/s40164-015-0004-3.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Bai M, Tsanou E, Agnantis NJ, Kamina S, et al. Proliferation profile of classical Hodgkin’s lymphomas. Increased expression of the protein cyclin D2 in Hodgkin’s and Reed-Sternberg cells. Mod Pathol. 2004;17(11):1338–45.PubMedCrossRefGoogle Scholar
  28. 28.
    Bai M, Skyrlas A, Agnantis NJ, et al. Diffuse large B-cell lymphomas with germinal center B-cell-like differentiation immunophenotypic profile are associated with high apoptotic index, high expression of the proapoptotic proteins bax, bak and bid and low expression of the antiapoptotic protein bcl-xl. Mod Pathol. 2004;17(7):847–56.PubMedCrossRefGoogle Scholar
  29. 29.
    Bai M, Agnantis NJ, Skyrlas A, et al. Increased expression of the bcl6 and CD10 proteins is associated with increased apoptosis and proliferation in diffuse large B-cell lymphomas. Mod Pathol. 2003;16(5):471–80.PubMedCrossRefGoogle Scholar
  30. 30.
    Bai M, Vlachonikolis J, Agnantis NJ, et al. Low expression of p27 protein combined with altered p53 and Rb/p16 expression status is associated with increased expression of cyclin A and cyclin B1 in diffuse large B-cell lymphomas. Mod Pathol. 2001;14(11):1105–13.PubMedCrossRefGoogle Scholar
  31. 31.
    Franco R, Camacho FI, Caleo A, et al. Nuclear bcl10 expression characterizes a group of ocular adnexa MALT lymphomas with shorter failure-free survival. Mod Pathol. 2006;19(8):1055–67.PubMedGoogle Scholar
  32. 32.
    Tanimoto K, Sekiguchi N, Yokota Y, et al. Fluorescence in situ hybridization (FISH) analysis of primary ocular adnexal MALT lymphoma. BMC Cancer. 2006;6:249.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Streubel B, Lamprecht A, Dierlamm J, et al. T(14;18) (q32;q21) involving IGH and MALT1 is a frequent chromosomal aberration in MALT lymphoma. Blood. 2003;101:2335–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Kim WS, Honma K, Karnan S, et al. Genome wide array-based comparative genomic hybridization of ocular marginal zone B cell lymphoma: comparison with pulmonary and nodal marginal zone B cell lymphoma. Genes Chromosomes Cancer. 2007;46:776–83.PubMedCrossRefGoogle Scholar
  35. 35.
    Schiby G, Polak-Charcon S, Mardoukh C, et al. Orbital marginal zone lymphomas: an immunohistochemical, polymerase chain reaction, and fluorescence in situ hybridization study. Hum Pathol. 2007;38:435–42.PubMedCrossRefGoogle Scholar
  36. 36.
    Matteucci C, Galieni P, Leoncini L, et al. Typical genomic imbalances in primary MALT lymphoma of the orbit. J Pathol. 2003;200:656–60.PubMedCrossRefGoogle Scholar
  37. 37.
    Wotherspoon AC, Pan LX, Diss TC, Isaacson PG. Cytogenetic study of B-cell lymphoma of mucosa-associated lymphoid tissue. Cancer Genet Cytogenet. 1992;58:35–8.PubMedCrossRefGoogle Scholar
  38. 38.
    Ye H, Liu H, Attygalle A, et al. Variable frequencies of t(11;18)(q21;q21) in MALT lymphomas of different sites: significant association with CagA strains of H pylori in gastric MALT lymphoma. Blood. 2003;102:1012–8.PubMedCrossRefGoogle Scholar
  39. 39.
    Streubel B, Simonitsch-Klupp I, Mullauer L, et al. Variable frequencies of MALT lymphoma-associated genetic aberrations in MALT lymphomas of different sites. Leukemia. 2004;18:1722–6.PubMedCrossRefGoogle Scholar
  40. 40.
    Akagi T, Motegi M, Tamura A, et al. A novel gene, MALT1 et 18q21, is involved in t(11;18)(q21;q21) found in low-grade B-cell lymphoma of mucosa-associated lymphoid tissue. Oncogene. 1999;18:5785–94.PubMedCrossRefGoogle Scholar
  41. 41.
