Prevalence of babesiosis in Sanga cattle in the Ohangwena region of Namibia

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1 B- 755 [1-5] Indian J. Anim. Res., Print ISSN: / Online ISSN: AGRICULTURAL RESEARCH COMMUNICATION CENTRE Prevalence of babesiosis in Sanga cattle in the Ohangwena region of Namibia Emmanuel Kamutyatsha Matheus 1, Johan Oosthuizen 1, Christian Anayochukwu Mbajiorgu 1 and James Wabwire Oguttu 1 * College of Agriculture and Environmental Sciences, Department of Agriculture and Animal Health,University of South Africa, Johannesburg, South Africa Received: Accepted: DOI: /ijar.B-755 ABSTRACT Three hundred and ninety two (n = 392) blood samples from randomly selected cattle were subjected to the indirect fluorescent antibody (IFA) test to test for antibodies against Babesia spp. The proportions of males (49%) and females (51%) included in the study did not differ significantly. Cattle that were 5 years constituted 63% of the sampled animals, while cattle that were 0-2 years old were in the minority (14%). Babesia bigemina had the highest prevalence (36.5%), while mixed infections had the least prevalence (13.2%). Based on age, cattle that were 3-4 years old had the highest prevalence of both B. bovis (23.9%) and B. bigemina (44.6 %). Cattle in the 0-2 year age category had the lowest prevalence of both B. bovis (12.3%) and B. bigemina (29.8 %). The 3-4 years old age category also had the highest prevalence (18.5 %) of mixed infections, while the 0-2-years old had the lowest (8.8%). Overall, B. bigemina had the highest prevalence; however the level of the prevalence of babesiosis in the study area was not at the point where the region could be considered endemically stable.there was no significant association between infection and age, gender and place. Key words: Babesiosis, Babesia spp., Distribution, Endemic stability, Namibia, Prevalence, Sanga cattle, Ticks, Vectors. INTRODUCTION Babesiosis is one of the most common and economically important tick-borne infectious diseases of domestic and wild animals. Babesia spp that cause the disease are transmitted to the cattle by parasitic ticks (heamoparasites) that feed on the blood of animals. Babesiosis hampers animal production by causing retarded growth, low meat production and even mortality of farm animals (Góes et al. 2008; Gualito et al. 2012; Robbins 2012). Clinical signs suspected to be associated with babesiosis have continuously been reported to the state veterinary offices (Republic of Namibia 2013). However, we could find no evidence of studies that have been conducted in the Ohangwena region to ascertain the level of prevalence of the disease. In order to fill the knowledge gap, the present study was planned with the objective of determining the sero-prevalence of different Babesia spp. in Sanga cattle, and to determine the most prevalent Babesia species in the study area. MATERIALS AND METHODS A total of 392 cattle were selected from various crush pens in all constituencies of the Ohangwena region. The collection of samples was done during the annual vaccination campaign against lung sickness that was conducted in The indirect fluorescent antibody test (IFAT), with a sensitivity of 95% and specificity of 99%, was employed to test for the presence of Babesia bovis and Babesia bigemina antibodies (OIE 2013). Raw data was entered into Microsoft Excel spreadsheet (Microsoft, Redmond, WA, USA) and evaluated for inconsistences and improbable entries before analysis commenced.the data was analysed using the statistical package SPSS version 23. The quantitative data was summarised using descriptive statistics and presented as frequency tables and graphs. Ausvet EpiTool was used to estimate the prevalence and compute the confidence intervals for the prevalence estimates. The chi-square test was used to compare the proportions of infected cattle for categorical variables like sex, age and constituencies. RESULTS AND DISCUSSION Distribution of cattle in the study area: Herds in the study area were made up of nearly equal numbers of male (49%) and female (51%) animals (Table 1). This suggests that farmers tend to keep as many male animals as female animals (cows and heifers combined). This is not consistent with the recommended herd ratio of four bulls per one hundred cows (1:25) for the extensive cattle rearing systems (Tschopp et al. 2010). This finding was expected, because under the traditional farming system, farmers tend to keep oxen for ploughing, slaughtering at weddings, mourning deaths, and *Corresponding author s Joguttu@unisa.ac.za College of Agriculture and Environmental Sciences, Department of Agriculture and Animal Health,University of South Africa, Johannesburg, South Africa

