Toxoplasma Gondii Cetacio Bra
Toxoplasma Gondii Cetacio Bra
Toxoplasma Gondii Cetacio Bra
Abstract
Toxoplasmosis is a parasitic disease caused by the protozoan Toxoplasma gondii. In cetaceans, T. gondii infection is a
significant cause of morbidity and mortality. Despite the worldwide range and broad cetacean host record of T. gondii
infection, there is limited information on toxoplasmosis in cetaceans from the Southern hemisphere. We investigated
the occurrence of T. gondii by histopathology and immunohistochemistry in tissue samples of 185 animals comprising
20 different cetacean species from Brazil. Three out of 185 (1.6%) animals presented T. gondii-associated lesions: a captive
killer whale Orcinus orca, a free-ranging common bottlenose dolphin Tursiops truncatus and a free-ranging Guiana dolphin
Sotalia guianensis. The main lesions observed in these animals were necrotizing hepatitis, adrenalitis and lymphadenitis
associated with protozoal cysts or extracellular tachyzoites presenting immunolabeling with anti-T. gondii antibodies.
This study widens the spectrum of species and the geographic range of this agent in Brazil, and provides the first reports
of T. gondii infection in a captive killer whale and in a free-ranging common bottlenose dolphin in South America.
Keywords: Toxoplasmosis, mortality, stranding, South America, protozoan infection, marine mammal.
Resumo
Toxoplasmose é uma doença parasitária causada pelo protozoário Toxoplasma gondii. A infecção por T. gondii é uma
causa significativa de morbidade e mortalidade, nos cetáceos. Apesar da abrangência mundial e amplo registro de espécies
de cetáceos infectadas por T. gondii, informações sobre toxoplasmose em cetáceos do hemisfério sul são limitadas. Neste
estudo pesquisou-se por meio de histopatologia e imuno-histoquímica a ocorrência de T. gondii em amostras de tecido
de 185 animais, compreendendo 20 diferentes espécies de cetáceos que ocorrem no Brasil. Três dos 185 (1,6%) animais
apresentaram lesões associadas a T. gondii: uma orca Orcinus orca mantida em cativeiro, um golfinho-nariz-de-garrafa
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396 396/402 Costa-Silva, S. et al. Braz. J. Vet. Parasitol.
Tursiops truncatus e um boto-cinza Sotalia guianensis de vida livre. As principais lesões observadas nesses animais foram
hepatite, adrenalite e linfadenite necrotizantes associadas a cistos protozoários ou taquizoítos extracelulares, marcados
com anticorpos anti-T. gondii. O presente estudo amplia o espectro de espécies susceptíveis a esse agente e o seu alcance
geográfico no Brasil, fornecendo o primeiro relato da infecção por T. gondii em uma orca mantida em cativeiro e em
um golfinho-nariz-de-garrafa de vida livre na América do Sul.
Palavras-chave: Toxoplasmose, mortalidade, encalhe, América do Sul, infecção por protozoários, mamífero
marinho.
death, on March 7th, 1988. No clinical data were available. Samples and lymphoid necrosis, interstitial pneumonia, adrenal necrosis,
of lungs, liver, spleen, kidneys, skeletal muscle, glandular stomach, and non-suppurative encephalitis and meningoencephalitis
large intestine, thyroid glands, and lymph nodes were collected with bradyzoites and free tachyzoites (INSKEEP et al., 1990;
upon necropsy. The only reported macroscopic finding was a MIGAKI et al., 1990; MIKAELIAN et al., 2000; RESENDES et al.,
renal cyst. Microscopically, the main lesions included moderate 2002; VAN BRESSEM et al., 2009; GONZALES-VIERA et al.,
to marked, multifocal, acute fibrinosuppurative and hemorrhagic 2013; ROE et al., 2013). In T. gondii‑positive cases, all tested
bronchopneumonia with protozoan cysts, moderate randomly tissues were negative for morbillivirus, suggesting that T. gondii
multifocal to coalescent necrotizing hepatitis with protozoan cysts possibly acted as a primary agent, as previously observed
(compatible with T. gondii), marked necrosuppurative lymphadenitis, (DI GUARDO et al., 2010; GONZALES-VIERA et al., 2013;
acute multifocal interstitial nephritis with mild‑moderate mixed ROE et al., 2013). The scarce number of brain samples available
infiltrate, mild to moderate, multifocal, chronic membranous for this study (n = 4) probably prevented the identification of
glomerulonephritis, and acute fibrinoid vasculitis. T. gondii-associated lesions in nervous tissue, which is commonly
Case No 2 (MM#178) was a juvenile male common bottlenose involved in cetacean toxoplasmosis cases (DI GUARDO et al.,
dolphin of 2.43 m total body length, that stranded alive and died 2010; SIERRA et al., 2014).