    Streubel B, Vinatzer U, Lamprecht A, Raderer M, Chott A. T(3;14)(p14.1;q32) involving IGH and FOXP1 is a novel recurrent chromosomal aberration in MALT lymphoma. Leukemia. 2005;19:652–8.PubMedGoogle Scholar
  42. 42.
    Willis T, Jadayel DM, Du MQ, et al. Bcl10 is involved int (1; 14) (p22; q32) of MALT B cell lymphoma and mutated in multiple tumor types. Cell. 1999;96:35–45.PubMedCrossRefGoogle Scholar
  43. 43.
    Coupland SE. Molecular pathology of lymphoma. Eye (Lond). 2013;27(2):180–9. doi: 10.1038/eye.2012.247.CrossRefGoogle Scholar
  44. 44.
    Cani Andi K, Soliman Moaaz, Hovelson Daniel H, et al. Comprehensive genomic profiling of orbital and ocular adnexal lymphomas Identifies frequent alterations in MYD88 and chromatin modifiers: new routes to targeted therapies. Mod Pathol. 2016;29(7):685–97. doi: 10.1038/modpathol.2016.79.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Perrone S, D’Elia GM, Annechini G, Pulsoni A. Infectious aetiology of marginal zone lymphoma and role of anti-infective therapy. Mediterr J Hematol Infect Dis. 2016;8(1):e2016006. doi: 10.4084/MJHID.2016.006.eCollection2016.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Wohrer S, Troch M, Streubel B, et al. MALT lymphoma in patients with autoimmune diseases: a comparative analysis of characteristics and clinical course. Leukemia. 2007;21(8):1812–8. doi: 10.1038/sj.leu.2404782.PubMedCrossRefGoogle Scholar
  47. 47.
    Ponzoni M, Govi S, Licata G, et al. A reappraisal of the diagnostic and therapeutic management of uncommon histologies of primary ocular adnexal lymphoma. Oncologist. 2013;18(7):876–84. doi: 10.1634/theoncologist.2012-0425.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Du MQ. MALT lymphoma: recent advances in aetiology and molecular genetics. J Clin Exp Hematopathol. 2007;47:31–42.CrossRefGoogle Scholar
  49. 49.
    Marcucci F, Mele A. Hepatitis viruses and non-Hodgkin lymphoma: epidemiology, mechanisms of tumorigenesis, and therapeutic opportunities. Blood. 2011;117(6):1792–8. doi: 10.1182/blood-2010-06-275818.PubMedCrossRefGoogle Scholar
  50. 50.
    Landau DA, Saadoun D, Calabrese LH, Cacoub P. The pathophysiology of HCV induced B-cell clonal disorders. Autoimmun Rev. 2007;6(8):581–7. doi: 10.1016/j.autrev.2007.03.010.PubMedCrossRefGoogle Scholar
  51. 51.
    Inokuchi M, Ito T, Uchikoshi M, et al. Infection of B cells with hepatitis C virus for the development of lymphoproliferative disorders in patients with chronic hepatitis C. J Med Virol. 2009;81(4):619–27. doi: 10.1002/jmv.21388.PubMedCrossRefGoogle Scholar
  52. 52.
    Willemze R, Jaffe ES, Burg G, et al. WHO-EORTC classification for cutaneous lymphomas. Blood. 2005;105(10):3768–85. doi: 10.1182/blood-2004-09-3502.PubMedCrossRefGoogle Scholar
  53. 53.
    Takino H, Li C, Hu S, et al. Primary cutaneous marginal zone B-cell lymphoma: a molecular and clinicopathological study of cases from Asia, Germany, and the United States. Mod Pathol. 2008;21(12):1517–26. doi: 10.1038/modpathol.2008.159.PubMedCrossRefGoogle Scholar
  54. 54.
    Cerroni L, Zochling N, Putz B, Kerl H. Infection by Borrelia burgdorferi and cutaneous B-cell lymphoma. J Cutan Pathol. 1997;24(8):457–61. doi: 10.1111/j.1600-0560.1997.tb01318.x.PubMedCrossRefGoogle Scholar
  55. 55.
