Skip to main content
Top

07-02-2016 | Hematologic cancers | Book chapter | Article

Epidemiology and Etiology of Non-Hodgkin Lymphoma

Authors: Brian C.-H. Chiu, Ningqi Hou

Publisher: Springer International Publishing

Abstract

Non-Hodgkin lymphoma (NHL) consists of many histologically and biologically distinct lymphoid malignancies with poorly understood, but possibly distinct, etiologies. The patterns of incidence and time trend vary not only by age, sex, and race/ethnicity in the USA, but also show significant geographic differences, suggesting the potential role of infectious agents, environmental factors, and lifestyle factors in addition to host genetic status in the development of NHL. Important pathogenetic mechanisms include immune modulation and chronic antigen stimulation. Epidemiologic studies in the past two decades have provided intriguing new insights on the possible causes of lymphoma and support the idea that there is some mechanistic commonality of lymphomagenesis, but significant etiologic heterogeneity clearly exists. This review presents a summary of the current understanding of the descriptive epidemiology and etiology of NHL and suggests areas of focus for future epidemiologic research.
Literature
1.
American Cancer Society (2014) Cancer facts and figures 2014. Atlanta, GA
2.
Howlader N, Noone AM, Krapcho M, Garshell J, Miller D, Altekruse SF et al (2014). SEER cancer statistics review, 1975–2011. National Cancer Institute. Bethesda, MD. http://​seer.​cancer.​gov/​csr/​1975_​2011/​, based on November 2013 SEER data submission, posted to the SEER web site, April 2014
3.
Swerdlow SH, Campo E (2008) WHO classification: pathology and genetics of tumors of haematopoietic and lymphoid tissues. IARC Press, Lyon
4.
Shankland KR, Armitage JO, Hancock BW (2012) Non-Hodgkin lymphoma. Lancet 380(9844):848–857PubMed
5.
Evens AM, Winter JN, Gordon LI, Chiu BC-H, Tsang R, Rosen ST (2013). Non-Hodgkin lymphoma. In: Pazdur R, Wagman LD, Camphausen KA, Hoskins WJ (eds) Cancer management: a multidisciplinary approach. UBM Medica, Norwalk, CT
6.
Hartge P, Wang SS, Bracci PM, Devesa SS, Holly EA (2006) Non-Hodgkin lymphoma. In: Schottenfeld D, Fraumeni JFJ (eds) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, New York, pp 898–918
7.
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(15):1240–1251PubMed
8.
Chiu BC, Weisenburger DD (2003) An update of the epidemiology of non-Hodgkin’s lymphoma. Clin Lymphoma 4(3):161–168PubMed
9.
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):265–276PubMedCentralPubMed
10.
Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C et al GLOBOCAN 2010 v1.0, Cancer incidence and mortality worldwide: IARC CancerBase No.10. 2012. Available from http://​globocan.​iarc.​fr
11.
Biagi JJ, Seymour JF (2002) Insights into the molecular pathogenesis of follicular lymphoma arising from analysis of geographic variation. Blood 99(12):4265–4275PubMed
12.
Lee MY, Tan TD, Feng AC, Liu MC (2006) Clinicopathological analysis of 598 malignant lymphomas in Taiwan: seven-year experience in a single institution. Am J Hematol 81(8):568–575PubMed
13.
Yang QP, Zhang WY, Yu JB, Zhao S, Xu H, Wang WY et al (2011) Subtype distribution of lymphomas in Southwest China: analysis of 6,382 cases using WHO classification in a single institution. Diagn Pathol 6:77PubMedCentralPubMed
14.
Yoon SO, Suh C, Lee DH, Chi HS, Park CJ, Jang SS et al (2010) Distribution of lymphoid neoplasms in the Republic of Korea: analysis of 5,318 cases according to the World Health Organization classification. Am J Hematol 85(10):760–764PubMed
15.
Laurini JA, Perry AM, Boilesen E, Diebold J, Maclennan KA, Muller-Hermelink HK et al (2012) Classification of non-Hodgkin lymphoma in Central and South America: a review of 1,028 cases. Blood 120(24):4795–4801PubMed
16.
Clarke CA, Glaser SL, Gomez SL, Wang SS, Keegan TH, Yang J et al (2011) Lymphoid malignancies in U.S. Asians: incidence rate differences by birthplace and acculturation. Cancer Epidemiol Biomark Prev 20(6):1064–1077
17.
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(2):224–230PubMed
18.
Ekstrom-Smedby K (2006) Epidemiology and etiology of non-Hodgkin lymphoma–a review. Acta Oncol 45(3):258–271PubMed
19.
Shiels MS, Engels EA, Linet MS, Clarke CA, Li J, Hall HI et al (2013) The epidemic of non-Hodgkin lymphoma in the United States: disentangling the effect of HIV, 1992–2009. Cancer Epidemiol Biomark Prev 22(6):1069–1078
20.
Aschebrook-Kilfoy B, Caces DB, Ollberding NJ, Smith SM, Chiu BC (2013) An upward trend in the age-specific incidence patterns for mantle cell lymphoma in the USA. Leuk Lymphoma 54(8):1677–1683PubMed
21.
Liu L, Wang H, Chen Y, Rustveld L, Liu G, Du XL (2013) Splenic marginal zone lymphoma: a population-based study on the 2001–2008 incidence and survival in the United States. Leuk lymphoma 54(7):1380–1386PubMed
22.
Zhou Y, Wang H, Fang W, Romaguer JE, Zhang Y, Delasalle KB et al (2008) Incidence trends of mantle cell lymphoma in the United States between 1992 and 2004. Cancer 113(4):791–798PubMed
23.
Devesa SS, Fears T (1992) Non-Hodgkin’s lymphoma time trends: United States and international data. Cancer Res 52(19 Supplement):5432s–5440s
24.
