Gastrointestinal nematodiasis of goats in Somali pastoral areas, Ethiopia

Abstract

Livestock, mainly goats, are crucial for animal protein, household income, economic security, and wealth creation in the pastoral areas of eastern Ethiopia. However, gastrointestinal parasitosis poses a substantial challenge in this sector. A cross-sectional study was conducted in the Gursum district of the Somali region, Ethiopia, to investigate the prevalence and intensity of gastrointestinal nematodes in goats and their associated risk factors. A total of 384 goat fecal samples were collected and examined using flotation and McMaster egg counting techniques for GIT nematodes. Coprological cultures have also been conducted for nematode identification. Fecal samples showed an overall parasite prevalence of 54.17%, with identified nematodes including Haemonchus (24%), Strongyloides (10.4%), Trichostrongles (6.5%), Nematodirus (6%), Oesophagostomum (5.5%) and Trichuris (1.87%). Older and poor body condition animals had higher chances of hosting nematodes than younger (OR = 0.245; CI = 0.144–0.417) and good body condition animals (OR = 0.069; CI = 0.030–0.157), according to multivariate logistic regression analysis. Quantitative examination of eggs revealed light 75(36.06%), moderate 99(47.60%), and heavy infection (n = 34, 16.35%). Analysis of the different study variables indicated that the age and body condition of the animals and the season of the year had a statistically significant association with the prevalence of GIT nematode infections (P-value <0.05). The high prevalence and intensity of GIT nematodiasis in goats from the study area warrants immediate attention and the implementation of strategic control and prevention measures.

1. Introduction

Goats were domesticated before cattle and sheep and are now a crucial livestock species, especially in tropical and subtropical areas. They provide income and work opportunities for rural communities, and are raised for milk, meat, hair, and leather (Monau et al., 2020). Given their short intergenerational cycles and absence of religious stigmas, goats are ideal for human consumption. Additionally, their meat is a rich source of protein and can aid in reducing the protein malnutrition gap among consumers (Nair et al., 2021). The goat intestine is used to make the catgut, which is still used as a material for internal human surgical sutures and strings for musical instruments (Kim et al., 2020).

Despite the large population of goats (30.20 million) in Ethiopia (CSA, 2016), the economic benefits of livestock are restricted due to diseases, malnutrition, inadequate management, and lack of access to veterinary care, despite being an abundant resource. This contributes to high morbidity and mortality rates, with annual losses of up to 50% of the total livestock product value (Innocent et al., 2022). Goats frequently contract gastrointestinal (GI) parasitic infections, particularly nematodes, which result in significant economic losses due to animal mortality and decreased weight gain (Dey et al., 2020).

Gastrointestinal nematode (GIN) parasites are a substantial burden in most goat production systems worldwide because of their impact on productivity and the indirect costs of control measures implemented by livestock producers (Gilleard et al., 2021). The burden of nematode parasitism is particularly severe in developing countries, where inadequate nutrition and a lack of efficient control methods leads to compromised natural immunity, contributing to low productivity and a high mortality rate (Sebro et al., 2022). Nematode parasites have adverse effects on animals such as reducing their growth rate, causing weight loss, and delaying their maturity, particularly in those being raised for slaughter (de Waal and Rinaldi, 2023). Numerous GI nematodes belonging to the genera Haemonchus, Trichostrongylus, Oesophagostomum, Bunostomum, Strongyloides, Cooperia, Nematodirus, and Trichuris have been reported in parasitological studies conducted in various parts of the country (Berhe and Aragaw, 2019; Haile et al., 2018; Kenea et al., 2015). Studies on gastrointestinal parasites of goats from various parts of Ethiopia have revealed a prevalence range of 40%–80% (Abdo et al., 2017; Ayana and Ifa, 2015; Hurisa et al., 2021).

Ethiopia is located in the tropical latitudes of Africa and has a diverse topography, a wide range of climatic characteristics, and a multitude of agro-ecological zones, making it suitable for various agricultural production systems. This has led to the development of a wide range of farm animal genetic resources across the country (Tamiru, 2018). Nematode parasites in Ethiopia are prevalent because of poor animal health services, mixed farming practices, communal grazing with different animal species, and favorable geographic conditions (Dawit et al., 2022). Parasite management, especially that of gastrointestinal worms, is a common animal health concern in farms and ranches. Anthelmintics are the usual methods for controlling nematodes, either for prevention or treatment. Effective control strategies can reduce the effects of helminths. Understanding the epidemiology and ecology of parasites in local conditions is crucial. Identifying the specific groups present in a flock or herd is essential for implementing effective control measures (Zajac and Garza, 2020). The prevalence of GIT parasites, the genera and species involved in helminthic parasites, and the intensity of infection vary considerably depending on local environmental factors such as humidity, temperature, rainfall, vegetation, and management practices (Belina et al., 2017). Considering the economic importance of gastrointestinal nematode infections, the present study was designed to estimate the prevalence of gastrointestinal nematodes affecting goats in Gursum district, and to identify various risk factors influencing the prevalence and intensity of GIT nematodes in goats in the study area.

