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Annals of Hematology

, Volume 97, Issue 10, pp 1851–1857 | Cite as

Treating synchronous bilateral ocular adnexal marginal zone lymphoma: the consortium for improving survival of lymphoma study

  • Sung Yong Oh
  • Won Seog Kim
  • Hye-Jin Kang
  • Ji Hyun Lee
  • Seok Jae Huh
  • Seok Jin Kim
  • Dok Hyun Yoon
  • Jung Yong Hong
  • Won Sik Lee
  • Hyo Jung Kim
  • Jong Ho Won
  • Byeong-Bae Park
  • Soon II Lee
  • Cheolwon Suh
Original Article

Abstract

Both-side synchronous involvement has been reported to account for 7–24% of ocular adnexal marginal zone lymphoma (OAML). We conducted a retrospective analysis to identify the clinical features and treatment outcomes of synchronous bilateral OAML (SB-OAML) by treatment modality. We analyzed patients with a histologic diagnosis of SB-OAML, excluding metachronous bilateral involved OAML. We enrolled a total of 95 patients for this analysis, 36 males and 59 females; the median patient age was 42 years (range 16–77 years). Eleven (11.6%) patients had been treated with chemotherapy or chemo-immunotherapy (eight R-CVP, two CVP, and one R-CHOP). The median number of treatments was 6 (range 6–8); there were 9 complete responses (CRs; 81.8%) and 2 partial responses (PRs; 18.2%). Nearly all patients (88.4%) received radiotherapy in both eyes, and the median radiation dose was 27 Gy (range 20–40 Gy) to each eye; 68 CRs (80.9%) and 14 PRs (16.7%) were achieved. Ten-year progression-free survival (PFS) and overall survival (OS) rates were 79.8 and 91.1%, respectively. Radiotherapy continued to be an independent prognostic marker, with the hazard of progression (P = 0.036). Eleven patients (13.1%) had surgery for cataract treatment during follow-up, and patients who received low-dose radiation (< 30.3 Gy) experienced fewer cataract operations. SB-OAML was predominantly observed in young females, and they had good response and prognosis regardless of treatment modalities. Low-dose radiotherapy to both eyes showed a tendency of longer PFS than did chemotherapy and could decrease cataract operations.