Olson JE, Janney CA, Rao RD, Cerhan JR, Kurtin PJ, Schiff D et al (2002) The continuing increase in the incidence of primary central nervous system non-Hodgkin lymphoma: a surveillance, epidemiology, and end results analysis. Cancer 95(7):1504–1510PubMed
25.
Kadan-Lottick NS, Skluzacek MC, Gurney JG (2002) Decreasing incidence rates of primary central nervous system lymphoma. Cancer 95(1):193–202PubMed
26.
O’’eill BP, Decker PA, Tieu C, Cerhan JR (2013) The changing incidence of primary central nervous system lymphoma is driven primarily by the changing incidence in young and middle-aged men and differs from time trends in systemic diffuse large B-cell non-Hodgkin’s lymphoma. Am J Hematol 88(12):997–1000
27.
Bassig BA, Lan Q, Rothman N, Zhang Y, Zheng T (2012) Current understanding of lifestyle and environmental factors and risk of non-hodgkin lymphoma: an epidemiological update. J Cancer Epidemiol 2012:978930PubMedCentralPubMed
28.
Boffetta P, Armstrong B, Linet M, Kasten C, Cozen W, Hartge P (2007) Consortia in cancer epidemiology: lessons from InterLymph. Cancer Epidemiol Biomark Prev 16(2):197–199
29.
Morton LM, Wang SS, Cozen W, Linet MS, Chatterjee N, Davis S et al (2008) Etiologic heterogeneity among non-Hodgkin lymphoma subtypes. Blood 112(13):5150–5160PubMedCentralPubMed
30.
Morton LM, Sampson JN, Cerhan JR, Turner JJ, Vajdic CM, Wang SS et al (2014) Rationale and design of the International Lymphoma Epidemiology Consortium (InterLymph) non-Hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):1–14PubMed
31.
Rabkin CS, Ward MH, Manns A, Blattner WA (1997) Epidemiology of non-Hodgkin’s lymphomas. In: Magrath IT (ed) The non-Hodgkin’s lymphomas, 2nd edn. Oxford University Press, New York, pp 171–186
32.
Filipovich AH, Mathur A, Kamat D, Shapiro RS (1992) Primary immunodeficiencies: genetic risk factors for lymphoma. Cancer Res 52(19S):5465–5467
33.
Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM (2007) Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet 370(9581):59–67PubMed
34.
Engels EA, Pfeiffer RM, Goedert JJ, Virgo P, McNeel, Timothy S, Scoppa SM et al (2006) Trends in cancer risk among people with AIDS in the United States 1980–2002. AIDS (London, England) 20(12):1645–1654
35.
Shiels MS, Cole SR, Wegner S, Armenian H, Chmiel JS, Ganesan A et al (2008) Effect of HAART on incident cancer and noncancer AIDS events among male HIV seroconverters. J Acquir Immune Defic Syndr 48(4):485–490PubMedCentralPubMed
36.
Palackdharry CS (1994) The epidemiology of non-Hodgkin’s lymphoma: why the increased incidence? Oncology 8(8):67–78PubMed
37.
Clarke CA, Morton LM, Lynch C, Pfeiffer RM, Hall EC, Gibson TM et al (2013) Risk of lymphoma subtypes after solid organ transplantation in the United States. Br J Cancer 109(1):280–288PubMedCentralPubMed
38.
Gibson TM, Engels EA, Clarke CA, Lynch CF, Weisenburger DD, Morton LM (2014) Risk of diffuse large B-cell lymphoma after solid organ transplantation in the United States. Am J Hematol 89(7):714–720PubMed
39.
Quinlan SC, Morton LM, Pfeiffer RM, Anderson LA, Landgren O, Warren JL et al (2010) Increased risk for lymphoid and myeloid neoplasms in elderly solid-organ transplant recipients. Cancer Epidemiol Biomark Prev 19(5):1229–1237
40.
Jiang Y, Villeneuve PJ, Fenton SS, Schaubel DE, Lilly L, Mao Y (2008) Liver transplantation and subsequent risk of cancer: findings from a Canadian cohort study. Liver Transpl 14(11):1588–1597PubMed
41.
Jiang Y, Villeneuve PJ, Wielgosz A, Schaubel DE, Fenton SS, Mao Y (2010) The incidence of cancer in a population-based cohort of Canadian heart transplant recipients. Am J Transplant 10(3):637–645PubMed
42.
Kim CJ, Freedman DM, Curtis RE, Berrington de Gonzalez A, Morton LM (2013) Risk of non-Hodgkin lymphoma after radiotherapy for solid cancers. Leuk Lymphoma 54(8): 1691–1697
43.
Krishnan B, Morgan GJ (2007) Non-Hodgkin lymphoma secondary to cancer chemotherapy. Cancer Epidemiol Biomark Prev 16(3):377–380
44.
Castillo JJ, Dalia S, Pascual SK (2010) Association between red blood cell transfusions and development of non-Hodgkin lymphoma: a meta-analysis of observational studies. Blood 116(16):2897–2907PubMed
45.
Chow EJ, Holly EA (2002) Blood transfusions as a risk factor for non-Hodgkin’s lymphoma in the San Francisco Bay Area: a population-based study. Am J Epidemiol 155(8):725–731PubMed
46.
Maguire-Boston EK, Suman V, Jacobsen SJ, Moore SB, Habermann TM, Cerhan JR et al (1999) Blood transfusion and risk of non-Hodgkin’s lymphoma. Am J Epidemiol 149(12):1113–1118PubMed
47.
Cerhan JR, Kricker A, Paltiel O, Flowers CR, Wang SS, Monnereau A et al (2014) Medical history, lifestyle, family history, and occupational risk factors for diffuse large B-cell lymphoma: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):15–25PubMed
48.
