Gastrointestinal Helminths in Camels Slaughtered at Tamboul, Sudan: Prevalence and Risk Factor Analysis

 Corresponding author: Omer Hassan Mohamed Copyright © 2025 Author(s) retain the copyright of this article. This article is published under the terms of the Creative Commons Attribution License 4.0. Gastrointestinal Helminths in Camels Slaughtered at Tamboul, Sudan: Prevalence and Risk Factor Analysis Gayes Abdallah Abdallah 1, Awad Mahgoub Atta EL-Mannan 1, Fudol Husain Fudol Ismail 1, Habib Abaker Edrees Ahmed 1, Haytham Adam Abaker Boush 1, Motasem Mohammed Essa Saleh 1, Nabila Nasir Mandel Athrag 1, Salwa Abd Alrhman Ahmed 1, Samah Adam Ahmed Adam 1, Thoruaya Abd Alrhman Mohammed Ahme 1 and Omer Hassan Mohamed 2, * 1 Faculty of Veterinary Medicine, University of Al-butana, Sudan. 2 Faculty of Animal Production, University of Gezira, Sudan. GSC Biological and Pharmaceutical Sciences, 2025, 33(02), 392-399 Publication history: Received on 08 October 2025; revised on 14 November 2025; accepted on 17 November 2025 Article DOI: https://doi.org/10.30574/gscbps.2025.33.2.0426 Abstract Gastrointestinal helminth infections represent a major constraint to livestock productivity in arid and semi-arid regions. This study aimed to determine the prevalence, diagnostic performance, and associated risk factors of gastrointestinal helminths in camels slaughtered at the Tamboul Slaughterhouse, Gezira State, Sudan. A total of 60 camels were examined using three diagnostic techniques: direct faecal smear, sedimentation, and flotation tests. Helminth eggs were identified microscopically and classified to genus level. Of the total examined animals, 49 (81.7%) tested positive for one or more helminth genera. The most frequently detected species were Schistosoma (18.3%), Taenia (15.0%), and Paramphistomum (11.6%). The direct faecal smear demonstrated the highest diagnostic sensitivity (81.7%), while the flotation method showed the lowest (25%). Chi-square tests indicated no significant association between infection status and sex (χ²(1) = 0.00, p = 1.00), age (χ²(3) = 3.56, p = 0.314), or geographical origin (χ²(2) = 3.99, p = 0.136). The results confirm that gastrointestinal helminthiasis is endemic among camels in the Tamboul region, although infection prevalence did not differ significantly among demographic groups. The high infection rate highlights the need for improved helminth surveillance, regular deworming programs, and enhanced husbandry practices to reduce parasitic burdens and economic losses in camel production systems. Keywords: Camels; Gastrointestinal Helminths; Prevalence; Sudan; Chi-Square Analysis; Epidemiology 1. Introduction The dromedary camel (Camelus dromedarius) is a species of immense cultural, social, and economic importance across arid and semi-arid regions of Africa and Asia. Camels are uniquely adapted to extreme environmental conditions, serving as a vital source of meat, milk, wool, and reliable transport in environments unsuitable for other livestock (Yakaka et al., 2017). In Sudan, the camel population ranks as the second largest globally, estimated to exceed 4.85 million heads in 2017 (Department of Statistics, 2017). This population is distributed across numerous states, with major concentrations in the western and eastern regions, including North Kordofan, Kassala, and the River Nile state, where approximately 83,550 heads are found (Ishraga, 2013). The Butana area, a critical grazing zone, and Tamboul, a major market hub in the River Nile State, are particularly important centres for camel husbandry and trade. Despite their hardiness, camels are highly susceptible to parasitic diseases, with gastrointestinal (GI) helminthiasis representing a significant constraint on productivity and profitability. Helminth infections result in major economic losses through reduced feed efficiency, impaired milk and meat yield, low calving rates, and decreased working GSC Biological and Pharmaceutical Sciences, 2025, 33(02), 392-399 393 performance, sometimes leading to mortality (Anvar & Khan, 1998). Furthermore, several camel parasites, such as Schistosoma bovis and larval cestodes, carry zoonotic potential, posing a risk to public health (Abdel Rahman et al., 2001). Clinical signs of heavy infection typically include weight loss, emaciation, diarrhea, anaemia, and enteritis (Fowler, 1996). However, infections are often subclinical or asymptomatic, wherein the animal's productivity is compromised without obvious