• RAWA YOUSIF HAMA SALIH Department of Hematology, Azadi Teaching Hospital, Duhok, Kurdistan Region, Iraq
  • RAFIL T.YAQO Lecturer, Department of Pathology, College of Medicine, University of Duhok, Kurdistan Region, Iraq.
  • SARAH AL ALLAWI, Azadi Teaching Hospital, Duhok, Kurdista
  • NASIR AL-ALLAWI Professor, Department of Pathology, College of Medicine, University of Duhok, Kurdistan Region, Iraq.
Keywords: EBV, Hodgkin Lymphoma, Iraq, EBER, LMP1



Background: Epstein Barr virus (EBV) has been linked to the etiology of several malignancies, including Hodgkin's Lymphoma (HL). However, the degree of this association varies between different geographical regions and age of EBV exposure. No study has addressed such an association in Kurdistan, northern Iraq, and thus this study was initiated.

Patients and methods: A total of 91 patients diagnosed as HL over a 10 year period were studied. These patients had their records and slides reviewed and the additional immunohistochemistry, including that for LMP1 as well as in situ hybridization for EBER performed.

Results: The patients had a mean age (SD) of 28.8 (16.2) years and had a male to female ratio of 1.7:1. They included 3.3% with Nodular Lymphocyte Predominant HL (NLPHL) and 96.7% Classical HL (cHL). The most common 2 subtypes of the latter were nodular sclerosis (NS) and mixed cellularity (MC) at 52.7% and 36.6% respectively. It was found that 40 cases (44.0%) were latent membrane protein 1 (LMP1) and/or EBER positive. The positivity was significantly higher in males (P=0.009), mixed cellularity subtype (P<0.001) and in the ages ≥45 and ≤15 years when compared to those 16- 44 years (P=0.004).

Conclusion: HL in Iraqi Kurdistan demonstrates a frequency of EBV virus infection that approaches the levels seen in Western countries and is coupled with a changing histological pattern of classical HL from MC to NS. This is likely to be a reflection of the improving socioeconomic status of the population of the region.


Download data is not yet available.


