Skip to main content
SpringerLink
Log in

Assessing the bioavailability and bioaccessibility of metals and metalloids

  • Bioavailability - the underlying basis for Risk Based Land Management
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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):50–58

    CAS  Google Scholar 

  • 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 1–19

    Google Scholar 

  • Alexander FW, Clayton BE, Delves HT (1974) Mineral and trace-metal balances in children receiving normal and synthetic diets. Quarterly J Med 43(169):89–111

    Google Scholar 

  • 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):551–554

    CAS  Google Scholar 

  • 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):655–661

    CAS  Google Scholar 

  • 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 117–139

  • 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 42:1275–1281

    CAS  Google Scholar 

  • Bridges CC, Zalpus RK (2005) Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharmacol 204(3):274–308

    CAS  Google Scholar 

  • 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 Queensland

  • 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):23–34

    CAS  Google Scholar 

  • 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):71–79

    CAS  Google Scholar 

  • 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):111–118

    CAS  Google Scholar 

  • 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):273–282

    CAS  Google Scholar 

  • 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):1–10

    CAS  Google Scholar 

  • 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):177–187

    CAS  Google Scholar 

  • 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):269–282

    CAS  Google Scholar 

  • Council of Standards Australia (1997) Australian standard leaching procedure (ASLP AS4439.1, As4439.2, AS4439.3). Council of Standards Australia, Australia

  • Daugherty AL, Mrsny RJ (1999) Transcellular uptake mechanisms of the intestinal epithelial barrier. Part one. Pharm Sci Technol Today 2(4):144–151

    CAS  Google Scholar 

  • 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):461–468

    CAS  Google Scholar 

  • Dean JR, Ma R (2007) Approaches to assess the oral bioaccessibility of persistent organic pollutants: a critical review. Chemosphere 68(8):1399–1407

    CAS  Google Scholar 

  • Degan LP, Philips SF (1996) Variability of gastrointestinal transit in healthy women and men. Gut 39(2):299–305

    Google Scholar 

  • Denys S, Caboche J, Tack K, Delalain P (2007) Bioaccessibility of lead in high carbonate soils. J Environ Sci Health A 42(9):1331–1339

    CAS  Google Scholar 

  • 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 46:6252–6260

    CAS  Google Scholar 

  • 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):189–198

    CAS  Google Scholar 

  • 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 191–198

  • Drexler JW, Brattin WJ (2007) An in vitro procedure for estimation of lead relative bioavailability: with validation. Hum Ecol Risk Assess 13(2):383–401

    CAS  Google Scholar 

  • enHealth (2004) Environmental health risk assessment—guidelines for assessing human health for environmental hazards. Department of Health and Ageing and enHealth Council, Canberra

    Google Scholar 

  • 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):2049–2055

    CAS  Google Scholar 

  • 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):388–398

    CAS  Google Scholar 

  • 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):83–88

    CAS  Google Scholar 

  • 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, 1–3

  • 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):151–163

    CAS  Google Scholar 

  • 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):215–222

    CAS  Google Scholar 

  • Friedman HI, Nylund B (1980) Intestinal fat digestion, absorption, and transport. A review. Am J Clin Nutr 33(5):1108–1139

    CAS  Google Scholar 

  • 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):2576–2585

    CAS  Google Scholar 

  • 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 1313–1352

  • 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):182–184

    CAS  Google Scholar 

  • Guyton AC (1991) Textbook of medical physiology. WB Saunders, Philadelphia

    Google Scholar 

  • Hack A, Selenka F (1996) Mobilization of PAH and PCB from contaminated soil using a digestive tract model. Toxicol Lett 88(1–3):199–210

    CAS  Google Scholar 

  • 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):358–362

    CAS  Google Scholar 

  • Hillgren KM, Kato A, Borchardt RT (1995) In-vitro systems for studying intestinal drug absorption. Med Res Rev 15(2):83–109

    CAS  Google Scholar 

  • Holman HYN (2000) In-vitro gastrointestinal mimetic protocol for measuring bioavailable contaminants. US Patent 6,040,188, University of California, USA

  • Hughes MF, Menache M, Thompson DJ (1994) Dose-dependent disposition of sodium arsenate in mice following acute oral exposure. Fundam Appl Toxicol 22(1):80–89

    CAS  Google Scholar 

  • Hursh JB, Suomela J (1968) Absorption of 212Pb from the gastrointestinal tract of man. Acta Oncol 7(2):108–120

    CAS  Google Scholar 

  • Johnson LR (2001) Gastric secretion. In: Johnson LR (ed) Gastrointestinal physiology, 6th edn. Mosby Publishing, St. Louis, pp 1281–1310

