Abstract
Purpose
The effect of fruit and vegetable intake on the risk of nasopharyngeal carcinoma (NPC) remains uncertain due to limited published evidence. We performed a matched case–control study to investigate the relationship between the intake of fruit and vegetables and the risk of NPC.
Methods
Between July 2009 and March 2011, 600 (448 male, 152 female), NPC incident cases from a single hospital in Guangzhou, Guangdong Province, China, a high-incidence area, were enrolled in the study. 600 controls, matched by gender, age (±3 years) and household type (urban/rural) were also enrolled. Face-to-face interviews were used to collect habitual dietary intakes and information on various covariates.
Results
Multivariate conditional logistic regression analyses showed significant, dose-dependent inverse associations between the intake of vegetables, fruit or a combination of the two and the risk of NPC, even after adjustments for social-economic status, body mass index, dietary factors and other potential covariates. The adjusted odds ratios (95% confidence intervals) for NPC in the top quartile of vegetable intake, fruit intake or a combination of the two, as compared to the lowest quartile, were 0.33 (0.22–0.50), 0.70 (0.47–1.04) and 0.37 (0.25–0.55), respectively. Dark green leafy vegetables, carrots, peppers and tomatoes, citrus fruit and pome fruit showed much more pronounced benefits with regards to NPC than other types of fruit and vegetables. Interaction analyses demonstrated that the effects of total combined vegetable and fruit intake were much more significant in subjects with a higher education level (p interaction: 0.027), and the benefits of fruit were observed in males, but not in females (p interaction: 0.088).
Conclusion
Our findings suggest that a greater consumption of fruit and vegetables may lower the risk of NPC in Chinese adults.
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Abbreviations
- BMI:
-
Body mass index
- CI:
-
Confidence interval
- EB virus:
-
Epstein–Barr virus
- NPC:
-
Nasopharyngeal carcinoma
- OR:
-
Odds ratio
- FFQ:
-
Food frequency questionnaire
- TNM stages:
-
Tumor-lymph-node-metastasis stages
- UICC/AJCC:
-
International Union Against Cancer/American Joint Committee on Cancer
- VCA-IgA:
-
Viral capsid antigen antibody A
- EA-IgA:
-
Early antigen antibody A
- SD:
-
Standard deviation
- MET:
-
Metabolic equivalent
References
Curado MP, Edwards B, Shin HR et al. (2007) Cancer incidence in five continents, Vol. IX IARC Sci Publ No 160, IARC, Lyon
GLOBOCAN 2008 (2010) Cancer incidence and mortality worldwide: IARC cancer base no. 10 [Internet]. http://globocan.iarc.fr
Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74–108
Jia WH, Huang QH, Liao J, Ye W, Shugart YY (2006) 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 6:178
Chang ET, Adami HO (2006) The enigmatic epidemiology of nasopharyngeal carcinoma. Cancer Epidemiol Biomarkers Prev 15:1765–1777
WCRF/AICR (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington, DC
Gallicchio L, Matanoski G, Tao XG et al (2006) Adulthood consumption of preserved and non preserved vegetables and the risk of nasopharyngeal carcinoma: a systematic review. Int J Cancer 119:1125–1135
Jia WH, Luo XY, Feng BJ et al (2010) Traditional Cantonese diet and nasopharyngeal carcinoma risk: a large-scale case-control study in Guangdong, China. BMC Cancer 10:446. doi:10.1186/1471-2407-10-446
Armstrong RW, Imrey PB, Lye MS, Armstrong MJ, Yu MC, Sani S (1998) Nasopharyngeal carcinoma in Malaysian Chinese: salted fish and other dietary exposures. Int J Cancer 77:228–235
Chen DL, Huang TB (1997) A case-control study of risk factors of nasopharyngeal carcinoma. Cancer Lett 117:17–22
Farrow DC, Vaughan TL, Berwick M, Lynch CF, Swanson GM, Lyon JL (1998) Diet and nasopharyngeal cancer in a low-risk population. Int J Cancer 78:675–679
