EPIDEMIOLOGICAL IMPLICATIONS OF TICK-BORNE DISEASES IN SMALLHOLDER DAIRY PRODUCTION IN SOUTHEAST UGANDA FOLLOWING TSETSE AND TRYPANOSOMOSIS CONTROL 

CONSEQUENCES EPIDEMIOLOGIQUES DES MALADIES TRANSMISES PAR LES TIQUES DANS LES PETITES EXPLOITATIONS  DE BETAIL LAITIER AU SUD-EST DE L’OUGANDA,  APRES LE CONTROLE DES TSETSE ET DE LA TRYPANOSOMOSE

C.P.Otim, D.W. Kakaire, C.M.B. Ssekitto, Barasa & Wejuli

Livestock Health Research Institute, P.O. Box 96, Tororo, Uganda

Résumé

            Une étude longitudinale a été menée dans les districts de Bugiri et de Busia en Ouganda, d’août 2001 à mai 2002, suite au contrôle des tsétsé et de la trypanosomose, afin de déterminer la prévalence d’anticorps contre les maladies transmises par les tiques et d’établir le lien entre la prévalence et l’incidence des maladies transmises par les tiques, et l’âge auquel les veaux sont menacés par les maladies transmises par les tiques. En moyenne, 65 et 116 bovins, respectivement de Bugiri et de Busia, ont fait l’objet d’une surveillance pendant l’étude. La mortalité a été utilisée comme indicateur de l’incidence de maladies transmises par les tiques. Sur les 148 échantillons de sérum testés à l’aide de la technique ELISA, 73,2 %, 80,5 %, 39,6%, 57,3% et 49,7 % des bovins avaient des anticorps respectivement contre Theileria parva, T. mutans, C. ruminantium, A. marginale et B. bigemina. Les taux de prévalence de l’anticorps contre T. parva, aux mois de décembre 2001, de mars et de mai 2002 étaient respectivement de 53,3 %, 63 % et 65,5 %. Le nombre de bovins porteurs d’anticorps contre T. parva à Busia était moins élevé que celui de Bugiri. Sept sur les 19 veaux âgés de 2 à 4 mois sont morts des suites de la Fièvre de la Côte-Est (ECF), et quatre bovins adultes de race croisée sont morts à Bugiri. Il est évident que le taux de prévalence des maladies transmises par les tiques est élevé chez les bovins de la zone d’étude. La tranche d’âge la plus menacée par les maladies transmises par les tiques est celle de 2 à 6 mois. La lutte contre les tiques à l’aide d’acaracides a réduit le nombre de bovins affectés par les maladies transmises par les tiques. Il est, par conséquent, recommandé d’adopter les acaracides à double fin pour lutter à la fois contre les tiques et les tsétsé dans les districts de Busia et de Bugiri. Des efforts devront être faits pour évaluer l’impact de ces technologies avant de les vulgariser, de préférence à travers l’adoption d’une approche communautaire pour encourager la pleine participation des éleveurs.

Summary

            A longitudinal study was carried out in Bugiri and Busia districts of Uganda from August 2001 to May 2002, following tsetse and trypanosomosis control, to determine the antibody prevalence of tick-borne diseases (TBD), establish the relationship between prevalence and tick-borne disease incidence and the age at which calves are a risk of tick-borne diseases. On average 65 and 116 cattle in Bugiri and Busia respectively were followed in the study. Mortality was used as an indicator of tick-borne disease incidence. Of the 148 serum samples tested using ELISA, 73.2%, 80.5%, 39.6%, 57.3%, 49.7% of the cattle had antibodies against Theileria parva, T. mutans, C. ruminantium, A. marginale and B. bigemin, respectively.  T. parva antibody prevalence in December 2001;  March and May 2002 was 53.3%, 63.0% and 65.5% respectively.  The number of cattle carrying T. parva antibody prevalence in Busia was lower than those in Bugiri. Seven out of 19 calves aged between 2-4 months died from East Coast Fever (ECF) and 4 cross-bred adult cattle died in Bugiri. It is evident that the prevalence of TBDs is high among cattle in the study area. The age group most at risk of TBDs is 2 – 6 months of age. Tick control using acaricides reduced the number of cattle affected by TBDs. It was therefore recommended that use of dual purpose acaricides for controlling both ticks and tsetse be adopted in Busia and Bugiri districts. However, efforts should be made to assess the impact of these technologies before they are disseminated, preferably through adopting community-based approach to encourage full participation of farmers.

