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Map of Turkiye, illustrating the sample-collection region. (A):Turkiye’s placement on the globe map. (B): The area of the study, which took place in Turkiye’s Mediterranean region. (C): The study area included two provinces and five local districts.Blood samples from 640 apparently healthy, small ruminants (503 goats, 137 sheep) were collected into vacuum tubes containing anticoagulant (K3-EDTA) and stored at −20 °C until DNA extraction. The genomic DNA was extracted from 200 μL of EDTA-anticoagulated blood using a kit (PureLinkTM Genomic DNA Mini Kit, Invitrogen Corporation, Carlsbad, CA, USA), as directed by the manufacturer. The genomic DNA concentration was determined using spectrophotometry (NanoDrop® ND- 2000 UV/Vis Spectrophotometer, Thermo Fisher Scientific Inc., Wilmington, DE, USA).
Source publication
Small ruminant piroplasmosis is the hemoparasitic infection of sheep and goats caused by Babesia and Theileria species responsible for clinical infections with high mortality outcomes. The disease is transmitted by ixodid ticks and prevalent in the tropical and subtropical regions of the world, including Türkiye. A prevalence survey, using molecula...
Citations
... Ticks (Acari: Ixodidae) are known to infest a wide range of hosts, including humans, livestock, pets, wildlife, reptiles, and birds, and are the second most common arthropod vector for disease transmission after mosquitoes [5,6]. Tick-borne diseases (TBDs) such as theileriosis, babesiosis, anaplasmosis, and ehrlichiosis are critical health challenges for small ruminants in tropical and subtropical regions [7][8][9][10][11][12][13][14]. ...
Simple Summary
In this study, pathogen-free Rhipicephalus bursa colonies were established for vector competence research, and their life cycle parameters were analyzed. Initially, engorged R. bursa females were collected from naturally infested sheep, goats, and cattle. The engorged females were placed in an incubator to lay eggs and produce larvae (F1 larvae). Two New Zealand rabbits and two pathogen-free splenectomized sheep were used to obtain subsequent generations. The F1 and F2 unfed larvae were fed on rabbits, and F1 and F2 unfed adults were fed on sheep. F3 larvae were obtained from engorged F2 females. At the end of all developmental stages, tick pools were screened using nPCR for tick-borne pathogens and found to be pathogen-free. The sheep were clinically monitored for 63 days, during which no clinical signs of disease were observed, and all tests for the presence of tick-borne pathogens yielded negative results. F3 larvae were confirmed as pathogen-free and suitable for vector competence studies. Under laboratory conditions, the R. bursa life cycle was completed in 72–153 days. This study demonstrated that pathogen-free R. bursa colonies can be maintained over multiple generations, offering a reliable model for vector competence research. Establishing these colonies and documenting their biological parameters is crucial for advancing strategies in vector-borne disease control.
... According to Robert Koch's postulates [17], then, in vivo isolation of the newly identified Babesia sp. was made from a naturally infected goat, and named Babesia aktasi [18]. In our large molecular survey carried out in the Mediterranean region of Türkiye, it was detected that 22.5% of the goats (113/503) were infected with the parasite [19]. Then, an experimental study performed on the immunocompetent goats revealed that B. aktasi did not cause typical clinical findings of babesiosis (anemia, icterus, hemoglobinuria) except for increased body temperature [20]. ...
... In particular, the disease is reported to be more prevalent in the Central and Southeastern Anatolia regions of Türkiye [22]. Babesia ovis, B. crassa, and B. motasi have been molecularly identified in small ruminant and ixodid ticks in Türkiye [19,[23][24][25][26]. ...
... Thin blood smears and DNA isolated from EDTA blood samples were screened for the presence of Babesia spp., Theileria spp., and Anaplasma spp. using microscopy and nested PCR [19,24]. Seventeen male goats (14 purebred Saanen, 3 indigenous goats) that tested negative for the selected pathogens were purchased and maintained at the Ministry of Agriculture, Elazığ Veterinary Control Institute, small ruminant unit. ...
