CLINICO-EPIDEMIOLOGY AND HAEMATO-BIOCHEMICAL STRESS ASSOCIATED WITH PARASITIC INFESTATION ALONG WITH THERAPEUTIC TRIALS IN GOATS
A. Raza¹$, R. A. Gul¹$, H. Anjum2$, M. A. Raza¹, K. Mehmood1*, M. T. Ghori¹, M. Altaf¹, A. I. Malik¹, K. Li3, E. M. Al Olayan4, M. K. Okla5, R. Sultan6, and F. A. Kiani7
1Department of Clinical Medicine and Surgery, Faculty of Veterinary and Animal Sciences, Islamia University Bahawalpur 63100, Pakistan.
2Medicine Section, Department of Clinical Sciences, College of Veterinary and Animal Sciences, Jhang, Pakistan
3Institute of Traditional Chinese Veterinary Medicine, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, PR China
4Department of Zoology, Faculty of Science, King Saud University, Riyadh, Saudi Arabia
5Botany and Microbiology Department, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
6Department of Pathology, Faculty of Veterinary Sciences, Cholistan University of Veterinary and Animal Sciences, Bahawalpur, 63100, Pakistan
7Department of Clinical Science, Faculty of Veterinary Sciences, Bahauddin Zakariya University, Multan 60800, Pakistan
$These authors made equal contribution
*Corresponding author’s E-mail: khalid.mehmood@iub.edu.pk
ABSTRACT
Parasite infection poses a significant risk to goat health due to low birth weights, poor body condition, low weight gain, and difficulties in kidding. This study aims to investigate the clinico-hematology and epidemiology of parasites along with the therapeutic effect of eprinomectin in goats in south Punjab. A total of 320 goats were selected to collect 160 fecal samples and 160 skin scraping samples. For therapeutic trials, six healthy goats and six goats having parasitic infection were selected to apply eprinomectin. Blood samples were taken from both groups for serum biochemistry and complete blood count. Overall prevalence of ectoparasites was 31.8%. The Bahawalpur area has high prevalence of ectoparasite (59.3%) with a significant difference that include a higher prevalence in older goats (52%) as compared to younger goats (24.44%). In the ectoparasite, ticks are the major species that are more prevalent (20%) than Lice (8.75%) and Mites (3.12%) in goats. The prevalence of endoparasites was 56.8%. Our study also revealed that Ahmedpur area has high prevalence of endoparasite (78.1%), including a higher prevalence in older goats (64.66%) as compared to younger (26.31%). Among endoparasites, the prevalent species were Toxocara (11.25%), Stronglyus (9.37%), Emaria (17.5%), Haemonchus (6.25%), Marshliagia (1.25%), Monizia (5.0%), and Gardia (6.25%) in the Bahawalpur area. Hematological results revealed a significant (P<0.05) variation in WBC, RBC, hemoglobin and MCV between infected and healthy groups on 7th day, while WBC, MCV, and MCH showed a significant difference (P<0.05) on 14th day after the eprinomectin administration. On the 14th day after treatment, albumin, SGOT, total protein, and SGPT values were not significantly different (P>0.05) in both groups, which showed that eprinomectin did not cause stress or any physiological changes in goats. Therapeutic trials revealed that 3 (50%) goats were recovered on the 7th day, while 5 (83%) goats were completely recovered on 14th day. It has been demonstrated that parasitic infestation in goats is a major problem in the Bahawalpur division, and eprinomectin can reduce the the parasitic burden and improve animal health.
