Prevalence and Associated Risk Factors of Ovine Oestrosis in Dendi District of Central Ethiopia

Introduction

Myiasis is an infestation of tissue and organs of animals or man with dipteran fly larvae.^1–3 Oestrosis is a myiasis caused by dipteran flies of the family Oestridae, genus Oestrus, and species of Oestrus ovis. O. ovis, the sheep bot fly, is an economically important, obligatory parasite of the nasal cavities and adjoining sinuses of sheep and goats.^3,4 Oestrosis is primarily a disease of sheep, which are widely distributed across the world. Goats are less affected than sheep. Other animals, including humans, are also affected.^2,5

The O. ovis infestation phase arises when the adult fly starts to deposit the larvae. Larvae pass through three stages or instars.⁶ The female O. ovis fly is viviparous and deposits L1 in or around the nostrils. Inside the nasal cavities, the first instar larvae attach to the mucous membrane, change to second instars, move up to the sinuses and molt to L3. Finally, mature third instar larvae return to the nasal passage, are expelled out by the sneezing action of the host, and pupate in the soil to give rise to further generations of adults.^2,5

Oestrus ovis is a problem for sheep and goats worldwide.⁶ Both adult and larval stages have an effect on the host. The activities of adult flies during the deposition of larvae cause annoyance, which results in loss of body condition.^2,5 Infestation by larvae of O. ovis causes great irritation to the host which results from mechanical activity of the mouth hooks and larval spines as well as the effect of proteolytic enzymes excreted or secreted by O. ovis larvae. The damage caused by the larval stage depends on the number of larvae and the site of infestation.² The activities of larvae in sheep cause nasal discharge, sneezing and dyspnea. Death of larvae inside the sinus predisposes sheep to secondary bacterial infection. Larvae sometimes migrate into the brain of sheep and cause in coordination called “false gid”.^4,6

Oestrosis in small ruminants causes substantial economic losses to sheep and goat producers.^6,7 The pathogenic effects cause a reduction in production and serious economic losses, which have been estimated at 1.1–4.6 kg of meat, 200–500 g of wool, and up to 10% of milk per animal.² Mozaffari et al⁷ also reported a 10% mortality rate of sheep with O. ovis infestation. Besides, oestrosis has public health significance. In humans, O. ovis larvae infestation causes ocular myiasis (ophthalmomyiasis)⁸ and, rarely, nasal myiasis.^9,10

In Ethiopia, a few studies were conducted on ovine oestrosis. Prevalence of 77.42% in Debre Zeit area, Central Ethiopia,¹¹ 94.6% in Central Oromia¹² and 69.8% in Ambo were reported in sheep.¹³ These shows, O. ovis are a common and important parasite of sheep in the country. Moreover, presence of large number of sheep population, conducive climatic conditions for the parasite to complete its life cycle, extensive grazing system used in which the animal on pasture throughout all months of the year and increased production systems in the country create ideal conditions for the spreading out of this type of parasitism in small ruminants. Although, the impact of O. ovis on sheep producer is known, larval burden, prevalence and risk factors associated with parasite distribution are not known in Dendi district. An assessment of the current situation of ovine oestrosis in the study area will provide baseline information against the diseases and plays a significant role in designing strategic control toward the parasites. Therefore, the objectives of this study were to estimate the prevalence, larval burden, risk factors associated with O. ovis infestation and predilection site of the larvae in sheep slaughtered at Ginchi town, Dendi district of West Shoa Zone, Ethiopia.

Materials and Methods

Study Area

The study was conducted from November 2017 to April 2018 in the Dendi district of the West Shewa Zone, Oromia regional state, Ethiopia. Dendi district is located 79 km from Addis Ababa with an elevation ranging from 2000 to 3288 meters above sea level. Geographically, the district lies within the coordinates of 8°43ꞌN-9°17ꞌN and 37°47ꞌE-38°20ꞌE. Dendi is bordered on the west by Ambo, on the east by Ejerie, on the north by Jeldu and on the south by the Southwest Shewa Zone. The administrative town of Dendi district is Ginchi. The temperature ranges from 9.3–23.8°C and the annual rainfall of the Dendi district ranges from 750–1170 mm. The number of sheep in the West Shewa Zone was estimated to be around 1,028,162.¹⁴

Study Animal

The study was carried out in sheep bought for slaughter by restaurant owners of Ginchi town, Dendi district, West Shewa Zone, Oromia regional state, Ethiopia. The sheep slaughtered here came from surrounding kebeles of the district. For the prevalence study, only apparently healthy animals able to be slaughtered and both female and male with the age reached for slaughter (approximately 6 months and above) were included in the study. Dentation was used to estimate the age of each sheep,¹⁵ which was then divided into two groups: adult (> 1 year) and young (1 year) to determine the presence of age-related O. ovis larvae infestation.¹² Information on the origin and sex of the sheep was obtained from restaurant owners.

Study Design

A cross-sectional study was conducted to estimate the prevalence and risk factors associated with O. ovis in sheep in the study area, as well as to determine the larvae burden and preferred site of O. ovis larvae.

Sampling Technique

Five restaurants found in Ginchi town, Dendi district, West Shewa were selected purposively. Weekly visits to selected restaurants private slaughter slabs were made to collect the samples. Slaughtered sheep heads were randomly selected from each of the selected restaurants.

Collection and Examination of Sheep Heads

Heads of selected sheep were put into separate plastic bags, labeled, stored in the icebox and transported to the laboratory of Veterinary Laboratory Technology, Guder Mamo Mezemir Campus, Ambo University, for examination. In the laboratory, the skin was removed and the head was parted longitudinally into two symmetrical parts by using a hand saw,^11–13 and inspected visually for infestation. From positive sheep heads, all existing larvae were collected using forceps and counted. The site in which the larvae were found was recorded.

