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Emerging Themes in Brucella and Brucellosis

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

Deadline for manuscript submissions: closed (31 May 2022) | Viewed by 39311

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Special Issue Editors

Dr. Adrian Whatmore

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Guest Editor

OIE/FAO Reference Laboratory for Brucellosis, Department of Bacteriology, Animal & Plant Health Agency, Addlestone KT15 3NB, UK
Interests: veterinary bacteriology; brucellosis; molecular diagnostics; molecular typing; taxonomy

Dr. John McGiven

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Guest Editor

OIE/FAO Reference Laboratory for Brucellosis, Department of Bacteriology, Animal & Plant Health Agency, Addlestone KT15 3NB, UK
Interests: brucellosis; immunology; serodiagnostics; vaccines

Special Issue Information

Dear Colleagues,

Brucellosis remains a formidable challenge, recognized by the WHO as one of the most significant zoonotic diseases globally, and still endemic in large parts of the world. Despite the pathogen gaining more attention in recent years, with significant increases in publication profiles and increasing data from countries with endemic disease, it still fulfils the oft-used mantra as a ‘neglected’ disease. Much has changed in recent years with new tools and technologies and emerging themes challenging our existing understanding of the group. New Brucella species and ecosystems have emerged, the significance of which remain unclear, while key gaps in knowledge remain with respect to the long-standing species infecting livestock and humans. New molecular and, latterly, genomic tools promise to improve our understanding of the disease’s epidemiology and the pathogen’s biology. There is still much to learn about pathogenic mechanisms and there is an ongoing quest for effective novel vaccines with more desirable properties, particularly in regard to attenuation for humans.

In this Special Issue, we aim to both summarize current knowledge and explore emerging themes and developments in our understanding of the pathogen, the disease, and their global impact. We thus invite submission of research and review articles that cover any aspect of the bacteriology, epidemiology, molecular biology, genomics, or pathogenesis of Brucella species or vaccine development or diagnostics for Brucellosis. We look forward to your contribution.

This Special Issue is jointly organized between Microorganisms and Pathogens journals. Authors in the Special Issue can submit their papers to Microorganisms or Pathogens. The conjunct Special Issue in Pathogens: Emerging Themes in Brucella and Brucellosis.

Dr. Adrian Whatmore
Dr. John McGiven
Guest Editors

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Keywords

Brucella
Brucellosis
epidemiology
genomics
pathogenesis
vaccine

Published Papers (11 papers)

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Research

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18 pages, 3052 KiB

Open AccessArticle

Adaptation of Brucella melitensis Antimicrobial Susceptibility Testing to the ISO 20776 Standard and Validation of the Method

by Alina Tscherne, Enrico Mantel, Talar Boskani, Sylwia Budniak, Mandy Elschner, Antonio Fasanella, Siri L. Feruglio, Domenico Galante, Christian G. Giske, Roland Grunow, Judit Henczko, Christin Hinz, Wojciech Iwaniak, Daniela Jacob, Agnieszka Kedrak-Jablonska, Veronica K. Jensen, Tone B. Johansen, Gunnar Kahlmeter, Viviana Manzulli, Erika Matuschek, Falk Melzer, Maria S. Nuncio, Joseph Papaparaskevas, Ana Pelerito, Margrete Solheim, Susanne Thomann, Athanasios Tsakris, Tara Wahab, Marcin Weiner, Lothar Zoeller and Sabine Zange Show full author list Hide full author list

Microorganisms 2022, 10(7), 1470; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10071470 - 20 Jul 2022

Cited by 6 | Viewed by 2568

Abstract

Brucellosis, mainly caused by Brucella (B.) melitensis, is associated with a risk of chronification and relapses. Antimicrobial susceptibility testing (AST) standards for B. melitensis are not available, and the agent is not yet listed in the EUCAST breakpoint tables. CLSI recommendations for B. melitensis exist, but they do not fulfill the requirements of the ISO 20776 standard regarding the culture medium and the incubation conditions. Under the third EU Health Programme, laboratories specializing in the diagnostics of highly pathogenic bacteria in their respective countries formed a working group within a Joint Action aiming to develop a suitable method for the AST of B. melitensis. Under the supervision of EUCAST representatives, this working group adapted the CLSI M45 document to the ISO 20776 standard after testing and validation. These adaptations included the comparison of various culture media, culture conditions and AST methods. A Standard Operation Procedure was derived and an interlaboratory validation was performed in order to evaluate the method. The results showed pros and cons for both of the two methods but also indicate that it is not necessary to abandon Mueller–Hinton without additives for the AST of B. melitensis. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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10 pages, 1094 KiB

