Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T09:25:32.714Z Has data issue: false hasContentIssue false

Dual congenital transmission of Toxoplasma gondii and Sarcocystis neurona in a late-term aborted pup from a chronically infected southern sea otter (Enhydra lutris nereis)

Published online by Cambridge University Press:  23 October 2015

KAREN SHAPIRO*
Affiliation:
Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California Davis, One Shields Ave, Davis California 95616, USA One Health Institute, University of California Davis, One Shields Ave, Davis California 95616, USA
MELISSA A. MILLER
Affiliation:
One Health Institute, University of California Davis, One Shields Ave, Davis California 95616, USA California Department of Fish and Wildlife, Marine Wildlife Veterinary Care and Research Center, 1451 Shaffer Road, Santa Cruz California 95060, USA
ANDREA E. PACKHAM
Affiliation:
Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California Davis, One Shields Ave, Davis California 95616, USA
BEATRIZ AGUILAR
Affiliation:
Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California Davis, One Shields Ave, Davis California 95616, USA
PATRICIA A. CONRAD
Affiliation:
Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California Davis, One Shields Ave, Davis California 95616, USA One Health Institute, University of California Davis, One Shields Ave, Davis California 95616, USA
ELIZABETH VANWORMER
Affiliation:
One Health Institute, University of California Davis, One Shields Ave, Davis California 95616, USA
MICHAEL J. MURRAY
Affiliation:
Monterey Bay Aquarium, 886 Cannery Row, Monterey California 93940, USA
*
*Corresponding author: Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California Davis, 4206 VM3A, One Shields Ave, Davis California 95616, USA. E-mail: kshapiro@ucdavis.edu

Summary

Toxoplasma gondii and Sarcocystis neurona are protozoan parasites with terrestrial definitive hosts, and both pathogens can cause fatal disease in a wide range of marine animals. Close monitoring of threatened southern sea otters (Enhydra lutris nereis) in California allowed for the diagnosis of dual transplacental transmission of T. gondii and S. neurona in a wild female otter that was chronically infected with both parasites. Congenital infection resulted in late-term abortion due to disseminated toxoplasmosis. Toxoplasma gondii and S. neurona DNA was amplified from placental tissue culture, as well as from fetal lung tissue. Molecular characterization of T. gondii revealed a Type X genotype in isolates derived from placenta and fetal brain, as well as in all tested fetal organs (brain, lung, spleen, liver and thymus). This report provides the first evidence for transplacental transmission of T. gondii in a chronically infected wild sea otter, and the first molecular and immunohistochemical confirmation of concurrent transplacental transmission of T. gondii and S. neurona in any species. Repeated fetal and/or neonatal losses in the sea otter dam also suggested that T. gondii has the potential to reduce fecundity in chronically infected marine mammals through parasite recrudescence and repeated fetal infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Andrade, G. M. Q., Vasconcelos-Santos, D. V., Carellos, E. V. M., Romanelli, R. M. C., Vitor, R. W. A., Carneiro, A. and Januario, J. N. (2010). Congenital toxoplasmosis from a chronically infected woman with reactivation of retinochoroiditis during pregnancy. Jornal De Pediatria 86, 8588.CrossRefGoogle ScholarPubMed
