The emergence of Brucella canis as a public health threat in Europe: what we know and what we need to learn

References

• Day MJ. Cats are not small dogs: is there an immunological explanation for why cats are less affected by arthropod-borne disease than dogs? Parasit Vectors. 2016;9:507. doi:10.1186/s13071-016-1798-5
   PubMed Web of Science ®Google Scholar
• HCSP. Avis relatif à la conduite à tenir vis-à-vis de personnes exposées à des animaux contaminés par Brucella canis. publique HC de la santé, editor. 2022; Available from: https://www.hcsp.fr/Explore.cgi/Telecharger?NomFichier=hcspa20220318_cotevividepeexdeanatdebrca.pdf.
   Google Scholar
• HAIRS members and external experts. Risk review and statement on the risk Brucella canis presents to the UK human population [Internet]. HAIRS; 2021. Available from: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/960013/20210210_Brucella_canis_statement.pdf.
   Google Scholar
• Celli J. The intracellular life cycle of Brucella spp. Microbiol Spectr. 2019;7. Available from: https://www.ncbi.nlm.nih.gov/pubmed/30848234.
   PubMed Web of Science ®Google Scholar
• Stranahan LW, Arenas-Gamboa AM. When the going gets rough: The significance of Brucella lipopolysaccharide phenotype in host-pathogen interactions. Front Microbiol. 2021;12:713157. doi:10.3389/fmicb.2021.713157
   PubMed Web of Science ®Google Scholar
• Fernández AG, Hielpos MS, Ferrero MC, et al. Proinflammatory response of canine trophoblasts to Brucella canis infection. PLOS ONE. 2017;12:e0186561.
   PubMed Web of Science ®Google Scholar
• Ahmed W, Zheng K, Liu ZF. Establishment of chronic infection: Brucella’s stealth strategy. Front Cell Infect Microbiol. 2016;6:30. doi:10.3389/fcimb.2016.00030
   PubMed Web of Science ®Google Scholar
• Bin Park W, Kim S, Kyung SM, et al. Gene expression of toll-like receptors, cytokines and a nuclear factor and cytokine secretion in DH82 canine macrophage cells infected with Brucella canis. Vet Immunol Immunopathol. 2023;260:110607. doi:10.1016/j.vetimm.2023.110607
   PubMed Web of Science ®Google Scholar
• Lucero NE, Corazza R, Almuzara MN, et al. Human Brucella canis outbreak linked to infection in dogs. Epidemiol Infect. 2010;138:280–285. doi:10.1017/S0950268809990525
   PubMed Web of Science ®Google Scholar
• Hensel ME, Negron M, Arenas-Gamboa AM. Brucellosis in dogs and public health risk. Emerg Infect Dis. 2018;24:1401–1406. doi:10.3201/eid2408.171171
   PubMed Web of Science ®Google Scholar
• Carmichael LE, Joubert JC. Transmission of Brucella canis by contact exposure. Cornell Vet. 1988;78:63–73.
   PubMedGoogle Scholar
• De Massis F, Sacchini F, Averaimo D, et al. First isolation of Brucella canis from a breeding kennel in Italy. Vet Ital. 2021;57:3.
   PubMed Web of Science ®Google Scholar
• Ferreira Vicente A, Girault G, Corde Y, et al. New insights into phylogeography of worldwide Brucella canis isolates by comparative genomics-based approaches: focus on Brazil. BMC Genomics. 2018;19:636. doi:10.1186/s12864-018-5001-6
   PubMed Web of Science ®Google Scholar
• Buhmann G, Paul F, Herbst W, et al. Canine Brucellosis: insights into the epidemiologic situation in Europe. Front Vet Sci. 2019;6:151. doi:10.3389/fvets.2019.00151
   PubMed Web of Science ®Google Scholar
• Whatmore P, Friggens. Second UK isolation of Brucella canis. Vet Rec. 2017;180:617.
   Web of Science ®Google Scholar
• Egloff S, Schneeberger M, Gobeli S, et al. Brucella canis infection in a young dog with epididymitis and orchitis. Schweiz Arch Tierheilkd. 2018;160:743–748. doi:10.17236/sat00190
   PubMed Web of Science ®Google Scholar
• van Dijk MAM, Engelsma MY, Visser VXN, et al. Transboundary spread of Brucella canis through import of infected dogs, The Netherlands, November 2016–December 2018. Emerg Infect Dis. 2021;27:1783–1788. doi:10.3201/eid2707.201238
   PubMed Web of Science ®Google Scholar
• Ahmet Murat S, Altuntaş MB, ÖZ Gülserenyildiz, et al. The first-time isolation of Brucella canis from two aborted bitches in a kennel in Turkey. Turk J Vet Anim Sci. 2018;42:3.
