Korean J Hematol.  2012 Jun;47(2):92-104. 10.5045/kjh.2012.47.2.92.

Epidemiologic overview of malignant lymphoma

• Huh J

• KMID: 2083602
• DOI: http://doi.org/10.5045/kjh.2012.47.2.92

Abstract

Malignant lymphoma encompasses a wide variety of distinct disease entities. It is generally more common in developed countries and less common in developing countries. The East Asia region has one of the lowest incidence rates of malignant lymphoma. The incidence of malignant lymphoma around the world has been increasing at a rate of 3-4% over the last 4 decades, while some stabilization has been observed in developed countries in recent years. The reasons behind this lymphoma epidemic are poorly understood, although improving diagnostic accuracy, the recent AIDS epidemic, an aging world population and the increasing adoption of cancer-causing behaviors are suggested as contributing factors. Etiologies of malignant lymphoma include infectious agents, immunodeficiency, autoimmune disease, exposure to certain organic chemicals, and pharmaceuticals. The distribution of many subtypes exhibit marked geographic variations. Compared to the West, T/natural killer (NK) cell lymphomas (T/NK-cell lymphoma) and extranodal marginal zone lymphoma of mucosa-associated lymphoid tissue (MALT lymphoma) are relatively more common, whereas other B-cell lymphomas, particularly follicular lymphoma and chronic lymphocytic leukemia/small lymphocytic lymphoma, are less common in Asia. Some subtypes of T/NK-cell lymphomas defined by Epstein-Barr virus association are predominantly Asian diseases, if not exclusively so. Both ethnic and environmental factors play roles in such diversity. In this review, we discuss the geographic distribution and etiology of malignant lymphoma, as well as the trend.

Keyword

Malignant lymphoma; Epidemiology; Asia

MeSH Terms

Adoption
Aging
Asia
Asian Continental Ancestry Group
Autoimmune Diseases
Developed Countries
Developing Countries
Far East
Herpesvirus 4, Human
Humans
Incidence
Leukemia, Lymphocytic, Chronic, B-Cell
Lymphoma
Lymphoma, B-Cell
Lymphoma, B-Cell, Marginal Zone
Lymphoma, Follicular
Organic Chemicals
Organic Chemicals

Figure

• 

  Fig. 1 World map of the estimated age-standardized incidence rates (per 100,000 WHO world standard population) of non-Hodgkin lymphoma and Hodgkin lymphoma combined. Source: GLOBOCAN (http://globocan.iarc.fr/) from CANCERMondial (http://www-dep.iarc.fr/).

• 

  Fig. 2 Nominal gross domestic product (GDP) per capita world map 2008. Source: CIA World Factbook 2008. Abbreviation: PPP, purchasing power parity.

• 

  Fig. 3 Trends in estimated age-standardized (world) incidence rates of non-Hodgkin lymphoma. Source: CI5plus in CANCERMondial.

• 

  Fig. 4 Trends in estimated age-standardized (world) incidence rates of Hodgkin lymphoma. Source: CI5plus in CANCERMondial (http://www-dep.iarc.fr/).

• 

  Fig. 5 Age-specific incidence rates (ASR) of non-Hodgkin lymphoma and Hodgkin lymphoma in Korea in 2008. Source: Park et al. [8].

• 

  Fig. 6 Age distribution of malignant lymphoma at diagnosis for 1989-2008 at Asan Medical Center. Source: Yoon et al. [7]. Abbreviations: CLL/SLL, chronic lymphocytic leukemia/small lymphocytic lymphoma; MCL, mantle cell lymphoma; FL, follicular lymphoma; MALT, mucosa-associated lymphoid tissue; DLBCL, diffuse large B-cell lymphoma; NK, natural killer; PTCL, peripheral T-cell lymphoma, not otherwise specified; NHL, non-Hodgkin lymphoma.

Reference

1. Jaffe ES, Harris NL, Stein H, editors. Pathology and genetics of tumours of haematopoietic and lymphoid tissues. 2001. Lyon, France: IARC Press.

2. Harris NL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J. Lymphoma classification-From controversy to consensus: the R.E.A.L. and WHO classification of lymphoid neoplasms. Ann Oncol. 2000. 11:Suppl 1. 3–10.