    Goodlad JR, Davidson MM, Hollowood K, et al. Primary cutaneous B-cell lymphoma and Borrelia burgdorferi infection in patients from the Highlands of Scotland. Am J Surg Pathol. 2000;24(9):1279–85. doi: 10.1097/00000478-200009000-00012.PubMedCrossRefGoogle Scholar
  56. 56.
    Goebel N, Serr A, Mittelviefhaus H, Reinhard T, Bogdan C, Auw-Haedrich C. Chlamydia psittaci, Helicobacter pylori and ocular adnexal lymphoma-is there an association? German experience. Leuk Res. 2007;31(10):1450–2. doi: 10.1016/j.leukres.2006.12.005.PubMedCrossRefGoogle Scholar
  57. 57.
    Ferreri AJ, Guidoboni M, Ponzoni M, et al. Evidence for an association between Chlamydia psittaci and ocular adnexal lymphomas. J Natl Cancer Inst. 2004;96(8):586–94. doi: 10.1093/jnci/djh102.PubMedCrossRefGoogle Scholar
  58. 58.
    Ponzoni M, Ferreri AJ, Guidoboni M, et al. Chlamydia infection and lymphomas: association beyond ocular adnexal lymphomas highlighted by multiple detection methods. Clin Cancer Res. 2008;14(18):5794–800. doi: 10.1158/1078-0432.CCR-08-0676.PubMedCrossRefGoogle Scholar
  59. 59.
    Chanudet E, Zhou Y, Bacon CM, et al. Chlamydia psittaci is variably associated with ocular adnexal MALT lymphoma in different geographical regions. J Pathol. 2006;209(3):344–51. doi: 10.1002/path.1984.PubMedCrossRefGoogle Scholar
  60. 60.
    Rosado MF, Byrne GE, Ding F, et al. Ocular adnexal lymphoma: a clinicopathologic study of a large cohort of patients with no evidence for an association with Chlamydia psittaci. Blood. 2006;107(2):467–72. doi: 10.1182/blood-2005-06-2332.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Daibata M, Nemoto Y, Togitani K, et al. Absence of Chlamydia psittaci in ocular adnexal lymphoma from Japanese patients. Br J Haematol. 2006;132(5):651–2. doi: 10.1111/j.1365-2141.2005.05943.x.PubMedCrossRefGoogle Scholar
  62. 62.
    Decaudin D, Dolcetti R, de Cremoux P, et al. Variable association between Chlamydophila psittaci infection and ocular adnexal lymphomas: methodological biases or true geographical variations? Anticancer Drugs. 2008;19(8):761–5. doi: 10.1097/CAD.0b013e32830b58c4.PubMedCrossRefGoogle Scholar
  63. 63.
    Usui Y, Rao NA, Takase H, et al. Comprehensive polymerase chain reaction assay for detection of pathogenic DNA in lymphoproliferative disorders of the ocular adnexa. Nat Sci Rep. 2016;. doi: 10.1038/srep36621.Google Scholar
  64. 64.
    Flanders AE, Espinosa GA, Markiewicz DA, Howell DD. Orbital lymphoma. Role of CT and MRI. Radiol Clin North Am. 1987;25:601–13.PubMedGoogle Scholar
  65. 65.
    Polito E, Leccisotti A, Galieni P. Clinical and radiological presentation of 95 orbital lymphoid tumors. Graefe Arch Clin Exp Ophthalmol. 1996;234:504–9.CrossRefGoogle Scholar
  66. 66.
    Valenzuela AA, Allen C, Grimes D, Wong D, Sullivan TJ. Positron emission tomography in the detection and staging of ocular adnexal lymphoproliferative disease. Ophthalmology. 2006;113:2331–7.PubMedCrossRefGoogle Scholar
  67. 67.
    Sullivan TJ, Valenzuela AA. Imaging features of ocular adnexal lymphoproliferative disease. Eye. 2006;20:1189–95.PubMedCrossRefGoogle Scholar
  68. 68.
