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This study was supported by the projects and funds PID2019-104439RB-C21/AEI/10.13039/501100011033 from the Agencia Estatal de Investigacion (AEI, Spain), co-funded by the European Regional Development Fund of the European Union: a Way to Make Europe (ERDF); ED431C 2021/11 and ED431B 2020/13 from the Conselleria de Cultura, Educacion e Ordenacion Universitaria (Xunta de Galicia) and ERDF. GRUPIN IDI/2022/000033 by the Regional Ministry of Science of Asturias (IDI/2022/000033). Co-funded by Independent Research Found Denmark (grant number 4184-00050) to the project Combining non-essential metabolic targets into suitable targets for control of uropathogenic Escherichia coli.

Analysis of institutional authors

García Abad, IsidroAuthor

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June 29, 2023
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Genomics, biofilm formation and infection of bladder epithelial cells in potentially uropathogenic Escherichia coli (UPEC) from animal sources and human urinary tract infections (UTIs) further support food-borne transmission

Publicated to:One Health. 16 100558-100558 - 2023-05-20 16(), DOI: 10.1016/j.onehlt.2023.100558

Authors: Garcia, Vanesa; Leston, Luz; Parga, Ana; Garcia-Menino, Isidro; Fernandez, Javier; Otero, Ana; Olsen, John E; Herrero-Fresno, Ana; Mora, Azucena

Affiliations

CIBER de Enfermedades Respiratorias (CibeRes), Instituto de Salud Carlos III, Madrid, Spain. - Author
Departamento de Microbioloxía e Parasitoloxía, Facultade de Bioloxía, Edificio CIBUS, Universidade de Santiago de Compostela, Santiago de Compostela 15782, Spain. - Author
Department for Biological Safety, German Federal Institute for Risk Assessment, Berlin 10589, Germany. - Author
Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Frederiksberg 1870, Denmark. - Author
German Fed Inst Risk Assessment, Dept Biol Safety, D-10589 Berlin, Germany - Author
Grupo de Microbiología Traslacional, Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo 33011, Spain. - Author
Hosp Univ Cent Asturias HUCA, Serv Microbiol, Oviedo 33011, Spain - Author
Inst Invest Sanitaria Principado Asturias ISPA, Grp Microbiol Traslac, Oviedo 33011, Spain - Author
Inst Invest Sanitaria Santiago de Compostela IDIS, Santiago 15706, Spain - Author
Inst Salud Carlos III, CIBER Enfermedades Resp CIBERES, Madrid, Spain - Author
Instituto de Investigación Sanitaria de Santiago de Compostela (IDIS), Santiago 15706, Spain. - Author
Laboratorio de Referencia de Escherichia coli (LREC), Dpto. de Microbioloxía e Parasitoloxía, Universidade de Santiago de Compostela (USC), Lugo 27002, Spain. - Author
Pragmatech AI Solut, Artificial Intelligence & Stat Dept, Res & Innovat, Oviedo 33011, Spain - Author
Research & Innovation, Artificial Intelligence and Statistical Department, Pragmatech AI Solutions, Oviedo 33011, Spain. - Author
Servicio de Microbiología, Hospital Universitario Central de Asturias (HUCA), Oviedo 33011, Spain. - Author
Tech Univ Denmark, Natl Food Inst, DK-2800 Lyngby, Denmark - Author
Univ Copenhagen, Fac Hlth & Med Sci, Dept Vet & Anim Sci, DK-1870 Frederiksberg, Denmark - Author
Univ Santiago de Compostela USC, Dept Microbiol & Parasitol, Lab Referencia Escherichia Coli LREC, Lugo 27002, Spain - Author
Univ Santiago de Compostela, Fac Biol, Dept Microbiol & Parasitol, Edificio CIBUS, Santiago De Compostela 15782, Spain - Author
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Abstract

Escherichia coli is the main cause of urinary tract infections (UTI). While genomic comparison of specific clones recovered from animals, and human extraintestinal infections show high identity, studies demonstrating the uropathogenicity are lacking. In this study, comparative genomics combined with bladder-cell and biofilm formation assays, were performed for 31 E. coli of different origins: 7 from meat (poultry, beef, and pork); 2 from avian-farm environment; 12 from human uncomplicated UTI, uUTI; and 10 from human complicated UTI, cUTI. These isolates were selected based on their genetic uropathogenic (UPEC) status and phylogenetic background. In silico analysis revealed similar virulence-gene profiles, with flagella, type 1 and curli fimbriae, outer-membrane proteins (agn43, ompT, iha), and iron-uptake (iutA, entA, and fyuA) associated-traits as the most prevalent (>65%). In bladder-cell assays, moderate to strong values of association (83%, 60%, 77.8%) and invasion (0%, 70%, 55.5%) were exhibited by uUTI, cUTI, and animal-derived isolates, respectively. Of interest, uUTI isolates exhibited a significantly lower invasive capacity than cUTI isolates (p < 0.05). All isolates but one produced measurable biofilm. Notably, 1 turkey meat isolate O11:H6-F-ST457, and 2 cUTI isolates of the pandemic lineages O83:H42-F-ST1485-CC648 and O25b:H4-B2-ST131, showed strong association, invasion and biofilm formation. These isolates showed common carriage of type 1 fimbriae and csg operons, toxins (hlyF, tsh), iron uptake systems (iutA, entA, iroN), colicins, protectins (cvaC, iss, kpsM, traT), ompT, and malX. In summary, the similar in vitro behaviour found here for certain E. coli clones of animal origin would further reinforce the role of food-producing animals as a potential source of UPEC. Bladder-cell infection assays, combined with genomics, might be an alternative to in vivo virulence models to assess uropathogenicity.© 2023 The Author(s).

Keywords

biofilmcell infectioncoliepidemiologyfood-bornest1193upecutivirulenceAutotransporter proteinBiofilmCell infectionEE. coliFood-borneSt1193UpecUti

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal One Health due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2023, it was in position 54/408, thus managing to position itself as a Q1 (Primer Cuartil), in the category Public, Environmental & Occupational Health.

From a relative perspective, and based on the normalized impact indicator calculated from the Field Citation Ratio (FCR) of the Dimensions source, it yields a value of: 7.61, which indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: Dimensions Jul 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-07-05, the following number of citations:

  • WoS: 8
  • Europe PMC: 4

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-05:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 53.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 83 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 22.8.
  • The number of mentions on the social network X (formerly Twitter): 13 (Altmetric).
  • The number of mentions in news outlets: 2 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Denmark; Germany.