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Dietary acrylamide exposure was associated with increased cancer mortality in Chinese elderly men and women: a 11-year prospective study of Mr. and Ms. OS Hong Kong

Abstract

Aim

Our study aims to investigate the association between dietary acrylamide exposure and cancer mortality among Chinese elderly.

Methods

A prospective cohort of 4000 elderly men and women aged 65 years and above (Mr. and Ms. OS Hong Kong study) was recruited from local communities from 2001 to 2003. Dietary exposure to acrylamide was evaluated at baseline based on a validated food frequency questionnaire and an acrylamide database from the 1st Hong Kong Total Diet Study. Data on mortality statistics through March 2014 were obtained from the Death Registry of the Department of Health of Hong Kong with a median follow-up of 11.1 years. Cox proportional hazards models were used to examine the association between the acrylamide exposure and cancer mortality. Sex hormones were assessed in men.

Results

During a median follow-up of 11.1 years (39,271 person-years), we ascertained 330 cancer deaths. Vegetables (43.7%) and cereals (28.9%) products were the major contributors to dietary acrylamide. Compared with the lowest quartile of acrylamide intake (<9.9 µg/day), the multivariable hazard ratios for the highest quartile (>17.1 µg/day) were 1.9 (95% CI 1.3–2.8; P trend < 0.01), 1.9 (95% CI 1.0–3.6; P trend = 0.05), and 2.0 (95% CI 1.0–4.0; P trend = 0.06) for the cancer mortality from overall, digestive and respiratory system, respectively. The associations were attenuated to null after further adjustment for circulating free estradiol in men. No statistically significant interactions were observed between acrylamide exposure and sex, obesity and overall lifestyle pattern scores.

Conclusions

The longitudinal data provided evidence that dietary acrylamide, in amounts that Chinese elderly are typically exposed to, was associated with increased cancer mortality. Circulating free estradiol may mediate the association in men.

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References

  1. Besaratinia A, Pfeifer GP (2007) A review of mechanisms of acrylamide carcinogenicity. Carcinogenesis 28(3):519–528

    CAS  Article  PubMed  Google Scholar 

  2. Bongers ML, Hogervorst JG, Schouten LJ, Goldbohm RA, Schouten HC, van den Brandt PA (2012) Dietary acrylamide intake and the risk of lymphatic malignancies: the Netherlands Cohort Study on diet and cancer. PLoS One 7(6):e38016

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Bull RJ, Robinson M, Stober JA (1984) Carcinogenic activity of acrylamide in the skin and lung of Swiss-ICR mice. Cancer Lett 24(2):209–212

    CAS  Article  PubMed  Google Scholar 

  4. Catalgol B, Ozhan G, Alpertunga B (2009) Acrylamide-induced oxidative stress in human erythrocytes. Hum Exp Toxicol 28(10):611–617

    CAS  Article  PubMed  Google Scholar 

  5. Centre for Food Safety, Food and Environmental Hygiene Department (2011) The first Hong Kong Total Diet Study. Methodology 1–34

  6. Dybing E, Farmer PB, Andersen M, Fennell TR, Lalljie SP, Müller DJ, Olin S, Petersen BJ, Schlatter J, Scholz G, Scimeca JA, Slimani N, Törnqvist M, Tuijtelaars S, Verger P (2005) Human exposure and internal dose assessments of acrylamide in food. Food Chem Toxicol 43(3):365–410

    CAS  Article  PubMed  Google Scholar 

  7. Folkerd EJ, Dowsett M (2010) Influence of sex hormones on cancer progression. J Clin Oncol 28(26):4038–4044

    CAS  Article  PubMed  Google Scholar 

  8. Friedman M (2003) Chemistry, biochemistry, and safety of acrylamide. A review. J Agric Food Chem 51(16):4504–4526

    CAS  Article  PubMed  Google Scholar 

  9. Hirvonen T, Kontto J, Jestoi M, Valsta L, Peltonen K, Pietinen P, Virtanen SM, Sinkko H, Kronberg-Kippila C, Albanes D, Virtamo J (2010) Dietary acrylamide intake and the risk of cancer among Finnish male smokers. Cancer Causes Control 21(12):2223–2229

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Hogervorst JG, Schouten LJ, Konings EJ, Goldbohm RA, van den Brandt PA (2007) A prospective study of dietary acrylamide intake and the risk of endometrial, ovarian, and breast cancer. Cancer Epidemiol Biomarkers Prev 16(11):2304–2313

    CAS  Article  PubMed  Google Scholar 

  11. Hogervorst JG, Schouten LJ, Konings EJ, Goldbohm RA, van den Brandt PA (2008a) Dietary acrylamide intake and the risk of renal cell, bladder, and prostate cancer. Am J Clin Nutr 87(5):1428–1438

    CAS  PubMed  Google Scholar 

  12. Hogervorst JG, Schouten LJ, Konings EJ, Goldbohm RA, van den Brandt PA (2008b) Dietary acrylamide intake is not associated with gastrointestinal cancer risk. J Nutr 138(11):2229–2236