Small ruminant babesiosis remains a neglected disease despite causing significant economic losses to sheep and goat herds in many regions around the world. The pathogenesis and clinical manifestations of ovine babesiosis are well-known, but there is a lack of information regarding caprine babesiosis. Since the discovery of the first Babesia spp. in 1888, several species/subspecies/genotypes, including Babesia aktasi, have been described. Our recent molecular survey revealed that the parasite is highly prevalent (22.5%) in indigenous goats from Mediterranean region of Türkiye. The aim of this experimental study was to determine the pathogenicity and virulence of B. aktasi in immunosuppressed (n = 5) and immunocompetent (n = 7) purebred Saanen goats. The goats were experimentally infected with fresh B. aktasi infected blood, and examined for clinical, parasitological, hematological, and serum biochemical findings throughout the infection. Following the parasite inoculation, intra-erythrocytic parasites were detected from the 1st day post-infection, followed by an increase in rectal temperature and parasitemia. The parasitemia was detected ranging from 4.3% to 33.5% in the immunosuppressed group, while it was 2.1% to 7.6% in the immunocompetent. Severe clinical symptoms characterized by anemia, jaundice, and hemoglobinuria developed in both groups. A statistically significant inverse correlation was observed between the increase in parasitemia and RBC, WBC, HCT, and Hb values in the goats compared to pre-infection levels. Values of AST, ALT, GGT, Total bilirubin, and Albumin showed a significant increase, with all the immunosuppressed goats dying on the 4th and 7th days post-infection, while four out of seven immunocompetent goats died on between 6-8th days. Severe edema in the lungs, frothy fluid in the trachea, jaundice in the subcutaneous and mesenteric fat, and dark red urine were detected in necropsy. The results obtained in this study demonstrated that B. aktasi was highly pathogenic to purebred Saanen goats. Current work assures valuable insights into the pathogenesis and virulence of B. aktasi and serves as a foundation for future studies to develop effective control strategies against caprine babesiosis.
... This study aims to address this gap by focusing on the mitochondrial genome of B. ovis, an apicomplexan parasite prevalent in sheep in Türkiye [27][28][29][30]. Through sequencing and analyzing the B. ovis-Alacakaya strain, we seek to clarify its phylogenetic relationships and classification within the Babesia genus. ...
This study presents the first comprehensive analysis of the mitochondrial genome of Babesia ovis, a significant pathogen in ovine babesiosis in Türkiye. The B. ovis mitochondrial genome is a linear monomeric molecule of 6015 bp with an A + T content of 70.5%, featuring terminal inverted repeats (TIRs) at both ends. It encodes three essential proteins (Cox1, Cox3, and Cob) and six fragments of large subunit rRNA genes. Comparative analysis revealed high sequence identity with Babesia sp. Xinjiang (87.5%) and Babesia sp. Dunhuang (87.5%), suggesting a close evolutionary relationship. The study highlights the conservation of mitochondrial gene content across Babesia and Theileria species, emphasizing their utility in phylogenetic studies. The findings also suggest that TIR variability plays a role in mitochondrial genome size differences, influencing species-specific adaptations. This research provides valuable insights into the evolution and functional adaptations of B. ovis and underscores the potential of mitochondrial genomic data in enhancing diagnostic and therapeutic strategies for babesiosis. Further exploration of mitochondrial genomes in Babesia species is essential for understanding their biology and developing effective control measures.
... Among them, the RLB assay, which combines PCR with a blotting procedure, can simultaneously detect and identify Babesia, Theileria, Anaplasma, and Ehrlichia species in a single sample [40,41]. The assay was previously used as a screening tool in our laboratory for epidemiological surveys [36,38,42]; however, it is labor-intensive and has a slow turnaround. ...
... The assay was used to analyze 97 blood samples collected from apparently healthy goats for the presence of B. aktasi DNA. Additionally, 44 archived DNA samples, previously identified as B. aktasi-positive via the reverse line blot (RLB) assay [42], were reanalyzed, and the results were compared to evaluate the consistency of detection between the two methods. These findings provide a basis for the development of a reliable diagnostic tool for B. aktasi in both clinical and research settings ...
... A total of 97 whole-blood samples were collected from the jugular vein of the apparently healthy indigenous goats into 5 mL vacuum tubes with EDTA in breeding farms located in the villages of Anamur district in Mersin Province, Turkey where B. aktasi is known to be endemic [42]. The DNA extraction was made from 200 µL blood samples using the PureLink™ Genomic DNA Mini Kit (Invitrogen Corporation, Carlsbad, CA, USA) according to the kit guide. ...