1.         Introduction

            South Eastern (SE) Uganda, where Farming in Tsetse controlled Areas (FITCA) project is based consists mainly of agro-pastoral farming. The majority of the cattle are indigenous local zebu cattle. The very few smallhoder dairy farms have crossbred and few pure exotic cattle.  Bugiri and Busia curved out of Iganga and Tororo districts have very few exotic and crossbred cattle.  Like in other districts, increased production and productivity of livestock in cross-bred cattle is limited among others by widespread incidence of animal diseases of which ticks and tsetse together with the diseases they transmit rank high.

            Ticks and Tick-borne diseases (TBDs) cause economic losses to individual farmers and   government.  Losses from ticks and TBDs vary in different areas and breeds and are attributed to drop in milk yields debility, morbidity and mortality (Otim, 1989).  Animals that recover, suffer from weight loss, produce low milk yield, provide less draught power and may experience reduced fertility and delays in reaching maturity (Mukhebi et al., 1992).  Important issues concerning TBDs and the control measures required to reduce livestock production losses created by them are centered on the economics of the various control measures. For Uganda, increased information concerning the economics of the ticks and TBD control is required to provide better recommendation to farmers (Moran, 1996)

            Control measures for diseases are usually derived from their significant epidemiological parameters and patterns (Brown 1997).  The epidemiology of TBDs in most of the districts in S.E. Uganda is unknown. This study was therefore carried out to evaluate the epidemiological implications of TBDs on smallholder dairy production systems following Tsetse and Trypanosomosis control hence identifying appropriate control strategies.

2.         Materials and Methods

2.1       Study site

            The study was initially planned for Tororo district. However, after consultation with the District Veterinary Officer, Tororo; area Veterinarians and some farmers, it was decided that Tororo district would not be suitable for the project.  This was because immunisation against ECF had been extensively carried out in cross-bred and exotic cattle in Tororo district.  The small districts of Busia and Bugiri bordering Tororo, which had a few crossbred cattle, were found suitable for this study.

            District extension staffs together with farmers were sensitized through 2 meetings.  Farmers were then identified and selected on the basis of their interest in improving their animal production and productivity.

2.2       Methodology

2.2.1.   Cattle for study

            The age of cattle selected for study varied from calves (0-12 months) for indigenous zebu and all ages for exotic and cross-bred cattle breeds. All cattle selected for the study were ear tagged. The majority of the animals were grazed communally, while others were either tethered or zero-grazed.  Farmers carrying out tick and tsetse control using various acaricides were identified.

2.2.2.   Sampling

            Blood samples were collected from the jugular vein using non-heparinised vacutainers. Haematocrit centrifugation test (HCT) was performed to determine the prevalence of trypanosomosis.  The packed cell volume (PCV) for each animal was measured (Murray, 1977et al.).  Serum samples were separated and ELISA test was performed to determine the antibody prevalence to TBDs (Katende et al., 1998).  ELISA test was carried on samples collected in August, December 2001 and March, May 2002. Antibody ELISA test was conducted for all haemoparasites namely: Theileria parva, T. mutans, Cowdria ruminatium, Babesia bigemina, Anaplasma marginale, Trypanosome brucei, T. vivax and T. congolense for all blood samples collected during the baseline survey, August 2001.  However, for subsequent samples, tests were only conducted for T. parva, B. bigemina and A. marginal.  The preportions of cattle carrying antibodies to either T. parva, B. bigemina or A. marginale alone or in combination in different cattle age groups were compared and their significant difference determined using a Chi-square test. The same comparison was made between cattle receiving either tick control alone, both tick and tsetse control and no tick control at all. Blood smears were made and stained with Giemsa and examined under oil immersion for haemoparasites.

2.2.3.   Monitoring

            The district extension officers carried out clinical monitoring of the cattle fortnightly while laboratory staff monitored them monthly.  Upon receiving a report of a sick animal a follow-up was made by the district extension veterinary officers. Physical examination was conducted, temperatures taken and tentative diagnosis made and where necessary, blood smears were collected. The extension veterinary officers when informed in time carried out postmortem examination on dead animals. The incidence of TBDs cases were reflected by the mortality rate due to tick-borne diseases and frequency of treatments.

