{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T13:54:59Z","timestamp":1780494899023,"version":"3.54.1"},"reference-count":49,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2024,3,15]],"date-time":"2024-03-15T00:00:00Z","timestamp":1710460800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,3,28]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>The prevalence of azole-resistant Aspergillus fumigatus is increasing worldwide and is speculated to be related to the use of azole pesticides. Aspergillus spp., the causative agent of aspergillosis, could be brought into domestic dwellings through food. However, studies on azole-resistant Aspergillus spp. in food products are limited. Therefore, we aimed to isolate Aspergillus spp. from processed foods and commercial agricultural products and performed drug susceptibility tests for azoles. Among 692 food samples, we isolated 99 strains of Aspergillus spp. from 50 food samples, including vegetables (22.9%), citrus fruits (26.3%), cereals (25.5%), and processed foods (1.8%). The isolates belonged to 18 species across eight sections: Aspergillus, Candidi, Clavati, Flavi, Fumigati, Nidulantes, Nigri, and Terrei. The most frequently isolated section was Fumigati with 39 strains, followed by Nigri with 28 strains. Aspergillus fumigatus and A. welwitschiae were the predominant species. Ten A. fumigatus and four cryptic strains, four A. niger cryptic strains, two A. flavus, and four A. terreus strains exceeded epidemiological cutoff values for azoles. Aspergillus tubingensis, A. pseudoviridinutans, A. lentulus, A. terreus, and N. hiratsukae showed low susceptibility to multi-azoles. Foods containing agricultural products were found to be contaminated with Aspergillus spp., with 65.3% of isolates having minimal inhibitory concentrations below epidemiological cutoff values. Additionally, some samples harbored azole-resistant strains of Aspergillus spp. Our study serves as a basis for elucidating the relationship between food, environment, and clinically important Aspergillus spp.<\/jats:p>","DOI":"10.1093\/mmy\/myae026","type":"journal-article","created":{"date-parts":[[2024,3,15]],"date-time":"2024-03-15T06:49:51Z","timestamp":1710485391000},"source":"Crossref","is-referenced-by-count":7,"title":["Isolation of azole-resistant <i>Aspergillus<\/i> spp. from food products"],"prefix":"10.1093","volume":"62","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8081-4674","authenticated-orcid":false,"given":"Satomi","family":"Uehara","sequence":"first","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yumi","family":"Takahashi","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Keiko","family":"Iwakoshi","sequence":"additional","affiliation":[{"name":"Department of Food Safety, Tokyo Metropolitan Institute of Public Health , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yukari","family":"Nishino","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kotono","family":"Wada","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asuka","family":"Ono","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daisuke","family":"Hagiwara","sequence":"additional","affiliation":[{"name":"Faculty of Life and Environmental Sciences, University of Tsukuba MiCS, University of Tsukuba , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Takashi","family":"Chiba","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Keiko","family":"Yokoyama","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kenji","family":"Sadamasu","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Tokyo Metropolitan Insitute of Public Health , 3-24-1 Hyakunin-cho, Shinjuku-ku,Tokyo , Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,3,15]]},"reference":[{"key":"2024042216504980400_bib1","doi-asserted-by":"crossref","first-page":"1347","DOI":"10.3201\/eid2507.181625","article-title":"Environmental hotspots for azole resistance selection of Aspergillus fumigatus, the Netherlands","volume":"25","author":"Schoustra","year":"2019","journal-title":"Emerg Infect. Dis."},{"key":"2024042216504980400_bib2","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1111\/jam.14217","article-title":"Aspergillus species collected from environmental air samples in Portugal-molecular identification, antifungal susceptibility and sequencing of cyp51A gene on A. fumigatus sensu stricto itraconazole resistant","volume":"126","author":"Monteiro","year":"2019","journal-title":"J Appl Microbiol"},{"key":"2024042216504980400_bib3","doi-asserted-by":"crossref","first-page":"e02295","DOI":"10.1128\/AEM.02295-20","article-title":"Dynamics of Aspergillus fumigatus in azole fungicide-containing plant waste in the Netherlands (2016\u20132017)","volume":"87","author":"Zhang","year":"2021","journal-title":"Appl Environ Microbiol"},{"key":"2024042216504980400_bib4","doi-asserted-by":"crossref","first-page":"81","DOI":"10.3201\/eid2601.190885","article-title":"High azole resistance in Aspergillus fumigatus isolates from strawberry fields, China, 2018","volume":"26","author":"Chen","year":"2020","journal-title":"Emerg Infect. Dis."