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Environmental Science and Pollution Research

, Volume 22, Issue 12, pp 8802–8825 | Cite as

Assessing the bioavailability and bioaccessibility of metals and metalloids

  • Jack C. NgEmail author
  • Albert Juhasz
  • Euan Smith
  • Ravi Naidu
Bioavailability - the underlying basis for Risk Based Land Management

Abstract

Bioavailability (BA) determines the potential harm of a contaminant that exerts on the receptor. However, environmental guidelines for site contamination assessment are often set assuming the contaminant is 100 % bioavailable. This conservative approach to assessing site risk may result in the unnecessary and expensive remediation of a contaminated site. The National Environmental Protection Measures in Australia has undergone a statutory 5-year review that recommended that contaminant bioavailability and bioaccessibility (BAC) measures be adopted as part of the contaminated site risk assessment process by the National Environment Protection Council. We undertook a critical review of the current bioavailability and bioaccessibility approaches, methods and their respective limitations. The ‘gold’ standard to estimate the portion of a contaminant that reaches the system circulatory system (BA) of its receptor is to determine BA in an in vivo system. Various animal models have been utilised for this purpose. Because of animal ethics issues, and the expenses associated with performing in vivo studies, several in vitro methods have been developed to determine BAC as a surrogate model for the estimation of BA. However, few in vitro BAC studies have been calibrated against a reliable animal model, such as immature swine. In this review, we have identified suitable methods for assessing arsenic and lead BAC and proposed a decision tree for the determination of contaminant bioavailability and bioaccessibility for health risk assessment.

Keywords

Bioavailability Bioaccessibility Metals Metalloids Risk assessment Site contamination 

References

  1. Abu-Bakar A, Arthur DM, Wikman AS, Rahnasto M, Juvonen RO, Vepsäläinen J, Raunio H, Ng JC, Lang MA (2012) Metabolism of bilirubin by human cytochrome P450 2A6. Toxicol Appl Pharmacol 261(1):50–58Google Scholar
  2. Aharoni C, Sparks DL (1991) Kinetics of soil chemical reactions—a theoretical treatment. In: Sparks DL, Suarez DL (eds) Rates of soil chemical processes. SSSA, Madison, WI, pp 1–19Google Scholar
  3. Alexander FW, Clayton BE, Delves HT (1974) Mineral and trace-metal balances in children receiving normal and synthetic diets. Quarterly J Med 43(169):89–111Google Scholar
  4. Alvaro D, Cantafora A, Attili AF, Ginanni Corradini S, De Luca C (1986) Relationships between bile salts, hydrophobicity and phospholipid composition in bile of various animal species. Comp Biochem Physiol B 83(3):551–554Google Scholar
  5. Arthur DM, Ng JC, Lang MA, Abu-Bakar A (2012) Urinary excretion of bilirubin oxidative metabolites in arsenite-induced mice. J Toxicol Sci 37(3):655–661Google Scholar
  6. Basta NT, Rodriguez RR, Casteel SW (2001) Bioavailability and risk of arsenic exposure by the soil ingestion pathway. In: Frankenberger WT (ed) Environmental chemistry of arsenic. Marcel Dekker, New York, pp 117–139Google Scholar
  7. Basta NT, Foster JN, Dayton EA, Rodriguez RR, Casteel SW (2007) The effect of dosing vehicle on arsenic bioaccessibility in smelter-contaminated soils. J Environ Sci Health A 42:1275–1281Google Scholar
  8. Bridges CC, Zalpus RK (2005) Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharmacol 204(3):274–308Google Scholar
  9. Bruce SL (2004) Development of a risk assessment tool to minimise the impact of arsenic and lead toxicity from mine tailings. PhD thesis, The University of QueenslandGoogle Scholar
  10. Bruce SL, Noller BN, Grigg AH, Mullen BF, Mulligan DR, Ritchie PJ, Currey N, Ng JC (2003) A field study conducted at Kidston Gold Mine, to evaluate the impact of arsenic and zinc from mine tailing to grazing cattle. Toxicol Lett 137(1–2):23–34Google Scholar
