Abstract
Incidence of various Hodgkin (HL) and non-Hodgkin lymphoma (NHL) subtypes and association with viruses in Lebanon are not known. We undertook a nationwide study of 272 patients diagnosed with lymphoma in 2007. HL comprised 32.7 % (n = 89) of cases while NHL represented 67.3 % (n = 183). Consistent with the literature, nodular sclerosis was the most predominant HL subtype (n = 57/89). Among NHL, B-cell NHL represented 88 % (n = 161/183), T-cell NHL 9 % (n = 17/183), whereas in 2.7 % it was not classifiable. The B-cell NHL comprised predominantly diffuse large B-cell lymphoma (46 %) and follicular lymphoma (23 %). 81 cases were reviewed by a panel of pathologists with 87.6 % concordance rate. Serology was negative for hepatitis C in 122 tested cases. HIV was positive in 2 cases. Two adult T-cell leukemia/lymphoma were HTLV-I positive. EBV IgG were positive in 88.5 % of cases. 38 EBV seropositive cases [27 NHL (24 B-cell, 3 T-cell) and 11 HL] were studied for EBV genome expression using EBV-encoded RNA (EBER)-in situ hybridization. EBER expression was positive in 8 (21 %) cases (6 HL, 2 T-cell NHL). The distribution of lymphoma subtypes in Lebanon appears similar to that of Western countries. The high rate of EBV positivity in HL and T-cell lymphoma by EBER deserves further investigation.
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References
Morton LM, Wang SS, Devesa SS, Hartge P, Weisenburger DD, Linet MS (2006) Lymphoma incidence patterns by WHO subtype in the United States, 1992–2001. Blood 107(1):265–276. doi:10.1182/blood-2005-06-2508
Roman E, Smith AG (2011) Epidemiology of lymphomas. Histopathology 58(1):4–14. doi:10.1111/j.1365-2559.2010.03696.x
Smith A, Roman E, Howell D, Jones R, Patmore R, Jack A (2010) The Haematological Malignancy Research Network (HMRN): a new information strategy for population based epidemiology and health service research. Br J Haematol 148(5):739–753. doi:10.1111/j.1365-2141.2009.08010.x
Cancer Facts and Figures 2010 (Accessed February 16, 2011)
Ekstrom-Smedby K (2006) Epidemiology and etiology of non-Hodgkin lymphoma—a review. Acta Oncol 45(3):258–271. doi:10.1080/02841860500531682
Zuckerman E, Zuckerman T, Levine AM, Douer D, Gutekunst K, Mizokami M, Qian DG, Velankar M, Nathwani BN, Fong TL (1997) Hepatitis C virus infection in patients with B-cell non-Hodgkin lymphoma. Ann Intern Med 127(6):423–428
Muller AM, Ihorst G, Mertelsmann R, Engelhardt M (2005) Epidemiology of non-Hodgkin’s lymphoma (NHL): trends, geographic distribution, and etiology. Ann Hematol 84(1):1–12. doi:10.1007/s00277-004-0939-7
Suarez F, Lortholary O, Hermine O, Lecuit M (2006) Infection-associated lymphomas derived from marginal zone B cells: a model of antigen-driven lymphoproliferation. Blood 107(8):3034–3044. doi:10.1182/blood-2005-09-3679
Yamaguchi K, Takatsuki K (1993) Adult T cell leukaemia–lymphoma. Baillieres Clin Haematol 6(4):899–915
Baris D, Zahm SH (2000) Epidemiology of lymphomas. Curr Opin Oncol 12(5):383–394
Cartwright R, Brincker H, Carli PM, Clayden D, Coebergh JW, Jack A, McNally R, Morgan G, de Sanjose S, Tumino R, Vornanen M (1999) The rise in incidence of lymphomas in Europe 1985–1992. Eur J Cancer 35(4):627–633