Asmundsson, I. M. and Rosenthal, B. M. (2006). Isolation and characterization of microsatellite markers from Sarcocystis neurona, a causative agent of equine protozoal myeloencephalitis. Molecular Ecology Notes 6, 810.CrossRefGoogle Scholar
Barbosa, L., Johnson, C. K., Lambourn, D. M., Gibson, A. K., Haman, K. H., Huggins, J., Sweeny, A. R., Sundar, N., Raverty, S. J. and Grigg, M. E. (2015). A novel Sarcocystis neurona genotype XIII is associated with severe encephalitis in an unexpectedly broad range of marine mammals from the northeastern Pacific ocean. International Journal for Parasitology 45, 595603.CrossRefGoogle Scholar
Bonametti, A. M., Passo, J. N., daSilva, E. M. K. and Macedo, Z. S. (1997). Probable transmission of acute toxoplasmosis through breast feeding. Journal of Tropical Pediatrics 43, 116116.CrossRefGoogle ScholarPubMed
Bresciani, K. D. S., Costa, A. J., Toniollo, G. H., Luvizzoto, M. C. R., Kanamura, C. T., Moraes, F. R., Perri, S. H. V. and Gennari, S. M. (2009). Transplacental transmission of Toxoplasma gondii in reinfected pregnant female canines. Parasitology Research 104, 12131217.CrossRefGoogle ScholarPubMed
Carlson-Bremer, D., Colegrove, K. M., Gulland, F. M. D., Conrad, P. A., Mazet, J. A. K. and Johnson, C. K. (2015). Epidemiology and pathology of Toxoplasma gondii in free-ranging California sea lions (Zalophus californianus). Journal of Wildlife Diseases 51, 362373.CrossRefGoogle ScholarPubMed
Coe, J. E. and Race, R. E. (1978). Ontogeny of mink IgG and IgM. Proceedings of the Society for Experimental Biology and Medicine 157, 289292.CrossRefGoogle Scholar
Domingo, M., Visa, J., Pumarola, M., Marco, A. J., Ferrer, L., Rabanal, R. and Kennedy, S. (1992). Pathological and immunocytochemical studies of Morbillivirus infection in Striped Dolphins (Stenella coeruleoalba). Veterinary Pathology 29, 110.CrossRefGoogle ScholarPubMed
Duarte, P. C., Conrad, P. A., Barr, B. C., Wilson, W. D., Ferraro, G. L., Packham, A. E., Carpenter, T. E. and Gardner, I. A. (2004). Risk of transplacental transmission of Sarcocystis neurona and Neospora hughesi in California horses. Journal of Parasitology 90, 13451351.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Frenkel, J. K. (1972). Cyst-induced toxoplasmosis in cats. Journal of Protozoology 19, 155177.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Jones, J. L. (2008). Toxoplasma gondii infection in humans and animals in the United States. International Journal of Parasitology 38, 12571278.CrossRefGoogle ScholarPubMed
Dubey, J. P., Zarnke, R., Thomas, N. J., Wong, S. K., Van Bonn, W., Briggs, M., Davis, J. W., Ewing, R., Mense, M., Kwok, O. C., Romand, S. and Thulliez, P. (2003). Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals. Veterinary Parasitology 116, 275296.CrossRefGoogle ScholarPubMed
Dubey, J. P., Black, S. S., Verma, S. K., Calero-Bernal, R., Morris, E., Hanson, M. A. and Cooley, A. J. (2014). Sarcocystis neurona schizonts-associated encephalitis, chorioretinitis, and myositis in a two-month-old dog simulating toxoplasmosis, and presence of mature sarcocysts in muscles. Veterinary Parasitology 202, 194200.CrossRefGoogle Scholar
Dubey, J. P., Howe, D. K., Furr, M., Saville, W. J., Marsh, A. E., Reed, S. M. and Grigg, M. E. (2015). An update on Sarcocystis neurona infections in animals and Equine Protozoal Myeloencephalitis (EPM). Veterinary Parasitology 209, 142.CrossRefGoogle ScholarPubMed
