New Manifestations of Infection with Apicomplexan Protozoal Parasites in Pinnipeds Stranded along the Central California Coast: A Summary of Pathologic Findings
IAAAM 2012
Kathleen M. Colegrove1; Daphne Carlson-Bremer2; Bradd C. Barr3; Frances M.D. Gulland4; Patricia A. Conrad5
1Zoological Pathology Program, University of Illinois at Urbana-Champaign, Maywood, IL, USA; 2Vanderbilt Institute for Global Health, Vanderbilt University, Nashville, TN, USA; 3California Animal Health and Food Safety Laboratory, Davis, CA, USA; 4The Marine Mammal Center, Marin Headlands, Sausalito, CA, USA; 5Department of Pathology, Microbiology, and Immunology, School of Veterinary Medicine, University of California, Davis, CA, USA

Abstract

Marine mammals serve as definitive or intermediate hosts for several apicomplexan protozoan parasites, most notably Eimeria phocae, Toxoplasma gondii, and Sarcocystis sp.6 In general, very little is known about the extent and diversity of coccidian parasites infecting pinnipeds. The purpose of this presentation is to summarize the pathologic findings associated with apicomplexan parasite infection in stranded pinnipeds with an emphasis on several newly encountered manifestations of infection identified by our research group. In Pacific harbor seals (Phoca vitulina), infection with Toxoplasma gondii or Sarcocystis neurona causes meningoencephalitis.3,5 Additionally, dual infection with both parasites has been documented and in one study death was shown to be more likely in dual infections versus infection with a single species.5 In California sea lions (Zalophus californianus, CSLs), T. gondii most commonly causes meningoencephalitis and myocarditis, though in a recent survey disease due to infection was uncommon. Toxoplasma gondii can also cause abortion and fetal infection in CSLs. Sarcocystis neurona can cause meningoencephalitis in CSLs, though in many cases the most significant lesion is a severe polymyositis. Myositis may affect the thoracic and cervical skeletal muscle, diaphragm, and esophagus and in some cases death is secondary to respiratory compromise and aspiration pneumonia. The myositis is characterized by chronic active non-suppurative inflammation, large regions of myocyte necrosis, and myocyte regeneration. Sarcocysts can be noted within skeletal muscle, though often are adjacent to areas of severe inflammation. Sarcocystis-induced myositis has been successfully treated using ponazuril.2

Enteric protozoal infection has recently been identified in stranded CSLs.4 By histopathology and electron microscopy, sexual and asexual stages were identified indicating that sea lions are definitive hosts of the organisms, though infection was only associated with mild, clinically insignificant enteritis. Analysis of PCR amplified ITS-1 gene sequences identified three novel sequences with closest homology to Neospora caninum and organisms were designated coccidians "A", "B", and "C". Oocysts with DNA sequences matching coccidians "A" and "B" have also been identified in CSL feces.1

Coccidian "C" has also recently been identified in two Pacific harbor seals with disseminated protozoal infection indicating that CSLs are definitive hosts for at least one coccidian species that can cause disease in a marine mammal intermediate host. One affected seal was a neonate that had no evidence of having nursed prior to death, indicating that infection occurred in utero. The other seal was a pup and lesions included severe granulomatous and suppurative thymitis and lymphadenitis. There were numerous protozoal zoites and schizonts within lesions. Schizonts exhibited unique morphologic characteristics.

Taken together these findings suggest that some pinniped species may serve as definitive or intermediate hosts of previously undescribed protozoal species. Infection with apicomplexan protozoa may result in lesions distinct from the more typically described meningoencephalitis, hepatitis, and muscle cysts typically associated with T. gondii and S. neurona infections.

Acknowledgements

The authors wish to thank the staff and volunteers of The Marine Mammal Center, Dr. Michael Kinsel, and the histology laboratory at University of Illinois at Urbana-Champaign. This work was funded in part by the NSF-EID grant from the Ocean Division and Biological Sciences Directorate (OCE-1065990).

References

1.  Carlson-Bremer D, Johnson CK, Miller RH, Gulland FM, Conrad PA, Wasmuth JD, Colegrove KM, Grigg ME. Identification of two novel coccidian species shed by California sea lions (Zalophus californianus). J Parasitol. 2012;98(2):347–354. (Epub 2011Nov 17).

2.  Carlson-Bremer D, Gulland FM, Johnson CK, Colegrove KM, Van Bonn WG. Diagnosis and treatment of Sarcocystis neurona-induced myositis in a free-ranging California sea lion. J Am Vet Med Assoc. 2012;240:324–328.

3.  Colegrove KM, Greig D, Gulland FM. Causes of stranding of phocids [Northern elephant seals (Mirounga angustirostris) and Pacific harbor seals (Phoca vitulina)] along the central California coast, 1992–2001. Aquat Mamm. 2005;31:1–10.

4.  Colegrove KM, Grigg ME, Carlson-Bremer D, Miller RH, Gulland FM, Ferguson DJ, Rejmanek D, Barr BC, Nordhausen R, Melli AC, Conrad PA. Discovery of three novel coccidian parasites infecting California sea lions (Zalophus californianus), with evidence of sexual replication and interspecies pathogenicity. J Parasitol. 2011;97:868–877.

5.  Gibson AK, Raverty S, Lambourn DM, Huggins J, Magargal SL, Grigg ME. Polyparasitism is associated with increased disease severity in Toxoplasma gondii-infected marine sentinel species. PloS Negl Trop Dis. 2001;5:e1142.

6.  Miller M. Tissue cyst-forming coccidian of marine mammals. In: Fowler M, Miller E (eds.), Zoo and Wild Animal Medicine, Current Therapy. Sixth ed. Philadelphia: W.B. Saunders Press; 2008:319–340.

  

Speaker Information
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Kathleen M. Colegrove
Zoological Pathology Program
University of Illinois at Urbana-Champaign
Maywood, IL, USA


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