Keywords: Eprinomectin, Parasitic infestation, Goat, Hematological changes, Oxidative stress
INTRODUCTION
Pakistan has agriculture-based economy where raising livestock is a major source of income for the local farmers (Raza et al., 2024), who in turn use it to raise their own standard of living and combat poverty (Khan et al., 2022; Irshad et al., 2023). Goat farming is essential to both developed and developing countries' economies, environment, and cultural perspectives (Maurizio et al., 2021). Small ruminants use less feed than other large animals and can produce valuable items (Irshad et al., 2023). However, parasitic infestation is a serious health problem that reduces the ability of these animals to produce meat, milk, and wool (Abah et al., 2022; Irshad et al., 2023). Ruminants, that are the backbone of the Pakistani agricultural economy are vulnerable due to the prevalence of both ectoparasites and endoparasites (Muhammad et al., 2021). More than 70% of people reside in rural areas, where domestic animals make up 11.4% of GDP and 53.2% of agricultural value (Anonymous, 2023). About 5% of Pakistan's milk is produced by sheep and goats (Muhammad et al., 2021). The degradation of hides and skin, which eventually reduces their market value in the leather industry, is directly related to tick infestation (Abah et al., 2022; Sajid et al., 2020).
Parasitic infestation indirectly leads to increased mortality rates, reduced milk production, and the devastating conditions which include, severe allergies, and the underlying causes of anaplasmosis, theileriosis, and babesiosis (Sajid et al., 2020; Hussein et al., 2023). In general, gastrointestinal parasites hamper the health of animals, especially in low-income and emerging nations (Alvi et al., 2022; Irshad et al., 2023). It is reported that GI parasites were to be present in 65.37% of goats and sheep, with 63.21% of goats and 68.3% of sheep having parasitic infestation. Six parasite species have been reported in sheep and goats: Coccidia spp., Haemonchus contortus, Strongyloides papillosus, Trichuris ovis, Dictyocaulus filarial, and Moniezia spp (Fthenakis and Papadopoulos, 2018; Maurizio et al., 2021; Irshad et al., 2023). Livestock has become a significant source of wealth and a representation of the agribusiness that produces dairy, meat, and a variety of other items (Muhammad et al., 2021). Small ruminants make up to two billion of the three billion ruminants (Riaz et al., 2021). It is beneficial to use small-scale ruminant farming as a capital asset for food production and breeding stock (Riaz et al., 2021; Qamar and Alkheraije, 2023; Men et al., 2022). Lice, ticks, and mites are examples of ectoparasites; these parasites reside on their hosts' skin and depend on them for growth, reproduction, and nutrition (Muhammad et al., 2021). Certain regions of Pakistan have more ectoparasitic infestation than others due to suitable temperature, lack of awareness among livestock owners, lack of veterinary facilities, and insufficient management strategies (Muhammad et al., 2021). The ectoparasitic infections produce skin abrasions and hemorrhages which spread several illnesses among other animals, they pose a severe threat to the financial sustainability of ruminant production (Muhammad et al., 2021).
Gastrointestinal (GI) parasites impair goat reproductive systems through weight loss, reduced production, and even mortality (Degla et al., 2022). Ruminants suffer from hematological and metabolic disorders caused by helminthiasis (Nawaz et al., 2022). Anorexia, weight loss, poor reproductive outcomes, decreased productivity and reproductive ability, and even death of kids can result from these parasitic infestations (Zurbano et al., 2023). Trichostrongylus are the most common nematodes in small ruminants worldwide (Rostang et al., 2020). Trematodes are members of the fluke family and nematodes are often referred to as roundworms (Ruhoollah et al., 2023). Numerous diseases such as oesophagostomiasis, paramphistomiasis, fascioliasis, Trichostrongylosis, and hemonchosis can seriously harm livestock (Ruhoollah et al., 2023).
GI parasitism has harmful effects on the health, well-being and production of livestock (Ruhoollah et al., 2023). Reducing the burden of parasite resistance and adaptation requires an innovative strategy for ongoing parasitic control (Al-Hoshani et al., 2023; Rostang et al., 2020). On the other hand, modern approach to give drugs to animals is topical drug administration (Güngör Akbaş et al., 2022; Kandeel et al., 2022). Eprinomectin (EPM), a macrocyclic lactone is widely used by veterinarians because of its low excretion in milk and potent antiparasitic properties for both ectoparasites and endoparasites. (Gao et al., 2022). The goal of this research was to study clinico-epidemiological investigation of ecto and endo parasites as well as exploit the effect of EPM on parasitic control in goats in the south Punjab.