Keywords

Ocular adnexal marginal zone lymphoma Synchronous Bilateral 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Margo CE, Mulla ZD (1998) Malignant tumors of the orbit. Analysis of the Florida Cancer registry. Ophthalmology 105:185–190CrossRefGoogle Scholar
  2. 2.
    Fung CY, Tarbell NJ, Lucarelli MJ, Goldberg SI, Linggood RM, Harris NL, Ferry JA (2003) Ocular adnexal lymphoma: clinical behavior of distinct World Health Organization classification subtypes. Int J Radiat Oncol Biol Phys 57:1382–1391CrossRefGoogle Scholar
  3. 3.
    Moslehi R, Coles FB, Schymura MJ (2011) Descriptive epidemiology of ophthalmic and ocular adnexal non-Hodgkin’s lymphoma. Expert Rev Ophthalmol 6:175–180CrossRefGoogle Scholar
  4. 4.
    Oh DE, Kim YD (2007) Lymphoproliferative diseases of the ocular adnexa in Korea. Arch Ophthalmol 125:1668–1673CrossRefGoogle Scholar
  5. 5.
    Cho EY, Han JJ, Ree HJ, Ko YH, Kang YK, Ahn HS, Ahn SD, Park CJ, Huh J (2003) 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 73:87–96CrossRefGoogle Scholar
  6. 6.
    Yoon JS, Ma KT, Kim SJ, Kook K, Lee SY (2007) Prognosis for patients in a Korean population with ocular adnexal lymphoproliferative lesions. Ophthal Plast Reconstr Surg 23:94–99CrossRefGoogle Scholar
  7. 7.
    Oh SY, Ryoo BY, Kim WS, Park YH, Kim K, Kim HJ, Kwon JM, Lee J, Ko YH, Ahn YC, Oh SJ, Lee SI, Kim HJ, Kwon HC, Bang SM, Kim JH, Park J, Lee SS, Kim HY, Park K (2007) Nongastric marginal zone B-cell lymphoma: analysis of 247 cases. Am J Hematol 82:446–452CrossRefGoogle Scholar
  8. 8.
    Desai A, Joag MG, Lekakis L, Chapman JR, Vega F, Tibshirani R, Tse D, Markoe A, Lossos IS (2017) Long-term course of patients with primary ocular adnexal MALT lymphoma: a large single-institution cohort study. Blood 129:324–332CrossRefGoogle Scholar
  9. 9.
    Guffey Johnson J, Terpak LA, Margo CE, Setoodeh R (2016) Extranodal marginal zone B-cell lymphoma of the ocular adnexa. Cancer Control 23:140–149CrossRefGoogle Scholar
  10. 10.
    Nam H, Ahn YC, Kim YD, Ko Y, Kim WS (2009) Prognostic significance of anatomic subsites: results of radiation therapy for 66 patients with localized orbital marginal zone B cell lymphoma. Radiother Oncol 90:236–241CrossRefGoogle Scholar
  11. 11.
    Lee SE, Paik JS, Cho WK, Choi BO, Lee SN, Jung SE, Park KS, Kang CS, Kim SH, Yang SW, Cho SG (2011) Feasibility of the TNM-based staging system of ocular adnexal extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma). Am J Hematol 86:262–266CrossRefGoogle Scholar
  12. 12.
    Uno T, Isobe K, Shikama N, Nishikawa A, Oguchi M, Ueno N, Itami J, Ohnishi H, Mikata A, Ito H (2003) 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 98:865–871CrossRefGoogle Scholar
  13. 13.
    Stefanovic A, Lossos IS (2009) Extranodal marginal zone lymphoma of the ocular adnexa. Blood 114:501–510CrossRefGoogle Scholar
  14. 14.
    Martinet S, Ozsahin M, Belkacemi Y et al (2003) 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 55:892–898CrossRefGoogle Scholar
  15. 15.
    Raderer M, Streubel B, Woehrer S, Puespoek A, Jaeger U, Formanek M, Chott A (2005) High relapse rate in patients with MALT lymphoma warrants lifelong follow-up. Clin Cancer Res 11:3349–3352CrossRefGoogle Scholar
  16. 16.
    Lee SW, Suh CO, Kim GE, Yang WI, Lee SY, Hahn JS, Park JO (2002) Role of radiotherapy for primary orbital lymphoma. Am J Clin Oncol 25:261–265CrossRefGoogle Scholar
  17. 17.
    Woolf DK, Kuhan H, Shoffren O, Akinnawo EM, Sivagurunathan B, Boyce H, Plowman PN (2015) Outcomes of primary lymphoma of the ocular adnexa (orbital lymphoma) treated with radiotherapy. Clin Oncol 27:153–159CrossRefGoogle Scholar
  18. 18.
