Skip to main content

Advertisement

SpringerLink
Log in

Viral and non-viral risk factors for non-Hodgkin’s lymphoma in Egypt: heterogeneity by histological and immunological subtypes

  • Original Paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Objective

Non-Hodgkin’s lymphomas (NHL) are etiologically heterogeneous malignancies. In Egypt, we previously reported an association of increased NHL risk with chronic hepatitis C virus (HCV) infection. Our present aim is to assess the association between HCV infection and histological subtypes of NHL.

Methods

We conducted a case–control study at the National Cancer Institute of Cairo University. Cases with NHL (n = 486) were matched to controls (n = 786) who were orthopedic patients from the same referral regions. Participants provided a blood sample for HCV markers (anti-HCV, HCV RNA) and answered a questionnaire on possible risk factors. Case–control differences were assessed by odds ratios and 95% confidence intervals from logistic regression analysis.

Results

Cases with diffuse large B cell lymphoma (n = 146), chronic lymphocytic leukemia (n = 58), marginal zone lymphoma (n = 24), follicular lymphoma (n = 23), and mantle cell lymphoma (n = 16) were recruited. HCV RNA prevalence was 27% in controls and 26%–48% in the NHL subgroups: it was associated (p < 0.001) with diffuse large B cell, marginal zone, and follicular lymphomas with odds ratios of 3.2, 4.4, and 3.3, respectively.

Conclusion

HCV is a risk factor for diffuse large B cell, marginal zone, and follicular lymphomas in Egypt.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

NHL:

Non-Hodgkin’s lymphoma

HCV:

Hepatitis C virus

CLL:

Chronic lymphocytic leukemia

WHO:

World Health Organization

OR:

Odds ratio

CI:

Confidence interval

NCI:

National Cancer Institute

EIA:

Enzyme-linked immunoassay

RT-PCR:

Reverse transcription-polymerase chain reaction

References

  1. World Health Organization (2000) Hepatitis C Infection. Report Number 164

  2. Abdel-Aziz F, Habib M, Mohamed MK et al (2000) Hepatitis C virus (HCV) infection in a community in the Nile Delta: population description and HCV prevalence. Hepatology 32:111–115. doi:10.1053/jhep.2000.8438

    Article  PubMed  CAS  Google Scholar 

  3. Darwish MA, Faris R, Clemens JD, Rao MR, Edelman R (1996) High seroprevalence of hepatitis A, B, C, and E viruses in residents in an Egyptian village in The Nile Delta: a pilot study. Am J Trop Med Hyg 54:554–558

    PubMed  CAS  Google Scholar 

  4. Ezzat S, Abdel-Hamid M, Eissa SA et al (2005) Associations of pesticides, HCV, HBV, and hepatocellular carcinoma in Egypt. Int J Hyg Environ Health 208:329–339. doi:10.1016/j.ijheh.2005.04.003

    Article  PubMed  CAS  Google Scholar 

  5. Frank C, Mohamed MK, Strickland GT et al (2000) The role of parenteral antischistosomal therapy in the spread of hepatitis C virus in Egypt. Lancet 355:887–891. doi:10.1016/S0140-6736(99)06527-7

    Article  PubMed  CAS  Google Scholar 

  6. Quinn ER, Chan CH, Hadlock KG, Foung SK, Flint M, Levy S (2001) The B-cell receptor of a hepatitis C virus (HCV)-associated non-Hodgkin lymphoma binds the viral E2 envelope protein, implicating HCV in lymphomagenesis. Blood 98:3745–3749. doi:10.1182/blood.V98.13.3745

    Article  PubMed  CAS  Google Scholar 

  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 107:3034–3044. doi:10.1182/blood-2005-09-3679

    Article  PubMed  CAS  Google Scholar 

  8. Turner NC, Dusheiko G, Jones A (2003) Hepatitis C and B-cell lymphoma. Ann Oncol 14:1341–1345. doi:10.1093/annonc/mdg363

    Article  PubMed  CAS  Google Scholar 

  9. 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 15:2078–2085. doi:10.1158/1055-9965.EPI-06-0308

    Article  PubMed  CAS  Google Scholar 

  10. Cowgill KD, Loffredo CA, Eissa SA et al (2004) Case–control study of non-Hodgkin’s lymphoma and hepatitis C virus infection in Egypt. Int J Epidemiol 33:1034–1039. doi:10.1093/ije/dyh183

    Article  PubMed  Google Scholar 

  11. Abdel-Hamid M, Edelman DC, Highsmith WE, Constantine NT (1997) Optimization, assessment, and proposed use of a direct nested reverse transcription-polymerase chain reaction protocol for the detection of hepatitis C virus. J Hum Virol 1:58–65