  • 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):69–78

    CAS  Google Scholar 

  • 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):961–966

    CAS  Google Scholar 

  • 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):2180–2186

    CAS  Google Scholar 

  • 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):9487–9494

    CAS  Google Scholar 

  • 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):4503–4509

    CAS  Google Scholar 

  • 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 44:5240–5247

    CAS  Google Scholar 

  • 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):10676–10683

    CAS  Google Scholar 

  • Kasprzak KS (2002) Oxidative DNA and protein damage in metal-induced toxicity and carcinogenesis. Free Radic Biol Med 32(10):958–967

    CAS  Google Scholar 

  • Kelley ME, Brauning SE, Schoof RA, Ruby MV (2002) Assessing oral bioavailability of metals in soil. Battelle Press, Columbus, pp 1–124

  • 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):279–299

    CAS  Google Scholar 

  • 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 196–210

  • Krishnamohan M (2008) Carcinogenicity of monomethylarsonous acid (MMAIII) and sodium arsenate (AsV) and identification of early warning biomarkers. PhD thesis, The University of Queensland

  • 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):89–97

    CAS  Google Scholar 

  • 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):235–243

    CAS  Google Scholar 

  • 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 1577–1622

  • 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):27–39

    CAS  Google Scholar 

  • 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):2812–2818

    CAS  Google Scholar 

  • 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):197–209

    Google Scholar 

  • 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):254–258

    CAS  Google Scholar 

  • Moore MR, McColl KEL, Rimington C, Goldberg A (1987) Disorders of porphyrin metabolism. Plenum Medical Book Company, New York

    Google Scholar 

  • 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 978-0-444-52169-9

  • 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 978-0-444-52

    Google Scholar 

  • 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 978-0-444-52

    Google Scholar 

  • Naidu R, Nathanail P, Wong MH (2013a) Bioavailability—the underlying basis for risk based land management. Environ Sci Pollut Res Int (in this issue)

  • 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

  • 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):484–489

    CAS  Google Scholar 

  • NEPC (1999) National Environment Protection (assessment of site contamination) measure 1999. National Environment Protection Council, Adelaide

    Google Scholar 

  • 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 355–363

    Google Scholar 

  • 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 123:889–892

    CAS  Google Scholar 

  • 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 231–242

    Google Scholar 

  • 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 179–193

    Google Scholar 

  • 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 163–181

    Google Scholar 

  • 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):176–184

    CAS  Google Scholar 

  • 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 1–74

  • NRC (National Research Council) (2003) Bioavailability of contaminants in soils and sediments: processes, tools and applications. The National Academies Press, Washington

    Google Scholar 

  • Odanaka Y, Matano O, Goto S (1980) Biomethylation of inorganic arsenic by the rat and some laboratory animals. Bull Environ Contam Toxicol 24(1):452–459

    CAS  Google Scholar 

  • Oomen AG (2000) Determinants of oral bioavailability of soil-borne contaminants. Dutch National Institute of Public Health and the Environment, Bilthoven, the Netherlands

    Google Scholar 

  • 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):3326–3334

    CAS  Google Scholar 

  • 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):281–287

    CAS  Google Scholar 

  • 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):183–188

    CAS  Google Scholar 

  • Owen BA (1990) Literature-derived absorption coefficients for 39 chemicals via oral and inhalation routes of exposure. Regul Toxicol Pharmacol 11(3):237–252

    CAS  Google Scholar 

  • 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):1251–1261

    CAS  Google Scholar 

  • 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 33:477–493

    Google Scholar 

  • 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 409:5076–5085

    Google Scholar 

  • Pomroy C, Charbonneau SM, McCullough RS, Tam GKH (1980) Human retention studies with 74As. Toxicol Appl Pharmacol 53(3):550–556

    CAS  Google Scholar 

  • Pouschat P, Zagury GJ (2006) In vitro gastrointestinal bioavailability of arsenic in soils collected near CCA-treated utility poles. Environ Sci Technol 40(13):4317–4323

    CAS  Google Scholar 

  • Rabinowitz MB, Wetherill GW, Kopple JD (1976) Kinetic analysis of lead metabolism in healthy humans. J Clin Invest 58(2):260–270

    CAS  Google Scholar 

  • 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):167–177

    CAS  Google Scholar 

  • 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):303–310

    CAS  Google Scholar 

  • 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 33:642–649

    CAS  Google Scholar 

  • Rotard W, Christmann W, Knoth W, Mailahn W (1995) Bestimmung der resorptionsverfügbaren PCDD/PCDF aus Kieselrot. UWSF-Z Umweltchem Ökotox 7:3–9

    CAS  Google Scholar 

  • 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 58:945–954

    CAS  Google Scholar 

  • Ruby MV, Davis A, Kempton JH, Drexler JW, Bergstrom PD (1992) Lead bioavailability—dissolution kinetics under simulated gastric conditions. Environ Sci Technol 26(6):1242–1248

