Research Article Risk Factors Associated with Prevalence of Bovine Hydatidosis in Cattle Slaughtered at Khartoum State

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1 Journal of Applied and Industrial Sciences, 2016,4(1): 21-26, ISSN: (PRINT), ISSN: (ONLINE) 21 Research Article Risk Factors Associated with Prevalence of Bovine Hydatidosis in Cattle Slaughtered at Khartoum State Elsair, A 1, Abdelrahim,A.I. 2, Adil M. A. Salman 3* 1-3 College of Veterinary Medicine- University of Bahri *Corresponding author E. mail: adilsal400@bahri.edu.sd (Received: October 02, 2015; Accepted: March21, 2016) Abstract- Across-sectional study was conducted to estimate the prevalence and risk factors associated with hydatidosis in cattle slaughtered at Khartoum state. Out of 210 cattle examined pathologically for the presence of Hydatid cyst, 12 animals were found to be positive for hydatidosis with 5.7% prevalence rate. Univariate analysis showed statistical significant association between age, sex, source and body condition of the animals and hydatidosis with variable degrees. Exceptionally, the study revealed highly significant association between prevalence of Echinococcosis and presence of dogs. In conclusion, it was found that presence of dogs roaming within and around the slaughterhouses is a real threatening to the public health and that is by consuming the infected offal. Therefore, reduction or eradication of this stray dogs population is a necessity for controlling the hydatid disease in the Sudan. Index terms: Bovine Hydatidosis, Cattle, Breeding, Khartoum. I. INTRODUCTION Hydatidosis is a chronic parasitic zoonotic disease, a name given to a condition due to infection with the larval stage of the dog tapeworm, Echinococcus granulosus. It occurs throughout the world. It is of considerable public health hazard and economical losses due to decreased livestock production and condemnation of offals containing hydatid cysts in slaughterhouses [1]. Several factors appear to be associated with the spreading of the disease among animals as well as humans. Most of the previous relevant studies though investigating this disease thoroughly, yet they neglected the true factors responsible for its prevalence and distribution. It was a first attempt to investigate the risk factors responsible for the transmission of this serious parasitic zoonotic disease. The main objectives of this study were: 1- To estimate the prevalence of bovine hydatidosis in cattle slaughtered at Khartoum state. 2- To investigate the risk factors associated with bovine hydatidosis in Khartoum State. II. MATERIALS AND METHODS Study area Khartoum state slaughterhouses were selected since they receive slaughter animals from all over the country and so they are a true reflection to hydatidosis in the other states. The Study samples were collected from 210 randomly selected cattle slaughtered at four abattoirs, namely, Elkadaruo( n=64), Elsalam,(n=41) Elsahafa(n=58) and Ghanaoua.(n=47). A welldesigned questionnaire was prepared to collect data on the risk factors incriminated. The selected potential risk factors that might influence the prevalence of bovine hydatidosis and play a role in transmission of the disease are: Age, sex, breed, body condition, previous exposures to the disease, grazing system, and presence of dogs, herd size, source and presence of other animals. The hydatid cysts in the livers and lungs were detected as described by [2-4]. The risk factors were determined as follows: 1- Age of the animals slaughtered was estimated on the basis of the dentitions [5] and they were categorized into two groups 2- Sex they were either male or female. 3- They were received from Khartoum, White Nile or Darfur states. 4- Breed of animals either local or cross breeds. 5- Presence of other animals as noticed and includes sheep, goats, and camels in addition to dogs. 6- Body condition was estimated during antemortem and postmortem inspections and classified into 2 groups either poor or good. 7- Disease exposure was determined through information about previous history of presence of hydatidosis and they were either, exposed previously to hydatidosi or not. 8- Grazing system was determined through data collected from the questionnaire and the farming was either open or semi-closed.