3. Swerdlow SH. WHO classification of tumours of haematopoietic and lymphoid tissues. 2007. 4th ed. Lyon, France: IARC Press.

4. Roman E, Smith AG. Epidemiology of lymphomas. Histopathology. 2011. 58:4–14.

5. Morton LM, Turner JJ, Cerhan JR, et al. Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph). Blood. 2007. 110:695–708.

6. Turner JJ, Morton LM, Linet MS, et al. InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): update and future directions. Blood. 2010. 116:e90–e98.

7. Yoon SO, Suh C, Lee DH, et al. Distribution of lymphoid neoplasms in the Republic of Korea: analysis of 5318 cases according to the World Health Organization classification. Am J Hematol. 2010. 85:760–764.

8. Park HJ, Park EH, Jung KW, et al. Statistics of hematologic malignancies in Korea: incidence, prevalence and survival rates from 1999 to 2008. Korean J Hematol. 2012. 47:28–38.

9. CANCERmondial. 2008. Accessed April 5, 2012. Lyon, France: International Agency for Research on Cancer;http://www.dep.iarc.fr/.

10. Parkin DM. International Association of Cancer Registries. Cancer incidence in five continents. 2005. Vols. I-VIII. Lyon, France: IARC Press.

11. Curado MP. International Association of Cancer Registries. Cancer incidence in five continents. 2007. Vol. IX. Lyon, France: IARC Press.

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

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

14. Blinder V, Fisher SG. The role of environmental factors in the etiology of lymphoma. Cancer Invest. 2008. 26:306–316.

15. Müller AM, Ihorst G, Mertelsmann R, Engelhardt M. Epidemiology of non-Hodgkin's lymphoma (NHL): trends, geographic distribution, and etiology. Ann Hematol. 2005. 84:1–12.

16. Baris D, Zahm SH. Epidemiology of lymphomas. Curr Opin Oncol. 2000. 12:383–394.

17. Glaser SL, Swartz WG. Time trends in Hodgkin's disease incidence. The role of diagnostic accuracy. Cancer. 1990. 66:2196–2204.

18. Glaser SL. Reproductive factors in Hodgkin's disease in women: a review. Am J Epidemiol. 1994. 139:237–246.

19. Correa P, O'Conor GT. Epidemiologic patterns of Hodgkin's disease. Int J Cancer. 1971. 8:192–201.

20. MacMahon B. Epidemiology of Hodgkin's disease. Cancer Res. 1966. 26:1189–1201.

21. Glaser SL, Jarrett RF. The epidemiology of Hodgkin's disease. Baillieres Clin Haematol. 1996. 9:401–416.

22. Mani H, Jaffe ES. Hodgkin lymphoma: an update on its biology with new insights into classification. Clin Lymphoma Myeloma. 2009. 9:206–216.

23. Jarrett RF. Viruses and Hodgkin's lymphoma. Ann Oncol. 2002. 13:Suppl 1. 23–29.

24. Ko YH, Kim CW, Park CS, et al. 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. 1998. 83:806–812.

25. Vose J, Armitage J, Weisenburger D. International peripheral T-cell and natural killer/T-cell lymphoma study: pathology findings and clinical outcomes. J Clin Oncol. 2008. 26:4124–4130.

26. Kim JM, Ko YH, Lee SS, et al. WHO Classification of malignant lymphomas in Korea: Report of the Third Nationwide Study. Korean J Pathol. 2011. 45:254–260.

27. Parkin DM. International variation. Oncogene. 2004. 23:6329–6340.

28. Clarke CA, Glaser SL, Gomez SL, et al. Lymphoid malignancies in U.S. Asians: incidence rate differences by birthplace and acculturation. Cancer Epidemiol Biomarkers Prev. 2011. 20:1064–1077.

29. Carreon JD, Morton LM, Devesa SS, et al. Incidence of lymphoid neoplasms by subtype among six Asian ethnic groups in the United States, 1996-2004. Cancer Causes Control. 2008. 19:1171–1181.