    Gayed I, Eskandari MF, McLaughlin P, Pro B, Diba R, Esmaeli B. Value of positron emission tomography in staging ocular adnexal lymphomas and evaluating their response to therapy. Ophthalmic Surg Lasers Imaging. 2007;38:319–25.PubMedGoogle Scholar
  69. 69.
    Kennerdell JS, Flores NE, Hartsock RJ. Low-dose radiotherapy for lymphoid lesions of the orbit and ocular adnexa. Ophthal Plast Reconstr Surg. 1999;15:129–33.PubMedCrossRefGoogle Scholar
  70. 70.
    Coupland SE, Hummel M, Stein H. Ocular adnexal lymphomas: five case presentations and a review of the literature. Surv Ophthalmol. 2002;47(5):470–90.PubMedCrossRefGoogle Scholar
  71. 71.
    Graue GF, Finger PT, Maher E, et al. Ocular adnexal lymphoma staging and treatment: American Joint Committee on Cancer versus Ann Arbor. Eur J Ophthalmol. 2013;23(3):344–55. doi: 10.5301/ejo.5000224.PubMedCrossRefGoogle Scholar
  72. 72.
    Jenkins C, Rose GE, Bunce C, et al. Histological features of ocular adnexal lymphoma (REAL classification) and their association with patient morbidity and survival. Br J Ophthalmol. 2000;84:907–13.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Tanimoto K, Kaneko A, Suzuki S, et al. Long-term follow-up results of no initial therapy for ocular adnexal MALT lymphoma. Ann Oncol. 2006;17:135–40.PubMedCrossRefGoogle Scholar
  74. 74.
    Lee JL, Kim MK, Lee KH, et al. Extranodal marginal zone B-cell lymphomas of mucosa associated lymphoid tissue-type of the orbit and ocular adnexa. Ann Hematol. 2005;84:13–8.PubMedCrossRefGoogle Scholar
  75. 75.
    Restrepo A, Raez LE, Byrne GE Jr, et al. Is central nervous system prophylaxis necessary in ocular adnexal lymphoma? Crit Rev Oncog. 1998;9:269–73.PubMedGoogle Scholar
  76. 76.
    Sasai K, Yamabe H, Dodo Y, Kashii S, Nagata Y, Hiraoka M. Non-Hodgkin’s lymphoma of the ocular adnexa. Acta Oncol. 2001;40:485–90.PubMedCrossRefGoogle Scholar
  77. 77.
    Bolek TW, Moyses HM, Marcus RB Jr, et al. Radiotherapy in the management of orbital lymphoma. Int J Radiat Oncol Biol Phys. 1999;44:31–6.PubMedCrossRefGoogle Scholar
  78. 78.
    Le QT, Eulau SM, George TI, et al. Primary radiotherapy for localized orbital MALT lymphoma. Int J Radiat Oncol Biol Phys. 2002;52:657–63.PubMedCrossRefGoogle Scholar
  79. 79.
    Liao SL, Kao SC, Hou PK, Chen MS. Results of radiotherapy for orbital and adnexal lymphoma. Orbit. 2002;21:117–23.PubMedCrossRefGoogle Scholar
  80. 80.
    Hasegawa M, Kojima M, Shioya M, et al. Treatment results of radiotherapy for malignant lymphoma of the orbit and histopathologic review according to the WHO classification. Int J Radiat Oncol Biol Phys. 2003;57:172–6.PubMedCrossRefGoogle Scholar
  81. 81.
    Stafford SL, Kozelsky TF, Garrity JA, et al. Orbital lymphoma: radiotherapy outcome and complications. Radiother Oncol. 2001;59:139–44.PubMedCrossRefGoogle Scholar
  82. 82.
    Uno T, Isobe K, Shikama N, et al. Radiotherapy for extranodal, marginal zone, B-cell lymphoma of mucosa-associated lymphoid tissue originating in the ocular adnexa: a multiinstitutional, retrospective review of 50 patients. Cancer. 2003;98:865–71.PubMedCrossRefGoogle Scholar
  83. 83.
