Ignacio Moriyón

Universidad de Navarra, Iruña, Navarre, Spain

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Publications (137)476.77 Total impact

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    ABSTRACT: Available reports on brucellosis in Nigeria are largely confined to cattle while it is believed that other ruminants like sheep and goats are equally exposed to the disease. To have an insight into the role of goats in the epidemiology of brucellosis in Nigeria, we conducted a cross-sectional study between June 2011 and May 2013 to determine the seroprevalence of brucellosis in goats in some selected states in Nigeria. Serum samples were collected from goats at different locations and tested for antibodies to Brucella spp using the Rose Bengal Test (RBT), samples positive by RBT were further subjected to Competitive Enzyme Linked Immunosorbent Assay (cELISA). Data collected to determine risk factors were also analysed using chi-square and logistics regression statistics. Out of a total of 2827 samples tested from the different states (Benue = 331; Borno =195; Oyo = 2155; Sokoto = 146), we recorded an overall seroprevalence of 2.83% (Benue = 17.30%; Borno = 2.05%; Oyo = 0.60% and Sokoto = 0.00%) by RBT. The cELISA further supported 9.45% (7/74) of the total RBT positive samples. Logistic regression analysis showed that the location (p = 0.004) and source (p < 0.0001); are probable risk factors to be considered in the epidemiology of brucellosis with sex (p = 0.179); age (p = 0.791) and breed (p = 0.369) not playing any major role. Our findings reveal a relatively low seroprevalence of brucellosis among goats screened except for Benue State. Since most of the goats sampled in the present study were from the abattoirs, further farm level investigations are required to determine the role of goats in the epidemiology of brucellosis in Nigeria since they share common environment with sheep and cattle that are natural hosts of Brucella species which are of major public health threat.
    Full-text · Article · Dec 2015 · African journal of medicine and medical sciences
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    ABSTRACT: Brucellosis is a highly contagious zoonosis caused by bacteria of the genus Brucella and affecting domestic and wild mammals. In this paper, the bacteriological and serological evidence of brucellosis in Sub-Saharan Africa (SSA) and its epidemiological characteristics are discussed. The tools available for the diagnosis and treatment of human brucellosis and for the diagnosis and control of animal brucellosis and their applicability in the context of SSA are presented and gaps identified. These gaps concern mostly the need for simpler and more affordable antimicrobial treatments against human brucellosis, the development of a B. melitensis vaccine that could circumvent the drawbacks of the currently available Rev 1 vaccine, and the investigation of serological diagnostic tests for camel brucellosis and wildlife. Strategies for the implementation of animal vaccination are also discussed.
    Full-text · Article · Nov 2015 · Acta tropica
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    ABSTRACT: Brucellosis is a worldwide widespread zoonosis caused by bacteria of the genus Brucella. Control of this disease in a given area requires an understanding of the Brucella species circulating in livestock and humans. However, because of the difficulties intrinsic to Brucella isolation and typing, such data are scarce for resource-poor areas. The paucity of bacteriological data and the consequent imperfect epidemiological picture are particularly critical for Sahelian and Sub-Sahara African countries. Here, we report on the characterization of 34 isolates collected between 1976 and 2012 from cattle, sheep and horses in Nigeria. All isolates were identified as Brucella abortus by Bruce-ladder PCR and assigned to biovar 3 by conventional typing. Further analysis by enhanced AMOS-ERY PCR showed that all of them belonged to the 3a sub-biovar, and MLVA analysis grouped them in a cluster clearly distinct from that formed by European B. abortus biovar 3b strains. Nevertheless, MLVA detected heterogeneity within the Nigerian biovar 3a strains. The close genetic profiles of the isolates from cattle, sheep and horses, suggest that, at least in some parts of Nigeria, biovar 3a circulates among animal species that are not the preferential hosts of B. abortus. Consistent with previous genetic analyses of 7 strains from Ivory Cost, Gambia and Togo, the analysis of these 34 Nigerian strains supports the hypothesis that the B. abortus biovar 3a lineage is dominant in West African countries. Copyright © 2015 Elsevier B.V. All rights reserved.