Simple Summary
We developed a new test to detect Babesia aktasi, a parasite that infects goats, using a method called semi-nested PCR. This method focuses on a specific part of the parasite’s DNA to ensure accuracy. We checked the test against several other similar parasites to make sure it only detected B. aktasi, which it did successfully. To see how sensitive our test is, we used blood samples with known amounts of the parasite and found that our test could detect even very low levels of infection. Our results show that this new test is both highly accurate and sensitive, making it a valuable tool for identifying B. aktasi infections in goats. This new PCR method provides a reliable tool for detecting B. aktasi in goats, which is crucial for managing and preventing the spread of this infection, ultimately protecting goat health and improving agricultural productivity.
Abstract
We developed and evaluated a semi-nested PCR assay for the detection of Babesia aktasi infection in goats based on the sequence of the B. aktasi 18S ribosomal RNA gene. Following in silico screening, the specificity of the primers was assessed using reference DNA samples, including B. ovis, B. motasi, B. crassa, B. venatorum, B. divergens, B. capreoli, Theileria ovis, and T. annulata. To determine the sensitivity of the method, blood infected with 2% parasitemia of B. aktasi was diluted to 10-fold serial dilutions. The method specifically amplified a 438 bp fragment of B. aktasi DNA, but did not demonstrate cross-amplification with the other hemoparasites tested. The sensitivity assay indicated that this PCR method was able to detect infection at a dilution of 10⁻⁸ of 2% parasitemia (0.074 parasites/200 µL). Ninety-seven blood samples collected from goats were used to analyze for B. aktasi, and the infection was detected in 18.5% of the goats. Additionally, the method was also applied to 44 field DNA samples that were detected to be positive for B. aktasi by reverse line blotting (RLB), and showed 84.1% agreement. The findings revealed that newly developed semi-nested PCR can detect B. aktasi infections in goats with high sensitivity and specificity.
... In fact, our molecular survey which aimed to determine the frequency of B. aktasi in goats and sheep in the Mediterranean region of Türkiye indicated a high prevalence in local goats. However, the parasite was not detected in the sampled sheep grazing in the same flock with the goats in the region [19]. These epidemiological data strongly support the fact that B. aktasi may not be infective for sheep. ...
... Peripheral thin blood smears from the ear vein of the same animals were prepared for the microscopic examination. Thin blood smears and DNAs isolated from EDTA blood samples were screened by microscopy and nested PCR for the presence of Babesia spp., Theileria spp., and Anaplasma spp., respectively [19,20]. For the amplification of Anaplasma spp., the primers Ec9/Ec12A [21] and 16S8FE/B-GA1B [22] were used. ...
... Among these, B. ovis primarily affects sheep, causing clinical symptoms such as fever, anemia, jaundice, and hemoglobinuria, while B. motasi is more prevalent in goats, causing mild clinical manifestations [31]. Our previous field survey in the Mediterranean region of Türkiye revealed a high prevalence of B. aktasi in goats [19], while no molecular evidence of B. aktasi infection was found in sheep grazing in the same pasture [19]. However, this finding needed to be supported by in vivo experimental study. ...
Simple Summary
In this study, an experimental investigation was conducted to assess the pathogenicity of Babesia aktasi in immune-suppressed sheep. For this purpose, five immune-suppressed lambs under one year of age were infected by intravenous injection of fresh blood containing approximately 9.2% and 12% parasitemia of B. aktasi. Following parasite injection, the lambs were monitored daily for clinical and microscopic findings of babesiosis for 30 days. Throughout this period, no clinical and microscopic signs of babesiosis were observed in the lambs. Of the five recipient lambs, two tested negative for B. aktasi in nested PCR up to 30 days post-infection. Among the remaining three lambs, two were PCR positive on the first day, and the other one remained positive until the fourth day post-infection. DNA sequencing confirmed that the PCR positivity in the recipient lambs originated from the inoculum. These findings indicate that immune-suppressed lambs do not appear to be susceptible to infection with B. aktasi, which is highly pathogenic to immune-suppressed indigenous goats.
