Heterogeneities in Leishmania infantum Infection: Using Skin Parasite Burdens to Identify Highly Infectious Dogs

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Abstract
The relationships between heterogeneities in host infection and infectiousness (transmission to arthropod vectors) can provide important insights for disease management. Here, we quantify heterogeneities in Leishmania infantum parasite numbers in reservoir and non-reservoir host populations, and relate this to their infectiousness during natural infection. Tissue parasite number was evaluated as a potential surrogate marker of host transmission potential. Parasite numbers were measured by qPCR in bone marrow and ear skin biopsies of 82 dogs and 34 crab-eating foxes collected during a longitudinal study in Amazon Brazil, for which previous data was available on infectiousness (by xenodiagnosis) and severity of infection. Parasite numbers were highly aggregated both between samples and between individuals. In dogs, total parasite abundance and relative numbers in ear skin compared to bone marrow increased with the duration and severity of infection. Infectiousness to the sandfly vector was associated with high parasite numbers; parasite number in skin was the best predictor of being infectious. Crab-eating foxes, which typically present asymptomatic infection and are non-infectious, had parasite numbers comparable to those of non-infectious dogs. Skin parasite number provides an indirect marker of infectiousness, and could allow targeted control particularly of highly infectious dogs. Zoonotic visceral leishmaniasis is a sandfly-borne disease of humans and dogs caused by the intracellular parasite Leishmania infantum. Dogs are the proven reservoir. The disease is usually fatal unless treated, and is of global health significance. Diagnosis of canine infections relies on serum antibody-based tests that measure infection. In some endemic regions, a test-and-slaughter policy of seropositive dogs forms part of the national control policy to reduce human infection. However, this strategy is not considered effective. Since not all infected dogs are infectious to sandfly vectors, one option is to target control at infectious dogs, as only these dogs maintain transmission. We quantify Leishmania numbers in individual host tissues from time of infection using molecular methods. Comparing these results with their infectiousness to sandflies, we also evaluate the performance of molecular and immunological assays to identify infectious animals. Parasite numbers varied substantially between individuals, increasing with duration and severity of disease. Infectiousness to the sandfly vector was associated with high parasite numbers, and parasite loads in the skin was the best predictor of being infectious. The results suggest that molecular quantitation is useful in identifying individuals and populations responsible for maintaining transmission, with potential application in operational control programmes.

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