PERSISTENCE OF OUTBREAKS OF HAEMORRHAGIC T. VIVAX INFECTION IN CATTLE IN EASTERN UGANDA AND IMPLICATION ON ITS EMERGENCY CONTROL IN VIEW OF DECENTRALIZED VETERINARY SERVICES 

PERSISTANCE DES EPIDEMIES D’INFECTION HEMORRAGIQUE DE T.VIVAX CHEZ LES BOVINS A L’EST DE L’OUGANDA ET CONSEQUENCES SUR SON CONTROLE D’URGENCE EN VUE DE LA DECETRALISATION DES SERVICES VETERINAIRES

J.W. Magona¹, J. Walubengo¹ & J.J. Odimim²

¹Livestock Health Research institute, P.O. Box 96, Tororo, Uganda.
²FITCA (Uganda), Ministry of Agriculture, Animal Industry and Fisheries, P.O. 531, Entebbe,Uganda

Résumé

            Une épidémie d’infection hémorragique de Trypanosoma vivax a, de juillet à octobre 2004, frappé de nouveau le district de Tororo, en Ouganda, qui est infesté par Glossina f. fuscipes et G. pallidipes. La précédente épidémie avait sévi en 1997 dans les districts de Tororo et Mbale, à l’Est du pays. Au cours d’une enquête, 1.400 bovins sélectionnés dans 14 villages du district de Tororo ont été dépistés de la trypanosomose à l’aide d’une combinaison de tests HCT et BCT. L’épidémie a frappé trois villages où le taux de mortalité des bovins serait élevé : d’après les données recueillies dans un village, 29 troupeaux composés au début de 888 bovins n’en comptent plus que 33. Les bovins affectés présentaient, avant leur mort, des signes cliniques tels que le saignement des oreilles, l’amaigrissement prononcé, l’anémie, la faiblesse générale et l’hypertrophie des ganglions lymphatiques. L’infection trypanosomienne dominante chez les bovins dans les trois villages affectés était due à Trypanosoma vivax : dans le village de Gombe, T. vivax (17 %) et T. congolense (3 %) étaient présents chez 100 bovins testés, tandis que dans le village de Winyaka, T. vivax    (13 %) et T. congolense (3%) étaient présents, et le taux d’infection mixte (T. congolense/T. vivax) était de        2 % ; dans la zone d’Amori, T. vivax (22 %) et T. congolense (11 %) étaient présents, et le taux d’infection mixte (T. congolense/T. vivax) était de 4 %. Les facteurs qui influencent la réapparition de l’infection hémorragique à T. vivax doivent être bien compris pour prévoir et mettre en œuvre de promptes mesures de contrôle. Cependant, le plus inquiétant est que suite à la décentralisation des services vétérinaires en Ouganda, on a confié aux services publics des districts la responsabilité de lutter contre les tsétsé et la trypanosomose, sans leur procurer les ressources et la capacité nécessaires pour financer et mettre en œuvre la lutte d’urgence contre ces fléaux. Cette politique devra certainement être révisée pour que soient restaurées les mesures d’intervention rapide requises pour lutter contre de telles épidémies qui déciment les troupeaux bovins.

Summary

            Recently in July –October 2004, an outbreak of haemorrhagic Trypanosoma vivax infection in cattle occurred again in Tororo district of Uganda infested with Glossina f. fuscipes and G. pallidipes. The previous outbreak had occurred in 1997 in Tororo and Mbale districts of Eastern Uganda. In an investigation, 1400 cattle from 14 villages in Tororo district were screened for trypanosomosis using a combination of HCT and BCT. The outbreak occurred in 3 villages where cattle mortality was reported to be high: data from one village revealed that 29 herds that originally had a total of 888 cattle had been left with only 33. Affected cattle manifested bleeding through ears, experienced severe weight loss, had anaemia, weakness, and enlarged lymph nodes before death. The dominant trypanosome infection in cattle in the 3 affected villages was Trypanosoma vivax: Gombe village, T.v (17%) and T.c (3%) in 100 cattle tested. While in Winyaka village, T.v (13%), T.c (3%) and mixed infection (T.c/T.v)-2%, and Amori zone, T.v (22%), T.c (11%) and mixed infection (Tc/Tv)-4%. Factors that influence the re-occurrence of haemorrhagic T. vivax need to be understood in order to predict and institute prompt control measures. However, of more concern is that decentralization of veterinary services in Uganda has delegated the control of tsetse and trypanosomosis to local government in districts without resources and capacity to finance and implement emergency disease control. This policy may need to be revisited to re-instate rapid response required in the control of such outbreaks that decimate herds of cattle.

