{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,2]],"date-time":"2026-10-02T19:21:56Z","timestamp":1790968916528,"version":"4.1.0"},"reference-count":57,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2023,8,15]],"date-time":"2023-08-15T00:00:00Z","timestamp":1692057600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"University of Gdansk","award":["1220.121.9.2021"],"award-info":[{"award-number":["1220.121.9.2021"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>In this study, we investigated the occurrence of plasmid-mediated quinolone resistance (PMQR) in extended-spectrum \u03b2-lactamase- (ESBL) and\/or AmpC-type \u03b2-lactamase-producing Enterobacterales isolates from free-living birds in Poland. The prevalence of the qnrB19 gene was 63%, and the distribution of isolates in terms of bacterial species was as follows: 67% (22\/33) corresponded to Escherichia coli, 83% (5\/6) to Rahnella aquatilis, 44% (4\/9) to Enterobacter cloacae and 33% (1\/3) to Klebsiella pneumoniae. The qnrB19 gene was also found in a single isolate of Citrobacter freundii. The molecular characteristics of qnrB19-positive isolates pointed to extended-spectrum beta lactamase CTX-M as the most prevalent one (89%) followed by TEM (47%), AmpC (37%) and SHV (16%). This study demonstrates the widespread occurrence of PMQR-positive and ESBL\/AmpC-producing Enterobacterales isolates in fecal samples from wild birds. In this work, plasmid pAM1 isolated from Escherichia coli strain SN25556 was completely sequenced. This plasmid is 3191 nucleotides long and carries the qnrB19 gene, which mediates decreased susceptibility to quinolones. It shares extensive homology with other previously described small qnrB19-harboring plasmids. The nucleotide sequence of pAM1 showed a variable region flanked by an oriT locus and a Xer recombination site. The presence of a putative recombination site was detected, suggesting that interplasmid recombination events might have played a role in the development of pAM1. Our results highlight the broad geographical spread of ColE-type Qnr resistance plasmids in clinical and environmental isolates of Enterobacterales. As expected from the results of phenotypic susceptibility testing, no resistance genes other than qnrB19 were identified.<\/jats:p>","DOI":"10.3390\/ijms241612804","type":"journal-article","created":{"date-parts":[[2023,8,15]],"date-time":"2023-08-15T11:06:16Z","timestamp":1692097576000},"page":"12804","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["High Prevalence of Plasmid-Mediated Quinolone Resistance among ESBL\/AmpC-Producing Enterobacterales from Free-Living Birds in Poland"],"prefix":"10.3390","volume":"24","author":[{"given":"Beata","family":"Furmanek-Blaszk","sequence":"first","affiliation":[{"name":"Department of Microbiology, Faculty of Biology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marian","family":"Sektas","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Biology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8850-7276","authenticated-orcid":false,"given":"Bartosz","family":"Rybak","sequence":"additional","affiliation":[{"name":"Department of Environmental Toxicology, Faculty of Health Sciences with Institute of Maritime and Tropical Medicine, Medical University of Gdansk, Debowa Str. 23A, 80-204 Gdansk, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,8,15]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"e00007-19","DOI":"10.1128\/CMR.00007-19","article-title":"Transferable mechanisms of quinolone resistance from 1998 onward","volume":"32","author":"Ruiz","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"5638","DOI":"10.1073\/pnas.082092899","article-title":"Mechanism of plasmid-mediated quinolone resistance","volume":"99","author":"Tran","year":"2002","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1586\/14787210.6.5.685","article-title":"Plasmid-mediated quinolone resistance","volume":"6","author":"Cano","year":"2008","journal-title":"Expert Rev. Anti. Infect. Ther."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"475","DOI":"10.1128\/microbiolspec.PLAS-0006-2013","article-title":"Plasmid-mediated quinolone resistance","volume":"2","author":"Jacoby","year":"2014","journal-title":"Microbiol. Spectr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1016\/S0140-6736(97)07322-4","article-title":"Quinolone resistance from a transferable plasmid","volume":"351","author":"Pascual","year":"1998","journal-title":"Lancet"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"4979","DOI":"10.1128\/AAC.05187-11","article-title":"Citrobacter spp. as a source of qnrB alleles","volume":"55","author":"Jacoby","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"664","DOI":"10.1128\/CMR.00016-09","article-title":"Plasmid-mediated quinolone resistance: A multifaceted threat","volume":"22","author":"Strahilevitz","year":"2009","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1278","DOI":"10.1093\/jac\/dkr084","article-title":"International