Response of four indigenous cattle breeds to natural tsetse and trypanosomosis challenge in the Ghibe valley of Ethiopia.

A comparative study on the response of four indigenous cattle breeds of Ethiopia, namely Abigar, Horro, Sheko and Gurage, to natural challenge of trypanosomosis in the Tolley-Gullele area of the Ghibe valley has been undertaken from August 2000 until August 2004. Fifty female yearlings each of Horro, Sheko and Abigar and 31 of the Gurage were purchased from their natural habitats and introduced in to medium to high tsetse-trypanosomosis challenge area of the Ghibe valley. While the natural habitats of first three breeds are naturally infested with tsetse flies and trypanosomosis, that of the Gurage is known to be very minimal, if any, and hence the Gurage breed was used in this study as the known susceptible breed. During the study animal health, production performance and tsetse fly situation were monitored monthly. The Sheko breed has manifested very significantly (p<0.001) high overall average packed cell volume (PCV) values (25%) compared to that of Abigar (24%), Horro (23%) and Gurage (22%). It also had the lowest mean trypanosome prevalence rate of 9% against 23% of Horro, 26% of Abigar and 27% of Gurage, and the least number of Berenil treatments (1.36) compared to Abigar (4.0), Horro (4.6) and Gurage (6.7). While the Abigar manifested high sensitivity and frequent death to PCV depression, the Horro showed strong resilience to PCV depression and better response to Berenil treatment assistance. At this stage the Sheko breed was also found to be equal to the other breeds in its reproductive performance. These results need to be substantiated with further in-depth investigation including immune response, animal behavior and environmental influences.

Variations in packed red cell volume and trypanosome prevalence and relationships with reproductive traits in east African Zebu cows exposed to drug-resistant trypanosomes.

Approximately 320 East African Zebu cows over 36 months of age were monitored monthly from 1986 to 1992 in nine village herds in an area of high trypanosomiasis risk in southwest Ethiopia where there was resistance to all available trypanocidal drugs. Cows were individually treated with diminazene aceturate, either when they were detected parasitaemic and their packed red cell volume (PCV) decreased below 26%, or when they showed clinical signs of trypanosomiasis. The average annual monthly trypanosome prevalence was 24% and the number of treatments of diminazene aceturate per cow per year was 3.1, both of which increased with age. Mean PCV decreased and mean trypanosome prevalence increased during lactation. There was a significant linear association between the time detected parasitaemic during the first 150 days of lactation and calving interval. When corrected for frequency of parasitaemia and treatment there was also an average reduction of 8.4 +/- 2.6 days in calving interval per % unit increase in PCV. Age at first calving decreased by 0.44 +/- 0.26 months per % unit increase in mean PCV maintained between 24 and 30 months corrected for parasitaemia and treatment. The percentage of pregnancies terminating in abortions significantly increased from 6.8 +/- 1.0% to 10.4 +/- 1.3% when cows detected parasitaemic at least once during the last three months of pregnancy were compared with cows not detected parasitaemic. The largest increase to 19.4 +/- 4.3% was in cows with low mean PCVs < 22%. It was concluded that cows which were able to maintain higher than average PCVs when parasitaemic showed superior reproductive performance than those with lower than average PCVs.

Long-term occurrence of Trypanosoma congolense resistant to diminazene, isometamidium and homidium in cattle at Ghibe, Ethiopia.

