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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Veterinary Microbiology".

Deadline for manuscript submissions: closed (28 February 2022) | Viewed by 34163

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Dr. María Laura Boschiroli

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Unité Zoonoses Bactériennes, Laboratoire de Santé Animale de Maisons-Alfort, ANSES, 14 rue Pierre et Marie Curie, 94701 Maisons-Alfort CEDEX, France
Interests: Mycobacterium bovis; animal tuberculosis; bovine tuberculosis; zoonotic diseases

Dr. Lorraine Michelet

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Guest Editor

Unité Zoonoses Bactériennes, Laboratoire de Santé Animale de Maisons-Alfort, ANSES, 14 rue Pierre et Marie Curie, 94701 Maisons-Alfort CEDEX, France
Interests: zoonotic diseases; tropical diseases; microbiology; phylogenetic analysis; infectious diseases; statistical analysis; evolution

Special Issue Information

Dear Colleagues,

Due to the Mycobacterium tuberculosis complex (MTBC), animal tuberculosis (TB)—including bovine tuberculosis—is one of the most significant and widely spread infectious diseases of livestock in the world, despite decades of control programs and research efforts. Together with the zoonotic aspects of this disease and the important economic and sociological problems that it implies, animal TB constitutes a major concern both to human and veterinary public health sectors. Animal TB is a distinct example of how modifications of ecosystems by human practices can lead to the creation of complex reservoirs, influence the transmission and spread of the disease and hinder control and eradication programs. For this Special Issue, we seek original research papers dedicated to animal TB due to MTBC organisms, focused on studies of multi-host reservoirs and their roles in the emergence, transmission and/or maintenance of disease in livestock. System-based studies that integrate host/pathogen research with the epidemiology and population dynamics of the disease, its pathogenesis and animal farming practices including farmer behavior are also welcome.

Dr. María Laura Boschiroli
Dr. Lorraine Michelet
Guest Editors

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Keywords

Mycobacterium bovis
animal tuberculosis
bovine tuberculosis
infectious diseases
zoonotic diseases
livestock
epidemiology
pathogenesis

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Published Papers (10 papers)

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Research

14 pages, 1872 KiB

Open AccessArticle

Experimental Infection of Captive Red Foxes (Vulpes vulpes) with Mycobacterium bovis

by Céline Richomme, Sandrine Lesellier, Francisco Javier Salguero, Jacques Laurent Barrat, Jean-Marc Boucher, Jennifer Danaidae Reyes-Reyes, Sylvie Hénault, Krystel De Cruz, Jennifer Tambosco, Lorraine Michelet, Justine Boutet, Rubyat Elahi, Konstantin P. Lyashchenko, Conor O’Halloran, Ana Balseiro and Maria Laura Boschiroli

Microorganisms 2022, 10(2), 380; https://doi.org/10.3390/microorganisms10020380 - 6 Feb 2022

Cited by 1 | Viewed by 3891

Abstract

In Europe, animal tuberculosis (TB) due to Mycobacterium bovis involves multi-host communities that include cattle and wildlife species, such as wild boar (Sus scrofa), badgers (Meles meles) and red deer (Cervus elaphus). Red fox (Vulpes vulpes) infections have also been recently reported in some TB endemic regions in the Iberian Peninsula and France, with some of the infected animals shedding M. bovis in urine and feces. In order to understand the pathogenesis of M. bovis infection in foxes and the associated risk of transmission, 12 captive foxes (6 females and 6 males) were inoculated orally with 2 × 10⁷ colony-forming units of a French field isolate of M. bovis. Clinical samples (urine, feces and oropharyngeal swabs) were collected every four weeks and tested for molecular diagnosis and bacteriology. Serological responses were measured by IDEXX M. bovis Ab Test and Multi Antigen Print Immunoassay (MAPIA). At a post-mortem examination performed 12 weeks post infection (wpi), tissues were tested for the presence of M. bovis and associated gross and microscopic TB-like lesions. M. bovis was detected by PCR in bladder swabs of 3 animals at 12 wpi. It was also detected pre-mortem at different time points of the experiment in the oropharyngeal mucus of three individuals and in the feces of nine foxes, with two of them confirmed by bacteriology. All 12 foxes had at least 4 PCR positive samples (out of the 23 tested), and all but 1 fox had at least 1 culture positive sample. The culture negative fox was PCR positive in both retropharyngeal and mesenteric lymph nodes, in line with the results of the other animals. Seroconversion was observed in all foxes except one during the experiment, and in nine at the final time point. No gross visible lesions were found in any animal at the post-mortem examination. The histology showed small granulomas within the lymph nodes, tonsils, liver and lungs from eight animals, with the presence of few acid-fast bacilli. These results confirmed that all orally-infected foxes developed mild TB lesions but they were able to shed mycobacteria in about 75% of cases, 1 month post-infection (9 out 12 foxes). These results show that it is possible to induce typical TB infection experimentally in captive foxes, with measurable M. bovis excretion; such an experimental system could be useful for future evaluations of diagnostics and vaccines in this species. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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15 pages, 4852 KiB