    PubMed  CAS  Google Scholar 

  12. De Re V, De Vita S, Marzotto A et al (2000) 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 96:3578–3584

    PubMed  Google Scholar 

  13. Gisbert JP, Garcia-Buey L, Pajares JM, Moreno-Otero R (2003) Prevalence of hepatitis C virus infection in B-cell non-Hodgkin’s lymphoma: systematic review and meta-analysis. Gastroenterology 125:1723–1732. doi:10.1053/j.gastro.2003.09.025

    Article  PubMed  Google Scholar 

  14. Shapira MY, Muszkat M, Braunstein I, Gotsman I (2001) Co-occurrence of hepatocellular carcinoma and lymphoma in patients with hepatitis C virus cirrhosis. J Clin Gastroenterol 32:368–369. doi:10.1097/00004836-200104000-00023

    Article  PubMed  CAS  Google Scholar 

  15. Talamini R, Montella M, Crovatto M et al (2004) Non-Hodgkin’s lymphoma and hepatitis C virus: a case–control study from northern and southern Italy. Int J Cancer 110:380–385. doi:10.1002/ijc.20137

    Article  PubMed  CAS  Google Scholar 

  16. Arican A, Sengezer T, Bozdayi M et al (2000) Prevalence of hepatitis-G virus and hepatitis-C virus infection in patients with non-Hodgkin’s lymphoma. Med Oncol 17:123–126. doi:10.1007/BF02796207

    Article  PubMed  CAS  Google Scholar 

  17. Shariff S, Yoshida EM, Gascoyne RD et al (1999) Hepatitis C infection and B-cell non-Hodgkin’s lymphoma in British Columbia: a cross-sectional analysis. Ann Oncol 10:961–964. doi:10.1023/A:1008361311409

    Article  PubMed  CAS  Google Scholar 

  18. Cucuianu A, Patiu M, Duma M et al (1999) Hepatitis B and C virus infection in Romanian non-Hodgkin’s lymphoma patients. Br J Haematol 107:353–356. doi:10.1046/j.1365-2141.1999.01692.x

    Article  PubMed  CAS  Google Scholar 

  19. Gasztonyi B, Par A, Szomor A et al (2000) Hepatitis C virus infection associated with B-cell non-Hodgkin’s lymphoma in Hungarian patients. Br J Haematol 110:497–498

    PubMed  CAS  Google Scholar 

  20. Silvestri F, Baccarani M (1997) Hepatitis C virus-related lymphomas. Br J Haematol 99:475–480. doi:10.1046/j.1365-2141.1997.4023216.x

    Article  PubMed  CAS  Google Scholar 

  21. Zuckerman E, Zuckerman T, Levine AM et al (1997) Hepatitis C virus infection in patients with B-cell non-Hodgkin lymphoma. Ann Intern Med 127:423–428

    PubMed  CAS  Google Scholar 

  22. Collier JD, Zanke B, Moore M et al (1999) No association between hepatitis C and B-cell lymphoma. Hepatology 29:1259–1261. doi:10.1002/hep.510290422

    Article  PubMed  CAS  Google Scholar 

  23. Ellenrieder V, Weidenbach H, Frickhofen N et al (1998) HCV and HGV in B-cell non-Hodgkin’s lymphoma. J Hepatol 28:34–39. doi:10.1016/S0168-8278(98)80199-2

    Article  PubMed  CAS  Google Scholar 

  24. Hausfater P, Cacoub P, Rosenthal E et al (2000) Hepatitis C virus infection and lymphoproliferative diseases in France: a national study. The GERMIVIC Group. Am J Hematol 64:107–111. doi:10.1002/(SICI)1096-8652(200006)64:<107::AID-AJH6>3.0.CO;2-C

    Article  PubMed  CAS  Google Scholar 

  25. Sanchez Ruiz AC, Yebra BM, Portero F, Provencio PM, Miralles FC, Espana SP (2001) Prevalence of hepatitis C virus infection in patients with non-Hodgkin’s lymphoma. Med Clin (Barc.) 116:333–334

    CAS  Google Scholar 

  26. Zucca E, Bertoni F, Roggero E, Cavalli F (2000) The gastric marginal zone B-cell lymphoma of MALT type. Blood 96:410–419

    PubMed  CAS  Google Scholar 

  27. de Sanjose S, Benavente Y, Vajdic CM et al (2008) Hepatitis C and non-Hodgkin lymphoma among 4784 cases and 6269 controls from the International Lymphoma Epidemiology Consortium. Clin Gastroenterol Hepatol 6:451–458. doi:10.1016/j.cgh.2008.02.011

