The Evolving Epidemiology of Nasopharyngeal Carcinoma.
Animals
Case-Control Studies
China
/ epidemiology
Epstein-Barr Virus Infections
/ epidemiology
Feeding Behavior
Fishes
Food, Preserved
/ adverse effects
Geography
Herpesvirus 4, Human
/ pathogenicity
Humans
Incidence
Nasopharyngeal Carcinoma
/ epidemiology
Nasopharyngeal Neoplasms
/ epidemiology
Risk Factors
Sodium Chloride, Dietary
/ adverse effects
Journal
Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology
ISSN: 1538-7755
Titre abrégé: Cancer Epidemiol Biomarkers Prev
Pays: United States
ID NLM: 9200608
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
received:
01
12
2020
revised:
15
01
2021
accepted:
26
03
2021
pubmed:
15
4
2021
medline:
27
1
2022
entrez:
14
4
2021
Statut:
ppublish
Résumé
The epidemiology of nasopharyngeal carcinoma (NPC) has long been a source of fascination due to the malignancy's striking geographic distribution, the involvement of the oncogenic Epstein-Barr virus (EBV), the unique association with intake of Chinese-style salt-preserved fish, and etiologic heterogeneity by histologic subtype. This review summarizes the current epidemiologic literature on NPC, highlighting recent results from our population-based case-control study in southern China. Findings from our case-control study provide new insight into the epidemiology of NPC, including a diminished role of Chinese-style salt-preserved fish, a profound impact of EBV genetic sequence variation, modest positive associations with passive smoking and household air pollution, and possible effects of oral health and the oral microbiome. Recent findings from other studies include a protective association with infectious mononucleosis, suggesting a causal role of early EBV infection; familial risk conferred by shared genetic variation in the host antibody-mediated immune response to EBV infection; and an unclear association with occupational exposure to formaldehyde. To shed further light on the interplay of environmental, genetic, and viral causes of NPC, large pooled studies must accumulate sufficient cases with detailed exposure data. New epidemiologic findings have reshaped the causal model for NPC.
Sections du résumé
BACKGROUND
The epidemiology of nasopharyngeal carcinoma (NPC) has long been a source of fascination due to the malignancy's striking geographic distribution, the involvement of the oncogenic Epstein-Barr virus (EBV), the unique association with intake of Chinese-style salt-preserved fish, and etiologic heterogeneity by histologic subtype.
METHODS
This review summarizes the current epidemiologic literature on NPC, highlighting recent results from our population-based case-control study in southern China.
RESULTS
Findings from our case-control study provide new insight into the epidemiology of NPC, including a diminished role of Chinese-style salt-preserved fish, a profound impact of EBV genetic sequence variation, modest positive associations with passive smoking and household air pollution, and possible effects of oral health and the oral microbiome. Recent findings from other studies include a protective association with infectious mononucleosis, suggesting a causal role of early EBV infection; familial risk conferred by shared genetic variation in the host antibody-mediated immune response to EBV infection; and an unclear association with occupational exposure to formaldehyde.
CONCLUSIONS
To shed further light on the interplay of environmental, genetic, and viral causes of NPC, large pooled studies must accumulate sufficient cases with detailed exposure data.
IMPACT
New epidemiologic findings have reshaped the causal model for NPC.
Identifiants
pubmed: 33849968
pii: 1055-9965.EPI-20-1702
doi: 10.1158/1055-9965.EPI-20-1702
doi:
Substances chimiques
Sodium Chloride, Dietary
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1035-1047Informations de copyright
©2021 American Association for Cancer Research.
Références
Muir CS. Nasopharyngeal cancer–a historical vignette. CA Cancer J Clin. 1983;33:180–5.
Ye W, Chang ET, Liu Z, Liu Q, Cai Y, Zhang Z, et al. Development of a population-based cancer case-control study in southern China. Oncotarget. 2017;8:87073–85.
Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global cancer observatory: cancer today. 2018a.
Bray F, Colombet M, Mery L, Piñeros M, Znaor A, Zanetti R, et al. Cancer incidence in five continents, Vol. XI (electronic version). 2017.
Chan JKC, Bray F, McCarron P, Foo W, Lee AWM, Yip T, et alBarnes L, Eveson JW, Reichart P, Sidransky D. Nasopharyngeal carcinoma. World Health Organization classification of tumours. Pathology & genetics. Head and neck tumours. 2005;85–97.
Vaughan TL, Shapiro JA, Burt RD, Swanson GM, Berwick M, Lynch CF, et al. Nasopharyngeal cancer in a low-risk population: defining risk factors by histological type. Cancer Epidemiol Biomarkers Prev. 1996;5:587–93.
Li CC, Yu MC, Henderson BE. Some epidemiologic observations of nasopharyngeal carcinoma in Guangdong, People's Republic of China. Natl Cancer Inst Monogr. 1985;69:49–52.
Wee JTS, Ha TC, Loong SLE, Qian C-N. Is nasopharyngeal cancer really a "Cantonese cancer"?. Chin J Cancer. 2010;29:517–26.
Mousavi SM, Sundquist J, Hemminki K. Nasopharyngeal and hypopharyngeal carcinoma risk among immigrants in Sweden. Int J Cancer. 2010;127:2888–92.
Yu WM, Hussain SS. Incidence of nasopharyngeal carcinoma in Chinese immigrants, compared with Chinese in China and South East Asia: review. J Laryngol Otol. 2009;123:1067–74.
Parkin DM, Iscovich J. Risk of cancer in migrants and their descendants in Israel: II. Carcinomas and germ-cell tumours. Int J Cancer. 1997;70:654–60.
Flores AD, Dickson RI, Riding K, Coy P. Cancer of the nasopharynx in British Columbia. Am J Clin Oncol. 1986;9:281–91.
Buell P. Race and place in the etiology of nasopharyngeal cancer: a study based on California death certificates. Int J Cancer. 1973;11:268–72.
Jeannel D, Ghnassia M, Hubert A, Sancho-Garnier H, Eschwège F, Crognier E, et al. Increased risk of nasopharyngeal carcinoma among males of French origin born in Maghreb (north Africa). Int J Cancer. 1993;54:536–9.