Linet MS, Vajdic CM, Morton LM, de Roos AJ, Skibola CF, Boffetta P et al (2014) Medical history, lifestyle, family history, and occupational risk factors for follicular lymphoma: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):26–40PubMed
49.
Slager SL, Benavente Y, Blair A, Vermeulen R, Cerhan JR, Costantini AS et al (2014) medical history, lifestyle, family history, and occupational risk factors for chronic lymphocytic leukemia/small lymphocytic lymphoma: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):41–51PubMed
50.
Cerhan JR, Wallace RB, Folsom AR, Potter JD, Munger RG, Prineas RJ (1993) Transfusion history and cancer risk in older women. Ann Intern Med 119:8–15PubMed
51.
Smedby KE, Askling J, Mariette X, Baecklund E (2008) Autoimmune and inflammatory disorders and risk of malignant lymphomas–an update. J Intern Med 264(6):514–527PubMed
52.
Bracci PM, Benavente Y, Turner JJ, Paltiel O, Slager SL, Vajdic CM et al (2014) Medical history, lifestyle, family history, and occupational risk factors for marginal zone lymphoma: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):52–65PubMed
53.
Ekstrom Smedby K, Vajdic CM, Falster M, Engels EA, Martinez-Maza O, Turner J et al (2008) Autoimmune disorders and risk of non-Hodgkin lymphoma subtypes: a pooled analysis within the InterLymph consortium. Blood. 111(8):4029–3408
54.
Vajdic CM, Landgren O, McMaster ML, Slager SL, Brooks-Wilson A, Smith A et al (2014) Medical history, lifestyle, family history, and occupational risk factors for lymphoplasmacytic lymphoma/waldenstrom’s macroglobulinemia: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):87–97PubMed
55.
Oertel SH, Riess H (2002) Immunosurveillance, immunodeficiency and lymphoproliferations. Recent Results Cancer Res 159:1–8PubMed
56.
Cleghorn FR, Manns A, Falk R, Hartge P, Hanchard B, Jack N et al (1995) Effect of human T-lymphotropic virus type I infection on non-Hodgkin’s lymphoma incidence. J Natl Cancer Inst 87(13):1009–1014PubMed
57.
Kondo T, Kono H, Miyamoto N, Yoshida R, Toki H, Matsumoto I et al (1989) Age- and sex-specific cumulative rate and risk of ATLL for HTLV-I carriers. Int J Cancer 43(6):1061–1064PubMed
58.
Giam CZ, Jeang KT (2007) HTLV-1 tax and adult T-cell leukemia. Front Biosci 12:1496–1507PubMed
59.
Knowles DM, Cesarman E (1997) The Kaposi’s sarcoma-associated herpesvirus (human herpesvirus-8) in Kaposi’s sarcoma, malignant lymphoma, and other diseases. Ann Oncol 8(Suppl 2):123–129PubMed
60.
Engels EA, Chatterjee N, Cerhan JR, Davis S, Cozen W, Severson RK et al (2004) Hepatitis C virus infection and non-hodgkin lymphoma: results of the NCI-seer multi-center case-control study. Int J Cancer 111(1):76–80PubMed
61.
Hausfater P, Rosenthal E, Cacoub P (2000) Lymphoproliferative diseases and hepatitis C virus infection. Ann Med Interne 151(1):53–57
62.
Ohsawa M, Shingu N, Miwa H, Yoshihara H, Kubo M, Tsukuma H et al (1999) Risk of non-Hodgkin’s lymphoma in patients with hepatitis C virus infection. Int J Cancer 80(2):237–239PubMed
63.
Pioltelli P, Gargantini L, Cassi E, Santoleri L, Bellati G, Magliano EM et al (2000) Hepatitis C virus in non-Hodgkin’s lymphoma. A reappraisal after a prospective case-control study of 300 patients. Lombart study group of HCV-lymphoma. Am J Hematol 64(2):95–100PubMed
64.
Montella M, Crispo A, de Bellis G, Izzo F, Frigeri F, Ronga D et al (2001) HCV and cancer: a case-control study in a high-endemic area. Liver 21(5):335–341PubMed
65.
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 Biomark Prev 15(11):2078–2085
66.
de Sanjose S, Benavente Y, Vajdic CM, Engels EA, Morton LM, Bracci PM et al (2008) Hepatitis C and non-Hodgkin lymphoma among 4,784 cases and 6,269 controls from the International Lymphoma Epidemiology Consortium. Clin Gastroenterol Hepatol 6(4):451–458PubMedCentralPubMed
67.
Nieters A, Kallinowski B, Brennan P, Ott M, Maynadie M, Benavente Y et al (2006) Hepatitis C and risk of lymphoma: results of the European multicenter case-control study EPILYMPH. Gastroenterology 131(6):1879–1886PubMed
68.
Wotherspoon AC (1998) Gastric lymphoma of mucosa-associated lymphoid tissue and Helicobacter pylori. Annu Rev Med 49:289–299PubMed
69.
Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E et al (1994) Helicobacter pylori infection and gastric lymphoma. N Engl J Med 330(18):1267–1271PubMed
70.
Wotherspoon AC, Doglioni C, Diss TC, Pan L, Moschini A, de Boni M et al (1993) Regression of primary low-grade B-cell gastric lymphoma of mucosa-associated lymphoid tissue type after eradication of Helicobacter pylori. Lancet 342(8871):575–577PubMed
71.
Goodlad JR, Davidson MM, Hollowood K, Ling C, MacKenzie C, Christie I et al (2000) Primary cutaneous B-cell lymphoma and Borrelia burgdorferi infection in patients from the Highlands of Scotland. Am J Surg Pathol 24(9):1279–1285PubMed
72.