    CAS  Google Scholar 

  • 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):2870–2877

    CAS  Google Scholar 

  • 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):422–430

    CAS  Google Scholar 

  • 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):3697–3705

    CAS  Google Scholar 

  • 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):4905–4911

    CAS  Google Scholar 

  • 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):164–169

    CAS  Google Scholar 

  • 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):4164–4171

    CAS  Google Scholar 

  • 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 37:1365–1370

    CAS  Google Scholar 

  • 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 33:513–521

    CAS  Google Scholar 

  • 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, Bilthoven

  • Smith E, Weber J, Juhasz AL (2009) Arsenic distribution and bioaccessibility across particle size fractions in historically contaminated soils. Environ Geochem Health 31(s1):85–92

    CAS  Google Scholar 

  • 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):319–322

    CAS  Google Scholar 

  • 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):279–285

    CAS  Google Scholar 

  • 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):59–67

    CAS  Google Scholar 

  • Tso P (1994) Intestinal lipid absorption. In: Johnson LR (ed) Physiology of the gastrointestinal tract, vol. 2, 3rd edn. Raven, New York, pp 1867–1907

  • USEPA (1992) Toxicity characterization leaching procedure 1311. www.epa.gov/hazard/testmethods/SW846/pdfs1311.pdf. Accessed 25 December 2012

  • 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 20460

  • 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 20460

  • 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 20460

  • 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 20460

  • USEPA IEUBK (2007) User’s guide for the integrated exposure uptake biokinetic model for lead in children (IEUBK). Windows. USEPA

  • 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 20460

  • 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 20460

  • 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 171–179

    Google Scholar 

  • Vahter M, Norin H (1980) Metabolism of 74As-labeled trivalent and pentavalent inorganic arsenic in mice. Environ Res 21(2):446–457

    CAS  Google Scholar 

  • Vahter M, Couch R, Nermell B, Nilsson R (1995) Lack of methylation of inorganic arsenic in the chimpanzee. Toxicol Appl Pharmacol 133(2):262–268

    CAS  Google Scholar 

  • 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):1203–1211

    Google Scholar 

  • Walsh JH (1994) Gastrointestinal hormones. In: Johnson LR (ed) Physiology of the gastrointestinal tract, vol. 1. Raven, New York, pp 1–128

  • 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):502–506

    CAS  Google Scholar 

  • Weis CP, La Velle JM (1991) Characteristics to consider when choosing an animal model for the study of lead bioavailability. Chem Speciat Bioavailab 3:113–119

    CAS  Google Scholar 

  • 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 353:207–213

    CAS  Google Scholar 

  • 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):169–177

    CAS  Google Scholar 

  • 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):263–273

    CAS  Google Scholar 

  • 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):1303–1315

    CAS  Google Scholar 

  • 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 409:4016–4030

    CAS  Google Scholar 

  • Yamauchi H, Yamamura Y (1979) Dynamic change of inorganic arsenic and methylarsenic compounds in human urine after oral intake as arsenic trioxide. Ind Health 17:79–83

    CAS  Google Scholar 

  • Yamauchi H, Yamamura Y (1985) Metabolism and excretion of orally administered arsenic trioxide in the hamster. Toxicology 34(2):113–121

    CAS  Google Scholar 

  • 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):4562–4569

    CAS  Google Scholar 

  • 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):125–134

    Google Scholar 

  • 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):77–84

    CAS  Google Scholar 

  • Zhitkovich A (2005) Importance of chromium–DNA adducts in mutagenicity and toxicity of chromium(VI). Chem Res Toxicol 18(1):3–11

    CAS  Google Scholar 

  • Ziegler EE, Edwards BB, Jensen RL, Mahaffy KR, Fomon S (1978) Absorption and retention of lead by infants. Pediatr Res 12(1):29–34

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The University of Queensland, National Research Centre for Environmental Toxicology (Entox), Brisbane, Queensland, 4108, Australia

    Jack C. Ng

  2. Centre for Environmental Risk Assessment and Remediation (CERAR), University of South Australia, Adelaide, Australia

    Albert Juhasz, Euan Smith & Ravi Naidu

  3. CRC—Contamination Assessment and Remediation of the Environment, Mawson Lakes, Adelaide, Australia

    Jack C. Ng, Albert Juhasz, Euan Smith & Ravi Naidu

Authors
  1. Jack C. Ng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Albert Juhasz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Euan Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ravi Naidu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jack C. Ng.

Additional information

Responsible editor: Céline Guéguen

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ng, J.C., Juhasz, A., Smith, E. et al. Assessing the bioavailability and bioaccessibility of metals and metalloids. Environ Sci Pollut Res 22, 8802–8825 (2015). https://doi.org/10.1007/s11356-013-1820-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-1820-9

Keywords

Search

Navigation