Ferlay J, Colombet M, Bray F. Cancer incidence in five continents, CI5 I-X: IARC CancerBase No. 9 [Internet]. 2018.
Hsu C, Shen Y-C, Cheng C-C, Hong R-L, Chang C-J, Cheng A-L. Difference in the incidence trend of nasopharyngeal and oropharyngeal carcinomas in Taiwan: implication from age-period-cohort analysis. Cancer Epidemiol Biomarkers Prev. 2006;15:856–61.
Singapore Cancer Registry, 50 Years of Cancer Registration. Singapore Cancer Registry 50th Anniversary Monograph, 1968–2017. 2019.
Wei KR, Yu YL, Yang YY, Ji MF, Yu BH, Liang ZH, et al. Epidemiological trends of nasopharyngeal carcinoma in China. Asian Pac J Cancer Prev. 2010;11:29–32.
Jia W-H, Huang Qi-H, Liao J, Ye W, Shugart Yy, Liu Q, et al. Trends in incidence and mortality of nasopharyngeal carcinoma over a 20–25 year period (1978/1983–2002) in Sihui and Cangwu counties in southern China. BMC Cancer. 2006;6:178.
Tse LA, Yu IT-S, Mang OW-K, Wong S-L. Incidence rate trends of histological subtypes of nasopharyngeal carcinoma in Hong Kong. Br J Cancer. 2006;95:1269–73.
SEER, Surveillance, Epidemiology, and End Results (SEER) Program () SEER*Stat Database: Incidence - SEER Research Limited-Field Data, 9 Registries, Nov 2019 Sub (1975–2017) - Linked To County Attributes - Time Dependent (1990–2017) Income/Rurality, 1969–2017 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, released April 2020, based on the November 2019 submission. 2020a.
Argirion I, Zarins KR, Ruterbusch JJ, Vatanasapt P, Sriplung H, Seymour EK, et al. Increasing incidence of Epstein-Barr virus-related nasopharyngeal carcinoma in the United States. Cancer. 2020;126:121–30.
Klein G, Klein E, Kashuba E. Interaction of Epstein-Barr virus (EBV) with human B-lymphocytes. Biochem Biophys Res Commun. 2010;396:67–73.
The evaluation of carcinogenic risks to humans [monograph on the internet]. Volume 100B. Biological agents. 2012;1–475.
Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513:202–9.
Kangro HO, Osman HK, Lau YL, Heath RB, Yeung CY, Ng MH. Seroprevalence of antibodies to human herpesviruses in England and Hong Kong. J Med Virol. 1994;43:91–6.
Levine R, Zhu K, Gu Y, Brann E, Hall I, Caplan L, et al. Self-reported infectious mononucleosis and 6 cancers: a population-based, case-control study. Scand J Infect Dis. 1998;30:211–4.
Liu Z, Fang F, Chang ET, Adami H-O, Ye W. Sibship size, birth order and risk of nasopharyngeal carcinoma and infectious mononucleosis: a nationwide study in Sweden. Int J Epidemiol. 2016;45:825–34.
da Costa VG, Marques-Silva AC, Moreli ML. The Epstein-Barr virus latent membrane protein-1 (LMP1) 30-bp deletion and XhoI-polymorphism in nasopharyngeal carcinoma: a meta-analysis of observational studies. Syst Rev. 2015;4:46.
Xu M, Yao Y, Chen H, Zhang S, Cao Su-M, Zhang Z, et al. Genome sequencing analysis identifies Epstein-Barr virus subtypes associated with high risk of nasopharyngeal carcinoma. Nat Genet. 2019;51:1131–6.
Cui Q, Feng Fu-T, Xu M, Liu W-S, Yao Y-Y, Xie S-H, et al. Nasopharyngeal carcinoma risk prediction via salivary detection of host and Epstein-Barr virus genetic variants. Oncotarget. 2017;8:95066–74.
Coghill AE, Hsu W-L, Yang Qi, Wang C-P, Lou P-J, Yu KJ, et al. Elevated antibodies against Epstein-Barr virus among individuals predicted to carry nasopharyngeal carcinoma susceptibility variants. J Gen Virol. 2018;99:1268–73.
Pickard A, Chen C-J, Diehl SR, Liu M-Y, Cheng Yu-J, Hsu W-L, et al. Epstein-Barr virus seroreactivity among unaffected individuals within high-risk nasopharyngeal carcinoma families in Taiwan. Int J Cancer. 2004;111:117–23.
Qin H-De, Jia W-H, Zhang L-L, Liu Na, Zhou X-Xi, Wang M-H, et al. Elevated Epstein-Barr virus seroreactivity among unaffected members of families with nasopharyngeal carcinoma. J Med Virol. 2011;83:1792–8.
Hutajulu SH, Ng N, Jati BR, Fachiroh J, Herdini C, Hariwiyanto B, et al. Seroreactivity against Epstein-Barr virus (EBV) among first-degree relatives of sporadic EBV-associated nasopharyngeal carcinoma in Indonesia. J Med Virol. 2012;84:768–76.
Fogg MH, Wirth LJ, Posner M, Wang F. Decreased EBNA-1-specific CD8+ T cells in patients with Epstein-Barr virus-associated nasopharyngeal carcinoma. Proc Natl Acad Sci U S A. 2009;106:3318–23.
Chien Y-C, Chen J-Y, Liu M-Y, Yang H-I, Hsu M-M, Chen C-J, et al. Serologic markers of Epstein-Barr virus infection and nasopharyngeal carcinoma in Taiwanese men. N Engl J Med. 2001;345:1877–82.
Lanier A, Bender T, Talbot M, Wilmeth S, Tschopp C, Henle W, et al. Nasopharyngeal carcinoma in Alaskan Eskimos Indians, and Aleuts: a review of cases and study of Epstein-Barr virus, HLA, and environmental risk factors. Cancer. 1980;46:2100–6.
Zeng Y, Zhang LG, Wu YC, Huang YS, Huang NQ, Li JY, et al. Prospective studies on nasopharyngeal carcinoma in Epstein-Barr virus IgA/VCA antibody-positive persons in Wuzhou City, China. Int J Cancer. 1985;36:545–7.
