Skip to main content

Advertisement

Log in

Epidemiology of non-Hodgkin’s lymphoma (NHL): trends, geographic distribution, and etiology

  • Review Article
  • Published:
Annals of Hematology Aims and scope Submit manuscript

Abstract

While for most cancers incidence and mortality are decreasing, those of non-Hodgkin’s lymphoma (NHL) are steadily increasing. Research to define reasons for this increase is extensive, but has not yet resolved them. We have conducted a literature analysis on trends regarding changes in the incidence, geographic distribution, and etiologic factors of NHL. From our own and previous analyses, an increasing NHL incidence at a rate of 3–4% per year was observed for the 1970s and 1980s. This stabilized in the 1990s, nevertheless still with an annual rise of 1–2%, resulting in almost a doubling of the NHL incidence. This rise has been noted worldwide, particularly in elderly persons >55 years. Concerning gender subgroups, a male predominance throughout all age groups is apparent. Although the NHL incidence has historically been higher in whites than blacks, disproportional increases have recently been observed in the latter group. Increases in high-grade NHL and extranodal disease are predominant. Differences in geographic distribution are striking for follicular lymphoma, which is more common in Western countries than elsewhere. Asians have higher rates of aggressive NHL, T-cell lymphomas, and extranodal disease. In the Middle East, high rates of intestinal extranodal disease are observed, whereas in Africa, endemic Burkitt’s lymphoma accounts for a substantial proportion. Risks for developing NHL include immunosuppression and a causal link between infectious agents, and lymphomagenesis has also been determined, particularly for human T-cell leukemia/lymphoma virus type 1 (HTLV-1), Epstein-Barr virus (EBV), and Helicobacter pylori infections. Exposure to environmental agents and occupational risks have been studied; however, their significance is as yet uncertain.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Adami J, Gabel H, Lindelof B, Ekstrom K, Rydh B, Glimelius B, Ekbom A, Adami HO, Granath F (2003) Cancer risk following organ transplantation: a nationwide cohort study in Sweden. Br J Cancer 89:1221–1227

    Article  CAS  PubMed  Google Scholar 

  2. Altekruse SF, Henley SJ, Thun MJ (1999) Deaths from hematopoietic and other cancers in relation to permanent hair dye use in a large prospective study (United States). Cancer Causes Control 10:617–625

    Article  CAS  PubMed  Google Scholar 

  3. Anderson JR, Armitage JO, Weisenburger DD (1998) Epidemiology of the non-Hodgkin’s lymphomas: distributions of the major subtypes differ by geographic locations. Non-Hodgkin’s lymphoma classification project. Ann Oncol 9:717–720

    Article  CAS  PubMed  Google Scholar 

  4. Arisawa K, Soda M, Endo S, Kurokawa K, Katamine S, Shimokawa I, Koba T, Takahashi T, Saito H, Doi H, Shirahama S (2000) Evaluation of adult T-cell leukemia/lymphoma incidence and its impact on non-Hodgkin lymphoma incidence in southwestern Japan. Int J Cancer 85:319–324

    Article  CAS  PubMed  Google Scholar 

  5. Ballerini P, Gaidano G, Gong JZ, Tassi V, Saglio G, Knowles DM, Dalla-Favera R (1993) Multiple genetic lesions in acquired immunodeficiency syndrome-related non-Hodgkin’s lymphoma. Blood 81:166–176

    CAS  PubMed  Google Scholar 

  6. Banks PM (1992) Changes in diagnosis of non-Hodgkin’s lymphomas over time. Cancer Res 52:5453s–5455s

    CAS  PubMed  Google Scholar 

  7. Bentham G (1996) Association between incidence of non-Hodgkin’s lymphoma and solar ultraviolet radiation in England and Wales. BMJ 312:1128–1131

    CAS  PubMed  Google Scholar 

  8. Boice JD Jr (1992) Radiation and non-Hodgkin’s lymphoma. Cancer Res 52:5489s–5491s

    PubMed  Google Scholar 

  9. Cancer facts and figures 2004. American Cancer Society (www.cancer.org)

  10. Cantor KP, Blair A, Everett G, VanLier S, Burmeister L, Dick FR, Gibson RW, Schuman L (1988) Hair dye use and risk of leukemia and lymphoma. Am J Public Health 78:570–571

