Abstract
Background and purpose
Adult T-cell leukemia/lymphoma (ATLL) is an aggressive hematological malignancy caused by human T-cell leukemia virus type-1 (HTLV-1); no effective methods have yet been identified to prevent development of ATLL in carriers of HTLV-1. This study investigated the association between cigarette smoking and the risk of ATLL development among Japanese carriers of HTLV-1.
Methods
This study examined the association between smoking and development of ATLL in a cohort of 1,332 Japanese HTLV-1 carriers aged 40–69 years free of ATLL at baseline from two different HTLV-1-endemic areas of Japan. Cox proportional hazards models adjusted for sex, geographic area, age at baseline, and alcohol drinking were used to estimate the effect of cigarette smoking on ATLL development.
Results
Between 1993 and 2012, 25 new ATLL cases were identified among these subjects. The overall crude incidence rate for ATLL was 1.08 per 1,000 person-years among HTLV-1 carriers and was higher among male carriers than among female carriers (2.21 vs. 0.74). The risk of ATLL development increased significantly with increasing numbers of cigarettes smoked per day (hazard ratio for every increment of 20 cigarettes, 2.03; 95 % confidence interval (CI) 1.13–3.66 overall, 2.07 (95 % CI 1.13–3.73) in male carriers).
Conclusions
Cigarette smoking may influence ATLL development among HTLV-1 carriers in Japan.
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References
Takatsuki K, Uchiyama T, Sagawa K, Yodoi J (1977) Adult T cell leukemia in Japan. In: Seno S, Takaku S, Irino S (eds) Topics in Hematology. Excepta Medica, Amsterdam, pp 73–77
Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gallo RC (1980) Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci USA 77:7415–7419
Yoshida M, Miyoshi I, Hinuma Y (1982) Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc Natl Acad Sci USA 79:2031–2035
Gessain A, Cassar O (2012) Epidemiological aspects and world distribution on HTLV-1 infection. Front Microbiol 3:1–23
Tajima K (1990) The 4th nation-wide study of adult T-cell leukemia/lymphoma (ATL) in Japan: estimates of risk of ATL and its geographical and clinical features. The T-cell and B-cell Malignancy Study Group. Int J Cancer 36:643–649
Inaba S, Sato H, Okochi K, Fukada K et al (1989) Prevention of transmission of human T-lymphotropic virus type 1 (HTLV-1) through transfusion, by donor screening with antibody to the virus: one-year experience. Transfusion 29:7–11
Hino S (2011) Establishment of the milk-borne transmission as a key factor for the peculiar endemicity of human T-lymphotropic virus type 1 (HTLV-1): the ATL Prevention Program Nagasaki. Proc Jpn Acad Ser B Phys Biol Sci 87(4):152–166
Satake M, Yamaguchi K, Tadokoro K (2012) Current prevalence of HTLV-1 in Japan as determined by screening of blood donors. J Med Virol 84(2):327–335
Yamada Y, Atogami S, Hasegawa H, Kamihira S, Soda M, Satake M, Yamaguchi K (2011) Nationwide survey of adult T-cell leukemia/lymphoma (ATL) in Japan. Rinsho Ketsueki 52(11):1765–1771 (Japanese)
Murphy EL, Hanchard B, Figueroa JP et al (1989) Modeling the risk of adult T-cell leukemia/lymphoma in persons infected with human T-lymphotropic virus type 1. Int J Cancer 43(2):250–253
Yamaguchi K, Watanabe T (2002) Human T lymphotropic virus type-1 and adult T-cell leukemia in Japan. Int J Hematol 76(2):240–245
Wilks R (1996) Patterns of HTLV-1 infection among family members of patients with adult T-cell leukemia/lymphoma and HTLV-1 associated myelopathy/tropical spastic paraparesis. Int J Cancer 65(2):272–273
Iwanaga M, Watanabe T, Yamaguchi K (2012) Adult T-cell leukemia: a review of epidemiological evidence. Front Microbiol 10(3):322
Yamagishi M, Watanabe T (2012) Molecular hallmarks of adult T cell leukemia. Front Microbiol 17(3):334
Arisawa K, Katamine S, Kamihira S et al (2002) A nested case-control study of risk factors for adult T-cell leukemia/lymphoma among human T-cell lymphotropic virus type-I carriers in Japan. Cancer Causes Control 13(7):657–663