collaborative study on the occurrence of plasmid-mediated quinolone resistance in Salmonella enterica and Escherichia coli isolated from animals, humans, food and the environment in 13 European countries","volume":"66","author":"Veldman","year":"2011","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Miranda, C.D., Concha, C., Godoy, F.A., and Lee, M.R. (2022). Aquatic environments as hotspots of transferable low-level quinolone resistance and their potential contribution to high-level quinolone resistance. Antibiotics, 11.","DOI":"10.3390\/antibiotics11111487"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"4019","DOI":"10.1128\/AAC.00294-09","article-title":"Characterization of the plasmid-borne quinolone resistance gene qnrB19 in Salmonella enterica serovar Typhimurium","volume":"53","author":"Dionisi","year":"2009","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1093\/jac\/dkp383","article-title":"pSGI15, a small ColE-like qnrB19 plasmid of a Salmonella enterica serovar Typhimurium strain carrying Salmonella genomic island 1 (SGI1)","volume":"65","author":"Hammerl","year":"2010","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"2467","DOI":"10.1128\/AAC.01615-12","article-title":"Differential distribution of plasmid-mediated quinolone resistance genes in clinical Enterobacteria with unusual phenotypes of quinolone susceptibility from Argentina","volume":"57","author":"Andres","year":"2013","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2826","DOI":"10.3389\/fmicb.2019.02826","article-title":"Diverse fluoroquinolone resistance plasmids from retail meat E. coli in United States","volume":"10","author":"Tyson","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Juraschek, K., Malekzadah, J., Malorny, B., Kasbohrer, A., Schwarz, S., Meemken, D., and Hammerl, J.A. (2022). Characterization of qnrB-carrying plasmids from ESBL- and non-ESBL-producing Escherichia coli. BMC Genom., 23.","DOI":"10.1186\/s12864-022-08564-y"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2929","DOI":"10.1128\/AAC.00349-08","article-title":"ISEcp1-mediated transposition of qnrB-like gene in Escherichia coli","volume":"52","author":"Cattoir","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1128\/AAC.00866-10","article-title":"qnrB19 gene bracketed by IS26 on a 40-kilobase IncR plasmid from an Escherichia coli isolate from a veal calf","volume":"55","author":"Hordijk","year":"2011","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1016\/j.ijantimicag.2010.02.015","article-title":"Characterisation of qnr plasmid-mediated quinolone resistance in Enterobacteriaceae from Italy: Association of the qnrB19 allele with the integron element ISCR1 in Escherichia coli","volume":"35","author":"Richter","year":"2010","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1093\/jac\/dks024","article-title":"Detection of qnr genes among Escherichia coli isolates of animal origin and complete sequence of the conjugative qnrB19-carrying plasmid pQNR2078","volume":"67","author":"Schink","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1821","DOI":"10.1128\/AAC.06036-11","article-title":"Small plasmids harboring qnrB19: A model for plasmid evolution mediated by site-specific recombination at oriT and Xer sites","volume":"56","author":"Tran","year":"2012","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Ares-Arroyo, M., Rocha, E.P.C., and Gonzalez Zorn, B. (2021). Evolution of ColE1-like plasmids across \u03b3-Proteobacteria: From bacteriocin production to antimicrobial resistance. PLoS Genet., 17.","DOI":"10.1371\/journal.pgen.1009919"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Rybak, B., Krawczyk, B., Furmanek-Blaszk, B., Wysocka, M., Fordon, M., Ziolkowski, P., Meissner, W., Stepniewska, K., and Sikorska, K. (2022). Antibiotic resistance, virulence and phylogenetic analysis of Escherichia coli strains isolated from free-living birds in human habitats. PLoS ONE, 17.","DOI":"10.1371\/journal.pone.0262236"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Amin, M.B., Saha, S.R., Islam, M.R., Haider, S.M.A., Hossain, M.I., Chowdhury, A.S.M.H.K., Rousham, C.K., and Islam, M.A. (2021). High prevalence of plasmid-mediated quinolone resistance (PMQR) among E. coli from aquatic environments in Bangladesh. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0261970"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.ygeno.2009.09.002","article-title":"Bacterial genomic G+C composition-eliciting environmental adaptation","volume":"95","author":"Mann","year":"2010","journal-title":"Genomics"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1111\/j.1574-6968.2010.02119.x","article-title":"Characterization of antimicrobial resistance in Salmonella enterica food and animal isolates from Colombia: Identification of a qnrB19-mediated quinolone resistance marker in two novel serovars","volume":"313","author":"Karczmarczyk","year":"2010","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1006\/plas.1997.1303","article-title":"Characterization of the replication and mobilization regions of the multiresistance Klebsiella pneumoniae plasmid pJHCMW1","volume":"38","author":"Dery","year":"1997","journal-title":"Plasmid"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Lin, M.