2. Materials and methods

2.1. Description of the study area

The study was conducted in Gursum district, Somali region, Ethiopia, which is located 600 km east of Addis Ababa. The district has an altitude of 1200–1600 m above sea level, and the temperature of the area is generally high year-round, with mean annual minimum and maximum temperatures of 20 and 35 °C, respectively. The mean annual rainfall is approximately 700 mm and bimodal. The two most common production systems used for livestock herding in rural areas are agro-pastoralist and free-range pastoralist. Sorghum, maize, barley, wheat, and beans are among the most widely farmed crops. The estimated goat population in the district is approximately 13,885 (CSA, 2016; Tumusiime et al., 2022) (See Fig. 1).

Fig. 1.

Map of the study area (Gursum district in Fafan zone Somali region, Ethiopia).

2.2. Study population

The study animals consisted of indigenous breeds of goats from Gursum District that are raised in pastoral rearing practices that allow free communal grazing, usually mixed with livestock from other villages, where animals move from areas of feed shortage to areas of abundant feed, particularly during the drought season. Goats of all age categories and both sexes were included in the study. Animals that had received anthelminthic treatment for the past two months were excluded from the study.

2.3. Study design

A cross-sectional study was conducted from December 2020 to May 2021 to estimate the prevalence rate and identify the associated risk factors for the occurrence of gastrointestinal nematodes in goats in the study area.

2.4. Sample size determination and sampling method

The sample size was calculated based on the formula described by Thrusfield (Thrusfield, 2018), using 50% expected prevalence, 5% absolute precision, and a 95% confidence interval. A total of 384 animals were sampled. The district was chosen conveniently based on the goat production population, accessibility to vehicles, proximity to livestock markets, and presence of animal watering sites. However, a simple random sampling (SRS) method was used to choose pastoral associations (PAs) and herds from a list provided by the District Pastoral Development Office. The sample size was proportionally distributed to the selected PAs and herds based on the total goat population. Finally, individual animals were sampled at each interval using SRS. The data of the animal related to age, sex, body condition score (BCS). The ages of the sampled animals were determined by asking the owners and evaluating their dentition (Kumsa et al., 2011). The BCS of the study animals was evaluated by looking at the back and flank and categorized as good, medium, and poor (Pant et al., 2009).

2.5. Sample collection and laboratory investigation

A fecal sample of approximately 6 g was collected directly from the rectum of each animal using a gloved finger, placed in separate universal bottles, and immediately transported to the Jigjiga University laboratory using cold boxes for coprological examination. Information related to the age, sex, and body condition of the animals and the sampling seasons (dry or wet) was recorded.

2.5.1. Coprological examination

The fecal samples were examined qualitatively for the presence of nematodes by flotation and quantitatively to assess the number of eggs per gram of feces using McMaster. Saturated sodium chloride was used to prepare the flotation fluid, and the nematode parasite eggs were identified. For positive samples, a McMaster egg count was performed, and egg counts of 50–799, 800–1200, and over 1200 eggs per gram of feces were considered light, moderate, and massive infections, respectively (Bowman, 2020). Positive samples were continued for larval culture, and subsequently, the infective larvae (L3) were separated to the genus level based on the morphologic features as outlined by (Taylor et al., 2015; Zajac et al., 2021).

2.6. Data analysis

The collected data were recorded in Microsoft Excel and analyzed using SPSS version 23. Descriptive statistics were used to establish GIT nematode prevalence, and the chi-square (X²) test was used to examine the association between GIT nematode prevalence and risk variables. Furthermore, the odds ratio of each risk factor for GIT nematode infection was determined using a logistic regression model, adjusted for potential confounding factors. The analysis used a 95% confidence level with significance level of a P-value < 0.05.

3. Results

According to the current study, the overall prevalence of gastrointestinal nematodes in goats in the study area was 54.17%. Among the identified parasitic genera, Haemonchus was the most common with prevalence of 24%, followed by Strongyloides 10.4%, Trichostrongles 6.5%, Nematodirus 6%, Oesophagostomum 5.5%, and Trichuris 1.87%.

The prevalence of GINs in goats among PAs was higher in Fayanbira (64.3%) and Halo-hako (53.1%) than in Fafan (48.9%) and Gursum (50.0%). Similarly, the study revealed that GINs were more prevalent in young goats (71.2%) than in adult goats (45.9%) and in females (57.8%) than in males (48.3%). Furthermore, goats with poor body condition showed a higher prevalence of GINs (85.5%), followed by goats with medium body condition (52.5%), and good body condition (40.2%). More goats were infected during the wet season than the dry season (66.4% and 49.5%, respectively). Age, body condition, and seasonal variations were significantly associated with the prevalence of GIN parasite infection (P < 0.05). However, there was a statistically insignificant difference in the prevalence of GINs between the sexes of goats and locations (P > 0.05) (see Table 1).