shortly after stranding, on October 29th, 2001, in Lagos Region, In this study, we evaluated cetacean samples from geographic
Rio de Janeiro state, Brazil (22°56’S, 42°19’W). Samples of lungs, areas that correspond to a large portion of the Brazilian coastline,
liver, kidneys, and large intestine were collected upon necropsy. most of them coastal species, mainly franciscanas (Pontoporia
No gross findings were reported. The main microscopic findings blainvillei) (55.0%) and Guiana dolphins (14.5%). Coastal
observed were moderate to severe, multifocal random to coalescing cetaceans, considered suitable sentinels of the marine environmental
necrotizing hepatitis with protozoan cysts compatible with T. gondii ecosystem and important indicators of marine pollution, are
and moderate to marked, multifocal, acute fibrinosuppurative usually more exposed to anthropogenic activities (WELLS et al.,
bronchopneumonia. 2004; BOSSART, 2011; MOURA et al., 2014). From these,
Case No 3 (MM#67) was a 1.86 m-long adult, female Guiana we found histological and immunohistochemical evidences of
dolphin that stranded dead on March 3th, 1998, in Paranaguá Bay, toxoplasmosis in one Guiana dolphin. This is the third report of
Paraná state, Brazil (25°31’S, 48°30’W). No necropsy records toxoplasmosis in this species (BANDOLI & OLIVEIRA, 1977;
were available. Samples of eye and adrenal glands were evaluated. GONZALES‑VIERA et al., 2013). This animal presented severe
Microscopically, the main finding was marked, multifocal, adrenalitis, similar to what was reported by Gonzales-Viera et al.
acute necrotizing adrenalitis with numerous protozoal cysts and (2013) in another Guiana dolphin from the same area (Paranaguá
extracellular tachyzoites compatible with T. gondii, and further Bay) that died in the same year (1998). Given the marked pattern
highlighted with PAS and Giemsa stains. of site fidelity presented by Guiana dolphins (MOURA et al.,
2014), this result suggests a common source of exposure to
T. gondii and a possible negative impact of toxoplasmosis on this
Discussion population. Although the low occurrence of T. gondii infection
found in the present study does not allow us to infer further
Despite the widespread geographical range of T. gondii infection, on this protozoan’s geographic distribution, the location of the
in Brazil, the current knowledge regarding cetacean toxoplasmosis Guiana dolphin case and previous reports suggest that infection
is limited to few species and studies (BANDOLI & OLIVEIRA, may occur at higher rates in coastal areas of Brazil. Coastal areas
1977; SANTOS et al., 2011; GONZALES-VIERA et al., 2013). usually receive freshwater run-offs and terrestrial biologic pollutants,
Based on microscopical and immunohistochemical examinations, contributing to the presence of T. gondii (SHAPIRO et al., 2015).
we provide the first description of T. gondii in a common These results also suggest areas in which future research efforts
bottlenose dolphin of South America, and in a captive killer whale. should be concentrated.