30. Hjalgrim H, Engels EA. Infectious aetiology of Hodgkin and non-Hodgkin lymphomas: a review of the epidemiological evidence. J Intern Med. 2008. 264:537–548.

31. WHO International Agency for Research on Cancer. IARC Monographs on the evaluation of carcinogenic risks to humans. 2012. Vol. 100. Lyon, France: IARC Press.

32. Magrath I. Epidemiology: clues to the pathogenesis of Burkitt lymphoma. Br J Haematol. 2012. 156:744–756.

33. Alexander FE, Lawrence DJ, Freeland J, et al. An epidemiologic study of index and family infectious mononucleosis and adult Hodgkin's disease (HD): evidence for a specific association with EBV+ve HD in young adults. Int J Cancer. 2003. 107:298–302.

34. Huh J, Park C, Juhng S, Kim CE, Poppema S, Kim C. A pathologic study of Hodgkin's disease in Korea and its association with Epstein-Barr virus infection. Cancer. 1996. 77:949–955.

35. Koh YW, Yoon DH, Suh C, Huh J. Impact of the Epstein-Barr virus positivity on Hodgkin's lymphoma in a large cohort from a single institute in Korea. Ann Hematol. 2012. [Epub ahead of print].

36. Yoon SO, Yu E, Cho YM, et al. Post-transplant lymphoproliferative disorders: clinicopathological analysis of 43 cases in a single center, 1990-2009. Clin Transplant. 2012. 26:67–73.

37. Asano N, Yamamoto K, Tamaru J, et al. Age-related Epstein-Barr virus (EBV)-associated B-cell lymphoproliferative disorders: comparison with EBV-positive classic Hodgkin lymphoma in elderly patients. Blood. 2009. 113:2629–2636.

38. Hofscheier A, Ponciano A, Bonzheim I, et al. Geographic variation in the prevalence of Epstein-Barr virus-positive diffuse large B-cell lymphoma of the elderly: a comparative analysis of a Mexican and a German population. Mod Pathol. 2011. 24:1046–1054.

39. Park S, Lee J, Ko YH, et al. The impact of Epstein-Barr virus status on clinical outcome in diffuse large B-cell lymphoma. Blood. 2007. 110:972–978.

40. Au WY, Weisenburger DD, Intragumtornchai T, et al. Clinical differences between nasal and extranasal natural killer/T-cell lymphoma: a study of 136 cases from the International Peripheral T-Cell Lymphoma Project. Blood. 2009. 113:3931–3937.

41. Ko YH, Cho EY, Kim JE, et al. NK and NK-like T-cell lymphoma in extranasal sites: a comparative clinicopathological study according to site and EBV status. Histopathology. 2004. 44:480–489.

42. Jo JC, Yoon DH, Kim S, et al. Clinical features and prognostic model for extranasal NK/T-cell lymphoma. Eur J Haematol. 2012. [Epub ahead of print].

43. Aozasa K, Takakuwa T, Hongyo T, Yang WI. Nasal NK/T-cell lymphoma: epidemiology and pathogenesis. Int J Hematol. 2008. 87:110–117.

44. Kojya S, Matsumura J, Ting L, et al. Familial nasal NK/T-cell lymphoma and pesticide use. Am J Hematol. 2001. 66:145–147.

45. Xu JX, Hoshida Y, Yang WI, et al. Life-style and environmental factors in the development of nasal NK/T-cell lymphoma: a case-control study in East Asia. Int J Cancer. 2007. 120:406–410.

46. Kimura H, Ito Y, Kawabe S, et al. EBV-associated T/NK-cell lymphoproliferative diseases in nonimmunocompromised hosts: prospective analysis of 108 cases. Blood. 2012. 119:673–686.

47. Cohen JI, Kimura H, Nakamura S, Ko YH, Jaffe ES. Epstein-Barr virus-associated lymphoproliferative disease in non-immuno-compromised hosts: a status report and summary of an international meeting, 8-9 September 2008. Ann Oncol. 2009. 20:1472–1482.

48. Suzuki K, Ohshima K, Karube K, et al. Clinicopathological states of Epstein-Barr virus-associated T/NK-cell lymphoproliferative disorders (severe chronic active EBV infection) of children and young adults. Int J Oncol. 2004. 24:1165–1174.