2 22 9- Presence of dogs with the animals tested, was determined according to information collected through the questionnaire and they were either present or absent. 10- Herd size was categorized into three groups: small less than 50 cattle, Medium between , and Large more than 100. Statistical analysis The test animals were selected by using systematic random sampling and the prevalence rate was calculated using the formula described by Martin [6]. III. RESULTS AND DISCUSSION General results Out of 210 bovine carcasses inspected, only 12 with a percentage rate of 5.7% were found to be positive for hydatidosis (Table 1). Table 1: Overall infection rate in 210 cattle carcasses slaughtered at Khartoum state. No of animals inspected Positive % Negative % Age of animals In this study infection was more in animals of 5 years or more (9.4%) compared to animals less than 5 years (1.9%) (Table2). The Chi-square test showed significant association between the infection and age of animal (P-value=0.018)(Table2). Sex of animals 210 cattle were examined for hydatid cysts according to sex. 8 animals were female compared to 202 males (Table 2). Among these females only 3 animals were found infected with an infection rate of (37.5%), however, out of 202 males 9 males were found infected with an infection rate of (4.5%) (Table2). The Chi-square test showed significant correlation between hydatid cyst infection and sex of animal (p - value = 0.007) (Table 2). Source of animals Out of 210 cattle inspected, one cattle from Khartoum (0.4%), 8 cattle from Darfur (3.8) and 3 cattle from white Nile State (1.4) were found positive for bovine hydatidosis.( Table2).The highest rate of infection was in White Nile State (11.5%), Darfur had infection rate of (10.0%) (Table 2). The Chisquare results showed that there is significant association between hydatid infection and source of animal (p value = 0.006) (Table 2). Breeds Out of 204 local animals, 11 were infected. The rate of infection was (5.4%). The total number of cross breed animals examined was 6. Among these, there was only one case infected with (16.6%) infection rate (Table 2). The Chi-square test showed insignificant association between hydatid cyst infection and breed (p value = 0.301) (Table 2). Presence of other animals The prevalence of hydatid cyst in Presence of other animals in the herd was investigated as shown in (Table 2 ), 53 cattle were found with other animals and 157 of cattle were found separated from other animals. Infection was more in mixed herd (9.4%) compared to cattle separated from animals (4.5%)(Table2). The Chi-square test showed insignificant association between hydatid cyst and presence of other animals (p value = 0.156) (Table2). Body condition The body condition of animals and the prevalence of hydatid cyst has been investigated. In good condition the rate of infection was (0.6%), while 45 of cattle were found to be in poor condition and the rate of infection was (24.4%) (Table2). Chi-square test showed insignificant association between the infection and body condition (p-value = 0.00) (Table2). Disease exposure 75 of cattle were previously exposed to the disease and the rate of infection was (8.0%), while 135 were not with (4.4%) infection rate (Table 2). Chi-square test showed insignificant association between the infection and disease exposure (p-value = 0.223) (Table 2). Grazing system Grazing system of animals and the presence of hydatid cyst has been investigated. 140 cattle were reared in a semi closed system showed an infection rate of (5.0%), while 70 of cattle were reared in an open grazing system with an infection rate of (7.1%)(Table 2). Chi-square test showed no significant association between the infection and grazing system (p-value = 0.366) (Table2). Presence of dogs The correlation between presences of dogs in association with the hydatid cyst infection has been investigated. The rate of infection is higher in the presence of dogs (20.4%) compared to a rate of the infection of (0.6%) when dogs were absent (Table 2).

3 23 The Chi-square test showed highly significant association between the infection and presence of dogs (p value= 0.000) (Table). Herd size Herd size of animals and the prevalence of hydatid cyst have been investigated. 49 cattle were classified as small and the rate of infection was (4.1%), 143 cattle were classified as medium herd size with an infection rate of(5.6%) and 18 of cattle were classified as large with an infection rate of (11.1)(Table 2). Chi-square test showed no significant association between the infection and herd size (p value=0.335) (Table 2). Table 2: Risk factors associated with the prevalence of bovine hydatidosis in cattle slaughtered at Khartoum state Risk factor No. inspected No. Affected (%) p-value Age of animals 0.018* <5 years (1.9) >5 years (9.4) Sex of animals 0.007* Female 8 3 (37.5) Male (4.5) Source of animals 0.006* Local (1.0) Darfur 80 8 (10.0) White Nile 26 3 (11.5) Breed Cross 6 1 (16.7) Local (5.4) Presence of other animals No (4.5) Yes 53 5 (9.4) Body condition 0.000** Poor (24.4) Good (0.6) Disease exposure Yes 75 6 (8.0) No (4.4) Grazing system Semi closed (5.0) Open 70 5 (7.0) Presence of dogs 0.000** No (0.6) Yes (20.4) Herd size Small 49 2 (4.1) Medium (5.6) Large 18 2 (11.1) *significant at P < 0.05, **significant at P < 0.01

4 24 Fig. 1: Diagrams illustrating risk factors associated with the prevalence of bovine hydatidosis in cattle slaughtered at Khartoum State. Though Echinococcosis is an important zoonotic disease, however, it is a neglected public health problem in Africa, especially in rural communities. The disease causes considerable economic loss via condemnation of offal in slaughterhouses. In addition, it may culminate in an anaphylactic reaction, which may be fatal in human. Generally, many potential risk factors might influence the prevalence of bovine hydatidosis and play a role in transmission of the disease. In spite of this, no in-depth studies were adopted to investigate the association of these risk factors with the prevalence of this important zoonotic disease. The overall prevalence rate recorded in this study (5.7%) was comparable with previous studies conducted in the same abattoirs but disagrees with that reported in Sinnar and Blue Nile [7]. Though many studies were conducted to reveal the infection rate of hydatidosis in different parts of the Sudan, however, no attempts were done to investigate the risk factors necessary for dissemination of the disease. In this scientific work, the prevalence rate of bovine Echinococcosis was investigated in association with many incriminated risk factors which may lead to spreading of the disease.

