Revisiting Trypanosoma rangeli Transmission Involving Susceptible and Non-Susceptible Hosts

Abstract

Trypanosoma rangeli infects several triatomine and mammal species in South America. Its transmission is known to occur when a healthy insect feeds on an infected mammal or when an infected insect bites a healthy mammal. In the present study we evaluated the classic way of T. rangeli transmission started by the bite of a single infected triatomine, as well as alternative ways of circulation of this parasite among invertebrate hosts. The number of metacyclic trypomastigotes eliminated from salivary glands during a blood meal was quantified for unfed and recently fed nymphs. The quantification showed that ~50,000 parasites can be liberated during a single blood meal. The transmission of T. rangeli from mice to R. prolixus was evaluated using infections started through the bite of a single infected nymph. The mice that served as the blood source for single infected nymphs showed a high percentage of infection and efficiently transmitted the infection to new insects. Parasites were recovered by xenodiagnosis in insects fed on mice with infections that lasted approximately four months. Hemolymphagy and co-feeding were tested to evaluate insect-insect T. rangeli transmission. T. rangeli was not transmitted during hemolymphagy. However, insects that had co-fed on mice with infected conspecifics exhibited infection rates of approximately 80%. Surprisingly, 16% of the recipient nymphs became infected when pigeons were used as hosts. Our results show that T. rangeli is efficiently transmitted between the evaluated hosts. Not only are the insect-mouse-insect transmission rates high, but parasites can also be transmitted between insects while co-feeding on a living host. We show for the first time that birds can be part of the T. rangeli transmission cycle as we proved that insect-insect transmission is feasible during a co-feeding on these hosts.

Fig 1. Infection rates of R. prolixus 5^th instar nymphs that fed on T. rangeli-infected mice on different days after infection.

The data shown represent the mean of three biological replicates, except from the data for 126 days post infection, which are based on a single experiment using five tested insects. For the other replicates, 25–30 nymphs were used for each evaluation day.

Fig 2. Number of parasites found in the intestinal tract of T. rangeli-infected R. prolixus 5^th instar nymphs that were fed on mice at different stages of infection.

The horizontal lines represent the median value obtained for each group.

Fig 3. Rates of infection of nymphs that co-fed with T. rangeli-infected conspecifics (uninf = uninfected; inf = infected).

In the 5uninf/1inf assay using pigeons as hosts, recipient insects were 6 cm apart from the donor.

Fig 4. Complement-mediated T. rangeli metacyclic trypomastigote lysis by mouse and pigeon serum.

Data are presented as the percentage of lysed trypomastigotes after 30 min of incubation whit non-heat inactivated serum (n = 3).