   Web of Science ®Google Scholar
• Holst BS, Lofqvist K, Ernholm L, et al. The first case of Brucella canis in Sweden: background, case report and recommendations from a northern European perspective. Acta Vet Scand. 2012;54:18. doi:10.1186/1751-0147-54-18
   PubMed Web of Science ®Google Scholar
• Kaden R, Agren J, Ferrari S, et al. Whole-genome sequence of Brucella canis strain SVA13, isolated from an infected dog. Genome Announc. 2014: 2. Available from: https://www.ncbi.nlm.nih.gov/pubmed/25035330.
   Google Scholar
• Morgan, Rys, Wake, et al. Brucella canis in a dog in the UK. Vet Rec. 2017;180:384–385. doi:10.1136/vr.j2143
   PubMed Web of Science ®Google Scholar
• Corrente M, Franchini D, Decaro N, et al. Detection of Brucella canis in a dog in Italy. New Microbiol 2010;33:337–341.
   PubMed Web of Science ®Google Scholar
• Dentinger CM, Jacob K, Lee LV, et al. Human Brucella canis infection and subsequent laboratory exposures associated with a puppy, New York city, 2012. Zoonoses Public Health. 2015;62:407–414. doi:10.1111/zph.12163
   PubMed Web of Science ®Google Scholar
• Kolwijck E, Lutgens SP, Visser VX, et al. First case of human Brucella canis infection in The Netherlands. Clin Infect Dis. 2022. Available from: https://www.ncbi.nlm.nih.gov/pubmed/35653425.
   PubMed Web of Science ®Google Scholar
• Ledbetter EC, Landry MP, Stokol T, et al. Brucella canis endophthalmitis in 3 dogs: clinical features, diagnosis, and treatment. Vet Ophthalmol. 2009;12:183–191. doi:10.1111/j.1463-5224.2009.00690.x
   PubMed Web of Science ®Google Scholar
• Alton GG, Jones LM, Angus RD, et al. Techniques for the brucellosis laboratory. Paris: INRA; 1988.
   Google Scholar
• Elbehiry A, Aldubaib M, Al Rugaie O, et al. Proteomics-based screening and antibiotic resistance assessment of clinical and sub-clinical Brucella species: an evolution of brucellosis infection control. PloS One. 2022;17:e0262551.
   PubMed Web of Science ®Google Scholar
• Ferreira L, Vega Castano S, Sanchez-Juanes F, et al. Identification of Brucella by MALDI-TOF mass spectrometry. Fast and reliable identification from agar plates and blood cultures. PLoS One. 2010;5:e14235. doi:10.1371/journal.pone.0014235
   PubMed Web of Science ®Google Scholar
• Scholz HC, Pfeffer M, Witte A, et al. Specific detection and differentiation of Ochrobactrum anthropi, Ochrobactrum intermedium and Brucella spp. by a multi-primer PCR that targets the recA gene. J Med Microbiol. 2008;57:64–71. doi:10.1099/jmm.0.47507-0
   PubMed Web of Science ®Google Scholar
• Bounaadja L, Albert D, Chénais B, et al. Real-time PCR for identification of Brucella spp.: a comparative study of IS711, bcsp31 and per target genes. Vet Microbiol. 2009;137:156–164. doi:10.1016/j.vetmic.2008.12.023
   PubMed Web of Science ®Google Scholar
• Lopez-Goni I, Garcia-Yoldi D, Marin CM, et al. New Bruce-ladder multiplex PCR assay for the biovar typing of Brucella suis and the discrimination of Brucella suis and Brucella canis. Vet Microbiol. 2011;154:152–155. doi:10.1016/j.vetmic.2011.06.035
   PubMed Web of Science ®Google Scholar
• Girault G, Perrot L, Mick V, et al. High-resolution melting PCR as rapid genotyping tool for Brucella species. Microorganisms 2022: 10. Available from: https://www.ncbi.nlm.nih.gov/pubmed/35208791.