Bosetti C, Levi F, Ferlay J, Lucchini F, Negri E, La Vecchia C (2008) Incidence and mortality from non-Hodgkin lymphoma in Europe: the end of an epidemic? Int J Cancer 123(8):1917–1923. doi:10.1002/ijc.23722
Greiner TC, Medeiros LJ, Jaffe ES (1995) Non-Hodgkin’s lymphoma. Cancer 75(1 Suppl):370–380
Eltom MA, Jemal A, Mbulaiteye SM, Devesa SS, Biggar RJ (2002) Trends in Kaposi’s sarcoma and non-Hodgkin’s lymphoma incidence in the United States from 1973 through 1998. J Natl Cancer Inst 94(16):1204–1210
Clarke CA, Glaser SL (2002) Changing incidence of non-Hodgkin lymphomas in the United States. Cancer 94(7):2015–2023. doi:10.1002/cncr.10403
Carreon JD, Morton LM, Devesa SS, Clarke CA, Gomez SL, Glaser SL, Sakoda LC, Linet MS, Wang SS (2008) Incidence of lymphoid neoplasms by subtype among six Asian ethnic groups in the United States, 1996–2004. Cancer Causes Control 19(10):1171–1181. doi:10.1007/s10552-008-9184-z
Nakatsuka S, Aozasa K (2006) Epidemiology and pathologic features of Hodgkin lymphoma. Int J Hematol 83(5):391–397. doi:10.1532/IJH97.05184
Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55(2):74–108
Mueller N (1994) Another view of the epidemiology of non-Hodgkin’s lymphoma. Oncology (Williston Park) 8(9):83
Glaser SL, Swartz WG (1990) Time trends in Hodgkin’s disease incidence. The role of diagnostic accuracy. Cancer 66(10):2196–2204
Jaffe ES, Harris N, Stein H, Vardiman JW (2001) Pathology and genetics of tumours of haematopoietic and lymphoid tissues. IARC Press, Lyon
Shamseddine A, Sibai AM, Gehchan N, Rahal B, El-Saghir N, Ghosn M, Aftimos G, Chamsuddine N, Seoud M (2004) Cancer incidence in postwar Lebanon: findings from the first national population-based registry, 1998. Ann Epidemiol 14(9):663–668. doi:10.1016/j.annepidem.2003.12.002
Castella A, Joshi S, Raaschou T, Mason N (2001) Pattern of malignant lymphoma in the United Arab Emirates—a histopathologic and immunologic study in 208 native patients. Acta Oncol 40(5):660–664
Bamanikar S, Thunold S, Devi KR, Bamanikar A (1995) The pattern of malignant lymphoma in Oman. J Trop Med Hyg 98(5):351–354
Akhtar SS, Haque IU, Wafa SM, El-Saka H, Saroor AM, Nadrah HM (2009) Malignant lymphoma in Al-Qassim, Saudi Arabia, reclassified according to the WHO classification. Saudi Med J 30(5):677–681
Haddadin WJ (2005) Malignant lymphoma in Jordan: a retrospective analysis of 347 cases according to the World Health Organization classification. Ann Saudi Med 25(5):398–403
Shome DK, George SM, Al-Hilli F, Satir AA (2004) Spectrum of malignant lymphomas in Bahrain. Leitmotif of a regional pattern. Saudi Med J 25(2):164–167
Temmim L, Baker H, Al-Jarallah M, Manguno H, Madda JP, Sinowatz F (2004) Clinical characteristics and pathological classification of non-Hodgkin’s lymphoma in Kuwait. Results of a collaborative study with the International Lymphoma Study Group (ILSG). Leuk Lymphoma 45(9):1865–1871. doi:10.1080/10428190410001697386
Kadin ME, Berard CW, Nanba K, Wakasa H (1983) Lymphoproliferative diseases in Japan and Western countries: proceedings of the United States–Japan Seminar, September 6 and 7, 1982, in Seattle, Washington. Hum Pathol 14(9):745–772
