Transmission of Toxoplasma: Clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment

Conrad, Patricia A.; Miller, Melissa A.; Kreuder, Christine; James, E.; Mazet, Jonna A. K.; Dabritz, Haydee A.; Jessup, David A.; Gulland, Frances M. D.; Grigg, Michael E.

doi:10.1016/j.ijpara.2005.07.002

Cited by 288 publications

(235 citation statements)

References 107 publications

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“…Historically, two new genetic types, Type X (Miller et al, 2004) and Type A (Sundar et al, 2008), have been described from sea otters. In one report, Type X was associated with increased mortality in sea otters (Conrad et al, 2005). Types A and X have identical RFLP profiles and belong to Type 12 in this study.…”

Section: Marine Mammalssupporting

confidence: 71%

“…The Southern sea otter is listed as a threatened species under the Endangered Species Act in the USA. Toxoplasma gondii can cause fatal illness in sea otters and other marine mammals (Kreuder et al, 2003;Conrad et al, 2005;Honnold et al, 2005;Thomas et al, 2007;Dubey, 2010;Gibson et al, 2011). Sea otters are presumed to acquire T. gondii infection from the contamination of marine waters with oocysts washed from land (Miller et al, 2008b).…”

Section: Marine Mammalsmentioning

confidence: 99%

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Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type

Dubey

Velmurugan

Rajendran

et al. 2011

International Journal for Parasitology

162

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a b s t r a c tLittle is known of the genetic diversity of Toxoplasma gondii circulating in wildlife. In the present study wild animals, from the USA were examined for T. gondii infection. Tissues of naturally exposed animals were bioassayed in mice for isolation of viable parasites. Viable T. gondii was isolated from 31 animals including, to our knowledge for the first time, from a bald eagle (Haliaeetus leucocephalus), five gray wolves (Canis lupus), a woodrat (Neotoma micropus), and five Arctic foxes (Alopex lagopus). Additionally, 66 T. gondii isolates obtained previously, but not genetically characterised, were revived in mice. Toxoplasma gondii DNA isolated from these 97 samples (31 + 66) was characterised using 11 PCR-restriction fragment length polymorphism (RFLP) markers (SAG1, 5 0 -and 3 0 -SAG2, alt.SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1 and Apico). A total of 95 isolates were successfully genotyped. In addition to clonal Types II, and III, 12 different genotypes were found. These genotype data were combined with 74 T. gondii isolates previously characterised from wildlife from North America and a composite data set of 169 isolates comprised 22 genotypes, including clonal Types II, III and 20 atypical genotypes. Phylogenetic network analysis showed limited diversity with dominance of a recently designated fourth clonal type (Type 12) in North America, followed by the Type II and III lineages. These three major lineages together accounted for 85% of strains in North America. The Type 12 lineage includes previously identified Type A and X strains from sea otters. This study revealed that the Type 12 lineage accounts for 46.7% (79/169) of isolates and is dominant in wildlife of North America. No clonal Type I strain was identified among these wildlife isolates. These results suggest that T. gondii strains in wildlife from North America have limited diversity, with the occurrence of only a few major clonal types. Ó

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Section: Marine Mammalssupporting

confidence: 71%

Section: Marine Mammalsmentioning

confidence: 99%

Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type

Dubey

Velmurugan

Rajendran

et al. 2011

International Journal for Parasitology

162

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“…Although we found no statistical associations between sea otter deaths due to T. gondii infection and runoff events, other studies support the hypothesis of a land to sea flow of this zoonotic parasite (Miller et al, 2002a;Conrad et al, 2005). Unlike S. neurona, T. gondii might have a more chronic onset of disease in sea otters, similar to the pathophysiology of toxoplasmosis in humans (Hill and Dubey, 2002).…”

Section: Discussioncontrasting

confidence: 39%

Temporal Association Between Land-Based Runoff Events and California Sea Otter (Enhydra Lutris Nereis) Protozoal Mortalities