   PubMed Web of Science ®Google Scholar
• Keid LB, Soares RM, Vieira NR, et al. Diagnosis of canine brucellosis: comparison between serological and microbiological tests and a PCR based on primers to 16S-23S rDNA interspacer. Vet Res Commun. 2007;31:951–965. doi:10.1007/s11259-006-0109-6
   PubMed Web of Science ®Google Scholar
• Keid LB, Soares RM, Vasconcellos SA, et al. A polymerase chain reaction for detection of Brucella canis in vaginal swabs of naturally infected bitches. Theriogenology. 2007;68:1260–1270. doi:10.1016/j.theriogenology.2007.08.021
   PubMed Web of Science ®Google Scholar
• Boeri EJ, Wanke MM, Madariaga MJ, et al. Comparison of four polymerase chain reaction assays for the detection of Brucella spp. in clinical samples from dogs. Vet World. 2018;11:201–208. doi:10.14202/vetworld.2018.201-208
   PubMed Web of Science ®Google Scholar
• Batinga MCA, de Lima JTR, Gregori F, et al. Comparative application of IS711-based polymerase chain reaction (PCR) and loop-mediated isothermal amplification (LAMP) for canine brucellosis diagnosis. Mol Cell Probes. 2018;39:1–6. doi:10.1016/j.mcp.2018.02.003
   PubMed Web of Science ®Google Scholar
• Ashford R, Brucella W. Mol typing bact infect. de Filippis. Springer International Publishing; 2022. p. 217–245.
   Google Scholar
• Carmichael LE, Joubert JC. A rapid slide agglutination test for the serodiagnosis of Brucella canis infection that employs a variant (M-) organism as antigen. Cornell Vet. 1987;77:3–12.
   PubMedGoogle Scholar
• Keid LB, Soares RM, Vasconcellos SA, et al. Comparison of agar gel immunodiffusion test, rapid slide agglutination test, microbiological culture and PCR for the diagnosis of canine brucellosis. Res Vet Sci. 2009;86:22–26. doi:10.1016/j.rvsc.2008.05.012
   PubMed Web of Science ®Google Scholar
• Keid LB, Diniz JA, Oliveira TM, et al. Evaluation of an immunochromatographic test to the diagnosis of Canine Brucellosis caused by Brucella canis. Reprod Domest Anim. 2015;50:939–944. doi:10.1111/rda.12612
   PubMed Web of Science ®Google Scholar
• Wanke MM, Cairó F, Rossano M, et al. Preliminary study of an immunochromatography test for serological diagnosis of canine brucellosis. Reprod Domest Anim Zuchthyg. 2012;47(Suppl 6):370–372. doi:10.1111/rda.12108
   PubMedGoogle Scholar
• Escobar GI, Boeri EJ, Ayala SM, et al. The feasibility of using antigens prepared with rough Brucella strains for diagnosis of canine brucellosis. Rev Argent Microbiol. 2010;42:35–40.
   PubMed Web of Science ®Google Scholar
• Badakhsh FF, Carmichael LE, Douglass JA. Improved rapid slide agglutination test for presumptive diagnosis of canine brucellosis. J Clin Microbiol. 1982;15:286–289. doi:10.1128/jcm.15.2.286-289.1982
   PubMed Web of Science ®Google Scholar
• Zoha SJ, Carmichael LE. Serological responses of dogs to cell wall and internal antigens of Brucella canis (B. canis). Vet Microbiol. 1982;7:35–50. doi:10.1016/0378-1135(82)90004-9
   PubMed Web of Science ®Google Scholar
• Lucero NE, Escobar GI, Ayala SM, et al. Sensitivity and specificity of an indirect enzyme-linked immunoassay for the diagnosis of Brucella canis infection in dogs. J Med Microbiol. 2002;51:656–660. doi:10.1099/0022-1317-51-8-656
   PubMed Web of Science ®Google Scholar
• de Oliveira MZ, Vale V, Keid L, et al. Validation of an ELISA method for the serological diagnosis of canine brucellosis due to Brucella canis. Res Vet Sci. 2011;90:425–431. doi:10.1016/j.rvsc.2010.07.004
   PubMed Web of Science ®Google Scholar
• Baldi PC, Wanke MM, Loza ME, et al. Brucella abortus cytoplasmic proteins used as antigens in an ELISA potentially useful for the diagnosis of canine brucellosis. Vet Microbiol. 1994;41:127–134. doi:10.1016/0378-1135(94)90142-2
   PubMed Web of Science ®Google Scholar
• Baldi PC, Wanke MM, Loza ME, et al. Diagnosis of canine brucellosis by detection of serum antibodies against an 18 kDa cytoplasmic protein of Brucella spp. Vet Microbiol. 1997;57:273–281. doi:10.1016/S0378-1135(97)00134-X
   PubMed Web of Science ®Google Scholar
• Cortina ME, Novak A, Melli LJ, et al. Development of improved enzyme-based and lateral flow immunoassays for rapid and accurate serodiagnosis of canine brucellosis. Vet Microbiol. 2017;208:174–180. doi:10.1016/j.vetmic.2017.08.005
   PubMed Web of Science ®Google Scholar
• Mateu-de-Antonio EM, Martín M, Soler M. Use of indirect enzyme-linked immunosorbent assay with hot saline solution extracts of a variant (M-) strain of Brucella canis for diagnosis of brucellosis in dogs. Am J Vet Res. 1993;54:1043–1046.