    CAS  PubMed  Google Scholar 

  11. Carli PM, Boutron MC, Maynadie M, Bailly F, Caillot D, Petrella T (1994) Increase in the incidence of non-Hodgkin’s lymphomas: evidence for a recent sharp increase in France independent of AIDS. Br J Cancer 70:713–715

    CAS  PubMed  Google Scholar 

  12. Cartwright RA (1992) Changes in the descriptive epidemiology of non-Hodgkin’s lymphoma in Great Britain? Cancer Res 52:5441s–5442s

    CAS  PubMed  Google Scholar 

  13. Casanova M, Cole P, Collins JJ, Conolly R, Delzell E, Heck Hd HA, Leonard R, Lewis R, Marsh GM, Ott MG, Sorahan T, Axten CW (2004) Mortality from lymphohematopoietic malignancies among workers in formaldehyde industries. J Natl Cancer Inst 96:966–967

    Google Scholar 

  14. Cerhan JR, Wallace RB, Folsom AR, Potter JD, Sellers TA, Zheng W, Lutz CT (1997) Medical history risk factors for non-Hodgkin’s lymphoma in older women. J Natl Cancer Inst 89:314–318

    CAS  PubMed  Google Scholar 

  15. Cerhan JR, Janney CA, Vachon CM, Habermann TM, Kay NE, Potter JD, Sellers TA, Folsom AR (2002) Anthropometric characteristics, physical activity, and risk of non-Hodgkin’s lymphoma subtypes and B-cell chronic lymphocytic leukemia: a prospective study. Am J Epidemiol 156:527–535

    Article  PubMed  Google Scholar 

  16. Clarke CA (2001) Changing incidence of Kaposi’s sarcoma and non-Hodgkin’s lymphoma among young men in San Francisco. AIDS 15:1913–1915

    Article  CAS  PubMed  Google Scholar 

  17. Clarke CA, Glaser SL (2002) Changing incidence of non-Hodgkin lymphomas in the United States. Cancer 94:2015–2023

    Article  PubMed  Google Scholar 

  18. Collins JJ, Ireland B, Buckley CF, Shepperly D (2003) Lymphohaematopoeitic cancer mortality among workers with benzene exposure. Occup Environ Med 60:676–679

    Article  CAS  PubMed  Google Scholar 

  19. Cook-Mozaffari P, Newton R, Beral V, Burkitt DP (1998) The geographical distribution of Kaposi’s sarcoma and of lymphomas in Africa before the AIDS epidemic. Br J Cancer 78:1521–1528

    CAS  PubMed  Google Scholar 

  20. Corrao G, Corazza GR, Bagnardi V, Brusco G, Ciacci C, Cottone M, Sategna Guidetti C, Usai P, Cesari P, Pelli MA, Loperfido S, Volta U, Calabro A, Certo M, Club del Tenue Study Group (2001) Mortality in patients with coeliac disease and their relatives: a cohort study. Lancet 358:356–361

    Article  CAS  PubMed  Google Scholar 

  21. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860–867

    Article  CAS  PubMed  Google Scholar 

  22. Dal Maso L, Serraino D, Franceschi S (2001) Epidemiology of AIDS-related tumours in developed and developing countries. Eur J Cancer 37:1188–1201

    Article  CAS  PubMed  Google Scholar 

  23. Dalton SO, Johansen C, Mellemkjaer L, Sorensen HT, McLaughlin JK, Olsen J, Olsen JH (2000) Antidepressant medications and risk for cancer. Epidemiology 11:171–176

    Article  CAS  PubMed  Google Scholar 

  24. Devesa SS, Fears T (1992) Non-Hodgkin’s lymphoma time trends: United States and international data. Cancer Res 52:5432s–5440s

    CAS  PubMed  Google Scholar 

  25. De Vita S, Sacco C, Sansonno D, Gloghini A, Dammacco F, Crovatto M, Santini G, Dolcetti R, Boiocchi M, Carbone A, Zagonel V (1997) Characterization of overt B-cell lymphomas in patients with hepatitis C virus infection. Blood 90:776–782

