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\title{Prevalence and Risk Factors of Bovine Trypanosomiasis in Khartoum State, Sudan, April-July 2012}
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             \author[1]{Sara M.E.O.  Elmahi}

             \author[2]{Mubarak A.M.  Mahmoud}

             \author[3]{Ammar I.A.  Yousof}

             \author[4]{Abdelhamid A.M.  Elfadil}

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\date{\small \em Received: 7 December 2018 Accepted: 1 January 2019 Published: 15 January 2019}

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\begin{abstract}
        


A cross-sectional study was conducted in the dry season from April to July 2012 in Khartoum State, Sudan to: estimate the prevalence of bovine trypanosomiasis (BT), identify the prevailing species of trypanosomes and investigate the associated potential risk factors of the disease.           Blood samples were collected from 271 randomly selected cattle of the eight study areas and evaluated through             standard parasitological methods (Haematocrit Centrifugation Technique (HCT) and thin blood smear). Also, the packed cell volume (PCV) of each animal was measured using Haematocrit Techniques for anemia estimation. The results indicated that the overall prevalence of BT was 4.8% (13/271). All the trypanosomes encountered in cattle belonged to a single species of Trypanosoma vivax. For investigation of associated risk factors of the disease, a univariate analysis using the Chi-square (?2) test identified 15 risk factors statistically significantly associated with BT (p ? 0.25). These 15 risk factors were entered to the multivariate analysis using logistic regression for further analysis. The significant level of association in the multivariate analysis was set at (p? 0.05). The multivariate analysis revealed four risk factors that had significant associations with BT (p ? 0.05). These were treatment of sick animals (p = 0.012), presence of other animal species in the farm (p = 0.003), veterinary care            (p = 0.023) and location of livestock market (p = 0.004). The results of the study indicated that BT is prevalent in Khartoum State and the predominant trypanosome was T. vivax. Furthermore, the risk factors found statistically significantly associated (p ? 0.05) with BT in this study should be considered as predictors for the disease and should be taken into account when planning for control programs of               the disease.

\end{abstract}


\keywords{prevalence, risk factors, cattle, trypanosome- vivax, Khartoum state, sudan.}