Open AccessArticle

Development of a Multiplex Bead Assay to Detect Serological Responses to Brucella Species in Domestic Pigs and Wild Boar with the Potential to Overcome Cross-Reactivity with Yersinia enterocolitica O:9

by Antonia Touloudi, John McGiven, Shaun Cawthraw, George Valiakos, Polychronis Kostoulas, Lucy Duncombe, Christian Gortázar, Mariana Boadella, Marina Sofia, Zoi Athanasakopoulou, Dimitris C. Chatzopoulos, Vassiliki Spyrou, Liljana Petrovska and Charalambos Billinis

Microorganisms 2022, 10(7), 1362; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10071362 - 06 Jul 2022

Cited by 3 | Viewed by 1306

Abstract

The aim of this study was to develop a multiplex bead assay using a Brucella rLPS antigen, a Brucella suis smooth antigen, and a Yersinia enterocolitica O:9 antigen that not only discriminates Brucella-infected from Brucella-uninfected pigs and wild boar, but also overcomes the cross reactivity with Y. enterocolitica O:9. Sera from 126 domestic pigs were tested: 29 pigs were Brucella infected, 80 were non-infected and 17 were confirmed to be false positive serological reactors (FPSR). Sera from 49 wild boar were tested: 18 were positive and 31 were negative. Using the rLPS antigen, 26/29 Brucella-infected domestic pigs and 15/18 seropositive wild boar were positive, while 75/80 non-Brucella infected domestic pigs, all FPSR, and all seronegative wild boar were negative. Using the smooth B. suis 1330 antigen, all Brucella-infected domestic pigs, 9/17 FPSR and all seropositive wild boar were positive, while all non-infected pigs and 30/31 seronegative wild boar were negative. The ratio of the readouts from the smooth B. suis antigen and Y. enterocolitica O:9 antigen enabled discriminating all Brucella infected individuals from the FPSR domestic pigs. These results demonstrate the potential of this assay for use in the surveillance of brucellosis, overcoming the cross-reactivity with Y. enterocolitica. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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19 pages, 1306 KiB

Open AccessArticle

The Tip of Brucella O-Polysaccharide Is a Potent Epitope in Response to Brucellosis Infection and Enables Short Synthetic Antigens to Be Superior Diagnostic Reagents

by Lucy Duncombe, Laurence Howells, Anna Haughey, Andrew V. Taylor, Daryan Kaveh, Sevil Erdenliğ Gϋrbilek, Anne Dell, Paul G. Hitchen, Stuart M. Haslam, Satadru Sekhar Mandal, N. Vijaya Ganesh, David R. Bundle and John McGiven

Microorganisms 2022, 10(4), 708; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10040708 - 25 Mar 2022

Cited by 1 | Viewed by 2070

Abstract

Brucellosis is a global disease and the world’s most prevalent zoonosis. All cases in livestock and most cases in humans are caused by members of the genus Brucella that possess a surface O-polysaccharide (OPS) comprised of a rare monosaccharide 4-deoxy-4-formamido-D-mannopyranose assembled with α1,2 and α1,3 linkages. The OPS of the bacterium is the basis for serodiagnostic tests for brucellosis. Bacteria that also contain the same rare monosaccharide can induce antibodies that cross-react in serological tests. In previous work we established that synthetic oligosaccharides, representing elements of the Brucella A and M polysaccharide structures, were excellent antigens to explore the antibody response in the context of infection, immunisation and cross reaction. These studies suggested the existence of antibodies that are specific to the tip of the Brucella OPS. Sera from naturally and experimentally Brucella abortus-infected cattle as well as from cattle experimentally infected with the cross-reactive bacterium Yersinia enterocolitica O:9 and field sera that cross react in conventional serological assays were studied here with an expanded panel of synthetic antigens. The addition of chemical features to synthetic antigens that block antibody binding to the tip of the OPS dramatically reduced their polyclonal antibody binding capability providing conclusive evidence that the OPS tip (non-reducing end) is a potent epitope. Selected short oligosaccharides, including those that were exclusively α1,2 linked, also demonstrated superior specificity when evaluated with cross reactive sera compared to native smooth lipopolysaccharide (sLPS) antigen and capped native OPS. This surprising discovery suggests that the OPS tip epitope, even though common to both Brucella and Y. enterocolitica O:9, has more specific diagnostic properties than the linear portion of the native antigens. This finding opens the way to the development of improved serological tests for brucellosis. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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11 pages, 945 KiB