Henle W, Ho HC, Henle G, Kwan HC. Antibodies to Epstein-Barr virus-related antigens in nasopharyngeal carcinoma. Comparison of active cases with long-term survivors. J Natl Cancer Inst. 1973;51:361–9.
de Schryver A, Klein G, Henle W, Henle G. EB virus-associated antibodies in Caucasian patients with carcinoma of the nasopharynx and in long-term survivors after treatment. Int J Cancer. 1974;13:319–25.
Ji M-F, Huang Qi-H, Yu X, Liu Z, Li X, Zhang Li-F, et al. Evaluation of plasma Epstein-Barr virus DNA load to distinguish nasopharyngeal carcinoma patients from healthy high-risk populations in Southern China. Cancer. 2014;120:1353–60.
Coghill AE, Bu W, Nguyen H, Hsu W-L, Yu KJ, Lou P-J, et al. High levels of antibody that neutralize B-cell infection of Epstein-Barr virus and that bind EBV gp350 are associated with a lower risk of nasopharyngeal carcinoma. Clin Cancer Res. 2016;22:3451–7.
Coghill AE, Bu W, Hsu W-L, Nguyen H, Yu KJ, Chien Y-C, et al. Evaluation of total and IgA-specific antibody targeting Epstein-Barr virus glycoprotein 350 and nasopharyngeal carcinoma risk. J Infect Dis. 2018;218:886–91.
Hording U, Nielsen HW, Daugaard S, Albeck H. Human papillomavirus types 11 and 16 detected in nasopharyngeal carcinomas by the polymerase chain reaction. Laryngoscope. 1994;104:99–102.
Lin Z, Khong B, Kwok S, Cao H, West RB, Le Q-T, et al. Human papillomavirus 16 detected in nasopharyngeal carcinomas in white Americans but not in endemic Southern Chinese patients. Head Neck. 2014;36:709–14.
Ye Y-F, Xiang YQ, Fang F, Gao R, Zhang LF, Xie SH, et al. Hepatitis B virus infection and risk of nasopharyngeal carcinoma in Southern China. Cancer Epidemiol Biomarkers Prev. 2015;24:1766–73.
Mahale P, Sturgis EM, Tweardy DJ, Ariza-Heredia EJ, Torres HA. Association between hepatitis C virus and head and neck cancers. J Natl Cancer Inst. 2016;108:djw035.
Shebl FM, Bhatia K, Engels EA. Salivary gland and nasopharyngeal cancers in individuals with acquired immunodeficiency syndrome in United States. Int J Cancer. 2010;126:2503–8.
Engels EA, Pfeiffer RM, Fraumeni JF, Kasiske BL, Israni AK, Snyder JJ, et al. Spectrum of cancer risk among US solid organ transplant recipients. JAMA. 2011;306:1891–901.
Huo Z, Li C, Xu X, Ge F, Wang R, Wen Y, et al. Cancer risks in solid organ transplant recipients: results from a comprehensive analysis of 72 cohort studies. Oncoimmunology. 2020;9:1848068.
Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet. 2007;370:59–67.
The evaluation of carcinogenic risks to humans [monograph on the Internet]. Volume 100E. Personal habits and indoor combustions. 2012;1–538.
Xue W-Q, Qin H-D, Ruan H-L, Shugart YY, Jia W-H. Quantitative association of tobacco smoking with the risk of nasopharyngeal carcinoma: a comprehensive meta-analysis of studies conducted between 1979 and 2011. Am J Epidemiol. 2013;178:325–38.
Long M, Fu Z, Li P, Nie Z. Cigarette smoking and the risk of nasopharyngeal carcinoma: a meta-analysis of epidemiological studies. BMJ Open. 2017;7:e016582.
Hsu W-L, Chien Y-C, Huang Y-T, Yu KJ, Ko J-Y, Lin C-Y, et al. Cigarette smoking increases the risk of nasopharyngeal carcinoma through the elevated level of IgA antibody against Epstein-Barr virus capsid antigen: a mediation analysis. Cancer Med. 2020;9:1867–76.
Hu T, Lin C-Y, Xie S-H, Chen G-H, Lu Yu-Q, Ling W, et al. Smoking can increase nasopharyngeal carcinoma risk by repeatedly reactivating Epstein-Barr Virus: an analysis of a prospective study in southern China. Cancer Med. 2019;8:2561–71.
Xu F-H, Xiong D, Xu Ya-F, Cao Su-M, Xue W-Q, Qin H-De, et al. An epidemiological and molecular study of the relationship between smoking, risk of nasopharyngeal carcinoma, and Epstein-Barr virus activation. J Natl Cancer Inst. 2012;104:1396–410.
Chang ET, Liu Z, Hildesheim A, Liu Q, Cai Y, Zhang Z, et al. Active and passive smoking and risk of nasopharyngeal carcinoma: a population-based case-control study in Southern China. Am J Epidemiol. 2017;185:1272–80.
Yang XR, Diehl S, Pfeiffer R, Chen CJ, Hsu WL, Dosemeci M, et al. Evaluation of risk factors for nasopharyngeal carcinoma in high-risk nasopharyngeal carcinoma families in Taiwan. Cancer Epidemiol Biomarkers Prev. 2005;14:900–5.
West S, Hildesheim A, Dosemeci M. Non-viral risk factors for nasopharyngeal carcinoma in the Philippines: results from a case-control study. Int J Cancer. 1993;55:722–7.
Fachiroh J, Sangrajrang S, Johansson M, Renard H, Gaborieau V, Chabrier A, et al. Tobacco consumption and genetic susceptibility to nasopharyngeal carcinoma (NPC) in Thailand. Cancer Causes Control. 2012;23:1995–2002.
Feng B-J, Khyatti M, Ben-Ayoub W, Dahmoul S, Ayad M, Maachi F, et al. Cannabis, tobacco and domestic fumes intake are associated with nasopharyngeal carcinoma in North Africa. Br J Cancer. 2009;101:1207–12.
Oudjehih M, Deltour I, Bouhidel ML, Bouhidel A, Marref A, Luzon V, et al. Smokeless tobacco use, cigarette smoking, and upper aerodigestive tract cancers: a case-control study in the Batna Region, Algeria, 2008–2011. Tob Use Insights. 2020;13:1179173x20902239.