Ho FC, Todd D, Loke SL, Ng RP, Khoo RK (1984) Clinico-pathological features of malignant lymphomas in 294 Hong Kong Chinese patients, retrospective study covering an eight-year period. Int J Cancer 34(2):143–148
Ko YH, Kim CW, Park CS, Jang HK, Lee SS, Kim SH, Ree HJ, Lee JD, Kim SW, Huh JR (1998) REAL classification of malignant lymphomas in the Republic of Korea: incidence of recently recognized entities and changes in clinicopathologic features. Hematolymphoreticular Study Group of the Korean Society of Pathologists. Revised European–American lymphoma. Cancer 83(4):806–812. doi:10.1002/(SICI)1097-0142(19980815)83:4<806::AID-CNCR26>3.0.CO;2-V
Shih LY, Liang DC (1991) Non-Hodgkin’s lymphomas in Asia. Hematol Oncol Clin N Am 5(5):983–1001
Ameen R, Sajnani KP, Albassami A, Refaat S (2010) Frequencies of non-Hodgkin’s lymphoma subtypes in Kuwait: comparisons between different ethnic groups. Ann Hematol 89(2):179–184. doi:10.1007/s00277-009-0801-z
Al-Kuraya K, Narayanappa R, Al-Dayel F, El-Solh H, Ezzat A, Ismail H, Belgaumi A, Bavi P, Atizado V, Sauter G, Simon R (2006) Epstein-Barr virus infection is not the sole cause of high prevalence for Hodgkin’s lymphoma in Saudi Arabia. Leuk Lymphoma 47(4):707–713. doi:10.1080/10428190500286879
Allemani C, Sant M, De Angelis R, Marcos-Gragera R, Coebergh JW (2006) Hodgkin disease survival in Europe and the U.S.: prognostic significance of morphologic groups. Cancer 107(2):352–360. doi:10.1002/cncr.21995
Makar RR, Saji T, Junaid TA (2003) Epstein–Barr virus expression in Hodgkin’s lymphoma in Kuwait. Pathol Oncol Res 9(3):159–165
Al-Shemmari SH, Al-Humood S, Ameen R, Kamlesh S, Nemec J, Varghese A (2004) Hodgkin’s disease: Kuwait experience. Med Princ Pract 13(4):201–205. doi:10.1159/000078316
Proctor IE, McNamara C, Rodriguez-Justo M, Isaacson PG, Ramsay A (2011) Importance of expert central review in the diagnosis of lymphoid malignancies in a regional cancer network. J Clin Oncol 29(11):1431–1435. doi:10.1200/JCO.2010.31.2223
Lester JF, Dojcinov SD, Attanoos RL, O’Brien CJ, Maughan TS, Toy ET, Poynton CH (2003) The clinical impact of expert pathological review on lymphoma management: a regional experience. Br J Haematol 123(3):463–468
Ferri C, Caracciolo F, Zignego AL, La Civita L, Monti M, Longombardo G, Lombardini F, Greco F, Capochiani E, Mazzoni A et al (1994) Hepatitis C virus infection in patients with non-Hodgkin’s lymphoma. Br J Haematol 88(2):392–394
Pozzato G, Mazzaro C, Crovatto M, Modolo ML, Ceselli S, Mazzi G, Sulfaro S, Franzin F, Tulissi P, Moretti M et al (1994) Low-grade malignant lymphoma, hepatitis C virus infection, and mixed cryoglobulinemia. Blood 84(9):3047–3053
Dal Maso L, Franceschi S (2006) Hepatitis C virus and risk of lymphoma and other lymphoid neoplasms: a meta-analysis of epidemiologic studies. Cancer Epidemiol Biomarkers Prev 15(11):2078–2085. doi:10.1158/1055-9965.EPI-06-0308
Hausfater P, Cacoub P, Sterkers Y, Thibault V, Amoura Z, Nguyen L, Ghillani P, Leblond V, Piette JC (2001) Hepatitis C virus infection and lymphoproliferative diseases: prospective study on 1,576 patients in France. Am J Hematol 67(3):168–171. doi:10.1002/ajh.1101
Udomsakdi-Auewarakul C, Auewarakul P, Sukpanichnant S, Muangsup W (2000) Hepatitis C virus infection in patients with non-Hodgkin lymphoma in Thailand. Blood 95(11):3640–3641
