Hookworm Clearance in South American Fur Seal pups (Arctocephalus australis): Mechanisms and Role in Pup Survival
IAAAM 2017
Mauricio Seguel1,3*+; Francisco Muñoz2; Diego Perez-Venegas3; Josefina Gutierrez2; Ananda Muller4; Elizabeth Howerth1; Nicole Gottdenker1
1Department of Pathology, College of Veterinary Medicine, University of Georgia, Athens, GA, USA; 2Animal Pathology Department, Facultad de Ciencias Veterinarias, Universidad Austral de Chile, Valdivia, Chile; 3Programa de Doctorado en Medicina de la Conservacion, Universidad Andres Bello, Santiago, Chile; 4Department of Veterinary Clinical Sciences, Universidad Austral de Chile, Valdivia, Chile

Abstract

Hookworms (Uncinaria sp.) are a major cause of pup mortality in many otariid populations, including South American fur seals at Guafo Island, in the Chilean Patagonia.1,2,3 A unique feature of otariid hookworm infections is the clearance of nematodes from the intestine when pups are between 2 to 6 months old.3 However, the details of this process and its consequences for pup survival are unknown. The objectives of the study were to determine how hookworms are cleared from the intestine, and to know if this process is important for fur seal pup survival. Between 2014 and 2017 Austral summers, hookworm infection was closely monitored in a total of 490 pups when they were between 1 to 80 days old. Pups were captured every 7 to 15 days to follow the development of hookworm disease, and in each capture feces and blood were collected and fecal flotation and complete CBCs were performed. A randomly selected subset of hookworm-infected pups (n=160) were treated with ivermectin, and in 2016, pups (n=35) with different hookworm infection intensities were challenged with phytohemagglutinin (PHA). Additionally, we performed necropsies, complete histopathology and CD3, Iba-1 and CD79a immunohistochemistry in 50 hookworm-infected and 15 hookworm-free (control) pups found dead during the study. The serum of some pups (n=30) was tested for the presence of parasite IgG by developing immunohistochemistry protocols using hookworm tissues. Hookworm patent period ranged from 18 to 65 days. Pups with lower hookworm burden, and higher numbers of lymphocytes and basophils in the blood eliminated hookworms earlier in the season (Generalized linear model, negative binomial distribution, p<0.001). These pups also had a stronger inflammatory reaction in the PHA challenge and higher numbers of T-lymphocytes in the intestine when compared to pups that did not clear hookworm infection (Mann–Whitney U test, p-values <0.001). Approximately 40% of the pups with high hookworm burden were able to eliminate hookworms and survive. In these pups, clearance was associated with the presence of high numbers of lymphocytes, basophils, and parasite-specific IgG in the blood. This IgG binds to the intestinal brush border of the hookworms, an important nematode structure for blood digestion and absorption. Animals with severe hookworm infection that failed to expel the parasite died due to hookworm disease. Factors that significantly increased the probability of pup mortality were lower hemoglobin concentration and longer duration of hookworm infection. As has been described in other mammals,4 South American fur seal pups clear hookworm infection through an immune-mediated mechanism, where T-lymphocytes, basophils and parasite-specific IgG are key players. The capacity of a pup to mount the immune response required for parasite clearance significantly impacts its chances of hookworm elimination and survival. This study shows how variations in the host immune response to parasitic infection can have population level effects in marine vertebrates.

Acknowledgements

Work partially funded by Morris Animal Foundation (grant D16ZO-413), Society for Marine Mammalogy Small Grants-in-Aid and Rufford small grant foundation. We appreciate the field collaboration of Dr Lorraine Barbosa, Dr Ignacio Silva, Eugene DeRango and Dr Hector Paves. We thank the logistical support of the Chilean Navy and Guafo Island lighthouse crews.

* Presenting author
+ Student presenter

Literature Cited

1.  Seguel M, Munoz F, Navarrete MJ, Paredes E, Howerth E, Gottdenker, N. 2017. Hookworm infection in South American fur seal (Arctocephalus australis) pups: pathology and factors associated with host tissue damage and mortality. Vet Pathol. 54:288–297.

2.  Seguel M, Paves H, Paredes E, Schlatter R. 2013. Causes of mortality in South American fur seal pups (Arctophoca australis gracilis) at Guafo Island, southern Chile (2004–2008). Mar Mammal Sci. 29:36–47.

3.  Lyons ET, Spraker TR, De Long RL, Ionita M, Melin SR, Nadler S, Tolliver SC. 2011. Review of research on hookworms (Uncinaria lucasi Stiles, 1901) in northern fur seals (Callorhinus ursinus Linnaeus, 1758). Parasitol Res. 109:257–65.

4.  Fujiwara RT, Geiger SM, Bethony J, Mendez S. 2006. Comparative immunology of human and animal models of hookworm infection. Parasite Immunol. 28:285–93.

  

Speaker Information
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Mauricio Seguel
Department of Pathology, College of Veterinary Medicine
University of Georgia
Athens, GA, USA


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