MATERIALS AND METHODS
Study Area: The regions selected for this research were Yazman, Khairpur (Tamewali), Hasilpur, Bahawalpur City, Ahmedpur of the Bahawalpur Division. The information on the animals were entered on performa, including age, sex, breed, grazing location and gastrointestinal problem. Most of the animals were fed by grazing on seasonal pastures. Animals with poor feeding practices, poor housing management, and neglected medical care were included in this study after a comprehensive examination. Total (n=320) samples were collected from goats which were further subdivided into 160 fecal samples and 160 skin scraping samples. A total of 32 samples were taken from each Tehsil of the Bahawalpur division (Bahawalpur, Khairpur, Hasilpur, Yazman, Ahmedpur) were taken and same number of skins scraping samples for ectoparasites. Some parasites were possible to identify with naked eye, but remaining samples were preserved in ethanol according to previous study (Raza et al., 2024).
Ethical Approval: The ORIC office of Islamia University of Bahawalpur approved the ethical guidelines for this study. Before to take any animal samples, consent from the farmers was obtained.
Processing of Samples: The collected sample were observed under microscope in the laboratory of the Department of Clinical Medicine & Surgery, IUB. Faecal samples were examined using flotation and direct smear techniques for subsequent microscopic examination. For the examination of skin-scraping sample, a drop of KOH and an equal amount of skin-scraping material were placed on clean glass slide. The smear was examined under a microscope to check for the presence of parasites after the application of cover slip (Raza et al., 2024).
Eprinomectin (EPM) Administration: The topical EPM formulation was prepared according to Raza et al. (2024). A 5ml preparation was prepared for each animal. A total of 12 goats of both sexes were divided into two groups. Animals in Group A received the formulation of topical administration, whereas Group B was the control group and received no formulation. After administration of the therapy, all the goats were monitored for 14 days to determine any potential effects on the animals. Examine the application site for any indications of discomfort, such as pain, redness, allergies, peeling, or hair loss, any variations in the group’s social interactions and eating behavior, changes in body temperature, diarrhea, and mental states to observe the stress. The fecal samples were taken on 7th & 14th days to check therapeutic efficacy of EPM.
Collection and Processing of Blood Samples: The blood samples of goats were collected from both groups on 1st day and 14th day. The collected blood samples were processed for CBC and biochemical analysis. The blood analysis was performed by using a hematological analyser (BK-5000VET, Biobase industry Shandong Co., Ltd. China) at Central Diagnostic Laboratory Complex, IUB. Serum biochemistry was performed with the commercially available kits by following the manufacturer's instructions.
Statistical Analysis: The data was analysed using the SPSS software. The prevalence data was analyzed using the odd ratio and the Mental Haensel chi-square. The data on blood and serum were analysed using one-way ANOVA. However, the statistical significance level was P<0.05.
RESULTS
Prevalence of Ectoparasites in Goats: In current research, overall, 31.8% prevalence of ectoparasite is found in goats in south Punjab as shown in Table 1. The prevalence of ectoparasites in goats was higher in Bahawalpur area (59.3%) and the lowest in Khairpur (18.75%) area while Yazman, Ahmedpur and Hasilpur have a prevalence 31.25%, 28.1% and 21.8% prevalence respectively with a significant difference (P=0.04). The prevalence of ectoparasite was also studied sex wise that is 30.9% in males as compared to females with 32.6% with odds ratio = 0.92 [reciprocal = 1.08]. Similarly, in goats, prevalence of ectoparasite infestation was higher in older goats (52%) as compared to adults (24.44%) and sucklers (15%) with significant difference (P=0.005) when it was studied age wise. It has also been observed that the prevalence of tick infestation is significantly (P=0.029) higher (20%) in goats as compared to Lice (8.75%) and Mites (3.12%).
