Brucellosis is an important neglected bacterial zoonotic disease in sub-Saharan Africa, including Somalia. A cross-sectional study was conducted in the Garowe district, Nugal region, Somalia, from May 2022 to January 2023 to estimate the seroprevalence of small ruminant brucellosis and assess owners’ knowledge, attitudes, and practices toward brucellosis. A total of 384 sheep and goats were selected using a simple random sampling technique and screened for Brucella antibodies by the Modified Rose Bengal Plate Test, and positive samples were then further confirmed using an indirect enzyme-linked immunosorbent assay. For the questionnaire survey, 384 households were selected randomly, and a structured questionnaire was used to assess owners’ knowledge, attitudes, and practices toward brucellosis. The overall brucellosis seroprevalence was 4.7% in small ruminants (95% CI: 2.8-7.3), and the true seroprevalence was calculated as 5.2%. According to the multivariable logistic regression analysis, sex was found to be a potential risk factor for small ruminant brucellosis (P < .05). More specifically, female sheep and goats were 9.13 times (aOR 9.13, 95% CI: 1.18-70.33) more likely to become seropositive than males. The owners’ knowledge, attitudes, and practices toward brucellosis were found to be low, and education level was associated with owners’ knowledge (χ2 = 16.78; P < .001), attitudes (χ2 = 19.4; P < .001) and practices (χ2 = 34.0; P < .001). There is also a significant association between owner knowledge, attitudes, and practices and seropositivity of brucellosis in sheep and goats. Moderate seroprevalence, together with insufficient knowledge, attitudes, and practices of owners, makes brucellosis a threat to animals and the entire community. Hence, raising community awareness of the disease is essential to reduce the impact on small ruminant productivity and the risks to public health.
Introduction
Small ruminants constitute the largest population of domestic animals in Somalia, but the country fails to utilize these resources optimally because of different factors in which diseases stand first. One of many infectious diseases impeding small ruminant production is brucellosis.1
Small ruminant brucellosis is caused mainly by Brucella melitensis and B. ovis and, in sporadic cases, by B. abortus.2 The disease has a major socioeconomic impact on the livelihood of communities that depend on animal production, especially in developing countries where disease control programs are either nonexistent or inadequate. These losses are associated with abortion, neonatal death, reduced fertility, decreased milk production, and trade restrictions for animals and their products.3 The disease is transmitted from infected to susceptible sheep and goats through sexual contact, ingesting contaminated pastures, feedstuffs and water or licking infected placentae, foeti or the genitalia of infected female animals soon after abortion or delivery.4 The prevalence of brucellosis in Somalia is 4% and 3.1% in sheep and 4.9% and 3.9% in goats according to RBT and I-ELISA, respectively.5,6
Brucellosis is a zoonotic, chronic, debilitating disease in humans, with an estimated half a million human annual cases reported globally.7 The consumption of contaminated raw animal products and direct contact with contaminated tissues or secretions of infected animals are the main routes of infection in humans.7 A very important approach to the control of brucellosis is the one health approach to control and prevent human and animal brucellosis.8 Therefore, assessing owners’ knowledge, attitudes and practices (KAPs) toward brucellosis and determining the associations between owners’ KAPs and brucellosis seropositivity in their animals are important for establishing prevention and control strategies for both animals and humans. Hence, the aim of this study was to estimate the seroprevalence of small ruminant brucellosis and assess owners’ KAPs toward brucellosis in the Garowe district, which is in Puntland, Somalia.
Materials and Methods
Study area and animal population
The study was conducted in Garowe district, Nugal region in Somalia. The district is situated between 8°24'N latitude and 48°29'E longitude (Figure 1). The agroecology of the district is arid, with altitudes ranging from 100 to 500 m above sea level. It receives average annual rainfall between 10.8 mm and 51 mm/year, and the temperature ranges from 23°C in the winter to 41°C in the summer. Pastoral production systems are the main production systems used in the area, and livestock production, especially goat, sheep and camel production, is a major component of the livelihood of the community. The district has a total population of 3 555 266 livestock, with 1 959 593 goats, 1 217 801 sheep, and 377 872 camels. Animals are managed under an extensive management system, graze freely during the day, are kept in poorly constructed fenced barns at night, and they share common grazing and watering points. Sheep and goats found in the Garowe districts composed the source population, and all sheep and goats above 4 months of age were eligible for inclusion in this study.9
Study design and period
A cross-sectional study was conducted between May 2022 and January 2023 to estimate the seroprevalence and associated risk factors for sheep and goat brucellosis and to assess the knowledge, attitudes and practices of owners toward brucellosis in the Garowe district, Nugal region, Somalia.