Open AccessArticle

Experimental Mycobacterium microti Infection in Bank Voles (Myodes glareolus)

by Enric Vidal, Judit Burgaya, Lorraine Michelet, Claudia Arrieta-Villegas, Guillermo Cantero, Krystel de Cruz, Jennifer Tambosco, Michelle Di Bari, Romolo Nonno, Maria Laura Boschiroli and Bernat Pérez de Val

Microorganisms 2022, 10(1), 135; https://doi.org/10.3390/microorganisms10010135 - 10 Jan 2022

Cited by 4 | Viewed by 3569

Abstract

Voles are maintenance hosts of Mycobacterium microti. In line with the goal to eradicate tuberculosis (TB) in livestock, the role of this mycobacteria needs to be assessed since it might interfere with current M. bovis/M. caprae surveillance strategies. To better understand the pathogenesis of TB in voles, an experimental infection model was set up to reproduce M. microti infection in laboratory Bank voles (Myodes glareolus). Two infection routes (intragastric and intraperitoneal) and doses (10⁵ and 10⁶ CFU/0.1 mL) were assessed. Voles were culled at different post-infection time points. Serology, histopathology, acid-fast bacilli staining, qPCR, and mycobacterial culture from tissues were performed. In addition, qPCR from feces and oral swabs were conducted to assess bacterial shedding. The model allowed us to faithfully reproduce the disease phenotype described in free-ranging voles and characterize the pathogenesis of the infection. Most animals showed multifocal and diffuse granulomatous lesions in the liver and spleen, respectively. Less frequently, granulomas were observed in lungs, lymph nodes, muscles, and salivary gland. Mycobacterial DNA was detected in feces from a few animals but not in oral swabs. However, one contact uninfected vole seroconverted and showed incipient TB compatible lesions, suggesting horizontal transmission between voles. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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14 pages, 1251 KiB

Open AccessArticle

Mycobacterium microti at the Environment and Wildlife Interface

by Valentina Tagliapietra, Maria Beatrice Boniotti, Anna Mangeli, Iyad Karaman, Giovanni Alborali, Mario Chiari, Mario D’Incau, Mariagrazia Zanoni, Annapaola Rizzoli and Maria Lodovica Pacciarini

Microorganisms 2021, 9(10), 2084; https://doi.org/10.3390/microorganisms9102084 - 2 Oct 2021

Cited by 17 | Viewed by 2623

Abstract

An unexpected high presence of Mycobacterium microti in wild boar in Northern Italy (Garda Lake) has been reported since 2003, but the factors contributing to the maintenance of this pathogen are still unclear. In this study, we investigated the presence of M. microti in wild rodents and in water and soil samples collected at wild boar aggregation areas, such as watering holes, with the aim of clarifying their role in M. microti transmission. In total, 8 out of 120 captured animals tested positive for the Mycobacterium tuberculosis complex (MTBC) as assessed by real-time PCR, and six samples were confirmed to be M. microti. A strain with a genetic profile similar to those previously isolated in wild boars in the same area was isolated from one sample. Of the 20 water and 19 mud samples, 3 and 1, respectively, tested positive for the presence of MTBC, and spacer oligotype SB0118 (vole type) was detected in one sample. Our study suggests that wild rodents, in particular Apodemus sylvaticus, Microtus sp. and Apodemus flavicollis, play roles in the maintenance of M. microti infections in wild boar through ingestion or by contact with either infected excreta or a contaminated environment, such as at animal aggregation sites. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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24 pages, 1554 KiB