Roggero E, Zucca E, Mainetti C, Bertoni F, Valsangiacomo C, Pedrinis E et al (2000) Eradication of Borrelia burgdorferi infection in primary marginal zone B-cell lymphoma of the skin. Hum Pathol 31(2):263–268PubMed
73.
Guidoboni M, Ferreri AJ, Ponzoni M, Doglioni C, Dolcetti R (2006) Infectious agents in mucosa-associated lymphoid tissue-type lymphomas: pathogenic role and therapeutic perspectives. Clin Lymphoma Myeloma 6(4):289–300PubMed
74.
Anderson LA, Atman AA, McShane CM, Titmarsh GJ, Engels EA, Koshiol J (2014) Common infection-related conditions and risk of lymphoid malignancies in older individuals. Br J Cancer 110(11):2796–2803
75.
Tavani A, La Vecchia C, Franceschi S, Serraino D, Carbone A (2000) Medical history and risk of Hodgkin’s and non-Hodgkin’s lymphomas. Eur J Cancer Prev 9(1):59–64PubMed
76.
Liu YC, Yang YH, Hsiao HH, Yang WC, Liu TC, Chang CS et al (2012) Herpes zoster is associated with an increased risk of subsequent lymphoid malignancies—a nationwide population-based matched-control study in Taiwan. BMC Cancer 12:503PubMedCentralPubMed
77.
Adami J, Nyren O, Bergstrom R, Ekbom A, Engholm G, Englund A et al (1998) Smoking and the risk of leukemia, lymphoma, and multiple myeloma (Sweden). Cancer Causes Control 9(1):49–56PubMed
78.
Willett EV, Smith AG, Dovey GJ, Morgan GJ, Parker J, Roman E (2004) Tobacco and alcohol consumption and the risk of non-Hodgkin lymphoma. Cancer Causes Control 15(8):771–780PubMed
79.
Besson H, Brennan P, Becker N, Nieters A, De Sanjose S, Font R et al (2006) Tobacco smoking, alcohol drinking and non-Hodgkin’s lymphoma: a European multicenter case-control study (Epilymph). Int J Cancer 119(4):901–908PubMed
80.
Herrinton LJ, Friedman GD (1998) Cigarette smoking and risk of non-Hodgkin’s lymphoma subtypes. Cancer Epidemiol Biomark Prev 7(1):25–28
81.
Talamini R, Polesel J, Montella M, Maso LD, Crispo A, Spina M et al (2005) Smoking and non-Hodgkin lymphoma: case-control study in Italy. Int J Cancer 115(4):606–610PubMed
82.
Stagnaro E, Tumino R, Parodi S, Crosignani P, Fontana A, Masala G et al (2004) Non-Hodgkin’s lymphoma and type of tobacco smoke. Cancer Epidemiol Biomark Prev 13(3):431–437
83.
Sergentanis TN, Kanavidis P, Michelakos T, Petridou ET (2013) Cigarette smoking and risk of lymphoma in adults: a comprehensive meta-analysis on Hodgkin and non-Hodgkin disease. Eur J Cancer Prev 22(2):131–150PubMed
84.
Besson H, Renaudier P, Merrill RM, Coiffier B, Sebban C, Fabry J et al (2003) Smoking and non-Hodgkin’s lymphoma: a case-control study in the Rhone-Alpes region of France. Cancer Causes Control 14(4):381–389PubMed
85.
Morton LM, Hartge P, Holford TR, Holly EA, Chiu BC, Vineis P et al (2005) Cigarette smoking and risk of non-Hodgkin lymphoma: a pooled analysis from the International Lymphoma Epidemiology Consortium (InterLymph). Cancer Epidemiol Biomark Prev 14(4):925–933
86.
Schollkopf C, Smedby KE, Hjalgrim H, Rostgaard K, Gadeberg O, Roos G et al (2005) Cigarette smoking and risk of non-Hodgkin’s lymphoma–a population-based case-control study. Cancer Epidemiol Biomark Prev 14(7):1791–1796
87.
Aschebrook-Kilfoy B, Cocco P, La Vecchia C, Chang ET, Vajdic CM, Kadin ME et al (2014) Medical history, lifestyle, family history, and occupational risk factors for mycosis fungoides and sezary syndrome: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):98–105PubMed
88.
Monnereau A, Slager SL, Hughes AM, Smith A, Glimelius B, Habermann TM et al (2014) Medical history, lifestyle, and occupational risk factors for hairy cell leukemia: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):115–124PubMed
89.
Bell DA, Liu Y, Cortopassi GA (1995) Occurrence of bcl-2 oncogene translocation with increased frequency in the peripheral blood of heavy smokers. J Natl Cancer Inst 87(3):223–224PubMed
90.
Chiu BC, Dave BJ, Blair A, Gapstur SM, Chmiel JS, Fought AJ et al (2007) Cigarette smoking, familial hematopoietic cancer, hair dye use, and risk of t(14;18)-defined subtypes of non-Hodgkin’s lymphoma. Am J Epidemiol 165(6):652–659PubMed
91.
Schroeder JC, Olshan AF, Dent RB, Weinberg CR, Yount B, Cerhan JR et al (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 13(2):159–168PubMed
92.
Diver WR, Teras LR, Gaudet MM, Gapstur SM (2014) Exposure to environmental tobacco smoke and risk of non-Hodgkin lymphoma in nonsmoking men and women. Am J Epidemiol 179(8):987–995PubMed
93.
Chang ET, Clarke CA, Canchola AJ, Lu Y, Wang SS, Ursin G et al (2010) Alcohol consumption over time and risk of lymphoid malignancies in the California teachers study cohort. Am J Epidemiol 172(12):1373–1383PubMedCentralPubMed
94.
Chiu BC, Cerhan JR, Gapstur SM, Sellers TA, Zheng W, Lutz CT et al (1999) Alcohol consumption and non-Hodgkin lymphoma in a cohort of older women. Br J Cancer 80(9):1476–1482PubMedCentralPubMed
95.