Iwanaga M, Watanabe T, Utsunomiya A et al (2010) Human T-cell leukemia virus type I (HTLV-1) proviral load and disease progression in asymptomatic HTLV-1 carriers: a nationwide prospective study in Japan. Blood 116(8):1211–1219
Seiki M, Hattori S, Hitayama Y, Yoshida M (1983) Human adult T-cell leukemia virus: complete nucleotides sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci USA 80:3618–3622
Wong-Staal F, Gallo RC (1985) Human T-lymphotropic retroviruses. Nature 317:395–403
Fircanis S, Merriam P, Khan N, Castillo JJ (2014) The relation between cigarette smoking and risk of acute myeloid leukemia: an updated meta-analysis of epidemiological studies. Am J Hematol 89(8):E125–E132
Tsugane S, Sawada N (2014) The JPHC study: design and some findings on the typical Japanese diet. Jpn Clin Oncol 44(9):777–782
Fritz AG (2000) International Classification of Diseases for Oncology: ICD-O, 3rd edn. World Health Organization, Geneva
Cox DR (1972) Regression models and life tables (with discussion). J R Stat Soc Series B Stat Methodol 34:187–220
Tokudome S, Shimamoto Y, Sumida I (1993) Smoking and T-cell leukemia/lymphoma. Eur J Cancer Prev 2:84–86
Hisada M, Okayama A, Shioiri S, Spiegelman DL, Stuver SO, Mueller NE (1998) Risk factors for adult T-cell leukemia among carriers of human T-lymphotropic virus type I. Blood 92:3357–3361
Morton LM, Hartge P, Holford TR et al (2005) Cigarette smoking and risk of non-Hodgkin lymphoma: a pooled analysis from the International Lymphoma Epidemiology Consortium (interlymph). Cancer Epidemiol Biomarkers Prev 14:925–933
Besson H, Brennan P, Becker N, Nieters A, De Sanjosé S, Font R, Maynadié M, Foretova L, Cocco PL, Staines A, Vornanen M, Boffetta P (2006) Tobacco smoking, alcohol drinking and non-Hodgkin’s lymphoma: a European multicenter case-control study (Epilymph). Int J Cancer 119(4):901–908
Diver WR, Patel AV, Thun MJ, Tears LR, Gapstur SM (2012) The association between cigarette smoking and non-Hodgkin lymphoid neoplasms in a large US cohort study. Cancer Causes Control 23:1231–1240
Kamper-Jørgensen M, Rostgaard K, Glaser SL, Zahm SH, Cozen W et al (2013) Cigarette smoking and risk of Hodgkin lymphoma and its subtypes: a pooled analysis from the International Lymphoma Epidemiology Consortium (InterLymph). Ann Oncol 24(9):2245–2255
Castillo JJ, Dalia S (2012) Cigarette smoking is associated with a small increase in the incidence of non-Hodgkin lymphoma: a meta-analysis of 24 observational studies. Leuk Lymphoma 53(10):1911–1919
Diver WR, Patel AV, Thun MJ, Teras LR, Gapstur SM (2012) The association between cigarette smoking and non-Hodgkin lymphoid neoplasms in a large US cohort study. Cancer Causes Control 23(8):1231–1240
Ceasrman E, Chadburn A, Inghirami G et al (1992) Structual and functional analysis of oncogenes and tumor suppressor genes in adult T-cell leukemia/lymphoma shows freaquent p53 mutations. Blood 80:3205–3216
Hatta Y, Koeffler HP (2002) Role of tumor suppressor genes in the development of adult T cell leukemia/lymphoma (ATL). Leukemia 16:1069–1085
Okamoto T (1989) Multi-step carcinogenesis model for adult T-cell leukemia. Jpn J Cancer Res 80:191–195
Tajima K, Kuroishi T (1985) Estimation of rate of incidence of ATL among ATLV(HTLV-1) carriers in Kyushu, Japan. Jpn J Clin Oncol 15:423–430
Yeager DS, Krosnick JA (2010) The validity of self-reported nicotine product use in the 2001–2008 National Health and Nutrition Examination Survey. Med Care 48:1128–1132
Acknowledgments
The authors thank the staff of each JPHC study area and the central office for their painstaking efforts to conduct the baseline survey and follow-up. We are indebted to the Ibaraki, Niigata, Osaka, Kochi, Nagasaki, and Okinawa Cancer Registries for providing their incidence data. This study was supported by the National Cancer Center Research and Development Fund (23-A-31[toku] and 26-A-2) (since 2011) and a Grant-in-Aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan (from 1989 to 2010).
