Preventive Veterinary Medicine 115 (2014) 64–68

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Estimated prevalence and risk factors associated with clinical Lumpy skin disease in north-eastern Ethiopia Birhanu Hailu a,b , Tadele Tolosa a,f,∗ , Getachew Gari c , Teshale Teklue a,d , Belay Beyene a,e a Department of Microbiology and Veterinary Public Health, College of Agriculture, Veterinary Medicine, Jimma University, PO Box 307, Jimma, Ethiopia b Semera University, Faculty of Veterinary Medicine, PO Box 132, Semera, Ethiopia c National Animal Health Diagnostic and Investigation Center, PO Box 04, Sebeta, Ethiopia d Alamata Agricultural Research Center, PO Box 56, Alamata, Ethiopia e Wollega University, College of Agriculture and Natural Resources, Shambu Campus, Shambu, Ethiopia f M-team and Mastitis and Milk Quality Research Unit, Department of Reproduction, Obstetrics, and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium

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Article history: Received 12 July 2013 Received in revised form 8 March 2014 Accepted 11 March 2014

Keywords: Afar Cattle Lumpy skin disease Herd level prevalence Risk factors Tigray Ethiopia

a b s t r a c t Lumpy skin disease (LSD) is one of the major livestock disease problems in most areas of Ethiopia. A questionnaire-based cross-sectional study was conducted from October 2011 to February 2012 in four selected districts of Afar and Tigray regions to estimate the herdlevel prevalence of LSD, and to assess its associated risk factors. Herd-owners were selected based on the willingness to provide information to complete the questionnaire. A total of 393 questionnaires were collected. Out of 393 herd-owners, 173 reported having LSD in their herds, giving an estimated herd- and animal-level prevalence of (44%, 95% CI: 37–50%) and (7.4%, 95% CI: 6–8%), respectively. Herd prevalence between regions and among the districts were significantly different (2 = 8, P < 0.01 and 2 = 9.9, P < 0.01), respectively. The risk factors of LSD occurrence were introduction of a new animal to the herd, herd size, and utilization of communal grazing and watering points. These management characteristics cannot be readily changed in the studied area, hence, disease control should rely on a greater use of effective LSD vaccines. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Lumpy skin disease (LSD) is a viral disease caused by Lumpy skin disease virus classified in the Capripoxvirus genus of the Poxviridae family (Kitching and Mellor, 1986). Different capripoxviruses are responsible for diseases of

∗ Corresponding author at: Jimma University College of Agriculture and Veterinary Medicine, Microbiology and Veterinary Public Health, PO Box 307, Jimma, Oromia, Ethiopia. Tel.: +251 471 115405/+251 917 804070(mob.); fax: +251 917 110934.. E-mail address: [email protected] (T. Tolosa). http://dx.doi.org/10.1016/j.prevetmed.2014.03.013 0167-5877/© 2014 Elsevier B.V. All rights reserved.

major economic importance in ruminants, and the Nettling virus is a prototype strain that causes LSD in cattle. Lumpy skin disease has a different geographical distribution from sheep and goat pox, suggesting that cattle strains of capripoxvirus do not infect and transmit to sheep and goats (World Organization for Animal Health, 2010). The severity of the disease depends on the virulence of the viral strain, host susceptibility, and breed type of the animals (Mathews, 1982; CFSPH, 2008). The disease has been associated with the wet season of the year, introduction of new animals to the herd, communal grazing and watering points (Gari et al., 2011; Tuppurainen and Oura, 2012).