    CAS  Article  PubMed  Google Scholar 

  13. Hogervorst JG, Schouten LJ, Konings EJ, Goldbohm RA, van den Brandt PA (2009) Lung cancer risk in relation to dietary acrylamide intake. J Natl Cancer Inst 101(9):651–662

    CAS  Article  PubMed  Google Scholar 

  14. Hogervorst JG, Fortner RT, Mucci LA, Tworoger SS, Eliassen AH, Hankinson SE, Wilson KM (2013) Associations between dietary acrylamide intake and plasma sex hormone levels. Cancer Epidemiol Biomarkers Prev 22(11):2024–2036

    CAS  Article  PubMed  Google Scholar 

  15. Hogervorst JG, de Bruijn-Geraets D, Schouten LJ, van Engeland M, de Kok TM, Goldbohm RA, van den Brandt PA, Weijenberg MP (2014) Dietary acrylamide intake and the risk of colorectal cancer with specific mutations in KRAS and APC. Carcinogenesis 35(5):1032–1038

    CAS  Article  PubMed  Google Scholar 

  16. Hogervorst JG, van den Brandt PA, Godschalk RW, van Schooten FJ, Schouten LJ (2016) The influence of single nucleotide polymorphisms on the association between dietary acrylamide intake and endometrial cancer risk. Sci Rep 6:34902

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Hogervorst JG, van den Brandt PA, Godschalk RW, van Schooten FJ, Schouten LJ (2017) Interactions between dietary acrylamide intake and genes for ovarian cancer risk. Eur J Epidemiol 32(5):431–441

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. JECFA (2005) Summary and conclusions of the sixty-fourth meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA), 1–47

  19. Johnson KA, Gorzinski SJ, Bodner KM, Campbell RA, Wolf CH, Friedman MA, Mast RW (1986) Chronic toxicity and oncogenicity study on acrylamide incorporated in the drinking water of Fischer 344 rats. Toxicol Appl Pharmacol 85(2):154–168

    CAS  Article  PubMed  Google Scholar 

  20. Kendall A, Folkerd EJ, Dowsett M (2007) Influences on circulating oestrogens in postmenopausal women: relationship with breast cancer. J Steroid Biochem Mol Biol 103(2):99–109

    CAS  Article  PubMed  Google Scholar 

  21. Labrie F, Cusan L, Gomez JL, Martel C, Berube R, Belanger P, Belanger A, Vandenput L, Mellstrom D, Ohlsson C (2009) Comparable amounts of sex steroids are made outside the gonads in men and women: strong lesson for hormone therapy of prostate and breast cancer. J Steroid Biochem Mol Biol 113(1–2):52–56

    CAS  Article  PubMed  Google Scholar 

  22. Larsson SC, Akesson A, Wolk A (2009) Dietary acrylamide intake and prostate cancer risk in a prospective cohort of Swedish men. Cancer Epidemiol Biomarkers Prev 18(6):1939–1941

    CAS  Article  PubMed  Google Scholar 

  23. Lau EM, Leung PC, Kwok T, Woo J, Lynn H, Orwoll E, Cummings S, Cauley J (2006) The determinants of bone mineral density in Chinese men—results from Mr. Os (Hong Kong), the first cohort study on osteoporosis in Asian men. Osteoporos Int 17(2):297–303

    CAS  Article  PubMed  Google Scholar 

  24. Lipunova N, Schouten LJ, van den Brandt PA, Hogervorst JG (2016) A prospective cohort study on dietary acrylamide intake and the risk for cutaneous malignant melanoma. Eur J Cancer Prev doi:10.1097/CEJ.0000000000000268

    Google Scholar 

  25. Mottram DS, Wedzicha BL, Dodson AT (2002) Acrylamide is formed in the Maillard reaction. Nature 419(6906):448–449

    CAS  Article  PubMed  Google Scholar 

  26. Mucci LA, Adami HO, Wolk A (2006) Prospective study of dietary acrylamide and risk of colorectal cancer among women. Int J Cancer 118(1):169–173

    CAS  Article  PubMed  Google Scholar 

  27. Nagata C, Konishi K, Tamura T, Wada K, Tsuji M, Hayashi M, Takeda N, Yasuda K (2015) Associations of acrylamide intake with circulating levels of sex hormones and prolactin in premenopausal Japanese women. Cancer Epidemiol Biomarkers Prev 24(1):249–254

    CAS  Article  PubMed  Google Scholar 

  28. Olesen PT, Olsen A, Frandsen H, Frederiksen K, Overvad K, Tjonneland A (2008) Acrylamide exposure and incidence of breast cancer among postmenopausal women in the Danish Diet, Cancer and Health Study. Int J Cancer 122(9):2094–2100

    CAS  Article  PubMed  Google Scholar 

  29. Olsen A, Christensen J, Outzen M, Olesen PT, Frandsen H, Overvad K, Halkjaer J (2012) Pre-diagnostic acrylamide exposure and survival after breast cancer among postmenopausal Danish women. Toxicology 296(1–3):67–72