Zheng Ym, Tuppin P, Hubert A, Jeannel D, Pan Yj, Zeng Y, et al. Environmental and dietary risk factors for nasopharyngeal carcinoma: a case-control study in Zangwu County, Guangxi, China. Br J Cancer. 1994;69:508–14.
Guo X, Johnson RC, Deng H, Liao J, Guan Li, Nelson GW, et al. Evaluation of nonviral risk factors for nasopharyngeal carcinoma in a high-risk population of Southern China. Int J Cancer. 2009;124:2942–7.
He Y-Q, Xue W-Q, Shen G-P, Tang L-L, Zeng Yi-X, Jia W-H. Household inhalants exposure and nasopharyngeal carcinoma risk: a large-scale case-control study in Guangdong, China. BMC Cancer. 2015;15:1022.
Adoga AA, Kokong DD, Nimkur TL, Ma'an ND. Environmental and life-style related risk factors for sinonasal and nasopharyngeal malignancies among a prospective cohort in Jos, Nigeria. Int J Otolaryngol. 2018;2018:8524861.
Jeannel D, Hubert A, De Vathaire F, Ellouz R, Camoun M, Ben Salem M, et al. Diet, living conditions and nasopharyngeal carcinoma in Tunisia–a case-control study. Int J Cancer. 1990;46:421–5.
Shanmugaratnam K, Tye CY, Goh EH, Chia KB. Etiological factors in nasopharyngeal carcinoma: a hospital-based, retrospective, case-control, questionnaire study. IARC Sci Publ. 1978;20:199–212.
Geser A, Charnay N, Day NE, de-The G, Ho HC. Environmental factors in the etiology of nasopharyngeal carcinoma: report on a case-control study in Hong Kong. IARC Sci Publ. 1978;20:213–29.
Yu MC, Ho JH, Lai SH, Henderson BE. Cantonese-style salted fish as a cause of nasopharyngeal carcinoma: report of a case-control study in Hong Kong. Cancer Res. 1986;46:956–61.
Yu MC, Mo CC, Chong WX, Yeh FS, Henderson BE. Preserved foods and nasopharyngeal carcinoma: a case-control study in Guangxi, China. Cancer Res. 1988;48:1954–9.
Yu MC, Garabrant DH, Huang T-Bo, Henderson BE. Occupational and other non-dietary risk factors for nasopharyngeal carcinoma in Guangzhou, China. Int J Cancer. 1990;45:1033–9.
Friborg JT, Yuan J-M, Wang R, Koh W-P, Lee H-P, Yu MC. Incense use and respiratory tract carcinomas: a prospective cohort study. Cancer. 2008;113:1676–84.
Chen Y, Chang ET, Liu Z, Liu Q, Cai Y, Zhang Z, et al. Residence characteristics and risk of nasopharyngeal carcinoma in southern China: a population-based case-control study. Environ Int. 2021;151:106455.
Fan H-C, Chen C-Y, Hsu Yi-C, Chou R-H, Teng C-LJ, Chiu C-H, et al. Increased risk of incident nasopharyngeal carcinoma with exposure to air pollution. PLoS One. 2018;13:e0204568.
Huang H-C, Tantoh DM, Hsu S-Yi, Nfor ON, Frank C-FL, Lung C-C, et al. Association between coarse particulate matter (PM10–2.5) and nasopharyngeal carcinoma among Taiwanese men. J Investig Med. 2020;68:419–24.
Yang T, Liu Y, Zhao W, Chen Z, Deng J. Association of ambient air pollution with nasopharyngeal carcinoma incidence in ten large Chinese cities, 2006–2013. Int J Environ Res Public Health. 2020;17:1824.
The evaluation of carcinogenic risks to humans [monograph on the Internet]. 1993;1–599.
Armstrong RW, Imrey PB, Lye MS, Armstrong MJ, Yu MC, Sani S. Nasopharyngeal carcinoma in Malaysian Chinese: salted fish and other dietary exposures. Int J Cancer. 1998;77:228–35.
Yuan J-M, Wang X-Li, Xiang Y-B, Gao Yu-T, Ross RK, Yu MC. Preserved foods in relation to risk of nasopharyngeal carcinoma in Shanghai, China. Int J Cancer. 2000;85:358–63.
Jia W-H, Luo X-Yu, Feng B-J, Ruan H-L, Bei J-X, Liu W-S, et al. Traditional Cantonese diet and nasopharyngeal carcinoma risk: a large-scale case-control study in Guangdong, China. BMC Cancer. 2010;10:446.
Gallicchio L, Matanoski G, Tao XG, Chen L, Lam TK, Boyd K, et al. Adulthood consumption of preserved and nonpreserved vegetables and the risk of nasopharyngeal carcinoma: a systematic review. Int J Cancer. 2006;119:1125–35.
Ning J-P, Yu MC, Wang Q-S, Henderson BE. Consumption of salted fish and other risk factors for nasopharyngeal carcinoma (NPC) in Tianjin, a low-risk region for NPC in the People's Republic of China. J Natl Cancer Inst. 1990;82:291–6.
Farrow DC, Vaughan TL, Berwick M, Lynch CF, Swanson GM, Lyon JL. Diet and nasopharyngeal cancer in a low-risk population. Int J Cancer. 1998;78:675–9.
Barrett D, Ploner A, Chang ET, Liu Z, Zhang C-X, Liu Q, et al. Past and recent salted fish and preserved food intakes are weakly associated with nasopharyngeal carcinoma risk in adults in Southern China. J Nutr. 2019;149:1596–605.
Yu MC, Huang TB, Henderson BE. Diet and nasopharyngeal carcinoma: a case-control study in Guangzhou, China. Int J Cancer. 1989;43:1077–82.
Liu Y-T, Dai J-J, Xu C-H, Lu Y-K, Fan Yu-Y, Zhang X-L, et al. Greater intake of fruit and vegetables is associated with lower risk of nasopharyngeal carcinoma in Chinese adults: a case-control study. Cancer Causes Control. 2012;23:589–99.
Polesel J, Serraino D, Negri E, Barzan L, Vaccher E, Montella M, et al. Consumption of fruit, vegetables, and other food groups and the risk of nasopharyngeal carcinoma. Cancer Causes Control. 2013;24:1157–65.