  11. Buchet JP, Lauwerys R, Roels H (1981a) Comparison of the urinary excretion of arsenic metabolites after a single oral dose of sodium arsenite, monomethylarsonate, or dimethylarsinate in man. Int Arch Occup Environ Health 48(1):71–79Google Scholar
  12. Buchet JP, Lauwerys R, Roels H (1981b) Urinary excretion of inorganic arsenic and its metabolites after repeated ingestion of sodium metaarsenite by volunteers. Int Arch Occup Environ Health 48(2):111–118Google Scholar
  13. Button M, Watts MJ, Cave MR, Harrington CF, Jenkin GT (2009) Earthworms and in vitro physiologically-based extraction tests: complementary tools for a holistic approach towards understanding risk at arsenic-contaminated sites. Environ Geochem Health 31(2):273–282Google Scholar
  14. Carrizales L, Razo I, Téllez-Hernández JI, Torres-Nerio R, Torres A, Batres LE, Cubillas AC, Díaz-Barriga F (2006) Exposure to arsenic and lead of children living near a copper-smelter in San Luis Potosi, Mexico: importance of soil contamination for exposure of children. Environ Res 101(1):1–10Google Scholar
  15. Casteel SW, Cowart RP, Weis CP, Henningsen GM, Hoffman E, Brattin WJ, Guzman RE, Starost MF, Payne JT, Stockham SL, Becker SV, Drexler JW, Turk JR (1997) Bioavailability of lead to juvenile swine dosed with soil from the Smuggler Mountain NPL site of Aspen, Colorado. Fundam Appl Toxicol 36(2):177–187Google Scholar
  16. Charman WN, Porter CJH, Mithani S, Dressman JB (1997) Physicochemical and physiological mechanisms for the effects of food on drug absorption: the role of lipids and pH. J Pharm Sci 86(3):269–282Google Scholar
  17. Council of Standards Australia (1997) Australian standard leaching procedure (ASLP AS4439.1, As4439.2, AS4439.3). Council of Standards Australia, AustraliaGoogle Scholar
  18. Daugherty AL, Mrsny RJ (1999) Transcellular uptake mechanisms of the intestinal epithelial barrier. Part one. Pharm Sci Technol Today 2(4):144–151Google Scholar
  19. Davis A, Ruby MV, Bergstrom PD (1992) Bioavailability of arsenic and lead in soils from the Butte, Montana, mining district. Environ Sci Technol 26(3):461–468Google Scholar
  20. Dean JR, Ma R (2007) Approaches to assess the oral bioaccessibility of persistent organic pollutants: a critical review. Chemosphere 68(8):1399–1407Google Scholar
  21. Degan LP, Philips SF (1996) Variability of gastrointestinal transit in healthy women and men. Gut 39(2):299–305Google Scholar
  22. Denys S, Caboche J, Tack K, Delalain P (2007) Bioaccessibility of lead in high carbonate soils. J Environ Sci Health A 42(9):1331–1339Google Scholar
  23. Denys S, Caboche J, Tack K, Rychen G, Wragg J, Cave M, Jondreville C, Feidt C (2012) In-vivo validation of the unified BARGE method to assess the bioaccessibility of arsenic, antimony, cadmium, and lead in soils. Environ Sci Technol 46:6252–6260Google Scholar
  24. Devesa-Rey R, Paradelo R, Díaz-Fierros F, Barral MT (2008) Fractionation and bioavailability of arsenic in the bed sediments of the Anllóns River (NW Spain). Water Air Soil Pollut 195(1–4):189–198Google Scholar
  25. Diacomanolis V, Ng JC, Noller BN (2007) Development of mine site close-out criteria for arsenic and lead using a health risk approach. In: Fourie A, Tibbett M, Wiertz J (eds) Mine Closure 2007—Proceedings of the Second International Seminar on Mine Closure, Santiago, Chile, 16–19 October, pp 191–198Google Scholar
  26. Drexler JW, Brattin WJ (2007) An in vitro procedure for estimation of lead relative bioavailability: with validation. Hum Ecol Risk Assess 13(2):383–401Google Scholar
  27. enHealth (2004) Environmental health risk assessment—guidelines for assessing human health for environmental hazards. Department of Health and Ageing and enHealth Council, CanberraGoogle Scholar
  28. Fendorf S, La Force MJ, Li GC (2004) Temporal changes in soil partitioning and bioaccessibility of arsenic, chromium, and lead. J Environ Qual 33(6):2049–2055Google Scholar
  29. Freeman GB, Johnson JD, Killinger JM, Liao SC, Feder PI, Davis AO, Ruby MV, Chaney RL, Lovre SC, Bergstrom PD (1992) Relative bioavailability of lead from mining waste soil in rats. Fundam Appl Toxicol 19(3):388–398Google Scholar
