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A multi-day environmental study of polycyclic aromatic hydrocarbon exposure in a high-risk region for esophageal cancer in China

Journal of Exposure Science & Environmental Epidemiology volume 23, pages 52–59 (2013)Cite this article

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Abstract

Linzhou, China has one of the highest rates of esophageal squamous cell carcinoma in the world. Exposure to carcinogenic polycyclic aromatic hydrocarbons (PAHs), such as benzo[a]pyrene (BaP), may have a role in this increased risk. To better understand PAH sources, we measured PAHs in the air and food of 20 non-smokers over multiple days and compared the concentrations with a urinary PAH biomarker, 1-hydroxypyrene glucuronide (1-OHPG). Sampling occurred over 4 consecutive days. Kitchen air samples (days 2–3) and duplicate diet samples (days 1–4) were analyzed for 14 or more unique PAHs, including BaP. Daily urine samples (days 1–3) were analyzed for 1-OHPG. Mixed-effects models were used to evaluate the associations between air or food PAH concentrations and urine 1-OHPG concentrations. The median kitchen air BaP concentration was 10.2 ng/m3 (interquartile range (IQR): 5.1–20.2 ng/m3). The median daily food BaP concentration and intake were 0.08 ng/g (IQR=0.04–0.16 ng/g) and 86 ng/day (IQR=41–142 ng/day), respectively. The median 1-OHPG concentration was 3.36 pmol/ml (IQR=2.09–6.98 pmol/ml). In mixed-effects models, 1-OHPG concentration increased with same-day concentration of food BaP (P=0.07). Although PAH concentrations in air were not associated with 1-OHPG concentrations, the high concentrations of PAHs in both air and food suggest that they are both important routes of exposure to PAHs in this population. Further evaluation of the role of PAH exposure from air and food in the elevated rates of esophageal cancer in this region is warranted.

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References

  1. Ke L. Mortality and incidence trends from esophagus cancer in selected geographic areas of China circa 1970–90. Int J Cancer 2002: 102: 271–274.

    Article  CAS  PubMed  Google Scholar 

  2. Blot W.J., McLaughlin J.K., and Fraumeni J.F.J. Esophageal Cancer. In: Schottenfeld D., Fraumeni Jr J.F. (Eds.). Int J Cancer Epidemiology and Prevention. Oxford University Press: Oxford, 2006, pp 697–706.

    Chapter  Google Scholar 

  3. Freedman N.D., Abnet CC., Leitzmann M.F., Mouw T., Subar A.F., Hollenbeck A.R., et al. A prospective study of tobacco, alcohol, and the risk of esophageal and gastric cancer subtypes. Am J Epidemiol 2007: 165: 1424–1433.

    Article  PubMed  Google Scholar 

  4. Nasrollahzadeh D., Kamangar F., Aghcheli K., Sotoudeh M., Islami F., Abnet C.C., et al. Opium, tobacco, and alcohol use in relation to oesophageal squamous cell carcinoma in a high-risk area of Iran. Br J Cancer 2008: 98: 1857–1863.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Tran G.D., Sun X.D., Abnet C.C., Fan J.H., Dawsey S.M., Dong Z.W., et al. Prospective study of risk factors for esophageal and gastric cancers in the Linxian general population trial cohort in China. Int J Cancer 2005: 20: 113.

    Google Scholar 

  6. IARC (International Agency for Research on Cancer). Monograph on Some Non-Heterocyclic Polycyclic Aromatic Hydrocarbons and Some Related Exposures Vol. 92. IARC Press: Lyon, France, 2010.

  7. Abedi-Ardekani B., Kamangar F., Hewitt S.M., Hainaut P., Sotoudeh M., Abnet C.C., et al. Polycyclic aromatic hydrocarbon exposure in oesophageal tissue and risk of oesophageal squamous cell carcinoma in north-eastern Iran. Gut 2010: 59: 1178–1183.

    Article  CAS  PubMed  Google Scholar 

  8. Fagundes R.B., Abnet C.C., Strickland P.T., Kamangar F., Roth M.J., Taylor P.R., et al. Higher urine 1-hydroxy pyrene glucuronide (1-OHPG) is associated with tobacco smoke exposure and drinking mate in healthy subjects from Rio Grande do Sul, Brazil. BMC Cancer 2006: 6: 139.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Kamangar F., Strickland P.T., Pourshams A., Malekzadeh R., Boffetta P., Roth M.J., et al. High exposure to polycyclic aromatic hydrocarbons may contribute to high risk of esophageal cancer in northeastern Iran. Anticancer Res 2005: 25: 425–428.

    CAS  PubMed  Google Scholar 

  10. Roth M.J., Qiao Y.L., Rothman N., Tangrea J.A., Dawsey S.M., Wang G.Q., et al. High urine 1-hydroxypyrene glucuronide concentrations in Linxian, China, an area of high risk for squamous oesophageal cancer. Biomarkers 2001: 6: 381–386.