    CAS  Article  PubMed  Google Scholar 

  30. Pelucchi C, La Vecchia C, Bosetti C, Boyle P, Boffetta P (2011) Exposure to acrylamide and human cancer—a review and meta-analysis of epidemiologic studies. Ann Oncol 22(7):1487–1499

    CAS  Article  PubMed  Google Scholar 

  31. Pelucchi C, Bosetti C, Galeone C, La Vecchia C (2015) Dietary acrylamide and cancer risk: an updated meta-analysis. Int J Cancer 136(12):2912–2922

    CAS  Article  PubMed  Google Scholar 

  32. Shipp A, Lawrence G, Gentry R, McDonald T, Bartow H, Bounds J, Macdonald N, Clewell H, Allen B, Van Landingham C (2006) Acrylamide: review of toxicity data and dose-response analyses for cancer and noncancer effects. Crit Rev Toxicol 36(6–7):481–608

    CAS  Article  PubMed  Google Scholar 

  33. Sickles DW, Sperry AO, Testino A, Friedman M (2007) Acrylamide effects on kinesin-related proteins of the mitotic/meiotic spindle. Toxicol Appl Pharmacol 222(1):111–121

    CAS  Article  PubMed  Google Scholar 

  34. Södergard R, Bäckström T, Shanbhag V, Carstensen H (1982) Calculation of free and bound fractions of testosterone and estradiol-17β to human plasma proteins at body temperature. J Steroid Biochem 16(6):801–810

    Article  PubMed  Google Scholar 

  35. Stadler RH (2005) Acrylamide formation in different foods and potential strategies for reduction. Adv Exp Med Biol 561:157–169

    CAS  Article  PubMed  Google Scholar 

  36. Stewart BW, Wild CP (2014) World Cancer Report 2014

  37. Wilson KM, Vesper HW, Tocco P, Sampson L, Rosén J, Hellenäs KE, Törnqvist M, Willett WC (2009) Validation of a food frequency questionnaire measurement of dietary acrylamide intake using hemoglobin adducts of acrylamide and glycidamide. Cancer Causes Control 20(3):269–278

    Article  PubMed  Google Scholar 

  38. Washburn RA, Smith KW, Jette AM, Janney CA (1993) The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 46(2):153–162

    CAS  Article  PubMed  Google Scholar 

  39. WHO/FAO (2002) Health implications of acrylamide in food. Report of a Joint FAO/WHO Consultation. WHO. http://apps.who.int/iris/bitstream/10665/42563/1/9241562188.pdf. Accessed 19 July 2017

  40. Wilson KM, Mucci LA, Rosner BA, Willett WC (2010) A prospective study on dietary acrylamide intake and the risk for breast, endometrial, and ovarian cancers. Cancer Epidemiol Biomarkers Prev 19(10):2503–2515

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Wirfalt E, Paulsson B, Tornqvist M, Axmon A, Hagmar L (2008) Associations between estimated acrylamide intakes, and hemoglobin AA adducts in a sample from the Malmo Diet and Cancer cohort. Eur J Clin Nutr 62(3):314–323

    CAS  Article  PubMed  Google Scholar 

  42. Wong WW, Chung SW, Lam CH, Ho YY, Xiao Y (2014) Dietary exposure of Hong Kong adults to acrylamide: results of the first Hong Kong Total Diet Study. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 31(5):799–805

    CAS  Article  PubMed  Google Scholar 

  43. Woo J, Leung SSF, Ho SC, Lam TH, Janus ED (1997) A food frequency questionnaire for use in the Chinese population in Hong Kong: description and examination of validity. Nutr Res 17(11):1633–1641

    CAS  Article  Google Scholar 

  44. Zhou PP, Zhao YF, Liu HL, Ma YJ, Li XW, Yang X, Wu YN (2013) Dietary exposure of the Chinese population to acrylamide. Biomed Environ Sci 26(6):421–429

    PubMed  Google Scholar 

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Acknowledgements

We wish to thank all participants for their participation and Dr. Edith Lau for her contribution in setting up the cohort.

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Affiliations

Authors

Contributions

ZML conceptualized the study, analyzed the data, interpreted the results, and drafted the manuscript. Suyang Wu helped in the calculation of dietary acrylamide exposure. All the coauthors critically commented on and revised the manuscript.

Corresponding authors

Correspondence to Zhao-min Liu or Lap Ah Tse.

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Conflict of interest

None of the authors have competing interests to report.

Funding

The study was supported by the National Institutes of Health R01 Grant AR049439–01A1 and the Research Grants Council Earmarked Grant CUHK4101/02 M. The funders played no role in the study design, data collection and analysis, interpretation of the data, as well as in writing the manuscript.

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Liu, Zm., Tse, L.A., Ho, S.C. et al. Dietary acrylamide exposure was associated with increased cancer mortality in Chinese elderly men and women: a 11-year prospective study of Mr. and Ms. OS Hong Kong. J Cancer Res Clin Oncol 143, 2317–2326 (2017). https://doi.org/10.1007/s00432-017-2477-4

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Keywords

  • Dietary exposure
  • Acrylamide
  • Cancer mortality
  • Chinese elderly