3.         Results

            Altogether 21 farms were selected, 8 from Bugiri and 13 from Busia.  All farms grazed their animals communally. But those with exotic and cross-bred cattle supplemented the grazing with cut and carry fodder provided in the evening.  The majority of the farms had small herds. 

            Cattle tagged at the beginning of the study were 71 in Bugiri and 77 in Busia of which 25 and 17 were exotic and crossbred respectively.  By the end of the study in May, there were altogether 65 and 116 cattle in Bugiri and Busia respectively (Table 1).  Over the study period, there were changes in the herds under study; calves were born, some cattle died, got transferred or were sold (Table 2).

Table 1.           No of cattle in the study

Table 2.      Experimental animal dynamics

            At the beginning of the study, 25% (n=2) and 12.5% (n=1) farms in Bugiri used Supona and Decatix for tick control respectively.  By the end of the study, 2 (25%) farms used Supona, 1 farm used Amitraz, and 1 farm used Decatix and 1 farm used spot-on for tick control in Bugiri District.  Meanwhile in Busia district 10 of 13 farms  (77%) used Ectobanâ (Cypermethrin and Cymiazole) and 1 farm used Triatixâ (Amitraz) at the beginning of the study. Decatixâ, Spot-onâ and Ectobanâ were used for both tsetse and tick control.  Altogether 12 farms (92.3%) practiced control of both tsetse and ticks (Table 3)

Table 3.      Vector control

            There were 34 (23%) , 41 (27.7%) and 73 (49.3%) cattle undergoing no tick control, tick control alone or tick ad tsetse control at the beginning of the study respectively. However at the end of the study, 38 (21%), 58 (32%) and 85 (47%) cattle with no tick control, tick control only or tick and tsetse control showing overall increase of  2% of cattle getting tick control.

            Of the 148 serum samples tested using ELISA, 73.2% were positive for Theileria parva antibodies, 80.5% for T. mutans, 39.6% for C. ruminantium, 57.3% for  A. marginale, 49.7% for B. bigemina, 28.8% for  T. brucei,  43.5% for T. vivax and 11% for T. congolense T. parva antibody prevalence in December  2001;  March and May 2002 was 53.3%, 63.0% and 65.5% respectively (Table 4).  The number of cattle carrying T. parva antibody prevalence in Busia was lower than those in Bugiri. 

Table 4. Percentage of cattle with TBD antibodies at the beginning (baseline survey) of the study.

The overall trend of the prevalence of antibodies against T. parva, B. bigemina, A. marginale in cattlethrough the study period is shown in Fig. 1

            Meanwhile, the prevalence of antibodies against T. parva, B. bigemina, A. marginale in cattle and overall prevalence of antibodies against TBDs at the beginning of the study and subsequent periods after the commencement of study is shown in Tables 5a, 5b, 5c and 5 d.

Table 5a: Percentage (in brackets) of cattle of different age groups carrying antibodies against T. parva, B. bigemina and A. marginale at the beginning of the study (baseline survey), August  2001.

Table5b: Percentage (in brackets) of cattle of different age groups carrying antibodies against T. parva, B. bigemina and A. marginale at the beginning of the study at December, 2001

Table5c: Percentage (in brackets) of cattle of different age groups carrying antibodies against T. parva, B. bigemina and A. marginale at the beginning of the study at March, 2002

Table5d Percentage (in brackets) of cattle of different age groups carrying antibodies against T. parva, B. bigemina and A. marginale at the beginning of the study at May, 2002

            Calves aged between 0 - 2 months of age at the beginning of the study had a lower prevalence of antibodies T. parva as compared to other age groups: 2-4 months (P<0.05,  X2 =4.5);  for 4-6 and 6-12 months (P<0.01; X2 = 7.2 and 8.9 for 4-6 and 6-12 months respectively) and adults (P<0.05, X2 =5.6).  As the tick control intervention progressed, the prevalence of antibodies in calves below 2 months decreased,  but maintaining a  highly significant difference (P<0.01) with lower prevalence of antibodies as compared to other age groups up to the 4th month of study. But from March, 2002 (7 months after the intervention) on ward, the prevalence of  T. parva antibodies in calves of less than 2 months was similar to 2-4 months calf age group,  but not with calves beyond 4 months of age and adult cattle. Also the calves of 2-4 months of age had a highly significant T. parva antibody prevalence (P<0.01, X2 =10.5) at the beginning than at the end of study (May, 2002; 10 months after intervention). For calves beyond 4 months of age, there was no significance difference in prevalence of T. parva antibodies at the beginning and also at the end of the experiment.