    Full-text · Article · Aug 2015 · Veterinary Microbiology
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    ABSTRACT: Tuberculosis and brucellosis are two major zoonosis, endemic in Morocco, leading to many impacts in animal and human health. They cause also an important socio economic effect. The present study was implemented to reach the objectives of an EU (European Union) project (Integrated Control Of Neglected Zoonoses). The workshop interested in the zoonosis of ruminant included the update of the epidemiological data in a pilot area situated in the north of Morocco. To reach the objectives of the research, a survey was directed with 125 randomly sampled household keepers, in parallel to a comparative intradermo-tuberculination for 1194 cattle, blood samples was taken from the same cattle and 1082 small ruminants. The screening of brucellosis accomplished using the buffered antigen test “Rose Bengale test”. A bacteriological brucellosis diagnosis and a PCR (Polimerase Chain Reaction) were performed to 21 milk samples, from seropositive cattle. Our investigation results on an overall prevalence of 18.8% for bovine tuberculosis, 1.3% for bovine brucellosis, the prevalence of infected farms with bovine tuberculosis and brucellosis were respectively 56% and 6.8%. Brucella was isolated from two samples and typing with the multiplex PCR assay ‘Bruceladder’ characterised strains as Brucella. abortus. Analysis of risk factors for the transmission of two zoonoses to humans, leads to a percentage of presence ranging from 8.6% to peddling milk, to 100% for the consumption of raw milk. The truth that adapted awareness is essential for complement the struggle against zoonoses stems from the comparison of the results of testing to the beliefs of breeders. A need for a socio-economic study has been recognized to discover the cost effectiveness for any control strategy which will be implemented in the future. For tuberculosis, a study investigating the prevalence of M. Bovis in humans needs to be implemented to generate a complete analysis of the cost of bovine tuberculosis.
    No preview · Conference Paper · Jun 2015
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    ABSTRACT: Tuberculosis and brucellosis are two major zoonosis, endemic in Morocco, leading to many impacts in animal and human health. They cause also an important socio economic effect. The present study was implemented to reach the objectives of an EU (European Union) project (Integrated Control Of Neglected Zoonoses). The workshop interested in the zoonosis of ruminant included the update of the epidemiological data in a pilot area situated in the north of Morocco. To reach the objectives of the research, a survey was directed with 125 randomly sampled household keepers, in parallel to a comparative intradermo-tuberculination for 1194 cattle, blood samples was taken from the same cattle and 1082 small ruminants. The screening of brucellosis accomplished using the buffered antigen test “Rose Bengale test”. A bacteriological brucellosis diagnosis and a PCR (Polimerase Chain Reaction) were performed to 21 milk samples, from seropositive cattle. Our investigation results on an overall prevalence of 18.8% for bovine tuberculosis, 1.3% for bovine brucellosis, the prevalence of infected farms with bovine tuberculosis and brucellosis were respectively 56% and 6.8%. Brucella was isolated from two samples and typing with the multiplex PCR assay ‘Bruceladder’ characterised strains as Brucella. abortus. Analysis of risk factors for the transmission of two zoonoses to humans, leads to a percentage of presence ranging from 8.6% to peddling milk, to 100% for the consumption of raw milk. The truth that adapted awareness is essential for complement the struggle against zoonoses stems from the comparison of the results of testing to the beliefs of breeders. A need for a socio-economic study has been recognized to discover the cost effectiveness for any control strategy which will be implemented in the future. For tuberculosis, a study investigating the prevalence of M. Bovis in humans needs to be implemented to generate a complete analysis of the cost of bovine tuberculosis.
    No preview · Conference Paper · Jun 2015
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    Full-text · Article · Mar 2015 · PLoS neglected tropical diseases
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    ABSTRACT: Abstract Brucella is the causing agent of a chronic zoonosis called brucellosis. The Brucella beta-1,2 cyclic glucan (CβG) is a virulence factor, which has been described as a potent immune stimulator, albeit with no toxicity for cells and animals. We first used a genome-wide approach to characterize human myeloid dendritic cell (mDC) responses to CβG. Transcripts related to inflammation (IL-6, IL2RA, PTGS2), chemokine (CXCR7, CXCL2) and anti-inflammatory pathways (TNFAIP6, SOCS3) were highly expressed in CβG-treated mDC. In mouse GMCSF-derived DC, CβG triggered the expression of both activation (CXCL2, KC) and inhibition (SOCS3 and TNFAIP6) molecules. We then characterized the inflammatory infiltrates at the level of mouse ear when injected with CβG or LPS. CβG yielded a lower and transient recruitment of neutrophils compared to LPS. The consequence of these dual pro- and anti-inflammatory signals triggered by CβG corresponds to the induction of a controlled local inflammation.