  30. Freeman GB, Johnson JD, Killinger JM, Liao SC, Davis AO, Ruby MV, Chaney RL, Lovre SC, Bergstrom PD (1993a) Bioavailability of arsenic in soil impacted by smelter activities following oral administration in rabbits. Fundam Appl Toxicol 21(1):83–88Google Scholar
  31. Freeman GB, Johnson JD, Llao SC, Schoof RA, Bergstrom PD (1993a) Pilot study of absolute bioavailability of arsenic in soil impacted by smelter activities following oral administration in rabbits and monkeys. In: Proceedings of International Conference on Arsenic Exposure and Health Effects, New Orleans, July 28–30, 1993, SEGH, 1–3Google Scholar
  32. Freeman GB, Johnson JD, Liao SC, Feder PI, Davis AO, Ruby MV, Schoof RA, Chaney RL, Bergstrom PD (1994) Absolute bioavailability of lead acetate and mining waste lead in rats. Toxicology 91(2):151–163Google Scholar
  33. Freeman GB, Schoof RA, Ruby MV, Davis AO, Dill JA, Liao SC, Lapin CA, Bergstrom PD (1995) Bioavailability of arsenic in soil and house dust impacted by smelter activities following oral administration in cynomolgus monkeys. Fundam Appl Toxicol 28(2):215–222Google Scholar
  34. Friedman HI, Nylund B (1980) Intestinal fat digestion, absorption, and transport. A review. Am J Clin Nutr 33(5):1108–1139Google Scholar
  35. Girouard E, Zagury GJ (2009) Arsenic bioaccessibility in CCA-contaminated soils: influence of soil properties, arsenic fractionation and particle-size fraction. Sci Total Environ 407(8):2576–2585Google Scholar
  36. Gorelick FS, Jamieson JD (1994) The pancreatic acinar cell: structure–functional relationship. In: Johnson LR (ed) Physiology of the gastrointestinal tract, vol. 2. Raven, New York, pp 1313–1352Google Scholar
  37. Groen K, Vaessen HAMG, Kliest JJG, Deboer JLM, Vanooik T, Timmerman A, Vlug RF (1994) Bioavailability of inorganic arsenic from bog containing soil in the dog. Environ Health Perspect 102(2):182–184Google Scholar
  38. Guyton AC (1991) Textbook of medical physiology. WB Saunders, PhiladelphiaGoogle Scholar
  39. Hack A, Selenka F (1996) Mobilization of PAH and PCB from contaminated soil using a digestive tract model. Toxicol Lett 88(1–3):199–210Google Scholar
  40. Hamel SC, Buckley B, Lioy PJ (1998) Bioaccessibility of metals in soils for different liquid to solid ratios in synthetic gastric fluid. Environ Sci Technol 32(3):358–362Google Scholar
  41. Hillgren KM, Kato A, Borchardt RT (1995) In-vitro systems for studying intestinal drug absorption. Med Res Rev 15(2):83–109Google Scholar
  42. Holman HYN (2000) In-vitro gastrointestinal mimetic protocol for measuring bioavailable contaminants. US Patent 6,040,188, University of California, USAGoogle Scholar
  43. Hughes MF, Menache M, Thompson DJ (1994) Dose-dependent disposition of sodium arsenate in mice following acute oral exposure. Fundam Appl Toxicol 22(1):80–89Google Scholar
  44. Hursh JB, Suomela J (1968) Absorption of 212Pb from the gastrointestinal tract of man. Acta Oncol 7(2):108–120Google Scholar
  45. Johnson LR (2001) Gastric secretion. In: Johnson LR (ed) Gastrointestinal physiology, 6th edn. Mosby Publishing, St. Louis, pp 1281–1310Google Scholar
  46. Juhasz AL, Smith E, Weber J, Rees M, Rofe A, Kuchel T, Sansom L, Naidu R (2007a) In-vitro assessment of arsenic bioaccessibility in contaminated (anthropogenic and geogenic) soils. Chemosphere 69(1):69–78Google Scholar
  47. Juhasz AL, Smith E, Weber J, Rees M, Rofe A, Kuchel T, Sansom L, Naidu R (2007b) Comparison of in vivo and in vitro methodologies for the assessment of arsenic bioavailability in contaminated soils. Chemosphere 69(6):961–966Google Scholar
  48. Juhasz A, Smith E, Weber J, Naidu R, Rees M, Rofe A, Kuchel T, Sansom L (2008) Effect of soil ageing on in vivo arsenic bioavailability in two dissimilar soils. Chemosphere 71(11):2180–2186Google Scholar
  49. Juhasz AL, Smith E, Weber J, Naidu R, Rees M, Rofe A, Kuchel T, Sansom L (2009a) Assessment of four commonly employed in vitro arsenic bioaccessibility assays for predicting in vivo arsenic bioavailability in contaminated soils. Environ Sci Technol 43(24):9487–9494Google Scholar