    PubMed  Google Scholar 

  26. Dong C, Hemminki K (2001) Second primary neoplasms among 53 159 haematolymphoproliferative malignancy patients in Sweden, 1958–1996: a search for common mechanisms. Br J Cancer 85:997–1005

    Article  CAS  PubMed  Google Scholar 

  27. Echimane AK, Ahnoux AA, Adoubi I, Hien S, M’Bra K, D’Horpock A, Diomande M, Anongba D, Mensah-Adoh I, Parkin DM (2000) Cancer incidence in Abidjan, Ivory Coast: first results from the cancer registry, 1995–1997. Cancer 89:653–663

    Article  CAS  PubMed  Google Scholar 

  28. Ferlay J, Bray F, Pisani P, Parkin DM (2001) Globocan 2000: cancer incidence, mortality and prevalence worldwide, version 1.0. IARC CancerBase No. 5. IARC, Lyon. Limited version available from http://www-dep.iarc.fr/globocan/globocan.htm (last updated on 03/02/2001)

    Google Scholar 

  29. Ferreri AJ, Guidoboni M, Ponzoni M, De Conciliis C, Dell’Oro S, Fleischhauer K, Caggiari L, Lettini AA, Dal Cin E, Ieri R, Freschi M, Villa E, Boiocchi M, Dolcetti R (2004) Evidence for an association between Chlamydia psittaci and ocular adnexal lymphomas. J Natl Cancer Inst 96:586–594

    Google Scholar 

  30. Ferri C, Caracciolo F, Zignego AL, La Civita L, Monti M, Longombardo G, Lombardini F, Greco F, Capochiani E, Mazzoni A (1994) Hepatitis C virus infection in patients with non-Hodgkin’s lymphoma. Br J Haematol 88:392–394

    CAS  PubMed  Google Scholar 

  31. Filipovich AH, Mathur A, Kamat D, Shapiro RS (1992) Primary immunodeficiencies: genetic risk factors for lymphoma. Cancer Res 52:5465s–5467s

    CAS  PubMed  Google Scholar 

  32. Franchini G, Fukumoto R, Fullen JR (2003) T-cell control by human T-cell leukemia/lymphoma virus type 1. Int J Hematol 78:280–296

    CAS  PubMed  Google Scholar 

  33. Freedman DM, Zahm SH, Dosemeci M (1997) Residential and occupational exposure to sunlight and mortality from non-Hodgkin’s lymphoma: composite (threefold) case-control study. BMJ 314:1451–1455

    CAS  PubMed  Google Scholar 

  34. Gisbert JP, Khorrami S, Calvet X, Pajares JM (2004) Pantoprazole based therapies in Helicobacter pylori eradication: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 16:89–99

    CAS  PubMed  Google Scholar 

  35. Gniadecki R, Rossen K, Ralfkier E, Thomsen K, Skovgaard GL, Jonsson V (2004) CD56+ lymphoma with skin involvement: clinicopathologic features and classification. Arch Dermatol 140:427–436

    Google Scholar 

  36. Green PH, Fleischauer AT, Bhagat G, Goyal R, Jabri B, Neugut AI (2003) Risk of malignancy in patients with celiac disease. Am J Med 115:191–195

    Article  PubMed  Google Scholar 

  37. Greiner TC, Medeiros LJ, Jaffe ES (1995) Non-Hodgkin’s lymphoma. Cancer 75:370–380

    CAS  PubMed  Google Scholar 

  38. Gridley G, McLaughlin JK, Ekbom A, Klareskog L, Adami HO, Hacker DG, Hoover R, Fraumeni JF Jr (1993) Incidence of cancer among patients with rheumatoid arthritis. J Natl Cancer Inst 85:307–311

    CAS  PubMed  Google Scholar 

  39. Groves FD, Linet MS, Travis LB, Devesa SS (2000) Cancer surveillance series: non-Hodgkin’s lymphoma incidence by histologic subtype in the United States from 1978 through 1995. J Natl Cancer Inst 92:1240–1251