Elbez-Rubinstein, A., Ajzenberg, D., Darde, M.-L., Cohen, R., Dumetre, A., Yera, H., Gondon, E., Janaud, J.-C. and Thulliez, P. (2009). Congenital toxoplasmosis and reinfection during pregnancy: case report, strain characterization, experimental model of reinfection, and review. Journal of Infectious Diseases 199, 280285.CrossRefGoogle ScholarPubMed
Gavinet, M. F., Robert, F., Firtion, G., Delouvrier, E., Hennequin, C., Maurin, J. R., TourteSchaefer, C. and DupouyCamet, J. (1997). Congenital toxoplasmosis due to maternal reinfection during pregnancy. Journal of Clinical Microbiology 35, 12761277.CrossRefGoogle ScholarPubMed
Grigg, M. E. and Boothroyd, J. C. (2001). Rapid identification of virulent type I strains of the protozoan pathogen Toxoplasma gondii by PCR-restriction fragment length polymorphism analysis at the B1 gene. Journal of Clinical Microbiology 39, 398400.CrossRefGoogle ScholarPubMed
Hide, G., Morley, E. K., Hughes, J. M., Gerwash, O., Elmahaishi, M. S., Elmahaishi, K. H., Thomasson, D., Wright, E. A., Williams, R. H., Murphy, R. G. and Smith, J. E. (2009). Evidence for high levels of vertical transmission in Toxoplasma gondii . Parasitology 136, 18771885.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Dunachie, J. F., Siim, J. C. and Work, K. (1969). Life cycle of Toxoplasma gondii . British Medical Journal 4, 806806.CrossRefGoogle ScholarPubMed
Innes, E. A. (2007). The host-parasite relationship in pregnant cattle infected with Neospora caninum . Parasitology 134, 19031910.CrossRefGoogle ScholarPubMed
Jardine, J. E. and Dubey, J. P. (2002). Congenital toxoplasmosis in a Indo-Pacific bottlenose dolphin (Tursiops aduncus). Journal of Parasitology 88, 197199.CrossRefGoogle Scholar
Jones, J., Lopez, A. and Wilson, M. (2003). Congenital toxoplasmosis. American Family Physician 67, 21312138.Google ScholarPubMed
Kreuder, C., Miller, M. A., Jessup, D. A., Lowenstine, L. J., Harris, M. D., Ames, J. A., Carpenter, T. E., Conrad, P. A. and Mazet, J. A. (2003). Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998–2001. Journal of Wildlife Diseases 39, 495509.CrossRefGoogle ScholarPubMed
Lapointe, J. M., Duignan, P. J., Marsh, A. E., Gulland, F. M., Barr, B. C., Naydan, D. K., King, D. P., Farman, C. A., Huntingdon, K. A. B. and Lowenstine, L. J. (1998). Meningoencephalitis due to a Sarcocystis neurona-like protozoan in Pacific harbor seals (Phoca vitulina richardsi). Journal of Parasitology 84, 11841189.CrossRefGoogle ScholarPubMed
Lindsay, D. S., Thomas, N. J., Rosypal, A. C. and Dubey, J. P. (2001). Dual Sarcocystis neurona and Toxoplasma gondii infection in a Northern sea otter from Washington state, USA. Veterinary Parasitology 97, 319327.CrossRefGoogle Scholar
Lopes de Azevedo, K. M., Setubal, S., Silami Lopes, V. G., Bastos Camacho, L. A. and de Oliveira, S. A. (2010). Congenital toxoplasmosis transmitted by human immunodeficiency-virus infected women. Brazilian Journal of Infectious Diseases 14, 186189.CrossRefGoogle Scholar
Miller, M., Conrad, P., James, E. R., Packham, A., Toy-Choutka, S., Murray, M. J., Jessup, D. and Grigg, M. (2008). Transplacental toxoplasmosis in a wild southern sea otter (Enhydra lutris nereis). Veterinary Parasitology 153, 1218.CrossRefGoogle Scholar
Miller, M. A. (2008). Tissue cyst-forming coccidia of marine mammals. In Zoo and Wild Animal Medicine Vol. 6 (ed. Fowler, M. and Miller, R.), pp. 319340. Sounders Elsevier, St. Louis.CrossRefGoogle Scholar
Miller, M. A., Gardner, I. A., Kreuder, C., Paradies, D. M., Worcester, K. R., Jessup, D. A., Dodd, E., Harris, M. D., Ames, J. A., Packham, A. E. and Conrad, P. A. (2002 a). Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). International Journal of Parasitology 32, 9971006.CrossRefGoogle ScholarPubMed