    Harada K, Murakami N, Kitaguchi M, Sekii S, Takahashi K, Yoshio K, Inaba K, Morota M, Ito Y, Sumi M, Suzuki S, Tobinai K, Uno T, Itami J (2014) Localized ocular adnexal mucosa-associated lymphoid tissue lymphoma treated with radiation therapy: a long-term outcome in 86 patients with 104 treated eyes. Int J Radiat Oncol Biol Phys 88:650–654CrossRefGoogle Scholar
  19. 19.
    Song EK, Kim SY, Kim TM et al (2008) Efficacy of chemotherapy as a first-line treatment in ocular adnexal extranodal marginal zone B-cell lymphoma. Annals of oncology : official journal of the European society for. Med Oncol 19:242–246Google Scholar
  20. 20.
    Ferreri AJ, Ponzoni M, Martinelli G, Muti G, Guidoboni M, Dolcetti R, Doglioni C (2005) Rituximab in patients with mucosal-associated lymphoid tissue-type lymphoma of the ocular adnexa. Haematologica 90:1578–1579PubMedGoogle Scholar
  21. 21.
    Salar A, Domingo-Domenech E, Panizo C, Nicolás C, Bargay J, Muntañola A, Canales M, Bello JL, Sancho JM, Tomás JF, Rodríguez MJ, Peñalver FJ, Grande C, Sánchez-Blanco JJ, Palomera L, Arranz R, Conde E, García M, García JF, Caballero D, Montalbán C, Grupo Español de Linfomas/Trasplante de Médula Ósea (GELTAMO) (2014) First-line response-adapted treatment with the combination of bendamustine and rituximab in patients with mucosa-associated lymphoid tissue lymphoma (MALT2008-01): a multicentre, single-arm, phase 2 trial. Lancet Haematol 1:e104–e111CrossRefGoogle Scholar
  22. 22.
    Zucca E, Conconi A, Martinelli G, Bouabdallah R, Tucci A, Vitolo U, Martelli M, Pettengell R, Salles G, Sebban C, Guillermo AL, Pinotti G, Devizzi L, Morschhauser F, Tilly H, Torri V, Hohaus S, Ferreri AJM, Zachée P, Bosly A, Haioun C, Stelitano C, Bellei M, Ponzoni M, Moreau A, Jack A, Campo E, Mazzucchelli L, Cavalli F, Johnson P, Thieblemont C (2017) Final results of the IELSG-19 randomized trial of mucosa-associated lymphoid tissue lymphoma: improved event-free and progression-free survival with rituximab plus chlorambucil versus either chlorambucil or rituximab monotherapy. J Clin Oncol Off J Am Soc Clin Oncol 35:1905–1912CrossRefGoogle Scholar
  23. 23.
    Kang HJ, Kim WS, Kim SJ, Lee JJ, Yang DH, Kim JS, Lee SR, Lee GW, Kim HJ, Kim HY, Oh SY, Kim HC, Eom HS, Chung J, Park J, Suh C, Ryoo BY (2012) Phase II trial of rituximab plus CVP combination chemotherapy for advanced stage marginal zone lymphoma as a first-line therapy: consortium for improving survival of lymphoma (CISL) study. Ann Hematol 91:543–551CrossRefGoogle Scholar
  24. 24.
    Nam SW, Woo KI, Kim YD (2018) Characteristics of primary extranodal marginal zone B-cell lymphoma in Korea: conjunctiva versus other ocular adnexa. Br J Ophthalmol 102:502–508PubMedGoogle Scholar
  25. 25.
    Kiesewetter B, Lukas J, Kuchar A, Mayerhoefer ME, Streubel B, Lagler H, Müllauer L, Wöhrer S, Fischbach J, Raderer M (2014) Clinical features, treatment and outcome of mucosa-associated lymphoid tissue (MALT) lymphoma of the ocular adnexa: single center experience of 60 patients. PLoS One 9:e104004CrossRefGoogle Scholar
  26. 26.
    Ferreri AJ, Dolcetti R, Du MQ et al (2008) Ocular adnexal MALT lymphoma: an intriguing model for antigen-driven lymphomagenesis and microbial-targeted therapy. Ann Oncol 19:835–846CrossRefGoogle Scholar
  27. 27.
    Matsuo T, Ichimura K, Okada H, Shinagawa K, Fukushima K, Okano M, Otsuka M, Yoshino T (2010) Clonal analysis of bilateral, recurrent, or systemically multifocal ocular adnexal lymphoma. J Clin Exp Hematop 50:27–38CrossRefGoogle Scholar
  28. 28.
    Thieblemont C, Cascione L, Conconi A, Kiesewetter B, Raderer M, Gaidano G, Martelli M, Laszlo D, Coiffier B, Lopez Guillermo A, Torri V, Cavalli F, Johnson PW, Zucca E (2017) A MALT lymphoma prognostic index. Blood 130:1409–1417CrossRefGoogle Scholar
  29. 29.
