Cetacean Strandings in Costa Rica 2004–2020: A Review of Marine Brucellosis Findings
IAAAM 2021

Gabriela Hernández-Mora1; Rocío González-Barrientos1; José David Palacios-Alfaro2; Marcela Suárez-Esquivel3; Nazareth Ruiz Villalobos3; Elías Barquero-Calvo3; Caterina Guzmán-Verri3; Brian C.W. Kot6; Andrés Granados Zapata4; Karol Roca Monge4; Gianmarco Bettoni5; Ignacio Monge Mora5; Ariana Perez Jiménez7; Edgardo Moreno3

1Servicio Nacional de Salud Animal (SENASA), Ministerio de Agricultura y Ganadería, Heredia, Costa Rica; 2Fundación Keto, San José, Costa Rica; 3Programa de Investigación en Enfermedades Tropicales, Escuela de Medicina Veterinaria Universidad Nacional, Heredia, Costa Rica; 4Escuela de Medicina Veterinaria, Universidad Nacional, Heredia, Costa Rica; 5Escuela de Medicina Veterinaria, Universidad San Francisco de Asís, San José, Costa Rica; 6Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong, People’s Republic of China; 7Universidad Técnica Nacional, Atenas, Alajuela, Costa Rica

Abstract

A total of 179 cetaceans from 21 species have been reported stranded on the Costa Rican shorelines from January 2004 to December 2020. From these, 96.6% (n=173) were reported stranded on the Pacific coast and 3.3% (n=6) on the Caribbean coast. These animals belonged to five different families, including Balaenopteridae, Physiteridae, Kogiidae, Ziphiidae, and Delphinidae.1

Striped dolphin (Stenella coeruleoalba) is the most frequently stranded species, representing 43.5% (n=78) of the total cases. Complete necropsies were performed on 75.6% (n=59) of these dolphins, and Brucella ceti ST26 was isolated from cerebrospinal fluid (CSF) in 71.2% (n=42).2 Meningoencephalitis with increased cerebrospinal fluid volume and opacity with secondary hydrocephalus continues to be the most common presentation.3-5 Following the standard protocols for postmortem computed tomography neuroimaging, these animals present different levels of enlargement of the temporal horns of the lateral ventricles with accumulation of CSF.6 Brucella ceti ST26 was also isolated from CSF, brain tissue, and atlanto-occipital joint from an individual common dolphin (Delphinus delphis) and from lungworms (Halocerchus spp.) from four striped dolphins.4,7

During this time, two striped dolphins and one dwarf sperm whale (Kogia sima) were reported as pregnant females, and placentitis was described in both species. Brucella ceti ST26 was isolated from the placenta, uterine fluids, milk, and calf of one of the striped dolphins; meanwhile, a marine Brucella ST27 was isolated from the K. sima and its calf.8 Individuals from other species have been reported as seropositive animals in the country; however, Brucellae were not cultured from them.5,7 These species include: blue whale (Balaenoptera musculus), Cuvier’s beaked whale (Ziphius cavirostris), bottlenose dolphin (Tursiops truncatus), rough tooth dolphin (Steno bredanensis), pantropical spotted dolphin (Stenella attenuata), Risso’s dolphin (Grampus griseus) for the Pacific shorelines, and Fraser’s dolphin (Lagenodelphis hosei) from the Caribbean coast.1

The combination of serology before a complete necropsy and bacteriology on freshly collected samples (in animals as code 2 and 3), as well as the use of the non-commercial selective medium with fewer antibiotics (CITA and Farrell’s medium), have been critical for the success of isolation of the Brucellae in these animals.9,10 Molecular techniques as MVLA-16 and whole-genome sequencing have been key tools for clustering the isolates according to host-geographical location.2 The real impact of mortality, either by reproductive failure or complications during the life span in the cetacean population with marine Brucella in the eastern tropical Pacific, is currently unknown since this clinical presentation has been reported in other oceanographic areas of the Pacific Ocean; however, laboratory capacity-building is needed to better understand this potentially zoonotic disease.