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LSD is one of the OIE (2010) notifiable diseases, is currently endemic in most African countries, and has expanded to the Middle East region (Tuppurainen and Oura, 2012). The disease is considered an important threat to beef and dairy industries (Kumar, 2011), affects cattle of all ages and breeds, and causes financial losses as a result of reduced milk production, beef loss and draft power loss, abortion, infertility, loss of condition, and damage to the hide (CFSPH, 2008). Eighty-five percent of the Ethiopian populations are dependent on smallholder agricultural production systems where livestock contributes a substantial role for mixed crop-livestock production activities (Tegegn, 1998). The sector is constrained by widely distributed livestock diseases of different species of animals, including LSD (Asfaw, 2003; Gari et al., 2010). However, limited research has been reported on the risk factors associated with clinical LSD occurrences (Gari et al., 2010) and its prevalence in different setting of the agricultural production systems in Ethiopia. In north-eastern Ethiopia, the agricultural system comprises mixed, pastoral and agro-pastoral farming systems, and there is high mobilization of livestock in search of water and pasture, as well as for trade purposes. Frequent outbreaks of LSD are reported in this area and hence, the main objective of this study was to understand the epidemiology of the disease, with the specific objectives being to estimate the herd- and animal-level prevalence in the study areas, to assess the risk factors associated with the occurrence of LSD at the herd level, and to determine the seasonal pattern of the disease in the area. 2. Materials and methods 2.1. Description of study area This study was conducted in Afar and Tigray regions in north-eastern Ethiopia. Two administrative zones (Zone-1 and Zone-4) out of five zones of Afar region were included in the study, and then one district from each zone was selected (Asiyta and Yallo, respectively). Asayita district was selected to include an agro-pastoral production system where irrigation farming is widely prevalent. Yallo district is located in the western part of Afar region bordering with Alamata and Raya Azebo districts of Tigray region. Yallo was selected for its location interfacing with the highland agro-climate in Alamata and Raya Azebo districts where the livestock are moved for grazing and watering during dry season (Philpott et al., 2005). There were two distinct agro-ecological climates prevailing in the Afar study area: lowland (2300 m). Tigray region also has five administrative zones and the study was carried out in the north-eastern zone in which the study districts Ofla and Alamata were located. These districts were selected for their seasonal shared communal grazing and watering resources, with a similar pastoral production system as in Yallo district but in a different agroecological setting. Pastoral production systems are where the society’s economy relies on livestock production, and livestock move from place to place in search of grazing and water for their livestock. Agro pastoral systems mainly

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sustain their livelihood on livestock production, but also practice some crop production. They have a transhumant mode of life. Mixed (sedentary) farming systems are practiced mainly in the highland agro-ecology, and the societies are occupied in crop production for their livelihood and rearing animals as part of the farming system. 2.2. Farm selection and questionnaire design A cross-sectional study was carried out between October 2011 and February 2012 to assess epidemiological factors associated with observed LSD in the previous two years (September 2009 to October 2011). Three to four Kebeles (the lowest administrative unit next to district in order of hierarchy in Ethiopia) were selected randomly from each district, and 20–30 herds were randomly selected from each Kebele. Herd-owners were selected based on willingness to complete the questionnaire. Questionnaire interviews were carried out in 15 Kebeles among 393 herds which included 3539 heads of cattle in the study. The questionnaire was designed to ascertain the presence of LSD based on the farmer’s ability to recognize clinical signs associated with the disease, and to gather information on herd size, cattle age structure and management practices (Table 1) (see annexed questionnaire). A total of sixteen questions were prepared which were grouped into three main sections. The first section was about the districts’ agro-ecologic conditions, herd size and herd structure. The second portion consisted of disease occurrence and questions related to season, year and month of LSD occurrence, frequency of occurrence, sex, age and breed of animals sick with LSD, and whether the animal with LSD died or not. The third section was related to herd management, which included questions about the seasonal movement of animals, farming systems, feeding and watering management, contact with sheep and goats, introduction of new animals, livestock market activity and known trade lines near the village, LSD vaccination status of the herd, and opinions of the herd owners regarding LSD prophylaxis and vaccination of the herds. The questionnaire was administered by face-to-face interviews with the herd owners using the local language. Commonly occurring skin diseases of cattle in the study areas were recorded from the district veterinary clinic for the differential diagnoses and to cross-check whether the herd owners correctly related the disease event with the clinical signs of LSD. 2.3. Statistical analysis A herd was considered infected when at least one animal in the herd was clinically affected. Herd-level prevalence was calculated based on the presence of the infection in the herd, while animal level prevalence was computed by dividing the number of clinically affected animals by the total number of animals which were at risk of getting the disease in the study group. The univariate association of potential risk factors with herd prevalence of LSD and the statistical significance variation was performed using Pearson’s homogeneity 2 test.

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Table 1 Univariate associations of potential risk factors to Lumpy skin disease occurrence. Variables

Factor levels

Total herds

Herds infected

Herd size

Small (2–11) Medium (12–21) Large (>22) Communal Separate Sedentary Agro pastoral Pastoral Yes No Yes No

315 65 11 376 17 200 113 80 94 299 195 198

123 39 13 171 2 74 61 38 64 109 71 102

Grazing/watering Farming system

New cattle introduction Vaccination status

Logistic regression was used to compute the strength of association (odds ratios) of the potential risk factors with LSD occurrence. The dependent variable was the disease occurrence as declared by the farmers based on its clinical manifestation in their herd. Variables with P < 0.20 were short-listed to consider in the final multivariable logistic regression. The model was built stepwise by forward adding short-listed factors and removing the factors when P > 0.05. The statistical analysis was undertaken using SPSS and Microsoft Excel software. The effects of interactions among significant variables in the final model were tested by pair-wise interactions in the multivariable logistic models. The model fitness was assessed using the likelihood ratio test. 3. Results Questionnaires were obtained from 393 herds. Fig. 1 shows the seasonal pattern of LSD outbreak reports during the year in the study areas. The month of August had the highest number of LSD outbreak reports. 3.1. Estimated LSD prevalence and farm characteristics In all farming systems and agro-climatic conditions, communal grazing and watering resource utilization was dominant (95.7%) and it was 100% in the pastoral and agropastoral areas. The average herd size was eleven head (ranged from 3 to 38). Mixed farming systems were practiced in Tigray