Open AccessArticle

Whole-Genome SNP Analysis Identifies Putative Mycobacterium bovis Transmission Clusters in Livestock and Wildlife in Catalonia, Spain

by Claudia Perea, Giovanna Ciaravino, Tod Stuber, Tyler C. Thacker, Suelee Robbe-Austerman, Alberto Allepuz and Bernat Pérez de Val

Microorganisms 2021, 9(8), 1629; https://doi.org/10.3390/microorganisms9081629 - 30 Jul 2021

Cited by 10 | Viewed by 4442

Abstract

The high-resolution WGS analyses of MTBC strains have provided useful insight for determining sources of infection for animal tuberculosis. In Spain, tuberculosis in livestock is caused by Mycobacterium bovis and Mycobacterium caprae, where wildlife reservoirs play an important role. We analyzed a set of 125 M. bovis isolates obtained from livestock and wildlife from Catalonia to investigate strain diversity and identify possible sources and/or causes of infection. Whole-genome SNP profiles were used for phylogenetic reconstruction and pairwise SNP distance analysis. Additionally, SNPs were investigated to identify virulence and antimicrobial resistance factors to investigate clade-specific associations. Putative transmission clusters (≤12 SNPs) were identified, and associated epidemiological metadata were used to determine possible explanatory factors for transmission. M. bovis distribution was heterogeneous, with 7 major clades and 21 putative transmission clusters. In order of importance, the explanatory factors associated were proximity and neighborhood, residual infection, livestock-wildlife interaction, shared pasture, and movement. Genes related to lipid transport and metabolism showed the highest number of SNPs. All isolates were pyrazinamide resistant, and five were additionally resistant to isoniazid, but no clade-specific associations could be determined. Our findings highlight the importance of high-resolution molecular surveillance to monitor bovine tuberculosis dynamics in a low-prevalence setting. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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15 pages, 1704 KiB

Open AccessArticle

Whole Genome Sequencing Refines Knowledge on the Population Structure of Mycobacterium bovis from a Multi-Host Tuberculosis System

by Ana C. Reis, Liliana C. M. Salvador, Suelee Robbe-Austerman, Rogério Tenreiro, Ana Botelho, Teresa Albuquerque and Mónica V. Cunha

Microorganisms 2021, 9(8), 1585; https://doi.org/10.3390/microorganisms9081585 - 26 Jul 2021

Cited by 14 | Viewed by 3846

Abstract

Classical molecular analyses of Mycobacterium bovis based on spoligotyping and Variable Number Tandem Repeat (MIRU-VNTR) brought the first insights into the epidemiology of animal tuberculosis (TB) in Portugal, showing high genotypic diversity of circulating strains that mostly cluster within the European 2 clonal complex. Previous surveillance provided valuable information on the prevalence and spatial occurrence of TB and highlighted prevalent genotypes in areas where livestock and wild ungulates are sympatric. However, links at the wildlife–livestock interfaces were established mainly via classical genotype associations. Here, we apply whole genome sequencing (WGS) to cattle, red deer and wild boar isolates to reconstruct the M. bovis population structure in a multi-host, multi-region disease system and to explore links at a fine genomic scale between M. bovis from wildlife hosts and cattle. Whole genome sequences of 44 representative M. bovis isolates, obtained between 2003 and 2015 from three TB hotspots, were compared through single nucleotide polymorphism (SNP) variant calling analyses. Consistent with previous results combining classical genotyping with Bayesian population admixture modelling, SNP-based phylogenies support the branching of this M. bovis population into five genetic clades, three with apparent geographic specificities, as well as the establishment of an SNP catalogue specific to each clade, which may be explored in the future as phylogenetic markers. The core genome alignment of SNPs was integrated within a spatiotemporal metadata framework to further structure this M. bovis population by host species and TB hotspots, providing a baseline for network analyses in different epidemiological and disease control contexts. WGS of M. bovis isolates from Portugal is reported for the first time in this pilot study, refining the spatiotemporal context of TB at the wildlife–livestock interface and providing further support to the key role of red deer and wild boar on disease maintenance. The SNP diversity observed within this dataset supports the natural circulation of M. bovis for a long time period, as well as multiple introduction events of the pathogen in this Iberian multi-host system. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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8 pages, 1185 KiB

