High levels of infectiousness of asymptomatic Leishmania (Viannia) braziliensis infections in wild rodents highlights their importance in the epidemiology of American Tegumentary Leishmaniasis in Brazil

Abstract

Background The epidemiological significance of wildlife infections with aetiological agents causing human infectious diseases is largely determined by their infection status, contact potential with humans (via vectors for vector-borne diseases), and their infectiousness to maintain onward transmission. This study quantified these parameters in wild and synanthropic naturally infected rodent populations in an endemic region of tegumentary leishmaniasis in northeast Brazil. Methods Capture-mark-recapture (CMR) of rodents was conducted over 27 months in domestic/peri domestic environs, household plantations and nearby Atlantic Forest (9,920 single trap nights). Rodent clinical samples (blood and ear tissue) were tested for infection by conventional PCR and quantitative PCR (qPCR) for L. (Viannia) braziliensis, and xenodiagnosis to measure infectiousness to the local sand fly vector. Results A total 603 individuals of 8 rodent species were (re)captured on 1,051 occasions. The most abundant species were Nectomys squamipes (245 individuals, 41% of the total catch), Rattus rattus (148, 25%), and Necromys lasiurus (83, 14%). All species were captured in greater relative frequencies in plantations; R. rattus was the only species captured in all three habitats including in and around houses. Four species, comprising 22.6% of individuals captured at least twice, were geolocated in more than one habitat type; 78.6% were infected with L. (V.) braziliensis, facilitating inter-species and inter-habitat transmission. Species specific period prevalence ranged between 0%-62% being significantly higher in N. squamipes (54–62%) and H. sciureus (43–47%). Xenodiagnosis was performed on 41 occasions exposing 1,879 Nyssomyia whitmani sand flies to five rodent species (37 individuals). Similar mean levels of infectiousness amongst the more common rodent species were observed. Longitudinal xenodiagnosis of the N. squamipes population revealed a persistent level of infectiousness over 13 months follow-up, infecting a median 48% (IQR: 30.1%-64.2%) of exposed blood-fed vectors. The proportion of exposed flies infected was greater in the low comparted to in the high seasonal period of vector abundance. L. (V.) braziliensis parasite loads in rodent blood quantified by qPCR were similar across rodent species but did not represent a reliable quantitative marker of infectiousness to sand flies. The standardised risk of rodent infection in plantations was 70.3% relative to 11.3% and 18.4% in peri domestic and forest habitats respectively. R. rattus was the only exception to this trend indicating greatest risk in the peri domestic environment. Conclusions The results support the view that a collective assemblage of wild and synanthropic rodent species is an important wild reservoir of L. (V.) braziliensis in this region, with N. squamipes and R. rattus probably playing a key role in transmission within and between habitat types and rodent species. Rodents, and by implication humans, are at risk of infection in all sampled habitats, but more so in homestead plantations. These conclusions are based on one of the longest CMR study of small rodents in an American Tegumentary Leishmaniasis (ATL) foci.

Assessing reservoir host status in leishmaniasis with special reference to the infectiousness of Leishmania (Viannia) braziliensis infections in wild rodents

“…Sinks are dead end infections that do not lead to new ones. The multi-host scenario is supported by recent observations that detected L. ( V. ) braziliensis in 6/8 different rodent species 10 captured an endemic American Cutaneous Leishmaniasis (ACL) focus. However, the multi-host concept may not apply to all species.…”

“…A study of the infectiousness of mice experimentally infected with L. (L.) donovani showed that parasite distribution in the skin was patchy 37 . In the L. (V.) braziliensi s CMR study 10 there was evidence of skin infections because of positive xenodiagnosis in animals whose blood qPCRs were negative. Also, in that study there was a poor relationship between ear skin positive qPCRs and positive xenodiagnosis suggesting the wrong site had been sampled.…”

“…A way of overcoming the limitations of studying infectiousness in laboratory bred reservoirs is to investigate it in natural infections and vectors. This was made possible during a longitudinal capture-mark-recapture (CMR) study of wild and synanthropic rodents naturally infected with Leishmania (V.) braziliensi s in northeast Brazil 10 . Over 27 months 603 rodents belonging to 8 species were re-captured on 1,051 occasions.…”

“…lasiurus , Oxymycterus dasytrichus and R. rattus ) with Nyssomyia whitmani and Lu. longipalpis 10 . All the species were infectious to sand flies.…”

Canine leishmaniasis in the Americas: etiology, distribution, and clinical and zoonotic importance

“…detected in dogs in the Americas are native to the Neotropical region and are primarily maintained by wildlife reservoirs [ 4 , 60 , 61 ]. For instance, small rodents are exceptional hosts for L. braziliensis [ 62 – 64 ].…”