{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,26]],"date-time":"2026-08-26T08:00:51Z","timestamp":1787731251430,"version":"build-2784847793"},"reference-count":46,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2023,5,14]],"date-time":"2023-05-14T00:00:00Z","timestamp":1684022400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Education, University and Scientific Research (MIUR), Italy","award":["PON_INN_RTDA_2021_62"],"award-info":[{"award-number":["PON_INN_RTDA_2021_62"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Escherichia coli is the bacterial pathogen most frequently associated with mare infertility. Here, we characterized 24 E. coli strains isolated from mares which presented signs of endometritis and infertility from a genotypic and phenotypic point of view. The majority of the isolates belonged to phylogenetic group B1 (9\/24, 37.5%). Regarding antibiotic resistance profiles, 10 out of 24 (41.7%) were multidrug-resistant (MDR). Moreover, 17 out of 24 (70.8%) were strong or moderate biofilm producers, and of these eight were MDR strains. Interestingly, 21 out of 24 (87.5%) E. coli strains were phenotypically resistant to ampicillin and 10 of them were also resistant to amoxicillin with clavulanic acid. Regarding the presence of selected virulence factors, 50% of the examined strains carried at least three of them, with fimH detected in all strains, and followed by kpsMTII (11\/24, 45.9%). No strain was able to invade HeLa cell monolayers. No relevant differences for all the investigated characteristics were shown by strains that grew directly on plates versus strains requiring the broth-enrichment step before growing on solid media. In conclusion, this work provides new insight into E. coli strains associated with mares\u2019 infertility. These results broaden the knowledge of E. coli and, consequently, add useful information to improve prevention strategies and therapeutic treatments contributing to a significant increase in the pregnancy rate in mares.<\/jats:p>","DOI":"10.3390\/ani13101639","type":"journal-article","created":{"date-parts":[[2023,5,15]],"date-time":"2023-05-15T08:28:16Z","timestamp":1684139296000},"page":"1639","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Genotypic and Phenotypic Characterization of Escherichia coli Isolates Recovered from the Uterus of Mares with Fertility Problems"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1789-7603","authenticated-orcid":false,"given":"Francesca Paola","family":"Nocera","sequence":"first","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples \u2018Federico II\u2019, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Linda","family":"Maurizi","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Angelo","family":"Masullo","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples \u2018Federico II\u2019, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mauro","family":"Nicoletti","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonietta Lucia","family":"Conte","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9067-6343","authenticated-orcid":false,"given":"Francesca","family":"Brunetti","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9730-2926","authenticated-orcid":false,"given":"Luisa","family":"De Martino","sequence":"additional","affiliation":[{"name":"Department of Veterinary Medicine and Animal Production, University of Naples \u2018Federico II\u2019, Via F. Delpino 1, 80137 Naples, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5474-007X","authenticated-orcid":false,"given":"Carlo","family":"Zagaglia","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7290-3813","authenticated-orcid":false,"given":"Catia","family":"Longhi","sequence":"additional","affiliation":[{"name":"Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,5,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Laseca, N., Anaya, G., Pe\u00f1a, Z., Pirosanto, Y., Molina, A., and Demyda Peyr\u00e1s, S. (2021). Impaired reproductive function in equines: From genetics to genomics. Animals, 11.","DOI":"10.3390\/ani11020393"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/j.tvjl.2005.08.005","article-title":"Making sense of equine uterine infections: The many faces of physical clearance","volume":"172","author":"Causey","year":"2006","journal-title":"Vet. J."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1111\/j.1439-0531.2009.01485.x","article-title":"Clinical and subclinical endometritis in the mare: Both threats to fertility","volume":"44","author":"LeBlanc","year":"2009","journal-title":"Reprod. Domest. Anim."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1186\/1751-0147-44-121","article-title":"Uterine microbiology and antimicrobial susceptibility in isolated bacteria from mares with fertility problems","volume":"44","author":"Albihn","year":"2003","journal-title":"Acta Vet. Scand."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.rvsc.2007.02.008","article-title":"Retrospective study of bacterial isolates and their antimicrobial susceptibilities in equine uteri during fertility problems","volume":"84","author":"Frontoso","year":"2008","journal-title":"Res. Vet. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Reshadi, P., Heydari, F., Ghanbarpour, R., Bagheri, M., Jajarmi, M., Amiri, M., Alizade, H., Badouei, M.A., Sahraei, S., and Adib, N. (2021). Molecular characterization and antimicrobial resistance of potentially human-pathogenic Escherichia coli strains isolated from riding horses. BMC Vet. Res., 17.","DOI":"10.1186\/s12917-021-02832-x"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1093\/infdis\/jiv429","article-title":"Extraintestinal pathogenic Escherichia coli, a common human pathogen: Challenges for vaccine development and progress in the field","volume":"213","author":"Poolman","year":"2016","journal-title":"J. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.vetmic.2018.08.009","article-title":"Multi-drug resistant Escherichia coli in diarrhoeagenic foals: Pulsotyping, phylotyping, serotyping, antibiotic resistance and virulence profiling","volume":"223","author":"Kennedy","year":"2018","journal-title":"Vet. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"661","DOI":"10.1177\/104063870802000524","article-title":"Bronchopneumonia associated with extraintestinal pathogenic Escherichia coli in a horse","volume":"20","author":"DebRoy","year":"2008","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1574-695X.2011.00797.x","article-title":"Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli.","volume":"62","author":"Garenaux","year":"2011","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"e00135-18","DOI":"10.1128\/CMR.00135-18","article-title":"Global extraintestinal pathogenic Escherichia coli (ExPEC) lineages","volume":"32","author":"Manges","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1111\/avj.12833","article-title":"Antimicrobial stewardship in equine practice","volume":"97","author":"Raidal","year":"2019","journal-title":"Aust. Vet. J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.3390\/ijms21041432","article-title":"Persistent breeding-induced endometritis in mares\u2014A multifaceted challenge: From clinical aspects to immunopathogenesis and pathobiology","volume":"21","author":"Canisso","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1128\/microbiolspec.UTI-0026-2016","article-title":"Invasion of host cells and tissues by uropathogenic bacteria","volume":"4","author":"Lewis","year":"2016","journal-title":"Microbiol. Spectr."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1537","DOI":"10.1016\/j.jiph.2020.06.032","article-title":"Virulence, phylogenetic background and antimicrobial resistance in Escherichia coli associated with extraintestinal infections","volume":"13","author":"Maruniak","year":"2020","journal-title":"J. Infect. Public Health"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4555","DOI":"10.1128\/AEM.66.10.4555-4558.2000","article-title":"Rapid and simple determination of the Escherichia coli phylogenetic group","volume":"66","author":"Clermont","year":"2000","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","first-page":"19","article-title":"Importance of broth-enrichment culture in equine endometritis diagnosis","volume":"44","author":"Nocera","year":"2021","journal-title":"New Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2559","DOI":"10.1128\/jcm.27.11.2559-2564.1989","article-title":"Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli","volume":"27","author":"Beutin","year":"1989","journal-title":"J. Clin. Microbiol."},{"key":"ref_19","unstructured":"(2018). Performance Standards for Antimicrobial Susceptibility Testing (Standard No. CLSI Approved Standard M100-S15)."},{"key":"ref_20","unstructured":"The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2018). Breakpoint Tables for Interpretation of MICs and Zone Diameters, EUCAST. Available online: http:\/\/www.eucast.org."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1111\/j.1472-765X.2004.01513.x","article-title":"Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface","volume":"38","author":"Ranin","year":"2004","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1086\/315217","article-title":"Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise","volume":"181","author":"Johnson","year":"2000","journal-title":"J. Infect. Dis."},{"key":"ref_24","first-page":"146","article-title":"Features of uropathogenic Escherichia coli able to invade a prostate cell line","volume":"39","author":"Longhi","year":"2016","journal-title":"New Microbiol."},{"key":"ref_25","unstructured":"Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., and Hornik, K. (2022). Cluster: Cluster Analysis Basics and Extensions, R Foundation. R Package Version 2.1.4."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e96","DOI":"10.1002\/cpbi.96","article-title":"Using ggtree to Visualize Data on Tree-Like Structures","volume":"69","author":"Yu","year":"2020","journal-title":"Curr. Protoc. Bioinform."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"3041","DOI":"10.1093\/molbev\/msy194","article-title":"Two methods for mapping and visualizing associated data on phylogeny using ggtree","volume":"35","author":"Yu","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1111\/2041-210X.12628","article-title":"GGTREE: An R package for visualization and annotation of phylogenetic trees with their covariates and other associated data","volume":"8","author":"Yu","year":"2017","journal-title":"Methods Ecol. Evol."