Trop Anim Health Prod DOI 10.1007/s11250-014-0646-x
REGULAR ARTICLES
Cystic hydatidosis in slaughtered goats from various municipal abattoirs in Oman Fadya Al-Kitani & Senan Baqir & Muhammad Hammad Hussain & Derek Roberts
Received: 9 June 2014 / Accepted: 13 July 2014 # Springer Science+Business Media Dordrecht 2014
Abstract A passive surveillance study was conducted from April 2012 to April 2013 to determine the incidence, the affect of age, sex and cyst location, fertility, and viability on the occurrence of cystic hydatidosis in slaughtered goats from six municipal abattoirs around Oman. Morphologic characterization of suspected visceral organs has shown that Echinococcos granulosus (E. granulosus) metacestodes were present in 9.2 % of the total samples (682). Incidence (per 10,000) varied from 1.4 to 1.5. There was a significant difference between abattoirs, with Salalah having the highest infection (63.2 %), followed by Nizwa (27.2 %), Al Buraimi (10.8 %), Bousher (7.2 %), and the lowest in Sohar (1.6 %). Infection was significantly higher in indigenous goats (22.1 %) compared with imported breeds (2.5 %) from Somalia. The visceral organs were found harboring one or more hydatid cysts. Greatest cyst infection was recorded in lungs (53.4 %), followed by heart (50 %), liver (6.2 %), and multiple organs (14 %). A significant difference was observed between females (25 %) and male goats (6 %). Furthermore, the fertility of the hydatid cysts was found higher in heart and lungs (100 %, 51.6 %) and the viability rate of protoscolices was high (64 %). The findings of this study demonstrated that cystic hydatidosis is common and widely distributed in local goats, and they might play an important role in the life cycle and transmission of this zoonosis in Oman.
Keywords Abattoirs . Cystic hydatidosis . Goats . Oman F. Al-Kitani (*) : S. Baqir : D. Roberts Department of Biology, College of Science, Sultan Qaboos University, Muscat, Oman e-mail:
[email protected] F. Al-Kitani : M. H. Hussain Animal Health Research Centre, Ministry of Agriculture and Fisheries, Muscat, Oman
Introduction Cystic hydatidosis is a silent cyclozoonotic infection of humans and domestic animals caused by infection with the larval (metacestode) stages of dog tapeworms belonging to the genus Echinococcus (family Taeniidae) and are also referred to as echinococcosis (Craig et al. 2007). The disease is known to be one of the most important parasitic infections in human and livestock worldwide, it is also considered an emerging or re-emerging disease, and the geographic distribution and extent are greater than previously believed (Thompson and McManus 2002; Torgerson and Budke 2003; Craig et al. 2007; Dakkak 2010). Cystic hydatidosis is a major public health problem and significant veterinary and economic impact (Craig and Pawlowski 2002; Sadjjadi 2006). In farm animals, cystic hydatidosis causes considerable economic problems due to significant losses of livers and reducing meat and milk production (Daryani et al. 2007). In addition, these losses are of significance in countries with low economic outputs where livestock production is of particular importance (Daryani et al. 2007; Berhe 2009). The life cycle of E. granulosus is indirect; it involves domestic and wild carnivores (e.g., dogs, jackals, hyenas, foxes, and wolves) as definitive hosts (Thompson 1995). However, domestic intermediate hosts such as livestock are major reservoirs of this disease for humans (Daryani et al. 2007). Cestode segments (proglottids) containing free eggs are released from the intestinal tract of the final hosts into the environment, where after accidental ingestion of eggs by an intermediate host (animal or human), a larval or cyst stage develops in the internal organs (Eckert and Deplazes 2004). The life cycle is completed when definitive hosts eat the infected organs with cystic hydatidosis (Cardonaa and Carmena 2013). E. granulosus has the ability to adapt to different hosts (domestic and wild animals and human) that help to distribute