    Article  CAS  PubMed  Google Scholar 

  40. Grulich AE, Wan X, Law MG, Milliken ST, Lewis CR, Garsia RJ, Gold J, Finlayson RJ, Cooper DA, Kaldor JM (2000) B-cell stimulation and prolonged immune deficiency are risk factors for non-Hodgkin’s lymphoma in people with AIDS. AIDS 14:133–140

    Google Scholar 

  41. Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, Delsol G, De Wolf-Peeters C, Falini B, Gatter KC (1994) A revised European–American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 84:1361–1392

    CAS  PubMed  Google Scholar 

  42. Harris NL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J, Lister TA, Bloomfield CD (1999) World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting—Airlie House, Virginia, November 1997. J Clin Oncol 17:3835–3849

    CAS  PubMed  Google Scholar 

  43. Hartge P, Devesa SS, Fraumeni JF Jr (1994) Hodgkin’s and non-Hodgkin’s lymphomas. Cancer Surv 19–20:423–453

    Google Scholar 

  44. Hartge P, Devesa SS, Grauman D, Fears TR, Fraumeni JF Jr (1996) Non-Hodgkin’s lymphoma and sunlight. J Natl Cancer Inst 88:298–300

    CAS  PubMed  Google Scholar 

  45. Hauptmann M, Lubin JH, Stewart PA, Hayes RB, Blair A (2003) Mortality from lymphohematopoietic malignancies among workers in formaldehyde industries. J Natl Cancer Inst 95:1615–1623

    Article  CAS  PubMed  Google Scholar 

  46. Hemminki K, Li X, Czene K (2004) Familial risk of cancer: data for clinical counseling and cancer genetics. Int J Cancer 108:109–114

    Google Scholar 

  47. Herrinton LJ, Friedman GD (1998) Cigarette smoking and risk of non-Hodgkin’s lymphoma subtypes. Cancer Epidemiol Biomarkers Prev 1:25–28

    Google Scholar 

  48. Herrinton LJ, Goldoft M, Schwartz SM, Weiss NS (1996) The incidence of non-Hodgkin’s lymphoma and its histologic subtypes in Asian migrants to the United States and their descendants. Cancer Causes Control 7:224–230

    CAS  PubMed  Google Scholar 

  49. Hoover RN (1992) Lymphoma risks in populations with altered immunity—a search for mechanism. Cancer Res 52:5477s–5478s

    CAS  PubMed  Google Scholar 

  50. Hu S, Ma F, Collado-Mesa F, Kirsner RS (2004) Ultraviolet radiation and incidence of non-Hodgkin’s lymphoma among Hispanics in the United States. Cancer Epidemiol Biomarkers Prev 13:59–64

    CAS  PubMed  Google Scholar 

  51. Intragumtornchai T, Wannakrairoj P, Chaimongkol B, Bhoopat L, Lekhakula A, Thamprasit T, Suwanwela N, Suthipinthawong C, Prayoonwiwat W, Meekungwal P, Sirijerachai C, Pairojkul C (1996) Non-Hodgkin’s lymphomas in Thailand. A retrospective pathologic and clinical analysis of 1391 cases. Cancer 78:1813–1819

    Article  CAS  PubMed  Google Scholar 

  52. Kadan-Lottick NS, Skluzacek MC, Gurney JG (2002) Decreasing incidence rates of primary central nervous system lymphoma. Cancer 95:193–202

    Article  PubMed  Google Scholar 

  53. Kato I, Koenig KL, Baptiste MS, Lillquist PP, Frizzera G, Burke JS, Watanabe H, Shore RE (2003) History of antibiotic use and risk of non-Hodgkin’s lymphoma (NHL). Int J Cancer 107:99–105

    Article  CAS  PubMed  Google Scholar 

  54. Kuppers R (2003) B cells under influence: transformation of B cells by Epstein-Barr virus. Nat Rev Immunol 3:801–812

    Article  PubMed  Google Scholar 

  55. Lecuit M, Abachin E, Martin A, Poyart C, Pochart P, Suarez F, Bengoufa D, Feuillard J, Lavergne A, Gordon JI, Berche P, Guillevin L, Lortholary O (2004) Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N Engl J Med 350:239–248