clinical illness (Borji et al., 2010). The helminth fauna of the camel GI tract is diverse, reported to include up to 50 species (Dakkak & Ouhelli, 1987). Seminal reviews and localized studies across camel-rearing countries have described these parasitic infections in detail (El-Bihari, 1985; Dakkak & Ouhelli, 1987). In Sudan, several studies have confirmed the presence of a wide array of helminths (Kheir et al., 1982; Elamin et al., 1984; Burger et al., 1989). The primary GI parasites identified include nematodes such as Haemonchus longistipes, Trichostrongylus probolurus, Cooperia pectinata, Oesophagostomum columbianum, Trichuris globulosa, and Setaria labiatopapilosa; trematodes like Fasciola gigantica and Schistosoma bovis; and cestodes including Avitellina spp. and Moniezia expansa. Local research has consistently shown high infection rates; for instance, Siddig and El Hussein (1998) reported an overall GI parasite prevalence of 85.4%, while Abdel Rahman et al. (2001) highlighted the high burdens of Trichostrongyles spp. and Haemonchus spp., particularly during the rainy season. The effective control and management of these parasites require a detailed understanding of the epizootiology, including the influence of host factors (age, sex, and breed) and environmental conditions (Gab, 1993). While most epizootiological studies rely on the identification of helminth eggs in faeces (Chhabra & Gupta, 2006), definitive diagnosis and accurate quantification of adult worm burdens are best achieved through post-mortem examination at abattoirs (Mirzayans & Halim, 1980). Given the economic significance of the camel market in Tamboul and the high parasitic prevalence in the region, comprehensive and current data utilizing abattoir examination are essential for designing sustainable control strategies that incorporate targeted anthelmintic use (e.g., Ivermectin, Albendazole) and improved husbandry practices (Stacey, 2015; Dennis et al., 2016). Despite the strategic importance of the Tamboul area, contemporary abattoir-based investigations correlating GI helminth infection with specific host and breed factors are scarce. Therefore, this study was designed to bridge this information gap. The primary aim of this study was to investigate the status of gastrointestinal helminthiasis in slaughtered dromedary camels sourced from the Tamboul market area. The specific objectives were to: (a) Determine the prevalence and intensity of gastrointestinal helminth infections in slaughtered dromedary camels (Camelus dromedarius) at Tamboul Slaughterhouse. (b) Identify and classify the different types, genera and species of gastrointestinal helminths (Trematodes, Cestodes and Nematodes). (c) Association Between Gastrointestinal Helminth Infections and Sex, Age and Geographical Origin, including Al-butana, Kassala, and Darfur in Camels Slaughtered at the Tamboul Slaughterhouse 2. Materials and Methods 2.1. Study Area This study was conducted at the Tamboul area (14°45'–15°30' N latitude and 33°5'–34°15' E longitude) in the eastern part of Al-Jazirah locality, Gezira State, Sudan. The location is approximately 150 Kilometres south of Khartoum. The area is characterized as being within the Savanna Zone. Tamboul is recognized as a major centre for camel slaughter in Sudan, providing a suitable site for the study. 2.2. Study Population and Sampling A total of sixty camels (Camelus dromedarius) were randomly selected for inclusion in this study at the Tamboul Slaughterhouse. The sampled animals were sourced from various major camel-rearing regions of Sudan, including Kassala, Butana, and Darfur. 2.3. Faecal Sample Collection A total of sixty faecal samples were collected, one from each individual camel, immediately following slaughter. Samples were collected directly from the rectum of both male and female animals during or immediately after defecation to ensure freshness. Each fresh faecal sample was placed into a clean, labelled plastic bag, sealed tightly, and transported under refrigeration (4∘C) to the laboratory at the College of Veterinary Medicine for processing. GSC Biological and Pharmaceutical Sciences, 2025, 33(02), 392-399 394 2.4. Laboratory Diagnosis (Coprological Examination) Faecal samples were processed and examined to diagnose the presence of gastrointestinal helminths using conventional parasitological methods, which included macroscopic and microscopic techniques. 