Table 1.

Prevalence and associated risk factors of GI nematodes in goats.

Variables	No of Examined (Prevalence)	X2	P-value
Location
Fafan area	94 (48.9%)	5.791	0.122
Halo-Hako area	96 (53.1%)
Gursum area	96(50.0%)
Fayanbira area	98 (64.3%)
Age
Young	125(71.2%)	21.66	0.0000
Adult	259 (45.9%)
Sex
Female	237 (57.8%)	3.30	0.0692
Male	147 (48.3%)
BSC
Poor	69 (85.5%)	37.96	0.0000
Medium	183 (52.5%)
Good	132 (40.2%)
Season
Dry	281 (49.8%)	7.965	0.005
Wet	103 (66.0%)

Multivariate logistic regression analysis revealed that older animals were more likely to be harboring nematode parasites compared to younger animals (OR = 0.245; CI = 0.144–0.417). Similarly, animals with a poor body condition score were more likely to be infected than those with a good body condition score adjusted (OR = 0.069; CI = 0.030–0.157). Moreover, seasonally, goats in the wet season had higher odds of being infected compared to goats in the dry season (OR = 2.509; CI = 1.473–4.271). There was a statistically significant difference in the proportion of goats with GINs in relation to the risk factors of age, BSC, and season (see Table 2).

Table 2.

Logistic regression analysis of GIN-infected animals with various host-related risk factors.

Variables	No of Examined (Prevalence)	OR(95% CI)	p-value
Location
Fafan area	94 (48.9%)		0.320
Halo-Hako area	96 (53.1%)	1.388 (0.727–2.649)	0.536
Bombas area	96(50.0%)	1.226 (0.643–2.338)	0.006
Fayanbira area	98 (64.3%)	2.486 (1.293–4.777)
Age
Young	125(71.2%)		0.000
Adult	259 (45.9%)	0.245(0.144–0.417)
Sex
Female	237 (57.8%)		0.188
Male	147 (48.3%)	0.729(0.456–1.166)
BSC
Poor	69 (85.5%)		0.000
Medium	183 (52.5%)	0.170(0.079–0.365)	0.000
Good	132 (40.2%)	0.069 (0.030–0.157)
Season
Dry	281 (49.8%)		0.001
Wet	103 (66.0%)	2.509 (1.473–4.271)

The McMaster egg counting approach was used to conduct an EPG count on 208 fecal samples that tested positive for GIN eggs in the qualitative parasitological examination. Accordingly, heavy infection (16.35%) was the least prevalent compared to moderate (47.5%) and light (36.06%) infections.

The current investigation revealed a strong correlation between parasite load and animal body condition, with a statistically significant difference (P < 0.001) (see Table 3). This was demonstrated by the fact that heavily affected goats had poorer BSC than animals that had medium-to-good BSC. However, there were no statistically significant differences between the two age and sex groups (P > 0.05). Additionally, this study found no significant relationship between location, season, and EPG (P > 0.05).

Table 3.

Intensities of GINs with different risk factors in the study area.

		Intensity of Parasite infection
Variable	No of Examined	Light (%)	Moderate (%)	Heavy (%)	X2	P-value
Location
Fafan area	46	16(34.8)	25(54.3)	5(10.9)	3.55	0.738
Halo-Hako area	51	20(39.2)	21(41.2)	10(19.6)
Gursum area	48	19(39.6)	20(41.7)	9(18.8)
Fayanbira area	63	20(31.7)	33(52.4)	10(15.9)
Age
Young	89	30(33.7)	40(44.9)	19(21.3)	2.85	0.241
Adult	119	45(37.8)	59(49.6)	15(12.6)
Sex
Female	137	45(32.8)	69(50.4)	23(16.8)	1.84	0.398
Male	71	30(42.3)	30(42.3)	11(15.5)
BSC
Poor	59	7(11.9)	25(42.4)	27(45.8)	59.35	0.000
Medium	96	40(41.7)	50(52.1)	6(6.2)
Good	53	28(52.8)	24(45.3)	1(1.9)
Season
Dry	140	54(38.6)	62(44.3)	24(17.1)	1.90	0.386
Wet	68	21(30.9)	37(54.4)	10(14.7)

