Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

An in vitro assessment of bioaccessibility of arsenicals in rice and the use of this estimate within a probabilistic exposure model

Abstract

In this study, an in vitro synthetic gastrointestinal extraction protocol was used to estimate bioaccessibility of different arsenicals present in 17 rice samples of various grain types that were collected across the United States. The across matrix average for total arsenic was 209 ng/g±153 (±2σ). The bioaccessibility estimate produced an across matrix average of 61%±19 (±2σ). The across matrix average concentrations of inorganic arsenic (iAs) and dimethylarsinic acid (DMA) were 81 ng/g±67.7 and 41 ng/g±58.1 (±2σ), respectively. This distribution of iAs concentrations in rice was combined with the distribution of consumption patterns (from WWEIA) in a Stochastic Human Exposure and Dose Simulator model to estimate population-based exposures. The mean consumption rate for the population as a whole was 15.7 g per day resulting in a 0.98 μg iAs per day exposure. The mean consumption rate for children 1–2 years old was 7 g per day resulting in a 0.48 μg iAs per day exposure. Presystemic biotransformation of DMA in rice was examined using an in vitro assay containing the anaerobic microbiota of mouse cecum. This assay indicated that DMA extracted from the rice was converted to dimethylthioarsinic acid, although a second oxygen–sulfur exchange to produce DMDTA was not observed.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. IARC. Some Drinking-water Disinfectants and Contaminants, Including Arsenic. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 84. IARC: Lyon, France, 2004. http://monographs.iarc.fr/ENG/Monographs/vol84/index.php.

  2. World Health Organization. Guidelines for Drinking Water Quality, 2nd edn, Vol. 1, France, 1993. http://www.emro.who.int/ceha/pdf/Guidelines_DrinkingWater_Recommendations.pdf.

  3. Cao X., Hao C.L., Wang G., Yang H.H., Chen D.Y., and Wang X.R. Sequential extraction combined with HPLC-ICP-MS for as speciation in dry seafood products. Food Chem 2009: 113 (2): 720–726.

    Article  CAS  Google Scholar 

  4. Shiomi K. Arsenic in marine organisms: chemical forms and toxicological aspects. In: Nriagu J.O. (ed). Arsenic in the Environment. Part II: Human Health and Ecosystem Effects. Wiley: New York, 1994, pp. 261–293.

    Google Scholar 

  5. Institute I.R.R. Rice in Human Nutrition. Food and Agriculture Organisation of the United Nations: Rome, 1993.

  6. Ackerman A.H., Creed P.A., Parks A.N., Fricke M.W., Schwegel C.A., and Creed J.T., et al. Comparison of a chemical and enzymatic extraction of arsenic from rice and an assessment of the arsenic absorption from contaminated water by cooked rice. Environ Sci Technol 2005: 39 (14): 5241–5246.

    Article  CAS  Google Scholar 

  7. Heitkemper D.T., Vela N.P., Stewart K.R., and Westphal C.S. Determination of total and speciated arsenic in rice by ion chromatography and inductively coupled plasma mass spectrometry. J Anal At Spectrom 2001: 16 (4): 299–306.

    Article  CAS  Google Scholar 

  8. Heitkemper D.T., Kubachka K.M., Halpin P.R., Allen M.N., and Shockey N.V. Survey of total arsenic and arsenic speciation in US-produced rice as a reference point for evaluating change and future trends. Food Addit Contam, Part B 2009: 2 (2): 112–120.

    Article  CAS  Google Scholar 

  9. Lamont W.H. Concentration of inorganic arsenic in samples of white rice from the United States. J Food Compos Anal 2003: 16 (6): 687–695.

    Article  CAS  Google Scholar 

  10. Laparra J.M., Velez D., Barbera R., Farre R., and Montoro R. Bioavailability of inorganic arsenic in cooked rice: practical aspects for human health risk assessments. J Agric Food Chem 2005: 53 (22): 8829–8833.

    Article  CAS  Google Scholar 

  11. Sanz E., Muñoz-Olivas R., and Cámara C. A rapid and novel alternative to conventional sample treatment for arsenic speciation in rice using enzymatic ultrasonic probe. Anal Chim Acta 2005: 535 (1–2): 227–235.

    Article  CAS  Google Scholar 

  12. Schoof R.A., Yost L.J., Eickhoff J., Crecelius E.A., Cragin D.W., and Meacher D.M., et al. A market basket survey of inorganic arsenic in food. Food Chem Toxicol 1999: 37 (8): 839–846.

    Article  CAS  Google Scholar 

  13. Torres-Escribano S., Leal M., Velez D., and Montoro R. Total and inorganic arsenic concentrations in rice sold in Spain, effect of cooking, and risk assessments. Environ Sci Technol 2008: 42 (10): 3867–3872.

    Article  CAS  Google Scholar 

  14. Williams P.N., Price A.H., Raab A., Hossain S.A., Feldmann J., and Meharg A.A. Variation in arsenic speciation and concentration in paddy rice related to dietary exposure. Environ Sci Technol 2005: 39 (15): 5531–5540.

