{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T12:35:07Z","timestamp":1787056507499,"version":"build-2736575974"},"reference-count":50,"publisher":"American Chemical Society (ACS)","issue":"13","license":[{"start":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T00:00:00Z","timestamp":1623628800000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-029"},{"start":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T00:00:00Z","timestamp":1623628800000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-037"},{"start":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T00:00:00Z","timestamp":1623628800000},"content-version":"stm-asf","delay-in-days":0,"URL":"https:\/\/doi.org\/10.15223\/policy-045"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,7,6]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Balkan endemic nephropathy (BEN) is a chronic tubulointerstitial nephropathy affecting residents of rural farming areas in many Balkan countries. Although it is generally believed that BEN is an environmental disease caused by multiple geochemical factors with much attention on aristolochic acids (AAs), its etiology remains controversial. In this study, we tested the hypothesis that environmental contamination and subsequent food contamination by polycyclic aromatic hydrocarbons (PAHs) and phthalate esters are AA toxicity factors and important to BEN development. We identified significantly higher concentrations of phenanthrene, anthracene, diethyl phthalate (DEP), dibutyl phthalate (DBP), and benzyl butyl phthalate (BBP) in both maize and wheat grain samples collected from endemic villages than from nonendemic villages. Other PAHs and phthalate esters were also detected at higher concentrations in the soil samples from endemic villages. Subsequent genotoxicity testing of cultured human kidney cells showed an alarming phenomenon that phenanthrene, DEP, BBP, and DBP can interact synergistically with AAs to form elevated levels of AA-DNA adducts, which are associated with both the nephrotoxicity and carcinogenicity of AAs, further increasing their disease risks. This study provides direct evidence that prolonged coexposure to these environmental contaminants via dietary intake may lead to greater toxicity and accelerated development of BEN.<\/jats:p>","DOI":"10.1021\/acs.est.1c00648","type":"journal-article","created":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T14:49:51Z","timestamp":1623682191000},"page":"9024-9032","source":"Crossref","is-referenced-by-count":26,"title":["Analysis\nof Polycyclic Aromatic Hydrocarbons and Phthalate\nEsters in Soil and Food Grains from the Balkan Peninsula: Implication on DNA Adduct Formation by Aristolochic\nAcid I and Balkan Endemic Nephropathy"],"prefix":"10.1021","volume":"55","author":[{"given":"Wanlin","family":"Guo","sequence":"first","affiliation":[{"name":"The Hong Kong University of Science and Technology , , Clear Water Bay , ,","place":["Kowloon, Hong Kong, 000000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiayin","family":"Zhang","sequence":"additional","affiliation":[{"name":"The Hong Kong University of Science and Technology , , Clear Water Bay , ,","place":["Kowloon, Hong Kong, 000000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhihan","family":"Sun","sequence":"additional","affiliation":[{"name":"The Hong Kong University of Science and Technology , , Clear Water Bay , ,","place":["Kowloon, Hong Kong, 000000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William H.","family":"Orem","sequence":"additional","affiliation":[{"name":"U.S. Geological Survey , , ,","place":["Reston, Virginia, United States, 20192"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3223-0594","authenticated-orcid":true,"given":"Calin A.","family":"Tatu","sequence":"additional","affiliation":[{"name":"University of Medicine and Pharmacy \u2033Victor Babes\u2033 Timisoara , , Pta. E. Murgu No.2 , ,","place":["Timisoara, Romania, 300041"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Niko S.","family":"Radulovic\u0301","sequence":"additional","affiliation":[{"name":"University of Nis\u030c , , ,","place":["Nis\u030c, Serbia, 18000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dragan","family":"Milovanovic\u0301","sequence":"additional","affiliation":[{"name":"Universitet u Nis\u030cu , ,","place":["Nis\u030c, Serbia, 18000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nikola M.","family":"Pavlovic\u0301","sequence":"additional","affiliation":[{"name":"Universitet u Nis\u030cu , ,","place":["Nis\u030c, Serbia, 18000"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8479-3172","authenticated-orcid":true,"given":"Wan","family":"Chan","sequence":"additional","affiliation":[{"name":"The Hong Kong University of Science and Technology , , Clear Water Bay , ,","place":["Kowloon, Hong Kong, 000000"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2021,6,14]]},"reference":[{"key":"2026081710284562700_cit1","doi-asserted-by":"publisher","first-page":"2595","DOI":"10.1007\/s00204-016-1819-3","article-title":"Balkan\nendemic nephropathy: An update\non its aetiology","volume":"90","author":"Stiborova\u0301","year":"2016","journal-title":"ArchToxicol"},{"key":"2026081710284562700_cit2","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1093\/ckj\/sft049","article-title":"Balkan\nendemic nephropathy\u2013current status and future perspectives","volume":"6","author":"Pavlovic\u0301","year":"2013","journal-title":"Clin. Kidney J."