Data Analysis

The collected data were entered into a Microsoft Excel spread sheet. The Statistical Package for the Social Sciences (SPSS) version 20 software was used to analyze the data. A Chi-square test (ᵡ²) was used to determine the statistical significance of the association of O. ovis infection with sex, age, and origin of sheep. The statistical analysis was considered significant at p< 0.05.

Results

From the total of 180 examined sheep heads, 104 (57.8%) were infested with larvae of O. ovis. The prevalence of O. ovis larvae infestation based on the sex, age, and origin of sheep were summarized in Table 1. In the present study, there was no significant variation (p > 0.05) of O. ovis infection between sexes, age, and origin of sheep.

Table 1 Prevalence of Oestrus ovis Infection on Basis of Sex, Age and Origin of Sheep

Larvae Burden of Oestrus ovis

The larvae found in all positive sheep heads were counted and recorded. From 104 infested sheep, a total of 664 larvae were detected in different parts of sheep heads. The mean larval intensity per infected sheep was 6.38. In this study, the number of recovered larvae ranged from 1 to 26. The maximum and minimum numbers of larvae detected in this study were 26 and 1, respectively (Table 2).

Table 2 Mean Larval Burdens in the Heads of Examined Sheep

Predilection Sites of Oestrus ovis Larvae

The nasal cavity, frontal sinus, and nasal sinus were the predilection sites of the detected O. ovis larvae in the current study. Smaller numbers of larvae were recovered from the nasal cavities of sheep (Table 3).

Table 3 Common Predilection Sites of Recovered Oestrus ovis Larvae

Discussions

This study revealed that O. ovis is a common and important parasite of sheep in the study area. In the current study, an overall 57.8% prevalence of O. ovis infestation was recorded in sheep. On the contrary, higher prevalence were reported by Yilma, Genet¹¹ in Debre Zeit, Central Ethiopia; Gebremedhin¹³ in Ambo; and Alem et al¹² in Central Oromia, Ethiopia. The difference in prevalence may be attributed to differences in sample size, study periods, and agroecology like moisture, temperatures, and altitude that create a suitable environment for the nasal bot fly to exist, the absence of treatments against this parasite, and the absence of community awareness of the effect and controlling methods of the parasite in the area.⁵

This study revealed a higher prevalence of ovine oestrosis in relation to the studies conducted in some other countries, which reported 13.7% in Brazil,¹⁶ 40.3% in North Eastern Turkey,¹⁷ 40.83% in Iraq,¹⁸ 19% in Ecuador,¹⁹ 38.71% in Eastern Turkey.²⁰ This might be due to the breed of sheep in other parts of the world being more resistant to oestrosis than the sheep in the study area. The climatic and geographical variations of the study area and other parts of the world might also have created differences in prevalence.

In the current study, a statistically significant difference (p>0.05) was not observed in the prevalence of O. ovis in relation to all considered risk factors such as sex, age, and origin of sheep in the study. This finding is similar to previous reports by Arslan et al¹⁷ and Özdal et al.²⁰ This might be due to the ability of the O. ovis fly to feed on any available animal.² This contradicts previous findings by Abo-Shehada et al;²¹ Shoorijeh et al;²² and, Gebremedhin¹³ who found a significant difference in O. ovis infestation between males and females. Significant variation in O. ovis infestation among young and adults, which is inconsistent with our findings, was reported by Yilma and Genet¹¹ Horak²³ and Papadopoulos et al²⁴ respectively.

In this study, no statistical difference (p > 0.05) was also found between the origins of sheep that were oestrosis positive. This might be due to the similarity of climatic conditions, which are an important factor for the distribution of the fly between the origins of the sheep.^5,25 This finding agreed with that of Murguı́a et al²⁶ in the Central Region of Yucatan, Mexico; Negm-Eldin et al²⁷ in the Green Mountain area of Libya, Saleem et al²⁸ in north India, which were insignificant with respect to the origin.

The current study revealed that there is a 6.38 mean larval burden of the O. ovis infestation in sheep. This disagrees with previous investigators’ findings by Caracappa et al,²⁹ Gebremedhin,¹³ Silva et al,¹⁶ Scala et al,³⁰ Alcaide et al³¹ who reported higher mean larval burdens from infected sheep. The differences might have originated from climatic and seasonal differences between the study areas and the immune state of the sheep. Poor management, presence of internal and external parasite infestation are also factors that aggravate the O. ovis infestation. The stocking density of the flock will also influence the infection of O. ovis.^4,5,32

O. ovis larvae were found in the nasal sinus, frontal sinus, and nasal cavity in the current study. Similar to our finding, the nasal and frontal sinus sites of O. ovis larvae was reported by Silva et al.¹⁶ Occurrence of O. ovis larvae in the nasal cavity of sheep was reported by Allaie et al.³

Conclusions and Recommendations

The prevalence of ovine oestrosis was identified for the first time in the study area, and the prevalence obtained was high. This indicates oestrosis is a common parasitic disease of sheep found in the Dendi district. Our study revealed that no statistical difference (p > 0.05) was found between age, sex, and origins of the animal and O. ovis infestation in sheep. The mean larval intensity per infected sheep was 6.38. During this study, the nasal cavity, frontal sinus and nasal sinus of sheep were identified as predilection sites of O. ovis larvae. Based on the above conclusions, the following facts are recommended: The seasonal variations in the distribution of O. ovis should be studied. Veterinary extension should be expanded to reduce O. ovis prevalence using appropriate antihelminthics and insect repellent insecticides.

Farmer’s awareness programs on the effects, prevention, and control methods of O. ovis infestation should be created.