    Article  CAS  Google Scholar 

  15. Zavala Y.J., Gerads R., Gurleyuk H., and Duxbury J.M. Arsenic in rice: II. Arsenic speciation in USA grain and implications for human health. Environ Sci Technol 2008: 42 (10): 3861–3866.

    Article  CAS  Google Scholar 

  16. Rodriguez R.R., Basta N.T., Casteel S.W., and Pace L.W. An in vitro gastrointestinal method to estimate bioavailable arsenic in contaminated soils and solid media. Environ Sci Technol 1999: 33 (4): 642–649.

    Article  CAS  Google Scholar 

  17. Kohlmeyer U., Jantzen E., Kuballa J., and Jakubik S. Benefits of high resolution IC-ICP-MS for the routine analysis of inorganic and organic arsenic species in food products of marine and terrestrial origin. Anal Bioanal Chem 2003: 377 (1): 6–13.

    Article  CAS  Google Scholar 

  18. He Y., and Zheng Y. Assessment of in vivo bioaccessibility of arsenic in dietary rice by a mass balance approach. Sci Total Environ 2010: 408 (6): 1430–1436.

    Article  CAS  Google Scholar 

  19. Juhasz A.L., Smith E., Weber J., Rees M., Rofe A., and Kuchel T., et al. In vivo assessment of arsenic bioavailability in rice and its significance for human health risk assessment. Environ Health Perspect 2006: 114 (12): 1826–1831.

    Article  CAS  Google Scholar 

  20. Mass M.J., Tennant A., Roop B.C., Cullen W.R., Styblo M., and Thomas D.J., et al. Methylated trivalent arsenic species are genotoxic. Chem Res Toxicol 2001: 14 (4): 355–361.

    Article  CAS  Google Scholar 

  21. Styblo M., Del Razo L.M., Vega L., Germolec D.R., LeCluyse E.L., and Hamilton G.A., et al. Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch Toxicol 2000: 74 (6): 289–299.

    Article  CAS  Google Scholar 

  22. Kubachka K.M., Kohan M.C., Conklin S.D., Herbin-Davis K., Creed J.T., and Thomas D.J. In vitro biotransformation of dimethylarsinic acid and trimethylarsine oxide by anaerobic microflora of mouse cecum analyzed by HPLC-ICP-MS and HPLC-ESI-MS. J Anal At Spectrom 2009: 24 (8): 1062–1068.

    Article  CAS  Google Scholar 

  23. Yoshida K., Kuroda K., Zhou X., Inoue Y., Date Y., and Wanibuchi H., et al. Urinary sulfur-containing metabolite produced by intestinal bacteria following oral administration of dimethylarsinic acid to rats. Chem Res Toxicol 2003: 16 (9): 1124–1129.

    Article  CAS  Google Scholar 

  24. Kuroda K., Yoshida K., Yoshimura M., Endo Y., Wanibuchi H., and Fukushima S., et al. Microbial metabolite of dimethylarsinic acid is highly toxic and genotoxic. Toxicol Appl Pharmacol 2004: 198 (3): 345–353.

    Article  CAS  Google Scholar 

  25. Naranmandura H., Ibata K., and Suzuki K.T. Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem Res Toxicol 2007: 20 (8): 1120–1125.

    Article  CAS  Google Scholar 

  26. Yost L.J., Tao S.-H., Egan S.K., Barraj L.M., Smith K.M., and Tsuji J.S., et al. Estimation of dietary intake of inorganic arsenic in US children. Hum Ecol Risk Assess 2004: 10 (3): 473–483.

    Article  CAS  Google Scholar 

  27. Meacher D.M., Menzel D.B., Dillencourt M.D., Bic L.F., Schoof R.A., and Yost L.J., et al. Estimation of multimedia inorganic arsenic intake in the U.S. population. Hum Ecol Risk Assess 2002: 8 (7): 1697–1721.

    Article  CAS  Google Scholar 

  28. U.S. Department of Agriculture A.R.S., Beltsville Human Nutrition Research Center, Food Surveys Research Group (Beltsville, MD) and U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics (Hyattsville, MD). What We Eat in America, NHANES 2001–2006. http://www.cdc.gov/nchs/nhanes/nhanes_questionnaires.htm (accessed April 2010).

  29. Xue J., Zartarian V.G., Özkaynak H., Dang W., Glen G., and Smith L., et al. A probabilistic arsenic exposure assessment for children who contact chromated copper arsenate (CCA)-treated playsets and decks, part 2: sensitivity and uncertainty analyses. Risk Anal 2006: 26 (2): 533–541.

    Article  Google Scholar 

  30. Zartarian V.G., Xue J., Özkaynak H., Dang W., Glen G., and Smith L., et al. A probabilistic arsenic exposure assessment for children who contact CCA-treated playsets and decks, part 1: model methodology, variability results, and model evaluation. Risk Anal 2006: 26 (2): 515–531.

    Article  Google Scholar 

  31. U.S. Rice Federation. Facts about the U.S. Rice Supply. http://www.usarice.com/doclib/188/3362.pdf, April 2008 (accessed April 2010).