Open AccessArticle

Mycobacterium microti Infection in Red Foxes in France

by Lorraine Michelet, Céline Richomme, Edouard Réveillaud, Krystel De Cruz, Jean-Louis Moyen and Maria Laura Boschiroli

Microorganisms 2021, 9(6), 1257; https://doi.org/10.3390/microorganisms9061257 - 9 Jun 2021

Cited by 7 | Viewed by 2573

Abstract

Mycobacterium microti, member of the Mycobacterium tuberculosis, complex is known to interfere in the screening and diagnosis of bovine tuberculosis. This pathogen is increasingly detected in the frame of surveillance programs for tuberculosis in livestock and wildlife. Recently, red foxes (Vulpes vulpes) were found infected by Mycobacterium bovis in four French endemic areas. M. microti infection was concomitantly found during this investigation. Rates of infection by M. microti and M. bovis are not different except in one of the four areas (lower prevalence for M. microti in Charente). As for M. bovis infection, none of the infected foxes presented gross TB-like lesions. Infection of red foxes by M. microti seems to occur by ingestion of contaminated food, as mesenteric lymph nodes are mostly infected albeit no fecal excretion could be detected. Red foxes appear to be susceptible to Mycobacterium microti infection but seem to play a role of dead-end host for the transmission of this bacillus. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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12 pages, 285 KiB

Open AccessArticle

Future Risk of Bovine Tuberculosis (Mycobacterium bovis) Breakdown in Cattle Herds 2013–2018: A Dominance Analysis Approach

by Andrew W. Byrne, Damien Barrett, Philip Breslin, Jamie M. Madden, James O’Keeffe and Eoin Ryan

Microorganisms 2021, 9(5), 1004; https://doi.org/10.3390/microorganisms9051004 - 6 May 2021

Cited by 6 | Viewed by 3039

Abstract

Bovine tuberculosis (bTB) remains a significant endemic pathogen of cattle herds, despite multi-decadal control programmes being in place in several countries. Understanding the risks of future bTB breakdown (BD) and the associated characteristics of herds and index breakdowns could help inform risk categorisation. Such risk categories could then contribute to tailored management and policies. Here, we estimated the future risk of herd BD for the cohort of herds that were derestricted during 2013 in Ireland using multivariable logit regression models, with a dominance analysis approach. One third of herds that were derestricted in 2013 experienced a breakdown during the follow-up five year period (1469/4459; 33%). BD length was a significant predictor of future risk, primarily driven by long BDs > 230 days relative to short BDs < 130 days (OR 95%CI: 1.157–1.851), as was having had a previous BD (OR 95%CI: 1.012–1.366). Herd-size was the dominant predictor of future risk (accounted for 46% of predicted variance), suggesting significant increase in risk of future breakdown with increasing (log) herd-size (OR 95%CI: 1.378–1.609). There was significant spatial variation in future risk across counties, and it was the second most dominant predictor of future risk (25% of predicted variance). The size of index breakdowns was not a strong predictor of future risk over a 5-year period. These findings can inform a risk-based policy development. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

23 pages, 5605 KiB

Open AccessArticle

Relative Contribution of Each Component of the French Ante-Mortem Surveillance System for Bovine Tuberculosis in Its Overall Sensitivity

by Valentine Guétin-Poirier, Julie Rivière and Barbara Dufour

Microorganisms 2021, 9(3), 643; https://doi.org/10.3390/microorganisms9030643 - 19 Mar 2021

Viewed by 2184

Abstract

The aim of this study was to assess the contribution to the sensitivity of the French ante-mortem surveillance system for bovine tuberculosis in cattle of each of the system’s components (periodic screening, epidemiological investigations, and screening exchanged animals), on a local scale defined by administrative areas. These components were individually assessed in previous studies by scenario tree modeling. We used scenario tree modeling at the herd level and combined the results to evaluate the overall sensitivity of the ante-mortem surveillance system. The probability to detect at least one infected herd was consistent with the location of the outbreaks detected in 2016. In areas with a high apparent incidence, the probability of an infected herd to be detected was satisfactory (for an infected herd there was a 100% probability to be detected over a two-year period). Periodic screening was the most important component for the overall sensitivity in infected areas. In other areas, where periodic screening had stopped, tracing-on epidemiological investigation was the most sensitive component of the system. Screening exchanged animals had a negligible part in the overall sensitivity of the surveillance system. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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20 pages, 4655 KiB