    Sassone M, Ponzoni M, Ferreri AJ (2017) Ocular adnexal marginal zone lymphoma: clinical presentation, pathogenesis, diagnosis, prognosis, and treatment. Best Pract Res Clin Haematol 30:118–130CrossRefGoogle Scholar
  30. 30.
    Yahalom J, Illidge T, Specht L, Hoppe RT, Li YX, Tsang R, Wirth A (2015) Modern radiation therapy for extranodal lymphomas: field and dose guidelines from the international lymphoma radiation oncology group. Int J Radiat Oncol Biol Phys 92:11–31CrossRefGoogle Scholar
  31. 31.
    Kaushik M, Pulido JS, Schild SE, Stafford S (2012) Risk of radiation retinopathy in patients with orbital and ocular lymphoma. Int J Radiat Oncol Biol Phys 84:1145–1150CrossRefGoogle Scholar
  32. 32.
    Tsang RW, Gospodarowicz MK, Pintilie M, Wells W, Hodgson DC, Sun A, Crump M, Patterson BJ (2003) Localized mucosa-associated lymphoid tissue lymphoma treated with radiation therapy has excellent clinical outcome. J Clin Oncol Off J Am Soc Clin Oncol 21:4157–4164CrossRefGoogle Scholar
  33. 33.
    Stafford SL, Kozelsky TF, Garrity JA, Kurtin PJ, Leavitt JA, Martenson JA, Habermann TM (2001) Orbital lymphoma: radiotherapy outcome and complications. Radiother Oncol 59:139–144CrossRefGoogle Scholar
  34. 34.
    Pinnix CC, Dabaja BS, Milgrom SA, Smith GL, Abou Z, Nastoupil L, Romaguera J, Turturro F, Fowler N, Fayad L, Westin J, Neelapu S, Fanale MA, Rodriguez MA, Hagemeister F, Lee HJ, Oki Y, Wang M, Samaniego F, Chi L, Esmaeli B (2017) Ultra-low-dose radiotherapy for definitive management of ocular adnexal B-cell lymphoma. Head Neck 39:1095–1100CrossRefGoogle Scholar
  35. 35.
    Fasola CE, Jones JC, Huang DD, le QT, Hoppe RT, Donaldson SS (2013) Low-dose radiation therapy (2 Gy x 2) in the treatment of orbital lymphoma. Int J Radiat Oncol Biol Phys 86:930–935CrossRefGoogle Scholar
  36. 36.
    Kim SY, Yang SW, Lee WS, Yang JW, Oh SY, Ahn HB, Yang DH, Park SK, Chang JH, Kim HJ, Lee MJ, Cho SG (2017) Frontline treatment with chemoimmunotherapy for limited-stage ocular adnexal MALT lymphoma with adverse factors: a phase II study. Oncotarget 8:68583–68590PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Sung Yong Oh
    • 1
  • Won Seog Kim
    • 2
  • Hye-Jin Kang
    • 3
  • Ji Hyun Lee
    • 1
  • Seok Jae Huh
    • 1
  • Seok Jin Kim
    • 2
  • Dok Hyun Yoon
    • 4
  • Jung Yong Hong
    • 4
  • Won Sik Lee
    • 5
  • Hyo Jung Kim
    • 6
  • Jong Ho Won
    • 7
  • Byeong-Bae Park
    • 8
  • Soon II Lee
    • 9
  • Cheolwon Suh
    • 4
    • 10
  1. 1.Department of Internal MedicineDong-A University HospitalBusanSouth Korea
  2. 2.Department of Medicine, Samsung Medical CenterSunkyunkwan University School of MedicineSeoulSouth Korea
  3. 3.Division of Hematology/Oncology, Department of Internal Medicine, Korea Cancer Center HospitalKorea Institute of Radiological and Medical SciencesSeoulSouth Korea
  4. 4.Department of Oncology, Asan Medical CenterUniversity of Ulsan College of MedicineSeoulSouth Korea
  5. 5.Department of Hematology, Busan Paik HospitalInje University College of MedicineBusanSouth Korea
  6. 6.Department of Internal Medicine, Hallym University Sacred Heart HospitalHallym University College of MedicineSeoulSouth Korea
  7. 7.Department of Internal Medicine, Soonchunhyang University Seoul HospitalSoonchunhyang University College of MedicineSeoulSouth Korea
  8. 8.Division of Hematology/Oncology, Department of Internal MedicineHanyang University College of MedicineSeoulSouth Korea
  9. 9.Department of Internal MedicineDankook University College of MedicineCheonanSouth Korea
  10. 10.Department of Hematology–OncologyAsan Medical Center University of Ulsan College of MedicineSongpa-guSouth Korea

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