Chiu BC, Weisenburger DD, Cantor KP, Zahm SH, Holmes F, Burmeister LF et al (2002) Alcohol consumption, family history of hematolymphoproliferative cancer, and the risk of non-Hodgkin’s lymphoma in men. Ann Epidemiol 12(5):309–315PubMed
96.
Holly EA, Lele C, Bracci PM, McGrath MS (1999) Case-control study of non-Hodgkin’s lymphoma among women and heterosexual men in the San Francisco Bay Area, California. Am J Epidemiol 150(4):375–389PubMed
97.
Morton LM, Holford TR, Leaderer B, Zhang Y, Zahm SH, Boyle P et al (2003) Alcohol use and risk of non-Hodgkin’s lymphoma among Connecticut women (United States). Cancer Causes Control 14(7):687–694PubMed
98.
Lim U, Morton LM, Subar AF, Baris D, Stolzenberg-Solomon R, Leitzmann M et al (2007) Alcohol, smoking, and body size in relation to incident Hodgkin’’ and non-Hodgkin’s lymphoma risk. Am J Epidemiol 166(6):697–708PubMed
99.
De Stefani E, Fierro L, Barrios E, Ronco A (1998) Tobacco, alcohol, diet and risk of non-Hodgkin’s lymphoma: a case-control study in Uruguay. Leuk Res 22(5):445–452PubMed
100.
Wang SS, Flowers CR, Kadin ME, Chang ET, Hughes AM, Ansell SM et al (2014) Medical history, lifestyle, family history, and occupational risk factors for peripheral T-cell lymphomas: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):66–75PubMed
101.
Mbulaiteye SM, Morton LM, Sampson JN, Chang ET, Costas L, de Sanjose S et al (2014) Medical history, lifestyle, family history, and occupational risk factors for sporadic burkitt lymphoma/leukemia: the InterLymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr. 2014(48):106–114PubMed
102.
Cross AJ, Lim U (2006) The role of dietary factors in the epidemiology of non-Hodgkin’s lymphoma. Leuk Lymphoma 47(12):2477–2487PubMed
103.
Skibola CF (2007) Obesity, diet and risk of non-Hodgkin lymphoma. Cancer Epidemiol Biomarkers Prev 16(3):392–395PubMedCentralPubMed
104.
Chiu BC, Cerhan JR, Folsom AR, Sellers TA, Kushi LH, Wallace RB et al (1996) Diet and risk of non-Hodgkin lymphoma in older women. JAMA 275(17):1315–1321PubMed
105.
Purdue MP, Bassani DG, Klar NS, Sloan M, Kreiger N (2004) Dietary factors and risk of non-Hodgkin lymphoma by histologic subtype: a case-control analysis. Cancer Epidemiol Biomarkers Prev 13(10):1665–1676PubMed
106.
Zhang S, Hunter DJ, Rosner BA, Colditz GA, Fuchs CS, Speizer FE et al (1999) Dietary fat and protein in relation to risk of non-Hodgkin’s lymphoma among women. J Natl Cancer Inst 91(20):1751–1758PubMed
107.
Aschebrook-Kilfoy B, Ollberding NJ, Kolar C, Lawson TA, Smith SM, Weisenburger DD et al (2012) Meat intake and risk of non-Hodgkin lymphoma. Cancer Causes Control 23(10):1681–1692PubMed
108.
Chang ET, Smedby KE, Zhang SM, Hjalgrim H, Melbye M, Ost A et al (2005) Dietary factors and risk of non-hodgkin lymphoma in men and women. Cancer Epidemiol Biomarkers Prev. 14(2):512–520PubMed
109.
Cross AJ, Ward MH, Schenk M, Kulldorff M, Cozen W, Davis S et al (2006) Meat and meat-mutagen intake and risk of non-Hodgkin lymphoma: results from a NCI-SEER case-control study. Carcinogenesis 27(2):293–297PubMed
110.
Daniel CR, Sinha R, Park Y, Graubard BI, Hollenbeck AR, Morton LM et al (2012) Meat intake is not associated with risk of non-Hodgkin lymphoma in a large prospective cohort of U.S. men and women. J Nutr 142(6):1074–1080PubMedCentralPubMed
111.
Charbonneau B, O’’onnor HM, Wang AH, Liebow M, Thompson CA, Fredericksen ZS et al (2013) Trans fatty acid intake is associated with increased risk and n3 fatty acid intake with reduced risk of non-hodgkin lymphoma. J Nutr 143(5):672–681PubMedCentralPubMed
112.
Zheng T, Holford TR, Leaderer B, Zhang Y, Zahm SH, Flynn S et al (2004) Diet and Nutrient Intakes and Risk of Non-Hodgkin’s Lymphoma in Connecticut Women. Am J Epidemiol 159(5):454–466PubMed
113.
Davis S (1992) Nutritional factors and the development of non-Hodgkin’s lymphoma: a review of the evidence. Cancer Res 52(19 Suppl):5492s–5495sPubMed
114.
Ollberding NJ, Aschebrook-Kilfoy B, Caces DB, Wright ME, Weisenburger DD, Smith SM et al (2013) Phytanic acid and the risk of non-Hodgkin lymphoma. Carcinogenesis 34(1):170–175PubMedCentralPubMed
115.
Calder PC, Kew S (2002) The immune system: a target for functional foods? Br J Nutr 88:S165–S177PubMed
116.
Kelemen LE, Cerhan JR, Lim U, Davis S, Cozen W, Schenk M et al (2006) Vegetables, fruit, and antioxidant-related nutrients and risk of non-Hodgkin lymphoma: a National Cancer Institute-Surveillance, epidemiology, and end results population-based case-control study. Am J Clin Nutr 83(6):1401–1410PubMed
117.