Ten trypanosome isolates were collected at random from cattle at Ghibe, Ethiopia, in February 1993 and all shown to be savannah-type Trypanosoma congolense. When inoculated into naïve Boran (Bos indicus) calves, all 10 isolates were resistant to diminazene aceturate (Berenil), isometamidium chloride (Samorin) and homidium chloride (Novidium) at doses of 7.0 mg/kg body weight (b.w.), 0.5 mg/kg b.w. and 1.0 mg/kg b.w., respectively. In order to determine whether this multiple-drug resistance was expressed by individual trypanosomes, clones were derived from two of the isolates and characterised in mice for their sensitivity to the three compounds; by comparison to drug-sensitive populations, the two clones expressed high levels of resistance to all 3 trypanocides. In experiments to characterise the uptake kinetics of [14C]-Samorin, the maximal rates of uptake (Vmax) for 4 Ghibe isolates ranged from 9.2 to 15.0 ng/10(8) trypanosomes/min. In contrast, Vmax for the isometamidium-sensitive clone T. congolense IL 1180 was 86.7 +/- 8.6 ng/10(8) trypanosomes/min. Lastly, molecular karyotypes were determined for eight isolates: seven different chromosome profiles were observed. These data indicate that in February 1993 there was a high prevalence of drug-resistant trypanosome populations with different chromosome profiles in cattle at Ghibe. Since a similar situation existed at the same site in July 1989, this suggests that the drug-resistance phenotype of trypanosomes at Ghibe had not altered over a 4 year period.

Epidemiology of bovine trypanosomiasis in the Ghibe valley, southwest Ethiopia. 1. Tsetse challenge and its relationship to trypanosome prevalence in cattle.

In this, the first of a series of papers on the epidemiology of bovine trypanosomiasis in the Ghibe valley, southwest Ethiopia, the tsetse populations and their relationships to the prevalence of trypanosome infections in cattle are described. The tsetse challenge to cattle at two sites sites in the area was estimated as the product of tsetse relative density and the trypanosome infection rate in flies. The proportion of feeds taken by tsetse from cattle was also considered. Three tsetse species were detected in the area, Glossina pallidipes, G. fuscipes and G. morsitans submorsitans. A significant correlation (r = 0.60, P < 0.001) was observed between the mean monthly estimates of tsetse challenge due to G. pallidipes and the prevalence of trypanosome infections in cattle the following month at one site, whilst at the other, no significant relationship was observed (P = 0.08). The tsetse density at both sites showed seasonal changes which were related to the monthly rainfall. Finally, variations in tsetse density appeared to be the main factor responsible for variation in tsetse challenge and thus trypanosome prevalence in cattle.

Epidemiology of bovine trypanosomiasis in the Ghibe valley, southwest Ethiopia. 2. Factors associated with variations in trypanosome prevalence, incidence of new infections and prevalence of recurrent infections.

An average of 840 East African Zebu cattle from nine herds in the Ghibe valley, southwest Ethiopia were monitored from January 1986 to April 1990. Each month blood samples were collected for analysis of packed red cell volume (PCV) and detection of trypanosomes. Animals found to be parasitaemic and with a PCV less than 26% were treated with diminazene aceturate at a dose of 3.5 mg/kg body weight. The majority of infections were associated with Trypanosoma congolense (84% of infections in adult cattle and 71% in cattle less than 24 months of age), and the mean percentage of adult animals detected parasitaemic 1 month after treatment of an infection with T. congolense was 27%. In order to assess possible existence of drug resistance, a model was applied which allowed monthly incidences of new infections to be distinguished from recurrent infections. This model showed that the monthly incidence of new infections of T. congolense in adult cattle increased significantly from 11% in 1986 to 24% in 1989 following a concomitant increase in the tsetse challenge. The corresponding increase in overall prevalence of T. congolense was from 17% to 38% and the mean prevalence of recurrent infections increased significantly from 6% to 14%. These findings ruled out the possibility that the high prevalence of trypanosome infections in cattle was due only to a high tsetse challenge and pointed to the existence of T. congolense populations which expressed resistance to diminazene. There were variations associated with season, herd, age and sex in the incidence of new infections, prevalence of recurrent infections and relapse to treatment.

Epidemiology of bovine trypanosomiasis in the Ghibe valley, southwest Ethiopia. 3. Occurrence of populations of Trypanosoma congolense resistant to diminazene, isometamidium and homidium.