5 25 The study showed significant association between the prevalence of hydatidosis and age (p-value=0.018). Animals above five years of age were highly infected (9.4%) than animals less than five years of age (1.9%). This finding is in agreement with previous reports [8-12]. This could b mainly due to their longer exposure to Echinococcus granulosus and to lower immunity. This study showed significant association between hydatid cyst infections and sex of animals (p-value= 0.007). The rate of infection within females was (37.5%), and that of males was (4.5%). Both males and females can be infected by hydatidosis but prevalence was significantly associated with the females. This agreed with a previous report [13].This observation may be due to the fewer number of females slaughter as compared to males. Again this significant association of hydatidosis to the female sex may be due to immunological factors,that the males are more resistant to the infection in terms of their defensive mechanism. In this study the highest rate of infection was in White Nile State (11.5%), Darfur had the infection rate of (10.0%), but in Khartoum State the rate was lower (1.0%). The Chi-square results showed a significant association among hydatid infection in the different areas of animal (p-value=0.006). This result agreed with earlier findings [13-14] who found that, the difference may be due to variation in the agro ecology of the study areas and the source and grazing system of the animals. The high rate of infection in the White Nile State might be due to the greater number of stray dogs. In addition, backyard slaughtering of ruminants might be also responsible for dissemination of the parasite. Besides, domestic dogs play a significant role in maintenance of the life cycle and become potential source of infection for domestic ungulates. Generally the variation in prevalence rate among different geographical locations could be attributed to the strain differences of Echinococcus granulosus that exists in different geographical location [15]. The present study showed significant association between hydatid cyst and Presence of other animals (p-value=0.156). Infection was more in mixed herd (9.4%) compared to animals separated from other animals (4.5%). According to the result mixed herd including dogs play a significant role in life cycle of the disease besides different infection may occur between different species of animals. The transmission of different strains of Echinococcus granulosus, might be also due to variations in feeding behaviors of the animals and animal husbandry practices. [2] Found that there is an evidence indicates the existence of a number of strains of Echinococcus grsanulosus, which differ morphologically and biochemically. These include strain which utilize sheep / dog, horse / dog, camel / dog, pig / dog, goat / dog, cattle / dog and man / dog cycles. Body condition significantly affected the prevalence of hydatidosis (p-value = 0.00). Animals with poor body condition revealed higher prevalence of hydatidosis (24.4%) compared to good body condition (0.6%). This finding is in agreement with the work of [16].This is in line with previous study [17] and disagree with [14] who found that hydatidosis was recorded in both good and poor animals. The differences between body conditions score may be due to the retarded growth, weight loss and moderate to severe infection in such animals as described by [18] that animal with poor body condition has low immunity to hydatid disease. Previous history of presence of hydatidosis showed significant association (p value = 0.223), the prevalence was highest in exposed animals. The association of dogs and presence of the hydatid cyst infection has been investigated. The rate of infection is higher in the presence of dogs (20.4%) compared to absence of dogs (0.6).The Chi-square test showed highly significant association between infection and presence of dogs ( p value = 0.000). This result is in agreement with [16]. It was also found that stray dogs play a significant role in maintenance of the life cycle and become potential source of infection for domestic animals [18]. According to [19] the lifecycle of the parasite in each location depends on various factors. The main factor is the facility to reach discarded entrails of livestock by dogs. In the fact the dogs may be infected by consuming non-disposed infected organs in abattoirs, then transmitting disease to live cattle when grazing on grass which infected by Echinococcus eggs. However, breed of animals and herd size seem to have no role to play in transmission of bovine hydatidosis.