Talamini R, Polesel J, Montella M, Dal Maso L, Crovatto M, Crispo A et al. (2006) Food groups and risk of non-Hodgkin lymphoma: a multicenter, case-control study in Italy. Int J Cancer 118(11): 2871–2876
118.
Rohrmann S, Becker N, Linseisen J, Nieters A, Rudiger T, Raaschou-Nielsen O et al (2007) Fruit and vegetable consumption and lymphoma risk in the European prospective investigation into cancer and nutrition (EPIC). Cancer Causes Control 18(5):537–549PubMed
119.
Thompson CA, Habermann TM, Wang AH, Vierkant RA, Folsom AR, Ross JA et al (2010) Antioxidant intake from fruits, vegetables and other sources and risk of non-Hodgkin’s lymphoma: the Iowa Women’s health study. Int J Cancer 126(4):992–1003PubMedCentralPubMed
120.
Ollberding NJ, Maskarinec G, Conroy SM, Morimoto Y, Franke AA, Cooney RV et al (2012) Prediagnostic circulating carotenoid levels and the risk of non-Hodgkin lymphoma: the Multiethnic Cohort. Blood 119(24):5817–5823PubMedCentralPubMed
121.
Erber E, Maskarinec G, Gill JK, Park SY, Kolonel LN (2009) Dietary patterns and the risk of non-Hodgkin lymphoma: the multiethnic cohort. Leuk Lymphoma 50(8):1269–1275PubMedCentralPubMed
122.
Ollberding NJ, Aschebrook-Kilfoy B, Caces DB, Smith SM, Weisenburger DD, Chiu BC (2013) Dietary patterns and the risk of non-hodgkin lymphoma. Public Health Nutr 1–7
123.
Marti A, Marcos A, Martinez JA (2001) Obesity and immune function relationships. Obes Rev 2(2):131–140PubMed
124.
Cerhan JR, Bernstein L, Severson RK, Davis S, Colt JS, Blair A et al (2005) Anthropometrics, physical activity, related medical conditions, and the risk of non-hodgkin lymphoma. Cancer Causes Control 16(10):1203–1214PubMed
125.
Skibola CF, Holly EA, Forrest MS, Hubbard A, Bracci PM, Skibola DR et al (2004) Body mass index, leptin and leptin receptor polymorphisms, and non-hodgkin lymphoma. Cancer Epidemiol Biomark Prev 13(5):779–786
126.
Chang ET, Hjalgrim H, Smedby KE, Akerman M, Tani E, Johnsen HE et al (2005) Body mass index and risk of malignant lymphoma in Scandinavian men and women. J Natl Cancer Inst 97(3):210–218PubMed
127.
Fernberg P, Odenbro A, Bellocco R, Boffetta P, Pawitan Y, Adami J (2006) Tobacco use, body mass index and the risk of malignant lymphomas–a nationwide cohort study in Sweden. Int J Cancer 118(9):2298–2302PubMed
128.
Tulinius H, Sigfusson N, Sigvaldason H, Bjarnadottir K, Tryggvadottir L (1997) Risk factors for malignant diseases: a cohort study on a population of 22,946 Icelanders. Cancer Epidemiol Biomark Prev 6(11):863–873
129.
Cerhan JR, Janney CA, Vachon CM, Habermann TM, Kay NE, Potter JD et al (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(6):527–535PubMed
130.
MacInnis RJ, English DR, Hopper JL, Giles GG (2005) Body size and composition and the risk of lymphohematopoietic malignancies. J Natl Cancer Inst 97(15):1154–1157PubMed
131.
Willett EV, Morton LM, Hartge P, Becker N, Bernstein L, Boffetta P et al (2008) Non-Hodgkin lymphoma and obesity: a pooled analysis from the InterLymph Consortium. Int J Cancer 122(9):2062–2070PubMedCentralPubMed
132.
Larsson SC, Wolk A (2007) Obesity and risk of non-Hodgkin’s lymphoma: a meta-analysis. Int J Cancer 121(7):1564–1570PubMed
133.
Larsson SC, Wolk A (2011) Body mass index and risk of non-Hodgkin’s and Hodgkin’’ lymphoma: a meta-analysis of prospective studies. Eur J Cancer 47(16):2422–2430PubMed
134.
Ames BN, Kammen HO, Yamasaki E (1975) Hair dyes are mutagenic: identification of a variety of mutagenic ingredients. Proc Natl Acad Sci USA 72(6):2423–2427PubMedCentralPubMed
135.
de Sanjose S, Benavente Y, Nieters A, Foretova L, Maynadie M, Cocco PL et al (2006) Association between personal use of hair dyes and lymphoid neoplasms in Europe. Am J Epidemiol 164(1):47–55
136.
Zhang Y, Holford TR, Leaderer B, Boyle P, Zahm SH, Flynn S et al (2004) Hair-coloring product use and risk of non-Hodgkin’s lymphoma: a population-based case-control study in Connecticut. Am J Epidemiol 159(2):148–154PubMed
137.
Zhang Y, Sanjose SD, Bracci PM, Morton LM, Wang R, Brennan P et al (2008) Personal use of hair dye and the risk of certain subtypes of non-Hodgkin lymphoma. Am J Epidemiol 167(11):1321–1331PubMedCentralPubMed
138.
Melbye M, Adami HO, Hjalgrim H, Glimelius B (1996) Ultraviolet light and non-Hodgkin’s lymphoma. Acta Oncol 35(6):655–657PubMed
139.
Hartge P, Lim U, Freedman DM, Colt JS, Cerhan JR, Cozen W et al (2006) Ultraviolet radiation, dietary vitamin D, and risk of non-Hodgkin lymphoma (United States). Cancer Causes Control 17(8):1045–1052PubMed
140.