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\let\tabcellsep& 	 	 		 \par
season from April to July 2012 in Khartoum State, Sudan to: estimate the prevalence of bovine trypanosomiasis (BT), identify the prevailing species of trypanosomes and investigate the associated potential risk factors of the disease. Blood samples were collected from 271 randomly selected cattle of the eight study areas and evaluated through standard parasitological methods (Haematocrit Centrifugation Technique (HCT) and thin blood smear). Also, the packed cell volume (PCV) of each animal was measured using Haematocrit Techniques for anemia estimation. The results indicated that the overall prevalence of BT was 4.8\% (13/271). All the trypanosomes encountered in cattle belonged to a single species of Trypanosoma vivax. For investigation of associated risk factors of the disease, a univariate analysis using the Chi-square (?2) test identified 15 risk factors statistically significantly associated with BT (p ? 0.25). These 15 risk factors were entered to the multivariate analysis using logistic regression for further analysis. The significant level of association in the multivariate analysis was set at (p? 0.05). The multivariate analysis revealed four risk factors that had significant associations with BT (p ? 0.05). These were treatment of sick animals (p = 0.012), presence of other animal species in the farm (p = 0.003), veterinary care (p = 0.023) and location of livestock market (p = 0.004). The results of the study indicated that BT is prevalent in Khartoum State and the predominant trypanosome was T. vivax. Furthermore, the risk factors found statistically significantly associated (p ? 0.05) with B T in this study should be considered as predictors for the disease and should be taken into account when planning for control programs of the disease. 
\section[{Introduction}]{Introduction}\par
frican animal trypanosomiasis is indisputably a great problem on the African scene, but the perspective alters when it is examined against a global background, even when taking into account mechanically and venereally transmitted African trypanosomes which have spread to other continents (Trypanosoma evansi causing surra, mechanically transmitted T. vivax and T. equiperdum the causal agent of the venereal disease dourine) \hyperref[b24]{(Uilenberg 1998)}.\par
Trypanosomiasis is a parasitic disease caused by species of flagellated protozoa belonging to the genus Trypanosoma which inhabit the blood plasma, various body tissues and fluids of vertebrate host. The disease is transmitted cyclically by tsetse flies (Glossina species), and non-cyclically by other biting flies \hyperref[b20]{(Tadesse et al. 2011)}. Trypanosomiasis induces loss of body condition in pregnant animals leading to birth of offspring with low birth weights, fetal and neonatal losses, besides production losses in lactating animals. The consequences of trypanosomiasis are less severe in better-nourished animals but good nutrition does not by itself provide protection. Adequate energy, protein and vitamin nutrition enhances the ability of trypanosome-infected animals to withstand the adverse effects of infection \hyperref[b17]{(Pathak 2009)}. T. vivax is enzootic in wide areas of Sudan more than 2,000 km away from the known tsetse belt of the country. Previous outbreaks of bovine trypanosomiasis (BT) reported to be due to T. congolense were reported as far north as Kosti area along the White Nile, more than 1,000 km north of the Tsetse belts. The transmission of the disease is due to the enormous populations of Tabanidae and biting flies \hyperref[b18]{(Rahman 2005)}. Trypanosoma infection restricts the animal production and causes economic losses by the clinical signs of the infection such as restricted growth, abortion, anemia, treatment cost, and death of the affected animals. Hence, the objectives of this study were to estimate the prevalence of BT in Khartoum State, to identify the prevailing species of trypanosomes and to investigate the potential risk factors associated with the disease. 
\section[{II.}]{II.} 
\section[{Materials and Methods}]{Materials and Methods} 
\section[{a) Study area}]{a) Study area}\par
Khartoum is the political capital of the Sudan. The state lies between longitudes 31.5?-34? east and latitude 15?-16? north in an area about 28.165 km 2   
\section[{b) Study design}]{b) Study design}\par
A cross sectional survey was conducted from April to July 2012 to estimate the prevalence of BT, to identify the prevailing species of trypanosomes and to investigate potential risk factors associated with the disease. 
\section[{c) Sampling Method}]{c) Sampling Method}\par
A multistage random sampling method was followed to select the study animals based on state, governorates (Khartoum, Khartoum North, and Omdurman), localities (Jabal Awlia, East Nile, Omdurman and Ombeda), and areas (Ombeda, Felstine, Almoilih, Aldekhinat, Edbabekir, Alozozab, Alkeriab and Suba). Finally, farms and animals were conveniently selected. 
\section[{i. Sample size determination}]{i. Sample size determination}\par
The sample size was determined using the following formula (Thrusfield 2005):n = (1.96) 2 × P? × Q?? L 2\par
Where: n = the sample size.\par
(1.96) 2 = constant. P\textasciicircum = expected prevalence of BT, which was 4.4\% \hyperref[b0]{(Abdalla et al. 2008}). Q\textasciicircum  = 1-P\textasciicircum  L 2 = allowable error (5\%). n= (1.96) 2 × 0.044 × 0.956 /0.0025= 64 samples.\par
To increase the precision of the study; the sample size was multiplied by 4 (Thrusfield 2005), so the number of samples became 256 samples. Finally, the investigators were able to collect samples from 271 animals. 
\section[{ii. Samples collection and laboratory tests}]{ii. Samples collection and laboratory tests}\par
