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The authors wish to express their gratitude to David Martinez and Daniel Fernandez de Luco (Universidad de Zaragoza), for providing samples. The Authors thank Sandro Pelini for providing assistance in the production of the GIS map. This research was supported by ANIHWA/Era-NET funds granted to Bru-Epidia project. Work at CITA-Spain was also sustained by Grants from MINECO (AGL2014-58795-C4-3R) and Aragon Government (Grupo de Investigacion A13-17D). Work at National and OIE Reference laboratory for Brucellosis, Istituto Zooprofilattico Sperimentale dell'Abruzzo e del Molise G. Caporale was also supported by the project IZSAM02/17RC from the Italian Ministry of Health ricerca corrente 2017 funds.Work at ANSES- France was supported by European Union Reference Laboratory for Brucellosis.

Analysis of institutional authors

Maria Munoz, PilarAuthorJesus De Miguel, MariaAuthorAndres-Barranco, SaraAuthorMaria Blasco, JoseAuthor

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September 17, 2019
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Article
Hybrid Gold

Phylogeography and epidemiology of Brucella suis biovar 2 in wildlife and domestic swine

Publicated to:Veterinary Microbiology. 233 68-77 - 2019-06-01 233(), DOI: 10.1016/j.vetmic.2019.04.025

Authors: Maria Munoz, Pilar; Mick, Virginie; Sacchini, Lorena; Janowicz, Anna; Jesus de Miguel, Maria; Cherfa, Moulay-Ali; Nevado, Celia Rodriguez; Girault, Guillaume; Andres-Barranco, Sara; Jay, Maryne; Di Giannatale, Elisabetta; Zilli, Katiuscia; Ancora, Massimo; Dondo, Alessandro; Zoppi, Simona; Cruz Arnal, Maria; Tittarellic, Manuela; De Massis, Fabrizio; Garin-Bastuji, Bruno; Maria Blasco, Jose; Garofolo, Giuliano

Affiliations

ANSES Paris Est Univ, EU OIE FAO, 14 Rue Pierre & Marie Curie, Maisons Alfort, France - Author
ANSES Paris Est Univ, Natl Reference Lab Brucellosis, Hlth Anim Lab, 14 Rue Pierre & Marie Curie, Maisons Alfort, France - Author
ANSES, Res & Reference Div, Strategy & Programmes Dept, 14 Rue Pierre & Marie Curie, Maisons Alfort, France - Author
APHA, 66 Ty Glas Rd, Cardiff CF14 5ZB, S Glam, Wales - Author
Departamento de Patología Animal, Universidad de Zaragoza, Zaragoza, Spain. - Author
EU/OIE/FAO & National Reference Laboratory for Brucellosis, Animal Health Laboratory, ANSES / Paris-Est University, 14 rue Pierre et Marie Curie, Maisons-Alfort, France. - Author
Ist Zooprofilatt Sperimentale Abruzzo & Molise G, Natl & OIE Reference Lab Brucellosis, Teramo, Italy - Author
Ist Zooprofilatt Sperimentale Piemonte Liguria &, Lab Patol Anim & Stabulario, Turin, Italy - Author
Laboratorio Patologia Animale e Stabulario, Istituto Zooprofilattico Sperimentale del Piemonte, Liguria e Valle d'Aosta "I. Altara", Torino, Italy. - Author
National and OIE Reference laboratory for Brucellosis, Istituto Zooprofilattico Sperimentale dell'Abruzzo e del Molise "G. Caporale", Teramo, Italy. - Author
National and OIE Reference laboratory for Brucellosis, Istituto Zooprofilattico Sperimentale dell'Abruzzo e del Molise "G. Caporale", Teramo, Italy. Electronic address: g.garofolo@izs.it. - Author
Unidad de Producción y Sanidad Animal, Instituto Agroalimentario de Aragón (IA2), Centro de Investigación y Tecnología Agroalimentaria de Aragón (CITA)-Universidad de Zaragoza, Zaragoza, Spain. - Author
Univ Lyon, VetAgro Sup, ANSES Lyon Lab, UMR Mycoplasmoses Ruminants, Lyon, France - Author
Univ Lyon, VetAgro Sup, ANSES Lyon Lab, UMR Mycoplasmoses Ruminants, Marcy Letoile, France - Author
Univ Zaragoza, Ctr Invest & Tecnol Agroalimentaria Aragon CITA, IA2, Unidad Prod & Sanidad Anim, Zaragoza, Spain - Author
Univ Zaragoza, Dept Patol Anim, Zaragoza, Spain - Author
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Abstract

Swine brucellosis due to Brucella suis biovar 2 (bv2) is enzootic in wild boar and hare in continental Europe and may cause major economic losses to the pig industry, mainly in free-ranged pig farms. The high nucleotide identity found among the B. suis biovar 2 isolates has long hindered the full understanding of the epidemiology and the phylogeography of the disease. Here, we used multilocus variable-number tandem-repeat (VNTR analysis (MLVA) and whole-genome analysis to identify single-nucleotide polymorphisms (SNPs) in order to gait insights from the largest B. suis bv2 dataset analyzed so far composed of domestic pigs and wildlife isolate collected throughout Europe since the 1970s. We found four major clades with a specific phylogeographic pattern. The Iberian Glade contains isolates exclusively from the Iberian Peninsula. The Central European clad includes most isolates from France, Northern Italy, Switzerland and an important proportion of those of Northern Spain. The Eastern European Glade clustered isolates from Croatia and Hungary mainly but also from areas of France, Germany, Italy and Poland. Finally, a separated Sardinian Glade grouped three isolates from this island At fine scale, MLVA demonstrated an endemic status of the infection in Europe and it allowed tracking a large outbreak formed by different farms from Spain linked to the same infection source. The whole genome SNPs analysis showed that the strains form genetically distinct clades, shared between wild boar and pigs, in agreement with the MLVA clades. Interestingly, all hare isolates clustered together within two groups compose exclusively of wildlife isolates. Our results support the hypothesis that maintenance and spread of B. suis bv2 in Europe is a dynamic process linked to the natural expansion of wild boar as the main wild reservoir of the infection, while spread over long distances is found largely dependent on anthropogenic activities.

Keywords

brucella suisbrucellosismlvaphylogeographyswineAbortusAnimalsAnimals, wildBacterial typing techniquesBoar sus-scrofaBrucella suisBrucellosisDifferentiationDisease outbreaksEuropeGenotypeInfectionLocusMinisatellite repeatsMlvaMultilocus sequence typingMultiplex pcrPhylogenyPhylogeographyPolymorphismPopulationsRelatednessSequenceSus scrofaSwineSwine diseasesWgsWhole genome sequencing

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Veterinary Microbiology 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, 2019, it was in position 7/141, thus managing to position itself as a Q1 (Primer Cuartil), in the category Veterinary Sciences. Notably, the journal is positioned above the 90th percentile.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 1.21. This 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: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Weighted Average of Normalized Impact by the Scopus agency: 1.17 (source consulted: FECYT Feb 2024)
  • Field Citation Ratio (FCR) from Dimensions: 10.52 (source consulted: Dimensions Sep 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-09-18, the following number of citations:

  • WoS: 31
  • Scopus: 33
  • Europe PMC: 26

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 2025-09-18:

  • 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: 71.
  • 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: 70 (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: 1.5.
  • The number of mentions on the social network X (formerly Twitter): 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: France; Italy; United Kingdom.

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: First Author (Muñoz Álvaro, Pilar María) and Last Author (Garofolo, Giuliano).

the author responsible for correspondence tasks has been Garofolo, Giuliano.