-H., Fu, J.-F., and Liu, S.-T. (2013). A repeat sequence causes competition of ColE1-type plasmids. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0061668"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3427","DOI":"10.1128\/AAC.00493-08","article-title":"The KQ element, a complex genetic region conferring transferable resistance to carbapenems, aminoglycosides, and fluoroquinolones in Klebsiella pneumoniae","volume":"52","author":"Rice","year":"2008","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1128\/AAC.49.1.447-450.2005","article-title":"ISEcp1B-mediated transposition of blaCTX-M in Escherichia coli","volume":"49","author":"Poirel","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2938","DOI":"10.1128\/AAC.47.9.2938-2945.2003","article-title":"Insertion sequence ISEcp1B is involved in expression and mobilization of a blaCTX-M \u03b2-lactamase gene","volume":"47","author":"Poirel","year":"2003","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e00088-17","DOI":"10.1128\/CMR.00088-17","article-title":"Mobile genetic elements associated with antimicrobial resistance","volume":"31","author":"Partridge","year":"2018","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"113","DOI":"10.3109\/03009734.2014.905663","article-title":"Antibiotic resistance in wild birds","volume":"19","author":"Bonnedahl","year":"2014","journal-title":"Upsala J. Med. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1121","DOI":"10.1093\/jac\/dkx488","article-title":"Plasmids carrying antimicrobial resistance in Enterobacteriaceae","volume":"73","author":"Rozwandowicz","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1089\/mdr.2016.0067","article-title":"Detection of a novel qnrB19-carrying plasmid variant mediating decreased fluoroquinolone susceptibility in Salmonella eneterica serovar Hadar","volume":"23","author":"Fiegen","year":"2017","journal-title":"Mircob. Drug Resist."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2632","DOI":"10.1128\/AAC.01722-08","article-title":"High prevalence of qnr genes in commensal enterobacteria from healthy children in Peru and Bolivia","volume":"53","author":"Pallecchi","year":"2009","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1128\/AAC.01160-09","article-title":"Characterization of small ColE-like plasmids mediating widespread dissemination of the qnrB19 gene in commensal enterobacteria","volume":"54","author":"Pallecchi","year":"2010","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1176","DOI":"10.1093\/jac\/dkr026","article-title":"Small qnrB-harbouring ColE-like plasmids widespread in commensal enterobacteria from a remote Amazonas population not exposed to antibiotics","volume":"66","author":"Pallecchi","year":"2011","journal-title":"J. Antimcrob. Chemother."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"648","DOI":"10.1128\/AEM.02459-14","article-title":"Plasmid \u2013mediated resistance to cephalosporins and fluoroquinolones in various Escherichia coli sequence types isolated from rooks wintering in Europe","volume":"81","author":"Jamborova","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e845","DOI":"10.1002\/mbo3.845","article-title":"Antimicrobial resistant and extended-spectrum \u03b2-lactamase producing Escherichia coli in common wild bird species in Switzerland","volume":"8","author":"Zurfluh","year":"2019","journal-title":"MicrobiologyOpen"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1007\/s00248-019-01375-x","article-title":"First report of KPC-2 and KPC-3-producing Enterobacteriaceae in wild birds in Africa","volume":"79","author":"Chairat","year":"2020","journal-title":"Microb. Ecol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Bonnedahl, J., Drobni, M., Gauthier-Clerc, M., Hernandez, J., Granholm, S., Kayser, Y., Melhus, A., Kahlmeter, G., Waldenstrom, J., and Johansson, A. (2009). Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the South of France. PLoS ONE, 4.","DOI":"10.1371\/journal.pone.0005958"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1111\/j.1758-2229.2010.00148.x","article-title":"CTX-M-15-type extended-spectrum beta-lactamases-producing Escherichia coli from wild birds in Germany","volume":"2","author":"Guenther","year":"2010","journal-title":"Environ. Microbiol. Rep."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1007\/s00248-015-0718-0","article-title":"Wild birds, frequent carriers of extended-spectrum \u03b2-lactamase (ESBL) producing Escherichia coli of CTX-M and SHV-12 types","volume":"72","author":"Alcala","year":"2016","journal-title":"Microb. Ecol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1089\/mdr.2018.0004","article-title":"Colonization with Enterobacteriaceae-producing ESBLs, AmpCs, and OXA-48 in wild avian species, Spain 2015\u20132016","volume":"24","author":"Oteo","year":"2018","journal-title":"Microb. Drug Resist."