Furthermore, the identification of toxoplasmosis in a Guiana Concerning killer whales, positive serology for T. gondii
dolphin corroborates with previous observations regarding this was reported in a killer whale calf that stranded alive in Japan,
species and geographic area, the Paranaguá Bay. On the other hand, in 1988 (MURATA et al., 2004), and T. gondii infection was
in spite of the high prevalence of T. gondii antibodies reported in identified by molecular techniques in a stranded killer whale from
free-ranging Amazon river dolphins (SANTOS et al., 2011), our the Northeastern Pacific, in California (GIBSON et al., 2011).
sampled captive Amazon river dolphin was T. gondii- negative. However, these reports lacked detailed pathological examinations.
We detected protozoal cysts and free tachyzoites of T. gondii In the present study, we provide the first histopathological and
by IHC and observed histological changes within multiorgan immunohistochemical evidences of toxoplasmosis in this species.
necroinflammatory foci, e.g., necrotizing hepatitis, necrosuppurative Based on the severity and extent of characteristic multiorganic
lymphadenitis (killer whale), necrotizing hepatitis (common bottlenose necroinflammatory foci, we believe that T. gondii played a major
dolphin), and necrotizing adrenalitis (Guiana dolphin). These lesions role in the death of the evaluated killer whale. In this case, potential
are in agreement with previous reports of T. gondii infection in environmental sources of T. gondii infectious forms may include
odontocetes (CRUICKSHANK et al., 1990; RESENDES et al., water and/or food contamination in one or more of the following
2002; DI GUARDO & MAZZARIOL, 2013) and mysticetes scenarios: (1) the facility’s water system (e.g., used to clean fish
(MAZZARIOL et al., 2012). The main lesions observed in cetacean and the enclosure, and fill the tank), especially considering that
cases of toxoplasmosis are necrotizing hepatitis, lymphadenitis sporulated oocysts of T. gondii are viable in saltwater for at least
400 400/402 Costa-Silva, S. et al. Braz. J. Vet. Parasitol.
Aquáticos do Rio Grande do Sul (GEMARS) Laboratório de Dubey JP, Fair PA, Sundar N, Velmurugan G, Kwok OC, McFee
Mamíferos Aquáticos e Bioindicadores ‘Profa. Izabel Gurgel’ - WE, et al. Isolation of Toxoplasma gondii from bottlenose dolphins
Faculdade de Oceanografia - Universidade do Estado do Rio de (Tursiops truncatus). J Parasitol 2008; 94(4): 821-823. http://dx.doi.
org/10.1645/GE-1444.1. PMid:18576793.
Janeiro (MAQUA), Museu Oceanográfico da FURG, Playcenter,
Projeto Biopesca - Universidade Estadual Paulista-UNESP, and Dubey JP, Lipscomb TP, Mense M. Toxoplasmosis in an elephant seal
Projeto Baleia Franca/Instituto Australis for providing the samples (Mirounga angustirostris). J Parasitol 2004; 90(2): 410-411. http://dx.doi.
and necropsy records. This study was co-financed by CAPES and org/10.1645/GE-155R. PMid:15165069.
FAPESP. The financial sources had no influence over the project’s Dubey JP, Mergl J, Gehring E, Sundar N, Velmurugan GV, Kwok
development. All procedures were performed in accordance with OC, et al. Toxoplasmosis in captive dolphins (Tursiops truncatus) and
the Ethical Committee of the School of Veterinary Medicine walrus (Odobenus rosmarus). J Parasitol 2009; 95(1): 82-85. http://dx.doi.
and Animal Sciences, University of São Paulo (process number: org/10.1645/GE-1764.1. PMid:19245284.
2551070144). JDD is the recipient of a post-doctoral fellowship by Dubey JP. The history of Toxoplasma gondii - The first 100 years. J Eukaryot
FAPESP (grant #2017/02223-8), and CNPq provided scholarship Microbiol 2008; 55(6): 467-475. http://dx.doi.org/10.1111/j.1550-
to J.L.C.-D (grant #305349/2015-5). 7408.2008.00345.x. PMid:19120791.
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