Acknowledgments

The authors thank the people who helped during stranding of cetaceans in coastal areas of Costa Rica: Coastguard, fire department, emergency service (911), SINAC, Parque Marino del Pacífico, personnel from PIET, Veterinary School, UNA and the National Service of Animal Health (SENASA), Costa Rica.

Literature Cited

1.  Hernández-Mora G, Bonilla-Montoya R, Barrantes-Granados O, Esquivel-Suárez A, Montero-Caballero D, González-Barrientos R, Fallas-Monge Z, Palacios-Alfaro JD, Baldi M, Campos E, Chanto G, Barquero-Calvo E, Chacón-Díaz C, Chaves-Olarte E, Guzmán Verri C, Romero-Zúñiga JJ, Moreno E. 2017. Brucellosis in mammals of Costa Rica: an epidemiological survey. PLoS One. 12(8):e0182644.

2.  Suárez-Esquivel M, Baker KS, Ruiz-Villalobos N, Hernández-Mora G, Barquero-Calvo E, González-Barrientos R, Castillo-Zeledón A, Jiménez-Rojas C, Chacón-Díaz C, Cloeckaert A, Chaves-Olarte E, Thomson NR, Moreno E, Guzmán-Verri C. 2017. Brucella genetic variability in wildlife marine mammals populations relates to host preference and ocean distribution. Genome Biol Evol. 9(7):1901–1912.

3.  Hernández-Mora G, González-Barrientos R, Morales JA, Chaves-Olarte E, Guzmán-Verri C, Barquero-Calvo E, De-Miguel MJ, Marín CM, Blasco JM, Moreno E. 2008. Neurobrucellosis in stranded dolphins, Costa Rica. Emerg Infect Dis. 14(9):1430–1433.

4.  González-Barrientos R, Morales JA, 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(4):347–352.

5.  Guzmán-Verri C, González-Barrientos R, Hernández-Mora G, Morales JA, Baquero-Calvo E, Chaves-Olarte E, Moreno E. 2012. Brucella ceti and brucellosis in cetaceans. Front Cell Infect Microbiol. 2:3.

6.  Kot BCW, Tsui HCL, Chung TYT, Lau APY. 2020. Postmortem neuroimaging of cetacean brains using computed tomography and magnetic resonance imaging. Front Mar Sci. 7:544037.

7.  Hernández-Mora G, Palacios-Alfaro JD, González-Barrientos R. 2013. Wildlife reservoirs of brucellosis: Brucella in aquatic environments. Rev Sci Tech. 32(1):89–103.

8.  Suárez-Esquivel M, Ruiz-Villalobos N, Hernández-Mora G, González-Barrientos R, Palacios-Alfaro JD, Barquero-Calvo E, Chaves-Olarte E, Thompon N, Moreno E, Guzmán-Verri C. 2019. Brucella sequence Type 27 isolated from dwarf sperm whale (Kogia sima) stranded in the Costa Rican Pacific coast. Access Microbiol. 1(1A).

9.  Hernández-Mora G, Manire CA, González-Barrientos R, Barquero-Calvo E, Guzmán-Verri C, Staggs L, Thompson R, Chaves-Olarte E, Moreno E. 2009. Serological diagnosis of Brucella infections in odontocetes. Clin Vaccine Immunol. 16(6):906–915.

10.  De Miguel MJ, Marín CM, Muñoz PM, Dieste L, Grilló MJ, Blasco JM. 2011. Development of a selective culture medium for primary isolation of the main Brucella species. J Clin Microbiol. 49(4):1458–1463.

 

Speaker Information
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Gabriela Hernandez-Mora
Servicio Nacional de Salud Animal (SENASA)
Ministerio de Agricultura y Ganadería
Heredia, Costa Rica


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