49. Cho KH, Kim CW, Heo DS, et al. Epstein-Barr virus-associated peripheral T-cell lymphoma in adults with hydroa vacciniforme-like lesions. Clin Exp Dermatol. 2001. 26:242–247.

50. Ishihara S, Yabuta R, Tokura Y, Ohshima K, Tagawa S. Hypersensitivity to mosquito bites is not an allergic disease, but an Epstein-Barr virus-associated lymphoproliferative disease. Int J Hematol. 2000. 72:223–228.

51. Kimura H, Hoshino Y, Kanegane H, et al. Clinical and virologic characteristics of chronic active Epstein-Barr virus infection. Blood. 2001. 98:280–286.

52. Tedeschi R, Luostarinen T, De Paoli P, et al. Joint Nordic prospective study on human herpesvirus 8 and multiple myeloma risk. Br J Cancer. 2005. 93:834–837.

53. Arisawa K, Soda M, Endo S, et al. Evaluation of adult T-cell leukemia/lymphoma incidence and its impact on non-Hodgkin lymphoma incidence in southwestern Japan. Int J Cancer. 2000. 85:319–324.

54. Kwon SY, Lim AH, Park JY, Han SH, Cho NS. Seroprevalence of human T-lymphotropic virus type 1 and 2 in Korean blood donors. J Med Virol. 2008. 80:1864–1867.

55. Kim JM, Chang KH, Choi YH, et al. Seroprevalence of HTLV-I in Cheju Island, a Korean island adjacent to the endemic area of Japan. J Acquir Immune Defic Syndr. 1999. 22:409–412.

56. Weng WK, Levy S. Hepatitis C virus (HCV) and lymphomagenesis. Leuk Lymphoma. 2003. 44:1113–1120.

57. Hermine O, Lefrère F, Bronowicki JP, et al. Regression of splenic lymphoma with villous lymphocytes after treatment of hepatitis C virus infection. N Engl J Med. 2002. 347:89–94.

58. Kang J, Cho JH, Suh CW, et al. High prevalence of hepatitis B and hepatitis C virus infections in Korean patients with hematopoietic malignancies. Ann Hematol. 2011. 90:159–164.

59. Park BB, Kim JS, Lee YY, et al. Clinical characteristics and outcome for hepatitis C virus-positive diffuse large B-cell lymphoma. Leuk Lymphoma. 2008. 49:88–94.

60. Marcucci F, Spada E, Mele A, Caserta CA, Pulsoni A. The association of hepatitis B virus infection with B-cell non-Hodgkin lymphoma - a review. Am J Blood Res. 2012. 2:18–28.

61. Engels EA, Cho ER, Jee SH. Hepatitis B virus infection and risk of non-Hodgkin lymphoma in South Korea: a cohort study. Lancet Oncol. 2010. 11:827–834.

62. Wang F, Xu RH, Luo HY, et al. Clinical and prognostic analysis of hepatitis B virus infection in diffuse large B-cell lymphoma. BMC Cancer. 2008. 8:115.

63. Kim YM, Jeong SH, Kim JW, et al. Chronic hepatitis B, non-Hodgkin's lymphoma, and effect of prophylactic antiviral therapy. J Clin Virol. 2011. 51:241–245.

64. Isaacson PG. Update on MALT lymphomas. Best Pract Res Clin Haematol. 2005. 18:57–68.

65. Sagaert X, Van Cutsem E, De Hertogh G, Geboes K, Tousseyn T. Gastric MALT lymphoma: a model of chronic inflammation-induced tumor development. Nat Rev Gastroenterol Hepatol. 2010. 7:336–346.

66. Youn HS, Baik SC, Cho YK, et al. Comparison of Helicobacter pylori infection between Fukuoka, Japan and Chinju, Korea. Helicobacter. 1998. 3:9–14.

67. Luminari S, Cesaretti M, Marcheselli L, et al. Decreasing incidence of gastric MALT lymphomas in the era of anti-Helicobacter pylori interventions: results from a population-based study on extranodal marginal zone lymphomas. Ann Oncol. 2010. 21:855–859.

