Infectiousness of Sylvatic and Synanthropic Small Rodents Implicates a Multi-host Reservoir of Leishmania (Viannia) braziliensis

Abstract

BackgroundThe possibility that a multi-host wildlife reservoir is responsible for maintaining transmission of Leishmania (Viannia) braziliensis causing human cutaneous and mucocutaneous leishmaniasis is tested by comparative analysis of infection progression and infectiousness to sandflies in rodent host species previously shown to have high natural infection prevalences in both sylvatic or/and peridomestic habitats in close proximity to humans in northeast Brazil.MethodsThe clinical and parasitological outcomes, and infectiousness to sandflies, were observed in 54 colonized animals of three species (18 Necromys lasiurus, 18 Nectomys squamipes and 18 Rattus rattus) experimentally infected with high (5.5×106/ml) or low (2.8×105/ml) dose L. (V.) braziliensis (MBOL/BR/2000/CPqAM95) inoculum. Clinical signs of infection were monitored daily. Whole animal xenodiagnoses were performed 6 months post inoculation using Lutzomyia longipalpis originating from flies caught in Passira, Pernambuco, after this parasite evaluation was performed at necropsy. Heterogeneities in Leishmania parasite loads were measured by quantitative PCR in ear skin, liver and spleen tissues.ResultsAll three rodent species proved to establish infection characterized by short-term self-resolving skin lesions, located on ears and tail but not on footpads (one site of inoculation), and variable parasite loads detected in all three tissues with maximum burdens of 8.1×103 (skin), 2.8×103 (spleen), and 8.9×102 (liver). All three host species, 18/18 N. lasiurus, 10/18 N. squamipes and 6/18 R. rattus, also proved infectious to sandflies in cross-sectional study. R. rattus supported significantly lower tissue parasite loads compared to those in N. lasiurus and N. squamipes, and N. lasiurus appeared to be more infectious, on average, than either N. squamipes or R. rattus.ConclusionsA multi-host reservoir of cutaneous leishmaniasis is indicated in this region of Brazil, though with apparent differences in the competence between the rodent species. The results provide preliminary insights into links between sylvatic and peri-domestic transmission cycles associated with overlaps in the rodent species’ ecological niches.

Aspects of the ecology of phlebotomine sand flies (Diptera: Psychodidae) in the Private Natural Heritage Reserve Sanctuary Caraça

“…Some mammalian species have been reported in the study area [18] that may have an important role in the maintenance of the Leishmania transmission cycle, since they can serve as reservoirs for this multi-reservoir parasite [25,26,7,27]. …”

Progress in the Mathematical Modelling of Visceral Leishmaniasis

“…In contrast, natural wildlife hosts (e.g. foxes and hares for L. infantum, rodents for L. braziliensis and L. tropica), in which infection is usually asymptomatic, show no apparent relationship between parasite loads and infectivity to sandflies (Courtenay et al, 2002a;Svobodova et al, 2003;Kassahun et al, 2015;Andrade et al, 2015;Molina et al, 2012).…”

Combining epidemiology with basic biology of sand flies, parasites, and hosts to inform leishmaniasis transmission dynamics and control

“…However, asymptomatic animals may have a longer infectious life expectancy than diseased, highly infectious individuals. The canine data reviewed above [ 37 ] suggest that qPCR has the most promise as a proxy for xenodiagnosis, but that relationship may vary with parasite tropism and Leishmania species [ 53 ]. The best specimen type (e.g., peripheral blood or skin biopsy), quantitative technique, and threshold will need to be rigorously validated against xenodiagnosis as the gold standard in each epidemiological setting.…”

“…Nonhomogeneous mixing of vectors and hosts usually results in higher transmission rates and greater infection persistence compared to homogeneously mixed populations [ 84 – 87 ]. In nature, infections of wildlife hosts of Leishmania are typically subclinical and benign, with varying degrees of tissue tropism, parasite loads, and infectiousness to sand flies, even when hosts live in close association with heavily infected vector populations [ 53 , 88 ]. Such observations highlight the specificity of host—parasite—vector relationships and the broad spectrum of possible modes of Leishmania maintenance and transmission.…”