   PubMed Web of Science ®Google Scholar
• Kim JW, Lee YJ, Han MY, et al. Evaluation of immunochromatographic assay for serodiagnosis of Brucella canis. J Vet Med Sci. 2007;69:1103–1107. doi:10.1292/jvms.69.1103
   PubMed Web of Science ®Google Scholar
• Ducrotoy MJ, Muñoz PM, Conde-Álvarez R, et al. A systematic review of current immunological tests for the diagnosis of cattle brucellosis. Prev Vet Med. 2018;151:57–72. doi:10.1016/j.prevetmed.2018.01.005
   PubMed Web of Science ®Google Scholar
• Santos RL, Souza TD, Mol JPS, et al. Canine brucellosis: an update. Front Vet Sci. 2021;8:594291. doi:10.3389/fvets.2021.594291
   PubMed Web of Science ®Google Scholar
• de Souza TD, de Carvalho TF, Mol J, et al. Tissue distribution and cell tropism of Brucella canis in naturally infected canine foetuses and neonates. Sci Rep. 2018;8:7203. doi:10.1038/s41598-018-25651-x
   PubMed Web of Science ®Google Scholar
• Falenski A, Mayer-Scholl A, Filter M, et al. Survival of Brucella spp. in mineral water, milk and yogurt. Int J Food Microbiol. 2011;145:326–330. doi:10.1016/j.ijfoodmicro.2010.11.033
   PubMed Web of Science ®Google Scholar
• Lawaczeck E, Toporek J, Cwikla J, et al. Brucella canis in a HIV-infected patient. Zoonoses Public Health. 2011;58:150–152. doi:10.1111/j.1863-2378.2010.01334.x
   PubMed Web of Science ®Google Scholar
• Lucero NE, Escobar GI, Ayala SM, et al. Diagnosis of human brucellosis caused by Brucella canis. J Med Microbiol. 2005;54:457–461. doi:10.1099/jmm.0.45927-0
   PubMed Web of Science ®Google Scholar
• Wallach JC, Giambartolomei GH, Baldi PC, et al. Human infection with M- strain of Brucella canis. Emerg Infect Dis. 2004;10:146–148. doi:10.3201/eid1001.020622
   PubMed Web of Science ®Google Scholar
• Pereira CR, Cotrim de Almeida JVF, Cardoso de Oliveira IR, et al. Occupational exposure to Brucella spp.: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2020;14:e0008164.
   PubMed Web of Science ®Google Scholar
• Ahmed-Bentley J, Roman S, Mirzanejad Y, et al. Laboratory exposures from an unsuspected case of human infection with Brucella canis. Emerg Infect Dis. 2021;27:2489–2491. doi:10.3201/eid2709.204701
   PubMed Web of Science ®Google Scholar
• Viana MVC, Wattam AR, Govil Batra D, et al. Genome sequences of three Brucella canis strains isolated from humans and a dog. Genome Announc. 2017;5:e01688–16.
   PubMedGoogle Scholar
• Lum MK, Pien FD, Sasaki DM. Human Brucella canis infection in Hawaii. Hawaii Med J. 1985;44:66–68.
   PubMedGoogle Scholar
• Nomura A, Imaoka K, Imanishi H, et al. Human Brucella canis infections diagnosed by blood culture. Emerg Infect Dis. 2010;16:1183–1185. doi:10.3201/eid1607.090209
   PubMed Web of Science ®Google Scholar
• Piao D, Wang H, Di D, et al. MLVA and LPS characteristics of Brucella canis isolated from humans and dogs in Zhejiang, China. Front Vet Sci. 2017;4:223. doi:10.3389/fvets.2017.00223
   PubMed Web of Science ®Google Scholar
• Mohamed Zahidi J, Ahmad N, Tay BY, et al. Genome sequences of Brucella melitensis, isolated from blood samples of brucellosis patients in Malaysia. Genome Announc. 2017;5. Available from: https://www.ncbi.nlm.nih.gov/pubmed/28774972.