Odds ratio – 2.34 8.58 6.26 – – 1.99 ?? 3.72 – 0.54 –

95% CI

P-value

– 1.36–4.04 1.9–39.4 1.4–27.7 – – 1.25–3.2 0.9–2.6 2.27–6.1 – 0.36–0.81 –

– 0.002 0.006 0.016 – 0.004 0.106 0.001 – 0.003 –

region, which constituted 50% of the study groups. Of the remaining 50% of study groups, 20% were from Yallo district and were pastoral, and 30% were from Asiyta district and were agro-pastoral. Forty-nine percent of the herd owners declared that sheep and goats shared the same grazing and watering points. The estimated herd- and animal-level prevalences were (44%, 95% CI: 37–50%) and (7.4%, 95% CI: 6–8%), respectively. Higher herd prevalence was recorded in Afar region at (51%, 95% CI: 40–61%) than in Tigray region at (37%, 95% CI: 29–45%) (P < 0.01). Among the four districts, higher herd prevalence was seen in Asiyta at (53%, 95% CI: 34–67%), followed by Yallo at (47.5%, 95% CI: 37–69%) (P < 0.01). The animal-level prevalence among the districts was also higher in Asiyta at (9%, 95% CI: 7.5–10%), but it was lower in both Alamata at (6.8%, 95% CI: 5.1–8.4%) and Yallo at (6.5%, 95% CI: 4.4–8.6%) with almost similar prevalence. The lowest animal-level prevalence was recorded in Ofla at (4.7%, 95% CI: 6.5–8.3%). 3.2. Risk factors associated with LSD occurrence In the univariate logistic regression results, communal grazing and watering management, introduction of new animals to the herd, herd size, farming system, and watering sources were associated with the prevalence of LSD (Table 1). The final multivariable logistic regression model revealed herd size, introduction of new animals to the herd, and communal grazing and watering points were the risk factors associated with the occurrence of LSD (Table 2).

Fig. 1. Seasonal pattern of Lumpy skin disease outbreak reports during the year (October 2011 to February 2012) in the study areas.

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Table 2 Risk factors associated with Lumpy skin disease occurrence using multivariable logistic modeling. Factor

ˇ

S.E.

Odds ratio

95% CI

P-value

Herd size New cattle introduction Grazing and watering

2.962 1.488 2.670

0.912 0.268 0.954

19.3 4.43 14.44

1.4–50 2.6–7.5 2.23–94.0

0.001 0.001 0.005

No significant interactions between independent variables remained in the final model. 4. Discussion In this study, farmers’ knowledge and experience were used to identify LSD in their herds based on clinical symptoms. District veterinarians were consulted to validate the information about the outbreak reports declared by the herd owners in these districts. Commonly occurring skin diseases, such as demodicosis, dermatophillosis and ringworm, were taken into consideration as differential diagnosis during the questionnaire survey. However, mild forms of the disease might escape from the farmer’s notice, and this limitation might have affected the estimation of the herd prevalence. Also, farmers/pastoralists did not distinguish whether the vaccination was against LSD or for another disease. For this reason, vaccination data were recorded from the respective district veterinary service offices. The present study indicated that the prevalence of LSD was varying in different agro-ecological areas, owing to the differences in farming systems, herd management, and herd sizes. The average herd-level prevalence of LSD in this study was 44%, which is in agreement with other reports (Ayre-Smith, 1960; Thomas, 2002; CFSPH, 2008; Brenner et al., 2006). In Ethiopia, the observed herd-level prevalence of LSD reported was 22.3%, 55.2% and 43.5% in highland, midland and lowland areas, respectively, with the average prevalence for the country being 42% (Gari et al., 2010). Average herd seroprevalence of 46% was also reported from three agro-climatic zones of highland, midland and lowland areas of Ethiopia (Gari et al., 2012). Lumpy skin disease occurrence has been associated with the prevalence of mechanical insect vectors, livestock density at grazing and watering points, husbandry systems, wet seasons, agro-ecologic conditions, and introduction of new animals without screening (Ali et al., 1990; Tuppurainen and Oura, 2012). The disease was highly prevalent in Afar region as compared to Tigray region. This could be due to large herd sizes in these pastoral communities, and mass migration and aggregation of the animals around the watering and grazing resources in Afar (Bossche and Coetzer, 2008). Asiyta district had the highest herd- and animal-level prevalence of the LSD, as compared to other districts. This might be explained due to the moist, humid climatic condition and the presence of flooding and irrigation in this district, which could facilitate multiplication of potential mechanical vectors to enhance disease transmission (Ali et al., 1990; Davies, 1991; Tuppurainen and Oura, 2012). Herds using communal grazing and watering points were six times more likely to develop the disease than