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"D\u00edaz-Bertrana, M.L., Deleuze, S., Pitti Rios, L., Yeste, M., Morales Fari\u00f1a, I., and Rivera del Alamo, M.M. (2021). Microbial Prevalence and Antimicrobial Sensitivity in Equine Endometritis in Field Conditions. Animals, 11.","DOI":"10.3390\/ani11051476"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1016\/S0093-691X(01)00548-9","article-title":"Effect of insemination time of frozen semen on incidence of uterine fluid in mares","volume":"56","author":"Watson","year":"2001","journal-title":"Theriogenology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"991","DOI":"10.1016\/j.theriogenology.2012.04.016","article-title":"Effect of immunomodulatory therapy on the endometrial inflammatory response to induced infectious endometritis in susceptible mares","volume":"78","author":"Christoffersen","year":"2012","journal-title":"Theriogenology"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.theriogenology.2018.03.017","article-title":"The anti-inflammatory effect of exogenous lactoferrin on breeding-induced endometritis when administered post-breeding in susceptible mares","volume":"114","author":"Fedorka","year":"2018","journal-title":"Theriogenology"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"543","DOI":"10.3389\/fmicb.2017.00543","article-title":"Horses in Denmark are a reservoir of diverse clones of methicillin-resistant and -susceptible Staphylococcus aureus","volume":"8","author":"Islam","year":"2017","journal-title":"Front Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"3108","DOI":"10.1128\/JCM.01468-12","article-title":"Improved multiplex PCR strategy for rapid assignment of the four major Escherichia coli phylogenetic groups","volume":"50","author":"Doumith","year":"2012","journal-title":"J. Clin. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Sheldon, I.M., Rycroft, A.N., Dogan, B., Craven, M., Bromfield, J.J., Chandler, A., Roberts, M.H., Price, S.B., Gilbert, R.O., and Simpson, K.W. (2010). Specific strains of Escherichia coli are pathogenic for the endometrium of cattle and cause pelvic inflammatory disease in cattle and mice. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009192"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Xu, C., Kong, L., Liao, Y., Tian, Y., Wu, Q., Liu, H., and Wang, X. (2022). Mini-Review: Antibiotic-resistant Escherichia coli from farm animal-associated sources. Antibiotics, 11.","DOI":"10.3390\/antibiotics11111535"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.jgar.2019.03.006","article-title":"In vitro antimicrobial susceptibility of equine clinical isolates from France, 2006\u20132016","volume":"19","author":"Duchesne","year":"2019","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1038\/nrmicro.2016.94","article-title":"Biofilms: An emergent form of bacterial life","volume":"14","author":"Flemming","year":"2016","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"799619","DOI":"10.3389\/fvets.2021.799619","article-title":"A novel approach to minimising acute equine endometritis that may help to prevent the development of the chronic state","volume":"8","author":"Morrell","year":"2022","journal-title":"Front. Vet. Sci."},{"key":"ref_40","first-page":"74","article-title":"Current understanding of bacterial biofilms and latent infections: A clinical perspective","volume":"41","author":"Ferris","year":"2017","journal-title":"Rev. Bras. Reprod. Anim."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1016\/j.jevs.2015.08.018","article-title":"The evaluation of biofilm-forming potential of Escherichia coli collected from the equine female reproductive tract","volume":"35","author":"Beehan","year":"2015","journal-title":"J. Equine Vet. Sci."},{"key":"ref_42","first-page":"315","article-title":"Bacterial endometritis: A focus on biofilms","volume":"6","author":"Ferris","year":"2014","journal-title":"Clin. Theriogenol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1016\/j.jevs.2013.10.082","article-title":"Evaluation of biofilms in gram-negative bacteria isolated from the equine uterus","volume":"34","author":"Ferris","year":"2014","journal-title":"J. Equine Vet. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1128\/JCM.02861-15","article-title":"In vitro efficacy of nonantibiotic treatments on biofilm disruption of gram-negative pathogens and an in vivo model of infectious endometritis utilizing isolates from the equine uterus","volume":"54","author":"Ferris","year":"2016","journal-title":"J. Clin. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"5818","DOI":"10.3168\/jds.2010-3550","article-title":"Molecular and epidemiological characterization of bovine intrauterine Escherichia coli","volume":"93","author":"Bicalho","year":"2010","journal-title":"J. Dairy Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1292\/jvms.21-0586","article-title":"Relationship between Escherichia coli virulence factors, notably kpsMTII, and symptoms of clinical metritis and endometritis in dairy cows","volume":"84","author":"Yamamura","year":"2022","journal-title":"J. Vet. Med. Sci."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/10\/1639\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:34:51Z","timestamp":1760124891000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/10\/1639"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,5,14]]},"references-count":46,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2023,5]]}},"alternative-id":["ani13101639"],"URL":"https:\/\/doi.org\/10.3390\/ani13101639","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,5,14]]}}}