},{"key":"2026081710284562700_cit3","doi-asserted-by":"publisher","first-page":"183","DOI":"10.1016\/0278-6915(92)90031-f","article-title":"Epidemiology of Balkan endemic nephropathy","volume":"30","author":"C\u030ceovic\u0301","year":"1992","journal-title":"Food Chem. Toxicol."},{"key":"2026081710284562700_cit4","doi-asserted-by":"publisher","first-page":"409","DOI":"10.1080\/08860220902839097","article-title":"Fifty years of Balkan\nendemic nephropathy Challenges\nof study using epidemiological method","volume":"31","author":"Stefanovic","year":"2009","journal-title":"Renal\nFailure"},{"key":"2026081710284562700_cit5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1159\/000090705","article-title":"Etiology of\nBalkan endemic nephropathy and associated urothelial cancer","volume":"26","author":"Stefanovic","year":"2006","journal-title":"Am. J. Nephrol."},{"key":"2026081710284562700_cit6","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1016\/j.mrrev.2007.07.003","article-title":"Metabolic\nactivation of carcinogenic aristolochic acid, a risk factor for Balkan\nendemic nephropathy","volume":"658","author":"Stiborova\u0301","year":"2008","journal-title":"Mutat. Res., Rev. Mutat.\nRes."},{"key":"2026081710284562700_cit7","doi-asserted-by":"publisher","first-page":"689","DOI":"10.1289\/ehp.106-1533478","article-title":"The etiology of\nBalkan endemic nephropathy: Still more questions than answers","volume":"106","author":"Tatu","year":"1998","journal-title":"Environ. Health Perspect."},{"key":"2026081710284562700_cit8","first-page":"34","article-title":"Weathered coal deposits and Balkan endemic nephropathy","volume":"9","author":"Feder","year":"2002","journal-title":"Facta Univ."},{"key":"2026081710284562700_cit9","first-page":"228","article-title":"Balkan endemic nephropathy\netiology: A link between geochemistry and medicine","volume":"55","author":"Suciu","year":"2005","journal-title":"Timisoara Med. J."},{"key":"2026081710284562700_cit10","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10653-013-9515-1","article-title":"Organic\ncompounds in water extracts of coal: Links to Balkan endemic nephropathy","volume":"36","author":"Maharaj","year":"2014","journal-title":"Environ. Geochem. 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Rare\nDis."},{"key":"2026081710284562700_cit18","first-page":"S9","article-title":"Relationship between weathered coal\ndeposits and the etiology of Balkan endemic nephropathy","volume":"40","author":"Feder","year":"1991","journal-title":"Kidney Int. Suppl."},{"key":"2026081710284562700_cit19","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1579\/0044-7447(2007)36[98:heotos]2.0.co;2","article-title":"Health effects of toxic organic substances from coal: Toward \u2033panendemic\u2033\nnephropathy","volume":"36","author":"Orem","year":"2007","journal-title":"Ambio."},{"key":"2026081710284562700_cit20","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1038\/sj.jes.7500489","article-title":"Evaluation\nof the hypothesis that Balkan endemic nephropathy\nis caused by drinking water exposure to contaminants leaching from\nPliocene coal deposits","volume":"16","author":"Voice","year":"2006","journal-title":"J. Exposure Sci. 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Coal Geol."},{"key":"2026081710284562700_cit23","doi-asserted-by":"publisher","first-page":"5928","DOI":"10.1021\/acs.jafc.6b02203","article-title":"Quantitation of aristolochic acids\nin corn, wheat grain,\nand soil samples collected in Serbia: Identifying a novel exposure\npathway in the etiology of Balkan endemic nephropathy","volume":"64","author":"Chan","year":"2016","journal-title":"J. Agric. Food Chem."},{"key":"2026081710284562700_cit24","doi-asserted-by":"publisher","first-page":"2446","DOI":"10.1021\/acs.chemrestox.0c00229","article-title":"Determination of aristolochic\nacids in vegetables: Nephrotoxic and carcinogenic environmental pollutants\ncontaminating a broad swath of the food supply and driving incidence\nof Balkan endemic nephropathy","volume":"33","author":"Au","year":"2020","journal-title":"Chem. Res. Toxicol."