2.5. Macroscopic Examination A preliminary diagnosis was performed by macroscopically examining the faecal samples for the presence of adult worms or segments of tapeworms (Hendrix & Robinson, 2006). All samples were subjected to three microscopic examination techniques for maximum recovery of helminth eggs and larvae. 2.6. Direct Smear Method A small amount of faeces was mixed with a drop of water on a clean glass slide to create a thin smear. This preparation was covered with a 22×22 mm coverslip and examined immediately under a light microscope using the 10× and 40× objective lenses (Hendrix & Robinson, 2006). 2.7. Floatation Technique The standard Willis technique was employed to detect nematode eggs, following the protocol described by Soulsby (1986). Approximately 1.0 ml of the mixed faecal specimen was diluted with a saturated sodium chloride (salt) solution in a tube, filling it until a convex meniscus was formed at the mouth. A coverslip was carefully placed on top to contact the solution. After 30-minute floatation period, the coverslip was swiftly removed, placed onto a clean slide, and examined under a low-power microscope for parasite eggs. 2.8. Sedimentation Technique The sedimentation technique was utilized to facilitate the recovery of heavy trematode eggs. Five to ten grams of faeces were mixed thoroughly with a sufficient volume of normal saline solution. The suspension was passed through a tea strainer into a beaker and subsequently into a conical flask. Normal saline was added to fill the flask, and the suspension was allowed to sediment and clarify. The supernatant was carefully decanted, and the flask was refilled with normal saline. This washing process was repeated until the supernatant fluid became clear. The final sediment was collected using a pipette, a few drops were transferred to a clean glass slide, covered with a 22×22 mm coverslip, and examined using 10× and 40× objective lenses (Soulsby, 1986). 2.9. Statistical Analysis Data analysis was performed using the Statistical Package for the Social Sciences (SPSS) software, version 20.0 (IBM Corp., Armonk, NY, USA). Descriptive statistics were used to summarize all variables. The Chi-square (χ2) test was applied to analyse potential risk factors associated with helminth infection. 3. Results 3.1. Overall Prevalence of Gastrointestinal Helminths A total of sixty camels (N=60) were examined for gastrointestinal (GIT) helminths at the Tamboul Slaughterhouse. Of these, 49/60 animals were positive, resulting in an overall prevalence rate of 81.7%, the remaining 11 camels were negative for GIT helminthic infection, representing 18.3% of the examined population (Table 1). Table 1 Diagnosis of Gastrointestinal helminths in camels in Tamboul slaughterhouse by Direct faecal smear test, Sedimentation Test and Flotation Test (N = 60) Total GIT helminthic Infection Test Negative (%) Positive (%) 60/60 (100%) 11/60 (18.3%) 49/60 (81.7%) Direct Faecal smear test 60/60 (100%) 26/60 (43.3%) 34/60 (56.7%) Sedimentation Test 60/60 (100%) 45/60 (75.0%) 15/60 (25.0%) Flotation Test GSC Biological and Pharmaceutical Sciences, 2025, 33(02), 392-399 395 3.2. Comparative Efficacy of Diagnostic Methods The detection efficacy of the three conventional parasitological methods varied. The Direct Faecal Smear Test yielded the highest positivity rate 49/60 (81.7%), then the Sedimentation Test yielded positivity rate 34/60 (56.74%), the Flotation Test recorded the lowest positivity rate 15/60 (25.0%) (Table 1). 3.3. Specific Helminth Types Identified The total positive infections were further characterized to identify the types of GIT helminths present in the onehumped camels. Schistosoma eggs/ova were detected at the highest rate, with a prevalence of 18.3% in the total camel population (N=60). The lowest observed rate was for Strongylus species, with a prevalence of 1.6% (Table 2). Table 2 Distribution and Prevalence of Gastrointestinal Helminths Types and Genus in Camels at Tamboul Slaughterhouse (N = 60) Genus Type Positive (%) Positive types (%) Schistosoma Trematodes (flukes) 11/60 (18.3%) 23/49 (46.9%) Fasciola Trematodes (flukes) 5/60 (8.3%) Paramphistomum Trematodes (flukes) 7/60 (11.6%) Taenia Cestodes (tapeworms) 9/60 (15%) 14/49 (28.6%) Moniezia Cestodes (tapeworms) 5/60 (8.3%) Trichostrongylus Nematodes (roundworms) 4/60 (7%) 12/49 (24.5%) Capillaria Nematodes (roundworms) 2/60 (3.3%) Ostertagia Nematodes (roundworms) 2/60 (3.3%) Strongylus Nematodes (roundworms) 1/60 (1.6%) Haemonchus Nematodes (roundworms) 3/60 (5.0%) Positive (%) 49/60 (81.7%) 49/49 (100%) Negative (%) 11/60 (18.3%) Total 60/60 (100%) 3.4. Association of Helminth Infection with Risk Factors 3.4.1. Sex and Infection Status When analysed by sex, 4 of 23 males (17.4%) and 7 of 37 females (18.9%) were infected with gastrointestinal helminths. The chi-square test revealed no statistically significant association between sex and infection status, χ²= (1, N = 60) = 0.00, p = 1.000 (Table 3). This indicates that both male and female camels were equally susceptible to gastrointestinal helminth infection. Table 3 Chi-Square Analysis of the Association Between Gastrointestinal Helminth Infections and Sex in Camels Slaughtered at the Tamboul Slaughterhouse (N = 60) P Value χ² (Chi-square) Total GIT helminthic Infection Sex Negative (%) Positive (%) 1.00 0.000 23/60 (38.3%) 4/11 (36%) 19/49 (38.8%) Males 37/60 (61.7%) 7/11 (64%) 30/49 (61.2%) Females 60/60 (100%) 11/11 (100%) 49/49 (100%) Total GSC Biological and Pharmaceutical Sciences, 2025, 33(02), 392-399 396 3.4.2. Age and Infection Status Infection prevalence was highest among camels aged 5–10 years (26.5%), compared to 8.3% in those under 5 years and 8.3% in those aged 11–15 years. However, the chi-square test indicated no significant association between age group and infection rate, χ²(3, N = 60) = 3.56, p = 0.314 (Table 4). 3.4.3. Geographical Origin and Infection Status The prevalence of infection varied slightly across geographical origins. Camels from Darfur showed a higher infection rate (30%) compared to those from Kassala (19%) and Al-Butana (5%). Nonetheless, this variation was not statistically significant, χ²(2, N = 60) = 3.99, p = 0.136 (Table 5). Table 4 Chi-Square Analysis of the Association Between Gastrointestinal Helminth Infections and Age in Camels Slaughtered at the Tamboul Slaughterhouse (N = 60) P Value χ² (Chi-square) Total GIT helminthic Infection Age / Month Negative (%) Positive (%) 0.314 3.56 12/60 (20.0%) 1/11 (9.1%) 11/49 (22.4%) > 5 34/60 (56.7%) 9/11 (81.8%) 25/49 (51.1%) 5-10 12/60 (20.0%) 1/11 (9.1%) 11/49 (22.4%) 11-15 2/60 (3.3%) 0/11 (0.0%) 2/49 (4.1%) < 15 60/60 (100%) 11/11 (100%) 49/49 (100%) Total Table 5 Chi-Square Analysis of the Association Between Gastrointestinal Helminth Infections and Geographical Origin in Camels Slaughtered at the Tamboul Slaughterhouse (N = 60) P Value χ² (Chi-square) Total GIT helminthic Infection Geographical Origin Negative (%) Positive (%) 0.136 3.99 19/60 (31.7%) 1/11 (9.0%) 18/49 (36.7%) Al-butana 21/60 (35.0%) 4/11 (36.4%) 17/49 (34.7%) Kassala 20/60 (33.3%) 6/11 (54.6%) 14/49 (28.6%) Darfur 60/60 (100%) 11/11 (100%) 49/49 (100%) Total Overall, these findings suggest that sex, age, and geographical origin were not significant predictors of gastrointestinal helminth infection among the examined camels. 4. Discussion A total of 60 camels slaughtered at the Tamboul abattoir were examined for gastrointestinal helminths using three diagnostic techniques: direct faecal smear, sedimentation, and flotation tests. Of these, 49 animals (81.7%) tested positive for at least one helminth species, indicating a high infection rate within the study population. Among the diagnostic methods, the direct faecal smear exhibited the highest detection rate (81.7%), followed by the sedimentation test (56.7%) and the flotation test (25.0%). The variation among diagnostic techniques suggests differences in sensitivity, likely related to egg density and type of helminth targeted by each method. These results support earlier findings that combining flotation and sedimentation enhances diagnostic accuracy for mixed infections (Soulsby, 1986; Charles & Robinson, 2006). The genera of helminths identified included Schistosoma spp. (18.3%), Fasciola spp. (8.3%), Paramphistomum spp. (11.6%), Taenia spp. (15%), Moniezia spp. (8.3%), Trichostrongylus spp. (7%), Haemonchus spp. (5%), Capillaria spp. (3.3%), Ostertagia spp. (3.3%), and Strongylus spp. (1.6%). Trematodes, particularly Schistosoma and Paramphistomum, were the dominant parasites, suggesting that local environmental conditions favor intermediate host GSC Biological and Pharmaceutical Sciences, 2025, 33(02), 392-399 397 proliferation, particularly in waterlogged areas. Similar findings were reported by Bogale et al. (2012) and Hailu and Ashenaf (2013), who observed high trematode prevalence in animals grazing near irrigation channels and marshlands. When infection prevalence was compared across sex, no statistically significant difference