Open AccessArticle

High-Resolution Melting PCR as Rapid Genotyping Tool for Brucella Species

by Guillaume Girault, Ludivine Perrot, Virginie Mick and Claire Ponsart

Microorganisms 2022, 10(2), 336; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10020336 - 01 Feb 2022

Cited by 11 | Viewed by 2348

Abstract

Brucella sp. are the causative agents of brucellosis. One of the main characteristics of the Brucella genus concerns its very high genetic homogeneity. To date, classical bacteriology typing is still considered as the gold standard assay for direct diagnosis of Brucella. Molecular approaches are routinely used for the identification of Brucella at the genus level. However, genotyping is more complex, and to date, no method exists to quickly assign a strain into species and biovar levels, and new approaches are required. Next generation sequencing (NGS) opened a new era into the diagnosis of bacterial diseases. In this study, we designed a high-resolution melting (HRM) method for the rapid screening of DNA and direct assignment into one of the 12 species of the Brucella genus. This method is based on 17 relevant single nucleotide polymorphisms (SNPs), identified and selected from a whole genome SNP (wgSNP) analysis based on 988 genomes (complete and drafts). These markers were tested against the collection of the European Reference Laboratory (EU-RL) for brucellosis (1440 DNAs extracted from Brucella strains). The results confirmed the reliability of the panel of 17 SNP markers, allowing the differentiation of each species of Brucella together with biovars 1, 2, and 3 of B. suis and vaccine strain Rev1 (B. melitensis) within 3 h, which is a considerable gain of time for brucellosis diagnosis. Therefore, this genotyping tool provides a new and quick alternative for Brucella identification based on SNPs with the HRM-PCR assay. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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20 pages, 4584 KiB

Open AccessArticle

Brucella abortus Encodes an Active Rhomboid Protease: Proteome Response after Rhomboid Gene Deletion

by María Inés Marchesini, Ansgar Poetsch, Leticia Soledad Guidolín and Diego J. Comerci

Microorganisms 2022, 10(1), 114; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10010114 - 06 Jan 2022

Cited by 3 | Viewed by 1872

Abstract

Rhomboids are intramembrane serine proteases highly conserved in the three domains of life. Their key roles in eukaryotes are well understood but their contribution to bacterial physiology is still poorly characterized. Here we demonstrate that Brucella abortus, the etiological agent of the zoonosis called brucellosis, encodes an active rhomboid protease capable of cleaving model heterologous substrates like Drosophila melanogaster Gurken and Providencia stuartii TatA. To address the impact of rhomboid deletion on B. abortus physiology, the proteomes of mutant and parental strains were compared by shotgun proteomics. About 50% of the B. abortus predicted proteome was identified by quantitative proteomics under two experimental conditions and 108 differentially represented proteins were detected. Membrane associated proteins that showed variations in concentration in the mutant were considered as potential rhomboid targets. This class included nitric oxide reductase subunit C NorC (Q2YJT6) and periplasmic protein LptC involved in LPS transport to the outer membrane (Q2YP16). Differences in secretory proteins were also addressed. Differentially represented proteins included a putative lytic murein transglycosylase (Q2YIT4), nitrous-oxide reductase NosZ (Q2YJW2) and high oxygen affinity Cbb3-type cytochrome c oxidase subunit (Q2YM85). Deletion of rhomboid had no obvious effect in B. abortus virulence. However, rhomboid overexpression had a negative impact on growth under static conditions, suggesting an effect on denitrification enzymes and/or high oxygen affinity cytochrome c oxidase required for growth in low oxygen tension conditions. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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Review

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23 pages, 383 KiB

Open AccessReview

Assays for Identification and Differentiation of Brucella Species: A Review

by Berzhan Kurmanov, Diansy Zincke, Wanwen Su, Ted L. Hadfield, Alim Aikimbayev, Talgat Karibayev, Maxat Berdikulov, Mukhit Orynbayev, Mikeljon P. Nikolich and Jason K. Blackburn

Microorganisms 2022, 10(8), 1584; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10081584 - 06 Aug 2022