},{"key":"2026081710284562700_cit25","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1002\/ijc.20564","article-title":"Human hepatic\nand renal microsomes, cytochromes P450 1A1\/2, NADPH: Cytochrome P450\nreductase and prostaglandin H synthase mediate the formation of aristolochic\nacid-DNA adducts found in patients with urothelial cancer","volume":"113","author":"Stiborova\u0301","year":"2005","journal-title":"Int. J. Cancer"},{"key":"2026081710284562700_cit26","doi-asserted-by":"publisher","first-page":"8","DOI":"10.2478\/v10102-010-0023-1","article-title":"Contribution\nof biotransformation enzymes to the development of renal injury and\nurothelial cancer caused by aristolochic acid: Urgent questions, difficult\nanswers","volume":"1","author":"Stiborova\u0301","year":"2008","journal-title":"Interdiscip. Toxicol."},{"key":"2026081710284562700_cit27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.taap.2019.114618","article-title":"Phenanthrene,\nbut not its isomer anthracene, effectively activates both human and\nmouse nuclear receptor constitutive androstane receptor (CAR) and\ninduces hepatotoxicity in mice","volume":"378","author":"Yang","year":"2019","journal-title":"Toxicol. Appl.\nPharmacol."},{"key":"2026081710284562700_cit28","doi-asserted-by":"publisher","first-page":"1695","DOI":"10.1093\/carcin\/bgg119","article-title":"Human cytosolic\nenzymes involved\nin the metabolic activation of carcinogenic aristolochic acid: Evidence\nfor reductive activation by human NAD (P) H: quinone oxidoreductase","volume":"24","author":"Stiborova\u0301","year":"2003","journal-title":"Carcinogenesis"},{"key":"2026081710284562700_cit29","doi-asserted-by":"publisher","first-page":"2141","DOI":"10.1007\/s00204-014-1360-1","article-title":"The influence of ochratoxin A on\nDNA adduct formation by the carcinogen aristolochic acid in rats","volume":"89","author":"Stiborova\u0301","year":"2015","journal-title":"Arch. Toxicol."},{"key":"2026081710284562700_cit30","first-page":"13","article-title":"The effects of heavy metal ions,\nphthalates and ochratoxin A on oxidation of carcinogenic aristolochic\nacid I causing Balkan endemic nephropathy","volume":"36","author":"Barta","year":"2015","journal-title":"Neuroendocrinol.\nLett."},{"key":"2026081710284562700_cit31","doi-asserted-by":"publisher","first-page":"104","DOI":"10.1016\/j.chroma.2005.10.013","article-title":"Determination\nof sixteen polycyclic aromatic hydrocarbons in aqueous and solid samples\nfrom an Italian wastewater treatment plant","volume":"1102","author":"Busetti","year":"2006","journal-title":"J. Chromatogr. A"},{"key":"2026081710284562700_cit32","doi-asserted-by":"publisher","first-page":"1084","DOI":"10.1007\/s00216-005-3218-0","article-title":"Determination\nof phthalate monoesters in human milk, consumer milk, and infant formula\nby tandem mass spectrometry (LC\u2013MS\u2013MS)","volume":"382","author":"Mortensen","year":"2005","journal-title":"Anal. Bioanal. Chem."},{"key":"2026081710284562700_cit33","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/S0003-2670(99)00829-6","article-title":"Determination of phthalates\nin water samples using polystyrene solid-phase extraction and liquid\nchromatography quantification","volume":"407","author":"Jara","year":"2000","journal-title":"Anal. Chim. Acta."},{"key":"2026081710284562700_cit34","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1021\/acs.chemrestox.8b00359","article-title":"Quantitation\nof DNA adducts in target and nontarget organs of aristolochic acid\nI-exposed rats: Correlating DNA adduct levels with organotropic activities","volume":"32","author":"Liu","year":"2019","journal-title":"Chem. Res. Toxicol."},{"key":"2026081710284562700_cit35","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1021\/acs.chemrestox.0c00004","article-title":"Quantitation\nof DNA adducts of aristolochic acids in repair-deficient cells: A\nmechanistic study of the DNA repair mechanism","volume":"33","author":"Au","year":"2020","journal-title":"Chem. Res. Toxicol."},{"key":"2026081710284562700_cit36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.envpol.2019.03.064","article-title":"Plastic film\nmulching increased the accumulation and human health risks of phthalate\nesters in wheat grains","volume":"250","author":"Shi","year":"2019","journal-title":"Environ. Pollut."},{"key":"2026081710284562700_cit37","doi-asserted-by":"publisher","first-page":"2051","DOI":"10.1002\/jssc.200900019","article-title":"Homogeneous\nliquid\u2013liquid extraction combined with high performance\nliquid chromatography-fluorescence detection for determination of\npolycyclic aromatic hydrocarbons in vegetables","volume":"32","author":"Zhao","year":"2009","journal-title":"J. Sep. Sci."