Miller, M. A., Gardner, I. A., Packham, A., Mazet, J. K., Hanni, K. D., Jessup, D., Estes, J., Jameson, R., Dodd, E., Barr, B. C., Lowenstine, L. J., Gulland, F. M. and Conrad, P. A. (2002 b). Evaluation of an indirect fluorescent antibody test (IFAT) for demonstration of antibodies to Toxoplasma gondii in the sea otter (Enhydra lutris). Journal of Parasitology 88, 594599.CrossRefGoogle ScholarPubMed
Miller, M. A., Barr, B. C., Nordhausen, R., James, E. R., Magargal, S. L., Murray, M., Conrad, P. A., Toy-Choutka, S., Jessup, D. A. and Grigg, M. E. (2009). Ultrastructural and molecular confirmation of the development of Sarcocystis neurona tissue cysts in the central nervous system of southern sea otters (Enhydra lutris nereis). International Journal of Parasitology 39, 13631372.CrossRefGoogle ScholarPubMed
Miller, M. A., Conrad, P. A., Harris, M., Hatfield, B., Langlois, G., Jessup, D. A., Magargal, S. L., Packham, A. E., Toy-Choutka, S., Melli, A. C., Murray, M. A., Gulland, F. M. and Grigg, M. E. (2010). A protozoal-associated epizootic impacting marine wildlife: mass-mortality of southern sea otters (Enhydra lutris nereis) due to Sarcocystis neurona infection. Veterinary Parasitology 172, 183194.CrossRefGoogle ScholarPubMed
Minkoff, H., Remington, J. S., Holman, S., Ramirez, R., Goodwin, S. and Landesman, S. (1997). Vertical transmission of toxoplasma by human immunodeficiency virus-infected women. American Journal of Obstetrics and Gynecology 176, 555559.CrossRefGoogle ScholarPubMed
Owen, M. R. and Trees, A. J. (1998). Vertical transmission of Toxoplasma gondii from chronically infected house (Mus musculus) and field (Apodemus sylvaticus) mice determined by polymerase chain reaction. Parasitology 116, 299304.CrossRefGoogle ScholarPubMed
Pivot, F. L., de Macedo, A. G., da Silva, M. V., Ferreira, F. B., Silva, D. A. O., Pompermayer, E., Sangioni, L. A., Mine, T. W. P. and Vogel, F. S. F. (2014). Serological status of mares in parturition and the levels of antibodies (IgG) against protozoan family Sarcocystidae from their pre colostral foals. Veterinary Parasitology 199, 107111.CrossRefGoogle Scholar
Powell, C. C., Brewer, M. and Lappin, M. R. (2001). Detection of Toxoplasma gondii in the milk of experimentally infected lactating cats. Veterinary Parasitology 102, 2933.CrossRefGoogle ScholarPubMed
Pusterla, N., Mackie, S., Packham, A. and Conrad, P. A. (2014). Serological investigation of transplacental infection with Neospora hughesi and Sarcocystis neurona in broodmares. Veterinary journal (London, England: 1997) 202, 649650.CrossRefGoogle ScholarPubMed
Rejmanek, D., Vanwormer, E., Miller, M. A., Mazet, J. A. K., Nichelason, A. E., Melli, A. C., Packham, A. E., Jessup, D. A. and Conrad, P. A. (2009). Prevalence and risk factors associated with Sarcocystis neurona infections in opossums (Didelphis virginiana) from central California. Veterinary Parasitology 166, 814.CrossRefGoogle ScholarPubMed
Rejmanek, D., Miller, M. A., Grigg, M. E., Crosbie, P. R. and Conrad, P. A. (2010 a). Molecular characterization of Sarcocystis neurona strains from opossums (Didelphis virginiana) and intermediate hosts from central California. Veterinary Parasitology 170, 2029.CrossRefGoogle ScholarPubMed
Rejmanek, D., Vanwormer, E., Mazet, J. A. K., Packham, A. E., Aguilar, B. and Conrad, P. A. (2010 b). Congenital transmission of Toxoplasma gondii in Deer Mice (Peromyscus maniculatus) after oral oocyst infection. Journal of Parasitology 96, 516520.CrossRefGoogle ScholarPubMed