Table 1. Prevalence of Ectoparasites in Goat
Parameters |
No +ve (Prevalence) |
Total |
95% CI |
Odd Ratio/ P-value |
Area wise |
|
Bahawalpur |
19 (59.3%)) |
32 |
41.90 to 75.22 |
P = 0.040 |
Ahmedpur |
9 (28.1%) |
32 |
14.67 to 45.38 |
Hasilpur |
7 (21.8%) |
32 |
10.10 to 38.55 |
Khairpur |
6 (18.75%) |
32 |
7.97 to 34.98 |
Yazman |
10 (31.25%) |
32 |
17.09 to 48.67 |
Total |
51 (31.8%) |
160 |
25.00 to 39.40 |
Sex wise |
|
Male |
21 (30.9%) |
68 |
20.78 to 42.58 |
OR = 0.92
[reciprocal = 1.08] |
Female |
30 (32.6%) |
92 |
23.63 to 42.67 |
Total |
51 (31.8%) |
160 |
25.00 to 39.40 |
Age-wise |
|
Suckler |
03 (15%) |
20 |
3.96 to 35.61 |
P = 0.005 |
Adult |
22 (24.44%) |
90 |
16.41 to 34.10 |
Old |
26 (52%) |
50 |
38.24 to 65.54 |
Total |
51 (31.8%) |
160 |
25.00 to 39.40 |
Species wise |
|
Ticks |
32 (20.0%) |
160
160
160 |
0.53 to 52.17 |
P = 0.029 |
Lice |
14 (8.75%) |
16.22 to 40.14 |
Mites |
5 (3.12%) |
6.37 to 33.15 |
Overall |
51 (31.8%) |
160 |
25.00 to 39.40 |
Prevalence of Endoparasites in Goats: Overall prevalence of endoparasites in goats in south Punjab was 56.8% (Table 2). It was observed that the Ahmedpur areas have a high prevalence (78.1%) of endoparasite, and the lowest prevalence was found in the Hasilpur (43.75%) area while Yazman, Khairpur, and Bahawalpur had a prevalence 56.2%, 53.1% and 53.1% prevalence, respectively, with non-significantly difference (P=0.362). An equal prevalence (56.8%) of endoparasite was observed in both males and females with an odds ratio = 1.00 [reciprocal = 1.00]. A similar pattern of endoparasite infestation was found in goats when studied age-wise, older goats were more infested with endoparasites (64.66%) as compared to adults (57.75%) and sucklers (26.31%) with non-significant difference (P=0.079). A different pattern had been observed with respect to endoparasite infestation in goats when it was analysed according to the species. The Cocci (Emaria) were more prevalent in goats (17.5%) as compared to Toxocara (11.25%), Stronglyus (9.37%), Haemonchus (6.25%), Marshliagia (1.25%), Monizia (5.0%), and Gardia (6.25%).
Table 2: Prevalence of endoparasites in goats
Parameters |
No. +ve
(Prevalence) |
Total |
95% CI |
Odd Ratio/ P-value |
Area wise |
|
Bahawalpur |
17 (53.1%) |
32 |
35.94 to 69.76 |
P = 0.362 |
Ahmedpur |
25 (78.1%) |
32 |
61.45 to 89.90 |
Hasilpur |
14 (43.75%) |
32 |
27.48 to 61.11 |
Khairpur |
17 (53.1%) |
32 |
35.94 to 69.76 |
Yazman |
18 (56.2%) |
32 |
38.89 to 72.52 |
Total |
91 (56.8%) |
160 |
49.11 to 64.39 |
Sex wise |
|
Male |
33 (56.8%) |
58 |
43.97 to 69.15 |
OR = 1.00
[reciprocal = 1.00] |
Female |
58 (56.8%) |
102 |
7.12 to 66.22 |
Total |
91 (56.8%) |
160 |
49.11 to 64.39 |
Age-wise |
|
Suckler |
05 (26.31%) |
19 |
10.34 to 49.06 |
P = 0.079 |
Adult |
41 (57.75%) |
71 |
46.06 to 68.82 |
Old |
45 (64.66%) |
70 |
52.58 to 74.83 |
Total |
91 (56.8%) |
160 |
49.11 to 64.39 |
Species wise |
|
Toxocara |
18 (11.25%) |
160
160
160
160
160
160
160 |
32.95 to 64.55 |
P = 0.290 |
Stronglyus |
15 (9.37%) |
38.39 to 75.37 |
Cocci (Emaria) |
28 (17.5%) |
64.40 to 90.81 |
Haemonchus |
10 (6.25%) |
40.79 to 86.62 |
Marshliagia |
02 (1.25%) |
6.02 to 73.81 |
Monizia |
08 (5.0%) |
20.61 to 62.11 |
Gardia |
10 (6.25%) |
27.29 to 68.57 |
Overall |
91 (56.8%) |
160 |
49.11 to 64.39 |
Haematological Parameters in Goats: On 1st and 14th days after the of administration he EPM, the haematological parameters of goats among healthy and infected animals are shown in Figure 1. According to the results WBC, RBCs, HGB and MCV of infected goats were significantly (P<0.05) different from those of healthy, whereas values of lymphocytes, hematocrit and MCH were non significantly different (P>0.05) on 1st day. After the administration of topical
agent on 14th days, the blood parameters including WBC, MCV and MCH of treated group were significantly (P<0.05) different from the healthy groups, whereas LYM, RBC, HGB and HCT were non significantly different (P>0.05).