Shapiro¹,

Miller²,

Mazet³

2012

Journal of Wildlife Diseases

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ABSTRACT:Toxoplasma gondii and Sarcocystis neurona have caused significant morbidity and mortality in threatened Southern sea otters (Enhydra lutris nereis) along the central California coast. Because only terrestrial animals are known to serve as definitive hosts for T. gondii and S. neurona, infections in otters suggest a land to sea flow of these protozoan pathogens. To better characterize the role of overland runoff in delivery of terrestrially derived fecal pathogens to the near shore, we assessed the temporal association between indicators of runoff and the timing of sea otter deaths due to T. gondii and S. neurona. Sea otter stranding records 1998-2004, from Monterey and Estero bays were reviewed and cases identified for which T. gondii or S. neurona were determined to be a primary or contributing cause of death. Precipitation and stream flow data from both study sites were used as indicators of land-based runoff. Logistic regression was applied to determine if a temporal association could be detected between protozoal mortalities and runoff indicators that occur in the 2 mo preceding mortality events. A significant association was found between S. neurona otter deaths at Estero Bay and increased stream flow that occurred 30-60 days prior to mortality events. At this site, the cause of otter mortality following increased river flows was 12 times more likely to be S. neurona infection compared with nonprotozoal causes of death. There were no significant associations between the timing of T. gondii otter deaths and indicators of overland runoff. Our results indicate that the association between overland runoff and otter mortalities is affected by geography as well as parasite type, and highlight the complex mechanisms that influence transmission of terrestrially derived pathogens to marine wildlife. Policy and management practices that aim to mitigate discharges of contaminated overland runoff can aid conservation efforts by reducing pathogen pollution of coastal waters, which impacts the health of threatened marine wildlife and humans.

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“…As these prey species are also consumed by humans, T. gondii infection in marine mammals could be an indirect indicator of the risk these species pose for causing T. gondii infection in humans. Otters are hypothesized to be an interesting link in the transmission of T. gondii from land to marine environments and were therefore included in this study (Conrad et al, 2005). A higher percentage of samples testing positive on all three tests was found in otters (28%) compared to marine mammals (2%), supporting this hypothesis.…”

Section: Animal Nomentioning

confidence: 55%

“…Immunosuppressive factors, such as polychlorbiphenyls and Morbillivirus infection could make marine mammals more susceptible to disease induced by T. gondii infection (Mazzariol et al, 2012). Besides being a pathogenic agent capable of affecting marine mammal health, T. gondii acts as an indicator of marine pollution , with marine mammals being excellent sentinel species (Conrad et al, 2005;de Moura et al, 2014;Jessup et al, 2004;Moore, 2008;Stewart et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

Toxoplasma gondii in stranded marine mammals from the North Sea and Eastern Atlantic Ocean: Findings and diagnostic difficulties

Velde

Devleesschauwer

Leopold³

et al. 2016

Veterinary Parasitology

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a b s t r a c tThe occurrence of the zoonotic protozoan parasite Toxoplasma gondii in marine mammals remains a poorly understood phenomenon. In this study, samples from 589 marine mammal species and 34 European otters (Lutra lutra), stranded on the coasts of Scotland, Belgium, France, The Netherlands and Germany, were tested for the presence of T. gondii. Brain samples were analysed by polymerase chain reaction (PCR) for detection of parasite DNA. Blood and muscle fluid samples were tested for specific antibodies using a modified agglutination test (MAT), a commercial multi-species enzyme-linked immunosorbent assay (ELISA) and an immunofluorescence assay (IFA). Out of 193 animals tested by PCR, only two harbour porpoise (Phocoena phocoena) cerebrum samples, obtained from animals stranded on the Dutch coast, tested positive. The serological results showed a wide variation depending on the test used. Using a cut-off value of 1/40 dilution in MAT, 141 out of 292 animals (41%) were positive. Using IFA, 30 out of 244 tested samples (12%) were positive at a 1/50 dilution. The commercial ELISA yielded 7% positives with a cut-off of the sample-to-positive (S/P) ratio ≥ 50; and 12% when the cut-off was set at S/P ratio ≥ 20. The high number of positives in MAT may be an overestimation due to the high degree of haemolysis of the samples and/or the presence of lipids. The ELISA results could be an underestimation due to the use of a multispecies conjugate. Our results confirm the presence of T. gondii in marine mammals in The Netherlands and show exposure to the parasite in both the North Sea and the Eastern Atlantic Ocean. We also highlight the limitations of the tests used to diagnose T. gondii in stranded marine mammals.

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Transmission of Toxoplasma: Clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment

Cited by 288 publications

References 107 publications

Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type

Genetic characterisation of Toxoplasma gondii in wildlife from North America revealed widespread and high prevalence of the fourth clonal type

Temporal Association Between Land-Based Runoff Events and California Sea Otter (Enhydra Lutris Nereis) Protozoal Mortalities

Toxoplasma gondii in stranded marine mammals from the North Sea and Eastern Atlantic Ocean: Findings and diagnostic difficulties

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