Feng XX, Wang MX, Li M, Tang X, Jiang H, Wang R, et al. Citrus fruit intake and the risk of nasopharyngeal carcinoma. Asia Pac J Clin Nutr. 2019;28:783–92.
Lee HP, Gourley L, Duffy SW, Esteve J, Lee J, Day NE. Preserved foods and nasopharyngeal carcinoma: a case-control study among Singapore Chinese. Int J Cancer. 1994;59:585–90.
Polesel J, Negri E, Serraino D, Parpinel M, Barzan L, Libra M, et al. Dietary intakes of carotenoids and other nutrients in the risk of nasopharyngeal carcinoma: a case-control study in Italy. Br J Cancer. 2012;107:1580–3.
Abe M, Shivappa N, Ito H, Oze I, Abe T, Shimizu Y, et al. Dietary inflammatory index and risk of upper aerodigestive tract cancer in Japanese adults. Oncotarget. 2018;9:24028–40.
Accardi G, Shivappa N, Di Maso M, Hébert JR, Fratino L, Montella M, et al. Dietary inflammatory index and cancer risk in the elderly: a pooled-analysis of Italian case-control studies. Nutrition. 2019;63–64:205–10.
Shivappa N, Hébert JR, Zucchetto A, Montella M, Libra M, Garavello W, et al. Increased risk of nasopharyngeal carcinoma with increasing levels of diet-associated inflammation in an Italian case-control study. Nutr Cancer. 2016;68:1123–30.
Edefonti V, Nicolussi F, Polesel J, Bravi F, Bosetti C, Garavello W, et al. Nutrient-based dietary patterns and nasopharyngeal cancer: evidence from an exploratory factor analysis. Br J Cancer. 2015;112:446–54.
Wang C, Lin X-L, Fan Yu-Y, Liu Y-T, Zhang X-L, Lu Y-K, et al. Diet quality scores and risk of nasopharyngeal carcinoma in Chinese adults: a case-control study. Nutrients. 2016;8:112.
Lo Y-Li, Pan W-H, Hsu W-L, Chien Y-C, Chen J-Y, Hsu M-M, et al. Partial least square discriminant analysis discovered a dietary pattern inversely associated with nasopharyngeal carcinoma risk. PLoS One. 2016;11:e0155892.
Turati F, Bravi F, Polesel J, Bosetti C, Negri E, Garavello W, et al. Adherence to the Mediterranean diet and nasopharyngeal cancer risk in Italy. Cancer Causes Control. 2017;28:89–95.
Huang TT, et al. Dietary patterns and risk of nasopharyngeal carcinoma: a population-based case-control study in southern China. Am J Clin Nutr.
Hildesheim A, West S, DeVeyra E, De Guzman MF, Jurado A, Jones C, et al. Herbal medicine use, Epstein-Barr virus, and risk of nasopharyngeal carcinoma. Cancer Res. 1992;52:3048–51.
Lin C, Cao Su-M, Chang ET, Liu Z, Cai Y, Zhang Z, et al. Chinese nonmedicinal herbal diet and risk of nasopharyngeal carcinoma: a population-based case-control study. Cancer. 2019;125:4462–70.
Zeng Y, Zhong JM, Mo YK, Miao XC. Epstein-Barr virus early antigen induction in Raji cells by Chinese medicinal herbs. Intervirology. 1983;19:201–4.
Chen L, Gallicchio L, Boyd-Lindsley K, Tao X, Robinson K, Lam TK, et al. Alcohol consumption and the risk of nasopharyngeal carcinoma: a systematic review. Nutr Cancer. 2009;61:1–15.
Du T, Chen K, Zheng S, Bao M, Huang Y, Wu K. Association between alcohol consumption and risk of nasopharyngeal carcinoma: a comprehensive meta-analysis of epidemiological studies. Alcohol Clin Exp Res. 2019;43:2262–73.
Friborg JT, Yuan J-M, Wang R, Koh W-P, Lee H-P, Yu MC. A prospective study of tobacco and alcohol use as risk factors for pharyngeal carcinomas in Singapore Chinese. Cancer. 2007;109:1183–91.
Li W, Ray RM, Gao DL, Fitzgibbons ED, Seixas NS, Camp JE, et al. Occupational risk factors for nasopharyngeal cancer among female textile workers in Shanghai, China. Occup Environ Med. 2006;63:39–44.
Feng R, Chang ET, Liu Q, Cai Y, Zhang Z, Chen G, et al. Intake of alcohol and tea and risk of nasopharyngeal carcinoma: a population- based case-control study in southern China. Cancer Epidemiol Biomarkers Prev. 2021;30:545–53.
Hsu W-L, Pan W-H, Chien Y-C, Yu KJ, Cheng Yu-J, Chen J-Y, et al. Lowered risk of nasopharyngeal carcinoma and intake of plant vitamin, fresh fish, green tea and coffee: a case-control study in Taiwan. PLoS One. 2012;7:e41779.
Ruan H-L, Xu F-H, Liu W-S, Feng Qi-S, Chen Li-Z, Zeng Yi-X, et al. Alcohol and tea consumption in relation to the risk of nasopharyngeal carcinoma in Guangdong, China. Front Med China. 2010;4:448–56.
Chung SD, Wu CS, Lin HC, Hung SH. Association between allergic rhinitis and nasopharyngeal carcinoma: a population-based study. Laryngoscope. 2014;124:1744–9.
Lin C, Lin S-W, Weng S-F, Lin Y-S. Subsequent risk of nasopharyngeal carcinoma among patients with allergic rhinitis: a nationwide population-based cohort study. Head Neck. 2014;37:413–7.
Hung SH, Chen PY, Lin HC, Ting J, Chung SD. Association of rhinosinusitis with nasopharyngeal carcinoma: a population-based study. Laryngoscope. 2014;124:1515–20.
Yuan J-M, Wang X-Li, Xiang Y-B, Gao Yu-T, Ross RK, Yu MC. Non-dietary risk factors for nasopharyngeal carcinoma in Shanghai, China. Int J Cancer. 2000;85:364–9.
Beachler DC, Engels EA. Chronic sinusitis and risk of head and neck cancer in the US elderly population. JAMA Otolaryngol Head Neck Surg. 2017;143:25–31.