},{"key":"2024042216504980400_bib5","doi-asserted-by":"crossref","first-page":"599233","DOI":"10.3389\/fmicb.2020.599233","article-title":"The multi-fungicide resistance status of Aspergillus fumigatus populations in arable soils and the wider European environment","volume":"11","author":"Fraaije","year":"2020","journal-title":"Front Microbiol"},{"key":"2024042216504980400_bib6","first-page":"2379","article-title":"Epidemiological studies of pan-azole resistant Aspergillus fumigatus populations sampled during tulip cultivation show clonal expansion with acquisition of multi-fungicide resistance as potential driver","volume-title":"Microorganisms","author":"Fraaije","year":"2021"},{"key":"2024042216504980400_bib7","doi-asserted-by":"crossref","first-page":"19","DOI":"10.3390\/genes13010019","article-title":"Genetic diversity and dispersal of Aspergillus fumigatus in arctic soils","volume":"13","author":"Korfanty","year":"2021","journal-title":"Genes (Basel)"},{"key":"2024042216504980400_bib8","doi-asserted-by":"crossref","first-page":"292","DOI":"10.3390\/jof7040292","article-title":"Triazole-resistance in environmental Aspergillus fumigatus in Latin American and African countries","volume":"7","author":"Resendiz-Sharpe","year":"2021","journal-title":"J Fungi (Basel)"},{"key":"2024042216504980400_bib9","doi-asserted-by":"crossref","first-page":"113385","DOI":"10.1016\/j.envpol.2019.113385","article-title":"Mutation in cyp51A and high expression of efflux pump gene of Aspergillus fumigatus induced by propiconazole in liquid medium and soil","volume":"256","author":"Cao","year":"2020","journal-title":"Environ Pollut"},{"key":"2024042216504980400_bib10","doi-asserted-by":"crossref","first-page":"1237","DOI":"10.1016\/j.scitotenv.2018.08.247","article-title":"Tebuconazole induces triazole-resistance in Aspergillus fumigatus in liquid medium and soil","volume":"648","author":"Cui","year":"2019","journal-title":"Sci Total Environ"},{"key":"2024042216504980400_bib11","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1093\/cid\/cix257","article-title":"Intercountry transfer of triazole-resistant Aspergillus fumigatus on plant bulbs","volume":"65","author":"Dunne","year":"2017","journal-title":"Clin Infect Dis"},{"key":"2024042216504980400_bib12","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1584\/jpestics.D20-017","article-title":"Isolation of azole-resistant Aspergillus fumigatus from imported plant bulbs in Japan and the effect of fungicide treatment","volume":"45","author":"Hagiwara","year":"2020","journal-title":"J Pestic Sci"},{"key":"2024042216504980400_bib13","doi-asserted-by":"crossref","first-page":"1021","DOI":"10.1016\/j.jiac.2020.05.008","article-title":"Characteristics of azole-resistant Aspergillus fumigatus attached to agricultural products imported to Japan","volume":"26","author":"Nakano","year":"2020","journal-title":"J Infect Chemother"},{"key":"2024042216504980400_bib14","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1111\/ina.12108","article-title":"Evaluation of invasive aspergillosis risk of immunocompromised patients alternatively hospitalized in hematology intensive care unit and at home","volume":"24","author":"Rocchi","year":"2014","journal-title":"Indoor Air"},{"key":"2024042216504980400_bib15","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1093\/mmy\/myw007","article-title":"Domestic mould exposure and invasive aspergillosis-air sampling of Aspergillus spp. Spores in homes of hematological patients, a pilot study","volume":"54","author":"Schweer","year":"2016","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib16","doi-asserted-by":"crossref","first-page":"2815","DOI":"10.1128\/AAC.02487-12","article-title":"Is azole resistance in Aspergillus fumigatus a problem in Spain?","volume":"57","author":"Escribano","year":"2013","journal-title":"Antimicrob Agents Chemother"},{"key":"2024042216504980400_bib17","doi-asserted-by":"crossref","first-page":"1656","DOI":"10.3389\/fmicb.2018.01656","article-title":"Aspergillus species and antifungals susceptibility in clinical setting in the North of Portugal: cryptic species and emerging azoles resistance in A. fumigatus","volume":"9","author":"Pinto","year":"2018","journal-title":"Front Microbiol"},{"key":"2024042216504980400_bib18","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1128\/aem.61.4.1323-1330.1995","article-title":"Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes","volume":"61","author":"Glass","year":"1995","journal-title":"Appl Environ Microbiol"},{"key":"2024042216504980400_bib19","doi-asserted-by":"crossref","first-page":"1316","DOI":"10.1080\/15572536.2006.11832738","article-title":"Polyphasic taxonomy of Aspergillus fumigatus and related species","volume":"97","author":"Hong","year":"2005","journal-title":"Mycologia"},{"key":"2024042216504980400_bib20","doi-asserted-by":"crossref","first-page":"2725","DOI":"10.1093\/molbev\/mst197","article-title":"MEGA6: Molecular evolutionary genetics analysis version 6.0","volume":"30","author":"Tamura","year":"2013","journal-title":"Mol Biol Evol"},{"key":"2024042216504980400_bib21","article-title":"Reference