    Google Scholar 

  56. Levine AM, Shibata D, Sullivan-Halley J, Nathwani B, Brynes R, Slovak ML, Mahterian S, Riley CL, Weiss L, Levine PH et al (1992) Epidemiological and biological study of acquired immunodeficiency syndrome-related lymphoma in the county of Los Angeles: preliminary results. Cancer Res 52:5482s–5484s

    CAS  PubMed  Google Scholar 

  57. Linet MS, Pottern LM (1992) Familial aggregation of hematopoietic malignancies and risk of non-Hodgkin’s lymphoma. Cancer Res 52:5468s–5473s

    CAS  PubMed  Google Scholar 

  58. Little RF, Pittaluga S, Grant N, Steinberg SM, Kavlick MF, Mitsuya H, Franchini G, Gutierrez M, Raffeld M, Jaffe ES, Shearer G, Yarchoan R, Wilson WH (2003) Highly effective treatment of acquired immunodeficiency syndrome-related lymphoma with dose-adjusted EPOCH: impact of antiretroviral therapy suspension and tumor biology. Blood 101:4653–4659

    Article  CAS  PubMed  Google Scholar 

  59. Lymphoma Study Group of Japanese Pathologists (2000) The World Health Organization classification of malignant lymphomas in Japan: incidence of recently recognized entities. Pathol Int 50:696–702

    Google Scholar 

  60. Maartense E, Kluin-Nelemans HC, Noordijk EM (2003) Non-Hodgkin’s lymphoma in the elderly. A review with emphasis on elderly patients, geriatric assessment, and future perspectives. Ann Hematol 82:661–670

    Article  CAS  PubMed  Google Scholar 

  61. Mariette X (2001) Lymphomas complicating Sjogren’s syndrome and hepatitis C virus infection may share a common pathogenesis: chronic stimulation of rheumatoid factor B cells. Ann Rheum Dis 60:1007–1010

    Article  CAS  PubMed  Google Scholar 

  62. McKean-Cowdin R, Feigelson HS, Ross RK, Pike MC, Henderson BE (2000) Declining cancer rates in the 1990s. J Clin Oncol 18:2258–2268

    CAS  PubMed  Google Scholar 

  63. McKenna DB, Stockton D, Brewster DH, Doherty VR (2003) Evidence for an association between cutaneous malignant melanoma and lymphoid malignancy: a population-based retrospective cohort study in Scotland. Br J Cancer 88:74–78

    Article  CAS  PubMed  Google Scholar 

  64. Morton LM, Engels EA, Holford TR, Leaderer B, Zhang Y, Zahm SH, Boyle P, Zhang B, Flynn S, Tallini G, Owens PH, Zheng T (2004) Hepatitis C virus and risk of non-Hodgkin lymphoma: a population-based case-control study among Connecticut women. Cancer Epidemiol Biomarkers Prev 13:425–430

    PubMed  Google Scholar 

  65. Nakhleh RE, Manivel JC, Copenhaver CM, Sung JH, Strickler JG (1991) In situ hybridization for the detection of Epstein-Barr virus in central nervous system lymphomas. Cancer 67:444–448

    CAS  PubMed  Google Scholar 

  66. Nelson RA, Levine AM, Marks G, Bernstein L (1997) Alcohol, tobacco and recreational drug use and the risk of non-Hodgkin’s lymphoma. Br J Cancer 76:1532–1537

    CAS  PubMed  Google Scholar 

  67. Nelson RA, Levine AM, Bernstein L (2001) Reproductive factors and risk of intermediate- or high-grade B-cell non-Hodgkin’s lymphoma in women. J Clin Oncol 19:1381–1387

    CAS  PubMed  Google Scholar 

  68. Newton R, Roman E, Fear N, Carpenter L (1996) Non-Hodgkin’s lymphoma and solar ultraviolet radiation. Data are inconsistent. BMJ 313:298

    CAS  Google Scholar 

  69. Newton R, Ferlay J, Beral V, Devesa SS (1997) The epidemiology of non-Hodgkin’s lymphoma: comparison of nodal and extra-nodal sites. Int J Cancer 72:923–930

    Article  CAS  PubMed  Google Scholar 

  70. Olson JE, Janney CA, Rao RD, Cerhan JR, Kurtin PJ, Schiff D, Kaplan RS, O’Neill BP (2002) The continuing increase in the incidence of primary central nervous system non-Hodgkin lymphoma: a surveillance, epidemiology, and end results analysis. Cancer 95:1504–1510

