Human Competence to Transmit Leishmania infantum to Lutzomyia longipalpis and the Influence of Human Immunodeficiency Virus Infection

Abstract

Visceral leishmaniasis (VL) caused by Leishmania infantum is a lethal disease transmitted by sand flies. Although, considered a zoonosis with dogs held as the main reservoirs, humans are also sources of infection. Therefore, control policies currently focused on dog culling may need to consider that VL and human immunodeficiency virus (HIV)/VL patients may also be infectious, contributing to transmission. Reservoir competence of patients with VL without and with HIV infection and of persons asymptomatically infected with Leishmania was assessed by xenodiagnosis with the vector Lutzomyia longipalpis. Parasites in sand fly's guts were identified by using optical microscopy and by conventional polymerase chain reaction (PCR). Leishmania infantum blood parasite burden was determined by quantitative PCR. Among the 61 participants, 27 (44%) infected sand flies as seen by microscopy or PCR. When infectiousness was assessed by microscopy, xenodiagnosis was positive in five (25%) patients not infected with HIV, whereas nine (45%) of those harboring HIV were positive. Among the 19 asymptomatic patients four (21%) infected sand flies only demonstrated by PCR. One (50%) asymptomatic patient with HIV had a positive xenodiagnosis by microscopy. 9/372 (2.4%) and 37/398 (9.2%) sand flies were infected when feeding in patients without and with HIV, respectively. Infectiousness was poorly correlated with quantitative PCR. The study shows that asymptomatic humans are capable of transmitting L. infantum, that ill persons with HIV infection are more infectious to sand flies, and that humans are more important reservoirs than previously thought. This fact may be considered when designing control policies for zoonotic VL.

Figure 1.

Algorithm used for selecting the study population. Patients with kala-azar, asymptomatic persons looking for diagnosis, and asymptomatic pregnant women were tested for human immunodeficiency virus (HIV). Those with and without (HIV) were separated between symptomatic and asymptomatic individuals.

Figure 2.

Correlation between the natural logarithm of parasite load (kDNA/mL, or amastigote-equivalents) as measured by quantitative polymerase chain reaction (PCR) from peripheral blood from each individual with visceral leishmaniasis or asymptomatically infected with Leishmania infantum and the infectiousness to Lutzomyia longipalpis as measured by the proportion of infected sand flies fed on that person. (A) by microscopy (r = 0.47; P < 0.001), (B) by PCR (r = 0.32; P < 0.001), and (C) by microscopy or PCR (r = 0.44; P < 0.001).