Blood samples were collected from each animal by puncture of the jugular vein using a sterile needle \hyperref[b4]{(Abenga et al. 2004}\hyperref[b6]{, Adam et al. 2011}\hyperref[b14]{, Mogona et al. 2011}\hyperref[b7]{, Batista et al. 2012}). Blood was obtained in dry clean sterile heparinized tube 5 milliliters (containing EDTA (ethylene diamine tetra acetic acid, as anticoagulant) and was put in cold box with ice and transported to the laboratory (Central Veterinary Research Institute Laboratories, Soba, Khartoum) as soon as possible for diagnosis. 
\section[{iii. Diagnostic techniques}]{iii. Diagnostic techniques}\par
For diagnosis, parasitological methods (Haematocrit Centrifugation Technique (HCT) and thin blood smear stained with Giemsa stain) was used to identify the parasite, also packed cell volume (PCV) of each animal was measured for anemia estimation. 
\section[{iv. Investigation of potential risk factors}]{iv. Investigation of potential risk factors}\par
A pre-tested questionnaire was completed in an interview with the farms owners and/or workers to collect information data about selected potential risk factors on the occurrence of BT. 
\section[{d) Statistical analysis}]{d) Statistical analysis}\par
The overall prevalence was calculated based on positive results divided by the total number of animals tested. Potential risk factors (independent variables) and the laboratory test outcome (dependent variable) were analyzed using SPSS (version 16.0). The Chi-square test (? 2 ) was used for univariate analysis; the significance level was set at p? 0.25. In order to control for confounding, risk factors found significant at p? 0.25 were entered to the multivariate analysis using logistic regression, the significance level of association was set at p? 0.05. The strength of association was measured by the odds ratio (OR) accompanied by the 95\% confidence interval (CI) for OR. 
\section[{III.}]{III.} 
\section[{Results}]{Results} 
\section[{a) Prevalence and trypanosome species}]{a) Prevalence and trypanosome species}\par
Out of the total 271 animals tested 13 were positive. The overall prevalence of BT in Khartoum state, Sudan was 4.8\% (13/271).The prevalent trypanosome species in the study was Trypanosoma vivax. 
\section[{b) Univariate analysis}]{b) Univariate analysis}\par
The Chi-square test (? 2 ) showed that there were 15 out of 33 potential risk factors statistically significantly associated with BT (P-value ? 0.25). These were: locality (p = 0.084), area (p = 0.000), sex (p = 0.219), body condition (p = 0.009), herd size (p = 0.094), treatment of sick animal (p = 0.003), presence of other species of animals in the farm (p = 0.000), farm hygiene (p = 0.148), veterinary care (p = 0.000), surgical operation or wound in the animal's body (p = 0.108), location of livestock market (p = 0.002), presence of insects in the farm (p = 0.108), species of insect found in the farm (p = 0.106), presence of ticks in the farm (p = 0.099) and farmer awareness about the disease (p = 0.065) (Table1). 
\section[{c) Multivariate analysis}]{c) Multivariate analysis}\par
The multivariate analysis using the logistic regression showed that there were four potential risk factors statistically significantly associated with BT (p? 0.05). These were: treatment of sick animals (p = 0.012), presence of other animal species in the farm (p = 0.003), veterinary care (p = 0.023) and location of livestock market (p = 0.004).\par
IV. 
\section[{Discussion}]{Discussion}\par
Trypanosomiasis is a major constraint that affects the health and productivity of livestock. The major consequences of infection include mortality, loss of body condition and abortion \hyperref[b10]{(Delafosse et al. 2006}). Among all species of animals, the diseasehas been regarded as one of the most serious animal disease problem in Sudan. Trypanosoma vivax occurs in most parts of the country \hyperref[b18]{(Rahman 2005)}.\par
In our study, the prevalence and risk factors of BT in Khartoum state, Sudan was investigated. T. vivax was the only trypanosome species found during the study period. This is in agreement with previous studies  {\ref (Tadesse et}  The prevalence in our study was 4.8\%. This result is not different from another study carried out in the Blue Nile area between Addamazin and Khartoum where the prevalence was 1\% in the dry season and 6\% in the rainy season \hyperref[b18]{(Rahman 2005)}, and in Sinnar, Sudan the prevalence was 4.4\% \hyperref[b0]{(Abdalla et al. 2008}). Another study carried out in Lake Chad showed a prevalence of 1.6\% \hyperref[b10]{(Delafosse et al. 2006)}. Also, in another study in South Western Ethiopia the prevalence was 4.4\% (Tadesse and Tsegaye 2010). However, the prevalence in our study was very low compared with other studies in Sudan and different countries which was 50.3\% in Sinnar, Sudan where there is no tsetse fly in the area \hyperref[b1]{(Abdalla et al. 2005}), 43\% in Blue Nile State, Sudan \hyperref[b19]{(Salim et al. 2011)}, and 70\% in Western Kenya \hyperref[b23]{(Thumbi et al. 2010}).The difference in BT prevalence between our study and different studies may be due to different factors associated with the disease like: Khartoum state is out of the tsetse belt and the disease is transmitted mechanically, environmental factors which affect the vector, control strategy applied in the areas, variation on climatic conditions and dry season which affects the vectors breeding and low parasitaemia.\par
Distribution of the prevalence of BT in the localities showed significant association (p = 0.084). The higher prevalence in Ombeda might be attributed to the proximity of the area to livestock market.\par
A significant association between the disease and areas was observed (p = 0.000). This association could be due to the presence of irrigation canals which extended in the area as well as good vegetation making a suitable environment for vector breeding.\par
This study showed a prevalence of 5.3\% in females. There was a significant association in the univariate analysis between BT and sex (p = 0.219). This result is in agreement with a previous study \hyperref[b14]{(Mogona et al. 2011}) which reported that a female is at risk two times higher than a male. Females have a higher prevalence than males, because females remain longer for production purposes, and also due to physiological stress like estrous cycle, pregnancy and lactation, so the disease has more chance to develop.\par