Wu EL, Riley CA, Hsieh M-C, Marino MJ, Wu X-C, McCoul ED. Chronic sinonasal tract inflammation as a precursor to nasopharyngeal carcinoma and sinonasal malignancy in the United States. Int Forum Allergy Rhinol. 2017;7:786–93.
Huang W-Y, Lin C-C, Jen Y-M, Lin K-T, Yang M-H, Chen C-M, et al. Association between adult otitis media and nasopharyngeal cancer: a nationwide population-based cohort study. Radiother Oncol. 2012;104:338–42.
Kim HJ, Ahn HS, Kang T, Bachert C, Song W-J. Nasal polyps and future risk of head and neck cancer: a nationwide population-based cohort study. J Allergy Clin Immunol. 2019;144:1004–10.
Xiao X, Zhang Z, Chang ET, Liu Z, Liu Q, Cai Y, et al. Medical history, medication use, and risk of nasopharyngeal carcinoma. Am J Epidemiol. 2018;187:2117–25.
Huang Po-W, Chiou Yi-R, Wu S-L, Liu Ju-C, Chiou K-R. Risk of nasopharyngeal carcinoma in patients with chronic rhinosinusitis: a nationwide propensity score matched study in Taiwan. Asia Pac J Clin Oncol. 2020.
Liu Z, Chang ET, Liu Q, Cai Y, Zhang Z, Chen G, et al. Oral hygiene and risk of nasopharyngeal carcinoma-a population-based case-control study in China. Cancer Epidemiol Biomarkers Prev. 2016;25:1201–7.
Debelius JW, Huang T, Cai Y, Ploner A, Barrett D, Zhou X, et al. Subspecies niche specialization in the oral microbiome is associated with nasopharyngeal carcinoma risk. mSystems. 2020;5:e00065–20.
Tseng K-S, Lin C, Lin Y-S, Weng S-F. Risk of head and neck cancer in patients with diabetes mellitus: a retrospective cohort study in Taiwan. JAMA Otolaryngol Head Neck Surg. 2014;140:746–53.
Peng Y-S, Lin Jr-R, Cheng Bi-H, Ho C, Lin Y-H, Shen C-H, et al. Incidence and relative risk for developing cancers in women with gestational diabetes mellitus: a nationwide cohort study in Taiwan. BMJ Open. 2019;9:e024583.
Zucchetto A, Taborelli M, Bosetti C, Montella M, La Vecchia C, Franchin G, et al. Metabolic disorders and the risk of nasopharyngeal carcinoma: a case-control study in Italy. Eur J Cancer Prev. 2018;27:180–3.
Hsieh S-H, Chiou W-Ko, Wang M-H, Lin J-D. Association of body weight with the risk for malignancies in hospitalized patients with or without diabetes mellitus in Taiwan. J Investig Med. 2014;62:37–42.
Yen Y-C, Lin C, Lin S-W, Lin Y-S, Weng S-F. Effect of metformin on the incidence of head and neck cancer in diabetics. Head Neck. 2015;37:1268–73.
Tseng CH. Metformin and risk of developing nasopharyngeal cancer in patients with type 2 diabetes mellitus. Metabolism. 2018;85:223–6.
The evaluation of carcinogenic risks to humans [monograph on the Internet]. 2012;1–599.
The evaluation of carcinogenic risks to humans [monograph on the Internet]. 2012;1–501.
ECHA, Substance Evaluation Conclusion as required by REACH Article 48 and Evaluation Report for Formaldehyde, EC No 200-001-8, CAS No 50-00-0. 2019.
Swenberg JA, Kerns WD, Mitchell RI, Gralla EJ, Pavkov KL. Induction of squamous cell carcinomas of the rat nasal cavity by inhalation exposure to formaldehyde vapor. Cancer Res. 1980;40:3398–402.
Albert RE, Sellakumar AR, Laskin S, Kuschner M, Nelson N, Snyder CA. Gaseous formaldehyde and hydrogen chloride induction of nasal cancer in the rat. J Natl Cancer Inst. 1982;68:597–603.
Armstrong RW, Imrey PB, Lye MS, Armstrong MJ, Yu MC, Sani S. Nasopharyngeal carcinoma in Malaysian Chinese: occupational exposures to particles, formaldehyde and heat. Int J Epidemiol. 2000;29:991–8.
Xie S-H, Yu IT-S, Tse LAh, Au JSK, Lau JSM. Occupational risk factors for nasopharyngeal carcinoma in Hong Kong Chinese: a case-referent study. Int Arch Occup Environ Health. 2017;90:443–9.
Hildesheim A, Dosemeci M, Chan CC, Chen CJ, Cheng YJ, Hsu MM, et al. Occupational exposure to wood, formaldehyde, and solvents and risk of nasopharyngeal carcinoma. Cancer Epidemiol Biomarkers Prev. 2001;10:1145–53.
Bachand AM, Mundt KA, Mundt DJ, Montgomery RR. Epidemiological studies of formaldehyde exposure and risk of leukemia and nasopharyngeal cancer: a meta-analysis. Crit Rev Toxicol. 2010;40:85–100.
Siew SS, Kauppinen T, Kyyrönen P, Heikkila P, Pukkala E. Occupational exposure to wood dust and formaldehyde and risk of nasal, nasopharyngeal, and lung cancer among Finnish men. Cancer Manag Res. 2012;4:223–32.
Meyers AR, Pinkerton LE, Hein MJ. Cohort mortality study of garment industry workers exposed to formaldehyde: update and internal comparisons. Am J Ind Med. 2013;56:1027–39.
Sernia S, Di Folco F, Altrudo P, Sbriccoli B, Sestili C, Colamesta V, et al. [Risk of nasopharyngeal cancer, leukemia and other tumors in a cohort of employees and students potentially exposed to (FA) formaldehyde in university laboratories]. Clin Ter. 2016;167:43–7.
Siew SS, Martinsen JI, Kjaerheim K, Sparén P, Tryggvadottir L, Weiderpass E, et al. Occupational exposure to wood dust and risk of nasal and nasopharyngeal cancer: a case-control study among men in four nordic countries-With an emphasis on nasal adenocarcinoma. Int J Cancer. 2017;141:2430–6.