In July 1989, blood samples were collected from parasitaemic cattle in the Ghibe valley, Ethiopia, frozen in liquid nitrogen and transported to Nairobi, Kenya. Twelve of the stabilates were inoculated into individual Boran (Bos indicus) calves and characterised for their sensitivity, in turn, to diminazene aceturate (Berenil), isometamidium chloride (Samorin) and homidium chloride (Novidium). All 12 stabilates produced infections which were shown to be Trypanosoma congolense and resistant to treatment with diminazene aceturate at a dose of 7.0 mg kg-1 body weight (b.w.). Eleven of the infections were also resistant to isometamidium chloride at a dose of 0.5 mg kg-1 b.w. and homidium chloride at a dose of 1.0 mg kg-1 b.w. The drug-sensitivity phenotypes of three of the same isolates were also determined in goats which were each treated with only one of the three trypanocides: all expressed the same phenotypes as the populations expressed in the aforementioned Boran calves. Five clones were derived from one of the isolates which expressed a high level of resistance to all three trypanocides; each clone expressed high levels of resistance to all three trypanocides when characterised in mice. Thus, the multi-resistance phenotype of the parental isolate was associated with expression of mutli-resistance by individual trypanosomes. Finally, molecular karyotypes and electrophoretic variants of six enzymes were determined for seven and eight of the isolates, respectively. Six different karyotypes were observed and all eight of the latter isolates belonged to different zymodemes, indicating that the multi-resistance phenotype at Ghibe was associated with many genetically distinct populations.

The incidence of new and the prevalence and persistence of recurrent trypanosome infections in cattle in southwest Ethiopia exposed to a high challenge with drug-resistant parasites.

A method is described for calculating new infection incidence from monthly field data collected between April 1994 and February 1998 from an average of 770 Ethiopian Highland Zebu cattle maintained under traditional management in the Ghibe valley, southwest Ethiopia and exposed to a high challenge with drug-resistant parasites. Each month cattle with a packed cell volume (PCV)<26% and detected as parasitaemic, or cattle showing clinical signs of trypanosomosis, were treated with diminazene aceturate at 3.5 mg/kg body weight. An infection was defined as a new infection if it was preceded by 2 previous months in which both samples had a PCV>/=26% and were not detected with trypanosomes. Using this definition the average monthly incidence of infections of Trypanosoma congolense in cattle over 36 months of age was 13.3%, and the prevalence of recurrent infections 13.0%. Assuming that an animal had recovered from infection when PCV again returned to 26% without parasites being detected, mean persistence of infection was 3.8 months (median between 2 and 3 months). In contrast, T. vivax infections were susceptible to diminazene. The incidence of T. vivax infections in adults was lower than for T. congolense (2.8%), and they were less pathogenic (mean reduction of 3.1% units of PCV due to T. vivax infection compared with 4.6% units for T. congolense). Also, fewer cases were treated. Calves were first detected parasitaemic at an average age of 8.8 months and their infections persisted longer than those in adults. The effect of age on incidence of infection was not significant beyond 15 months of age. Adult male cattle appeared to be more susceptible to T. congolense infection than adult female cattle.

Use of insecticide-impregnated targets for the control of tsetse flies (Glossina spp.) and trypanosomiasis occurring in cattle in an area of south-west Ethiopia with a high prevalence of drug-resistant trypanosomes.

In the Ghibe valley, south-west Ethiopia, a tsetse control trial using deltamethrin-impregnated targets was started in May 1990. The mean relative density of the main vector, Glossina pallidipes, fell from 2.1 flies per trap per day in the 12 months prior to introduction of tsetse control to 0.41 flies per trap per day in the 12 months after tsetse control was initiated. The annual mean prevalence of Trypanosoma congolense infections in cattle fell from 32% in the 2 years before tsetse control to 13% in the 2 years following deployment of targets. The largest reduction occurred in the first quarter of 1991 when the mean monthly trypanosome prevalence was 5%. There was also a decrease of approximately 75% in the estimated rate of relapse of trypanosome infections in cattle after treatment with diminazene aceturate. However, in June 1991, socio-political disturbances occurred in Ethiopia and were associated with substantial thefts of targets. Following these thefts, the mean relative density of G. pallidipes rose from 0.41 flies per trap per day in the period May 1990-April 1991, to 1.29 flies per trap per day in the period April 1992-March 1993. Associated with this rise, the mean trypanosome prevalence in cattle increased from 13% in the period May 1991-April 1992 to 28% in the period May 1992-April 1993. This was similar to the mean trypanosome prevalence in cattle during the pre-control period. Thus, while effective tsetse control methods can be used to reduce the transmission of trypanosomes their long-term impact is dependent on their sustainability.