   PubMedGoogle Scholar
• Schoenemann J, Lutticken R, Scheibner E. [Brucella canis infection in man]. Dtsch Med Wochenschr. 1986;111:20–22. doi:10.1055/s-2008-1068393
   PubMed Web of Science ®Google Scholar
• King J. Heartbroken woman forced to put five dogs down after contracting rare disease. METRO UK [Internet] 2022 Aug 14. Available from: https://metro.co.uk/2022/08/14/woman-forced-to-put-five-dogs-down-after-contracting-rare-disease-17180788/.
   Google Scholar
• Blankenship RM, Sanford JP. Brucella canis. A cause of undulant fever. Am J Med. 1975;59:424–426. doi:10.1016/0002-9343(75)90402-7
   PubMed Web of Science ®Google Scholar
• Tosi MF, Nelson TJ. Brucella canis infection in a 17-month-old child successfully treated with moxalactam. J Pediatr. 1982;101:725–727. doi:10.1016/S0022-3476(82)80301-6
   PubMed Web of Science ®Google Scholar
• McKee MA, Ballard JL. Mycotic aneurysms of the tibioperoneal arteries. Ann Vasc Surg. 1999;13:188–190. doi:10.1007/s100169900240
   PubMed Web of Science ®Google Scholar
• Ying W, Nguyen MQ, Jahre JA. Brucella canis endocarditis: case report. Clin Infect Dis. 1999;29:1593–1594. doi:10.1086/313545
   PubMed Web of Science ®Google Scholar
• Laine C, Johnson V, Scott H, et al. Human brucellosis: first calculated estimate of global annual incidence. Brucell 2022 Int Res conf.; Terramo, Italy: IZSAM; 2022.
   Google Scholar
• Eckstein C, Mol JPS, Costa FB, et al. Brucella ovis mutant in ABC transporter protects against Brucella canis infection in mice and it is safe for dogs. PLoS One. 2020;15:e0231893. doi:10.1371/journal.pone.0231893
   PubMed Web of Science ®Google Scholar
• Kim WK, Moon JY, Cho JS, et al. Brucella abortus lysed cells using GI24 induce robust immune response and provide effective protection in Beagles. Pathog Dis. 2018;76. Available from: https://www.ncbi.nlm.nih.gov/pubmed/29272378.
   PubMed Web of Science ®Google Scholar
• Hollett RB. Canine brucellosis: outbreaks and compliance. Theriogenology. 2006;66:575–587. doi:10.1016/j.theriogenology.2006.04.011
   PubMed Web of Science ®Google Scholar
• De Massis F, Sacchini F, Petrini A, et al. Canine brucellosis due to Brucella canis: description of the disease and control measures. Vet Ital. 2022;58:5–23.
   PubMed Web of Science ®Google Scholar
• Guarino C, Franklin-Guild R, Goodrich E, et al. Antibody response over time correlated with treatment outcome in 30 dogs naturally infected with Brucella canis (2017–2022). Am J Vet Res. 2023;1:1–7. doi:10.2460/ajvr.23.01.0014
   Google Scholar
• Wanke MM, Delpino MV, Baldi PC. Use of enrofloxacin in the treatment of canine brucellosis in a dog kennel (clinical trial). Theriogenology. 2006;66:1573–1578. doi:10.1016/j.theriogenology.2006.01.034
   PubMed Web of Science ®Google Scholar
• Liu Y, Sun J, Peng X, et al. Deletion of the LuxR-type regulator VjbR in Brucella canis affects expression of type IV secretion system and bacterial virulence, and the mutant strain confers protection against Brucella canis challenge in mice. Microb Pathog. 2020;139:103865. doi:10.1016/j.micpath.2019.103865
   PubMed Web of Science ®Google Scholar
• Stranahan LW, Chaki SP, Garcia-Gonzalez DG, et al. Evaluation of the efficacy of the Brucella canis RM6/66 DeltavjbR vaccine candidate for protection against B. canis infection in mice. mSphere. 2020;5. Available from: https://www.ncbi.nlm.nih.gov/pubmed/32434839.
   PubMed Web of Science ®Google Scholar