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Tom Van de Wiele,¹ Lynn Vanhaecke,¹ Charlotte Boeckaert,¹ Kerry Peru,² John Headley,² Willy Verstraete,¹ and Steven Siciliano³

¹Laboratory of Microbial Ecology and Technology (LabMET), Ghent University, Gent, Belgium; ²National Water Research Institute, Environment Canada, Saskatoon, Saskatchewan, Canada; ³Department of Soil Research, University of Saskatchewan, Saskatoon, Saskatchewan, Canada

Abstract
Ingestion is an important exposure route for polycyclic aromatic hydrocarbons (PAHs) to enter the human body. Although the formation of hazardous PAH metabolites by human biotransformation enzymes is well documented, nothing is known about the PAH transformation potency of human intestinal microbiota. Using a gastrointestinal simulator, we show that human intestinal microbiota can also bioactivate PAHs, more in particular to estrogenic metabolites. PAH compounds are not estrogenic, and indeed, stomach and small intestine digestions of 62.5 nmol naphthalene, phenanthrene, pyrene, and benzo(a) pyrene showed no estrogenic effects in the human estrogen receptor bioassay. In contrast, colon digests of these PAH compounds displayed estrogenicity, equivalent to 0.31, 2.14, 2.70, and 1.48 nmol 17-ethynylestradiol (EE2) , respectively. Inactivating the colon microbiota eliminated these estrogenic effects. Liquid chromatography-mass spectrometry analysis confirmed the microbial PAH transformation by the detection of PAH metabolites 1-hydroxypyrene and 7-hydroxybenzo(a) pyrene in colon digests of pyrene and benzo(a) pyrene. Furthermore, we show that colon digests of a PAH-contaminated soil (simulated ingestion dose of 5 g/day) displayed estrogenic activity equivalent to 0.58 nmol EE2, whereas stomach or small intestine digests did not. Although the matrix in which PAHs are ingested may result in lower exposure concentrations in the gut, our results imply that the PAH bioactivation potency of colon microbiota is not eliminated by the presence of soil. Moreover, because PAH toxicity is also linked to estrogenicity of the compounds, the PAH bioactivation potency of colon microbiota suggests that current risk assessment may underestimate the risk from ingested PAHs. Key words: aryl hydrocarbon receptor, estrogen receptor, oral exposure, simulator of the human intestinal microbial ecosystem (SHIME) . Environ Health Perspect 113:6-10 (2005) . doi:10.1289/ehp.7259 available via http://dx.doi.org/ [Online 22 September 2004]

Address correspondence to W. Verstraete, Laboratory of Microbial Ecology and Technology, Ghent University, Coupure Links, 653, B-9000 Gent, Belgium. Telephone: 32-9-264-59-76. Fax: 32-9-264-62-48. E-mail: willy.verstraete@ugent.be

Supplemental Material is available online (http://ehp.niehs.nih.gov/members/2004/7259/supplemental.pdf) .

We thank S. Dobbelaere, N. Boon, S. Seurinck, K. Verthé, and K. Rabaey for critically reading the manuscript.

This research was supported by the Fund for Scientific Research.

The authors declare they have no competing financial interests.

Received 17 May 2004 ; accepted 22 September 2004.