  50. Juhasz AL, Weber J, Smith E, Naidu R, Marschner B, Rees M, Rofe A, Kuchel T, Sansom L (2009b) Evaluation of SBRC-gastric and SBRC-intestinal methods for the prediction of in vivo relative lead bioavailability in contaminated soils. Environ Sci Technol 43(12):4503–4509Google Scholar
  51. Juhasz AL, Weber J, Naidu R, Gancarz D, Rofe A, Todor D, Smith E (2010) Determination of relative cadmium bioavailability in contaminated soils and it prediction using in vitro methodologies. Environ Sci Technol 44:5240–5247Google Scholar
  52. Juhasz AL, Weber J, Smith E (2011) Predicting arsenic relative bioavailability in contaminated soils using meta analysis and relative bioavailability–bioaccessibility regression models. Environ Sci Technol 45(24):10676–10683Google Scholar
  53. Kasprzak KS (2002) Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radic Biol Med 32(10):958–967Google Scholar
  54. Kelley ME, Brauning SE, Schoof RA, Ruby MV (2002) Assessing oral bioavailability of metals in soil. Battelle Press, Columbus, pp 1–124Google Scholar
  55. Kenyon EM, Hughes MF, Levander OA (1997) Influence of dietary selenium on the disposition of arsenate in the female B6C3F1 mouse. J Toxicol Environ Health A 51(3):279–299Google Scholar
  56. Kramer BK, Ryan PB (2000) Soxhlet and microwave extraction in determining the bioaccessibility of pesticides from soil and model solids. Proceedings of the 2000 Conference on Hazardous Waste Research, pp 196–210Google Scholar
  57. Krishnamohan M (2008) Carcinogenicity of monomethylarsonous acid (MMAIII) and sodium arsenate (AsV) and identification of early warning biomarkers. PhD thesis, The University of QueenslandGoogle Scholar
  58. Krishnamohan M, Qi L, Lam PKS, Moore MR, Ng JC (2007a) Urinary arsenic and porphyrin profile in C57BL/6J mice chronically exposed to monomethylarsonous acid (MMAIII) for two years. Toxicol Appl Pharmacol 224(1):89–97Google Scholar
  59. Krishnamohan M, Wu HJ, Huang SH, Maddelena R, Lam PKS, Moore MR, Ng JC (2007b) Urinary arsenic methylation and porphyrin profile of C57Bl/6J mice chronically exposed to sodium arsenate. Sci Total Environ 379(2–3):235–243Google Scholar
  60. Madara JL, Trier JS (1994) The functional morphology of the mucosa of the small intestine. In: Johnson LR (ed) Physiology of the gastrointestinal tract, vol. 2, 3rd edn. Raven, New York, pp 1577–1622Google Scholar
  61. Marafante E, Bertolero F, Edel J, Pietra R, Sabbioni E (1982) Intracellular interaction and biotransformation of arsenite in rats and rabbits. Sci Total Environ 24(1):27–39Google Scholar
  62. Marschner B, Welge P, Hack A, Wittsiepe J, Wilhelm M (2006) Comparison of soil Pb in vitro bioaccessibility and in vivo bioavailability with Pb pools from a sequential soil extraction. Environ Sci Technol 40(8):2812–2818Google Scholar
  63. Minekus M, Marteau P, Havenaar R, Huis in’t Veld JHJ (1995) A multicompartmental dynamic computer-controlled model simulating the stomach and small intestine. Altern Lab Anim 23(2):197–209Google Scholar
  64. Molly K, Van de Woestyne M, Verstraete W (1993) Development of a 5-step multi-chamber reactor as a simulation of the human intestinal microbial ecosystem. Appl Microbiol Biotechnol 39(2):254–258Google Scholar
  65. Moore MR, McColl KEL, Rimington C, Goldberg A (1987) Disorders of porphyrin metabolism. Plenum Medical Book Company, New YorkGoogle Scholar
  66. Naidu R, Bolan NS (2008) Contaminant chemistry in soils: key concepts and bioavailability. In: Naidu R (ed) Chemical bioavailability in terrestrial environment. Elsevier, Amsterdam, pp 9–38. ISBN 978-0-444-52169-9Google Scholar
  67. Naidu R, Bolan NS, Megharaj M, Juhasz AL, Gupta S, Clothier B, Schulin R (2008a) Bioavailability, definition, assessment and implications for risk assessment. In: Naidu R (ed) Chemical bioavailability in terrestrial environment. Elsevier, Amsterdam, pp 1–8, ISBN 978-0-444-52Google Scholar
  68. Naidu R, Pollard SJT, Bolan NS, Owens G, Pruszinski AW (2008b) Bioavailability: the underlying basis for risk based land management. In: Naidu R (ed) Chemical bioavailability in terrestrial environment. Elsevier, Amsterdam, pp 53–72, ISBN 978-0-444-52Google Scholar