Hughes AM, Armstrong BK, Vajdic CM, Turner J, Grulich AE, Fritschi L et al (2004) Sun exposure may protect against non-Hodgkin lymphoma: a case-control study. Int J Cancer 112(5):865–871PubMed
141.
Smedby KE, Hjalgrim H, Melbye M, Torrang A, Rostgaard K, Munksgaard L et al (2005) Ultraviolet radiation exposure and risk of malignant lymphomas. J Natl Cancer Inst 97(3):199–209PubMed
142.
Weihkopf T, Becker N, Nieters A, Mester B, Deeg E, Elsner G et al (2007) Sun exposure and malignant lymphoma: a population-based case-control study in Germany. Int J Cancer 120(11):2445–2451PubMed
143.
Kricker A, Armstrong BK, Hughes AM, Goumas C, Smedby KE, Zheng T et al (2008) Personal sun exposure and risk of non Hodgkin lymphoma: a pooled analysis from the InterLymph Consortium. Int J Cancer 122(1):144–154PubMed
144.
Ullrich SE (1996) Does exposure to UV radiation induce a shift to a Th-2-like immune reaction? Photochem Photobiol 64(2):254–258PubMed
145.
Reichrath J, Rappl G (2003) Ultraviolet light (UV)-induced immunosuppression: is vitamin D the missing link? J Cell Biochem 89(1):6–8PubMed
146.
Aref S, Ibrahim L, Azmy E (2013) Prognostic impact of serum 25-hydroxivitamin D [25(OH)D] concentrations in patients with lymphoid malignancies. Hematology 18(1):20–25
147.
Shanafelt TD, Drake MT, Maurer MJ, Allmer C, Rabe KG, Slager SL et al (2011) Vitamin D insufficiency and prognosis in chronic lymphocytic leukemia. Blood 117(5):1492–1498PubMedCentralPubMed
148.
Drake MT, Maurer MJ, Link BK, Habermann TM, Ansell SM, Micallef IN et al (2010) Vitamin D insufficiency and prognosis in non-Hodgkin’s lymphoma. J Clin Oncol 28(27):4191–4198PubMedCentralPubMed
149.
Luczynska A, Kaaks R, Rohrmann S, Becker S, Linseisen J, Buijsse B et al (2013) Plasma 25-hydroxyvitamin D concentration and lymphoma risk: results of the European prospective investigation into cancer and nutrition. Am J clin Nutr 98(3):827–838PubMed
150.
Purdue MP, Freedman DM, Gapstur SM, Helzlsouer KJ, Laden F, Lim U et al (2010) Circulating 25-hydroxyvitamin D and risk of non-hodgkin lymphoma: Cohort Consortium Vitamin D pooling project of rarer cancers. Am J Epidemiol 172(1):58–69PubMedCentralPubMed
151.
Boffetta P, de Vocht F (2007) Occupation and the risk of non-Hodgkin lymphoma. Cancer Epidemiol Biomark Prev 16(3):369–372
152.
Cocco P, Satta G, D’’ndrea I, Nonne T, Udas G, Zucca M et al (2013) Lymphoma risk in livestock farmers: results of the Epilymph study. Int J Cancer 132(11):2613–2618PubMed
153.
Espinosa A, Zock JP, Benavente Y, Boffetta P, Becker N, Brennan P et al (2013) Occupational exposure to immunologically active agents and risk for lymphoma: the European Epilymph case-control study. Cancer Epidemiol 37(4):378–384PubMed
154.
Skibola CF, Slager SL, Berndt SI, Lightfoot T, Sampson JN, Morton LM et al (2014) Medical history, lifestyle, family history, and occupational risk factors for adult acute lymphocytic leukemia: the InterLymph non-Hodgkin lymphoma subtypes Project. J Natl Cancer Inst Monogr 2014(48):125–129PubMed
155.
Cocco P, Satta G, Dubois S, Pili C, Pilleri M, Zucca M et al (2013) Lymphoma risk and occupational exposure to pesticides: results of the Epilymph study. Occup Environ Med 70(2):91–98PubMed
156.
Cantor KP, Blair A, Everett G, Gibson R, Burmeister LF, Brown LM et al (1992) Pesticides and other agricultural risk factors for non-Hodgkin’s lymphoma among men in Iowa and Minnesota. Cancer Res 52(9):2447–2455PubMed
157.
Zahm SH, Blair A. Pesticides and non-Hodgkin’s lymphoma. Cancer Res. 52(19 Supplement):5485s–5488s
158.
Zahm SH, Weisenburger DD, Babbitt PA, Saal RC, Vaught JB, Cantor KP et al (1990) A case-control study of non-Hodgkin’s lymphoma and the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D) in eastern Nebraska. Epidemiology 1(5): 49–356
159.
Chiu BC, Dave BJ, Blair A, Gapstur SM, Zahm SH, Weisenburger DD (2006) Agricultural pesticide use and risk of t(14;18)-defined subtypes of non-Hodgkin lymphoma. Blood 108(4):1363–1369PubMedCentralPubMed
160.
Schroeder JC, Olshan AF, Baric R, Dent GA, Weinberg CR, Yount B, et al. (2001) Agricultural risk factors for t(14;18) subtypes of non-Hodgkin’s lymphoma. Epidemiology 12(6):701-709
161.
Pimental D, McLaughlin L, Zepp A (1993) Environmental and economic impacts of reducing US agricultural pesticide use. In: Pimental D (ed) Handbook of pest management in agriculture, 1st edn. CRC Press, Boca Raton, pp 679–680
162.
Cocco P, t’’annetje A, Fadda D, Melis M, Becker N, de Sanjose S et al (2010) Occupational exposure to solvents and risk of lymphoma subtypes: results from the Epilymph case-control study. Occup Env Med 67(5):341–347
163.