Pira E, Romano C, Verga F, La Vecchia C. Mortality from lymphohematopoietic neoplasms and other causes in a cohort of laminated plastic workers exposed to formaldehyde. Cancer Causes Control. 2014;25:1343–9.
Chen YF, Chang ET, Liu Q, Cai Y, Zhang Z, Chen G, et al. Occupational exposures and risk of nasopharyngeal carcinoma in a high-risk area: a population-based case-control study. Cancer. 2021.
Blair A, Stewart P, O'Berg M, Gaffey W, Walrath J, Ward J, et al. Mortality among industrial workers exposed to formaldehyde. J Natl Cancer Inst. 1986;76:1071–84.
Hauptmann M, Lubin JH, Stewart PA, Hayes RB, Blair A. Mortality from solid cancers among workers in formaldehyde industries. Am J Epidemiol. 2004;159:1117–30.
Beane Freeman LE, Blair A, Lubin JH, Stewart PA, Hayes RB, Hoover RN, et al. Mortality from solid tumors among workers in formaldehyde industries: an update of the NCI cohort. Am J Ind Med. 2013;56:1015–26.
Marsh GM, Morfeld P, Zimmerman SD, Liu Y, Balmert LC. An updated re-analysis of the mortality risk from nasopharyngeal cancer in the National Cancer Institute formaldehyde worker cohort study. J Occup Med Toxicol. 2016;11:8.
Marsh GM, Morfeld P, Collins JJ, Symons J. Issues of methods and interpretation in the National Cancer Institute formaldehyde cohort study. J Occup Med Toxicol. 2014;9:22.
Möhner M, Liu Y, Marsh GM. New insights into the mortality risk from nasopharyngeal cancer in the National Cancer Institute formaldehyde worker cohort study. J Occup Med Toxicol. 2019;14:4.
Möhner M, Wendt A. A diagnostic bias might be a much simpler explanation for the apparently elevated risk for nasopharyngeal cancer with respect to formaldehyde. J Occup Med Toxicol. 2016;11:54.
Beigzadeh Z, Pourhassan B, kalantary S, Golbabaei F. Occupational exposure to wood dust and risk of nasopharyngeal cancer: a systematic review and meta-analysis. Environ Res. 2019;171:170–6.
E M, Yin J, Jin W, Mao Y, Wu Q, Qiu J. Wood dust exposure and risks of nasopharyngeal carcinoma: a meta-analysis. Eur J Public Health. 2020;30:817–22.
Ng TP. A case-referent study of cancer of the nasal cavity and sinuses in Hong Kong. Int J Epidemiol. 1986;15:171–5.
Zheng W, McLaughlin JK, Gao YT, Gao RN, Blot WJ. Occupational risks for nasopharyngeal cancer in Shanghai. J Occup Med. 1992;34:1004–7.
Zeng YX, Jia WH. Familial nasopharyngeal carcinoma. Semin Cancer Biol. 2002;12:443–50.
Bei JX, Jia WH, Zeng YX. Familial and large-scale case-control studies identify genes associated with nasopharyngeal carcinoma. Semin Cancer Biol. 2012;22:96–106.
Friborg J, Wohlfahrt J, Koch A, Storm H, Olsen OR, Melbye M. Cancer susceptibility in nasopharyngeal carcinoma families–a population-based cohort study. Cancer Res. 2005;65:8567–72.
Jia W-H, Feng B-J, Xu Z-Li, Zhang X-S, Huang P, Huang Li-Xi, et al. Familial risk and clustering of nasopharyngeal carcinoma in Guangdong. Cancer. 2004;101:363–9.
Yu KJ, Hsu W-L, Chiang C-Ju, Cheng Yu-J, Pfeiffer RM, Diehl SR, et al. Cancer patterns in nasopharyngeal carcinoma multiplex families in Taiwan. Int J Cancer. 2009;124:1622–5.
Liu Z, Chang ET, Liu Q, Cai Y, Zhang Z, Chen G, et al. Quantification of familial risk of nasopharyngeal carcinoma in a high-incidence area. Cancer. 2017;123:2716–25.
Jia W-H, Collins A, Zeng Yi-X, Feng B-J, Yu X-J, Huang Li-Xi, et al. Complex segregation analysis of nasopharyngeal carcinoma in Guangdong, China: evidence for a multifactorial mode of inheritance (complex segregation analysis of NPC in China). Eur J Hum Genet. 2005;13:248–52.
Lu S-J, Day NE, Degos L, Lepage V, Wang P-C, Chan So-Ha, et al. Linkage of a nasopharyngeal carcinoma susceptibility locus to the HLA region. Nature. 1990;346:470–1.
Feng B-J, Huang W, Shugart YY, Lee MK, Zhang F, Xia J-C, et al. Genome-wide scan for familial nasopharyngeal carcinoma reveals evidence of linkage to chromosome 4. Nat Genet. 2002;31:395–9.
Xiong W, Zeng ZY, Xia JH, Xia K, Shen SR, Li XL, et al. A susceptibility locus at chromosome 3p21 linked to familial nasopharyngeal carcinoma. Cancer Res. 2004;64:1972–4.
Hu Li-Fu, Qiu Q-H, Fu S-M, Sun Di, Magnusson K, He B, et al. A genome-wide scan suggests a susceptibility locus on 5p 13 for nasopharyngeal carcinoma. Eur J Hum Genet. 2008;16:343–9.
Dai J, Shen W, Wen W, Chang J, Wang T, Chen H, et al. Estimation of heritability for nine common cancers using data from genome-wide association studies in Chinese population. Int J Cancer. 2017;140:329–36.
Bei J-X, Li Yi, Jia W-H, Feng B-J, Zhou G, Chen Li-Z, et al. A genome-wide association study of nasopharyngeal carcinoma identifies three new susceptibility loci. Nat Genet. 2010;42:599–603.
Ng CC, Yew PY, Puah SM, Krishnan G, Yap LF, Teo SH, et al. A genome-wide association study identifies ITGA9 conferring risk of nasopharyngeal carcinoma. J Hum Genet. 2009;54:392–7.
Tang M, Lautenberger JA, Gao X, Sezgin E, Hendrickson SL, Troyer JL, et al. The principal genetic determinants for nasopharyngeal carcinoma in China involve the HLA class I antigen recognition groove. PLoS Genet. 2012;8:e1003103.