Remington, J. S., McLeod, R., Thulliez, P. and Desmonts, G. (2006). Toxoplasmosis. In Infectious Diseases of the Fetus and Newborn Infant (ed. Remington, J. S., McLeod, R., Thulliez, P. and Desmonts, G.), pp. 9471091. Elsevier Saunders, Philadelphia.CrossRefGoogle Scholar
Resendes, A. R., Almeria, S., Dubey, J. P., Obon, E., Juan-Salles, C., Degollada, E., Alegre, F., Cabezon, O., Pont, S. and Domingo, M. (2002). Disseminated toxoplasmosis in a Mediterranean pregnant Risso's dolphin (Grampus griseus) with transplacental fetal infection. Journal of Parasitology 88, 10291032.CrossRefGoogle Scholar
Riemann, H. P., Meyer, M. E., Theis, J. H., Kelso, G. and Behymer, D. E. (1975). Toxoplasmosis in an infant fed unpasteurized goat milk. Journal of Pediatrics 87, 573576.CrossRefGoogle Scholar
Sacks, J. J., Roberto, R. R. and Brooks, N. F. (1982). Toxoplasmosis infection associated with raw goats milk. Jama-Journal of the American Medical Association 248, 17281732.CrossRefGoogle Scholar
Shapiro, K., Miller, M. and Mazet, J. (2012). Temporal association between land-based runoff events and California sea otter (Enhydra lutris nereis) protozoal mortalities. Journal of Wildlife Diseases 48, 394404.CrossRefGoogle ScholarPubMed
Shapiro, K., Krusor, C., Mazzillo, F., Conrad, P. A., Largier, J. L., Mazet, J. A. K. and Silver, M. W. (2014 a). Aquatic polymers can drive pathogen transmission in coastal ecosystems. Proceedings of the Royal Society B 281, 20141287.CrossRefGoogle ScholarPubMed
Shapiro, K., VanWormer, E., Aguilar, B. and Conrad, PA. (2014 b). Surveillance for Toxoplasma gondii in California mussels (Mytilus californianus) reveals transmission of atypical genotypes from land to sea. Environmental Microbiology. doi:10.1111/1462-2920.12685 [Epub ahead of print].Google ScholarPubMed
Su, C., Shwab, E. K., Zhou, P., Zhu, X. Q. and Dubey, J. P. (2010). Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii . Parasitology 137, 111.CrossRefGoogle ScholarPubMed
Sundar, N., Cole, R. A., Thomas, N. J., Majumdar, D., Dubey, J. P. and Su, C. (2008). Genetic diversity among sea otter isolates of Toxoplasma gondii . Veterinary Parasitology 151, 125132.CrossRefGoogle ScholarPubMed
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal of Parasitology 30, 12171258.CrossRefGoogle ScholarPubMed
Thomas, N. J., Dubey, J. P., Lindsay, D. S., Cole, R. A. and Meteyer, C. U. (2007). Protozoal meningoencephalitis in sea otters (Enhydra lutris): a histopathological and immunohistochemical study of naturally occurring cases. Journal of Comparative Pathology 137, 102121.CrossRefGoogle ScholarPubMed
Valdes, V., Legagneur, H., Watrin, V., Paris, L. and Hascoet, J. M. (2011). Congenital toxoplasmosis due to maternal reinfection during pregnancy. Archives De Pediatrie 18, 761763.Google ScholarPubMed
VanWormer, E., Miller, M., Conrad, P., Grigg, M., Rejmanek, D., Carpenter, T. and Mazet, J. (2014). Using molecular epidemiology to track Toxoplasma gondii from terrestrial carnivores to marine hosts: implications for public health and conservation. PLoS Neglected Tropical Diseases 8, e2852.CrossRefGoogle ScholarPubMed
Wendte, J. M., Miller, M. A., Nandra, A. K., Peat, S. M., Crosbie, P. R., Conrad, P. A. and Grigg, M. E. (2010). Limited genetic diversity among Sarcocystis neurona strains infecting southern sea otters precludes distinction between marine and terrestrial isolates. Veterinary Parasitology 169, 3744.CrossRefGoogle ScholarPubMed