Sample size and sampling procedures
A single population proportion formula given by Thrusfield10 as where n = the total sample size, pexp = expected prevalence, and d = desired absolute precision, was used to determine the minimum sample size required to estimate the seroprevalence status of brucellosis in goats and sheep in the selected area. Thus, using 5% absolute precision, a 95% confidence level, and a 50% expected seroprevalence yielded a sample size of 384 study animals. The Garowe district has 16 villages from these villages, 4 villages were selected randomly, and 384 households were selected from these 4 villages by using an online random number generator. The lists of animal owners were our study frames and were found in each village administrative office.
Questionnaire survey and data measurement techniques
To collect relevant information about owners’ knowledge, attitudes, and practices toward brucellosis, a pretested structured questionnaire was administered to 384 randomly selected sheep and goats’ owners after translation into a local language (af-Soomaali) using a face-to-face interview. The questionnaire was developed by checking the face validity (matching each item to the conceptual domain) and content validity (representativeness) by 2 senior public health and microbiology professionals, and some amendments were made on the basis of their suggestions. The construct (convergent) validity was also checked by using both the average variance extracted and the factor loading of the 3 factors, with scores for knowledge, attitudes and practices of 0.621, 0.683, and 0.576, respectively, which was above the commonly accepted threshold of 0.50, indicating good convergent validity of the constructs. The lists of owners were obtained from each village administrative office. A pilot study of 30 individuals who were not included in the final analysis was used to test the internal consistency reliability. The results showed Cronbach’s alpha scores for knowledge, attitudes, and practices of .714, .801, and .836, respectively, indicating good internal consistency and reliability. The survey comprises 8 questions pertaining to knowledge assessment, 6 questions concerning attitudes, and 7 questions about practices.
Blood sample collection and serological tests
Seven milliliters of blood were aseptically drawn from the jugular vein of each sampled animal by using needle holders, simple vacutainer tubes, and needles. The blood samples were labeled and transported to the Garowe regional laboratory by using an ice box. Each blood sample was centrifuged for 3 minutes at 10,000 rpm to extract the serum, which was then siphoned into sterile cryovials. Finally, the sera were kept in a refrigerator at −20°C until they underwent serological testing to look for anti-Brucella antibodies.11
Screening was performed using Modified Rose Bengal Plate Test (MRBPT) (concentrated suspension of B. Melitensiss, Weybridge strain 99; Institut Pourquier, France), and confirmatory test using Indirect Enzyme-linked immune sorbent assay (I-ELISA) (ID Vet, 310, Innovative Diagnosis, France) were performed at the Garowe regional laboratory using test protocols outlined by the World Organization for Animal Health12 and the manufacturer’s specifications for the tests. Briefly, MRBPT was performed by mixing 75 µl of serum with 25 µl of antigen suspension on a glass plate and mixing thoroughly to create a circular approximately 2 cm in diameter. The mixture was subsequently agitated by shaking for 4 minutes at ambient temperature (25°C). Samples with agglutination were recorded as positive for MRBPT, whereas samples with no agglutination were recorded as negative. Both positive and negative controls were used. The low sensitivity, particularly in long-term chronic cases, relatively low specificity in endemic areas and the possibility of biological false negative reactions are the main limitations of MRBPT.
The I-ELISA test was conducted as follows: 190 µl of dilution buffer 2 was added to all the wells, 10 µl of the negative control was added to wells A1 and B1, 10 µl of the positive control was added to wells C1 and D1, and 10 µl of sample serum was added to the remaining wells. The plate was subsequently incubated for 45 minutes at 21°C, after which each well was washed 3 times with 300 µl of the wash solution. About 100 µl of multispecies Horseradish Peroxidase conjugate was added to each well, and the plate was incubated for 30 minutes at 21°C. Each well was washed 3 times with 300 µl of the wash solution. About 100 µl of the substrate solution was added to each well, and the plate was incubated for 15 minutes in the dark. About 100 µl of stop solution (Tetra methyl Benzidine substrate) was added to each well to stop the reaction, and the optical density (OD) at 450 nm was subsequently read and recorded for each sample. If the percentage of inhibition was 110% or lower, the outcome was categorized as negative. In cases where the percentage of inhibition fell between 110% and 120%, it was regarded as uncertain or doubtful. If the percentage of inhibition was 120% or above, the result was recorded as positive. Both positive and negative control sera were used. Since the sensitivity and specificity of I-ELISA are not 100%, we calculated the true seroprevalence by considering the sensitivity and specificity of I-ELISA (sensitivity, 0.93; specificity, 0.96). The potential for cross-reactivity of the secondary antibody is the limitation of I-ELISA.