Abstract
Our survey in the Mediterranean region of Türkiye revealed high prevalence of Babesia aktasi in goats, while no molecular evidence of the parasite was found in sheep grazing in the same pasture. We hypothesized that the parasite may not be infectious to sheep. To test this hypothesis, the present study was designed to evaluate the susceptibility of Akkaraman sheep breed to B. aktasi infection. Fifteen mL of fresh blood infected with B. aktasi was injected into immune-suppressed lambs (n = 5). The recipient lambs were monitored daily for clinical signs of babesiosis over 30 days, and blood was collected for microscopic and molecular diagnostic evaluation. The lambs did not display clinical and parasitological signs of babesiosis. Two out of five recipient lambs were nested PCR-negative for B. aktasi over 30 days post infection. Out of the remaining three lambs, two were PCR positive on the first day, and one recipient was positive until the fourth day post infection. DNA sequencing confirmed that the PCR positivity in the recipient lambs originated from the inoculum. These findings revealed that immune-suppressed sheep do not appear to be susceptible to infection with B. aktasi that is lethal to immune-suppressed indigenous goats.
... Our molecular survey carried out in the same region indicated that B. aktasi infections were highly prevalent in the goat populations, with a prevalence of 22.5% (113/503) [24]. Then, an experimental study revealed that B. aktasi caused typical clinical findings of babesiosis (fever, anemia, icterus, and hemoglobinuria) resulting in death in immune-suppressed indigenous goats [25]. ...
... The tick vector transmitting B. aktasi has not yet been identified. The tick survey demonstrated that the most common tick infesting goats in the region where the prevalence of B. aktasi is widespread was the two-host tick R. bursa [24]. This epidemiological overlap indicates that the potential tick vector responsible for the parasite transmission could be R. bursa. ...
... The samples were brought to the laboratory (Fırat University, Faculty of Veterinary Medicine, Department of Parasitology). Thin blood smears and DNA isolated from EDTA blood samples were tested to ensure the absence of the selected pathogens screened by microscopy and nPCR for the presence of Babesia, Theileria, and Anaplasma species [24,26]. Four goats (#Donor-1, #ID-1, #ID-2, and #ID-3) determined to be negative were purchased and transported to Fırat University Animal Hospital for splenectomy ( Figure 1a). ...
Simple Summary
The tick species involved in the transmission of Babesia aktasi, which is widespread in the Mediterranean region, is unknown. However, studies have shown that Rhipicephalus bursa is the most common tick species in the regions where the prevalence of B. aktasi is widespread. This finding increases the possibility that R. bursa may serve as a vector for the transmission of B. aktasi and encourages the evaluation of the vector competence of R. bursa. For this purpose, clinical babesiosis was induced in an immune-suppressed indigenous donor goat. Babesia spp.-free R. bursa larvae (n = 2000) and adults (n = 25) obtained from laboratory colonies fed on the donor goat. Following oviposition, PCR analysis of engorged female carcasses and engorged nymphs revealed the presence of B. aktasi, whereas no positivity was found in unfed larvae and adult ticks. The subsequent developmental stages of these ticks were used to infest three additional immune-suppressed goats. No clinical signs of babesiosis were observed in the infested goats. Moreover, molecular analysis did not detect DNA in the goats. These results demonstrated that R. bursa does not transmit B. aktasi, neither transovarially nor transstadially.
Abstract
A recent molecular survey revealed a high prevalence of Babesia aktasi in indigenous goats from the Mediterranean region of Türkiye, coinciding with heavy Rhipicephalus bursa infestations. This geographical overlap has raised the possibility that R. bursa may serve as a vector for the parasite. To evaluate the potential of R. bursa to serve as a vector for the parasite, an experimental study was conducted in indigenous goats. An immune-suppressed donor goat was intravenously injected with 15 mL of the cryopreserved B. aktasi stabilate, resulting in severe clinical babesiosis and parasitemia. Subsequently, R. bursa larvae and adults derived from Babesia-free laboratory colonies were allowed to feed on the infected donor goat. After oviposition, engorged female carcasses, representative engorged nymphs, unfed larvae, and adult pools were used for DNA extraction and PCR analysis. No PCR positivity was detected in any of the DNA samples, except for those with engorged female carcasses and nymphs. Three immune-suppressed recipient goats were infested with the unfed immature and mature ticks consuming the blood of a donor infected with B. aktasi. No clinical or parasitological findings were encountered in the recipient for 40 days post-infestation. These findings indicated that R. bursa was not a competent vector for B. aktasi.