  32. Hirata S., and Toshimitsu H. Determination of arsenic species and arsenosugars in marine samples by HPLC-ICP-MS. Appl Organomet Chem 2007: 21 (6): 447–454.

    Article  CAS  Google Scholar 

  33. Williams P.N., Raab A., Feldmann J., and Meharg A.A. Market basket survey shows elevated levels of as in south central US processed rice compared to california: consequences for human dietary exposure. Environ Sci Technol 2007: 41: 2178–2183.

    Article  CAS  Google Scholar 

  34. Glaser J.A., Foerst D.L., and McKee G.D. Trace analyses for wastewaters. Environ Sci Technol 1981: 15 (12): 1426–1435.

    Article  CAS  Google Scholar 

  35. Glahn R.P., Lee O.A., Yeung A., Goldman M.I., and Miller D.D. Caco-2 cell ferritin formation predicts nonradiolabeled food iron availability in an in vitro digestion/Caco-2 cell culture model. J Nutr 1998: 128 (9): 1555–1561.

    Article  CAS  Google Scholar 

  36. Glahn R.P., Cheng Z., Welch R.M., and Gregorio G.B. Comparison of iron bioavailability from 15 rice genotypes: studies using an in vitro digestion/Caco-2 cell culture model. J Agric Food Chem 2002: 50 (12): 3586–3591.

    Article  CAS  Google Scholar 

  37. Xue J., Zartarian V., Wang S.-W., Liu S.V., and Georgopoulos P. Probabilistic modeling of dietary arsenic exposure and dose and evaluation with 2003–2004 NHANES data. Environ Health Perspect 2009: 118 (3): 345–350.

    Article  Google Scholar 

  38. Conklin S.D., Ackerman A.H., Fricke M.W., Creed P.A., Creed J.T., and Kohan M.C., et al. In vitro biotransformation of an arsenosugar by mouse anaerobic cecal microflora and cecal tissue as examined using IC-ICP-MS and LC-ESI-MS/MS. Analyst 2006: 131 (5): 648–655.

    Article  CAS  Google Scholar 

  39. Conklin S.D., Fricke M.W., Creed P.A., and Creed J.T. Investigation of the pH effects on the formation of methylated thio-arsenicals, and the effects of pH and temperature on their stability. J Anal At Spectrom 2008: 23: 711–716.

    Article  CAS  Google Scholar 

  40. FDA. Total Diet Study, http://www.fda.gov/downloads/Food/FoodSafety/FoodContaminantsAdulteration/TotalDietStudy/UCM243059.pdf, 2007. Accessed 14 November 2011.

  41. Zavala Y.J., and Duxbury J.M. Arsenic in rice: I. Estimating normal levels of total arsenic in rice grain. Environ Sci Technol 2008: 42 (10): 3856–3860.

    Article  CAS  Google Scholar 

  42. Caroli S. The Determination of Chemical Elements in Food: Applications for Atomic and Mass Spectrometry. John Wiley & Sons, Inc.: Hoboken, New Jersey, 2007.

    Book  Google Scholar 

  43. D’Ilio S., Alessandrelli M., Cresti R., Forte G., and Caroli S. Arsenic content of various types of rice as determined by plasma-based techniques. Microchem J 2002: 73: 195–201.

    Article  Google Scholar 

  44. Duxbury J.M., Mayer A.B., Lauren J.G., and Hassan N. Food chain aspects of arsenic contamination in Bangladesh: effects on quality and productivity of rice. J Environ Sci Health 2003: 38: 61–69.

    Article  CAS  Google Scholar 

  45. Pizarro I., Gomez M., Palacios M.A., and Camara C. Evaluation of stability of arsenic species in rice. Anal Bioanal Chem 2003: 376: 102–109.

    Article  CAS  Google Scholar 

  46. Heikens A. Arsenic Contamination of Irrigation Water, Soil and Crops in Bangladesh: Risk Implications for Sustainable Agriculture and Food Safety in Asia. In: Food and Agriculture Organization (ed). Food and Agriculture Organization of the United Nations Regional Office for Asia and the Pacific: Bangkok, 2006. ftp://ftp.fao.org/docrep/fao/009/ag105e/ag105e00.pdf.

    Google Scholar 

  47. National Primary Drinking Water Regulations. Arsenic and Clarifications to Compliance and New Source Contaminants Monitoring 2001, Vol. 66, Federal Register: Environmental Protection Agency: Washington DC, pp. 6975–7066.

Download references

Acknowledgements

The United States Environmental Protection Agency through its Office of Research and Development funded and managed the research described here. It has been subjected to the Agency's administrative review and approved for publication. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to John T Creed.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Additional information

Supplementary Information accompanies the paper on the Journal of Exposure Science and Environmental Epidemiology website

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trenary, H., Creed, P., Young, A. et al. An in vitro assessment of bioaccessibility of arsenicals in rice and the use of this estimate within a probabilistic exposure model. J Expo Sci Environ Epidemiol 22, 369–375 (2012). https://doi.org/10.1038/jes.2012.24

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/jes.2012.24

Keywords

This article is cited by

Search

Quick links