herds grazing separately. Intermingling of different herds from various areas increases the frequency of herd contact, and enhances the chance of infection (Ocaido et al., 2009). Vectors with increased frequency of multiple blood feeding would increase the likelihood of the spread of the infection within and between herds (Gari et al., 2010; Tuppurainen and Oura, 2012). Introduction of new animals to the herd was highly associated with the occurrence of LSD, and the odds ratio of LSD occurrence was higher in those herds with new animal introduction. This is possibly due to herd owners buying infected animals without screening tests or quarantine periods for disease observation (Gari et al., 2010; Tuppurainen and Oura, 2012; Salib and Osman, 2011). Large herd size would increase the chance of infection with LSD occurrence than small herd size while communally grazing. Pastoral and agro-pastoral farming systems were found to be two times more likely than the sedentary farming system to get LSD infection, and this result was in agreement with the finding of Ocaido et al. (2009) where LSD was highly prevalent in agro-pastoral systems. In the dry season, pastoral herds were travelling long distances, which could increase the risk of disease occurrence (Brenner et al., 2006; Kumar, 2011; Magori Cohen et al., 2012). Vaccination was not associated with LSD occurrence, which might be explained by the fact that very few farmers vaccinated their animals annually, presumably due to lack of awareness in using the technology. 5. Conclusion Lumpy skin disease is widespread in these regions of Ethiopia. Hence, it is advisable to make efforts to increase LSD awareness, and to promote the use of vaccines for disease prevention and control. The implementation of appropriate measures in biosecurity and herd management could also reduce the occurrence of LSD in the study area and the economic losses incurred by farmers. Conflict of interest statement None of the authors has any financial or personal relationships that could inappropriately influence the contents of the paper. Acknowledgments The authors would like to thank Jimma University and Semera University for their financial support to conduct this study. We are also indebted to district veterinary experts for assisting us during the field work. We would like to thank Professor John VanLeeuwen Professor of Epidemiology and Ruminant Health Management Centre for

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Veterinary Epidemiologic Research Dept of Health Management Atlantic Veterinary College University of Prince Edward Island for taking his time for critical revision and language edition of the manuscript. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j. prevetmed.2014.03.013. References Ali, A.A., Esmat, M., Attia, H., Selim, A., Abdel-hamid, Y.M., 1990. Clinical and pathological studies of the lumpy skin disease in Egypt. Vet. Rec. 127, 549–550. Asfaw, W., 2003. Influence of animal diseases and sanitary regulations on livestock export trade and cases of export restrictions. In: Proceedings of the Annual Conference of the Ethiopian Society of Animal Production, pp. 23–34. Ayre-Smith, R.A., 1960. The symptoms and clinical diagnosis of lumpy skin disease virus. Vet. Rec. 72, 469–472. Bossche, P.V.d., Coetzer, J.A.W., 2008. Climate change and animal health in Africa. Rev. Sci. Tech. Off. Int. Epiz. 27 (2), 551–562. Brenner, J., Haimovitz, M., Orone, E., Stram, Y., Fridgut, O., Bumbarov, V., Kuznetzova, L., Oved, Z., Waerrman, A., Garazzi, S., Perl, S., Lahav, D., Edery, N., Yadin, H., 2006. Lumpy skin disease (LSD) in a large dairy herd in Israel. Isr. J. Vet. Med. 61, 73–77. CFSPH, 2008. The Center for Food Security and Public Health, Iowa State University, College of Veterinary Medicine and Institution of International Cooperation in Animal Biologics—An OIE Collaborating Center., pp. 1–4, http://www.cfsph.iastate.edu/Factsheets/pdfs/ lumpy skin disease.pdf. Davies, F.G., 1991. Lumpy skin disease of cattle: a growing problem in Africa and the Near East. World Anim. Rev. 68, 37–42.

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Estimated prevalence and risk factors associated with clinical Lumpy skin disease in north-eastern Ethiopia.

Lumpy skin disease (LSD) is one of the major livestock disease problems in most areas of Ethiopia. A questionnaire-based cross-sectional study was con...
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