The significant association of body condition with the disease in this study (p = 0.009) agrees with other studies (Tadesse and Tsegaye 2010, \hyperref[b8]{Begna et al. 2011}\hyperref[b9]{, Bitew et al. 2011}\hyperref[b15]{, Mulaw et al. 2011}) which found that the prevalence in poor body condition animals was significantly higher than good body condition animals (p? 0.05). This could be due to the chronic nature of the disease that resulted in anemia, poor body condition and emaciation.\par
There was a significant association between the disease and small herd size (p = 0.094). This could be attributed to the fact that most of < 30 groups, in this study, were located in areas with high density of insects, thus more fly attacks to the herd of small size than large size one.\par
The current study investigated the use of drugs for treatment of animals. There was significant association between the disease and treatment of sick animals (p= 0.003). The association of treatment of animals with the disease was also significant in the multivariate analysis (p = 0.012). These results agree with a previous study \hyperref[b13]{(Kidanemariam et al. 2002)} which reported that chemotherapy and chemoprophylaxis is important against trypanosomiasis. Logically, treatment of sick animals restricts spread of the disease.\par
There was significant association between BT and the presence of other species of animals in the farm (p = 0.000). This risk factor was also significant in the multivariate analysis (p = 0.003). This result agrees with \hyperref[b16]{Mustafa (2004)} who reported that sheep can act as a potential reservoir in mixed herd. Thus, presence of other species of animals in the farm may act as a source of the disease.\par
Also, the study investigated the farm hygiene as a risk factor possibly associated with the disease and there was a significant association between the disease and farm hygiene (p = 0.148). This could be attributed to the fact that poor farm hygiene provides a suitable environment for breeding of insects.\par
For veterinary care the study showed a significant association between BT and the availability of veterinary care in the univariate analysis (p = 0.000). Also, veterinary care had a significant association with BT (p = 0.000) in the multivariate analysis with a Year 2019 protective effect. Logically, veterinary care plays a role in restricting the disease by intervention if any clinical sings appear. Surgical operation and wounds in the animal's body were investigated and a significant association between BT and surgical operation or wounds in the animal's body was observed (p = 0.108). That is logical because surgical operation or wounds in the animal's body invite insects to have their blood meal. 
\section[{Global}]{Global}\par
There was a significant association between the disease and location of livestock market (p = 0.002). Also, location of livestock market had a significant association with the disease (p = 0.004) in the multivariate analysis. These findings are consistent with a previous study \hyperref[b3]{(Abdelkarim 1991}) which reported that Trypanosoma infected animals in the livestock market can act as a source of infection to the neighboring farms. Logically, if there is one animal with the disease in the market all the area around may be at risk when the vector is present.\par
Also, the study investigated presence of insects in the farms. There was a significant association between the disease and presence of insects in the farm (p = 0.108). Furthermore, another related risk factor investigated was insects' species found in the farm. There was a significant association between the disease and insects' species found in the farm (p = 0.106). This result agrees with a previous study \hyperref[b18]{(Rahman 2005}). These insect species may act as a mechanical vector for the disease.\par
Furthermore, presence of ticks in the farm was investigated in our study. There was a significant association between the disease and presence of ticks in the farm (p = 0.099). Ticks may predispose animals to infection with BT by infection with other tick-borne diseases which reduce the animal immunity.\par
Farmer awareness about the disease was investigated as a risk factor possibly associated with the disease. There was a significant association between the disease and farmer awareness (p = 0.065). Logically, aware farmer could apply control methods to control the disease and vectors.\par
In this study, the univariate analysis showed that 15 risk factors were statistically significantly associated with BT (p ? 0.25). However, in the multivariate analysis, there were only four risk factors that were found statistically significantly associated with BT (p ? 0.05), a result which indicates a presence of confounding between these risk factors.\par
V. 
\section[{Conclusion}]{Conclusion}\par
The current study confirmed that BT is widely distributed in Khartoum state farms with an overall prevalence of 4.8\%. Furthermore, the study indicated that T. vivax is the predominant species implicated in BT in Khartoum state.\par
The presence of various biting flies and the absence of tsetse flies in this investigation indicated that BT in Khartoum state is caused by mechanical transmission mediated by these biting flies.\par
The results of the multivariate analysis showed that four risk factors had statistically significant associations with BT (p? 0.05). These risk factors were: treatment of sick animals (p = 0.012), presence of other species of animals in the farm (p = 0.003), veterinary care (p = 0.023) and location of livestock market (p = 0.004). These risk factors should be considered as predictors for the disease and should be taken into account when planning for control programs of the disease.  \begin{figure}[htbp]
\noindent\textbf{1}\includegraphics[]{image-2.png}
\caption{\label{fig_1}Figure 1 :}\end{figure}
 \begin{figure}[htbp]
\noindent\textbf{} \par 
\begin{longtable}{}
\end{longtable} \par
 