    Article  PubMed  Google Scholar 

  71. Palackdharry CS (1994) The epidemiology of non-Hodgkin’s lymphoma: why the increased incidence? Oncology 8:67–73

    CAS  PubMed  Google Scholar 

  72. Parkin DM, Garcia-Giannoli H, Raphael M, Martin A, Katangole-Mbidde E, Wabinga H, Ziegler J (2000) Non-Hodgkin lymphoma in Uganda: a case-control study. AIDS 14:2929–2936

    Google Scholar 

  73. Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, Orentreich N, Vogelman JH, Friedman GD (1994) Helicobacter pylori infection and gastric lymphoma. N Engl J Med 330:1267–1271

    Article  CAS  PubMed  Google Scholar 

  74. Pearce N, Bethwaite P (1992) Increasing incidence of non-Hodgkin’s lymphoma: occupational and environmental factors. Cancer Res 52:5496s–5500s

    CAS  PubMed  Google Scholar 

  75. Persing DH, Prendergast FG (1999) Infection, immunity, and cancer. Arch Pathol Lab Med 123:1015–1022

    CAS  PubMed  Google Scholar 

  76. Rabkin CS, Tess BH, Christianson RE, Wright WE, Waters DJ, Alter HJ, Van Den Berg BJ (2002) Prospective study of hepatitis C viral infection as a risk factor for subsequent B-cell neoplasia. Blood 99:4240–4242

    Article  CAS  PubMed  Google Scholar 

  77. Ramos-Casals M, Trejo O, Garcia-Carrasco M, Cervera R, De La Red G, Gil V, Lopez-Guillermo A, Ingelmo M, Font J (2004) Triple association between hepatitis C virus infection, systemic autoimmune diseases, and B cell lymphoma. J Rheumatol 31:495–499

    Google Scholar 

  78. Rossi G, Donisi A, Casari S, Re A, Cadeo G, Carosi G (1999) The international prognostic index can be used as a guide to treatment decisions regarding patients with human immunodeficiency virus-related systemic non-Hodgkin lymphoma. Cancer 86:2391–2397

    Article  CAS  PubMed  Google Scholar 

  79. Sasieni P, Bataille V (1995) Non-Hodgkin’s lymphoma and skin cancer. Ultraviolet light is unlikely explanation for association. BMJ 311:749

    CAS  Google Scholar 

  80. Scherr PA, Hutchison GB, Neiman RS (1992) Non-Hodgkin’s lymphoma and occupational exposure. Cancer Res 52:5503s–5509s

    CAS  PubMed  Google Scholar 

  81. Schroeder JC, Olshan AF, Baric R, Dent GA, Weinberg CR, Yount B, Cerhan JR, Lynch CF, Schuman LM, Tolbert PE, Rothman N, Cantor KP, Blair A (2002) A case-control study of tobacco use and other non-occupational risk factors for t(14;18) subtypes of non-Hodgkin’s lymphoma (United States). Cancer Causes Control 2:159–168

    Google Scholar 

  82. Shih LY, Liang DC (1991) Non-Hodgkin’s lymphomas in Asia. Hematol Oncol Clin North Am 5:983–1001

    CAS  PubMed  Google Scholar 

  83. Sorensen HT, Mellemkjaer L, Nielsen GL, Baron JA, Olsen JH, Karagas MR (2004) Skin cancers and non-Hodgkin lymphoma among users of systemic glucocorticoids: a population-based cohort study. J Natl Cancer Inst 96:709–711

    Google Scholar 

  84. Sukpanichnant S, Sonakul D, Piankijagum A, Wanachiwanawin W, Veerakul G, Mahasandana C, Tanphaichitr VS, Suvatte V (1998) Malignant lymphoma in Thailand: changes in the frequency of malignant lymphoma determined from a histopathologic and immunophenotypic analysis of 425 cases at Siriraj Hospital. Cancer 83:1197–1204