    Ejima Y, Sasaki R, Okamoto Y, et al. Ocular adnexal mucosa-associated lymphoid tissue lymphoma treated with radiotherapy. Radiother Oncol. 2006;78:6–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Tsang RW, Gospodarowicz MK, Pintilie M, et al. Localized mucosa-associated lymphoid tissue lymphoma treated with radiation therapy has excellent clinical outcome. J Clin Oncol. 2003;21:4157–64.PubMedCrossRefGoogle Scholar
  85. 85.
    McKelvie PA, McNab A, Francis IC, Fox R, O’Day J. Ocular adnexal lymphoproliferative disease: a series of 73 cases. Clin Exp Ophthalmol. 2001;29:387–93.PubMedCrossRefGoogle Scholar
  86. 86.
    Galieni P, Polito E, Leccisotti A, et al. Localized orbital lymphoma. Haematologica. 1997;82:436–9.PubMedGoogle Scholar
  87. 87.
    Ben Simon GJ, Cheung N, McKelvie P, Fox R, McNab AA. Oral chlorambucil for extranodal, marginal zone, B-cell lymphoma of mucosa-associated lymphoid tissue of the orbit. Ophthalmology. 2006;113:1209–13.PubMedCrossRefGoogle Scholar
  88. 88.
    Charlotte F, Doghmi K, Cassoux N, et al. Ocular adnexal marginal zone B cell lymphoma: a clinical and pathologic study of 23 cases. Virchows Arch. 2006;448:506–16.PubMedCrossRefGoogle Scholar
  89. 89.
    Song EK, Kim SY, Kim TM, et al. Efficacy of chemotherapy as a first-line treatment in ocular adnexal extranodal marginal zone B-cell lymphoma. Ann Oncol. 2008;19:242–6.PubMedCrossRefGoogle Scholar
  90. 90.
    Rigacci L, Nassi L, Puccioni M, et al. Rituximab and chlorambucil as first-line treatment for low grade ocular adnexal lymphomas. Ann Hematol. 2007;86:565–8.PubMedCrossRefGoogle Scholar
  91. 91.
    Avilés A, Neri N, Calva A, Huerta-Guzmán J, Cleto S, Nambo MJ. Addition of a short course of chemotherapy did not improve outcome in patients with localized marginal B-cell lymphoma of the orbit. Oncology. 2006;70:173–6.PubMedCrossRefGoogle Scholar
  92. 92.
    Blasi MA, Gherlinzoni F, Calvisi G, et al. Local chemotherapy with interferon-alpha for conjunctival mucosa-associated lymphoid tissue lymphoma: a preliminary report. Ophthalmology. 2001;108:559–62.PubMedCrossRefGoogle Scholar
  93. 93.
    Di Gaetano N, Xiao Y, Erba E, et al. Synergism between fludarabine and rituximab revealed in a follicular lymphoma cell line resistant to the cytotoxic activity either drug alone. Br J Haematol. 2001;114:800–9.PubMedCrossRefGoogle Scholar
  94. 94.
    Reff ME, Carner K, Chambers KS, et al. Depletion of B-cells in vivo by a chimeric mouse human monoclonal antibody to CD20. Blood. 1994;83:435–45.PubMedGoogle Scholar
  95. 95.
    Sacchi S, Federico M, Vitolo U, et al. Clinical activity and safety of combination immunotherapy with IFN-2a and rituximab in patients with re-lapsed low grade non-Hodgkin’s lymphoma. Haematologica. 2001;86:951–8.PubMedGoogle Scholar
  96. 96.
    Czuczman MS, Weaver R, Alkuzweny B, Berlfein J, Grillo-Lopez AJ. Prolonged clinical and molecular remission in patients with low-grade or follicular non-Hodgkin’s lymphoma treated with rituximab plus CHOP chemotherapy: 9-year follow-up. J Clin Oncol. 2004;22:4711–6.PubMedCrossRefGoogle Scholar
  97. 97.