method for broth dilution antifungal susceptibility testing of filamentous fungi","volume-title":"Approved Standard.CLSI Document M38-A3","author":"CLSI","year":"2017","edition":"3rd ed"},{"key":"2024042216504980400_bib22","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1128\/JCM.02136-10","article-title":"Use of epidemiological cutoff values to examine 9-year trends in susceptibility of Aspergillus species to the triazoles","volume":"49","author":"Pfaller","year":"2011","journal-title":"J Clin Microbiol"},{"key":"2024042216504980400_bib23","doi-asserted-by":"crossref","first-page":"254","DOI":"10.3358\/shokueishi.55.254","article-title":"Studies on rapid multi-residue analysis of pesticides in agricultural products by LC-MS\/MS","volume":"55","author":"Iwakoshi","year":"2014","journal-title":"Shokuhin Eiseigaku Zasshi"},{"key":"2024042216504980400_bib24","first-page":"jkab427","article-title":"Evidence for the agricultural origin of resistance to multiple antimicrobials in Aspergillus fumigatus, a fungal pathogen of humans","volume-title":"G3","author":"Kang","year":"2022"},{"key":"2024042216504980400_bib25","doi-asserted-by":"crossref","first-page":"4053","DOI":"10.1128\/AEM.00231-09","article-title":"Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles","volume":"75","author":"Snelders","year":"2009","journal-title":"Appl Environ Microbiol"},{"key":"2024042216504980400_bib26","doi-asserted-by":"crossref","first-page":"22","DOI":"10.3390\/jof7010022","article-title":"Hospital environment as a source of azole-resistant Aspergillus fumigatus strains with TR34\/L98H and G448S Cyp51A mutations","volume":"7","author":"Gonzalez-Jimenez","year":"2021","journal-title":"J Fungi (Basel)"},{"key":"2024042216504980400_bib27","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1080\/02652030500344811","article-title":"Occurrence of ochratoxin A in commodities and processed food \u2013 A review of EU occurrence data","volume":"22","author":"J\u00f8rgensen","year":"2005","journal-title":"Food Addit Contam"},{"key":"2024042216504980400_bib28","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/978-1-4615-0629-4_2","article-title":"Biology and ecology of mycotoxigenic Aspergillus species as related to economic and health concerns","volume":"504","author":"Wilson","year":"2002","journal-title":"Adv Exp Med Biol"},{"key":"2024042216504980400_bib29","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.jiac.2019.09.002","article-title":"Prospective survey of Aspergillus species isolated from clinical specimens and their antifungal susceptibility: A five-year single-center study in Japan","volume":"26","author":"Toyotome","year":"2020","journal-title":"J Infect Chemother"},{"key":"2024042216504980400_bib30","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1093\/mmy\/myz072","article-title":"Species identification, antifungal susceptibility, and clinical feature association of Aspergillus section Nigri isolates from the lower respiratory tract","volume":"58","author":"Takeda","year":"2020","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib31","doi-asserted-by":"crossref","first-page":"e02583","DOI":"10.1128\/AAC.02583-16","article-title":"Drug sensitivity and resistance mechanism in Aspergillus Section Nigri strains from Japan","volume":"61","author":"Hashimoto","year":"2017","journal-title":"Antimicrob Agents Chemother"},{"key":"2024042216504980400_bib32","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1089\/mdr.2018.0300","article-title":"Novel point mutations in cyp51A and cyp51B genes associated with itraconazole and posaconazole resistance in Aspergillus clavatus isolates","volume":"25","author":"Abastabar","year":"2019","journal-title":"Microb Drug Resist"},{"key":"2024042216504980400_bib33","doi-asserted-by":"crossref","first-page":"611","DOI":"10.1128\/JCM.03088-14","article-title":"Aspergillus citrinoterreus, a new species of section terrei isolated from samples of patients with nonhematological predisposing conditions","volume":"53","author":"Guinea","year":"2015","journal-title":"J Clin Microbiol"},{"key":"2024042216504980400_bib34","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.2217\/fmb-2018-0178","article-title":"Sequence analysis of isolates of Aspergillus from patients with chronic and allergic aspergillosis reveals a spectrum of cryptic species","volume":"13","author":"Bongomin","year":"2018","journal-title":"Future Microbiol"},{"key":"2024042216504980400_bib35","doi-asserted-by":"crossref","first-page":"e01374","DOI":"10.1128\/AAC.01374-20","article-title":"Multicentric analysis of the species distribution and antifungal susceptibility of cryptic isolates from Aspergillus Section Fumigati","volume":"64","author":"Imbert","year":"2020","journal-title":"Antimicrob Agents Chemother"},{"key":"2024042216504980400_bib36","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1093\/mmy\/myx085","article-title":"Species of Aspergillus section Aspergillus from clinical samples in the United States","volume":"56","author":"Siqueira","year":"2018","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib37","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1007\/s11046-013-9690-8","article-title":"Pulmonary