Open AccessArticle

Use of Network Analysis and Spread Models to Target Control Actions for Bovine Tuberculosis in a State from Brazil

by Nicolas Cespedes Cardenas, Pilar Pozo, Francisco Paulo Nunes Lopes, José H. H. Grisi-Filho and Julio Alvarez

Microorganisms 2021, 9(2), 227; https://doi.org/10.3390/microorganisms9020227 - 22 Jan 2021

Cited by 4 | Viewed by 3445

Abstract

Livestock movements create complex dynamic interactions among premises that can be represented, interpreted, and used for epidemiological purposes. These movements are a very important part of the production chain but may also contribute to the spread of infectious diseases through the transfer of infected animals over large distances. Social network analysis (SNA) can be used to characterize cattle trade patterns and to identify highly connected premises that may act as hubs in the movement network, which could be subjected to targeted control measures in order to reduce the transmission of communicable diseases such as bovine tuberculosis (TB). Here, we analyzed data on cattle movement and slaughterhouse surveillance for detection of TB-like lesions (TLL) over the 2016–2018 period in the state of Rio Grande do Sul (RS) in Brazil with the following aims: (i) to characterize cattle trade describing the static full, yearly, and monthly snapshots of the network contact trade, (ii) to identify clusters in the space and contact networks of premises from which animals with TLL originated, and (iii) to evaluate the potential of targeted control actions to decrease TB spread in the cattle population of RS using a stochastic metapopulation disease transmission model that simulated within-farm and between-farm disease spread. We found heterogeneous densities of premises and animals in the study area. The analysis of the contact network revealed a highly connected (~94%) trade network, with strong temporal trends, especially for May and November. The TLL cases were significantly clustered in space and in the contact network, suggesting the potential for both local (e.g., fence-to-fence) and movement-mediated TB transmission. According to the disease spread model, removing the top 7% connected farms based on degree and betweenness could reduce the total number of infected farms over three years by >50%. In conclusion, the characterization of the cattle network suggests that highly connected farms may play a role in TB dissemination, although being close to infected farms was also identified as a risk factor for having animals with TLL. Surveillance and control actions based on degree and betweenness could be useful to break the transmission cycle between premises in RS. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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7 pages, 792 KiB

Open AccessCommunication

Mycobacterium microti Interferes with Bovine Tuberculosis Surveillance

by Lorraine Michelet, Krystel de Cruz, Jennifer Tambosco, Sylvie Hénault and Maria Laura Boschiroli

Microorganisms 2020, 8(12), 1850; https://doi.org/10.3390/microorganisms8121850 - 24 Nov 2020

Cited by 13 | Viewed by 2463

Abstract

Mycobacterium microti, a member of the Mycobacterium tuberculosis complex, was originally described as the cause of tuberculosis in wild rodents. However, in the last few years, an increasing number of cases have been reported in wildlife (wild boars and badgers) and livestock (goat and cattle) in the frame of bovine tuberculosis (bTB) surveillance program, demonstrating the risk of interference with bTB diagnosis in France. In 2019, we detected four cattle infected with M.microti, from three different herds in three different distant regions. For all these cases, ante-mortem diagnosis by the skin test (single intradermal comparative cervical tuberculin (SICCT)) was positive. Confirmation of M.microti infection was based on molecular tests, i.e., specific real-time PCR and spoligotyping. These results highlight a non-negligible risk of interference in the bTB diagnosis system and raise concern about the reliability of diagnostic tests used for bTB surveillance. The use of highly specific tests, like the interferon gamma test (IFN-γ) employed in France or new synthetic specific tuberculins for skin testing could alternatively be used to accurately identify M.bovis (or Mycobacterium caprae) infection at ante-mortem examination. At post-mortem diagnosis, the use of specific molecular tools should be considered to accurately distinguish pathogens within the MTBC and to avoid misleading bTB diagnosis. Full article

(This article belongs to the Special Issue Animal Tuberculosis Due to Mycobacterium tuberculosis complex Members)

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