    Demidem A, Lam T, Alas S, Hariharan K, Hanna N, Bonavida B. Chimericanti-CD20 (IDEC-c2b8) monoclonal antibody sensitizes a B cell lymphoma cell line to cell killing by cytotoxic drugs. Cancer Biother Radiopharm. 1997;12:177–86.PubMedCrossRefGoogle Scholar
  98. 98.
    Mathas S, Rickers A, Bommert K, Dorken B, Mapara MY. Anti-CD20-and B-cell receptor mediated apoptosis: evidence for shared intracellular signaling pathways. Cancer Res. 2000;60:7170–6.PubMedGoogle Scholar
  99. 99.
    Shan D, Ledbetter JA, Press O. Apoptosis of malignant human B cells by ligation of CD20 with monoclonal antibodies. Blood. 1998;91:1644–52.PubMedGoogle Scholar
  100. 100.
    Conconi A, Martinelli G, Thieblemont C, et al. Clinical activity of rituximab in extranodal marginal zone B-cell lymphoma of MALT type. Blood. 2003;102:2741–5.PubMedCrossRefGoogle Scholar
  101. 101.
    Raderer M, Jager G, Brugger S, et al. Rituximab for treatment of advanced extranodal marginal zone B cell lymphoma of the mucosa-associated lymphoid tissue lymphoma. Oncology. 2003;65:306–10.PubMedCrossRefGoogle Scholar
  102. 102.
    Lossos IS, Morgensztern D, Blaya M, Alencar A, Pereira D, Rosenblatt J. Rituximab for treatment of chemoimmunotherapy naive marginal zone lymphoma. Leuk Lymphoma. 2007;48:1630–2.PubMedCrossRefGoogle Scholar
  103. 103.
    Morgensztern D, Rosado MF, Serafini AN, Lossos IS. Somatostatin receptor scintigraphy in MALT lymphoma of the lacrimal gland treated with rituximab. Leuk Lymphoma. 2004;45:1275–8.PubMedCrossRefGoogle Scholar
  104. 104.
    Nuckel H, Meller D, Steuhl KP, Duhrsen U. Anti-CD20 monoclonal antibody therapy in relapsed MALT lymphoma of the conjunctiva. Eur J Haematol. 2004;73:258–62.PubMedCrossRefGoogle Scholar
  105. 105.
    Ferreri AJ, Ponzoni M, Martinelli G, et al. Rituximab in patients with mucosal-associated lymphoid tissue-type lymphoma of the ocular adnexa. Haematologica. 2005;90:1578–9.PubMedGoogle Scholar
  106. 106.
    Benetatos L, Alymara V, Asproudis I, Bourantas KL. Rituximab as first line treatment for MALT lymphoma of extraocular muscles. Ann Hematol. 2006;85:625–6.PubMedCrossRefGoogle Scholar
  107. 107.
    Heinz C, Merz H, Nieschalk M, Mueller-Miny H, Koch P, Heiligenhaus A. Rituximab for the treatment of extranodal marginal zone B-cell lymphoma of the lacrimal gland. Br J Ophthalmol. 2007;91:1563–4.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Tedder TF, Engel P. CD20: a regulator of cell-type progression of B-lymphocytes. Immunol Today. 1994;15:450–4.PubMedCrossRefGoogle Scholar
  109. 109.
    Lossos IS, Fabregas JC, Koru-Sengul T, et al. Phase II study of (90) Y Ibritumomab tiuxetan (Zevalin) in patients with previously untreated marginal zone lymphoma. Leuk Lymphoma. 2015;56(6):1750–5. doi: 10.3109/10428194.2014.975801.PubMedCrossRefGoogle Scholar
  110. 110.
    Ferreri AJ, Ponzoni M, Guidoboni M, et al. Regression of ocular adnexal lymphoma after Chlamydia psittaci-eradicating antibiotic therapy. J Clin Oncol. 2005;23:5067–73.PubMedCrossRefGoogle Scholar
  111. 111.
    Abramson DH, Rollins I, Coleman M. Periocular mucosa-associated lymphoid/low grade lymphomas: treatment with antibiotics. Am J Ophthalmol. 2005;140:729–30.PubMedCrossRefGoogle Scholar
  112. 112.
