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

Date Published: October 8, 2015

Publisher: Public Library of Science

Author(s): Maria S. Andrade, Orin Courtenay, Maria E. F. Brito, Francisco G. Carvalho, Ana Waléria S. Carvalho, Fábia Soares, Silvia M. Carvalho, Pietra L. Costa, Ricardo Zampieri, Lucile M. Floeter-Winter, Jeffrey J. Shaw, Sinval P. Brandão-Filho, Shaden Kamhawi.

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.

Partial Text: Transmission of zoonotic pathogens may involve one, or typically more than one, reservoir host. Compared to pathogens with single reservoir hosts, those involving multi-host communities usually show reduced transmission rates through a process of zooprophylaxis or “dilution effect” due to heterogeneities in their competence to support pathogen replication and in their infectious duration, resulting in reduced pathogen-host contact, or vector-infectious host contact in the case of vector-borne pathogens [1, 2, 3]. The less common case in nature is that multi-host communities are more homogeneous as competent reservoirs, such that transmission is amplified, otherwise known as zoopotentiation; complexities in these scenarios are discussed elsewhere [2, 4]. Quantification of host heterogeneity has led to a better understanding of transmission dynamics [1, 5, 6], and improved mathematical predictions of transmission hotspots towards development of disease surveillance and control strategies [7, 8].

Three rodent species (Necromys lasiurus syn. Bolomys lasiurus (Lund, 1840), Nectomys squamipes Brants, 1827 and Rattus rattus Linnaeus, 1758) were selected for comparative study as potentially important reservoirs based on demonstrating high prevalences of natural infection or/and high population densities, in previous field studies in endemic ZCL foci in Pernambuco, northeast Brazil [10, 11]. In this region, the reported incidence is 18.5 human cases per 100,000 inhabitants [16]. N. lasiurus and N. squamipes are usually associated with Atlantic rain forest and scrub/plantation habitats, whereas R. rattus is predominantly captured inside houses and animal sheds [11].

This study investigated the comparative development of experimental infection in three putative rodent reservoir species, and their relative ability to transmit L. braziliensis to blood-feeding sandflies. We show that all three rodent species established infections, supported persistent Leishmania burdens in multiple tissue, and presented transient clinical lesions which developed within an average 38–51 days post inoculation, that spontaneously resolved within an average 14–19 days. All three rodent species were also able to infect sandflies as demonstrated by xenodiagnosis performed at c. 6 months post inoculation, by which time all skin lesions had visually healed. We found an association between infectiousness to sand flies and Leishmania loads in ear skin tissue, but not to lesion presence/absence, onset or duration time. Comparing rodent species, N. lasiurus tended to have a greater likelihood of being infectious (18/18 animals), compared to the other two species, and for comparable skin log10Leishmania loads, both N. lasiurus and N. squamipes infected a greater average proportion of sand flies than did R. rattus. R. rattus also appeared less likely to establish experimental infection at either inoculum dose, evidenced by less clinical signs and lower parasite loads. Despite these observations, the low dose group of R. rattus still proved to be infectious to a small proportion of sand flies, at least at 6 months post inoculation. These collective results suggest that the investigated rodent species represent a multi-host reservoir, though with variable reservoir competence by cross-sectional comparison. Whether any single rodent species can maintain a transmission cycle independently (R0>1) requires further study and parameter estimation [28]. For example, there is likely to be a trade-off between duration and degree of infectiousness relative to the host’s life expectancy: low-level infectiousness over sustained periods could be more significant than high-level infectiousness over a shortened life expectancy resulting from acute infection; data on their comparative longitudinal profile to indicate life-long transmission potential would be informative (e.g.[29]).



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