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1186\/s13028-015-0166-3","article-title":"Carriage of CTX-M type extended spectrum \u03b2-lactamases (ESBL) in gulls across Europe","volume":"57","author":"Stedt","year":"2015","journal-title":"Acta Vet. Scand."},{"key":"ref_45","first-page":"10","article-title":"Overview of ESBL-producing Enterobacteriaceae from a Nordic perspective","volume":"4","author":"Brolund","year":"2014","journal-title":"Infect. Ecol. Epidemiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2954","DOI":"10.1093\/jac\/dkt260","article-title":"NDM-1 carbapenemase-producing Salmonella enterica subsp. enterica serovar Corvallis isolated from a wild bird in Germany","volume":"68","author":"Fischer","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1224","DOI":"10.1002\/ece3.2707","article-title":"VIM-1 carbapenemase producing Escherichia coli in gulls from southern France","volume":"7","author":"Vittecoq","year":"2017","journal-title":"Ecol. Evol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"803","DOI":"10.3201\/eid1305.061293","article-title":"Expanded-spectrum \u03b2-lactamase and plasmid-mediated quinolone resistance","volume":"13","author":"Poirel","year":"2007","journal-title":"Emerg. Infect. Dis."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Athanasakopoulou, Z., Reinicke, M., Diezel, C., Sofia, M., Chatzopoulos, D.C., Braun, S.D., Reissig, A., Spyrou, V., Monecke, V., and Ehricht, R. (2021). Antimicrobial resistance genes in ESBL-producing Escherichia coli isolates from animals in Greece. Antibiotics, 10.","DOI":"10.3390\/antibiotics10040389"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Silva-Sanchez, J., Cruz-Trujillo, E., Barrios, H., Reyna-Flores, F., Sanchez-Perez, A., Garza-Ramos, U., and Bacterial Resistance Consortium (2013). Characterization of plasmid-mediated quinolone resistance (PMQR) genes in extended-spectrum \u03b2-lactamase\u2013producing Enterobacteriaceae pediatric clinical isolates in Mexico. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0077968"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1016\/j.ijantimicag.2014.09.019","article-title":"Co-existence of plasmid-mediated quinolone resistance determinants and mutation in gyrA and parC among fluoroquinolone-resistant clinical Enterobacteriaceae isolated in tertiary hospital in Warsaw, Poland","volume":"45","author":"Piekarska","year":"2015","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"249","DOI":"10.17219\/acem\/94165","article-title":"Emergence of Enterobacteriaceae co-producing CTX-M-15, ArmA and PMQR in Poland","volume":"28","author":"Piekarska","year":"2019","journal-title":"Adv. Clin. Exp. Med."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"10818","DOI":"10.1007\/s11356-016-6221-4","article-title":"Prevalence of plasmid-mediated multidrug resistance determinants in fluoroquinolone-resistant bacteria isolated from sewage and surface water","volume":"23","author":"Osinska","year":"2016","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"151834","DOI":"10.1016\/j.scitotenv.2021.151834","article-title":"A rich mosaic of resistance in extended-spectrum \u03b2-lactamase-producing Escherichia coli isolated from red foxes (Vulpes vulpes) in Poland as a potential effect of increasing synanthropization","volume":"818","author":"Osinska","year":"2022","journal-title":"Sci. Total Environ."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"656223","DOI":"10.3389\/fmicb.2021.656223","article-title":"Antimicrobial resistance glides in the sky-free living birds as a reservoir of resistant Escherichia coli with zoonotic potential","volume":"12","author":"Skarzynska","year":"2021","journal-title":"Front. Microbiol."},{"key":"ref_56","unstructured":"Clinical Laboratory Standards Institute (CLSI) (2020). Performance Standards for Antimicrobial Susceptibility Testing, Clinical and Laboratory Standards Institute. [30th ed.]. CLSI Supplement M100."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1093\/jac\/dkm204","article-title":"Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates","volume":"60","author":"Cattoir","year":"2007","journal-title":"J. Antimicrob. Chemother."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/16\/12804\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:33:49Z","timestamp":1760128429000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/16\/12804"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,8,15]]},"references-count":57,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["ijms241612804"],"URL":"https:\/\/doi.org\/10.3390\/ijms241612804","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,8,15]]}}}