2 2 INDIAN JOURNAL OF ANIMAL RESEARCH other socio-cultural events. In addition, the majority of cattle (63%) sampled were older than five years. This could be because among pastoralist societies, female cattle are usually retained for as long as they are able to produce. This is used as strategy to maximise the growth of the herd ( Hangara et al. 2011). As a result, old animals are not culled, but are retained in the herd for a long time, which is contrary to what commercial farmers do (Muhanguzi et al. 2014). The bull-to-cow ratio as observed in the present study has been known to pose problems in cattle production systems, because it negatively affects conception and the fertility of the herd, and has the potential to cause financial losses (Hangara et al. 2011). Spatial distribution of Babesia species in the study area: Antibodies against Babesia species were detected in cattle. This is confirmed by government reports of clinical cases suspected to be bovine babesiosis in the study area (Republic of Namibia 2013). This finding was anticipated given that bovine babesiosis is known to be endemic to countries of southern Africa (Cammà et al., 2012). Babesia bigemina had a high concentration at the crush pens in the central part of the region along the border between Eenhana and Epembe constituencies, and towards the eastern part of the region. The implications of this finding is that although widely distributed, the spread of bovine babesiosis in the study area was not uniform. Some areas had higher concentration of cases than others (Fig 1). The differences may be as a result of differences in the microclimate in the region. Constituencies in the western part of the study area like Engela, Endola, Ongenga and Ohangwena, are more prone to floods than those in the eastern part of the study area. Therefore the wet conditions in the western parts are more conducive for the growth and multiplication of the vector ticks (Coşkun 2012; Marufu 2008). The phenomenon of moving and displacing cattle in search of better grazing areas, also plays a significant role in the spread of the disease. This causes changes in the host population. As animals move from one region to another they transfer ticks from one area to another. Such changes affect the timing of tick-borne infections and thus place a burden on the nation s tick-control programmes (Olwoch et al. 2008; Penzhorn 2015; Tembue et al. 2011). The prevalence of babesiosis in the study area: In the current study, the presence of antibodies showed that the animals (especially the adult ones), had been infected and/ or could be immune. We detected antibodies in calves above one year of age, by which time the maternal immunity should have diminished. During sampling, clinical signs such as pale mucus membranes and jaundice were observed in some cattle of which farmers reported heamoglobinuria. Under field conditions, antibodies against babesiosis drop to negative reading after 6-12 months, as no antibodies will be detected by the IFA test. Therefore, after 12 months the IFA test will return a negative result while the animal is immune. Based on this the observed cases suggest that there was continuous infection by Babesia parasites and the presence of parasite-infected vector ticks in the study area. This knowledge is necessary to define the epizootiological balance in the population and to determine control strategies for the disease (Chandrawathani and Lye 2010). Babesia parasites are mostly found in animals that graze on pastures where vector ticks prevail (Atif et al. 2013). The prevalence of positive cases in the current study was estimated at 16.6 % (95%; CI: ) for B. bovis and 36.5 % (95%; CI: ) for B. bigemina. This was lower than the prevalence of 76.0% for B. bovis and 78.8% for B. bigemina observed in Mozambique (Tembue et al. 2011). However, the prevalence was higher than that observed in Angola (1%) and South Africa (1.4%) (Kubelová et al. 2012; Mtshali et al. 2013). This was not expected given that Namibia is a semi-arid area (dryer than Angola and South Africa) and that the climate is therefore not considered to be conducive for the survival of the ticks that spread the disease (Republic of Namibia 2013). Table 1: Profile of cattle sampled in the Ohangwena region (n = 392) Constituencies Number of cattle Frequencies (%) Sex Age groups Female Male 0-2 years 3-4 years over 5 years n (%) n (%) n (%) n (%) n (%) Okongo 138 (35.2) 70 (17.9) 68 (17.3) 23 (5.9) 38 (9.7) 77 (19.6) Omundaungilo 24 (6.1) 13 (3.3) 11 (2.8) 4 (1.0) 2 (0.5) 18 (4.6) Epembe 24 (6.1) 14 (3.6) 10 (2.6) 4 (1.0) 5 (1.3) 15 (3.8) Eenhana 24 (6.1) 13 (3.3) 11 (2.8) 4 (1.0) 2 (0.5) 18 (4.6) Ondobe 32 (8.2) 20 (5.1) 12 (3.1) 5 (1.3) 6 (1.5) 21 (5.4) Omulonga 32 (8.1) 13 (3.3) 19 (4.8) 5 (1.3) 6 (1.5) 21 (5.4) Ohangwena 24 (6.1) 12 (3.1) 12 (3.1) 0 (0.0) 7 (1.8) 17 (4.3) Oshikango 8 (2.1) 5 (1.3) 3 (0.8) 3 (0.8) 0 (0.0) 5 (1.3) Engela 16 (4.1) 6 (1.5) 10 (2.6) 1 (0.3) 3 (0.8) 12 (3.1) Ongenga 32 (8.2) 15 (3.8) 17 (4.3) 2 (0.5) 11 (2.8) 19 (4.8) Endola 38 (9.7) 19 (4.8) 19 (4.8) 4 (1.0) 10 (2.6) 24 (6.1) Total 392 (100) 200 (51.0) 192 (49.0) 55 (14.0) 90 (23.0) 247 (63.0)

3 Like in other communal farming systems of Africa, Bos indicus cattle (Sanga cattle) of southern African origin are the dominant breeds in the study area. The breed is known for its ability to be naturally resistant to tick parasitism and tick-borne diseases (Jonsson et al. 2014). This could explain why the prevalence in this region for B. bovis (16.6%) and B. bigemina (36.5%) was generally lower than that observed in other studies conducted elsewhere, where several breed types, including the Bos taurus are reared (Jonsson et al. 2014). Rearing animals that are adapted to the local conditions and known prevailing diseases in the area reduces the risk of farmers losing their animals to these tick-borne diseases. However, lack of regular tick control could undermine the advantage of rearing animals that are resistant to tick-borne diseases, which could explain why the prevalence in the study area was as high as 36.5% in some cases. As shown in Fig 2, babesiosis was present in almost all the constituencies of the Ohangwena region. However, high prevalence rates tended to occur in the constituencies to the west of the region like Ongenga (65.6%; 95% CI: ), Ohangwena (58.3%; 95% CI: ) and Endola (55.3%; 95% CI: ), while the lowest prevalence occurred in the central region. As mentioned earlier, a large part of the grazing areas of the western region consisted of flood-water pans and as a result, these findings were expected. The slightly higher prevalence (36.2%; 95% CI: ) in Okongo might be the result of the migration of cattle from the western part of the region in search of better grazing in the Okongo constituency. This could be attributed to the fact that animals coming from west are infected and act as source of infection for the animals to the other parts of the study area. This affects the results in the sense that it contributes to the disease spreading across the whole region as was observed. As mentioned earlier, a large Fig-1: Distribution of babesiosis at crush pens in the Ohangwena region Vol. Issue, () part of the grazing areas of the western region consisted of flood-water pans, which creates conditions conducive for survival of the vector. In view of this, the result reported here were expected. Most prevalent Babesia species: B. bigemina was the most prevalent species, with an overall prevalence of 36.5% compared to the 16.6% of B. bovis. Babesia bigemina dominated in prevalence in all respects (spatial and hostrelated factors) (Table 2). The results of the current study are consistent with the findings of previous studies that observed that both species of these Babesia can occur in the same place, and that where both exist, the prevalence of B. bigemina tends to dominate over B. bovis. One possible explanation for this, could be the fact that B. bigemina has many vectors as compared to B. bovis (OIE 2013; Vos and Waal 2004). Babesia bovis is generally known to be more pathogenic than B. bigemina (Bock et al. 2004; OIE 2013; Vos and Waal 2004). Therefore B. bigemina, the less pathogenic species being the most prevalent species ( 36.5%) in the study area, could explain why clinical signs of acute infections were rarely observed during the study. In addition, the fact that B. bigemina was the most prevalent species is good news for the farmers in the study area. This is because it has been observed that that cattle infected with B. bigemina became carriers for a few months, while cattle infected with B. bovis tended to remain carriers of the disease for a long period (Lemma et al. 2015). The results reported here also revealed that, some cattle were simultaneously infected with both B. bovis and B. bigemina, while others were infected by a single species. This indicates that both parasites can live in a single host. This was in agreement with a similar study done in Malaysia by Chandrawathani and Lye (2010), where cattle were found to be