Introduction

            Haemorrhagic Trypanosoma vivax outbreaks have persisted in Eastern Uganda. The previous outbreak occurred in Tororo and Mbale districts in 1997 (Magona et al., 1997). Fatal, haemorrhagic T. vivax infection is characterized by bleeding through ears, severe weight loss, anaemia, weakness, enlarged lymph nodes and considerable mortality. Virulent and haemorrhagic forms of T.vivax infections have also been reported in dairy cattle at the Kenya Coast (Mwongela et al., 1981) and in local and exotic cattle in Somalia (Dirie et al., 1988). In this paper we describe the mortality that resulted from the recent outbreak and the associated prevalence of trypanosomosis amongst cattle herds in the affected villages in Tororo district, Uganda.

Materials and Methods

Affected areas

            The haemorrhagic T.vivax outbreak was reported in Amori village in Mulanda subcounty and in Nyabanja, Nyagoke, Mifumi and Senda villages in Kirewa subcounty of Tororo district, Uganda. Glossina f. fuscipes was the dominant species in these villages with scanty G. pallidipes (Magona et al., 2005).

Cattle sampling

            A total of 401 cattle of all ages presented by livestock owners at designated sites, were bled from the jugular and the blood was examined using both the Haematocrit centrifugation technique (Woo, 1969) and the Buffy coat technique (Murray et al., 1977) for trypanosomes. Trypanosome species identification was based on morphological differentiation on Giemsa-stained thin films. PCV was measured using a PCV reader (Hawksley, England).

Assessment of mortality

            Livestock owners were interviewed about the number of cattle that had died during the outbreak; cases that had previously had bleeding through ears, severe weight loss, anaemia, weakness, enlarged lymph nodes prior to death.

Control of the outbreak

            Control of haemorrhagic T. vivax outbreaks relies on mass treatment of cattle with trypanocidal drugs and prompt response is required to mitigate high mortality. However, it took one year for mass treatment to be conducted. While the outbreak began in July 2004, control was implemented in July 2005. The delay was due to lack of resources by the district to handle the outbreak as dictated by decentralization of veterinary services.

Data analysis

The proportion of anaemic cattle among the trypanosome-infected and non-infected cattle and their mean PCV were compared using the chi-square test and the Mann-Whitney U-test, respectively, performed in the computer programme Minitab (Minitab Statistical Software, Minitab Inc., Pennsylvania, U.S.A).  The 5% level of significance was used throughout.

Results

            A total of 158 livestock owners were interviewed in four villages. The 158 herds had previous 844 cattle of which 295 (35%) had died during the outbreak. The distribution of herd mortality rate among the cattle herds is shown in Figure 1. 65 herds out of 158 had not lost any cattle during the outbreak. The commonest herd mortality rate was 31-40% and 50 herds had had herd mortality rates of 50% and above.

            The prevalence of trypanosomosis among different cattle age groups is shown in Table 1. Yearlings (13-24 months old) had the highest prevalence of trypanosomosis (15.4%), followed by adult cattle (>24 months old) (11.8%) and calves (7-12 months old) (11.1%). Calves of up to 6 months old had the lowest prevalence of trypanosomosis (5.5%). The overall prevalence of 12.2% was found.

Figure 1: Distribution of herd mortality rate among cattle herds (n = 158) in areas affected by the haemorrhagic Trypanosoma vivax outbreak in Tororo district, Uganda, 2005

Table 1: Prevalence of trypanosomosis in different age groups of cattle in areas affected by the outbreak of haemorrhagic Trypanosoma vivax in Tororo district, Uganda, 2005

            The proportions of trypanosome infection due to the different trypanosome species are shown in Figure 2. Trypanosoma vivax was the dominant trypanosome species found and constituted 82% of the infections. Trypanosoma congolense constituted only 12% and mixed infection of T.vivax and T. congolense constituted only 6% of the trypanosome infections.

