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Review
. 2019 Aug 4:6:e00113.
doi: 10.1016/j.parepi.2019.e00113. eCollection 2019 Aug.

The elimination of Trypanosoma brucei gambiense? Challenges of reservoir hosts and transmission cycles: Expect the unexpected

Affiliations
Review

The elimination of Trypanosoma brucei gambiense? Challenges of reservoir hosts and transmission cycles: Expect the unexpected

D Mehlitz et al. Parasite Epidemiol Control. .

Abstract

The World Health Organisation has set the goal for elimination of Human African Trypanosomiasis (HAT), caused by Trypanosoma brucei gambiense (gHAT), as a public health problem for 2020 and for the total interruption of transmission to humans for 2030. Targeting human carriers and potential animal reservoir infections will be critical to achieving this ambitious goal. However, there is continuing debate regarding the significance of reservoir host animals, wild and domestic, in different epidemiological contexts, whilst the extent and duration of the asymptomatic human carrier state is similarly undefined. This paper reviews the status of the knowledge of latent infections in wild and domestic animal reservoir hosts towards the goal of better understanding their role in the transmission dynamic of the disease. Focus areas include the transmission cycles in non-human hosts, the infectivity of animal reservoirs to Glossina palpalis s.l., the longevity of infection and the stability of T. b. gambiense biological characteristics in antelopes and domestic animals. There is compelling evidence that T. b. gambiense can establish and persist in experimentally infected antelopes, pigs and dogs for a period of at least two years. In particular, metacyclic transmission of T. b. gambiense has been reported in antelope-G.p.palpalis-antelope and pig-G.p.gambiensis-pig cycles. Experimental studies demonstrate that the infectiveness of latent animal reservoir infections with T. b. gambiense is retained in animal-Glossina-animal cycles (antelopes and pigs) for periods of three years and human infectivity markers (human serum resistance, zymodeme, DNA) are stable in non-human hosts for the same period. These observations shed light on the epidemiological significance of animal reservoir hosts in specific ecosystems characterized by presently active, as well as known "old" HAT foci whilst challenging the concept of total elimination of all transmission by 2030. This target is also compromised by the existence of human asymptomatic carriers of T. b. gambiense often detected outside Africa after having lived outside tsetse infested areas for many years - sometimes decades. Non-tsetse modes of transmission may also play a significant but underestimated role in the maintenance of foci and also preclude the total elimination of transmission - these include mother to child transmission and sexual transmission. Both these modes of transmission have been the subject of case reports yet their frequency in African settings remains to be ascertained when the context of residual foci are discussed yet both challenge the concept of the possibility of the total elimination of transmission.

Keywords: Elimination; Glossina; Human African Trypanosomiasis (HAT); Infectivity to tsetse; Longevity of parasitaemia; Non-tsetse transmission; T. b. gambiense; Transmission cycles; Wild and domestic animal reservoirs.

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Conflict of interest statement

The authors declare they have no competing interest.

Figures

Fig. 1
Fig. 1
Diagram of successful experimental cyclical transmissions of patient derived T. b. gambiense (TH Gamey Dolo 80/Lib) to and between antelopes and a goat: Primary isolation by inoculation of patient's blood to a mangabey monkey (C. torquatus) and a giant rat (C. emini) and subpassages to M. natalensis followed by metacyclic infections of black backed duikers (C. dorsalis) with G. p. palpalis fed on the monkey and rodents and another metacyclic infection to a duiker and a goat; T. b. gambiense group 1 characteristics (Paindavoine et al., 1986) are retained until 1017 days after primary isolation.
Fig. 2
Fig. 2
Experimental metacyclic infections (G. p. palpalis) of black backed duikers (C. dorsalis) and a goat with patient derived T. b. gambiense (stock TH Gamey Dolo 80/Lib x): Course, level and duration of parasitaemia and persistence of human infectivity markers [gambiense group 1, (Paindavoine et al., 1986)] after two cyclical transmissions in non-human hosts.
Fig. 3
Fig. 3
Experimental metacyclic infections (G. p. gambiensis) of antelopes and pigs with patient derived T. b. gambiense (stock TH Gamey Dolo 80/Lib): Course and level of parasitaemia in bushbuck (T. scriptus), duikers (C. dorsalis) and domestic pigs.
Fig. 4
Fig. 4
Experimentally infected pigs: Level and longevity of parasitaemia after infections with bloodstream forms (pig 15 and 14) and metacyclic infections (G. p. gambiensis) (pig 24 and 29) with T. b. gambiense [TSw 65/82 KP I clone B, pig isolate from Cote D'Ivoire, human serum resistant, DNA hybridization gambiense (Paindavoine et al., 1986) and persistence of these human infectivity markers after two cyclical transmissions.

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