6 26 IV. CONCLUSION AND RECOMMENDATIONS It was found that presence of dogs within cattle herds or stray dogs roaming around the slaughterhouses is the most serious risk factor for dissemination of hydatidosis followed by age while breed and herd size were found to be of no significance in spreading of hydatid disease. It was that strategies for controlling this serious zoonotic disease in Sudan should be directed towards reduction if not eradication of the stray dogs population and that is through humane killing. REFERENCES [1] Assefa, AandTesfay. H (2014) Hydatidosis In Cattle Slaughtered At Adigrat Municipal Abattoir, Ethiopia International Journal Of Tropical Disease and Health 4.Polydorou, F Animal Health and Economics: Case Study of Echinococcosis with a reference to Cyprus. Bull. off. int. des epiz.,93: [2] Soulsby, E. J.L. M. (1982). Helminthes, arthropods and protozoa of domesticated animals, seventh edition, London: Baillieretindall, [3] Smyth JD, Barrett NJ (1980).Procedure for testing the viability of human hydatid cysts following surgical removal, especially after chemotherapy.trans. Royal Soc. Trop. Med. Hyg. 74: [4] Macpherson CNL (1985). Epidemiology of hydatid disease in Kenya.In a study of the domestic intermediate hosts in masailan. Trans. R. Soc. Trop. Med. Hyg. 79(2): [5] Wendimagegnehu, B., Berhanu and T.., Dawit G. (2014) Infection Rates andeconomic Significance of Bovine Hydatidosis Slaughtered in Soddo Municipality Abattoir ActaParasitologicaGlobalis 5 (1): [6] Martin, S.Wayne, M. A.,Willeberg, p. (1987).veterinary Epidemiology principal and methods (low state university press/ames. : PAHO. [7] Ibrahim, K.; Romig, T.; Peter, K. And Omer, R. A. (2011). Molecular survey on cystic echinococcosis in Sinnararea, Blue Nile state, Sudan. Chinese Medical Journal, Vol. 124, No. 18, [8] Regassa, F, Molla A, Bekelle J (2010). Study of the prevalence of cystic hydatidosis and its economic significance in cattle slaughtered at Hawassa Municipal abattoir, Ethiopia. Trop Anim Health Prod.;42: [9] Endrias, A., Yechale, T., Assefa M (2010). Bovine hydatidosis in Ambo municipal abattoir, West Shoa, Ethiopia. Ethiop Vet J. 14(1):1-14. [10] Genet, M., Tadesse, G., Basaznew B, Mersha C (2012). Pathological Conditions Causing Organ and Carcass Condemnation and Their Financial Losses in Cattle Slaughtered in Gondar, Northwest Ethiopia. African J Basic &Appl Sci.;4(6): [11] Endalew, D., Nuraddis, I (2013). Prevalence and economic importance of hydatidosis in cattle slaughtered at North Gondar Elfora abattoir. Europ J Appl Sci. 5(1): [12] Debela A, Fanta D, Benti D, Nebyu M and Zerihun A, ( 2014 ) Epidemiology and Financial Loss of Bovine Hydatidosis in Cattle Slaughtered at Nekemte Municipal Abattoir, Ethiopia ActaParasitologicaGlobalis 5 (2): [13] Okolugbo, B., Luka, S., Ndams I (2014). Enzyme-Linked Immunosorbent Assay (Elisa) In TheSerodiagnosis Of Hydatidosis In Camels (Camelus dromedarius) And Cattle In Sokoto, Northern Nigeria. The Internet Journal of Infectious Diseases.Volume 13 Number 1. [14] Abunna, F., Fentaye, S., Megersa, B., Regassa, A.(2012) Prevalence of bovine hydatidosis in Kombolcha ELFORA abattoir, North Eastern Ethiopia Open Journal of Animal Sciences. Vol.2, No.4, [15] McManus, D.P (2006). Molecular discrimination of taeniidcestodes. See comment in PubMed Commons below ParasitolInt 55 Suppl: S [16] Abera, M., Teame,S, and Sheferaw, D. (2013). Cystic Echinococcosis of Cattle injimma Municipal Abattoir, South West Ethiopia. DOI: /idosi.gv ISSN [17] Mulatu, M., Mekonnen, B., Tassew, H and Kumar, A (2013). Bovine Hydatidosis in Eastern Part of Ethiopia Momona Ethiopian Journal of Science (MEJS), V5(1) ,, CNCS, Mekelle University, ISSN: X [18] Polydorous Guadu, T., Gebremicael, Y and Chanie, M (2013) Economic and Zoonotic Importance of Bovine Hydatidosis in Shire Municipal Abattoir, North West Zone, Tigary Region, Ethiopia. Acta Parasitologica Globalis 4 (3): 92-98, 2013 ISSN [19] Tappe, K. H., Mousavi, S. J and Barazesh, A.(2011). Prevalence and fertility of hydatid cyst in slaughtered livestock of Urmia city, Northwest Iran. Journal of Parasitology and Vector Biology Vol. 3(2), pp