  69. Naidu R, Nathanail P, Wong MH (2013a) Bioavailability—the underlying basis for risk based land management. Environ Sci Pollut Res Int (in this issue)Google Scholar
  70. Naidu R, Channey R, McConnell S, Johnston N, Semple KT, McGrath S, Dries V, Nathanail P, Harmsen J, Pruszinski A, MacMillan J, Palanisami T (2013b) Towards bioavailability-based soil criteria: past, present and future perspectives. Environ Sci Pollut Res. doi: 10.1007/S11356-013-1617-X
  71. Navarro MC, Pérez-Sirvent C, Martínez-Sánchez MJ, Vidal V, Marimón J (2006) Lead, cadmium and arsenic bioavailability in the abandoned mine site of Cabezo Rajao (Murcia, SE Spain). Chemosphere 63(3):484–489Google Scholar
  72. NEPC (1999) National Environment Protection (assessment of site contamination) measure 1999. National Environment Protection Council, AdelaideGoogle Scholar
  73. Ng JC, Moore MR (1996) Bioavailability of arsenic in soils from contaminated sites using a 96 hour rat blood model. In: Langley A, Markey B, Hill H (eds) The health risk assessment and management of contaminated sites. Contaminated Sites Monograph Series, No. 5. Commonwealth Department of Human Services and Health and the Environmental Protection Agency, South Australian Health Commission, Adelaide, pp 355–363Google Scholar
  74. Ng JC, Kratzmann SM, Qi L, Crawley H, Chiswell B, Moore MR (1998) Speciation and bioavailability: risk assessment of arsenic contaminated sites in a residential suburb in Canberra. Analyst 123:889–892Google Scholar
  75. Ng JC, Qi L, Wang JP, Xiao XL, Shahin M, Moore MR, Prakash AS (2001) Mutations in C57Bl/6J and metallothionein knock-out mice ingested sodium arsenate in drinking water for over two years. In: Chappell WR, Abernathy CO, Calderon RL (eds) Arsenic: exposure and health effects. Elsevier Science, Oxford, pp 231–242Google Scholar
  76. Ng JC, Bruce SL, Noller BN (2003a) Chapter 14: Laboratory and field evaluation of potential arsenic exposure from mine tailings to grazing cattle. In: Chappell WR, Abernathy CO, Calderon RL (eds) Arsenic: exposure and health effects. Elsevier Science, Oxford, pp 179–193Google Scholar
  77. Ng JC, Noller BN, Bruce SL, Moore M (2003b) Bioavailability of metals and arsenic at contaminated sites from cattle dips, mined land and naturally occurring mineralisation origins. In: Langley A, Gilbey M, Kennedy B (eds) Health and environmental assessment of site contamination, 5th edn. NEPC Service Corporation, Adelaide, pp 163–181Google Scholar
  78. Ng JC, Wang JP, Zheng BS, Zhai C, Maddalena R, Liu F, Moore MR (2005) Urinary porphyrins as biomarkers for arsenic exposure among susceptible populations in Guizhou province, China. Toxicol Appl Pharmacol 206(2):176–184Google Scholar
  79. Ng JC, Juhasz AL, Smith E, Naidu R (2010) Contaminant bioavailability and bioaccessibility: Part 1. Scientific and Technical Review. CRC CARE Technical Report 14. CRC for Contamination Assessment and Remediation of the Environment, Adelaide, Australia, pp 1–74Google Scholar
  80. NRC (National Research Council) (2003) Bioavailability of contaminants in soils and sediments: processes, tools and applications. The National Academies Press, WashingtonGoogle Scholar
  81. Odanaka Y, Matano O, Goto S (1980) Biomethylation of inorganic arsenic by the rat and some laboratory animals. Bull Environ Contam Toxicol 24(1):452–459Google Scholar
  82. Oomen AG (2000) Determinants of oral bioavailability of soil-borne contaminants. Dutch National Institute of Public Health and the Environment, Bilthoven, the NetherlandsGoogle Scholar
  83. Oomen AG, Hack A, Minekus M, Zeydner E, Cornelis C, Schoeters G, Verstraete W, Van de Wiele T, Wragg J, Rompelberg CJM, Sips AJAM, Van Wynen JH (2002) Comparison of five in vitro digestion models to study the bioaccessibility of soil contaminants. Environ Sci Technol 36(15):3326–3334Google Scholar
  84. Oomen AG, Rompelberg CJM, Bruil MA, Dobbe CJG, Pereboom DPKH, Sips AJAM (2003) Development of an in vitro digestion model for estimation of bioaccessibility of soil contaminants. Arch Environ Contam Toxicol 44(3):281–287Google Scholar