\caption{\label{tab_1}}\end{figure}
 \begin{figure}[htbp]
\noindent\textbf{1} \par 
\begin{longtable}{P{0.43548387096774194\textwidth}P{0.0935483870967742\textwidth}P{0.19032258064516128\textwidth}P{0.017741935483870968\textwidth}P{0.05322580645161291\textwidth}P{0.0596774193548387\textwidth}}
Risk factors\tabcellsep No. tested\tabcellsep No. +ve (\%)\tabcellsep d. f.\tabcellsep ?²\tabcellsep p-value\\
1. Locality\tabcellsep \tabcellsep \tabcellsep \tabcellsep \tabcellsep \\
Ombeda\tabcellsep 22\tabcellsep 3 (13.6)\tabcellsep \tabcellsep \tabcellsep \\
Omdurman\tabcellsep 22\tabcellsep 0\tabcellsep 3\tabcellsep 6.648\tabcellsep 0.084\\
JabalAwlia\tabcellsep 34\tabcellsep 0\tabcellsep \tabcellsep \tabcellsep \\
East Nile\tabcellsep 193\tabcellsep 10 (5.2)\tabcellsep \tabcellsep \tabcellsep \\
2. Area\tabcellsep \tabcellsep \tabcellsep \tabcellsep \tabcellsep \\
Felstine\tabcellsep 22\tabcellsep 3 (13.6)\tabcellsep \tabcellsep \tabcellsep \\
Almoilh\tabcellsep 22\tabcellsep 0\tabcellsep \tabcellsep \tabcellsep \\
Aldkhinate\tabcellsep 34\tabcellsep 0\tabcellsep \tabcellsep \tabcellsep \\
Alozozab\tabcellsep 42\tabcellsep 1 (2.4)\tabcellsep 7\tabcellsep 27.293\tabcellsep 0.000\\
Eidbabeker\tabcellsep 67\tabcellsep 1 (1.5)\tabcellsep \tabcellsep \tabcellsep \\
Sudan university farm\tabcellsep 8\tabcellsep 0\tabcellsep \tabcellsep \tabcellsep \\
Alkeriab\tabcellsep 45\tabcellsep 8 (17.8)\tabcellsep \tabcellsep \tabcellsep \\
Soba\tabcellsep 31\tabcellsep 0\tabcellsep \tabcellsep \tabcellsep \\
3. Sex\tabcellsep \tabcellsep \tabcellsep \tabcellsep \tabcellsep \\
Male\tabcellsep 27\tabcellsep 0\tabcellsep 1\tabcellsep 1.511\tabcellsep 0.219\\
Female\tabcellsep 244\tabcellsep 13 (5.3)\tabcellsep \tabcellsep \tabcellsep \\
4. Body condition\tabcellsep \tabcellsep \tabcellsep \tabcellsep \tabcellsep \\
Poor Good\tabcellsep 119 122\tabcellsep 11 (9.2) 2 (1.6)\tabcellsep 2\tabcellsep 9.327\tabcellsep 0.009\\
Very good\tabcellsep 30\tabcellsep 0\tabcellsep \tabcellsep \tabcellsep \\
5. Herd size (\# of animals)\tabcellsep \tabcellsep \tabcellsep \tabcellsep \tabcellsep \\
<30\tabcellsep 195\tabcellsep 12(6.2)\tabcellsep 1\tabcellsep 2.803\tabcellsep 0.094\\
?30\tabcellsep 76\tabcellsep 1(1.3)\tabcellsep \tabcellsep \tabcellsep \\
6. Treatment of sick animals\tabcellsep \tabcellsep \tabcellsep \tabcellsep \tabcellsep \\
Not treated\tabcellsep 72\tabcellsep 8 (11.1)\tabcellsep 1\tabcellsep 8.559\tabcellsep 0.003\\
Treated\tabcellsep 199\tabcellsep 5 (2.5)\tabcellsep \tabcellsep \tabcellsep \end{longtable} \par
 
