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United States Department of Agriculture

Agricultural Research Service

Research Project: Managing the Emerging Risk of Trichinellosis in Organic and Free Range Pork

Location: Animal Parasitic Diseases

Title: Modeling effective transmission strategies and control of the world’s most successful parasite

Authors
item Turner, Matthew -
item Lenhart, Suzanne -
item Rosenthal, Benjamin
item Sullivan, Adam -
item Zhao, Xiaopeng -

Submitted to: Theoretical Population Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: April 1, 2013
Publication Date: June 1, 2013
Citation: Turner, M., Lenhart, S., Rosenthal, B.M., Sullivan, A., Zhao, X. 2013. Modeling effective transmission strategies and control of the world’s most successful parasite. Theoretical Population Biology. 86:50-61.

Interpretive Summary: Efforts to limit human exposure to parasites would benefit from explicit, quantitative representations of how these parasites are transmitted. Human toxoplasmosis, for example, occurs when people consume meat infected with this parasite, or when they ingest water or food contaminated with cysts excreted by cats. Cats acquire infection in the same ways, as do their prey. But their prey (for example, mice) can also acquire the infection congenitally. Here, we developed a series of mathematical equations intended to capture this complexity in order to predict the consequences of various interventions, including vaccination of cats and harvesting of their prey. We found that eradication efforts are hindered by the fact that the parasite can employ so many different routes of transmission, that even modest rates of cat predation are sufficient to ensure continued transmission, that congenital transmission must occur where cat predation rarely occurs, and that parasites may face tradeoffs in optimizing transmission to the predators or offspring of mice. The model enables consideration of the necessary proportions of cat vaccination and mouse harvesting that would be required to achieve adequate control. These results will be of interest to epidemiologists, mathematicians, parasitologists, veterinarians, and public health personnel.

Technical Abstract: Mathematical modelling can provide a useful means to interrogate complex biological phenomena, such as the conditions under which any of several available life history strategies contribute to the force of transmission of infectious and parasitic organisms. Here, we have developed a system of differential equations in order to model the complete lifecycle of Toxoplasma gondii, the agent responsible for human and veterinary toxoplasmosis. This parasite has achieved prevalence worldwide, infecting all warm-blooded vertebrates, relying on cats to complete its sexual phase of reproduction. Eating meats in which this parasite has encysted confers risk of infection to people and other animals, as does ingestion of water or foods contaminated with environmentally-resistant ’oocysts’ excreted by cats. Vertical transmission (from mother to off spring) is also possible, leading to disease risk and contributing additional means of ensuring perpetuation of transmission. Previous modelling efforts have emphasized (or limited) one particular route of transmission. In order to better assess the contributions of each transmission route, we have endeavored to construct and analyze the behavior of a series of equations intended to capture the salient features of each, and in order to better understand their relative contributions to transmission risk in a variety of circumstances. In particular, we extended previous models to include explicit considerations of virulence, vertical transmission, parasite induced changes in host behavior, and controls based on vaccination and harvest. Our analyses suggest 1) the summed contribution of each transmission route may ensure transmission in cases where no single transmission mode is sufficient to do so; 2) when predation is even moderately frequent, the predator-prey cycle is sufficient to sustain parasite transmission; 3) where predation only rarely occurs, vertical transmission is necessary to parasite persistence; 4) the parasite may face tradeoffs in optimal exploitation of intermediate hosts, if predation pressure varies and if increasing exploitation of mice (and other intermediate hosts) reduces the longevity of such hosts; 5) to extirpate the infection locally, cat vaccination might be ineffective except if also coupled with harvest of intermediate hosts; 6) protecting livestock and human health require sustained efforts at limiting transmission among the parasite’s principal hosts. A robust and flexible modelling framework should prove useful in addressing other aspects of this complex, important, and challenging problem in ecology and epidemiology.

Last Modified: 7/12/2014