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Appendix
Appendix
Members of the Japan Public Health Center-based Prospective Study (JPHC Study, principal investigator: S. Tsugane) Group are: S. Tsugane, N. Sawada, M. Iwasaki, S. Sasazuki, T. Yamaji, T. Shimazu and T. Hanaoka, National Cancer Center, Tokyo; J. Ogata, S. Baba, T. Mannami, A. Okayama, and Y. Kokubo, National Cerebral and Cardiovascular Center, Osaka; K. Miyakawa, F. Saito, A. Koizumi, Y. Sano, I. Hashimoto, T. Ikuta, Y. Tanaba, H. Sato, Y. Roppongi, T. Takashima and H. Suzuki, Iwate Prefectural Ninohe Public Health Center, Iwate; Y. Miyajima, N. Suzuki, S. Nagasawa, Y. Furusugi, N. Nagai, Y. Ito, S. Komatsu and T. Minamizono, Akita Prefectural Yokote Public Health Center, Akita; H. Sanada, Y. Hatayama, F. Kobayashi, H. Uchino, Y. Shirai, T. Kondo, R. Sasaki, Y. Watanabe, Y. Miyagawa, Y. Kobayashi, M. Machida, K. Kobayashi and M. Tsukada, Nagano Prefectural Saku Public Health Center, Nagano; Y. Kishimoto, E. Takara, T. Fukuyama, M. Kinjo, M. Irei, and H. Sakiyama, Okinawa Prefectural Chubu Public Health Center, Okinawa; K. Imoto, H. Yazawa, T. Seo, A. Seiko, F. Ito, F. Shoji and R. Saito, Katsushika Public Health Center, Tokyo; A. Murata, K. Minato, K. Motegi, T. Fujieda and S. Yamato, Ibaraki Prefectural Mito Public Health Center, Ibaraki; K. Matsui, T. Abe, M. Katagiri, M. Suzuki, K. and Matsui, Niigata Prefectural Kashiwazaki and Nagaoka Public Health Center, Niigata; M. Doi, A. Terao, Y. Ishikawa, and T. Tagami, Kochi Prefectural Chuo-higashi Public Health Center, Kochi; H. Sueta, H. Doi, M. Urata, N. Okamoto, F. Ide, H. Goto and R Fujita, Nagasaki Prefectural Kamigoto Public Health Center, Nagasaki; H. Sakiyama, N. Onga, H. Takaesu, M. Uehara, T. Nakasone and M. Yamakawa, Okinawa Prefectural Miyako Public Health Center, Okinawa; F. Horii, I. Asano, H. Yamaguchi, K. Aoki, S. Maruyama, M. Ichii, and M. Takano, Osaka Prefectural Suita Public Health Center, Osaka; Y. Tsubono, Tohoku University, Miyagi; K. Suzuki, Research Institute for Brain and Blood Vessels Akita, Akita; Y. Honda, K. Yamagishi, S. Sakurai and N. Tsuchiya, University of Tsukuba, Ibaraki; M. Kabuto, National Institute for Environmental Studies, Ibaraki; M. Yamaguchi, Y. Matsumura, S. Sasaki, and S. Watanabe, National Institute of Health and Nutrition, Tokyo; M. Akabane, Tokyo University of Agriculture, Tokyo; T. Kadowaki and M. Inoue, The University of Tokyo, Tokyo; M. Noda and T. Mizoue, National Center for Global Health and Medicine, Tokyo; Y. Kawaguchi, Tokyo Medical and Dental University, Tokyo; Y. Takashima and Y. Yoshida, Kyorin University, Tokyo; K. Nakamura and R. Takachi, Niigata University, Niigata; J. Ishihara, Sagami Women’s University, Kanagawa; S. Matsushima and S. Natsukawa, Saku General Hospital, Nagano; H. Shimizu, Sakihae Institute, Gifu; H. Sugimura, Hamamatsu University School of Medicine, Shizuoka; S. Tominaga, Aichi Cancer Center, Aichi; N. Hamajima, Nagoya University, Aichi; H. Iso and T. Sobue, Osaka University, Osaka; M. Iida, W. Ajiki, and A. Ioka, Osaka Medical Center for Cancer and Cardiovascular Disease, Osaka; S. Sato, Chiba Prefectural Institute of Public Health, Chiba; E. Maruyama, Kobe University, Hyogo; M. Konishi, K. Okada, and I. Saito, Ehime University, Ehime; N. Yasuda, Kochi University, Kochi; S. Kono, Kyushu University, Fukuoka; S. Akiba, Kagoshima University, Kagoshima; T. Isobe, Keio University; Y. Sato, Tokyo Gakugei University, Tokyo.
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Kondo, H., Soda, M., Sawada, N. et al. Smoking is a risk factor for development of adult T-cell leukemia/lymphoma in Japanese human T-cell leukemia virus type-1 carriers. Cancer Causes Control 27, 1059–1066 (2016). https://doi.org/10.1007/s10552-016-0784-8
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DOI: https://doi.org/10.1007/s10552-016-0784-8