Zheng YM, Tuppin P, Hubert A et al (1994) Environmental and dietary risk factors for nasopharyngeal carcinoma: a case-control study in Zangwu County, Guangxi, China. Br J Cancer 69:508–514
Yu MC, Mo CC, Chong WX, Yeh FS, Henderson BE (1988) Preserved foods and nasopharyngeal carcinoma: a case-control study in Guangxi, China. Cancer Res 48:1954–1959
Yuan JM, Wang XL, Xiang YB, Gao YT, Ross RK, Yu MC (2000) Preserved foods in relation to risk of nasopharyngeal carcinoma in Shanghai, China. Int J Cancer 85:358–363
Huang ZB, Jiang YM, Fang YM (2002) An epidemiological study on risk factors of nasopharyngeal carcinoma in Guangxi province. Industrial Health and Occupational Diseases 28:193–196
Yu MC, Huang TB, Henderson BE (1989) Diet and nasopharyngeal carcinoma: a case-control study in Guangzhou, China. Int J Cancer 43:1077–1082
Cai L, Yi YN (1996) A matched study with various controls in nasopharyngeal carcinoma epidemiology in Fujian province. J Fujian Med Coll 30:199–202
Ning JP, Yu MC, Wang QS, Henderson BE (1990) 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 82:291–296
Yan L, Xi Z, Drettner B (1989) Epidemiological studies of nasopharyngeal cancer in the Guangzhou area, China. Preliminary report. Acta Otolaryngol 107:424–427
Zou JM, Sun QF, Yuan YL et al (1999) A case-control study of nasopharyngeal carcinoma among inhabitants in high background radiation areas of Yangjinag, China. Chin J Radiat Mediat Prot 19:90–94
Koo LC, Mang OW, Ho JH (1997) An ecological study of trends in cancer incidence and dietary changes in Hong Kong. Nutr Cancer 28:289–301
Ward MH, Pan WH, Cheng YJ et al (2000) Dietary exposure to nitrite and nitrosamines and risk of nasopharyngeal carcinoma in Taiwan. Int J Cancer 86:603–609
Feng BJ, Jalbout M, Ayoub WB et al (2007) Dietary risk factors for nasopharyngeal carcinoma in Maghrebian countries. Int J Cancer 121:1550–1555
Willett W (1998) Nutritional epidemiology, 2nd edn. Oxford Universtiy Press Inc., New York
Gonzalez CA, Pera G, Agudo A et al (2006) Fruit and vegetable intake and the risk of stomach and oesophagus adenocarcinoma in the European prospective investigation into cancer and nutrition (EPIC-EURGAST). Int J Cancer 118:2559–2566. doi:10.1002/ijc.21678
Kjaerheim K, Gaard M, Andersen A (1998) The role of alcohol, tobacco, and dietary factors in upper aerogastric tract cancers: a prospective study of 10,900 Norwegian men. Cancer Causes Control 9:99–108
Tran GD, Sun XD, Abnet CC et al (2005) Prospective study of risk factors for esophageal and gastric cancers in the Linxian general population trial cohort in China. Int J Cancer 113:456–463. doi:10.1002/ijc.20616
Smith-Warner SA, Spiegelman D, Yaun SS et al (2003) Fruits, vegetables and lung cancer: a pooled analysis of cohort studies. Int J Cancer 107:1001–1011. doi:10.1002/ijc.11490
Mao YP, Xie FY, Liu LZ et al (2009) Re-evaluation of 6th edition of AJCC staging system for nasopharyngeal carcinoma and proposed improvement based on magnetic resonance imaging. Int J Radiat Oncol Biol Phys 73:1326–1334. doi:10.1016/j.ijrobp.2008.07.062
Zhang CX, Ho SC (2009) Validity and reproducibility of a food frequency questionnaire among Chinese women in Guangdong province. Asia Pac J Clin Nutr 18:240–250
Yang Y, Wang G, X. P (2002) China food composition tables 2002. Peking University Medical Press, Beijing
Nyberg F, Hou SM, Pershagen G, Lambert B (2003) Dietary fruit and vegetables protect against somatic mutation in vivo, but low or high intake of carotenoids does not. Carcinogenesis 24:689–696
Wettasinghe M, Bolling B, Plhak L, Parkin K (2002) Screening for phase II enzyme-inducing and antioxidant activities of common vegetables. J Food Sci 67:2583–2588. doi:10.1111/j.1365-2621.2002.tb08781.x
Xiao D, Vogel V, Singh SV (2006) Benzyl isothiocyanate-induced apoptosis in human breast cancer cells is initiated by reactive oxygen species and regulated by Bax and Bak. Mol Cancer Ther 5:2931–2945. doi:10.1158/1535-7163.MCT-06-0396