... It is transmitted by ticks of Hyalomma anatolicum and Haemaphysalis quinghaiensis species and exhibits low pathogenicity [2]. A recently discovered species, B. aktasi, has been identified as common among local breed goats in the Mediterranean region of Türkiye [6,30]. While it causes moderate infections in local breed goats, its pathogenicity in various goat breeds and potential hosts, as well as information regarding relevant vector ticks and natural reservoirs, remains unknown. ...
Babesiosis, caused by Babesia ovis, is a major seasonal issue in sheep, particularly in countries like Türkiye with high Rhipicephalus bursa tick populations. Previous studies employing various methods such as microscopy, serology, or molecular techniques have reported different epidemiological data concerning ovine babesiosis. Addressing this knowledge gap, our study employed a combined nested PCR (nPCR)/indirect ELISA (iELISA) approach, analyzing blood samples collected from 414 sheep between April and July 2023 using both techniques. nPCR amplified the 18S ribosomal RNA gene of B. ovis and determined a molecular prevalence of 1.9%. Conversely, serological testing using iELISA targeted the BoSA1 antigen and revealed a significantly higher positivity rate of 59.9% for anti-B. ovis antibodies. The temporary presence of Babesia after recovery reduces nPCR sensitivity, resulting in lower molecular prevalence. However, even if Babesia is not present in the host, anti-B. ovis antibodies remain in the serum for a long time and can be detected serologically. Our study underscores the necessity of concurrently employing molecular and serological methods for an accurate assessment of B. ovis prevalence. It highlights the importance of comprehensive epidemiological approaches for effective disease management in sheep populations.
... This disease is caused by protozoan parasites from the genus Babesia, with several species such as Babesia divergens, Babesia bigemina, Babesia ovis, and Babesia major known for their pathogenicity. These parasites infect a broad range of hosts, including cattle, dogs, cats, pigs, sheep, horses, and occasionally humans, with over 100 identified species, 18 of which are known to infect local animals and cause disease (2,3). ...
Background: Babesiosis, a significant tick-borne disease, poses a growing threat to small ruminants and public health due to the pathogenic Babesia parasite. This study focuses on the prevalence of Babesia in cows within the district of Dera Ismail Khan and its impact on red blood cells. Objective: The primary objective of this research was to detect the presence of the Babesia parasite in cows and assess its effects on red blood cells. Methods: Fifty blood samples were randomly collected from cows in Dera Ismail Khan. These samples underwent Giemsa staining and were subsequently examined under a light microscope to identify the presence of the Babesia parasite. Results: Of the 50 blood samples analyzed, only 5 (10%) tested positive for Babesia. This suggests a lower prevalence of babesiosis in the region. The parasite was observed to cause significant destruction of red blood cells. Conclusion: Although babesiosis is not widely prevalent in Dera Ismail Khan, its impact on infected cows is severe, leading to the destruction of red blood cells. Effective monitoring and control measures are essential to mitigate its spread and impact.
... However, Babesia ovis and Theileria ovis are the most common causative pathogens (Esmaeilnejad et al., 2020;Aydın et al., 2022;Galon et al., 2022b). Of the blood parasites, babesiosis is usually accompanied by anorexia, fever, polypnea, icterus, hemolytic anemia, hemoglobinuria, anemia, diarrhea, and in acute clinical cases, could be terminated by death (Galon et al., 2022b;Villanueva-Saz et al., 2022;Ulucesme et al., 2023). Other causes of discolored urine in sheep include bacillary hemoglobinuria caused by C. hemolyticum infection (Randhawa et al., 1995). ...
... Open Veterinary Journal, (2024), Vol. 14(4): 1059-1071 hemoglobinuria (Galon et al., 2022b;Villanueva-Saz et al., 2022;Ulucesme et al., 2023). From the case history, the remaining three animals (two bucks and a ram) had chronic toxicity with copper. ...
Background
Bloody urine is classified in farm animals as hematuria, hemoglobinuria, and myoglobinuria. In small ruminants, discolored urine is reported due to several etiologies which is sometimes fatal. Of these causes are babesiosis, bacillary hemoglobinuria, copper toxicity, and hypophosphatemia.
Aim
This study was designed to investigate the clinical, etiological, hematobiochemical, ultrasonographic, and pathological findings in rams and bucks with red urine syndrome.
