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A comprehensive meta-analysis of Brucella infections in aquatic mammals
VetIt.2427.14954.2

Keywords

Aquatic mammals
Brucella ceti
Brucella pinnipedialis
Brucellosis
Cetaceans
Marine mammals

How to Cite

Dadar, M., Shahali, Y., Fakhri, Y., & Godfroid, J. (2022). A comprehensive meta-analysis of Brucella infections in aquatic mammals . Veterinaria Italiana, 58(2). https://doi.org/10.12834/VetIt.2427.14954.2

Abstract

The presence of Brucella infections was documented in a large number of aquatic mammals, affecting wild animals living in oceans, seas, lakes and rivers within both northern and southern hemispheres. Through meta‑regression analysis, this study provides a comprehensive view of the prevalence of Brucella spp. in aquatic mammals, identifying risk subgroups as well as most common sampling and testing methods. Brucella ceti and Brucella pinnipedialis represent the main marine Brucella spp., with documented enzootic potential, for which information on standardized diagnostic methods for the implementation of efficient screening and monitoring programs is needed. A total of 71 articles investigating the occurrence of brucellosis in aquatic mammals since 1987, have met the inclusion criteria and have been included in this study. The prevalence of brucellosis in males (30.42%) was significantly higher than females (18.59%). The family of Delphinidae was the most studied among aquatic mammals with a total prevalence of 39.66%. Our meta‑regression analysis showed a strong and significant association between the prevalence of Brucella spp. in mammals and water temperature (C = 0.02, p value = 0.003), while no significant correlation was found with water salinity (C = ‑ 0.09; p value = 0.10). At least 130 species of aquatic mammals have been identified as potential hosts for Brucella spp. There is no systematic veterinary inspection and global or local requirements for the monitoring of brucellosis in aquatic mammals. The association of brucellosis prevalence and water temperature warrants further studies to assess the potential direct and indirect impacts of climate change on brucellosis in aquatic mammals. This study would help to determine the basis of adaptive management strategies in order to control enzootic brucellosis in wild aquatic mammals.

https://doi.org/10.12834/VetIt.2427.14954.2
VetIt.2427.14954.2

References

Alava J.J., Jiménez P.J., Fair P.A. & and Barrett-Lennard L. 2019. First Record of a Live-Stranded Killer Whale (Orcinus orca) in Coastal Ecuador and Insights on Killer Whale Occurrence in Ecuadorian Waters. Aquatic Mammals, 45, 106-115.

Alba P., Terracciano G., Franco A., Lorenzetti S., Cocumelli C., Fichi G., Eleni C., Zygmunt M.S., Cloeckaert A., & Battisti A. 2013. The presence of Brucella ceti ST26 in a striped dolphin (Stenella coeruleoalba) with meningoencephalitis from the Mediterranean Sea. Vet Microbiol , 164, 158-163.

Alekseev A.Y., Rozanova E., Ustinova E., Tumanov Y.I., Kuvshinova I. & Shestopalov A. 2007. The prevalence of antibodies to morbilliviruses, Brucella, and Toxoplasma in the Black Sea bottlenose dolphin Tursiops truncatus ponticus maintained in captivity. Russ J Mar Biol , 33, 425-428.

Alekseev A.Y., Reguzova A.Y., Rozanova E., Abramov A., Tumanov Y.V., Kuvshinova I. & Shestopalov A. 2009. Detection of specific antibodies to morbilliviruses, Brucella and Toxoplasma in the Black Sea dolphin Tursiops truncatus ponticus and the beluga whale Delphinapterus leucas from the Sea of Okhotsk in 2002–2007. Russ J Mar Biol, 35, 494-497.

Ávalos-Téllez R., Ramírez-Pfeiffer C., Hernández-Castro R., Díaz-Aparicio E., Sánchez-Domínguez C., Zavala-Norzagaray A., Arellano-Reynoso B., Suárez-Güemes F., Aguirre A.A. & Aurioles-Gamboa D. 2014. Infection of California sea lions (Zalophus californianus) with terrestrial Brucella spp. Vet J, 202, 198-200.

Bourg G., O’Callaghan D. & Boschiroli M.L. 2007. The genomic structure of Brucella strains isolated from marine mammals gives clues to evolutionary history within the genus. Vet Microbiol , 125, 375-380.