was detected between male and female camels, χ²(1, N = 60) = 0.00, p = 1.00. This result indicates that both sexes are equally exposed to infection, likely due to similar grazing patterns and management practices. Comparable outcomes have been reported by Lughano and Dominic (2015), who noted that gender does not significantly affect helminth infection when husbandry conditions are uniform. Similarly, no significant association was observed between infection status and age group, χ²(3, N = 60) = 3.56, p = 0.314. However, infection prevalence was slightly higher in camels aged 5–10 months (51.1%), possibly reflecting increased exposure post-weaning and immature immune responses. Younger camels are often more vulnerable to parasitic infections due to lower acquired immunity and longer pasture exposure (Abebew et al., 2011; Mavrot et al., 2015). Infection rates also varied according to geographical origin, with the highest prevalence observed among camels from Al-Butana (36.7%), followed by Kassala (34.7%) and Darfur (28.6%). However, this association was not statistically significant, χ²(2, N = 60) = 3.99, p = 0.136. These regional differences may reflect variations in climate, grazing systems, and access to snail-infested water bodies, as suggested by Keyyu et al. (2005). Overall, the study demonstrates that gastrointestinal helminths are endemic among camels in the Tamboul region, with trematodes and cestodes being predominant. Although infection patterns did not differ significantly across demographic factors, the high prevalence underscores the need for integrated control programs combining strategic deworming, pasture management, and vector control. These findings align with reports by Urquhart et al. (2013) and Zajac (2015), emphasizing that parasite transmission dynamics in arid zones are driven more by environmental and management conditions than by host factors alone. 5. Conclusion This study revealed a high prevalence (81.7%) of gastrointestinal helminths among camels in the Tamboul Slaughterhouse, indicating that parasitic infections remain a major health challenge in the region. The predominant helminth genera were Schistosoma, Taenia, Paramphistomum, and Trichostrongylus, reflecting the coexistence of trematode, cestode, and nematode infections under local environmental conditions. Although infection rates were slightly higher among females and middle-aged camels, statistical analysis showed no significant differences across sex, age, or geographical origin. These findings suggest that environmental contamination, grazing practices, and water source exposure are more influential in helminth transmission than intrinsic host factors. Therefore, the study recommends implementing regular deworming and strategic anthelmintic rotation to prevent resistance; conducting seasonal monitoring of infection patterns to identify high-risk periods; improving pasture and water management, including control of snail intermediate hosts; and enhancing veterinary extension programs to educate livestock owners on preventive measures. Sustained surveillance and integrated parasite control strategies are essential to safeguard animal health, improve productivity, and support the sustainable development of Sudan’s camel industry. Compliance with ethical standards Acknowledgments We extend our sincere thanks to the Department of Parasitology, Faculty of Veterinary Medicine, Al-Butana University, for providing the institutional support necessary to conduct this study. We also gratefully acknowledge the cooperation received from the staff at the Tamboul Slaughterhouse, where the samples for the identification of gastrointestinal helminths in camels were collected. Disclosure of conflict of interest No conflict of interest to be disclosed. GSC Biological and Pharmaceutical Sciences, 2025, 33(02), 392-399 398 Declaration We, the undersigned authors, hereby declare that the manuscript entitled: " Gastrointestinal Helminths in Camels Slaughtered at Tamboul, Sudan: Prevalence and Risk Factor Analysis" • Is our original work and has not been previously published, nor is it under consideration for publication elsewhere. • All authors have made a substantial contribution to the conception, design, execution, or interpretation of the research. • We confirm that the data and results presented herein are accurate and were derived and analysed with full scientific credibility and integrity. 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