    No preview · Article · Feb 2015 · Virulence
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    ABSTRACT: Swine brucellosis caused by Brucella suis biovar 2 is an emerging disease in Europe. Currently used diagnostic tests for swine brucellosis detect antibodies to the O-polysaccharide (O-PS) of Brucella smooth lipopolysaccharide (S-LPS) but their specificity is compromised by false-positive serological reactions (FPSRs) when bacteria carrying cross-reacting O-PS infect pigs. FPSRs occur throughout Europe, and the only tool available for a specific B. suis diagnosis is the intradermal test with Brucella protein extracts free of O-PS or S-LPS. Using sera of 162 sows naturally infected by B. suis biovar 2, 406 brucellosis-free sows, and 218 pigs of brucellosis-free farms affected by FPSR, we assessed the diagnostic performance of an indirect ELISA with rough LPS (thus devoid of O-PS) and of gel immunodiffusion, counterimmunoelectrophoresis, latex agglutination and indirect ELISA with O-PS free proteins in comparison with several S-LPS tests (Rose Bengal, complement fixation, gel immunodiffusion and indirect ELISA). When adjusted to 100% specificity, the sensitivity of the rough LPS ELISA was very low (30%), and adoption of other cut-offs resulted in poor specificity/sensitivity ratios. Although their specificity was 100%, the sensitivity of protein tests (ELISA, latex agglutination, counterimmunoelectrophoresis, and gel immunodiffusion) was only moderate (45, 58, 61 and 63%, respectively). Among S-LPS tests, gel immunodiffusion was the only test showing acceptable sensitivity/specificity (68 and 100%, respectively). Despite these shortcomings, and when the purpose is to screen out FPSR at herd level, gel immunodiffusion tests may offer a technically simple and practical alternative to intradermal testing. Copyright © 2015 Elsevier B.V. All rights reserved.
    No preview · Article · Feb 2015 · Journal of Microbiological Methods
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    ABSTRACT: Erythritol is an important nutrient for several α-2 Proteobacteria, including N2-fixing plant endosymbionts and Brucella, a worldwide pathogen that finds this four-carbon polyol in genital tissues. Erythritol metabolism involves phosphorylation to L-erythritol-4-phosphate by the kinase EryA and oxidation of the latter to L-3-tetrulose 4-phosphate by the dehydrogenase EryB. It is accepted that further steps involve oxidation by the putative dehydrogenase EryC and subsequent decarboxylation to yield triose-phosphates. Accordingly, growth on erythritol as the sole C source should require aldolase and fructose-1,6-bisphosphatase to produce essential hexose-6-monophosphate. However, we observed that a mutant devoid of fructose-1,6-bisphosphatases grew normally on erythritol and that EryC, which was assumed to be a dehydrogenase, actually belongs to the xylose isomerase superfamily. Moreover, we found that TpiA2 and RpiB, distant homologs of triose phosphate isomerase and ribose 5-phosphate isomerase B, were necessary, as previously shown for Rhizobium. By using purified recombinant enzymes, we demonstrated that L-3-tetrulose-4-phosphate was converted to D-erythrose 4-phosphate through three previously unknown isomerization reactions catalyzed by EryC (tetrulose-4-phosphate racemase), TpiA2 (D-3-tetrulose-4-phosphate isomerase; renamed EryH), and RpiB (D-erythrose-4-phosphate isomerase; renamed EryI), a pathway fully consistent with the isotopomer distribution of the erythrose-4-phosphate-derived amino acids phenylalanine and tyrosine obtained from bacteria grown on (13)C-labeled erythritol. D-erythrose-4-phosphate is then converted by enzymes of the pentose phosphate pathway to glyceraldehyde 3-phosphate and fructose 6-phosphate, thus bypassing fructose-1,6-bisphosphatase. This is the first description to our knowledge of a route feeding carbohydrate metabolism exclusively via D-erythrose 4-phosphate, a pathway that may provide clues to the preferential metabolism of erythritol by Brucella and its role in pathogenicity.