Data management and analysis
Data obtained from the laboratory results and questionnaire surveys were entered and stored in a Microsoft Excel spreadsheet. Descriptive and analytical statistics were computed using Stata version 16.0. Univariable logistic regression analysis was employed to assess the associations of small ruminant brucellosis with species, age, sex, and origin (potential predictor variables). In this model, we applied an intermethod model development approach; hence, all variables present in the univariable logistic regression analysis were also included in the multivariable logistic regression analysis, and there was no need to select independent variables since the number of available variables was limited (four). The collinearity between variables was checked by the variance inflation factor (VIF). A VIF greater than 5 indicates that there is collinearity between variables. The final multivariable logistic regression model was checked by using the Hosmer-Lemeshow test, and it was fitted for the sheep and goat datasets with χ2 test = 3.22, Df = 7, and P = .8639. For all the KAPs questions, the respondent received a score of 1 if the question was answered properly and a score of 0 otherwise. The respondents were further divided into 2 groups for KAP after all the scores for correctly answered questions were added and the mean was set as the cut-off point. Individuals who scored higher than or equal to the mean were classified as possessing good knowledge, desirable attitudes, and appropriate practices, whereas those who scored lower than the mean were classified as having poor knowledge, undesirable attitudes, and inappropriate practices.13 The chi-square (χ2) test was used to assess the associations of owners’ gender, age and education with their KAPs and owners’ KAPs with the seropositivity of their animals. Throughout the data presentation, we applied the 95% confidence level α = (100 − 95) = 5%, which is the type 1 error (the probability of rejecting the null hypothesis when it is actually true).
Results
Demographic information of the respondents
For the assessment of the KAPs of owners toward brucellosis, a total of 384 individuals were interviewed, and most of them (67.7%) were females. The majority (52.6%) of the respondents were aged between 18 and 30 years, and most of the animal owners (62.0%) were noneducated (Table 1).
Table 1.
Demographic information of the respondents in the Garowe district.
Seroprevalence of small ruminant brucellosis and associated factors
The overall seroprevalence of small ruminant brucellosis in the study area was 4.7%, and the true seroprevalence was calculated as 5.2%. Univariable logistic regression analysis revealed that sex was significantly associated with the seroprevalence of small ruminant brucellosis (P < .05) (Table 2).
Table 2.
Univariate logistic regression analysis of small ruminant brucellosis and associated risk factors.
The seropositivity of small ruminant brucellosis was independently associated with sex (P = .034). Accordingly, the likelihood of brucellosis seropositivity in female sheep and goats was 9.13 times (95% CIOR: 1.18-70.33) greater than that in male sheep and goats (Table 3).
Table 3.
Multivariable logistic regression analysis results of small ruminant brucellosis with associated factors in the Garowe district from May 2022 to January 2023.
Knowledge, attitudes, and practices of the owners toward small ruminant brucellosis
Knowledge of the respondents toward small ruminant brucellosis
Among all of the interviewees, 23.2% had information about brucellosis, and the majority (66.3%) obtained their information from veterinarians. Even if 76.4% of the respondents knew that brucellosis affects sheep and goats, only 13.2% knew the means of transmission of the disease between animals.
From the participants, only 14.6% were aware that brucellosis is a zoonotic disease, and the majority of them (85.4%) did not know how animals may spread disease to humans (Figure 2).
The mean knowledge score was 2.5 ± 2.82, with a minimum score of 0 and a maximum score of 8. Overall, only 16.9% had good knowledge about brucellosis. The respondents’ educational status was shown to be significantly associated with their knowledge (P < .001) (Table 4).
Table 4.
Knowledge level and association between knowledge and respondents’ sociodemographics in the Garowe district.
Respondent attitudes toward small ruminant brucellosis
Among all the participants, 14.6% believed that brucellosis is an important public health disease, and only 9.0% believed that family members are at risk of acquiring brucellosis. From all the respondents, 92.1% wanted to obtain more information about the disease. Only 3.4% and 4.5% of the participants thought that brucellosis can be avoided by cooking meat and boiling milk, respectively (Figure 3).
The mean score of participants’ attitudes toward the disease was 1.05 ± 0.97. The percentage of respondents who, generally, had a positive outlook on small ruminant brucellosis was 15.7%. Educated individuals had better desirable attitudes (53.8%) toward brucellosis than noneducated individuals (P < .001) (Table 5).
Table 5.
Attitude level and associations between attitudes and respondents’ sociodemographics.
Practices of respondents concerning small ruminant brucellosis
Goat milk and sheep milk were consumed by 71.9% of the respondents, and most of them consumed raw milk (89.1%). The majority of the participants (96.0%) assisted their sheep/goats during kidding and lambing, and most (97.7%) of them assisted without using personal protective equipment. Nearly all of the participants (97.7%) dispose the aborted/dead fetuses dropping to open dumps or giving to dogs (Figure 4).
