African animal and human trypanosomiasis in South Eastern Uganda: animal reservoirs, vector competence and characterisation of trypanosoma brucei isolates
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This study was designed to investigate the factors responsible for the persistence of sleeping sickness in southeastern Uganda. In addition to the general aspects, this investigation was specifically designed to study the role of the domestic animal and vector competence as factors in the transmission and persistence of sleeping sickness in the affected foci of southeastern Uganda. The study area was zoned according to the agricultural system and three zones (designated zone I, II and III representing Kamuli, Mukono and Tororo districts respectively) were studied as these were found to be predominant in many of the sleeping sickness foci of Kamuli, Mukono and Tororo. Investigations carried out have indicated a trypanosomosis prevalence of 13.25% among cattle, 17.53% among pigs, 1.75% among small ruminants and 0% in dogs. These figures are high especially in cattle and pigs, moreover, the Trypanozoon prevalence was estimated at 4.99% among cattle, 13.89% among pigs and 0.44% in the small ruminants. Using the human serum resistance tests and PCR, this study has continued to emphasise the importance of cattle as a reservoir for T.b. rhodesiense and in addition, these techniques have proved that the pig (both BIIT and PCR) and sheep (BIIT) are very important reservoirs of T.b.rhodesiense. The sole vector for sleeping sickness in zone and II was found to be G.fuscipes fuscipes. However, in zone III, both G.f.fuscipes and G.pallidipes were trapped, with G.f.fuscipes (99.72% of the total tsetse trapped) being the predominant vector. The prevalence of bovine trypanosomosis in zone I was 8.73%, with T.brcucei infections estimated at 3.87%. Of all the trypanosomes isolated from cattle, 44.33% were grouped as belonging to the T.brucei subgroup. On further characterisation with the human serum resistance test, none of these T.brucei subgroup isolates from cattle in this zone was potentially human infective. However, using the polymerase chain reaction (PCR), one of the T.brucei isolates was found to be carrying the human serum resistance associated (SRA) gene, an indication that it was potentially human infective (T.b.rhodesiense) thus helping to define the role played by cattle in the transmission of sleeping sickness in this zone. Meanwhile, in this zone (zone I), the point prevalence of trypanosomosis in pigs was 16.33% and T.brucei subgroup infection among the infected pigs was 82.48%. When the T.brucei subgroup isolates were analysed, 30.19% were found to be potentially human infective by the human serum resistance test and 75% of the T.brucei subgroup isolates analysed by PCR were found to be carrying the SRA gene. The presence of potentially human infective T.brucei subgroup in pigs makes this animal species the predominant reservoir and the major risk factor in the transmission and persistence of sleeping sickness in zone I. In addition, 30.6% of the tsetse in zone I get their blood-meal from pigs, which implies that the “pig-tsetse-human cycle” is the predominant sleeping sickness transmission cycle in zone I. The prevalence of bovine trypanosomosis in zone II was 13.08% with T.brucei subgroup infections estimated at 6.01%. Of the isolates characterized, 45.89% were grouped as T.brucei subgroup infections, of which 10.53% were potentially human infective according to the BIIT results and therefore grouped as T.b. rhodesiense. In addition 5% of the T.brucei subgroup isolates were found to be having the SRA gene. The cattle-tsetse-human sleeping sickness cycle is one of the two sleeping sickness transmission cycles in this zone. Similarly, the point prevalence of trypanosomosis in pigs in zone II was found to be 22.92%. The T.brucei subgroup infections among the trypanosomes isolated from the pigs was 85.51%. Of these T. brucei subgroup isolates, 26.09% were found to be potentially human infective as characterised by the BIIT. Using the SRA-PCR, 31.58% of the T. brucei subgroup analysed were found to be carrying the SRA gene. In addition to the cattle-tsetse-man cycle, the pig-tsetse-human sleeping sickness transmission cycle is the other major cycle in this zone which is supported by the 14.53% of the tsetse that get their bloodmeals from pigs in the zone. The prevalence of bovine trypanosomosis in zone III was 17.91% with T.brucei subgroup infections estimated at 7.34%. Of all the trypanosome infections among cattle in this area, 41% were grouped as T.brucei subgroup infections. Using the human BIIT, 47.30% of these T.brucei subgroup isolates were found to be potentially human infective and therefore grouped as T.b.rhodesiense. Similarly, 23.81% of the T.brucei subgroup isolates from cattle were confirmed to be carrying the SRA gene. Basing on these results, the cattle-tsetsehuman is the major sleeping sickness transmission cycle in zone III. Meanwhile, the prevalence of trypanosomosis in pigs in this zone was 2.44% and there were no T.brucei subgroup infections detected, implying that pigs may be playing a minimal role in the transmission of sleeping sickness in this zone. For the small ruminants kept in zone III trypanosomosis prevalence was 13.79%. All the trypanosome infections were found in the sheep. Interestingly, a potentially human infective T.brucei trypanosome was isolated from the sheep in this zone, suggesting that the sheep-tsetse-human sleeping sickness transmission cycle is contributing to the persistence of sleeping sickness in this area. The trypanosome infection rates in tsetse were 1.75% in zone I, 1.00% in zone II and 1.82% in zone III. The species trapped in zone I and II was G.f.fuscipes, which was also predominant in zone III with few catches of G.pallidipes. The infections were detected in female tsetse that were more than three weeks old. There were no infections among the male tsetse in all the zones which has been attributed to the low average age of the males (11days or less), implying that the males don’t live long enough to allow the infection to mature. The tsetse feeding preference studies have supported the major sleeping sickness transmission cycles for the three zones as suggested above. A total of 394 tsetse blood-meals were analysed to identify the host that was the source of the blood meal. Hosts for 75.64% of the bloodmeals were identified and at 26.4%, cattle were on average the most preferred host for G.f.fuscipes in southeastern Uganda (all the three study zones combined). Of the bloodmeals analysed, 55.1% were identified as having come from domestic animals and humans. This study has recorded large percentages of domestic animals as the major hosts for tsetse in all the three zones. There were however differences in the contribution of individual hosts in the three zones, with pigs being the major host in zone I, the monitor lizard and cattle for zones II and III. The results also indicate that under natural circumstances, G.f.fuscipes will feed on the available hosts in a given ecological environment. The preferred hosts were mainly cattle, pig, monitor lizard, sheep, goat, human, dog and chicken. This study has indicated that the domestic animal-tsetse-human cycle is the major sleeping sickness transmission cycle in all the three zones, the differences being the animals acting as the disease reservoirs in the three sleeping sickness foci (Agroecological zones) of southeastern Uganda.