Million K, Tournier F, Houcine O, Ancian P, Reichert U, Marano F (2001) Effects of retinoic acid receptor-selective agonists on human nasal epithelial cell differentiation. Am J Respir Cell Mol Biol 25:744–750
Arrigoni O, De Tullio MC (2002) Ascorbic acid: much more than just an antioxidant. Biochim Biophys Acta 1569:1–9. doi:S0304416501002355
Baumeister P, Huebner T, Reiter M, Schwenk-Zieger S, Harreus U (2009) Reduction of oxidative DNA fragmentation by ascorbic acid, zinc and N-acetylcysteine in nasal mucosa tissue cultures. Anticancer Res 29:4571–4574. doi:29/11/4571
Iwase Y, Takemura Y, Ju-ichi M et al (2000) Inhibitory effect of flavonoids from citrus plants on Epstein-Barr virus activation and two-stage carcinogenesis of skin tumors. Cancer Lett 154:101–105. doi:S0304-3835(00)00386-4
Kuo CL, Wu SY, Ip SW et al (2011) Apoptotic death in curcumin-treated NPC-TW 076 human nasopharyngeal carcinoma cells is mediated through the ROS, mitochondrial depolarization and caspase-3-dependent signaling responses. Int J Oncol 39:319–328. doi:10.3892/ijo.2011.1057
Huang TT, Lin HC, Chen CC et al (2010) Resveratrol induces apoptosis of human nasopharyngeal carcinoma cells via activation of multiple apoptotic pathways. J Cell Physiol 226:720–728. doi:10.1002/jcp.22391
Uzcudun AE, Retolaza IR, Fernandez PB et al (2002) Nutrition and pharyngeal cancer: results from a case-control study in Spain. Head Neck 24:830–840. doi:10.1002/hed.10142
Scagliusi FB, Ferriolli E, Pfrimer K et al (2008) Underreporting of energy intake in Brazilian women varies according to dietary assessment: a cross-sectional study using doubly labeled water. J Am Diet Assoc 108:2031–2040. doi:S0002-8223(08)01732-X
Stelmach W, Kaczmarczyk-Chalas K, Bielecki W, Drygas W (2004) The impact of income, education and health on lifestyle in a large urban population of Poland (Cindi programme). Int J Occup Med Environ Health 17:393–401
Shi L (1998) Sociodemographic characteristics and individual health behaviors. South Med J 91:933–941
Dorgan JF, Ziegler RG, Schoenberg JB et al (1993) Race and sex differences in associations of vegetables, fruits, and carotenoids with lung cancer risk in New Jersey (United States). Cancer Causes Control 4:273–281
Tse KP, Su WH, Yang ML et al (2011) A gender-specific association of CNV at 6p21.3 with NPC susceptibility. Hum Mol Genet 20:2889–2896. doi:10.1093/hmg/ddr191
Tian W, Zeng XM, Li LX et al (2006) Gender-specific associations between MICA-STR and nasopharyngeal carcinoma in a southern Chinese Han population. Immunogenetics 58:113–121. doi:10.1007/s00251-006-0093-6
Lampe JW, Fredstrom SB, Slavin JL, Potter JD (1993) Sex differences in colonic function: a randomised trial. Gut 34:531–536
IdS Silva (1999) Cancer epidemiology: principles and methods. IARC, Lyon
Chen YM, Ho SC, Woo JL (2006) Greater fruit and vegetable intake is associated with increased bone mass among postmenopausal Chinese women. Br J Nutr 96:745–751. doi:S000711450600287X
Macdonald HM, New SA, Reid DM (2005) Longitudinal changes in dietary intake in Scottish women around the menopause: changes in dietary pattern result in minor changes in nutrient intake. Public Health Nutr 8:409–416
Acknowledgments
We are grateful for the help from the doctors and nurses in two university affiliated hospitals (the Cancer Center and Ophthalmic Center) of Sun Yat-sen University for facilitating the recruitment and interviews. This study was supported by the 5010 Program for Clinical Researches of Sun Yat-sen University, Guangzhou, People’s Republic of China.
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The authors declare that they have no conflict of interest.
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Liu, Yt., Dai, Jj., Xu, Ch. 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 23, 589–599 (2012). https://doi.org/10.1007/s10552-012-9923-z
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DOI: https://doi.org/10.1007/s10552-012-9923-z