Cited by 16 | Viewed by 4344

Abstract

Brucellosis is one of the most important and widespread bacterial zoonoses worldwide. Cases are reported annually across the range of known infectious species of the genus Brucella. Globally, Brucella melitensis, primarily hosted by domestic sheep and goats, affects large proportions of livestock herds, and frequently spills over into humans. While some species, such as Brucella abortus, are well controlled in livestock in areas of North America, the Greater Yellowstone Ecosystem supports the species in native wild ungulates with occasional spillover to livestock. Elsewhere in North America, other Brucella species still infect domestic dogs and feral swine, with some associated human cases. Brucella spp. patterns vary across space globally with B. abortus and B. melitensis the most important for livestock control. A myriad of other species within the genus infect a wide range of marine mammals, wildlife, rodents, and even frogs. Infection in humans from these others varies with geography and bacterial species. Control in humans is primarily achieved through livestock vaccination and culling and requires accurate and rapid species confirmation; vaccination is Brucella spp.-specific and typically targets single livestock species for distribution. Traditional bacteriology methods are slow (some media can take up to 21 days for bacterial growth) and often lack the specificity of molecular techniques. Here, we summarize the molecular techniques for confirming and identifying specific Brucella species and provide recommendations for selecting the appropriate methods based on need, sensitivity, and laboratory capabilities/technology. As vaccination/culling approaches are costly and logistically challenging, proper diagnostics and species identification are critical tools for targeting surveillance and control. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

21 pages, 26036 KiB

Open AccessReview

Brucellosis in Humans and Animals in Kyrgyzstan

by Kalysbek Kydyshov, Nurbolot Usenbaev, Almaz Sharshenbekov, Narynbek Aitkuluev, Murat Abdyraev, Salamat Chegirov, Jarkynay Kazybaeva, Hanka Brangsch, Falk Melzer, Heinrich Neubauer and Mathias W. Pletz

Microorganisms 2022, 10(7), 1293; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10071293 - 25 Jun 2022

Cited by 11 | Viewed by 2909

Abstract

Brucellosis is a globally reemerging and neglected zoonosis causing serious public health problems as well as considerable economic losses due to infection of livestock. Although the epidemiology of brucellosis has been well studied and its various aspects in humans and animals are well understood, it is still one of the most challenging health problems in many developing countries such as Kyrgyzstan. This review describes epidemiological characteristics of brucellosis in humans and animals, its impact on animal production and the role of implemented infection control measures in Kyrgyzstan. Particularly, introduction of mass vaccination in small ruminants evidently contributed to control of brucellosis in Kyrgyzstan, reducing the number of infections in animals as well as humans. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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39 pages, 1930 KiB

Open AccessReview

Immunosuppressive Mechanisms in Brucellosis in Light of Chronic Bacterial Diseases

by Joaquin Miguel Pellegrini, Jean-Pierre Gorvel and Sylvie Mémet

Microorganisms 2022, 10(7), 1260; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10071260 - 21 Jun 2022

Cited by 3 | Viewed by 4786

Abstract

Brucellosis is considered one of the major zoonoses worldwide, constituting a critical livestock and human health concern with a huge socio-economic burden. Brucella genus, its etiologic agent, is composed of intracellular bacteria that have evolved a prodigious ability to elude and shape host immunity to establish chronic infection. Brucella’s intracellular lifestyle and pathogen-associated molecular patterns, such as its specific lipopolysaccharide (LPS), are key factors for hiding and hampering recognition by the immune system. Here, we will review the current knowledge of evading and immunosuppressive mechanisms elicited by Brucella species to persist stealthily in their hosts, such as those triggered by their LPS and cyclic β-1,2-d-glucan or involved in neutrophil and monocyte avoidance, antigen presentation impairment, the modulation of T cell responses and immunometabolism. Attractive strategies exploited by other successful chronic pathogenic bacteria, including Mycobacteria, Salmonella, and Chlamydia, will be also discussed, with a special emphasis on the mechanisms operating in brucellosis, such as granuloma formation, pyroptosis, and manipulation of type I and III IFNs, B cells, innate lymphoid cells, and host lipids. A better understanding of these stratagems is essential to fighting bacterial chronic infections and designing innovative treatments and vaccines. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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29 pages, 3265 KiB

Open AccessReview

The Retrospective on Atypical Brucella Species Leads to Novel Definitions

by Alessandra Occhialini, Dirk Hofreuter, Christoph-Martin Ufermann, Sascha Al Dahouk and Stephan Köhler

Microorganisms 2022, 10(4), 813; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10040813 - 14 Apr 2022