  85. Oomen AG, Rompelberg CJM, Van de Kemp E, Pereboom DPKH, De Zwart LL, Sips AJAM (2004) Effect of bile type on the bioaccessibility of soil contaminants in an in vitro digestion model. Arch Environ Contam Toxicol 46(2):183–188Google Scholar
  86. Owen BA (1990) Literature-derived absorption coefficients for 39 chemicals via oral and inhalation routes of exposure. Regul Toxicol Pharmacol 11(3):237–252Google Scholar
  87. Palumbo-Roe B, Klinck B (2007) Bioaccessibility of arsenic in mine waste-contaminated soils: a case study for an abandoned arsenic mine in SW England. J Environ Sci Health A 42(9):1251–1261Google Scholar
  88. Pelfrêne A, Waterlot C, Mazzuca M, Nisse C, Bidar G, Douay F (2011a) Assessing Cd, Pb, Zn human bioaccessibility in smelter-contaminated agricultural topsoils (northern France). Environ Geochem Health 33:477–493Google Scholar
  89. Pelfrêne A, Waterlot C, Douay F (2011b) In vitro digestion and DGT technique for estimating cadmium and lead bioavailability in contaminated soils: influence of gastric juice pH. Sci Total Environ 409:5076–5085Google Scholar
  90. Pomroy C, Charbonneau SM, McCullough RS, Tam GKH (1980) Human retention studies with 74As. Toxicol Appl Pharmacol 53(3):550–556Google Scholar
  91. Pouschat P, Zagury GJ (2006) In vitro gastrointestinal bioavailability of arsenic in soils collected near CCA-treated utility poles. Environ Sci Technol 40(13):4317–4323Google Scholar
  92. Rabinowitz MB, Wetherill GW, Kopple JD (1976) Kinetic analysis of lead metabolism in healthy humans. J Clin Invest 58(2):260–270Google Scholar
  93. Rees M, Sansom L, Rofe A, Juhasz AL, Smith E, Weber J, Naidu R, Kuchel T (2009) Principles and application of an in vivo swine assay for the determination of arsenic bioavailability in contaminated matrices. Environ Geochem Health 31(s1):167–177Google Scholar
  94. Roberts SM, Weimar WR, Vinson JRT, Munson JW, Bergeron RJ (2002) Measurement of arsenic bioavailability in soil using a primate model. Toxicol Sci 67(2):303–310Google Scholar
  95. Rodriguez RR, Basta NT, Casteel SW, Pace LW (1999) An in vitro gastrointestinal method to assess bioavailable arsenic in contaminated soils and solid media. Environ Sci Technol 33:642–649Google Scholar
  96. Rotard W, Christmann W, Knoth W, Mailahn W (1995) Bestimmung der resorptionsverfügbaren PCDD/PCDF aus Kieselrot. UWSF-Z Umweltchem Ökotox 7:3–9Google Scholar
  97. Roussel H, Waterlot C, Pelfrêne A, Pruvot C, Mazzuca M, Douay F (2010) Cd, Pb and Zn oral bioaccessibility of urban soils contaminated in the past by atmospheric emissions from two lead and zinc smelters. Arch Environ Contam Toxicol 58:945–954Google Scholar
  98. Ruby MV, Davis A, Kempton JH, Drexler JW, Bergstrom PD (1992) Lead bioavailability—dissolution kinetics under simulated gastric conditions. Environ Sci Technol 26(6):1242–1248Google Scholar
  99. Ruby MV, Davis A, Link TE, Schoof R, Chaney RL, Freeman GB, Bergstrom P (1993) Development of an in vitro screening test to evaluate the in vivo bioaccessibility of ingested mine-waste lead. Environ Sci Technol 27(13):2870–2877Google Scholar
  100. Ruby MV, Davis A, Schoof R, Eberle S, Sellstone CM (1996) Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environ Sci Technol 30(2):422–430Google Scholar
  101. Ruby MV, Schoof R, Brattin W, Goldade M, Post G, Harnois M, Mosby D, Casteel S, Berti W, Carpenter M, Edwards D, Cragin D, Chappell W (1999) Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environ Sci Technol 33(21):3697–3705Google Scholar
  102. Ruby MV, Fehling KA, Paustenbach DJ, Landenberger BD, Holsapple MP (2002) Oral bioaccessibility of dioxins/furans at low concentrations (50–350 ppt toxicity equivalent) in soil. Environ Sci Technol 36(22):4905–4911Google Scholar
  103. Sarkar D, Makris KC, Parra-Noonan MT, Datta R (2007) Effect of soil properties on arsenic fractionation and bioaccessibility in cattle and sheep dipping vat sites. Environ Int 33(2):164–169Google Scholar
  104. Schaider LA, Senn DB, Brabander DJ, McCarthy KD, Shine JP (2007) Characterization of zinc, lead, and cadmium in mine waste: implications for transport, exposure and bioavailability. Environ Sci Technol 41(11):4164–4171Google Scholar