    Grünberger B, Hauff W, Lukas J, et al. ‘Blind’ antibiotic treatment targeting Chlamydia is not effective in patients with MALT lymphoma of the ocular adnexa. Ann Oncol. 2006;17:484–7.PubMedCrossRefGoogle Scholar
  113. 113.
    Kiesewetter B, Raderer Markus. Antibiotic therapy in non-gastrointestinal MALT lymphoma: a review of the literature. Blood. 2013;122:1350–7.PubMedCrossRefGoogle Scholar
  114. 114.
    Yoon JS, Ma KT, Kim SJ, Kook K, Lee SY. Prognosis for patients in a Korean population with ocular adnexal lymphoproliferative lesions. Ophthal Plast Reconstr Surg. 2007;23:94–9.PubMedCrossRefGoogle Scholar
  115. 115.
    Husain A, Roberts D, Pro B, McLaughlin P, Esmaeli B. Meta-analyses of the association between Chlamydia psittaci and ocular adnexal lymphoma and the response of ocular adnexal lymphoma to antibiotics. Cancer. 2007;110:809–15.PubMedCrossRefGoogle Scholar
  116. 116.
    Wenzel C, Fiebiger W, Dieckmann K, Formanek M, Chott A, Raderer M. Extranodal marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue of the head and neck area: high rate of disease recurrence following local therapy. Cancer. 2003;97:2236–41.PubMedCrossRefGoogle Scholar
  117. 117.
    Zucca E, Conconi A, Pedrinis E, et al. Non gastric marginal zone B-cell lymphoma of mucosa-associated lymphoid tissue. Blood. 2003;101:2489–95.PubMedCrossRefGoogle Scholar
  118. 118.
    Kirkegaard Marina M, Rasmussen Peter K, Coupland Sarah E, et al. Conjunctival Lymphoma—an International multicenter retrospective study. JAMA Ophthalmol. 2016;. doi: 10.1001/jamaophthalmol.2015.6122.PubMedGoogle Scholar
  119. 119.
    Meunier J, Lumbroso-Le Rouic L, Vincent-Salomon A, et al. Ophthalmologic and intraocular non-Hodgkin’s lymphoma: a large single centre study of initial characteristics, natural history, and prognostic factors. Hematol Oncol. 2004;22:143–58.PubMedCrossRefGoogle Scholar
  120. 120.
    Martinet S, Ozsahin M, Belkacemi Y, et al. Outcome and prognostic factors in orbital lymphoma: a Rare Cancer Network study on 90 consecutive patients treated with radiotherapy. Int J Radiat Oncol Biol Phys. 2003;55:892–8.PubMedCrossRefGoogle Scholar
  121. 121.
    Chaidos AI, Bai MC, Kamina SA, Kanavaros PE, Agnantis NJ, Bourantas KL. Incidence of apoptosis and cell proliferation in multiple myeloma: correlation with bcl-2 protein expression and serum levels of interleukin-6 (IL-6) and soluble IL-6 receptor. Eur J Haematol. 2002;69(2):90–4.PubMedCrossRefGoogle Scholar
  122. 122.
    Bai M, Tsanou E, Agnantis NJ, et al. Expression of cyclin D3 and cyclin E and identification of distinct clusters of proliferation and apoptosis in diffuse large B-cell lymphomas. Histol Histopathol. 2003;18(2):449–57.PubMedGoogle Scholar
  123. 123.
    Korkolopoulou PA, Angelopoulou MK, Kontopidou FN, et al. Retinoblastoma gene product and P21 (WAF1, CIP1) protein expression in non-Hodgkin’s lymphomas: a multivariate survival analysis. Leuk Lymphoma. 2001;40:647–58.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Ophthalmology, Faculty of Medicine, School of Health SciencesUniversity of IoanninaIoanninaGreece
  2. 2.Department of Pathology, Faculty of Medicine, School of Health SciencesUniversity of IoanninaIoanninaGreece
  3. 3.Department of Anatomy-Histology-Embryology, Faculty of Medicine, School of Health SciencesUniversity of IoanninaIoanninaGreece

Personalised recommendations