    Article  CAS  Google Scholar 

  11. Roth M.J., Strickland K.L., Wang G.Q., Rothman N., Greenberg A., and Dawsey S.M. High levels of carcinogenic polycyclic aromatic hydrocarbons present within food from Linxian, China may contribute to that region's high incidence of oesophageal cancer. Eur J Cancer 1998: 34: 757–758.

    Article  CAS  PubMed  Google Scholar 

  12. Wornat M.J., Ledesma E.B., Sandrowitz A.K., Roth M.J., Dawsey S.M., Qiao Y.L., et al. Polycyclic aromatic hydrocarbons identified in soot extracts from domestic coal-burning stoves of Henan Province, China. Environ Sci Technol 2001: 35: 1943–1952.

    Article  CAS  PubMed  Google Scholar 

  13. Hakami R., Mohtadinia J., Etemadi A., Kamangar F., Nemati M., Pourshams A., et al. Dietary intake of benzo(a)pyrene and risk of esophageal cancer in north of Iran. Nutr Cancer 2008: 60: 216–221.

    Article  CAS  PubMed  Google Scholar 

  14. NIOSH (National Institute of Occupational Safety and Health). Polynuclear aromatic hydrocarbons by HPLC. Method 5506. In: NIOSH Manual of Analytical Methods 4th edn. Cincinatti, OH, 1998.

  15. Richter B., Jones B., Ezzell J., and Porter N. Accelerated solvent extraction: a technique for sample preparation. Anal Chem 1996: 68: 1033–1039.

    Article  CAS  Google Scholar 

  16. Strickland P.T., Kang D., Bowman E.D., Fitzwilliam A., Downing T.E., Rothman N., et al. Identification of 1-hydroxypyrene glucuronide as a major pyrene metabolite in human urine by synchronous fluorescence spectroscopy and gas chromatography-mass spectrometry. Carcinogenesis 1994: 15: 483–487.

    Article  CAS  PubMed  Google Scholar 

  17. Larsen K. Creatinine assay by a reaction kinetic principle. Clin Chim Acta 1972: 41: 209–217.

    Article  CAS  PubMed  Google Scholar 

  18. U.S. EPA (Environmental Protection Agency). 2011. Exposure factors handbook: 2011 edition. National Center for Environmental Assessment, Washington, DC; EPA/600/R-09/052F. Available from the National Technical Information Service, Springfield, VA, and online at http://www.epa.gov/ncea/efh.

  19. Jiang Y.F., Wang X.T., Wang F., Jia Y., Wu M.H., Sheng G.Y., et al. Levels, composition profiles and sources of polycyclic aromatic hydrocarbons in urban soil of Shanghai, China. Chemosphere 2009: 75: 1112–1118.

    Article  CAS  PubMed  Google Scholar 

  20. Lv J., Xu R., Wu G., Zhang Q., Li Y., Wang P., et al. Indoor and outdoor air pollution of polycyclic aromatic hydrocarbons (PAHs) in Xuanwei and Fuyuan, China. J Environ Monit 2009: 11: 1368–1374.

    Article  CAS  PubMed  Google Scholar 

  21. Yunker M.B., Macdonald R.W., Vingarzan R., Mitchell R.H., Goyette D., and Sylvestre S. PAHs in the Fraser River basin: a critical appraisal of PAH ratios as indicators of PAH source and composition. Organic Geochem 2002: 33: 489–515.

    Article  CAS  Google Scholar 

  22. Barr D.B., Wilder L.C., Caudill S.P., Gonzalez A.J., Needham L.L., and Pirkle J.L. Urinary creatinine concentrations in the U.S. population: implications for urinary biologic monitoring measurements. Environ Health Perspect 2005: 113: 192–200.

    Article  CAS  PubMed  Google Scholar 

  23. Li A., Schoonover T.M., Zou Q., Norlock F., Conory L.M., Scheff P.A., et al. Polycyclic aromatic hydrocarbons in residential air of ten Chicago area homes: concentrations and influencing factors. Atmospheric Environ 2005: 39: 3491–3501.

    Article  CAS  Google Scholar 

  24. Naumova Y.Y., Eisenreich S.J., Turpin B.J., Weisel C.P., Morandi M.T., Colome S.D., et al. Polycyclic aromatic hydrocarbons in the indoor and outdoor air of three cities in the U.S. Environ Sci Technol 2002: 36: 2552–2559.

    Article  CAS  PubMed  Google Scholar 

  25. Fromme H., Lahrz T., Piloty M., Gebhardt H., Oddoy A., and Ruden H. Polycyclic aromatic hydrocarbons inside and outside of apartments in an urban area. Sci Total Environ 2004: 326: 143–149.

    Article  CAS  PubMed  Google Scholar 

  26. Zhu L., Lu H., Chen S., and Amagai T. Pollution level, phase distribution and source analysis of polycyclic aromatic hydrocarbons in residential air in Hangzhou, China. J Hazard Mater 2009: 162: 1165–1170.