Tse Ka-Po, Su W-H, Chang K-P, Tsang N-M, Yu C-J, Tang P, et al. Genome-wide association study reveals multiple nasopharyngeal carcinoma-associated loci within the HLA region at chromosome 6p21.3. Am J Hum Genet. 2009;85:194–203.
Chin YM, Mushiroda T, Takahashi A, Kubo M, Krishnan G, Yap L-F, et al. HLA-A SNPs and amino acid variants are associated with nasopharyngeal carcinoma in Malaysian Chinese. Int J Cancer. 2015;136:678–87.
Cui Q, Feng Qi-S, Mo H-Y, Sun J, Xia Y-F, Zhang H, et al. An extended genome-wide association study identifies novel susceptibility loci for nasopharyngeal carcinoma. Hum Mol Genet. 2016;25:3626–34.
Simons MJ, Chan SH, Wee GB, Shanmugaratnam K, Goh EH, Ho JH, et al. Nasopharyngeal carcinoma and histocompatibility antigens. IARC Sci Publ. 1978;20:271–82.
Simons MJ, Day NE, Wee GB, Shanmugaratnam K, Ho HC, Wong SH, et al. Nasopharyngeal carcinoma V: immunogenetic studies of Southeast Asian ethnic groups with high and low risk for the tumor. Cancer Res. 1974;34:1192–5.
Goldsmith DB, West TM, Morton R. HLA associations with nasopharyngeal carcinoma in Southern Chinese: a meta-analysis. Clin Otolaryngol Allied Sci. 2002;27:61–7.
Hildesheim A, Wang CP. Genetic predisposition factors and nasopharyngeal carcinoma risk: a review of epidemiological association studies, 2000–2011: Rosetta Stone for NPC: genetics, viral infection, and other environmental factors. Semin Cancer Biol. 2012;22:107–16.
Yang H, Yu K, Zhang R, Li J, Wei X, Zhang Y, et al. The HLA-DRB1 allele polymorphisms and nasopharyngeal carcinoma. Tumour Biol. 2016;37:7119–28.
Wang T-M, Zhou T, He Y-Q, Xue W-Q, Zhang J-Bo, Zheng X-H, et al. Fine-mapping of HLA class I and class II genes identified two independent novel variants associated with nasopharyngeal carcinoma susceptibility. Cancer Med. 2018;7:6308–16.
Liu Z, Derkach A, Yu KJ, Yeager M, Chang YS, Chen CJ, et al. Patterns of human leukocyte antigen class I and class II associations and cancer. Cancer Res. 2020;81:1148–52.
Ioannidis JP. The mass production of redundant, misleading, and conflicted systematic reviews and meta-analyses. Milbank Q. 2016;94:485–514.
Zhao Y, Wang Y, Wu X, Wang J, Zhang L, Jia Y, et al. Quantitative assessment of the association between glutathione S-transferase M1 polymorphism and the risk of developing nasopharyngeal cancer. Oncol Lett. 2016;11:373–8.
Liu RR, Chen J-C, Li M-D, Li T, Tan Y, Zhang M. A meta-analysis of glutathione S-transferase M1 and T1 genetic polymorphism in relation to susceptibility to nasopharyngeal carcinoma. Int J Clin Exp Med. 2015;8:10626–32.
Yao K, Qin H, Gong L, Zhang R, Li L. CYP2E1 polymorphisms and nasopharyngeal carcinoma risk: a meta-analysis. Eur Arch Otorhinolaryngol. 2017;274:253–9.
Lin J, Ye Q, Wang Y, Wang Y, Zeng Y. Association between XRCC1 single-nucleotide polymorphisms and susceptibility to nasopharyngeal carcinoma: an update meta-analysis. Medicine. 2018;97:e11852.
Cui Q, Zuo X-Yu, Lian Yi-F, Feng Qi-S, Xia Y-F, He C-Y, et al. Association between XRCC3 Thr241Met polymorphism and nasopharyngeal carcinoma risk: evidence from a large-scale case-control study and a meta-analysis. Tumour Biol. 2016;37:14825–30.
Sahu SK, Chakrabarti S, Roy SD, Baishya N, Reddy RR, Suklabaidya S, et al. Association of p53 codon72 Arg>Pro polymorphism with susceptibility to nasopharyngeal carcinoma: evidence from a case-control study and meta-analysis. Oncogenesis. 2016;5:e225.
Li Z, Ge H, Xie Y-G, Xie G-Y, Lv C. Matrix metalloproteinase-1 (MMP1) polymorphism is associated with lowered risk of nasopharyngeal carcinoma in Asian population. Cell Biochem Biophys. 2015;71:999–1004.
Li Q, Ma C, Zhang Z, Chen S, Zhi W, Zhang L, et al. Association between cyclooxygenase-2 (COX-2) 8473 T > C polymorphism and cancer risk: a meta-analysis and trial sequential analysis. BMC Cancer. 2018;18:847.
Li L, Zhang ZT. Genetic association between NFKBIA and NFKB1 gene polymorphisms and the susceptibility to head and neck cancer: a meta-analysis. Dis Markers. 2019;2019:6523837.
Lee MH, Huang Y-H, Coghill AE, Liu Z, Yu KJ, Hsu W-L, et al. Epstein-Barr virus (EBV) based nasopharyngeal carcinoma (NPC) risk prediction scores are elevated in NPC multiplex family members compared to the general population in Taiwan. J Infect Dis. 2021;223:441–4.
Chen H, Chen S, Lu J, Wang X, Li J, Li L, et al. Multiparametric detection of antibodies against different EBV antigens to predict risk for nasopharyngeal carcinoma in a high-risk population of China. Cancer Prev Res. 2017;10:542–50.
Chen GH, Liu Z, Ji M-F, Pfeiffer RM, Huang Q-H, Lu Y-Q, et al. Prospective assessment of a nasopharyngeal carcinoma risk score in a population undergoing screening. Int J Cancer. 2020.
Chan KCA, Woo JKS, King A, Zee BCY, Lam WKJ, Chan SL, et al. Analysis of plasma Epstein-Barr virus DNA to screen for nasopharyngeal cancer. N Engl J Med. 2017;377:513–22.