Deng Q, Zheng T, Lan Q, Lan Y, Holford T, Chen Y et al (2013) Occupational solvent exposure, genetic variation in immune genes, and the risk for non-Hodgkin lymphoma. Eur J Cancer Prev 22(1):77–82PubMedCentralPubMed
164.
Linet MS, Pottern LM (1992) Familial aggregation of hematopoietic malignancies and risk of non-Hodgkin’s lymphoma. Cancer Res 52S:5468–5473
165.
Paltiel O, Schmit T, Adler B, Rachmilevitz EA, Polliack A, Cohen A et al (2000) The incidence of lymphoma in first-degree relatives of patients with hodgkin disease and non-Hodgkin lymphoma: results and limitations of a registry-linked study. Cancer 88(10):2357–2366PubMed
166.
Casey R, Brennan P, Becker N, Boffetta P, Cocco P, Domingo-Domenech E et al (2006) Influence of familial cancer history on lymphoid neoplasms risk validated in the large European case-control study epilymph. Eur J Cancer 42(15):2570–2576PubMed
167.
Wang SS, Slager SL, Brennan P, Holly EA, De Sanjose S, Bernstein L et al (2007) Family history of hematopoietic malignancies and risk of non-Hodgkin lymphoma (NHL): a pooled analysis of 10,211 cases and 11,905 controls from the International Lymphoma Epidemiology Consortium (InterLymph). Blood 109(8):3479–3488PubMedCentralPubMed
168.
Zhu K, Levine RS, Brann EA, Gu Y, Caplan LS, Hall I et al (2001) Risk factors for non-Hodgkin’s lymphoma according to family history of haematolymphoproliferative malignancies. Int J Epidemiol 30:818–824PubMed
169.
Skibola CF, Curry JD, Nieters A (2007) Genetic susceptibility to lymphoma. Haematologica 92(7):960–969PubMedCentralPubMed
170.
Bateman AC, Howell WM (1999) Human leukocyte antigens and cancer: is it in our genes? J Pathol 188(3):231–236PubMed
171.
Skibola CF, Bracci PM, Halperin E, Conde L, Craig DW, Agana L et al (2009) Genetic variants at 6p21.33 are associated with susceptibility to follicular lymphoma. Nat Genet 41(8):873–875PubMedCentralPubMed
172.
Smedby KE, Foo JN, Skibola CF, Darabi H, Conde L, Hjalgrim H et al (2011) GWAS of follicular lymphoma reveals allelic heterogeneity at 6p21.32 and suggests shared genetic susceptibility with diffuse large B-cell lymphoma. PLoS Genet 7(4):e1001378PubMedCentralPubMed
173.
Cerhan JR, Fredericksen ZS, Novak AJ, Ansell SM, Kay NE, Liebow M et al (2012) A two-stage evaluation of genetic variation in immune and inflammation genes with risk of non-Hodgkin lymphoma identifies new susceptibility locus in 6p21.3 region. Cancer Epidemiol Biomark Prev 21(10):1799–1806
174.
Lim U, Kocarnik JM, Bush WS, Matise TC, Caberto C, Park SL et al (2014) Pleiotropy of cancer susceptibility variants on the risk of non-Hodgkin lymphoma: the PAGE consortium. PLoS one 9(3):e89791PubMedCentralPubMed
175.
Slager SL, Rabe KG, Achenbach SJ, Vachon CM, Goldin LR, Strom SS et al (2011) Genome-wide association study identifies a novel susceptibility locus at 6p21.3 among familial CLL. Blood 117(6):1911–1916PubMedCentralPubMed
176.
Slager SL, Achenbach SJ, Asmann YW, Camp NJ, Rabe KG, Goldin LR et al (2013) Mapping of the IRF8 gene identifies a 3’TR variant associated with risk of chronic lymphocytic leukemia but not other common non-Hodgkin lymphoma subtypes. Cancer Epidemiol Biomark Prev 22(3):461–466
177.
Rothman N, Skibola CF, Wang SS, Morgan G, Lan Q, Smith MT et al (2006) Genetic variation in TNF and IL10 and risk of non-Hodgkin lymphoma: a report from the InterLymph Consortium. Lancet Oncol 7(1):27–38PubMed
178.
Niclot S, Pruvot Q, Besson C, Savoy D, Macintyre E, Salles G et al (2006) Implication of the folate-methionine metabolism pathways in susceptibility to follicular lymphomas. Blood 108(1):278–285PubMed
179.
Rudd MF, Sellick GS, Allinson R, Matutes E, Catovsky D, Houlston RS (2004) MTHFR polymorphisms and risk of chronic lymphocytic leukemia. Cancer Epidemiol Biomark Prev 13(12):2268–2270
180.
Skibola CF, Forrest MS, Coppede F, Agana L, Hubbard A, Smith MT et al (2004) Polymorphisms and haplotypes in folate-metabolizing genes and risk of non-Hodgkin lymphoma. Blood 104(7):2155–2162PubMed
181.
Morton LM, Slager SL, Cerhan JR, Wang SS, Vajdic CM, Skibola CF et al (2014) Etiologic heterogeneity among non-hodgkin lymphoma subtypes: the InterLymph non-Hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014(48):130–144PubMed
182.
Evens AM, Chiu BC (2008) The challenges of epidemiologic research in non-Hodgkin lymphoma. JAMA 300(17):2059–2061PubMed
183.
Turner JJ, Morton LM, Linet MS, Clarke CA, Kadin ME, Vajdic CM et al (2010) InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): update and future directions. Blood 116(20):e90–e98PubMedCentralPubMed
184.
Rimsza LM, Leblanc ML, Unger JM, Miller TP, Grogan TM, Persky DO et al (2008) Gene expression predicts overall survival in paraffin-embedded tissues of diffuse large B-cell lymphoma treated with R-CHOP. Blood 112(8):3425–3433PubMed