infected with one of the Babesia species (B. bigemina or B. bovis), or with both simultaneously. Prevalence based on sex and age: The prevalence was higher in males (42%) compared to females (38%) (Table3). however, this difference was not statistically significant (P > 0.05). This is consistent with the observation by Lemma et al. (2015), who reported an equal prevalence of babesiosis in female and male cattle (P > 0.05). The occurrence of tick fever increases directly in proportion to the age of the animal (OIE 2012; Zintl et al. 2005). In the current study, the highest prevalence of babesiosis was found in the 3-4-year age group (50%), followed by the group that was older than 5 years (37.9 %). Cattle aged between 0 and 2 years old had the lowest prevalence (33.3%) (Table 4). Furthermore, the findings of this study concurred with those by Abdullah-Al-Mahmud (2015), who reported a higher prevalence rate in cattle over three years of age than in younger ones (1 to 2 years of

4 4 INDIAN JOURNAL OF ANIMAL RESEARCH Fig-2: Prevalence of babesiosis in constituencies in the Ohangwena region Table 2: Frequencies and prevalence of positive samples (n = 392) Babesia Frequencies Prevalence 95% Confidence species of positive (%) Interval samples (n) Lower Upper Babesia bovis % Babesia bigemina % Mixed infections 51 13% age).the authors are of the view that this observation could be related to the traditional system of rearing cattle among pastoralists where young animals are left at home when the rest of the herd goes out to graze. In this way, the age category in question is at a lower risk of exposure to the tick vector. The results observed in this study suggest that the parasites had been circulating within the cattle population for some time. This was demonstrated by the fact that antibodies were detected in cattle above the age of twelve months. This happens if the cattle have continuously been exposed to the parasites. By twelve months, the maternal antibodies would have diminished and no antibodies would be detected if there was no exposure (Ekici and Sevinc 2009; Goff et al. 2002; Ríos-Tobón and Gutiérrez-Builes 2014). CONCLUSION Babesiosis was found to be widely distributed throughout the study area. The region was found to be endemically unstable for babesiosis. As a result, a vaccination protocol to establish good herd immunity is necessary to improve production. This study has clearly identified a need for more farmer education and awareness about tick-borne diseases and herd management to correct aspects like herd composition in the study area, and to institute effective tick control measures to limit the exposure of the animals to Babesia parasites. Farmers also have to be educated on the necessity to remove old animals to help improve the productivity and profitability of their enterprises. Our findings also confirmed that the Ohangwena region is endemically infected with bovine babesiosis and Table 3: Proportion of positive samples based on the sex of cattle in the Ohangwena region (n = 392) Babesia Spp. Sex Male (n = 192) Female (n = 200) n % ( a CI) n % ( a CI) Babesia bovis 28/ ( ) 37/ ( ) Babesia bigemina 74/ ( ) 69/ ( ) Mixed infections 21/ ( ) 30/ ( ) a CI (confidence interval) = 95% Table 4: Proportion of positive samples based on age of cattle in the Ohangwena region (n = 392) Babesia Spp. Age group (years) n % ( a CI) n % ( a CI) n % ( a CI) Babesia bovis 7/ ( ) 22/ ( ) 36/ ( ) Babesia bigemina 17/ ( ) 41/ ( ) 85/ ( ) Mixed infections 5/ ( ) 17/ ( ) 29/ ( ) a CI (confidence interval) = 95%, Non-Significant at P > 0.05

5 that there is a risk of the disease spreading to neighbouring countries such as Angola. ACKNOWLEDGEMENT Colleagues in the North-West Subdivision of the Directorate of Veterinary Services and the Ondangwa Veterinary Laboratory and Veterinary Central Laboratory in Windhoek are acknowledged for assisting in the sampling and processing of the samples. The Agricultural Research Vol. Issue, () Centre at the Onderstepoort Veterinary Institute in Pretoria, assisted with the laboratory analysis of the samples, farmers allowed their cattle to be sampled and language services department of the University of South Africa that copy edited the manuscript are gratefully acknowledged. COMPETING INTERESTS There are no competing interests that any of the authors are aware of. REFERENCES Abdullah-Al-Mahmud SHB and AH (2015). Prevalence of theileriosis and babesiosis in cattle in Sirajganj district of Bangladesh. Open Access Res. Artic.2(1): Age I, Soay T, Age B (1996). 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