Figure 1: Blood parameters variation in Goat on 1st and 14thdays. White blood cells (WBC), Lymphocytes (LYM), Granulocytes (GR), Red Blood Cells (RBC), Hemoglobin (HBG), Hematocrit (HCT), Mean Corpuscular Volume (MCV), Mean corpuscular hemoglobin (MCH). *P<0.05.
Serum Biochemical Changes in goats: During the trial after the administration of transdermal agentonthe14th day the serum biochemistry analysis of healthy and infected goatswas performed as shown in (Figure 2). According to the results all parameters were non-significantly different (P>0.05) in both groups. These results indicates thattopical agent has no stress on animals and physiological parameters in goat.
 Figure 2: Serum biochemistry values in goats on 14th day. Total protein (TP), albumin (ALB), glutamic-pyruvic transaminase (GPT), serum glutamic-oxaloacetic transaminase (SGOT). The values were non-significantly (P>0.05) different between healthyand infected goats
Therapeutic Efficacy of EPM: The animals were observed after the application of topical agent for therapeutic efficacy of EPM. The results indicated that on 7th day, 3 (50%) goats were recovered. However, on 14th day, 5(83%) goats were recovered (Table 3).
Table 3: Therapeutic efficacy ofthe topicalagent eprinomectin in goats
Days/ Animals |
Goats (n=6) |
Efficacy (%) |
Day 7th |
3 |
50 |
Day 14th |
5 |
83 |
DISCUSSION
Prevalence of Parasites: Ticks have gained notoriety over the last 10 years for their ability to spread sustainably throughout Pakistan (Hassan et al., 2018; Sajid et al., 2020). Previously it is reported that district Bannu, KPK, Pakistan had the highest prevalence of lice (22.8%), ticks (9%) and mites (7.5%) with an overall 48.8% of ectoparasitic infestation (Khan, 2015). According to the study, there are significant regional differences in the prevalence of ectoparasites in goats as Bahawalpur has the highest incidence (59.3%), while Khairpur has the lowest frequency (18.75%) that is less than previous reports (Abah et al., 2022; Khan, 2015) and variation in endoparasites also observed (Ghafar et al., 2020). Variations in temperature, environmental factors, and management practices in various locations may be among the reasons for these discrepancies (Abah et al., 2022; Ghafar et al., 2020). Ahmedpur tehsil revealed the highest incidence of endoparasite (78.1%), while Hasilpur had the lowest incidence of endoparasite infestation which account for 43.75%. Considerable variations in the environmental temperature and management practices were the factors that impacted the life cycle and dissemination of endoparasites (Ghafar et al., 2020; Shah et al., 2021). Further investigation into these factors is necessary to find out the reasons behind these variations. The results show that the prevalence of ectoparasites is somewhat lower in bucks (30.9%) than in Does (32.6%) as compared to the findings of Abah et al. (2022) who reported a higher prevalence among female goats (70.5%) than in males (29.4%). Similar results were also reported by Kasim et al. (2019) in their studies that males have lower prevalence of ectoparasite than female goats. Our research also showed that the prevalence of ectoparasites is greater in older goats (52%) than adults (24.44%) and sucklers (15%) compared to previous studies (Hassan et al., 2019; Maurizio et al., 2021; Zvinorova et al., 2016) and supporting the results of Kasim et al. (2019). The weak immune system associated with aging and/or cumulative exposure may be the cause of this age-related difference (Khan et al., 2022). According to our findings, there is an obvious age-related pattern to endoparasite infestations, with older goats exhibiting a higher incidence (64.66%) than adults (57.75%) and sucklers (26.31%) as reported previously (Abah et