},{"key":"2026081710284562700_cit38","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1016\/j.chroma.2013.11.017","article-title":"Determination of 23\nphthalic acid esters in food by liquid chromatography tandem mass\nspectrometry","volume":"1324","author":"Xu","year":"2014","journal-title":"J. Chromatogr. A"},{"key":"2026081710284562700_cit39","doi-asserted-by":"publisher","first-page":"1989","DOI":"10.1021\/acs.chemrestox.0c00170","article-title":"LC\u2013MS\/MS\ncoupled with a stable-isotope dilution method for the quantitation\nof thioproline-glycine: A novel metabolite in formaldehyde- and oxidative\nstress-exposed cells","volume":"33","author":"Pan","year":"2020","journal-title":"Chem. Res. Toxicol."},{"key":"2026081710284562700_cit40","doi-asserted-by":"publisher","first-page":"1815","DOI":"10.1021\/acs.chemrestox.0c00055","article-title":"Thioproline\nserves as an efficient\nantioxidant protecting human cells from oxidative stress and improves\ncell viability","volume":"33","author":"Ham","year":"2020","journal-title":"Chem. Res. Toxicol."},{"key":"2026081710284562700_cit41","doi-asserted-by":"publisher","first-page":"492","DOI":"10.1002\/ps.2780140506","article-title":"Relationships between\nlipophilicity and the distribution of non-ionised chemicals in barley\nshoots following uptake by the roots","volume":"14","author":"Briggs","year":"1983","journal-title":"Pestic.\nSci."},{"key":"2026081710284562700_cit42","doi-asserted-by":"publisher","first-page":"614","DOI":"10.1016\/j.envpol.2006.11.026","article-title":"Uptake of polycyclic aromatic hydrocarbons\nby maize plants","volume":"148","author":"Lin","year":"2007","journal-title":"Environ. Pollut."},{"key":"2026081710284562700_cit43","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-017-12437-w","article-title":"Uptake and translocation\nof polycyclic aromatic hydrocarbons (PAHs) and heavy metals by maize\nfrom soil irrigated with wastewater","volume":"7","author":"Zhang","year":"2017","journal-title":"Sci. Pep."},{"key":"2026081710284562700_cit44","doi-asserted-by":"publisher","first-page":"2634","DOI":"10.1039\/C2EM30433C","article-title":"Occurrence and risk\nassessment of polycyclic aromatic hydrocarbons in soil from the Tiefa\ncoal mine district, Liaoning, China","volume":"14","author":"Liu","year":"2012","journal-title":"J. Environ.\nMonit."},{"key":"2026081710284562700_cit45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1371\/journal.pone.0115863","article-title":"Accumulation,\nallocation, and risk assessment of polycyclic aromatic hydrocarbons\n(PAHs) in soil-Brassica chinensis system","volume":"10","author":"Zhang","year":"2015","journal-title":"PLoS\nOne"},{"key":"2026081710284562700_cit46","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1016\/j.jhazmat.2008.09.029","article-title":"Distribution of phthalate esters\nin urban soils of subtropical city, Guangzhou, China","volume":"164","author":"Zeng","year":"2009","journal-title":"J. Hazard. Mater."},{"key":"2026081710284562700_cit47","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1007\/s13593-014-0270-1","article-title":"Contamination and remediation of\nphthalic acid esters in agricultural soils in China: A review","volume":"35","author":"He","year":"2015","journal-title":"Agron. Sustainable Dev."},{"key":"2026081710284562700_cit48","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/w12030865","article-title":"Partition\nand fate of phthalate acid esters (PAEs)\nin a full-scale horizontal subsurface flow constructed wetland treating\npolluted river water","volume":"12","author":"Zheng","year":"2020","journal-title":"Water"},{"key":"2026081710284562700_cit49","unstructured":"Department of Environmental\nConservation\n          . Soil Cleanup Guidance; Final Commissioner Policy, CP-51, Alexander B. Grannis, Commissioner:\nNew York, 2010."},{"key":"2026081710284562700_cit50","doi-asserted-by":"publisher","first-page":"1554","DOI":"10.1021\/acs.est.9b05337","article-title":"Occurrence and environmental stability\nof aristolochic acids in groundwater collected from Serbia: Links\nto human exposure and Balkan endemic nephropathy","volume":"54","author":"Tung","year":"2019","journal-title":"Environ. Sci. Technol."}],"container-title":["Environmental Science &amp; Technology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acs.est.1c00648","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/esthag\/article-pdf\/55\/13\/9024\/3700628\/es1c00648.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/esthag\/article-pdf\/55\/13\/9024\/3700628\/es1c00648.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T14:45:14Z","timestamp":1786977914000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/esthag\/article\/55\/13\/9024\/383445\/Analysis-of-Polycyclic-Aromatic-Hydrocarbons-and"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,14]]},"references-count":50,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2021,6,14]]},"published-print":{"date-parts":[[2021,7,6]]}},"URL":"https:\/\/doi.org\/10.1021\/acs.est.1c00648","relation":{},"ISSN":["0013-936X","1520-5851"],"issn-type":[{"value":"0013-936X","type":"print"},{"value":"1520-5851","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,14]]}}}