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this parasite over a wide range. This leads to great genetic variation among E. granulosus strains (Thompson and McManus 2002). To date, molecular characterization of E. granulosus using mitochondrial DNA (mtDNA) sequences, have identified 10 distinct genetic strains (G1– G10) (Bowles and McManus 1993; Zhang et al. 1998; Snabel et al. 2000; McManus and Thompson 2003). In addition, these differences have important applications in the study of epidemiology and control of this parasite (Sharbatkhori et al. 2010). Cystic hydatidosis is endemic across Arab North Africa from Morocco to Egypt and in all the west Asian countries of the Middle East (Dar and Alkarmi 1997). It has been reported in livestock and in humans from many countries of the Middle East. Epidemiologic study on cystic echinococcosis in northern Iraq was conducted between 1990 and 1998 by Saeed et al. (2000); it has showed the infection rate in sheep, goat, and cattle were 15.0, 6.2, and 10 %, respectively, and high prevalence of E. granulosus was in dogs 49.5 %. In the eastern part of Kuwait, this disease was reported in sheep (Hassounah and Behbehani 1976). The prevalence of cystic hydatidosis in slaughtered animals in Saudi Arabia at Al-Baha region was studied by Ibrahim 2010 and found to be 32.85, 8.28, 12.61, and 6.56 % in camels, cattle, sheep, and goats, respectively. This disease was also reported in livestock in different parts of Iran (Ahmadi 2005; Sadjjadi 2006; Daryani, et al. 2007; Adinehbeigi, et al. 2013). In Oman, cystic hydatidosis is counted as a negligible disease in term of its importance, so its significance, economic impact and prevalence rate in domestic animals or human has not been established. However, a few seropositive cases of cystic hydatidosis have been reported from Dhofar region in human and camels (Idris et al. 1999; Sadjjadi 2006). Hence, this is the first reported attempted to provide a clearer picture of the prevalence and morphological characterization of slaughtered goats from six municipal abattoirs located at different governorates of the Sultanate. As such, the objectives of this study were to investigate the epidemiology of cystic hydatidosis in slaughtered goats according to their age, sex, cyst fertility, cyst viability, and cyst location from main six municipal abattoirs (Boushar, Nizwa, Salalah and Sohar, Sur, and Al Buraimi).
Materials and methods Location and description of study areas The epidemiologic surveillance for cystic hydatidosis was conducted during April 2012 to April 2013. Central municipal abattoirs located at six governorates were targeted in this study (Fig. 1); Muscat (Boushar centre municipal abattoirs), Dhofar (Salalah centre municipal abattoirs), Al Batinah (Sohar centre
Fig. 1 Map of the Sultanate of Oman shows the location of the six abattoirs (Salalah, Nizwa, Sur,Boushar, Al Buraimi and Sohar) in which the organs samples were collected
municipal abattoirs), Al Dakhiliyah (Nizwa centre municipal abattoirs), Al Sharqiyah (Sur centre municipal abattoirs), and Al Buraimi (Buraimi centre municipal abattoirs). The selected areas differ in their geography, climate, livestock husbandry and human behaviors. Study population During the study period, 1,352,439 slaughtered goats were examined at municipal abattoirs including males and females of various ages. Among this population, 682 of the slaughtered goats (235 indigenous and 447 imported breeds from Somalia) were suspected to have cystic hydatidosis, and their affected organs were removed for laboratory examination. Inspection and data collection of slaughtered goats Carcasses from the slaughtered goats were examined through visual inspection, palpation, and symmetric incision of different organs (liver, lungs, kidney, heart, spleen, muscles, and mesenteric fats) by the duty veterinarians at the slaughterhouses according to procedures recommended by (WHO/ OIE 2001). All the necessary information about each individual suspected slaughtered goat was recorded in a special Performa distributed for the purpose of this study: sex and age categories of the goat, presence or absence of cysts, multiple or single cyst infection, organs infected with cystic hydatidosis, and the origin of the goats.
Trop Anim Health Prod Table 1 Percent positivity of suspected samples (n=682) examined for cystic hydatidosis from six municipal abattoirs in Oman
Abattoir
No. of organs examined
Positive cases N (%)
Sohar Nizwa Al Buraimi Salalah Bousher
243 81 37 19 292
4 (1.6) 22 (27.2) 4 (10.8) 12 (63.2) 21 (7.2)
Sur Total
10 682
0 (0.0) 63 (9.2)
Sample collection and preparation The viscera organs (livers, lungs, hearts, muscles, and mesenteric fats) suspected for cystic hydatidosis were removed from the slaughtered goats and collected in sterile plastic bags labeled with a reference numbers and date for each sample. These samples were then transported in a cool box for laboratory analysis.