1. Kumar V, Abbas AK, Aster JC. Robbins Basic Pathology.10th edition. Philadelphia, Elsevier Publishers. 2017.
2. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al. WHO Classification of Tumors of Haemopietic and Lymphoid tissue. 4th edition.IARC 2017.
3. Massini G, Siemer D, Hohaus S. EBV in Hodgkin Lymphoma. Medit J Hemat Infect Dis. 2009; 1(2): e2009013.
4. Gandhi MK, Tellam JT, Khanna R. Epstein-Barr virus-associated Hodgkin's Lymphoma. Brit J Haematol. 2004; 125: 267-281.
5. Huang X, Nolte I, Gao Z, Vos H, Hepkema B, Poppema S, et al. Epidemiology of classical Hodgkin lymphoma and its association with Epstein barr virus in northern China. PLoS One. 2011; 6(6): e21152
6. Gulley ML, Glaser SL, Craig FE, Borowitz M, Mann RB, Shema SJ, Ambinder RF. Guidelines for interpreting EBER in situ hybridization and LMP1 immunohistochemical tests for detecting Epstein-Barr virus in Hodgkin Lymphoma. Amer J Clin Pathol. 2002; 117: 259-267.
7. Ministry of Health results on Iraqi Cancer Registry 2010. Iraqi Cancer Board, Baghdad-Iraq. 8. Yahya HI, Al-Saleem T, Tikriti F, Zardawi IM, Talib H. Hodgkin's disease in Iraq: A clinico-pathological study of 85 cases. Clin Oncol. 1979; 5:69-71
9. Alsabti EA. Histopathological subtypes of Hodgkin's disease in childhood in Iraq. Jpn J Exp Med. 1979; 49:319-24
10. Al-Barzinji RM. Hodgkin's Lymphoma: An epidemiological study in the Iraqi patients. The Iraqi Postgraduate Medical Journal. 2006; 5(3): 337-343.
11. Yaqo RT, Hughson MD, Sulayani FK, Al-Allawi NA. Malignant lymphoma in northern Iraq: A retrospective analysis of 270 cases according to the World Health Organization classification. Indian J Cancer. 2011; 48(4): 446-51.
12. Shamoon RP, Ali MD, ShabilaNP. Overview and outcome of Hodgkin's lymphoma:Experience of a single developing country oncology centre. PLoS One. 2018; 13(4): e0195629.
13. Al-Mudallal SS, Al-Sinjery GM. Immunohistochemical expression of Epstein Barr virus antigen latent membrane protein-1 and Bcl-2 in classical Hodgkin lymphoma. Iraqi J Med Sci. 2012; 10(3): 234-242.
14. Fadhil MS, Al-Nueimy WM, Lazim AF.Hodgkin's lymphoma. An immunohistochemical profile in northern Iraq. Saudi Med J. 2014; 35(5):448-53
15. Al-Diab AI, Siddiqui N, Sogiawalla FF, Fawzy EM. The changing trends of adult Hodgkin's disease in Saudi Arabia. Saudi Med J. 2003; 24(6): 617-622.
16. Sughayer M, Haddad HA, Al-Yousef RM, El-khateeb M, Abu Rass H. Epstein-Barr virus and Hodgkin Lymphoma in Jordan. Hematol Oncol Stem Cell Ther. 2014; 7(2): 85-89.
17. Pourtsidis A, Doganis D, Baka M, Bouhoutsou D, Varvoutsi M, Synodinou M, et al. Successful Treatment in Children with Hodgkin Lymphoma in Greece; A 20-Year Experience in a Single Institution.
Lymphoma. 2012; 2012, Article ID 215868, 7 pages.
18. Shenoy P, Maggioncalda A, Malik N, Flowers CR. Incidence Patterns and Outcomes for Hodgkin Lymphoma Patients in the United States. Advances in Hematology. 2011; 2011; Article ID 725219, 11 pages.
19. Karnik S, Srinivasan B, Nair S, Hodgkin's lymphoma: immunohistochemical features and its association with EBV LMP-1. Experience from a South Indian hospital. Pathology. 2003 ;35(3):20711
20. Engel M, Essop M F, Close P, Hartley P, Pallesen G, Sinclair-Smith C. Improved prognosis of Epstein-Barr virus associated childhood Hodgkin’s lymphoma: study of 47 South African cases. J Clin Pathol. 2000; 53(3):1826.
21. Elgui de Oliveira D, Bacchi MM, Abreu ES. Hodgkin's disease in adult and juvenile groups from two different geographic regions in Brazil: characterization of clinicopathologic aspects and relationship with EB virus infection. Am J Clin Pathol. 2002;118: 25-30.
22. Weinreb M, Day PJ, Niggli F, Green EK, Nyong'o AO, Othieno-Abingo NA, et al. The consistent association between EB virus and Hodgkin's disease in children in Kenya. Blood. 1996; 87:3828-3836. 23. Peh SC, Kim LH, Mun KS, Tan EL, Sam CK, Poppema S. Epstein-Barr virus (EBV) subtypes and variants in malignant tissue from Malaysian patients. J Clin Exp Hematopathol. 2003; 43(2): 61-9.
24. Andriko JA, Aguilera NS, Nandedkar MA. Childhood Hodgkins disease in the United States:an analysis of histologic subtypes and association with EB virus. Mod Pathol. 1997; 10:366-371.
25. Pallesan G, Hamilton-Dutoit SJ, Rowe M, Young LS. Expression of EB virus latent gene products in tumor cells of Hodgkin's disease. Lancet. 1991; 337:320-322.
26. Brousset P, Chittal S, Schleifer D, Icart J, Payen C, Huguet FR, et al. Detection of EB virus messenger RNA in Reed-Sternberg cells of Hodgkin's disease by in situ hybridization with biotinylated probes on specially processed modified acetone methyl benzoate xylene (ModAMex) sections. Blood. 1991; 77:1781-1786.
27. Al-Salam S, John A, Daoud S, Chong SM, Castella A. Expression of Epstein–Barr virus in Hodgkin lymphoma in a population of United Arab Emirates nationals. Leuk Lymphoma. 2008; 49 (9): 1769-77
28. Al-kuraya K, Narayanappa R, AlDayel F, El-Solh H, Ezzat A, Ismail H, et al. Epstein-Barr virus infection is not the sole cause of high prevalence of Hodgkin's lymphoma in Saudi Arabia. Leuk Lymphoma. 2006; 47: 707-713.
29. Glaser SL, Lin RJ, Stewart SL, Ambinder RF, Jarrett RF, Brousset P, et al. Epstein-Barr virus-associated Hodgkin's disease: epidemiological characteristics in international data. Int. J. Cancer. 1997; 70: 375–382
30. Carbone A, Gloghini A. Epstein Barr Virus-associated Hodgkin Lymphoma.
Cancers (Basel). 2018; 10(6). pii: E163.
31. Audouin J, Diebold J, Nathwani B, Ishak E, MacLennan K, MuellerHermelink HK, et al. Epstein-Barr virus and Hodgkin's Lymphoma in Cairo, Egypt J Hematopathol. 2010; 3: 11-18.
32. Chang ET, Zheng T, Lennette ET, Weir EG, Borowitz M, Mann RB, et al. Heterogeneity of risk factors and antibody profiles in Epstein-Barr virus genome positive and negative Hodgkin lymphoma. J Infect dis. 2004; 189: 2271-2281.
33. Campos AHJFM, Moreira A, Ribeiro KB, Paes RP, Zerbini MC, Aldred V, et al. Frequency of EBV associated classical Hodgkin Lymphoma decreases over a 54-year period in a Brazilian population. Scientific reports. 2018; 8: 1849.
34. Whitacre CC, Reingold SC, O'Looney PA. A gender gap in autoimmunity. Science. 1999; 283: 1277-1278.
How to Cite
YOUSIF HAMA SALIH, R., T.YAQO, R., AL ALLAWI, S., & AL-ALLAWI, N. (2019). HODGKIN LYMPHOMA AND ITS ASSOCIATION WITH EPSTEIN-BARR VIRUS IN KURDISTAN, NORTHERN IRAQ. Duhok Medical Journal, 13(2), 74-83. Retrieved from https://dmj.uod.ac/index.php/dmj/article/view/93