Bricker B.J., Ewalt D.R., MacMillan A.P., Foster G. & Brew S. 2000. Molecular characterization of Brucellastrains isolated from marine mammals. J Clin Microbiol , 38, 1258-1262.

Bricker B.J., Ewalt D.R. & Halling S.M. 2003. Brucella'HOOF-Prints': strain typing by multi-locus analysis of variable number tandem repeats (VNTRs). BMC Microbiol, 3, 15.

Buckle K., Roe W.D., Howe L., Michael S., Duignan P.J., Burrows E., Ha H.J., Humphrey S. & McDonald W.L. 2017. Brucellosis in endangered Hector’s Dolphins (Cephalorhynchus hectori). Vet Pathol, 54, 838-845.

Cloeckaert A., Verger J.-M., Grayon M., Paquet J.-Y., Garin-Bastuji B., Foster G. Godfroid J. 2001. Classification of Brucella spp. isolated from marine mammals by DNA polymorphism at the omp2 locus. Microbes and Infection, 3, 729-738.

Cloeckaert A., Vergnaud G. & Zygmunt M.S. 2020. Omp2b Porin Alteration in the Course of Evolution of Brucella spp. Frontiers Microbiol, 11, 284.

Cvetnić Ž., Duvnjak S., Đuras M., Gomerčić T., Reil I., Zdelar-Tuk M. & Špičić S. 2016. Evidence of Brucella strain ST27 in bottlenose dolphin (Tursiops truncatus) in Europe. Vet Microbiol, 196, 93-97.

Dadar M., Alamian S., Behrozikhah A.M., Yazdani F., Kalantari A., Etemadi A. & Whatmore A.M. 2019a. Molecular identification of Brucella species and biovars associated with animal and human infection in Iran. Proc. Veterinary Research Forum. Faculty of Veterinary Medicine, Urmia University, 315-320.

Dadar M., Shahali Y. & Wareth G. 2019b. Molecular Diagnosis of Acute and Chronic Brucellosis in Humans. In Microbial Technology for the Welfare of Society, Springer, 223-245.

Dadar M., Shahali Y. & Whatmore A.M. 2019c. Human brucellosis caused by raw dairy products: A review on the occurrence, major risk factors and prevention. Int J Food Microbiol, 292, 39-47.

Dadar M., Fakhri Y., Shahali Y. & Khaneghah A.M. 2020a. Contamination of milk and dairy products by Brucella species: A global systematic review and meta-analysis. Food Res Int, 128, 108775.

Dadar M., Shahali Y. & Fakhri Y. 2020b. A primary investigation of the relation between the incidence of brucellosis and climatic factors in Iran. Microb Pathog, 139, 103858.

Davison N.J., Brownlow A., McGovern B., Dagleish M.P., Perrett L.L., Dale E-J., Koylass M. & Foster G. 2015. First report of Brucella ceti-associated meningoencephalitis in a long-finned pilot whale Globicephala melas. Dis Aquat Organ, 116, 237-241.

Dawson C., Perrett L., Stubberfield E., Stack .J, Farrelly S., Cooley W., Davison N. & Quinney S. 2008a. Isolation and characterization of Brucella from the lungworms of a harbor porpoise (Phocoena phocoena). J Wildl Dis, 44, 237-246.

Dawson C.E., Stubberfield E.J., Perrett L.L., King A.C., Whatmore A.M., Bashiruddin J.B., Stack J.A. & MacMillan A.P. 2008b. Phenotypic and molecular characterisation of Brucella isolates from marine mammals. BMC Microbiol, 8, 224.

Duvnjak S., Špičić S., Kušar D., Papić B., Reil I., Zdelar-Tuk M., Pavlinec Ž., Đuras M., Gomerčić T. & Hendriksen R.S. 2017. Whole-genome sequence of the first sequence type 27 Brucella ceti strain isolated from European waters. Genome Announc, 5, e00988-00917.

Eisenberg T., Hamann H.-P., Kaim U., Schlez K., Seeger H., Schauerte N., Melzer F., Tomaso H., Scholz H.C. & Koylass M.S. 2012. Isolation of potentially novel Brucella spp. from frogs. Appl Environ Microbiol, 78, 3753-3755.