    Article  CAS  PubMed  Google Scholar 

  27. Masih J., Masih A., Kulshrestha A., Singhvi R., and Taneja A. Characteristics of polycyclic aromatic hydrocarbons in indoor and outdoor atmosphere in the North central part of India. J Hazard Mater 2010: 177: 190–198.

    Article  CAS  PubMed  Google Scholar 

  28. Kazerouni N., Sinha R., Hsu C.H., Greenberg A., and Rothman N. Analysis of 200 food items for benzo[a]pyrene and estimation of its intake in an epidemiologic study. Food Chem Toxicol 2001: 39: 423–436.

    Article  CAS  PubMed  Google Scholar 

  29. Berry M.R., Johnson L.S., Jones J.W., Rader J.I., Kendall D.C., and Sheldon L.S. Dietary characterizations in a study of human exposures in the lower Rio Grande Valley: I. Foods and beverages. Environ Int 1997: 23: 675–692.

    Article  CAS  Google Scholar 

  30. Buckley T.J., Waldman J.M., Dhara R., Greenberg A., Ouyang Z., and Lioy P.J. An assessment of a urinary biomarker for total human environmental exposure to benzo[a]pyrene. Int Arch Occup Environ Health 1995: 67: 257–266.

    Article  CAS  PubMed  Google Scholar 

  31. Kang D., Rothman N., Cho S.H., Lim H.S., Kwon H.J., Kim S.M., et al. Association of exposure to polycyclic aromatic hydrocarbons (estimated from job category) with concentration of 1-hydroxypyrene glucuronide in urine from workers at a steel plant. Occup Environ Med 1995a: 52: 593–599.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kang D.H., Rothman N., Poirier M.C., Greenberg A., Hsu C.H., Schwartz B.S., et al. Interindividual differences in the concentration of 1-hydroxypyrene-glucuronide in urine and polycyclic aromatic hydrocarbon-DNA adducts in peripheral white blood cells after charbroiled beef consumption. Carcinogenesis 1995b: 16: 1079–1085.

    Article  CAS  PubMed  Google Scholar 

  33. Iwegbue C.M. Polycyclic aromatic hydrocarbons profile of kitchen dusts. Bull Environ Contam Toxicol 2011: 86: 298–301.

    Article  CAS  PubMed  Google Scholar 

  34. Oanh N.T.K., Nghiem L., and Phyu Y.L. Emission of polycyclic aromatic hydrocarbons, toxicity, and mutagenicity from domestic cooking using sawdust briquettes wood, and kerosene. Environ Sci Technol 2002: 36: 833–839.

    Article  CAS  Google Scholar 

  35. Buckley T.J., and Lioy P.J. An examination of the time course from human dietary exposure to polycyclic aromatic hydrocarbons to urinary elimination of 1-hydroxypyrene. Br J Ind Med 1992: 49: 113–124.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Phillips D.H. Polycyclic aromatic hydrocarbons in the diet. Mutat Res 1999: 443: 139–147.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported in part by NCI contract N01-RC-47702 to the Cancer Institute, Chinese Academy of Medical Sciences; in part by the Intramural Research Program of the Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH; and in part by the Cancer Institute, Chinese Academy of Medical Sciences.

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Certain commercial equipment or instruments are identified in this paper to adequately specify the experimental procedures. Such identification does not imply recommendations or endorsement by the National Institute of Standards and Technology nor does it imply that the equipment or instruments are the best available for the purpose.

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Authors and Affiliations

  1. Division of Cancer Epidemiology and Genetics (DCEG), Occupational and Environmental Epidemiology Branch, National Cancer Institute, Bethesda, Maryland, USA

    Nicole C Deziel & Melissa C Friesen

  2. Department of Cancer Epidemiology, Cancer Institute, Chinese Academy of Medical Sciences, Beijing, China

    Wen-Qiang Wei, You-Lin Qiao & Yu Zhang

  3. Division of Cancer Epidemiology and Genetics (DCEG), Nutritional Epidemiology Branch, National Cancer Institute, Bethesda, Maryland, USA

    Christian C Abnet, Jian-Song Ren, Sanford M Dawsey & Mark J Roth

  4. Chesapeake Biological Laboratory, University of Maryland Center for Environmental Science, Solomons, Maryland, USA

    Deirdre Sunderland

  5. Analytical Chemistry Division, National Institute of Standards and Technology, Gaithersburg, Maryland, USA

    Michele M Schantz

  6. Department of Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, USA

    Paul T Strickland & Salahaddin Abubaker

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  1. Nicole C Deziel
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Correspondence to Nicole C Deziel.

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Deziel, N., Wei, WQ., Abnet, C. et al. A multi-day environmental study of polycyclic aromatic hydrocarbon exposure in a high-risk region for esophageal cancer in China. J Expo Sci Environ Epidemiol 23, 52–59 (2013). https://doi.org/10.1038/jes.2012.73

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  • DOI: https://doi.org/10.1038/jes.2012.73

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