  105. Schroder JL, Basta NT, Si J, Casteel SW, Evans T, Payton M (2003) In vitro gastrointestinal method to estimate relative bioavailable cadmium in contaminated soil. Environ Sci Technol 37:1365–1370Google Scholar
  106. Schroder JL, Basta NT, Casteel SW, Evans TJ, Payton ME, Si J (2004) Validation of the in vitro gastrointestinal (IVG) method to estimate relative bioavailable lead in contaminated soils. J Environ Qual 33:513–521Google Scholar
  107. Sips AJAM, Bruil MA, Dobbe CJG, van de Kamp E, Oomen AG, Pereboom DPKH, Rompelberg CJM, Zeilmaker MJ (2001) Bioaccessibility of contaminants from ingested soil in humans. Method and research on the bioaccessibility of lead and benzo[a]pyrene. RIVM report 711701012, National Institute for Public Health and the Environment, BilthovenGoogle Scholar
  108. Smith E, Weber J, Juhasz AL (2009) Arsenic distribution and bioaccessibility across particle size fractions in historically contaminated soils. Environ Geochem Health 31(s1):85–92Google Scholar
  109. Tam GKH, Charbonneau SM, Bryce F, Pomroy C, Sandi E (1979) Metabolism of inorganic arsenic (74As) in humans following oral ingestion. Toxicol Appl Pharmacol 50(2):319–322Google Scholar
  110. Tang X-Y, Tang L, Zhu YG, Xing BS, Duan J, Zheng MH (2006) Assessment of the bioaccessibility of polycyclic aromatic hydrocarbons in soils from Beijing using an in vitro test. Environ Pollut 140(2):279–285Google Scholar
  111. Tran HP, Prakash AS, Barnard R, Ng JC (2002) Arsenic inhibits the repair of DNA damage induced by benzo(a)pyrene. Toxicol Lett 133(1):59–67Google Scholar
  112. Tso P (1994) Intestinal lipid absorption. In: Johnson LR (ed) Physiology of the gastrointestinal tract, vol. 2, 3rd edn. Raven, New York, pp 1867–1907Google Scholar
  113. USEPA (1992) Toxicity characterization leaching procedure 1311. www.epa.gov/hazard/testmethods/SW846/pdfs1311.pdf. Accessed 25 December 2012
  114. USEPA (1994) Guidance manual for the integrated exposure uptake biokinetic model for lead in children, OSWER 9285.7-15-1, EPA/540/R-93/081. Office of Solid Waste and Emergency Response, United States Environmental Protection Agency, Washington, DC 20460Google Scholar
  115. USEPA (1996) Bioavailability of arsenic and lead in environmental substrates: results of an oral dosing study of immature swine, EPA 910/R-96-002. Superfund, United States Environmental Protection Agency, Washington, DC 20460Google Scholar
  116. USEPA (2007a) Guidance for evaluating the oral bioavailability of metals in soils for use in human health risk assessment, OSWER 9285.7-80. Office of Solid Waste and Emergency Response, United States Environment Protection Agency, Washington, DC 20460Google Scholar
  117. USEPA (2007b) Estimation of relative bioavailability of lead in soil and soil-like materials using in vivo and in vitro methods, OSWER 9285.7-77. Office of Solid Waste and Emergency Response, United States Environmental Protection Agency, Washington, DC 20460Google Scholar
  118. USEPA IEUBK (2007) User’s guide for the integrated exposure uptake biokinetic model for lead in children (IEUBK). Windows. USEPAGoogle Scholar
  119. USEPA (2008) Standard operating procedure for an in vitro bioaccessibility assay for lead in soil, EPA 9200.1-86. Office of Solid Waste and Emergency Response, United States Environment Protection Agency, Washington, DC 20460Google Scholar
  120. USEPA (2009) Validation assessment of in vitro lead bioaccessibility assay for predicting relative bioavailability of lead in soils and soil-like materials at superfund sites, OSWER 9200.3-51. United States Environment Protection Agency, Washington, DC 20460Google Scholar
  121. Vahter M (1994) Species differences in the metabolism of arsenic. In: Chappell WR, Abernathy CO, Cothern CR (eds) Arsenic: exposure and health. Science and Technology Letter, Northwood, UK, pp 171–179Google Scholar
  122. Vahter M, Norin H (1980) Metabolism of 74As-labeled trivalent and pentavalent inorganic arsenic in mice. Environ Res 21(2):446–457Google Scholar