Eisenberg T., Riße K., Schauerte N., Geiger C., Blom J. & Scholz H.C. 2017. Isolation of a novel ‘atypical’Brucella strain from a bluespotted ribbontail ray (Taeniura lymma). Antonie Van Leeuwenhoek, 110, 221-234.

Esquible J., Burek-Huntington K., Atkinson S., Klink A., Bortz E., Goldstein T., Beckmen K., Pabilonia K. & Tiller R. 2019. Pathological findings and survey for pathogens associated with reproductive failure in perinatal Steller sea lions Eumetopias jubatus. Dis Aquat Organ, 137, 131-144.

Ewalt D.R., Payeur J.B., Martin B.M., Cummins D.R. & Miller W.G. 1994. Characteristics of a Brucella species from a bottlenose dolphin (Tursiops truncatus). J Vet Diagn Invest, 6, 448-452.

Fakhri Y., Rahmani J., Oliveira C.A.F., Franco L.T., Corassin C.H., Saba S., Rafique J. & Mousavi Khaneghah A. 2019. Aflatoxin M1 in human breast milk: A global systematic review, meta-analysis, and risk assessment study (Monte Carlo simulation). Trends Food Sci Tech, 88, 333-342.

Foster G., MacMillan A., Godfroid J., Howie F., Ross H., Cloeckaert A., Reid R., Brew S. & Patterson I. 2002. A review of Brucella sp. infection of sea mammals with particular emphasis on isolates from Scotland. Vet Microbiol, 90, 563-580.

Foster G., Osterman B.S., Godfroid J., Jacques I. & Cloeckaert A. 2007. Brucella ceti sp. nov. and Brucella pinnipedialis sp. nov. for Brucella strains with cetaceans and seals as their preferred hosts. Int J syst Evol Microbiol, 57, 2688-2693.

Foster G., Nymo I.H., Kovacs K.M., Beckmen K.B., Brownlow A.C., Baily J.L., Dagleish M.P., Muchowski J., Perrett L.L. & Tryland M. 2018. First isolation of Brucella pinnipedialis and detection of Brucella antibodies from bearded seals Erignathus barbatus. Dis Aquat Organ, 128, 13-20.

Godfroid J., Nielsen K. & Saegerman C. 2010. Diagnosis of brucellosis in livestock and wildlife. Croat Med J, 51, 296-305.

Godfroid J., Scholz H., Barbier T., Nicolas C., Wattiau P., Fretin D., Whatmore A., Cloeckaert A., Blasco J. & Moriyon I. 2011. Brucellosis at the animal/ecosystem/human interface at the beginning of the 21st century. Prev Vet Med, 102, 118-131.

Goertz C.E., Frasca Jr S., Bohach G.A., Cowan D.F., Buck J.D., French R.A., De Guise S., Maratea J., Hinckley L. & Ewalt D. 2011. Brucella sp. vertebral osteomyelitis with intercurrent fatal Staphylococcus aureus toxigenic enteritis in a bottlenose dolphin (Tursiops truncatus). J Vet Diagn Invest, 23, 845-851.

González-Barrientos R., Morales J.-A., Hernández-Mora G., Barquero-Calvo E., Guzmán-Verri C., Chaves-Olarte E. & Moreno E. 2010. Pathology of striped dolphins (Stenella coeruleoalba) infected with Brucella ceti. J Comp Pathol, 142, 347-352.

González L., Patterson I., Reid R., Foster G., Barberan M., Blasco J., Kennedy S., Howie F., Godfroid J. & MacMillan A. 2002. Chronic meningoencephalitis associated with Brucella sp. infection in live-stranded striped dolphins (Stenella coeruleoalba). J Comp Pathol , 126, 147-152.

Greiner M., Verloo D. & de Massis F. 2009. Meta-analytical equivalence studies on diagnostic tests for bovine brucellosis allowing assessment of a test against a group of comparative tests. Prev Vet Med, 92, 373-381.

Hernández-Mora G., Palacios-Alfaro J. & González-Barrientos R. 2013. Wildlife reservoirs of brucellosis: Brucella in aquatic environments. Rev Sci Tech, 32, 89-103.

Higgins J.P. & Green S. 2011. Cochrane handbook for systematic reviews of interventions. John Wiley & Sons.