Cited by 13 | Viewed by 3997

Abstract

The genus Brucella currently comprises twelve species of facultative intracellular bacteria with variable zoonotic potential. Six of them have been considered as classical, causing brucellosis in terrestrial mammalian hosts, with two species originated from marine mammals. In the past fifteen years, field research as well as improved pathogen detection and typing have allowed the identification of four new species, namely Brucella microti, Brucella inopinata, Brucella papionis, Brucella vulpis, and of numerous strains, isolated from a wide range of hosts, including for the first time cold-blooded animals. While their genome sequences are still highly similar to those of classical strains, some of them are characterized by atypical phenotypes such as higher growth rate, increased resistance to acid stress, motility, and lethality in the murine infection model. In our review, we provide an overview of state-of-the-art knowledge about these novel Brucella sp., with emphasis on their phylogenetic positions in the genus, their metabolic characteristics, acid stress resistance mechanisms, and their behavior in well-established in cellulo and in vivo infection models. Comparison of phylogenetic classification and phenotypical properties between classical and novel Brucella species and strains finally lead us to propose a more adapted terminology, distinguishing between core and non-core, and typical versus atypical brucellae, respectively. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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19 pages, 2613 KiB

Open AccessReview

Brucella and Its Hidden Flagellar System

by Roberto F. Coloma-Rivero, Manuel Flores-Concha, Raúl E. Molina, Rodrigo Soto-Shara, Ángelo Cartes and Ángel A. Oñate

Microorganisms 2022, 10(1), 83; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10010083 - 31 Dec 2021

Cited by 7 | Viewed by 5344

Abstract

Brucella, a Gram-negative bacterium with a high infective capacity and a wide spectrum of hosts in the animal world, is found in terrestrial and marine mammals, as well as amphibians. This broad spectrum of hosts is closely related to the non-classical virulence factors that allow this pathogen to establish its replicative niche, colonizing epithelial and immune system cells, evading the host’s defenses and defensive response. While motility is the primary role of the flagellum in most bacteria, in Brucella, the flagellum is involved in virulence, infectivity, cell growth, and biofilm formation, all of which are very important facts in a bacterium that to date has been described as a non-motile organism. Evidence of the expression of these flagellar proteins that are present in Brucella makes it possible to hypothesize certain evolutionary aspects as to where a free-living bacterium eventually acquired genetic material from environmental microorganisms, including flagellar genes, conferring on it the ability to reach other hosts (mammals), and, under selective pressure from the environment, can express these genes, helping it to evade the immune response. This review summarizes relevant aspects of the presence of flagellar proteins and puts into context their relevance in certain functions associated with the infective process. The study of these flagellar genes gives the genus Brucella a very high infectious versatility, placing it among the main organisms in urgent need of study, as it is linked to human health by direct contact with farm animals and by eventual transmission to the general population, where flagellar genes and proteins are of great relevance. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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29 pages, 2022 KiB

Open AccessOpinion

Facing the Human and Animal Brucellosis Conundrums: The Forgotten Lessons

by Edgardo Moreno, José-María Blasco and Ignacio Moriyón

Microorganisms 2022, 10(5), 942; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10050942 - 30 Apr 2022

Cited by 15 | Viewed by 5500

Abstract

Brucellosis is a major zoonotic disease caused by Brucella species. Historically, the disease received over fifty names until it was recognized as a single entity, illustrating its protean manifestations and intricacies, traits that generated conundrums that have remained or re-emerged since they were first described. Here, we examine confusions concerning the clinical picture, serological diagnosis, and incidence of human brucellosis. We also discuss knowledge gaps and prevalent confusions about animal brucellosis, including brucellosis control strategies, the so-called confirmatory tests, and assumptions about the primary-binding assays and DNA detection methods. We describe how doubtfully characterized vaccines have failed to control brucellosis and emphasize how the requisites of controlled safety and protection experiments are generally overlooked. Finally, we briefly discuss the experience demonstrating that S19 remains the best cattle vaccine, while RB51 fails to validate its claimed properties (protection, differentiating infected and vaccinated animals (DIVA), and safety), offering a strong argument against its current widespread use. These conundrums show that knowledge dealing with brucellosis is lost, and previous experience is overlooked or misinterpreted, as illustrated in a significant number of misguided meta-analyses. In a global context of intensifying livestock breeding, such recurrent oversights threaten to increase the impact of brucellosis. Full article

(This article belongs to the Special Issue Emerging Themes in Brucella and Brucellosis)

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