Internal and external parasites of camels ( Camelusdromedarius ) slaughtered at Addis Ababa Abattoir , Ethiopia

A cross-sectional study was undertakento estimate the prevalence of internal and external parasites of camels slaughtered at Addis Ababa abattoir, Ethiopia. A total of 384 of camels originating from Borena and Metehara areas were examined during the study period and all (100%) of them were found to harbor at least two parasite species. In this study,the prevalence of tick, gastrointestinal parasites, Cephalopinatitillator,Hydatid cyst, and Sarcoptesscabiei var. cameliwere 100, 95.6, 68.2, 65 and 35.4%, respectively. The gastrointestinal parasite’s ova/oocyte identified includeStrongylus species, Trichurisspecies, Strongyloidesspecies and coccidiaat prevalence of 78.1, 47.1, 44.5 and 25.3%, respectively. Of the total 1347 pooled samples of tick collected from 40 randomly selected camels.Rhipicephaluspulchelis, Rhipicephalusevertsievertsi, Hyalomma dromedary, Amblyommagemma,Amblyommavariegatum and Boophilusdecolaratuswere identified at a proportion of 53.90, 21.01, 13.66, 7.5, 3.19 and 0.74%, respectively. The average tick burden from half body region of camels was 33.7 ± 6.24 (range 26 to 53).In general, this study indicates that parasites are still the major problems hindering the productivity and health of camels, hence implementation of strategic control measures and further studies are recommended to reduce the effect of parasites on camel health and productivity.


INTRODUCTION
Camels are an important source of milk, meat and their dung is used for fires.They are also used for riding and transport purpose.In Ethiopia, camels are exported mainly to Egypt and Sudan, and are also slaughtered for meat consumption duringritual occasions (Dirie and Abdurahman, 2003).Despite the fact that, camels provide lots of socio-economic advantagesand are the preferred domestic animal species in the ever-changing climate, so far it was neglected by researchers and development planners (Bekele, 2010).

Study area
This study was conducted at Addis Ababa abattoir enterprise, Akaki branch, Ethiopia.All camels slaughtered were originated from the Borana(semi-arid) and Kereyu(arid) areas of Ethiopia.Borana is located at approximately 600 km South of Addis Ababa at an altitude of 500 to 2500 m above sea level.It has an annual rainfall of 450 to 650mm in bimodal pattern with long rains expected between March and May and the short rains between October and November.Kereyu is located at about 250 km East of Addis Ababa at 80° 54 E longitude and altitude of 930 m above sea level.It has an average annual rainfall of 504mm.The mean annual maximum and minimum temperature are 32.40 and 18.5°C, respectively (NMSA, 1999).

Studytype and animals
Cross-sectional study was undertaken, from November to April, on 384 camels to assess the prevalence and species/genus level composition ofinternal and external parasites of camels slaughtered at Addis Ababa abattoir.The number of camels slaughtered varied from 7 to 11 each day.The abattoir was visited two days a week.All camels slaughtered during the time of visitwere examined and sampled without discrimination of their age, sex, body condition and origin.

Data collection
General physical examination was conducted on each camel in the lairage.All data regarding the age (based on dentition), sex, body condition (hump structure) and origin of camels were recorded appropriately (Schwartz and Dioli, 1992;CACIA, 1995).

Fecalsample collection and examination
Fresh fecal samples were collected directly from the rectum of slaughtered camels.Each samplewas placed and codedappropriately in universal bottles, and transported using ice box into parasitology laboratory of College of Agricultural and Veterinary Medicine, Addis Ababa University.The collected samples wereexamined using simple sedimentation method for trematodes eggs and floatation method for eggs of nematodes, cestodes and coccidianoocysts (Soulsby, 1982;Urquhart et al., 1996).

Sample collection and identification of tick and mange mite
All visible adult ticks were collected from half-body regions (on right side) of camels.Ticks were collected in labeled plastic bottles containing 70% ethanolfrom 40 randomly selected camels.Skin of suspected camels affected by mange was scraped until capillary bleeding and the scraping waspreserved in a labeled bottle containing 10% formalin.Both tick and skin scraping samples were taken into parasitology laboratories of College of Agricultural and Veterinary Medicineof Addis Ababa Universityand College of Veterinary Medicine of Mekelle University.Identification of tickswas performed using the keys of Okello-Onenet al. (1999) and Walker et al. (2003).Identification of mites was carried out with the help of morphological characteristics after processing with 10% KOHsolution (Soulsby, 1982;Urquhart et al., 1996).

Examination of Cephalopinatitillator and hydatidcyst
After slaughtering, camel heads were dissected and gross examination was performedon the nasal cavity, frontal sinuses, turbinate bones and nasopharynx for the presence of Cephalopinatitillaterlarvae.Liver, lungs and heart of slaughtered camels were grossly examined and palpated for the presence of hydatidcyst.The contents of hydatid cysts were examinedafter aspiration using syringe and incision.

Data analysis
The data was entered into Microsoft excel spreadsheet and coded appropriately.For data analysis, SPSS version 16 was used.In this data analysis, descriptive statistics was used to determine the prevalence of parasites in camel.The chi-square test was also used to determine the existence of any association between the infection and the risk factors like age, origin, body condition score and sex.In all cases, 95% confidence intervals andP<0.05wereset for significance.

