Parasite Prevalence in Slaughtered Animals in Relation to Host Origin and Host Age

The parasitic infection has significant public health implications and can greatly affect the economies of countries. Parasitic infections cause significant economic losses to the livestock industry and agricultural communities. Infected animals often die, experience weight loss, have reduced milk production and may have organs that are unsuitable for human consumption. These impacts have been documented in previous studies (Suarez and Busetti, 1995; Murshed et al., 2022). Liver flukes and Echinococcus granulosus are common parasites affecting livestock. Domesticated ruminants, such as cattle and sheep, are particularly vulnerable to Fasciola hepatica (Kaplan, 2001) and F. gigantica (Mungube et al., 2006; Gabriël et al., 2022), which are well-known parasites in some countries. These parasites can cause significant economic losses in the livestock industry. Young cattle with acute liver disease and older cattle with chronic liver disease exhibit clinical signs of digestive inefficiency (Doyle, 2003; Ibrahim, 2010; Gabriël et al., 2022).
       
In Saudi Arabia, hydatidosis is a prevalent liver parasite in animals and humans and this represents a significant public health concern (Ibrahim, 2010). Previous studies have been conducted in certain regions of the country regarding the prevalence of parasites infecting cattle, sheep, goats and camels (Ibrahim et al., 2008; Ibrahim, 2010; Toulah et al., 2012; Toulah et al., 2017; Murshed et al., 2022; Al-Ghamdi et al., 2023). The productivity of livestock production has been greatly impacted by parasitic diseases. The infection prevalence of parasites in native and imported slaughtered animals has not received much attention, despite the fact that Saudi Arabia has data on animal parasites. This study aimed to determine the infection prevalence of parasites in slaughtered animals in relation to host origin and host age.

The current investigation was conducted in Al Mekhwah Province, located in the southwestern region of Saudi Arabia (19°46'45"N, 41°26'8"E). The study area is located at an altitude of zero meters above sea level. Al Makhwah has a subtropical desert climate. The annual average temperature in the district is 26.66°C, which is 0.35% lower than the average temperature in Saudi Arabia. Al Makhwah receives an average of 31.38 millimeters of precipitation annually, with 71.05 rainy days (19.47% of the year).
       
A total of 1208 examined animals (264 cattle, 440 sheep and 504 goats) were examined for parasitic infection during the six months from September 2021 to February 2022. All the animals examined were slaughtered at official abattoirs in Al Makhwah City, Saudi Arabia. The distribution of the sampled host population by host origin is presented in Table (1). The collected parasites were preserved, processed and identified (Levine, 1978). The parasite specimens were identified following of Soulsby (1982) and Bowman (2019).
 

       
The ecological terminology used in this work was in accordance with the description provided by Bush et al., (1997). The chi-square test (χ²) was used to examine the difference in parasite prevalence among host age and host origin. All statistical tests were conducted using SPSS 22.00 (USA).

The community of parasites included six species: three trematodes (Dicrocoelium dendriticum, Fasciola hepatica and Fasciola giagantica), two cestodes (Monezia expansa and Echinococcus granulosus) and one nematode (Haemonchus contortus). The infection prevalence among goats, sheep and cattle was 6.34, 7.5 and 4.56% respectively (Table 2). These species match those documented by Ibrahim et al., (2008) in southwestern Saudi Arabia’s Al-Baha region.
 

       
E. granulosus (hydatid cyst) had the highest prevalence in cattle (4.85%), sheep (4.77%) and goats (3.76%) while H. contortus had the lowest prevalence (Table 2). These findings are consistent with previous studies conducted by Ibrahim et al., (2008) and Toulah et al., (2017). The high rate of infection of hydatidosis can be explained by the close relationship between dogs and animal herds, especially those of sheep and goats. The close relationship between dogs, sheep and humans makes it more likely for the parasite’s life cycle to be completed. The high infection rate may be attributed to factors connected to the social and economic conditions of the population, such as the extensive use of traditional methods in raising small ruminants (extensive or semi-extensive grazing), the existence of a large number of sheepdogs that are drawn to the sheep farming sites and the illegal slaughter of animals (Ibrahim, 2010).
       
There was variation in the overall prevalence per age of the host among the animals examined. Old animals (over 1 year old) have higher prevalence rates than young ones in cattle, sheep and goats (Fig 1). The study revealed that there is a strong correlation between the rate of infection and the age of the host in cattle, sheep and goats. Significant differences were found in overall prevalence in cattle (χ²= 32.67, df= 1, P<0.001), sheep (χ²= 82.38, df= 1, P<0.001) and goats (χ²= 47.72, df= 1, P<0.001). The prevalence of parasite infection is highest in older age. Study findings are consistent with El-Ghareeb et al., (2017) and Murshed et al., (2022). Murshed et al., (2022) found a significant positive association between age class and D. dendriticum infection. Age differences can lead to varying levels of exposure to infection, as older animals may have encountered more infectious stages. Moreover, the parasite’s development can be influenced by the host in which it resides. For instance, a larger host can provide more space and energy resources, which can facilitate parasite development.
 

       
The prevalence of infection differed significantly between native and imported slaughtered animals (P<0.001). The infection rate in native animals was low (infection rates were 5.42, 6.5 and 3.69% in cattle, sheep and goats respectively) as compared to imported ones (infection rates were 11.36, 17.5 and 16.67 % in cattle, sheep and goats respectively) (Table 3). The overall prevalence of the parasite in imported slaughtered animals was significantly higher than natives’ ones in cattle (χ² = 78.27, df= 1, P<0.001), sheep (χ²= 72.43, df= 1, P<0.001) and goats (χ²= 37.23, df= 1, P<0.001). The highest prevalence rate was found in D. dendriticum, F. hepatica, M. expansa E. granulosus and H. contortus in imported slaughtered animals (Table 3). Toulah et al., (2017) and Murshed et al., (2022) reported similar findings. Nabavi et al., (2014) found that imported cattle from Pakistan had a significantly higher prevalence of Hydatidosis (15.1%) compared to native cattle from Iran (5.3%). It is recommended that the slaughtering of imported livestock should take place in industrial centers in order to prevent a potential increase in canine echinococcosis, which can lead to hydatidosis in humans and farm animals. On the other hand, El-Ghareeb et al., (2017) found a low infection rate of imported animals. The higher prevalence of the parasite in imported animals may be attributed to the difference in the feeding system of animals in Saudi Arabia. Most native demotic animals in Saudi Arabia are fed manually and not in the pasture.
 

Based on our findings, Hydatidosis was identified as the most prevalent parasitic disease. Imported animals had a higher parasitic infection compared to local animals. It is essential to take necessary measures to prevent the transmission of Hydatidosis and improper organ condemnation from abattoirs. We recommend conducting further research to identify the reasons why imported animals are more likely to become infected than local animals.

A special thanks and appreciation to the Deputyship for Research and Innovation, Ministry of Education of Saudi Arabia for funding this research work through project number MOE-BU-2-2020.

Funding
 
This study was sponsored by the Saudi Arabian Deputyship for Research and Innovation under the project number MOE-BU-2-2020 and the authors would like to express their appreciation to them for funding this research.
 
Author contributions
 
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Mohamed M. Ibrahim, Ali Al-Ghamdi, Kareem Morsy and Eltahir Idris. The first draft of the manuscript was written by Mohamed Mousa Ibrahim and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
 
Data availability
 
Our manuscript has no associated data.
 
Ethics approval
 
No approval of research ethics committees was required to accomplish the goals of this study.

The authors have no relevant financial or non-financial interests to disclose.