4. Discussion

The current study found that the overall prevalence of GINs in goats in the study area was 54.17%, which agrees with prevalence reports of 52.67% from Hararghe, eastern Ethiopia (Belina et al., 2017) and 53.29% from Haramaya, eastern Ethiopia (Ahmed et al., 2017). However, it is comparatively lower than prevalence reports of 78.2% from Alage, Southern Ethiopia (Moje et al., 2021) and 100% nematode prevalence in goats from Nyagatare district, Rwanda (Tumusiime et al., 2022). Similarly, the current study disagrees with prevalence reports of 42.1% in Tullo district, western Hararghe, Ethiopia (Getachew et al., 2017) and 26.6% of GINs prevalence in goats from Damaturu, Yobe State, Nigeria (Adamu and Kyari, 2023). Factors affecting the prevalence of nematode infections in goats include ecological conditions, host diversity, and study methodology. Ecological and climatic conditions can impact the growth and transmission of parasites, while different host species may have varying levels of resistance. Animal movement can also spread parasites more rapidly. Varying sample sizes and detection methods used in studies can also affect prevalence rates (Nisa et al., 2021).

Examination of fecal cultures revealed GINs genera of Haemonchus 24%, Strongyloides spp. 10.4%, Trichostrongles 6.5%, Nematodirus 6%, Oesophagostomum 5.5% and Trichuris Spp.1.87% which agrees with genera reported from Eastern and Southeastern Ethiopia by (Belina et al., 2017; Moje et al., 2021).

GINs were more common in young goats (71.2%) than in adult goats (45.9%); however, there was no statistically significant correlation between the two. A similar result was reported in goat farms in Central Uganda, Lesotho, South Africa, and Madhya Pradesh, India (Matsepe et al., 2021; Mpofu et al., 2020; Nsereko et al., 2016; Singh et al., 2015). Comparatively, higher prevalence rates were observed in females (57.8%) than males (48.3%), which is in line with the study of (Dey et al., 2020) but disagrees with reports of higher rates in males from Sylhet, Bangladesh by (Islam et al., 2019) and from Ibadan in Nigeria (Olanike et al., 2015). However, female animals are more susceptible to GIT nematodes during pregnancy and the per-parturient period owing to stress and decreased immune status (Zajac and Garza, 2020).

Furthermore, goats with poor body conditions had a significantly higher prevalence of GINs than those with medium or good body conditions, which is consistent with previous studies in central, southern, and northern Ethiopia (Elemo and Geresu, 2017; Fayisa et al., 2020). In general, animals with poor body condition have significantly higher rates of gastrointestinal nematode infection than animals with other types of body condition. This could be attributed to the fact that poorly nourished animals are less capable of fighting infections, whereas well-fed animals are unlikely to succumb to the disease under ideal environmental conditions (Johnson et al., 2020).

The current study further revealed a significant difference between seasons (P < 0.05). More parasitic infections were detected during the wet season than during the dry season. This is in agreement with previous reports from the eastern highlands and pastoral areas of Ethiopia (Haile et al., 2018; Zeryehun, 2012) and from Tamil nadu, India by (Varadharajan and Vijayalakshmi, 2015). Increased browsing time in the warm rainy season increases the chance of contact between the host and parasites. According to previous reports, a lengthened browsing time increases the likelihood that the host and parasites will come into contact (Matsepe et al., 2021).

Accordingly, the intensity of GIN was determined by counting the number of eggs found in feces or eggs per gram of feces. The FEC indicated the presence of light, moderate, and heavy GIN infections in the study area. GIN infections were light (36.06%), moderate (47.60%) and heavy (16.35%). This contradicts previous findings of higher rates of heavy infection 48.5% moderate 30% and light 21.7% by (Ahmed et al., 2017) and heavy infection 56.5% moderate 34.5% and light 9% by (Getachew et al., 2017). and 9.2% of massively, 25.2% moderately and 65.6% lightly infected (Emiru et al., 2013). Possible reasons for the lower intensity of GIT nematode infection found in our study could be increased awareness of farmers about deworming or development of immunity among goats in the region. Further research is needed to explore these hypotheses and better understand factors affecting nematode infections in goats.

5. Conclusion and recommendations

The study indicated that the overall gastrointestinal nematode prevalence of goats in the study area was 54.17%, and the most prevalent nematode species identified were Haemonchus, Strongyloides, Trichostrongles, Nematodirus, Oesophagostomum and Trichuris in descending trend. The parasite infection was found to have a statistically significant association with the age and body condition of the study animals, as well as the season of the year. Therefore, an appropriate control and prevention program taking these findings into account should be designed and implemented. Further studies involving the economic significance, and public awareness of gastrointestinal nematodes of goats in the study area should also be conducted.

Financial support

This study was financially supported by Jigjiga University, Research and Community service Directorate.

Ethical statement

Ethical approval was obtained from Jigjiga University's research ethical committee who approved the research with permit No. JJU/REC/021/2020. Verbal consent was obtained from animal owners for collection of feces from the rectum of their goats.

Declaration of Competing Interest

The authors declare that there is no conflict of interest.