al., 2022; Kasim et al., 2019; Khan, 2015). However, additional in-depth study is needed to assess statistical significance and uncover the underlying reasons. The odds ratio of 0.92 indicates a minor protective effect in males similar to previous studies (Kasim et al., 2019; Khan et al., 2022). It's interesting to see that endoparasites are more common in both male and female goats (Maurizio et al., 2021; Zvinorova et al., 2016). The odds ratio of 1.00 suggests that there is no considerable difference in the sex-wise endoparasite infestation. This finding contradicts the studies that show variations in parasite infections based on gender (Maurizio et al., 2021; Zvinorova et al., 2016). The ticks have the highest prevalence (41%) compared to the study of Kasim et al. (2019), where lice have the highest prevalence (31.7%), followed by lice (26.9%) and mites (16.7%) that is similar to the study of Muhammad et al. (2021). Understanding the dynamics of these specific ectoparasite populations is crucial for the development of targeted control and prevention strategies (Ghafar et al., 2020; Kasim et al., 2019; Khan et al., 2022; Muhammad et al., 2021).
Hematobiochemical Changes and Oxidative Stress: According to previously research, blood sucking parasites are also one of the major causes of anemia in goats, effecting their growth and productivity (Kasim et al., 2019). Khan (2015) also reported that endoparasites are among the major problems in Pakistan effecting blood parameters. The hematology parameters are greatly varied by ectoparasites. Khan (2015) revealed a higher trend of ESR than normal goats. Furthermore, on the 14th day after treatment, serum biochemistry examination revealed that the values of albumin, SGOT, total protein, and GPT were not significantly affected in both groups showing that EPM did not cause stress or any physiological changes in goats.
Therapeutic Efficacy of Eprinomectin: Subclinical disease is the predominant result of infection by gastrointestinal parasites (Fthenakis and Papadopoulos, 2018; Maurizio et al., 2021). Understanding the prevalence of specific species is critical to carry out targeted treatment and management strategies (Muhammad et al., 2021; Ruhoollah et al., 2023). Rostang et al. (2020) also reported that goats are more susceptible to parasitic infestation, contrasting with the research of Kasim et al. (2019). The results of this study indicated that on 14th day 5 (83%) goats were recovered. EPM can be effectively employed for the treatment of parasites and large lungworms in sheep and goats as an injectable and pour-on drug (Hinney et al., 2022; Raza et al., 2024; Rehbein et al., 2014). Another researcher in his research also reported that Haemonchus contortus is the most pathogenic trichostrongyloid species in small ruminants that developed anthelmintic resistance (Hinney et al., 2022; Qamar and Alkheraije, 2023). Therefore, goat farmers should follow the administration of EPM drug to control parasites of goats.
Conclusion: It was concluded that endo and ectoparasites in goats are of considerable significance, whereas eprinomectin has beneficial effect by improving animal health and reducing parasitic infestation. The outcomes emphasized the use of eprinomectin for parasitic control for better animals’ health.
Funding: This study was funded by Office of Research, Innovation and Commercialization (ORIC), IUB (3878/ ORIC/IUB/2021), The Islamia University of Bahawalpur, Pakistan.
Acknowledgment: The authors would like to extend their sincere appreciation to the Research Supporting Project number (RSP2024R374), King Saud University, Riyadh, Saudi Arabia.
Conflict of Interest: The authors have declared no conflict of interest.
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