Higgins J.P.T. & Thompson S.G. 2002. Quantifying heterogeneity in a meta‐analysis. Stat Med, 21, 1539-1558.

Hunt T.D., Ziccardi M.H., Gulland F.M., Yochem P.K., Hird D.W., Rowles T. & Mazet J.A. 2008. Health risks for marine mammal workers. Dis Aquat Organ, 81, 81-92.

Jahans K., Foster G. & Broughton E. 1997. The characterisation of Brucella strains isolated from marine mammals. Vet Microbiol, 57, 373-382.

Jefferson T.A., Webber M.A. & Pitman RL. 2011. Marine mammals of the world: a comprehensive guide to their identification. The Netherland, Elsevier.

Jepson P., Brew S., MacMillan A., Baker J., Barnett J., Kirkwood J., Kuiken T., Robinson I. & Simpson V. 1997. Antibodies to Brucella in marine mammals around the coast of England and Wales. Vet Rec, 141, 513-515.

Liberati A., Altman D.G., Tetzlaff J., Mulrow C., Gøtzsche P.C., Ioannidis J.P., Clarke M., Devereaux P.J., Kleijnen J. & Moher D. 2009. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med, 6, 15-25.

Lulu A., Araj G., Khateeb M., Mustafa M., Yusuf A. & Fenech F. 1988. Human brucellosis in Kuwait: a prospective study of 400 cases. QJM: An International Journal of Medicine, 66, 39-54.

Maquart M., Le Flèche P., Foster G., Tryland M., Ramisse F., Djønne B., Al Dahouk S., Jacques I., Neubauer H. & Walravens K. 2009a. MLVA-16 typing of 295 marine mammal Brucella isolates from different animal and geographic origins identifies 7 major groups within Brucella ceti and Brucella pinnipedialis. BMC Microbiol, 9, 145.

Maquart M., Zygmunt M.S. & Cloeckaert A. 2009b. Marine mammal Brucella isolates with different genomic characteristics display a differential response when infecting human macrophages in culture. Microbes Infect, 11, 361-366.

McDonald W., Jamaludin R., Mackereth G., Hansen M., Humphrey S., Short P., Taylor T., Swingler J., Dawson C. & Whatmore A. 2006. Characterization of a Brucella sp. strain as a marine-mammal type despite isolation from a patient with spinal osteomyelitis in New Zealand. J Clin Microbiol, 44, 4363-4370.

Meegan J., Field C., Sidor I., Romano T., Casinghino S., Smith C.R., Kashinsky L., Fair P.A., Bossart G. & Wells R. 2010. Development, validation, and utilization of a competitive enzyme-linked immunosorbent assay for the detection of antibodies against Brucella species in marine mammals. J Vet Diagn Invest, 22, 856-862.

Miller W.G., Adams L.G., Ficht T.A., Cheville N.F., Payeur J.P., Harley D.R., House C. & Ridgway S.H. 1999. Brucella-induced abortions and infection in bottlenose dolphins (Tursiops truncatus). J Zoo Wildl Med, 30(1),100-110.

Moreno E., Guzmán-Verri C., Gonzalez-Barrios R., Hernandez G., Morales J.A., Barquero-Calvo E. & Chaves-Olarte E. 2012. Brucella ceti and brucellosis in cetaceans. Frontiers Cellular Infect Microbiol, 2, 3.

Nymo I.H., Tryland M.& Godfroid J. 2011. A review of Brucella infection in marine mammals, with special emphasis on Brucella pinnipedialis in the hooded seal (Cystophora cristata). Vet Res, 42, 93.

Ohishi K., Zenitani R., Bando T., Goto Y., Uchida K., Maruyama T., Yamamoto S., Miyazaki N. & Fujise Y. 2003. Pathological and serological evidence of Brucella-infection in baleen whales (Mysticeti) in the western North Pacific. Comp Immunol Microbiol Infect Dis, 26, 125-136.

Ohishi K., Takishita K., Kawato M., Zenitani R., Bando T., Fujise Y., Goto Y., Yamamoto S. & Maruyama T. 2004. Molecular evidence of new variant Brucella in North Pacific common minke whales. Microbes Infect, 6, 1199-1204.

Ohishi K., Fujise Y. & Maruyama T. 2008. 67 Brucella spp. in the western North Pacific and Antarctic cetaceans: a review. J Cetacean Res Manage, 10, 67-72.