RESULTS
Out of the 384 camels examined,all (100%) of them were found to harbor two or more of the parasite species.In this study, four species of the gastrointestinal (GIT) parasite, six species of tick, one species of mite, hydatid cyst and C.titillatorlarvae were identified.The preva-lence of tick,GIT parasite, C.titillator,hydatic cystand mange mite infestation were 100,95.6,68.2, 65 and 35.4%, respectively (Table 1).Ticks were observed on all (100%) of the examined camels (Table 1).Of the total 1347 pooled hard ticks collected from the half body region of 40 camels,Rhipicephaluspulchelis, Rhipicephalusevertsievertsi, Hyalommadromedary,Amblyommagemma,Amblyommav ariegatum and Boophilusdecolaratuswere identified at a proportion of 53.90, 21.01, 13.66, 7.5, 3.19 and 0.74%, respectively (Table 4).The average tick burden from half body region of camels was 33.7±6.24(range 26 to 53).In addition to tick infestation, 136 (35.4%) of the examined camelshad mange mite infestation and only Sarcoptesscabiei var.cameli was identified from all of the collected skin scraping samples (Table 1).
The GIT parasites ova/oocyte identified during the study period include Stronglusspecies, Trichuris species, Strongyloidesspecies and coccidia at prevalence of 78.1, 47.1, 44.5 and 25.3%, respectively (Table 1).No trematode and cestode ova were identified.In general, there was no significant difference in the prevalence of parasites between/among the different risk factors (Table 2).C. titillator larvae were found in the nasal cavity, pharynx, turbinates and sinuses of 68.2% (n=262) camels (Table 1).Hydatid cysts were encountered in 65% (n=250) of camels (Table 1).Hydatid cysts of variable sizes (2 to 8 cm in diameter) were found in the lung, liver, and in both organs of the same animals at a proportion of 59.6% (n=149), 9.6% (n=24) and 30.8% (n=77), respectively.There was significant difference (P-value < 0.0001) in the localization of hydatid cysts between lungs and liver (Table 3).They were also varied in number from 2 to 7 on single organ.62% of infected camels harbored only cysts that had calcified or yellowish material inside the capsule, but the rest (38%) harbored at least one cyst that had clear water like fluid inside the capsule.

DISCUSSION
The present study assesses the prevalence of internal and external parasites encountered on camels slaughtered at Addis Ababa Abattoir, Ethiopia.All (100%) had two or more of the parasite species.Similar studies conducted by Al-Ani etal.(1998)andSharrifetal.(1998)inJordan,Anwar  and Khan (1998) in Pakistan, Dia (2006) in Burkina Faso and Bekele (2010) in Southern Ethiopia also reported a higher prevalence of parasites in camel.This high prevalence of parasites could be related to rearing of camels in marginal areas where veterinary services are not available or very limited (Tefera, 2004).
In this study, tick infestation was detected in all (100%) of the examined camels.This result was supplementary to the findings of Al-Ani et al. (1998), Melaku and Fesseha (2001), Dia (2006), Bekele (2010) and Kiros et al. (2014).Of the total 1347 pooled samples of ticks collected from half body region of 40 randomly selected camels,R.pulchelis,R.evertsievertsi, H. dromedary, A.gemma, A.variegatum and B.decolaratus were identified at a proportion of 53.90, 21.01, 13.66, 7.5, 3.19 and 0.74%, respectively.The average tick burden in half body region of camels was 33.7±6.24(range 26 to 53).Similar species of ticks and greater tick load per camel were also reported by Zeleke and Bekele (2004), Bekele (2010), Nazifi et al. (2011) and Kiros et al. (2014).In addition to feeding on animal blood, ticks also act as vector for diseases, causing tick paralysis, and direct damage to tissue, so that providing entry for opportunistic micro-organisms and fly larvae.Tick infestation also causes loss of appetite, leading to a reduction in growth rate and decreased productivity, and results in increased calf mortality (Schwartz et al., 1983;Hart, 1990;Nelson et al., 1977;Jabbar et al., 2007).
The prevalence of hydatidcyst recorded in this study was 65%.This resultwas higher than the findings of Wubet (1987), Abdul-Salam (1988), Woldemeskel (2001), Ahmadi (2005), Bitsat (2009) and Mohammed (2010).The high prevalence in the present study could be due to the presence of high population of dogs which are closely associated with livestock in the field and barn as well as due to high population of wild carnivores in the area of the majority camels origin (Borena) (Balako, 1999) and due to lack of proper condemnation of organs infected with hydatidcyst in pastoral areas (Bekele, 2008).These facilitate easy access of infected organs to dogs and wild carnivores which are the principal definitive hosts and maintain the life cycle of the parasite.Hydatid cysts varied in number from 2 to 7 on single organ.They were also of variable sizes (2 to 8 cm in diameter) and found at the proportion of 59.6% in the lung, 9.6% in liver and 30.8% both in lung and liver of infected animals.However, the findings of Abdl-hafez et al. (1986), Kamhawi et al. (1995), Ibrahim and Craig (1998.) and Haridy et al. (2006) indicated a higher rate of liver infection than lung.62% of infected camels harbored only calcified cysts but the rest (38%) harbored at least one non calcified cyst.This was in accordance with Abdl-hafez et al. (1986), Kamhawi et al.(1995), Chai et al.(1998), Sharrif et al. (1998), Ahmadi (2005) and Bitsat (2009).
In general, this and others studies indicated that parasites are among the major constraints of camel health and production.Considering the existence of limited veterinary service in camel rearing areas, well integrated studies and appropriate control measure should be implemented to improve the health and productivity of camels.Furthermore, due to the zoonotic importance of hydatidosis and S.scabiei var.cameli,public awareness should be created to control these parasites.

Table 2 .
The distribution of tick, Cephalopinatitillator, hydatid cysts, Sarcoptesscabiei var.cameli and GIT parasites infestation among age, sex, origin and body condition score in camels slaughtered at Addis Ababa abattoir, Ethiopia.

Table 3 .
Organ distribution of hydatid cysts in camels slaughtered at Addis Ababa abattoir, Ethiopia.

Table 4 .
The proportion of tick species collected from 40 randomly selected camels slaughtered at Addis Ababa abattoir, Ethiopia.