aspergillosis and aflatoxins in chronic lung diseases","volume":"176","author":"Ali","year":"2013","journal-title":"Mycopathologia"},{"key":"2024042216504980400_bib38","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1111\/ina.12436","article-title":"Emergence of Aspergillus fumigatus azole resistance in azole-na\u00efve patients with chronic obstructive pulmonary disease and their homes","volume":"28","author":"Dauchy","year":"2018","journal-title":"Indoor Air"},{"key":"2024042216504980400_bib39","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.1080\/15287394.2012.721170","article-title":"Occupational exposure to Aspergillus by swine and poultry farm workers in Portugal","volume":"75","author":"Sabino","year":"2012","journal-title":"J Toxicol Environ Health A"},{"key":"2024042216504980400_bib40","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1093\/mmy\/myab027","article-title":"Different repartition of the cryptic species of black aspergilli according to the anatomical sites in human infections, in a French University hospital","volume":"59","author":"Gits-Muselli","year":"2021","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib41","doi-asserted-by":"crossref","first-page":"601","DOI":"10.3109\/13693786.2012.667578","article-title":"Rare and new etiological agents revealed among 178 clinical Aspergillus strains obtained from Czech patients and characterized by molecular sequencing","volume":"50","author":"Hubka","year":"2012","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib42","doi-asserted-by":"crossref","first-page":"71","DOI":"10.3314\/mmj.21-00014","article-title":"Ubiquitous distribution of azole-resistant Aspergillus fumigatus- related species in outdoor environments in Japan","volume":"62","author":"Watanabe","year":"2021","journal-title":"Med Mycol J"},{"key":"2024042216504980400_bib43","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1128\/AAC.05394-11","article-title":"Antifungal susceptibilities of Aspergillus fumigatus clinical isolates obtained in Nagasaki, Japan","volume":"56","author":"Tashiro","year":"2012","journal-title":"Antimicrob Agents Chemother."},{"key":"2024042216504980400_bib44","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1093\/mmy\/myz003","article-title":"Prospective multicenter surveillance of clinically isolated Aspergillus species revealed azole-resistant Aspergillus fumigatus isolates with TR34\/L98H mutation in the Kyoto and Shiga regions of Japan","volume":"57","author":"Tsuchido","year":"2019","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib45","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1111\/myc.13397","article-title":"The accuracy and clinical impact of the morphological identification of Aspergillus species in the age of cryptic species: A single-centre study","volume":"65","author":"Takeda","year":"2022","journal-title":"Mycoses"},{"key":"2024042216504980400_bib46","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1093\/mmy\/myu076","article-title":"Does farm fungicide use induce azole resistance in Aspergillus fumigatus?","volume":"53","author":"Kano","year":"2015","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/mmy\/myx016","article-title":"One-health pathogens in the Aspergillus viridinutans complex","volume":"56","author":"Talbot","year":"2018","journal-title":"Med Mycol"},{"key":"2024042216504980400_bib48","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1086\/599345","article-title":"Invasive aspergillosis due to Neosartorya udagawae","volume":"49","author":"Vinh","year":"2009","journal-title":"Clin Infect Dis"},{"key":"2024042216504980400_bib49","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1094\/PD-78-0971","article-title":"Reduction of imazalil effectiveness against citrus green mold in california packinghouses by resistant biotypes of Penicillium digitatum","volume":"78","author":"Eckert","year":"1994","journal-title":"Plant Dis"}],"container-title":["Medical Mycology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/mmy\/advance-article-pdf\/doi\/10.1093\/mmy\/myae026\/56991795\/myae026.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/mmy\/advance-article-pdf\/doi\/10.1093\/mmy\/myae026\/57301610\/myae026.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/mmy\/advance-article-pdf\/doi\/10.1093\/mmy\/myae026\/57301610\/myae026.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,4,22]],"date-time":"2024-04-22T16:51:14Z","timestamp":1713804674000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/mmy\/article\/doi\/10.1093\/mmy\/myae026\/7630188"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,15]]},"references-count":49,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2024,3,28]]}},"URL":"https:\/\/doi.org\/10.1093\/mmy\/myae026","relation":{},"ISSN":["1369-3786","1460-2709"],"issn-type":[{"value":"1369-3786","type":"print"},{"value":"1460-2709","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,4]]},"published":{"date-parts":[[2024,3,15]]},"article-number":"myae026"}}