    Article  CAS  PubMed  Google Scholar 

  85. Surveillance, Epidemiology, and End Results (SEER) Program (www.seer.cancer.gov) SEER*Stat Database: Incidence—SEER 9 Regs. Public-Use, Nov 2002 Sub (1973–2000). National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch, released April 2003

  86. Ward MH, Zahm SH, Weisenburger DD, Gridley G, Cantor KP, Saal RC, Blair A (1994) Dietary factors and non-Hodgkin’s lymphoma in Nebraska (United States). Cancer Causes Control 5:422–432

    CAS  PubMed  Google Scholar 

  87. Weisenburger DD (1994) Epidemiology of non-Hodgkin’s lymphoma: recent findings regarding an emerging epidemic. Ann Oncol 5:19–24

    Google Scholar 

  88. Westin EH, Longo DL (2004) Lymphoma and myeloma in older patients. Semin Oncol 31:198–205

    PubMed  Google Scholar 

  89. Willemze R (2003) Cutaneous T-cell lymphoma: epidemiology, etiology, and classification. Leuk Lymphoma 44:S49–S54

    Article  Google Scholar 

  90. Wingo PA, Cardinez CJ, Landis SH, Greenlee RT, Ries LA, Anderson RN, Thun MJ (2003) Long-term trends in cancer mortality in the United States, 1930–1998. Cancer 97:3133–3275

    Article  PubMed  Google Scholar 

  91. Wolfe F, Michaud K (2004) Lymphoma in rheumatoid arthritis: the effect of methotrexate and anti-tumor necrosis factor therapy in 18,572 patients. Arthritis Rheum 50:1740–1751

    Google Scholar 

  92. Wolk A, Gridley G, Svensson M, Nyren O, McLaughlin JK, Fraumeni JF, Adam HO (2001) A prospective study of obesity and cancer risk (Sweden). Cancer Causes Control 12:13–21

    Article  CAS  PubMed  Google Scholar 

  93. Wotherspoon AC (1998) Helicobacter pylori infection and gastric lymphoma. Br Med Bull 54:79–85

    CAS  PubMed  Google Scholar 

  94. Zahm SH, Blair A (1992) Pesticides and non-Hodgkin’s lymphoma. Cancer Res 52:5485s–5488s

    CAS  PubMed  Google Scholar 

  95. Zahm SH, Weisenburger DD, Babbitt PA, Saal RC, Vaught JB, Blair A (1992) Use of hair coloring products and the risk of lymphoma, multiple myeloma, and chronic lymphocytic leukemia. Am J Public Health 82:990–997

    CAS  PubMed  Google Scholar 

  96. Zahm SH, Weisenburger DD, Holmes FF, Cantor KP, Blair A (1997) Tobacco and non-Hodgkin’s lymphoma: combined analysis of three case-control studies (United States). Cancer Causes Control 2:159–166

    Google Scholar 

  97. Zhang SM, Hunter DJ, Rosner BA, Giovannucci EL, Colditz GA, Speizer FE, Willett WC (2000) Intakes of fruits, vegetables, and related nutrients and the risk of non-Hodgkin’s lymphoma among women. Cancer Epidemiol Biomarkers Prev 9:477–485

    CAS  PubMed  Google Scholar 

  98. Zhang Y, Holford TR, Leaderer B, Boyle P, Zahm SH, Flynn S, Tallini G, Owens PH, Zheng T (2004) Hair-coloring product use and risk of non-Hodgkin’s lymphoma: a population-based case-control study in Connecticut. Am J Epidemiol 159:148–154

    Google Scholar 

  99. Zhao X, Sun NC, Witt MD, Keller M, Niihara Y (2004) Changing pattern of AIDS: a bone marrow study. Am J Clin Pathol 121:393–401

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

With special thanks to Teresa Leigh for proofreading this paper. We also thank the internal reviewer in our institution, Prof. Dr. H. Veelken, as well as the anonymous external reviewer for critical reading of the manuscript and valuable suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monika Engelhardt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Müller, A.M.S., Ihorst, G., Mertelsmann, R. et al. Epidemiology of non-Hodgkin’s lymphoma (NHL): trends, geographic distribution, and etiology. Ann Hematol 84, 1–12 (2005). https://doi.org/10.1007/s00277-004-0939-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00277-004-0939-7

Keywords

Navigation