            The prevalence of antibodies to B. bigemina, had dissimilar pattern to T. parva antibody prevalence across age groups at the beginning of study. Calves of 2-4 months had a significantly lower antibody  prevalence than any age group (P<0.05; X2 =3.7 for calves 0-2 months; X2 =5 for calves 4-6 months; X2 =4.4 for calves 6-12 months and X2 =5.6 for adults). There was a sudden drop of antibodies to B. bigemina at 2-4 months of age (Table 6) thereafter calves attained a constant antibody prevalence beyond 4 months of age. On 4-7 months of tick control intervention, calves from 0-6 months had a similar antibody level against B. bigemina, with cattle beyond 6 months having significant antibody prevalence levels  (P<0.05).  However, at the end of the study, there was no significant difference (P>0.05) of Ab prevalence against B. bigemina across age groups. Also, by the end of study it was shown that there was highly significant difference (P<0.05, X2 =5) of prevalence of antibodies to B. bigemina, with high antibody prevalence being observed at the beginning for calves of 2-4 months of age.

            At inception of study, the prevalence of antibodies to A. marginale had a similar pattern to prevalence of  B. bigemina antibodies  across age groups with calves  of  2-4 months having lower levels than any other age group ((P<0.01,  X2 =6.7 for calves 4-6 months and  X2 =7.1for adults) P<0.05; X2 =4.6  calves 6-12 months). By December, after intervention there was increase of antibodies to A. marginale with age. From March to May 2002 (7th to 10th month of intervention) there was no significant difference (P<0.05) for prevalence of antibodies to A. marginale across age groups. There was highly significant difference of prevalence of to A. marginale in adult cattle (P<0.01, X2 = 8.5) at the beginning than at the end of the study, being very high at the start of the study.

            There was a significant difference (P<0.05, X2  = 6.2) of prevalence of antibodies between cattle that had no tick control and the ones that had tick control alone at the beginning of the study. The same was true between cattle that had no tick control and those that had both tsetse and tick control at the beginning of study.  The cattle, which were not sprayed, had high prevalence of antibodies to TBDs at the beginning of study than both groups of cattle that were sprayed.

Table 6: Prevalence of antibodies against TBDs  (T.parva, B. bigemina and A. marginale combined) in cattle with different tick control treatments: tick control alone, both tick and tsetse control and no tick control.

            Similarly by the end of the study, there was a very highly significant difference in prevalence of antibodies to TBDs between cattle that had no tick control and those that had tick control (P<0.001, X2 =22.2). Also, at the end there was a very highly significant difference (P<0.001, X2 = 21) in prevalence of antibodies to TBDs between the cattle that had no tick control and those where both ticks and tsetse were controlled. On contrary, there was no significant difference (P>0.05, X2= 0.13) in prevalence of antibodies to TBDs between cattle under tick control alone and those under both tick and tsetse control.

            There was significant difference (P<0.05) in prevalence of antibodies against TBDs in cattle at the beginning of study and at the end of study under tick control alone. Also there was highly significant difference in prevalence of antibodies against TBDs in cattle at the beginning of study and at the end of study under control of both tsetse and ticks (P<0.01, X2=10.6).

            Mixed infection with T. parva/T. mutans/C.ruminantium/B.bigemina/A.marginale was detected in 18 (12.2%) cattle. At the same time 13 (8.7%) cattle carried antibodies to all the three Trypanosome species.  However, it was surprising that no cattle had antibodies to both T. brucei and T. congolense alone (Fig 2).