    Full-text · Article · Dec 2014 · Proceedings of the National Academy of Sciences
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    ABSTRACT: Abstract The brucellae are α-Proteobacteria causing brucellosis, an important zoonosis. Although multiplying in endoplasmic reticulum-derived vacuoles, they cause no cell death, suggesting subtle but efficient use of host resources. Brucellae are amino-acid prototrophs able to grow with ammonium or use glutamate as the sole carbon-nitrogen source in vitro. They contain more than twice amino acid/peptide/polyamine uptake genes than the amino-acid auxotroph Legionella pneumophila, which multiplies in a similar vacuole, suggesting a different nutritional strategy. During these two last decades, many mutants of key actors in nitrogen metabolism (transporters, enzymes, regulators, etc.) have been described to be essential for full virulence of brucellae. Here, we review the genomic and experimental data on Brucella nitrogen metabolism and its connection with virulence. An analysis of various aspects of this metabolism (transport, assimilation, biosynthesis, catabolism, respiration and regulation) has highlighted differences and similarities in nitrogen metabolism with other α-Proteobacteria. Together, these data suggest that, during their intracellular life cycle, the brucellae use various nitrogen sources for biosynthesis, catabolism and respiration following a strategy that requires prototrophy and a tight regulation of nitrogen use.
    Full-text · Article · Dec 2014 · Critical Reviews in Microbiology
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    ABSTRACT: Current serological tests for swine brucellosis detect antibodies to the Brucella O-polysaccharide (O/PS). However, when infections by bacteria carrying cross-reacting O/PS occur, these tests suffer from false positive serological reactions (FPSR), and the skin test with Brucella soluble protein extracts is the best diagnostic alternative to differentiate true Brucella suis infections from FPSR in pigs. Since this test has been seldom used in B. suis infected swine, the clinical and histological features involved have not been described properly. Here, we describe the clinical and histological events in B. suis biovar 2 infected pigs skin tested with a cytosoluble O/PS free protein extract from rough Brucella abortus Tn5::per mutant. A similar extract from rough Ochrobactrum intermedium was also used for comparative purposes. No relevant differences were evidenced between the homologous and heterologous allergens, and the main clinical feature was an elevated area of the skin showing different induration degrees. Moreover, an important vascular reaction with hyperemia and haemorrhage was produced in most infected sows 24-48h after inoculation, thus facilitating the clinical interpretation of positive reactions. Histologically, combined immediate (type III) and delayed (type IV) hypersensitivity reactions were identified as the most relevant feature of the inflammatory responses produced. Copyright © 2014 Elsevier B.V. All rights reserved.
    No preview · Article · Nov 2014 · Veterinary Immunology and Immunopathology
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    ABSTRACT: Brucella spp. are Gram-negative bacteria that behave as facultative intracellular parasites of a variety of mammals. This genus includes smooth (S) and rough (R) species that carry S and R lipopolysaccharides (LPS), respectively. S-LPS is a virulence factor, and mutants affected in the S-LPS O-polysaccharide (R mutants), core oligosaccharide or both show attenuation. However, B. ovis is naturally R and is virulent in sheep. We studied the role of B. ovis LPS in virulence by mutating the orthologues of wadA, wadB and wadC, three genes known to encode LPS core glycosyltransferases in S brucellae. When mapped with antibodies to outer membrane proteins (Omps) and R-LPS, wadB and wadC mutants displayed defects in LPS structure and outer membrane topology but inactivation of wadA had little or no effect. Consistent with these observations, the wadB and wadC but not the wadA mutants were attenuated in mice. When tested as vaccines, the wadB and wadC mutants protected mice against B. ovis challenge. The results demonstrate that the LPS core is a structure essential for survival in vivo not only of S brucellae but also of a naturally R Brucella pathogenic species, and they confirm our previous hypothesis that the Brucella LPS core is a target for vaccine development. Since vaccine B. melitensis Rev 1 is S and thus interferes in serological testing for S brucellae, wadB mutant represents a candidate vaccine to be evaluated against B. ovis infection of sheep suitable for areas free of B. melitensis.