    Article  PubMed  Google Scholar 

  28. Schollkopf C, Smedby KE, Hjalgrim H et al (2008) Hepatitis C infection and risk of malignant lymphoma. Int J Cancer 122:1885–1890. doi:10.1002/ijc.23416

    Article  PubMed  CAS  Google Scholar 

  29. Seve P, Renaudier P, Sasco AJ et al (2004) Hepatitis C virus infection and B-cell non-Hodgkin’s lymphoma: a cross-sectional study in Lyon, France. Eur J Gastroenterol Hepatol 16:1361–1365. doi:10.1097/00042737-200412000-00021

    Article  PubMed  Google Scholar 

  30. Cerhan JR, Wallace RB, Folsom AR et al (1997) Medical history risk factors for non-Hodgkin’s lymphoma in older women. J Natl Cancer Inst 89:314–318

    PubMed  CAS  Google Scholar 

  31. Cerhan JR, Wallace RB, Dick F et al (2001) Blood transfusions and risk of non-Hodgkin’s lymphoma subtypes and chronic lymphocytic leukemia. Cancer Epidemiol Biomarkers Prev 10:361–368

    PubMed  CAS  Google Scholar 

  32. Kato I, Koenig KL, Baptiste MS et al (2003) History of antibiotic use and risk of non-Hodgkin’s lymphoma (NHL). Int J Cancer 107:99–105. doi:10.1002/ijc.11356

    Article  PubMed  CAS  Google Scholar 

  33. Holly EA, Bracci PM (2003) Population-based study of non-Hodgkin lymphoma, histology, and medical history among human immunodeficiency virus-negative participants in San Francisco. Am J Epidemiol 158:316–327. doi:10.1093/aje/kwg145

    Article  PubMed  Google Scholar 

  34. Besson H, Renaudier P, Merrill RM et al (2003) Smoking and non-Hodgkin’s lymphoma: a case–control study in the Rhone-Alpes region of France. Cancer Causes Control 14:381–389. doi:10.1023/A:1023978730962

    Article  PubMed  Google Scholar 

  35. Stagnaro E, Tumino R, Parodi S et al (2004) Non-Hodgkin’s lymphoma and type of tobacco smoke. Cancer Epidemiol Biomarkers Prev 13:431–437

    PubMed  Google Scholar 

  36. McDuffie HH, Pahwa P, Spinelli JJ et al (2002) Canadian male farm residents, pesticide safety handling practices, exposure to animals and non-Hodgkin’s lymphoma (NHL). Am J Ind Med Suppl 2:54–61. doi:10.1002/ajim.10041

    Article  Google Scholar 

  37. Miligi L, Costantini AS, Bolejack V et al (2003) Non-Hodgkin’s lymphoma, leukemia, and exposures in agriculture: results from the Italian multicenter case–control study. Am J Ind Med 44:627–636. doi:10.1002/ajim.10289

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by NIH Grant R01CA85888. The authors thank Karen Cowgill for her contributions to the study design and supervision of the initial years of field work. The Department of Pathology at the National Cancer Institute of Cairo University provided outstanding institutional support for the recruitment of cases and the confirmation of their diagnoses. Likewise, we are grateful to the Kasr El Aini Faculty of Medicine for supporting the recruitment of controls.

Author information

Authors and Affiliations

  1. Lombardi Cancer Center, Georgetown University, 3800 Reservoir Rd, P.O. Box 571465, Washington, DC, 20057-1465, USA

    Lenka Goldman & Christopher A. Loffredo

  2. MD Anderson, Houston, TX, USA

    Nathan Fowler

  3. National Liver Institute, Shibin El Kom, Egypt

    Sameera Ezzat

  4. National Cancer Institute, Cairo University, Cairo, Egypt

    Nadia Mokhtar, Amany Abdel-Hamid, Iman Gouda & Soheir Abdel Latif Eissa

  5. Minia University, Minia, Egypt

    Mohamed Abdel-Hamid

Authors
  1. Lenka Goldman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sameera Ezzat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nadia Mokhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Amany Abdel-Hamid
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nathan Fowler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Iman Gouda
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Soheir Abdel Latif Eissa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mohamed Abdel-Hamid
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Christopher A. Loffredo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher A. Loffredo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Goldman, L., Ezzat, S., Mokhtar, N. et al. Viral and non-viral risk factors for non-Hodgkin’s lymphoma in Egypt: heterogeneity by histological and immunological subtypes. Cancer Causes Control 20, 981–987 (2009). https://doi.org/10.1007/s10552-009-9316-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-009-9316-0

Keywords

Search

Navigation