            No deaths were reported in 0-2 month old calves. However, seven out of 19 calves aged between 2-4 months died from East Coast Fever (ECF). Three died before any treatment, two died after oxytetracycline treatment and two after treatment with Butalex

            Two Cross-bred calves, one each from Busia and Bugiri aged 4-6 months died of ECF without treatment as the farmers reported the cases late while 9 recovered after treatment. Meanwhile two cross-bred calves aged 6-12 months suffering from anaplasmosis were treated and recovered.

            Among the adult cattle, 4 crosses in Bugiri suffered from ECF and 2 died of anaplasmosis complications while 3 crosses and 1 local adult cow died of anaplasmosis.  Of the treated cattle 22.2% died of ECF, however, this is only 4.9 of all the animals in the study (Table 7).

Table 7.           Age specific mortalities due to TBDs

Note: All mortalities were due to ECF cases except those marked  * which  were due to anaplasmosis

            The variation of the mean packed cell volume and prevalence of trypanosomosis with time during the study period were as shown in Fig. 3. There was a highly significant difference (P<0.001) in the mean PCV observed at the beginning of the study (Bugiri  25.9 and Busia 26 ) and at end of study (Bugiri 35 and Busia 40).

            Using HCT, 6 cattle in Bugiri had trypanosome infection and all cattle in Busia were negative.  In December, 2 trypanosome infection were detected in 2 animals both in Bugiri and Busia and this trend persisted in Busia in March but by May no trypanosome infections were detected in both districts ( see Fig. 3).

            Examination of 148 Giemsa stained blood smears at the start of the study revealed that only 20 of the animals had Theileria and 2.7% Trypanosoma parasites.

4          Discussion and conclusion

            Bugiri and Busia districts have had tsetse fly infestation for a long time.  However, farmers in Busia as compared to Bugiri were sensitized to the trauma caused by tsetse fly infestation and have at one time or the other been sensitized in their control.  The farmers in Bugiri on the other hand are more commercially orientated compared to Busia farmers.

            Spraying for tsetse and tick control was well accepted and practised in Busia with 84.6% farmers at the beginning of the study as compared to only 37.5% in Bugiri.  With sensitization provided by the study, two more farmers joined the exercise. Farmers used Supona and amitraz for controlling ticks alone; and used Decatix, Spot On and ectoban for controlling both tsetse and ticks. A majority of farmers (77%) of farmers in Busia used ectoban.

            The high prevalence of TBDs (T. parva, T. mutans, C. ruminantium, A. marginale. B. bigemina) and of trypanosome infections (T. brucei, T. vivax and T. congolense)(Table 4) as revealed by antibody ELISA is not surprising.  Not all farmers practiced tick and tsetse control.  Even those who practice, do it irregularly and inefficiently.  The persistently high T. parva prevalence in the two districts is in agreement with findings by Otim et al (1999) in which they reported that 67.1% of calves in dairy farms in 16 districts carried antibodies to T. parva.

            From what has been observed about the trend of the prevalence of antibodies against T. parva infection across age groups of calves and adult cattle (see Fig. 1 and Tables 5a,b,c&d), it was shown that under proper tick control, calves could  delay to acquire immunity up to 4 months of age due to low tick challenge as compared to 2 months when there is no tick control(5a). In terms of management, calves below age of 4 months under proper tick control, are more venerable to ECF challenge. Care needs to be taken to protect them against ECF. These calves under this age group can be protected by immunization against ECF using infection and treatment method. Alternatively, farmers should be advised to take keen interest in their calves and observe their calves for ECF signs when they are 2-4 months old and treat them because this is period when they are more likely to get T. parva infection.

            There was a sudden drop of antibodies to B. bigemina infection at 2-4 months of age (Table 5a), after which calves attained a constant antibody prevalence beyond 4 months of age at the beginning of the study. This drop could most likely be associated with the waning of maternal immunity to babesiosis. The calves could now start picking up the infection at natural tick challenge so that by 4 –6 months the calves could fully be protected against babesiosis. It was shown that with intensification of tick control all age groups were not sufficiently protected against babesiosis, indicating that endemic stability could have been lost. This finding was exhibited by lack of significant difference  (P>0.05) of antibody prevalence against B. bigemina across age groups by 10th month of intensive tick control observed during the study. The vector of B. bigemina: Boophilus decoloratus populations could severely been reduced by tick control intervention.

