Indigenous African chickens (Gallus gallus domesticus) lack an anti-Trypanosoma factor and have a prospect for zoonotic transmission of African trypanosomiasis

Abstract

African trypanosomes evade host immune response through antigenic variation and utilize other immune modulatory mechanisms to survive in the immunologically hostile mammalian bloodstream. However, indigenous African chicken (Gallus gallus domesticus) exhibits lower susceptibility to trypanosomes, suggesting unique resistance mechanisms; but the exact factor(s) of resistance remains elusive. This study aims to elucidate the mechanisms underlying the observed resistance of indigenous African chickens to T. brucei brucei infection, and to assess their potential role as cryptic reservoirs in zoonotic transmission. Non-immunosuppressed and immunosuppressed chickens were intravenously inoculated with ∼2.5 × 10⁸ parasites, and parasitemia was monitored using microscopy, xenodiagnosis, and PCR. Rats served as controls and were intraperitoneally infected with 10⁴ parasites. Haematological parameters in both chickens and rats were assessed using standard methods. Furthermore, in vitro anti-Trypanosoma activity of normal and infected chicken blood components was evaluated. The results reveal that chickens displayed no microscopic parasitemia beyond 9 h post-infection (pi) and survived beyond 60 days, whereas rats passaged with over 10⁴-folds less trypanosomes developed parasitemia at day 5, which progressed and killed the rats between days 10–19. Further, while there were no significant haematological alterations over a 4-week observation period in the chicken, infected rats presented significant reductions in packed cell volume, haemoglobin, and red blood cell counts at peak infection, indicating anaemia sequelae. Additionally, infected rats exhibited neutropenia, lymphocytosis, increased hemolysis and mortality. Intriguingly, despite the observed trypanosomes suppression in chickens, incubation of trypanosomes with chicken blood, serum, or plasma revealed no intrinsic anti-Trypanosoma activity. But blood collected from infected chickens at 1- and 7-days post-infection successfully initiated infection in rats through xenodiagnosis, confirming transmissibility despite the absence of detectable parasitemia in chickens revealing a covert but potentially infectious state. Similarly, PCR detection at 7 dpi, indicated covert/suppressed infection. These findings suggest that indigenous African chickens, while resistant to overt trypanosomiasis, may act as cryptic reservoirs for Trypanosoma spp., potentially facilitating parasite zoonotic transmission.