Salem Z, Nuwaiyri-Salti N, Ramlawi F, Ramia S (2003) Hepatitis C virus infection in Lebanese patients with B-cell non-Hodgkin’s lymphoma. Eur J Epidemiol 18(3):251–253
Irani-Hakime N, Musharrafieh U, Samaha H, Almawi WY (2006) Prevalence of antibodies against hepatitis B virus and hepatitis C virus among blood donors in Lebanon, 1997–2003. Am J Infect Control 34(4):241–243. doi:10.1016/j.ajic.2005.06.009
Uchiyama T, Yodoi J, Sagawa K, Takatsuki K, Uchino H (1977) Adult T-cell leukemia: clinical and hematologic features of 16 cases. Blood 50(3):481–492
Bazarbachi A, Ghez D, Lepelletier Y, Nasr R, de The H, El-Sabban ME, Hermine O (2004) New therapeutic approaches for adult T-cell leukaemia. Lancet Oncol 5(11):664–672. doi:10.1016/S1470-2045(04)01608-0
Bitar N, Hajj HE, Houmani Z, Sabbah A, Otrock ZK, Mahfouz R, Zaatari G, Bazarbachi A (2009) Adult T-cell leukemia/lymphoma in the Middle East: first report of two cases from Lebanon. Transfusion 49(9):1859–1864. doi:10.1111/j.1537-2995.2009.02223.x
Spano JP, Atlan D, Breau JL, Farge D (2002) AIDS and non-AIDS-related malignancies: a new vexing challenge in HIV-positive patients. Part I: Kaposi’s sarcoma, non-Hodgkin’s lymphoma, and Hodgkin’s lymphoma. Eur J Intern Med 13(3):170–179
Dal Maso L, Serraino D, Franceschi S (2001) Epidemiology of AIDS-related tumours in developed and developing countries. Eur J Cancer 37(10):1188–1201
Rabkin CS (1994) Epidemiology of AIDS-related malignancies. Curr Opin Oncol 6(5):492–496
Carbone A, Gloghini A, Dotti G (2008) EBV-associated lymphoproliferative disorders: classification and treatment. Oncologist 13(5):577–585. doi:10.1634/theoncologist.2008-0036
Jones JF, Shurin S, Abramowsky C, Tubbs RR, Sciotto CG, Wahl R, Sands J, Gottman D, Katz BZ, Sklar J (1988) T-cell lymphomas containing Epstein–Barr viral DNA in patients with chronic Epstein–Barr virus infections. N Engl J Med 318(12):733–741. doi:10.1056/NEJM198803243181203
Rezk SA, Weiss LM (2007) Epstein–Barr virus-associated lymphoproliferative disorders. Hum Pathol 38(9):1293–1304. doi:10.1016/j.humpath.2007.05.020
Shibata D, Hansmann ML, Weiss LM, Nathwani BN (1991) Epstein–Barr virus infections and Hodgkin’s disease: a study of fixed tissues using the polymerase chain reaction. Hum Pathol 22(12):1262–1267
Evans AS, Gutensohn NM (1984) A population-based case–control study of EBV and other viral antibodies among persons with Hodgkin’s disease and their siblings. Int J Cancer 34(2):149–157
Pallesen G, Hamilton-Dutoit SJ, Rowe M, Young LS (1991) Expression of Epstein–Barr virus latent gene products in tumour cells of Hodgkin’s disease. Lancet 337(8737):320–322
Anagnostopoulos I, Herbst H, Niedobitek G, Stein H (1989) Demonstration of monoclonal EBV genomes in Hodgkin’s disease and Ki-1-positive anaplastic large cell lymphoma by combined Southern blot and in situ hybridization. Blood 74(2):810–816
Staratschek-Jox A, Kotkowski S, Belge G, Rudiger T, Bullerdiek J, Diehl V, Wolf J (2000) Detection of Epstein–Barr virus in Hodgkin-Reed-Sternberg cells: no evidence for the persistence of integrated viral fragments inLatent membrane protein-1 (LMP-1)-negative classical Hodgkin’s disease. Am J Pathol 156(1):209–216. doi:10.1016/S0002-9440(10)64721-9