Estimating the effects of tsetse control on livestock productivity--a case study in southwest Ethiopia.

A tsetse control campaign was started in January 1991 using a synthetic pyrethroid cypermethrin 'pour-on' applied monthly to cattle exposed to high levels of drug-resistant trypanosomes in the Ghibe valley of southwest Ethiopia. In December 1992, a cost-recovery scheme was introduced, and thereafter farmers paid for treatment. An average of 100 village Ethiopian Highland Zebu cattle were monitored monthly from March 1986 to February 1997. Individual animals in this herd were treated with diminazene aceturate (Berenil, Hoechst, Germany) at 3.5 mg/kg when trypanosomes were detected and their packed cell volume was less than 26%. Superimposed on this systematic trypanocidal chemotherapy, control of tsetse resulted in average reductions from 1992 to 1996 of 95% and 75% in the mean relative densities of tsetse and biting flies, respectively, and of 63% in the prevalence of trypanosomal infections in cattle. Despite these reductions, there was no significant increase in the body weight of the cows, calving rate or the mean body weight of calves at 12 months of age. There was, however, an average decrease of 57% in calf mortality (including still births) by 12 months of age, an increase of 49% in the ratio of live calves under 12 months of age to cows over 36 months of age, and an increase of 8% in the body weight of adult males.

Use of deltamethrin 'pour-on' insecticide for the control of cattle trypanosomosis in the presence of high tsetse invasion.

A deltamethrin 'pour-on' insecticide was applied monthly to over 2000 cattle exposed to a high challenge of drug-resistant trypanosomes and high tsetse re-invasion pressure in the Ghibe valley, south-west Ethiopia. Blood samples were taken monthly from an average of 760 cattle for determination of PCV and presence of trypanosomes. The area of the valley is approximately 350 km2 and the cattle grazed in roughly four locations covering about a quarter to half of the area. Two years before the trial commenced, Glossina morsitans submorsitans Newstead (Diptera: Glossinidae) began to invade the valley. Despite the use of the pour-on the mean apparent density of G. m. submorsitans continued to rise, and, during the 4 years of tsetse control, was more than three-fold higher than that recorded during the previous 18 months. Over the same period there was little change in the apparent density of Glossina pallidipes Austen (Diptera: Glossinidae). By contrast, the mean monthly prevalence of trypanosome infections in cattle over 36 months of age decreased from 38.3 to 29.0%, the incidence of new infections decreased from 26.6 to 16.0% (a reduction of 40%), and packed cell volume in cattle increased from 21.7 to 24.1%. Evidence of a change in apparent parasite transmission rate was demonstrated by regression of infection incidence in cattle on the logarithm of apparent density of G. m. submorsitans. Before the trial started the regression coefficient was 45.8 +/- 6.3 and this reduced to 9.2 +/- 2.5% incidence per log(e) (flies/trap/day) during the period of tsetse control. It was concluded that this indicated reductions in tsetse numbers in the immediate vicinities of cattle in a way that was not reflected in overall tsetse catches. Nevertheless, the comparatively high levels of trypanosome prevalence that persisted in the cattle demonstrates that, where invasion prevalence is high, treatment of small pockets of cattle will not eradicate tsetse. To achieve more significant reduction in trypanosome prevalence in cattle, integrated methods of control utilizing target barriers in the major routes of invasion will be needed.