    No preview · Article · Jul 2014 · Veterinary Research
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    ABSTRACT: Brucella spp. are Gram-negative bacteria that behave as facultative intracellular parasites of a variety of mammals. This genus includes smooth (S) and rough (R) species that carry S and R lipopolysaccharides (LPS), respectively. S-LPS is a virulence factor, and mutants affected in the S-LPS O-polysaccharide (R mutants), core oligosaccharide or both show attenuation. However, B. ovis is naturally R and is virulent in sheep. We studied the role of B. ovis LPS in virulence by mutating the orthologues of wadA, wadB and wadC, three genes known to encode LPS core glycosyltransferases in S brucellae. When mapped with antibodies to outer membrane proteins (Omps) and R-LPS, wadB and wadC mutants displayed defects in LPS structure and outer membrane topology but inactivation of wadA had little or no effect. Consistent with these observations, the wadB and wadC but not the wadA mutants were attenuated in mice. When tested as vaccines, the wadB and wadC mutants protected mice against B. ovis challenge. The results demonstrate that the LPS core is a structure essential for survival in vivo not only of S brucellae but also of a naturally R Brucella pathogenic species, and they confirm our previous hypothesis that the Brucella LPS core is a target for vaccine development. Since vaccine B. melitensis Rev 1 is S and thus interferes in serological testing for S brucellae, wadB mutant represents a candidate vaccine to be evaluated against B. ovis infection of sheep suitable for areas free of B. melitensis.
    Full-text · Article · Jul 2014 · Veterinary Research
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    ABSTRACT: Nigeria is the most populous country in Africa, has a large proportion of the world's poor livestock keepers, and is a hotspot for neglected zoonoses. A review of the 127 accessible publications on brucellosis in Nigeria reveals only scant and fragmented evidence on its spatial and temporal distribution in different epidemiological contexts. The few bacteriological studies conducted demonstrate the existence of Brucella abortus in cattle and sheep, but evidence for B. melitensis in small ruminants is dated and unclear. The bulk of the evidence consists of seroprevalence studies, but test standardization and validation are not always adequately described, and misinterpretations exist with regard to sensitivity and/or specificity and ability to identify the infecting Brucella species. Despite this, early studies suggest that although brucellosis was endemic in extensive nomadic systems, seroprevalence was low, and brucellosis was not perceived as a real burden; recent studies, however, may reflect a changing trend. Concerning human brucellosis, no studies have identified the Brucella species and most reports provide only serological evidence of contact with Brucella in the classical risk groups; some suggest brucellosis misdiagnoses as malaria or other febrile conditions. The investigation of a severe outbreak that occurred in the late 1970s describes the emergence of animal and human disease caused by the settling of previously nomadic populations during the Sahelian drought. There appears to be an increasing risk of re-emergence of brucellosis in sub-Saharan Africa, as a result of the co-existence of pastoralist movements and the increase of intensive management resulting from growing urbanization and food demand. Highly contagious zoonoses like brucellosis pose a threat with far-reaching social and political consequences.
    Full-text · Article · Jul 2014 · PLoS Neglected Tropical Diseases
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    ABSTRACT: The brucellae are the etiological agents of brucellosis, a worldwide-distributed zoonosis. These bacteria are facultative intracellular parasites, and thus are able to adjust their metabolism to the extra and intracellular environments encountered during an infectious cycle. However, this aspect of Brucella biology is imperfectly known and the nutrients available in the intracellular niche are unknown. Here, we investigated the central pathways of C metabolism used by Brucella abortus by deleting the putative fructose-1,6-bisphosphatases (fbp and glpX), phosphoenolpyruvate carboxykinase (pckA), pyruvate phosphate dikinase (ppdK) and malic enzyme (mae) genes. In gluconeogenic but not in rich media, growth of mutants ΔppdK and Δmae was severely impaired and growth of the double Δfbp-ΔglpX mutant was reduced. In macrophages, only ΔppdK and Δmae showed reduced multiplication, and studies with ΔppdK confirmed that it reached the replicative niche. Similarly, only ΔppdK and Δmae were attenuated in mice, the former being cleared by week 10 and the latter persisting longer than 12 weeks. We also investigated the glyoxylate cycle. Although aceA (isocitrate lyase) promoter activity was enhanced in rich medium, aceA disruption had no effect in vitro or on multiplication in macrophages or mouse spleens. The results suggest that B. abortus grows intracellularly using a limited supply of 6 C (and 5 C) sugars that is compensated by glutamate and possibly other amino acids entering the Krebs cycle without a critical role of the glyoxylate shunt.