Methods
Eighteen male animals (nine rams and nine bucks) of 6 months to 3 years were examined. Parallel, 10 healthy controls were used. They were admitted due to red urine, voiding of only urine drops, straining during the act of urination, grunting during urination, ventral abdominal edema, and abdominal distension. The duration of the disease ranged from 2 to 30 days. A history of chronic copper toxicosis was informed in two bucks and a ram. Two blood samples were collected from diseased as well as from controls in EDTA tubes (for complete blood count testing) and in plain tubes (for serum collection).
Results
Hematuria was found in 11 animals (seven bucks and four rams) while hemoglobinuria was detected in seven animals (five bucks and two rams). Sonographic findings in diseased animals included ruptured urinary bladder in 3, ruptured urethra in 5, penile calculi, uroperitoneum in 6, distended urinary bladder in 7, hydronephrosis in 5, echogenic deposits in the bladder in 3, and ventral urine accumulation in four animals. Laboratory evaluation of a Geimsa-stained blood smear confirmed the infection with Babesia in three bucks and a ram. Hemolytic anemia was marked in two bucks and a ram due to chronic copper toxicity. Biochemical abnormalities included hypoalbuminemia, hyperglobulinemia, increased blood urea nitrogen and creatinine concentration, and hyperglycemia. Postmortem examination was carried out on six animals (four rams and two bucks).
Conclusion
Discolored urine in rams and bucks in this study resulted from hematuria due to urinary calculi and pelvic abscessation or from hemoglobinuria due to Babesia infection or due to copper toxicity. Hemolytic anemia was the outstanding hematological finding and hypoalbuminemia, hyperglobulinemia, increased blood urea nitrogen (BUN) and creatinine, and hyperglycemia were the characteristic biochemical findings. Sonography of the urinary tract was very helpful in assessing the renal parenchyma, urinary bladder, and abdominal cavity for the verification of urolithiasis, hydronephrosis, intact or ruptured urinary bladder, uroperitoneum, and perforated urethra.
... Parasitic infestations due to endoparasites, ectoparasites (Majeed et al., 2015), or blood parasites (Ulucesme et al., 2023) in goats represent a big health issue worldwide (Majeed et al., 2015), leading to decreased milk and meat production, reduced performance, or mortality (Sazmand & Joachim., 2017). Research on goat parasites has garnered sustained global attention, with numerous studies aimed at better understanding these parasites and developing effective management strategies (Sutar et al., 2010 ;Rizwan et al., 2023). ...
The semi-arid regions of Algeria present unique challenges and opportunities for the study of parasitology, particularly in relation to goats. Goats are integral to the livelihoods of many rural communities in these regions, providing meat, milk, and other essential products. However, they are also susceptible to a wide range of parasites that can impact their health and productivity. This study aimed to investigate parasitic species in goats across six locations in the Laghouat region and assess their prevalence according to the several factors. A total of 144 animals (21 males and 123 females) from 11 different farms, were examined during 2022-2023. Fieldwork involved collecting goat excrement, ectoparasites, and blood samples. In the laboratory, five techniques, including direct examination, flotation, sedimentation, modified Ziehl-Nielsen techniques, blood smears, and ectoparasite observation, were used. Among the 144 animals examined, 97 showed endoparasite infestations. Coprological analysis revealed 28 endoparasites in Capra hircus goats, with the highest prevalence observed for Cryptosporidium spp. (34.7%), followed by nematode larva (22.9%), Fasciola hepatica (17.4%), Ascaris spp. (13.9%), Eimeria spp. and Eimeria granulosa, both with a prevalence of (12.5%). Eimeria parva and Skrjabinema spp. presented a similar rate of (11.1%). Ectoparasites were identified in (21.5%) of the examined goats, represented by two lice species: Linognathus africanus and Damalinia caprae, (20.8%). Piroplasmosis was detected in 20.1% of the total. Regarding the factors, season, animal's origin, treatment, type of production, and breeding system influenced endoparasites rate (P ˂ 0.05). Similar results were obtained for ectoparasites, except for treatment, which did not show any significant difference. For blood parasites infestation, statistical analysis did not reveal any significant differences, except for season and breeding system (P ˂ 0.05). the present study highlighted a large number and types of parasites affecting goats in Laghouat, which could lead to many pathologies and economic losses in consequences. Therefore, it is important to implement a coherent integrated pest control strategy and raising awareness among animal breeders about the multiple diseases that can affect their animals.