  123. Vahter M, Couch R, Nermell B, Nilsson R (1995) Lack of methylation of inorganic arsenic in the chimpanzee. Toxicol Appl Pharmacol 133(2):262–268Google Scholar
  124. Van de Wiele TR, Oomen AG, Wragg J, Cave M, Minekus M, Hack A, Cornelis C, Rompelberg CJ, De Zwart LL, Klinck B, Van Wijnen J, Verstraete W, Sips AJ (2007) Comparison of five in vitro digestion models to in vivo experimental results: lead bioaccessibility in the human gastrointestinal tract. J Environ Sci Health A 42(9):1203–1211Google Scholar
  125. Walsh JH (1994) Gastrointestinal hormones. In: Johnson LR (ed) Physiology of the gastrointestinal tract, vol. 1. Raven, New York, pp 1–128Google Scholar
  126. Wang JP, Maddalena R, Zheng B, Zai C, Liu F, Ng JC (2009) Arsenicosis status and urinary malondialdehyde (MDA) in people exposed to arsenic contaminated-coal in China. Environ Int 35(3):502–506Google Scholar
  127. Weis CP, La Velle JM (1991) Characteristics to consider when choosing an animal model for the study of lead bioavailability. Chem Speciat Bioavailab 3:113–119Google Scholar
  128. Wildgrube HJ, Stockhausen H, Petri J, Füssel U, Lauer H (1986) Naturally occurring conjugated bile acids measured by high-performance liquid chromatography in human, dog and rabbit bile. J Chromatog A 353:207–213Google Scholar
  129. Williams TM, Rawlins BG, Smith B, Breward N (1998) In vitro determination of arsenic bioavailability in contaminated soil and mineral beneficiation waste from Ron Phibun, Ssouthern Thailand: a basis for improved human risk assessment. Environ Geochem Health 20(4):169–177Google Scholar
  130. Wittsiepe J, Schrey P, Hack A, Selenka F, Wilhelm M (2001) Comparison of different digestive tract models for estimating bioaccessibility of polychlorinated dibenzo-p-dioxins and dibenzofurans (PCDD/F) from red slag ‘Kieselrot’. Int J Hyg Environ Health 203(3):263–273Google Scholar
  131. Wragg J, Cave M, Nathanail P (2007) A study of the relationship between arsenic bioaccessibility and its solid-phase distribution in soils from Wellingborough, UK. J Environ Sci Health A 42(9):1303–1315Google Scholar
  132. Wragg J, Cave M, Basta N, Brandon E, Casteel S, Denys S, Gron C, Oomen A, Reimer K, Tack K, van de Wiele T (2011) An inter-laboratory trial of the unified BARGE bioaccessibility method for arsenic, cadmium and lead in soil. Sci Total Environ 409:4016–4030Google Scholar
  133. Yamauchi H, Yamamura Y (1979) Dynamic change of inorganic arsenic and methylarsenic compounds in human urine after oral intake as arsenic trioxide. Ind Health 17:79–83Google Scholar
  134. Yamauchi H, Yamamura Y (1985) Metabolism and excretion of orally administered arsenic trioxide in the hamster. Toxicology 34(2):113–121Google Scholar
  135. Yang J, Barnett MO, Jardine PM, Basta NT, Casteel SW (2002) Adsorption, sequestration, and bioaccessibility of As(V) in soils. Environ Sci Technol 36(21):4562–4569Google Scholar
  136. Yu CH, Yin LM, Lioy PJ (2006) The bioaccessibility of lead (Pb) from vacuumed house dust on carpets in urban residences. Risk Anal 26(1):125–134Google Scholar
  137. Zakharyan RA, Wildfang E, Aposhian HV (1996) Enzymatic methylation of arsenic compounds. III. The marmoset and tamarin, but not the rhesus, monkeys are deficient in methyltransferases that methylate inorganic arsenic. Toxicol Appl Pharmacol 140(1):77–84Google Scholar
  138. Zhitkovich A (2005) Importance of chromium–DNA adducts in mutagenicity and toxicity of chromium(VI). Chem Res Toxicol 18(1):3–11Google Scholar
  139. Ziegler EE, Edwards BB, Jensen RL, Mahaffy KR, Fomon S (1978) Absorption and retention of lead by infants. Pediatr Res 12(1):29–34Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Jack C. Ng
    • 1
    • 3
    Email author
  • Albert Juhasz
    • 2
    • 3
  • Euan Smith
    • 2
    • 3
  • Ravi Naidu
    • 2
    • 3
  1. 1.The University of Queensland, National Research Centre for Environmental Toxicology (Entox)BrisbaneAustralia
  2. 2.Centre for Environmental Risk Assessment and Remediation (CERAR)University of South AustraliaAdelaideAustralia
  3. 3.CRC—Contamination Assessment and Remediation of the EnvironmentAdelaideAustralia

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