Skip to main content

Advertisement

Log in

Greater intake of fruit and vegetables is associated with lower risk of nasopharyngeal carcinoma in Chinese adults: a case–control study

  • Original paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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

  1. Curado MP, Edwards B, Shin HR et al. (2007) Cancer incidence in five continents, Vol. IX IARC Sci Publ No 160, IARC, Lyon

  2. GLOBOCAN 2008 (2010) Cancer incidence and mortality worldwide: IARC cancer base no. 10 [Internet]. http://globocan.iarc.fr

  3. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74–108

    Article  PubMed  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. Chang ET, Adami HO (2006) The enigmatic epidemiology of nasopharyngeal carcinoma. Cancer Epidemiol Biomarkers Prev 15:1765–1777

    Article  PubMed  CAS  Google Scholar 

  6. WCRF/AICR (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington, DC

    Google Scholar 

  7. 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

    Article  PubMed  CAS  Google Scholar 

  8. 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

    Article  PubMed  Google Scholar 

  9. 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

    Article  PubMed  CAS  Google Scholar 

  10. Chen DL, Huang TB (1997) A case-control study of risk factors of nasopharyngeal carcinoma. Cancer Lett 117:17–22

    Article  PubMed  CAS  Google Scholar 

  11. 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

    Article  PubMed  CAS  Google Scholar 

  12. 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

    Article  PubMed  CAS  Google Scholar 

  13. 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

    PubMed  CAS  Google Scholar 

  14. 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

    Article  PubMed  CAS  Google Scholar 

  15. 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

    Google Scholar 

  16. Yu MC, Huang TB, Henderson BE (1989) Diet and nasopharyngeal carcinoma: a case-control study in Guangzhou, China. Int J Cancer 43:1077–1082

    Article  PubMed  CAS  Google Scholar 

  17. 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

    Google Scholar 

  18. 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

    Article  PubMed  CAS  Google Scholar 

  19. Yan L, Xi Z, Drettner B (1989) Epidemiological studies of nasopharyngeal cancer in the Guangzhou area, China. Preliminary report. Acta Otolaryngol 107:424–427

    Article  PubMed  CAS  Google Scholar 

  20. 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

    Google Scholar 

  21. 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

    Article  PubMed  CAS  Google Scholar 

  22. 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

    Article  PubMed  CAS  Google Scholar 

  23. Feng BJ, Jalbout M, Ayoub WB et al (2007) Dietary risk factors for nasopharyngeal carcinoma in Maghrebian countries. Int J Cancer 121:1550–1555

    Article  PubMed  CAS  Google Scholar 

  24. Willett W (1998) Nutritional epidemiology, 2nd edn. Oxford Universtiy Press Inc., New York

    Book  Google Scholar 

  25. 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

    Article  PubMed  CAS  Google Scholar 

  26. 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

    Article  PubMed  CAS  Google Scholar 

  27. 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

    Article  PubMed  CAS  Google Scholar 

  28. 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

    Article  PubMed  CAS  Google Scholar 

  29. 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

    Article  PubMed  Google Scholar 

  30. 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

    PubMed  CAS  Google Scholar 

  31. Yang Y, Wang G, X. P (2002) China food composition tables 2002. Peking University Medical Press, Beijing

  32. 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

    Article  PubMed  CAS  Google Scholar 

  33. 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

    Article  CAS  Google Scholar 

  34. 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

    Article  PubMed  CAS  Google Scholar 

  35. 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

    PubMed  CAS  Google Scholar 

  36. Arrigoni O, De Tullio MC (2002) Ascorbic acid: much more than just an antioxidant. Biochim Biophys Acta 1569:1–9. doi:S0304416501002355

    Article  PubMed  CAS  Google Scholar 

  37. 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

    PubMed  CAS  Google Scholar 

  38. 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

    Article  PubMed  CAS  Google Scholar 

  39. 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

    PubMed  CAS  Google Scholar 

  40. 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

    Article  Google Scholar 

  41. 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

    Article  PubMed  Google Scholar 

  42. 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

    Article  PubMed  Google Scholar 

  43. 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

    PubMed  Google Scholar 

  44. Shi L (1998) Sociodemographic characteristics and individual health behaviors. South Med J 91:933–941

    Article  PubMed  CAS  Google Scholar 

  45. 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

    PubMed  CAS  Google Scholar 

  46. 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

    Article  PubMed  CAS  Google Scholar 

  47. 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

    Article  PubMed  CAS  Google Scholar 

  48. Lampe JW, Fredstrom SB, Slavin JL, Potter JD (1993) Sex differences in colonic function: a randomised trial. Gut 34:531–536

    Article  PubMed  CAS  Google Scholar 

  49. IdS Silva (1999) Cancer epidemiology: principles and methods. IARC, Lyon

    Google Scholar 

  50. 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

    Article  PubMed  CAS  Google Scholar 

  51. 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

    Article  PubMed  Google Scholar 

Download references

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.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yu-ming Chen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-012-9923-z

Keywords

Navigation