    Full-text · Article · Jun 2014 · Journal of Bacteriology
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    ABSTRACT: Brucellosis is a worldwide extended zoonosis caused by Brucella spp. These gram-negative bacteria are not readily detected by innate immunity, a virulence-related property largely linked to their surface lipopolysaccharide (LPS). The role of the LPS lipid A and O-polysaccharide in virulence is well known. Moreover, mutation of the glycosyltransferase gene wadC of B. abortus, although not affecting O-polysaccharide assembly onto the lipid-A core section causes a core oligosaccharide defect that increases recognition by innate immunity. Here, we report on a second gene (wadB) encoding a LPS core glycosyltransferase not involved in the assembly of the O-polysaccharide-linked core section. As compared to wild-type B. abortus, a wadB mutant was sensitive to bactericidal peptides and non-immune serum, and was attenuated in mice and dendritic cells. These observations show that as WadC, WadB is also involved in the assembly of a branch of Brucella LPS core and support the concept that this LPS section is a virulence-related structure.
    Full-text · Article · Jun 2014 · Microbial Pathogenesis
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    Full-text · Article · Apr 2014
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    ABSTRACT: Brucellosis is a worldwide extended zoonosis caused by Brucella spp. These gram-negative bacteria are not readily detected by innate immunity, a virulence-related property largely linked to their surface lipopolysaccharide (LPS). The role of the LPS lipid A and O-polysaccharide in virulence is well known. Moreover, mutation of the glycosyltransferase gene wadC of B. abortus, although not affecting O-polysaccharide assembly onto the lipid-A core section causes a core oligosaccharide defect that increases recognition by innate immunity. Here, we report on a second gene (wadB) encoding a LPS core glycosyltransferase not involved in the assembly of the O-polysaccharide-linked core section. As compared to wild-type B. abortus, a wadB mutant was sensitive to bactericidal peptides and non-immune serum, and was attenuated in mice and dendritic cells. These observations show that as WadC, WadB is also involved in the assembly of a branch of Brucella LPS core and support the concept that this LPS section is a virulence-related structure.
    Full-text · Article · Jan 2014 · Microbial Pathogenesis
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    Full-text · Dataset · Nov 2013
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    ABSTRACT: Swine brucellosis by Brucella suis biovar 2 is an emerging disease whose control is based on serological testing and culling. However, current serological tests detect antibodies to the O-polysaccharide (O/PS) moiety of Brucella smooth lipopolysaccharide (S-LPS), and thus lack specificity when infections by Yersinia enterocolitica O:9 and other gram-negative bacteria carrying cross-reacting O/PS occur. The skin test with the protein-rich brucellin extract obtained from rough B. melitensis B115 is assumed to be specific for discriminating these false positive serological reactions (FPSR). However, B115 strain, although unable to synthesize S-LPS, accumulates O/PS internally, which could cause diagnostic problems. Since the brucellin skin test has been seldom used in pigs and FPSR are common in these animals, we assessed its performance using cytosoluble protein extracts obtained from B. abortus rough mutants in manBcore or per genes (critical for O/PS biosynthesis) and B. melitensis B115. The diagnostic sensitivity and specificity were determined in B. suis biovar 2 culture positive and brucellosis free sows, and apparent prevalence in sows of unknown individual bacteriological and serological status belonging to B. suis biovar 2 naturally infected herds. Moreover, the specificity in discriminating brucellosis from FPSR was assessed in brucellosis free boars showing FPSR. The skin test with B. abortus ΔmanBcore and B. melitensis B115 allergens performed similarly, and the former one resulted in 100% specificity when testing animals showing FPSR in indirect ELISA, Rose Bengal and complement fixation serological tests. We conclude that O/PS-free genetically defined mutants represent an appropriate alternative to obtain Brucella protein extracts for diagnosing swine brucellosis.
    No preview · Article · Nov 2013 · Veterinary Microbiology

Publication Stats

5k Citations
476.77 Total Impact Points

Institutions

  • 1979-2015
    • Universidad de Navarra
      • • Department of Microbiology and Parasitology
      • • Department of Urology
      • • School of Medicine
      Iruña, Navarre, Spain
  • 2010
    • Hannover Medical School
      Hanover, Lower Saxony, Germany
  • 1987
    • University of Costa Rica
      • Centro de Investigación en Biología Celular y Molecular (CIBCM)
      San José, Provincia de San Jose, Costa Rica
  • 1986
    • Universidad de Pamplona
      Памплона, Norte de Santander, Colombia
  • 1983
    • University of Wisconsin–Madison
      Madison, Wisconsin, United States