Ragan V., Vroegindewey G. & Babcock S. 2013. International standards for brucellosis prevention and management. Rev Sci Tech, 32, 189-198.

Rhyan J.C., Gidlewski T., Ewalt D.R., Hennager S.G., Lambourne D.M. & Olsen SC. 2001. Seroconversion and abortion in cattle experimentally infected with Brucella sp. isolated from a Pacific harbor seal (Phoca vitulina richardsi). J Vet Diagn Invest, 13, 379-382.

Robards M.D. & Reeves R.R. 2011. The global extent and character of marine mammal consumption by humans: 1970–2009. Biol Conserv, 144, 2770-2786.

Ross H., Foster G., Reid R., Jahans K. & MacMillan A. 1994. Brucella species infection in sea-mammals. Vet Rec, 134(14), 359

Rostami A., Riahi S.M., Holland C.V., Taghipour A., Khalili-Fomeshi M., Fakhri Y., Omrani V.F., Hotez P.J. & Gasser R.B. 2019. Seroprevalence estimates for toxocariasis in people worldwide: A systematic review and meta-analysis. PLoS Negl Trop Dis, 13.

Rostami A., Riahi S.M., Gamble H.R., Fakhri Y., Shiadeh M.N., Danesh M., Behniafar H., Paktinat S., Foroutan M. & Mokdad A.H. 2020. Global prevalence of latent toxoplasmosis in pregnant women: a systematic review and meta-analysis. Clin Microbiol Infect, 26(6), 673-683.

Samaha H., Mohamed T.R., Khoudair R.M. & Ashour H.M. 2009. Serodiagnosis of brucellosis in cattle and humans in Egypt. Immunobiology, 214, 223-226.

Scholz H.C., Nöckler K., Göllner C., Bahn P., Vergnaud G., Tomaso H., Al Dahouk S., Kämpfer P., Cloeckaert A. & Maquart M. 2010. Brucella inopinata sp. nov., isolated from a breast implant infection. Int J Syst Evol Microbiol, 60, 801-808.

Sohn A.H., Probert W.S., Glaser C.A., Gupta N., Bollen A.W., Wong J.D., Grace E.M. & McDonald W.C. 2003. Human neurobrucellosis with intracerebral granuloma caused by a marine mammal Brucella spp. Emerg Infect Dis, 9, 485.

Wael F., Tayel A.A., Eltholth M.M. & Guitian J. 2010. Brucella infection in fresh water fish: Evidence for natural infection of Nile catfish, Clarias gariepinus, with Brucella melitensis. Vet Microbiol, 141, 321-325.

Whatmore A.M., Perrett L.L. & MacMillan A.P. 2007. Characterisation of the genetic diversity of Brucella by multilocus sequencing. BMC Microbiol, 7, 34.

Whatmore AM, Dawson C, Groussaud P, Koylass MS, King A, Shankster SJ, Sohn AH, Probert WS, and McDonald WL. 2008. Marine mammal Brucella genotype associated with zoonotic infection. Emerg Infect Dis 14, 517.

Whatmore A.M. 2009. Current understanding of the genetic diversity of Brucella, an expanding genus of zoonotic pathogens. Infect Genet Evol , 9, 1168-1184.

Whatmore A.M., Dawson C., Muchowski J., Perrett L.L., Stubberfield E., Koylass M., Foster G., Davison N.J., Quance C. & Sidor I.F. 2017. Characterisation of North American Brucella isolates from marine mammals. PLoS One, 12(9), e0184758.

Wu Q., McFee W.E., Goldstein T., Tiller R.V. & Schwacke L. 2014. Real-time PCR assays for detection of Brucella spp. and the identification of genotype ST27 in bottlenose dolphins (Tursiops truncatus). J Microbiol Methods, 100, 99-104.

Wu Q., McFee W.E., Fauquier D. & Schwacke L. 2017. Identification of Three Brucella ceti Genotypes in Bottlenose Dolphins (Tursiops truncatus) Using a Multiplex SYBR Green Real-Time PCR. Aquatic Mammals, 43, 3.

Copyright (c) 2022 Jacques Godfroid, Maryam Dadar, Youcef Shahali, Yadolah Fakhri