68. Bertoni F, Coiffier B, Salles G, et al. MALT lymphomas: pathogenesis can drive treatment. Oncology (Williston Park). 2011. 25:1134–1142. 1147

69. Dias C, Isenberg DA. Susceptibility of patients with rheumatic diseases to B-cell non-Hodgkin lymphoma. Nat Rev Rheumatol. 2011. 7:360–368.

70. Oh SY, Kim WS, Kim JS, et al. Primary thyroid marginal zone B-cell lymphoma of the mucosa-associated lymphoid tissue type: clinical manifestation and outcome of a rare disease - consortium for improving survival of lymphoma study. Acta Haematol. 2012. 127:100–104.

71. Willett EV, Morton LM, Hartge P, et al. Non-Hodgkin lymphoma and obesity: a pooled analysis from the InterLymph Consortium. Int J Cancer. 2008. 122:2062–2070.

72. Larsson SC, Wolk A. Body mass index and risk of non-Hodgkin's and Hodgkin's lymphoma: a meta-analysis of prospective studies. Eur J Cancer. 2011. 47:2422–2430.

73. Keegan TH, Glaser SL, Clarke CA, et al. Body size, physical activity, and risk of Hodgkin's lymphoma in women. Cancer Epidemiol Biomarkers Prev. 2006. 15:1095–1101.

74. Maskarinec G, Erber E, Gill J, Cozen W, Kolonel LN. Overweight and obesity at different times in life as risk factors for non-Hodgkin's lymphoma: the multiethnic cohort. Cancer Epidemiol Biomarkers Prev. 2008. 17:196–203.

75. Lim U, Morton LM, Subar AF, et al. Alcohol, smoking, and body size in relation to incident Hodgkin's and non-Hodgkin's lymphoma risk. Am J Epidemiol. 2007. 166:697–708.

76. Pylypchuk RD, Schouten LJ, Goldbohm RA, Schouten HC, van den Brandt PA. Body mass index, height, and risk of lymphatic malignancies: a prospective cohort study. Am J Epidemiol. 2009. 170:297–307.

77. Hursting SD, Nunez NP, Varticovski L, Vinson C. The obesity-cancer link: lessons learned from a fatless mouse. Cancer Res. 2007. 67:2391–2393.

78. Castillo JJ, Mull N, Reagan JL, Nemr S, Mitri J. Increased incidence of non-Hodgkin lymphoma, leukemia, and myeloma in patients with diabetes mellitus type 2: a meta-analysis of observational studies. Blood. 2012. 119:4845–4850.

79. Khan AE, Gallo V, Linseisen J, et al. Diabetes and the risk of non-Hodgkin's lymphoma and multiple myeloma in the European Prospective Investigation into Cancer and Nutrition. Haematologica. 2008. 93:842–850.

80. Morton LM, Hartge P, Holford TR, et al. Cigarette smoking and risk of non-Hodgkin lymphoma: a pooled analysis from the International Lymphoma Epidemiology Consortium (interlymph). Cancer Epidemiol Biomarkers Prev. 2005. 14:925–933.

81. Castillo JJ, Dalia S, Shum H. Meta-analysis of the association between cigarette smoking and incidence of Hodgkin's Lymphoma. J Clin Oncol. 2011. 29:3900–3906.

82. Troy JD, Hartge P, Weissfeld JL, et al. Associations between anthropometry, cigarette smoking, alcohol consumption, and non-Hodgkin lymphoma in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial. Am J Epidemiol. 2010. 171:1270–1281.

83. Kanda J, Matsuo K, Kawase T, et al. Association of alcohol intake and smoking with malignant lymphoma risk in Japanese: a hospital-based case-control study at Aichi Cancer Center. Cancer Epidemiol Biomarkers Prev. 2009. 18:2436–2441.

84. Negri E. Sun exposure, vitamin D, and risk of Hodgkin and non-Hodgkin lymphoma. Nutr Cancer. 2010. 62:878–882.

85. Kricker A, Armstrong BK, Hughes AM, et al. Personal sun exposure and risk of non Hodgkin lymphoma: a pooled analysis from the Interlymph Consortium. Int J Cancer. 2008. 122:144–154.