At the inception of the study, the prevalence of antibodies to A. marginale infection had a similar pattern to the prevalence of B. bigemina antibodies across age groups, with calves of  2-4 months having a lower level than other age groups. This drop could be explained due to waning of maternal antibodies. With intensification of tick control it was shown that the prevalence of antibodies to A. marginale infectiondecreased. Eventually, by the end of study there was no significant difference (P<0.05) in the prevalence of antibodies to A. marginale  infection across age groups implying that all cattle age groups had lost immunity against anapalasmosis. This could have grave consequences if tick control was suddenly relaxed leading to outbreaks of anaplasmosis when the vector tick population (B. decoloratus) builds up.

            In general, there were significantly more cattle without tick control carrying antibodies to TBDs at the beginning of the study (Table 7) than cattle with tick control alone or both tsetse and tick control. Later, by the end of the study, the difference (P<0.001)  between the prevalences of antibodies to TBDs even became bigger between cattle that were not sprayed with acaricides and  those that were sprayed. The level of antibody prevalence in both groups of cattle that were sprayed had a highly significant difference (P<0.01) in prevalence of antibodies to TBDs at the beginning and at end of the study, implying that tick control regimes (tick alone and both tsetse and ticks) were effective in reducing tick populations hence TBDs. It was shown either control of ticks alone by spraying cattle with Amitraz and Supona or spraying cattle with Decatix, Spot On and Ectoban for controlling both tsetse flies and ticks were equally effective in reducing the prevalence of antibodies to TBDs hence TBD’s exposure rates. Overall, it was shown that improved spraying mostly affected the B. bigemina and A. marginale infections since the vector B. decoloratus is known to be sensitive to tick control.  These observations, suggest that it is therefore better to adopt the use of dual purpose acaricides that control both tsetse and ticks. However, before, their use could be adopted, a benefit cost analysis should be conducted.

            The extent of mixed infection as indicated in Fig.2 is not surprising as vectors for all the parasites were available in the farms studied. Our failure to detect mixed infection with T. brucei / T .congolense is in agreement with earlier reports. Mixed infection with T. vivax / T. brucei and T. vivax / T. congolense but none with T. brucei / T. congolense in cattle have been reported by Magona et. al. , (1999) and Magona et., al. (2000).

            Cattle presented sick had mainly ECF and this affected animals up to 1 year of age for both exotic, crossbred and local Zebu and in addition adult exotic/cross-bred cattle came down with both ECF and anaplasmosis (Table 7).  Anaplasmosis affected cross-bred adult cattle mainly.  It is possible local cattle are usually exposed to infection early in life, when they acquire immunity.

            The low numbers of cattle with trypanosome is as a result of practicing prophylactic treatment for trypanosomosis and helminthosis every three months in almost all the farms. The incidence of animal trypanosomosis declined as revealed by improved PCV and declining prevalence of trypanosomosis (Fig. 3); and mortality due to ECF and anaplasmosis (Table 7). The growth rate and health of the calves improved compared to others in the neighbourhood as shown by improvement of PCV (Fig.3). 

            The farmers (84.6% farms) in Busia participate more in the control of both tsetse and ticks as compared to only 37.5% of farms in Bugiri. This implies more efforts should be spent in sensitising and recruiting more farmers in Bugiri to participate in the study. Community-based approach should be adopted so as to reduce overall costs. Overall, this study has been termed by the extension officers as a good learning platform for the farmers who have shown a lot of interest.  In Busia farms in the study have adopted demonstration sites for other farmers in the sub-counties involved.  The farmers have learnt to consult extension staff on the treatment of their sick animals. More funds are being sought to expand this study using a Busia model.

5.         Recommendation

            Although the results obtained in this study are not conclusive, it is evident that the prevalence of TBDs is high among cattle in the study area. The age group most at risk to TBDs is 2 – 6 month of age. Tick control using acaricides reduced the number of cattle affected by TBDs.

It is therefore recommended that: -

1. The use of dual purpose acaricides for controlling both ticks and tsetse should be adopted in Busia and Bugiri districts.
2. Efforts should be made to disseminate these technologies after their impacts have been studied
3. Community-based approach for participation of farmers should be adopted when these technologies are being transferred to farmers
4. More studies with a longer period of observation preferably 18-24 months is recommended.

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