            Mean PCV of trypanosome-infected and non-infected cattle in affected areas are shown in Table 2. The mean PCV of trypanosome-infected cattle (17.9%) was significantly lower than that of non-infected ones (25.8%) (P < 0.001). In addition, the proportion of anaemic cattle among trypanosome-infected cattle (81.6%) was significantly higher than that of non-infected cattle (37.2%) (c2 = 34.6, d.f. = 1, P < 0.001).

Figure 2: Proportions of different trypanosome species found in cattle in areas affected by haemorrhagic Trypanosoma vivax outbreak in Tororo district, Uganda, 2005

Table 2: Mean packed cell volume of trypanosome-infected and non-infected cattle in areas affected by haemorrhagic Trypanosoma vivax outbreak in Tororo district, Uganda, 2005

            The prevalence of trypanosomosis and mean PCV of cattle according their gender and functional status are shown in Table 3.  Males had a significantly higher prevalence of trypanosomosis (17.8%) than females (9.5%) (c2 = 5.58, d.f. = 1, P < 0.05) and significantly lower mean PCV (23.7%) than females (25.4%) (P < 0.05). There was no significant difference in prevalence of trypanosomosis between lactating and non-lactating females (c2 = 0.1, d.f. = 1, P = 0.74) and in terms of mean PCV between lactating and non-lactating females (P = 0.55). Furthermore, there was no significant difference in prevalence of trypanosomosis between draught males and non-draught males (c2 = 0.80.1, d.f. = 1, P = 0.37) and in terms of mean PCV between draught males and non-draught males (P = 0.20).

Table 3: Prevalence of trypanosomosis in female and male cattle in areas affected by haemorrhagic Trypanosoma vivax outbreak in Tororo district, Uganda, 2005

Discussion

            In the present study, we report on an outbreak of haemorrhagic T.vivax infection that occurred in Tororo district, an area predominantly infested with G.f.fuscipes but with scattered pockets of G. pallidipes, where such outbreaks have persisted. This study has revealed a 35% mortality rate of cattle in affected areas, where cattle manifested bleeding through ears, severe weight loss, anaemia, weakness, enlarged lymph nodes prior to death. This clinical manifestation of bleeding from the ears has been associated with rupture of the anterior capillaries in one or both pinnae of infected cattle (Dirie et al., 1988).

            A high prevalence of trypanosomosis was noticed among animals older than 7 months: yearlings (13-24 months old), adult cattle (>24 months old) and calves (7-12 months old), probably because these age groups are the ones that are taken for grazing in tsetse-infested riverine environment (Magona et al., 2000). The trypanosome infections were predominantly due to T.vivax, implicitly suggesting a large proportion of them were the virulent and haemorrhagic forms. The fact that trypanosome-infected cattle had significantly lower mean PCV and higher proportion of anaemic cattle than non-infected ones, provided additional evidence that the T.vivax detected in infected cattle was responsible for the syndrome.  A fact observed previous in similar outbreak the area (Magona et al., 1997).

            Although blood loss is known to be more severe in lactating cows and breeding bulls (Dirie et al., 1988), there was no significant difference observed between lactating and non-lactating cows and between draught males and non-draught male (breeding bulls) in terms of prevalence and mean PCV. However, evidence suggested males were more affected than females since males had a significantly higher prevalence and lower mean PCV than females.

            Unlike the chronic milder disease caused by other forms of T.vivax East Africa (Stephen, 1970) and in Uganda in particular (Magona et al., 2003), the clinical disease caused by virulent and haemorrhagic forms of T.vivax progress rapidly decimates cattle herds. Hence it requires rapid response in terms of chemotherapy. This needs a health delivery system that responds quickly. However, the current government policy of decentralization of veterinary services in Uganda that has delegated the control of tsetse and trypanosomosis to local government in districts without resources to finance and implement emergency disease control, making delivery of health service inefficient. For example, control was instituted to curb the outbreak in affected areas one year after the outbreak was first reported. This was attributed to the long bureaucratic procedures involved. This calls for revisiting this policy in order to re-instate rapid response required when controlling such outbreaks that decimate herds of cattle.

Acknowledgement

            We wish to thank Geoffery Odyek, Joseph Muboli and Robert Wabyanga for their technical assistance. This paper is published with the permission of Director, Livestock Health Research Institute.

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