Laboratory analysis 1. Morphological and microscopic examination of cystic hydatidosis suspected samples The cysts were examined morphologically, and observations regarding location, size, degeneration, and calcification were recorded. The fertility of cyst was judged by aspiration of the cystic fluid with a sterile syringe and examined under a stereo microscope for the presence of protoscolices. The morphology and ultra structure of the protoscolices were determined under the light microscope (×40). 2. Determination of the fertility status of the cysts Individual cysts were grossly examined for any evidence of degeneration and calcification. For the determination of the proportion of fertile cysts, the cyst wall was penetrated with a needle and opened up with a scalpel and scissors. The contents were transferred into a sterile container and
Goat population
Incidence per 10,000
26,420 1,542 13,625 23,765 96,088
1.51 142.67 2.94 5.05 2.19
7,277 1,352,439
0.00 0.47
examined microscopically (×40) for the presence of protoscolices by adding glycerin and placing between two microscopic slides (Macpherson1985). Cysts that contained no protoscolices as well as degenerated or calcified were considered unfertile. 3. Determination of the viability of the protoscolices The viability of protoscolices for each fertile cyst was determined by adding a drop of 0.1 % aqueous eosin solution stain (Smyth and Barrett 1980) to equal volumes of protoscolices in hydatid fluid on the microscope slide, with the principle that viable protoscolices should completely or partially exclude the dye while the dead ones take it up (Macpherson 1985).
Statistical analysis A computer software IBM SPSS version 21 was used for analysis. Chi-square test (χ2) with a p value of 0.01 was applied in this study.
Results and discussion This is a first epidemiologic report conducted to investigate the distribution of cystic hydatidosis in the slaughtered goats from six municipal abattoirs in the Sultanate of Oman. A
Table 2 Distribution of hydatid cysts in different organs with respect to fertility status Positivity
Fertility
Organs
Total
Positive N (%)
Fertile N (%)
Sterile N (%)
Calcified N (%)
Degenerated N (%)
Lungs Livers Lungs &Livers Heart Fats Multiple Total
58 406 5 2 168 43 682
31 (53.4) 25 (6.2) 0 (0.0) 1 (50.0) 0 (0.0) 6 (14.0) 63 (9.2)
16 (51.6) 7 (28) 0 (0.0) 1 (100) 0 (0.0) 1 (16.7) 25 (39.7)
9 (29) 5 (20) 0 (0.0) 0 (0.0) 0 (0.0) 1 (16.7) 15 (23.8)
0 (0.0) 10 (40) 0 (0.0) 0 (0.0) 0 (0.0) 4 (66.7) 14 (22.2)
6 (19.4) 3 (12) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 9 (14.3)
Trop Anim Health Prod Table 3 Sex- and age-related prevalence of cystic hydatidosis in slaughtered goats from six municipal abattoirs in Oman Sex categories
Age groups (years)
Breed
Male
Positive N (%)
Female
Positive N (%)
5
Positive N (%)
Local Imported Total
135 435 570
25 (18.5) 10 (2.3) 35 (6.1)
100 12 112
27 (27) 1 (8.3) 28 (25)
136 164 300
28 (20.6) 4 (2.4) 32 (10.7)
98 276 374
23 (23.5) 6 (2.2) 29 (7.8)
5 3 8
1 (20) 1 (33.3) 2 (25)
limitation of this study was the absent of abattoirs in some governorates such as Musandam and Al Wustah (Fig. 1), which were thus excluded from this study, and the fact that most local goats, especially in villages and farms, are home slaughtered without any supervision. The results of this study indicated the presence of cystic hydatidosis in the local and imported breeds of goats subjected to the routine slaughtering in different geographical locations of the Sultanate. The majority of goats slaughtered in the abattoirs were imported from Somalia, where cystic hydatidosis is endemic (Over et al. 1992). The findings showed that 9.2 % of the slaughtered goats from the studied municipal abattoirs were infected with cystic hydatidosis. However, the rate of infection was significantly different among the six abattoirs, and the percentages of prevalence varied per each study location. Out of 682 suspected slaughtered goats examined for cystic hydatidosis, 9.2 % (63/682) were found harboring hydatid cysts (Table 1). Significant difference (χ2=114.17, p