\caption{\label{tab_2}Table 1 :}\end{figure}
 \begin{figure}[htbp]
\noindent\textbf{2} \par 
\begin{longtable}{P{0.43142548596112307\textwidth}P{0.06241900647948164\textwidth}P{0.1376889848812095\textwidth}P{0.0642548596112311\textwidth}P{0.10464362850971923\textwidth}P{0.04956803455723542\textwidth}}
Risk factors\tabcellsep No. tested\tabcellsep No. +ve (\%)\tabcellsep OR\tabcellsep 95\% CI for OR\tabcellsep p-value\\
1. Treatment of sick animals Treated Not treated\tabcellsep 199 72\tabcellsep 5 (2.5) 8 (11.1)\tabcellsep ref 5.536\tabcellsep 1.4-21.06\tabcellsep 0.012\\
2. Presence of other animal species\tabcellsep \tabcellsep \tabcellsep \tabcellsep \tabcellsep \\
in the farm Not present\tabcellsep 204\tabcellsep 2 (1.0)\tabcellsep ref .076\tabcellsep 0.014-0.418\tabcellsep 0.003\\
Present\tabcellsep 67\tabcellsep 11(16.4)\tabcellsep \tabcellsep \tabcellsep \\
3. Veterinary care Available Not available\tabcellsep 150 121\tabcellsep 1 (0.7) 12 (9.9)\tabcellsep ref .092\tabcellsep 0.012 -0.724\tabcellsep 0.023\\
4. Location of livestock market Away from the farm Close to the farm\tabcellsep 204 67\tabcellsep 5 (2.5) 8 (11.9)\tabcellsep ref .118\tabcellsep 0.028-0.497\tabcellsep 0.004\end{longtable} \par
 
\caption{\label{tab_3}Table 2 :}\end{figure}
 			\footnote{Prevalence and Risk Factors of Bovine Trypanosomiasis in Khartoum State, Sudan, April-July 2012} 			\footnote{© 2019 Global Journals Prevalence and Risk Factors of Bovine Trypanosomiasis in Khartoum State, Sudan, April-July 2012} 		 		\backmatter  			  				\begin{bibitemlist}{1}
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