Khan G, Coates PJ, Kangro HO, Slavin G (1992) Epstein Barr virus (EBV) encoded small RNAs: targets for detection by in situ hybridisation with oligonucleotide probes. J Clin Pathol 45(7):616–620
Khan G (2009) Screening for Epstein–Barr virus in Hodgkin’s lymphoma. Methods Mol Biol 511:311–322. doi:10.1007/978-1-59745-447-6_13
Enblad G, Sandvej K, Sundstrom C, Pallesen G, Glimelius B (1999) Epstein–Barr virus distribution in Hodgkin’s disease in an unselected Swedish population. Acta Oncol 38(4):425–429
Chang KL, Albujar PF, Chen YY, Johnson RM, Weiss LM (1993) High prevalence of Epstein–Barr virus in the Reed–Sternberg cells of Hodgkin’s disease occurring in Peru. Blood 81(2):496–501
Katebi M, Sharifi N, Tarhini M, Otrock ZK, Bazarbachi A, Kchour G (2008) Frequency of Epstein–Barr virus expression in various histological subtypes of Hodgkin’s lymphoma. Histopathology 52(6):775–777. doi:10.1111/j.1365-2559.2008.03019.x
Mourad W, Alsohaibani MO, Saddik M, Bazerbashi S (1998) Epstein–Barr virus expression in Hodgkin’s disease: correlation with histologic subtypes and T and B lymphocyte distribution. Ann Saudi Med 18(4):296–300
Almasri NM, Khalidi HS (2004) Epstein–Barr virus expression in Hodgkin’s disease in Jordan. Saudi Med J 25(6):770–775
Levine PH, Pallesen G, Ebbesen P, Harris N, Evans AS, Mueller N (1994) Evaluation of Epstein–Barr virus antibody patterns and detection of viral markers in the biopsies of patients with Hodgkin’s disease. Int J Cancer 59(1):48–50
Enblad G, Sandvej K, Lennette E, Sundstrom C, Klein G, Glimelius B, Pallesen G (1997) Lack of correlation between EBV serology and presence of EBV in the Hodgkin and Reed–Sternberg cells of patients with Hodgkin’s disease. Int J Cancer 72(3):394–397. doi:10.1002/(SICI)1097-0215(19970729)72:3<394::AID-IJC3>3.0.CO;2-K
Axdorph U, Porwit-MacDonald A, Sjoberg J, Grimfors G, Ekman M, Wang W, Biberfeld P, Bjorkholm M (1999) Epstein–Barr virus expression in Hodgkin’s disease in relation to patient characteristics, serum factors and blood lymphocyte function. Br J Cancer 81(7):1182–1187. doi:10.1038/sj.bjc.6690827
Abdel-Fattah MM, Yassine OG (2007) Non-Hodgkin’s lymphomas in Alexandria, Egypt; incidence rates and trend study (1995–2004). Eur J Cancer Prev 16(5):479–485. doi:10.1097/01.cej.0000243858.91642.c9
Wu XC, Andrews P, Chen VW, Groves FD (2009) Incidence of extranodal non-Hodgkin lymphomas among whites, blacks, and Asians/Pacific Islanders in the United States: anatomic site and histology differences. Cancer Epidemiol 33(5):337–346. doi:10.1016/j.canep.2009.09.006
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This study was supported by an unrestricted grant from Hoffman La Roche pharmaceutical.
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Otrock, Z.K., Saab, J., Aftimos, G. et al. A Collaborative Nationwide Lymphoma Study in Lebanon: Incidence of Various Subtypes and Analysis of Associations with Viruses. Pathol. Oncol. Res. 19, 715–722 (2013). https://doi.org/10.1007/s12253-013-9634-0
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DOI: https://doi.org/10.1007/s12253-013-9634-0