Impact of mass chemotherapy in domestic livestock for control of zoonotic T. b. rhodesiense human African trypanosomiasis in Eastern Uganda

Abstract

Introduction: Human African trypanosomiasis (HAT) comprises two fatal parasitic diseases. Uganda is home to both chronic T. b. gambiense (gHAT) and the acute zoonotic form T. b. rhodesiense (rHAT) which occur in two large but discrete geographical foci. The area affected by rHAT has been rapidly expanding due to importation of T. b. rhodesiense infected cattle into tsetse infested but previously HAT free districts. Migration of rHAT has resulted in a considerable human health burden in these newly affected districts. Here, we examined the impact of a single, district-wide, mass chemotherapeutic livestock intervention, on T. b. rhodesiense prevalence in cattle and on incidence and distribution of human rHAT cases in Kamuli and Soroti districts in eastern Uganda.

Methods: A single mass intervention in domestic cattle (n=30,900) using trypanocidal drugs was undertaken in November and December 2002 under the EU funded Farming in Tsetse Controlled Areas (FITCA) programme. The intervention targeted removal of the reservoir of infection i.e. human infective T. b. rhodesiense parasites in cattle, in the absence of tsetse control. Interventions were applied in high-risk sub-counties of Kamuli district (endemic for rHAT) and Soroti district (where rHAT has been recently introduced). The prevalence of T. brucei s.l. and the human infective subspecies, T. b. rhodesiense in cattle (n=1833) was assessed before and 3 and 12 months after intervention using PCR-based methods. A combination of descriptive statistical analysis and spatial scan statistics were applied to analyse rHAT cases reported over a 5-year period (January 2000-July 2005).

Results: A single intervention was highly effective at removing human infective T. b. rhodesiense parasites from the cattle reservoir and contributed to a significant decrease in human rHAT cases. Intervention coverage was higher in Kamuli (81.1%) than in Soroti (47.3%) district but despite differences in coverage both districts showed a reduction in prevalence of T. b. brucei s.l. and T. b. rhodesiense. In Kamuli, the prevalence of T. brucei s.l. decreased by 54%, from 6.75% to 3.11%, 3, months post-intervention, rising to 4.7% at 12 months. The prevalence of T. b. rhodesiense was 3% pre-intervention and no T. b. rhodesiense infections were detected 3 and 12, months post-treatment. In Soroti, the prevalence of T. brucei s.l. in cattle decreased by 38% (from 21% to 13%) 3 months after intervention decreasing to less than 10% at 12 months. The prevalence of T. b. rhodesiense was reduced by 50% at 12-months post-intervention (6%-3%). Most notably, was the impact of the intervention on the population dynamics between T. b. brucei and human infective T. b. rhodesiense. Before intervention in Kamuli district 56% of T. b. brucei s.l. circulating in cattle were T. b. rhodesiense; at both 3 and 12 months after intervention none of the re-infecting T. b. brucei s.l. were human infective, T. rhodesiense. For human rHAT cases, there was a seven-fold decrease in rHAT incidence after intervention in Kamuli district (5.54 cases/1,000 head of population 2000-2002 to 0.76 cases/1,000, 2003-2005). Incidence data suggests that the intervention had minimal impact on the number of rHAT cases in Soroti overall, but showed a significant decrease in the seasonal peak of cases in the year following treatment.

Conclusion: A single intervention, targeted at cattle, introduced at district level, in the absence of tsetse control, was highly effective at removing human infective rHAT parasites from the cattle reservoir and contributed to a significant decrease in human rHAT cases. The differential impacts observed between the two districts are related to both the different stages of rHAT endemicity in the districts, and levels of intervention coverage achieved in the cattle population. Treatment of cattle to remove the reservoir of rHAT infection offers a promising and cost effective approach for the control of rHAT. It is important that cattle are treated before relocation to prevent possible merger of the two HAT foci, which would complicate diagnosis and treatment of both gHAT and rHAT.

Keywords: Animal African trypanosomiais (AAT); Animal reservoir; Burden; DALYs; Endemic; Human African trypanosomiasis (HAT); Outbreak; Reservoir; Sleeping sickness; T. b. gambiense; T. b. gambiense HAT (gHAT); T. b. rhodesiense; T. b. rhodesiense HAT (rHAT); Trypanocide; Uganda; Zoonosis.