The mean practice score of the participants was 1.02 ± 0.94. The percentage of respondents who generally had appropriate practices for small ruminant brucellosis was 3.5%. Similarly, educated individuals had better practices (17.1%) toward brucellosis than noneducated individuals (P < .001) (Table 6).
Table 6.
Associations between practices and respondents’ sociodemographics.
Association between owners’ knowledge, attitudes and practices and the seroprevalence of their sheep and goats
The associations between owners’ knowledge, attitudes and practices and the seropositivity of their animals were assessed by using univariable logistic analysis. There is a significant association between owners’ practices and the seropositivity of their animals; hence, sheep and goat brucellosis seropositivity is significantly lower (χ2, 37.9, P < .001) in owners who have appropriate practices for brucellosis than in those who have inappropriate practices. However, the knowledge and attitudes of owners are not significantly associated with sheep and goat brucellosis seropositivity (Table 7).
Table 7.
Associations between owners’ knowledge, attitudes and practices and the seroprevalence in their animals.
Discussion
Recognizing the distribution of a disease and the knowledge, attitudes and practices of the community is a basic element in implementing disease prevention and control programs.14
Among the 384 serum samples collected for seroprevalence investigation, 32 (8.3%) were positive for MRBPT, of which 18 (4.7%) were positive for I-ELISA. Therefore, by considering the sensitivity and specificity of the I-ELISA test, the final true seroprevalence was calculated as 5.2%. Hence, the true seroprevalence of small ruminant brucellosis in the study area was 5.2%.
The current overall seroprevalence of 5.2% is in agreement with that of 4.0% in Somalia,6 6.4% in eastern Ethiopia,15 and 5.82% in Karnataka in the southern province of India.16 The similarities between these results can be explained by the fairly comparable agroecology and animal management systems. The agroecology of these 3 study areas is arid and semiarid, where there is scarcity of feed and water, and animals are managed in the extensive management system, where they share common grazing and watering points.15-17 The types of diagnostic tests used in all of these studies are MRBT and i-ELISA, which may make the results comparable.15-17 However, the results of the current study are higher than 0.24% in West Hararghe, Ethiopia,18 0.40% in Kajiado County, Kenya,19 and 1.1% in southern Cameroon.20 The high seroprevalence of small ruminant brucellosis in our study compared with the abovementioned results might be due to environmental and animal management differences. Since the annual rainfall in our study area is low (a maximum of 123 mm/year),17 there is a shortage of water and feed in the area because flocks move to search for feed and water, which increases the probability of direct or indirect contact between animals and may increase the risk of brucellosis transmission. In addition, there is no brucellosis vaccination program in our study area.17 These practices of pastoralism and communal grazing, together with a lack of stable access to veterinary and public health services, can make small ruminant brucellosis endemic in the area.21
Compared with males, female sheep and goats were more likely to become seropositive for brucellosis (P < .05). This finding is in agreement with other studies conducted in different areas.20,22,23 The high seroprevalence of brucellosis in females compared with that in males may be related to age; since most males are sold at an early age for meat purposes, young male animals are dominant than adult males. Even if animals become infected by Brucella at an early age, the organism localizes itself in the regional lymph nodes without provoking antibody production until the animal becomes sexually mature and produces sex hormones that stimulate the growth and multiplication of Brucella.24 In addition, it may be linked with the hormone erythritol. Erythritol is a sugar alcohol present in relatively high concentrations in the placenta and fetal fluids of pregnant animals, providing a comfortable environment for the growth and multiplication of Brucella organisms. A higher concentration of erythritol sugar is found in females than in males, increasing the susceptibility of female animals to brucellosis.24
In our study, 23.2% of the interviewees had information about brucellosis. This finding is consistent with 20% in the East Wallaga Zone, Ethiopia,25 but higher than null awareness in selected districts of the southern region.3 However, this figure is lower than the 84% reported in Kenya26 and 56.8% reported in Saudi Arabia.27 The low level of knowledge of owners about brucellosis in our study compared with that in Saudi Arabia and Kenya may be related to differences in educational level and information accessibility among the study participants. For example, the majority (63.6%) of the study participants in Saudi Arabia were bachelor’s degree holders and above,27 and in Kenya, the study was conducted in Kiambu County, which neighbors Nairobi, the capital city of Kenya, which has good infrastructure with accessible medical and veterinary services.26 Among the participants, only 14.6% were aware that brucellosis is a zoonotic disease, and the majority (85.4%) did not know how animals may spread disease to humans. This implies that there may be a shallow and insufficient level of understanding of brucellosis in these regions.
The majority (97.7%) of the participants assisted their ewes and did so during parturition without using personal protective equipment. Similar findings have been reported in the Nugaal region of Somalia28 and the southern region of Ethiopia.3 The reason behind this may be the poor knowledge of the animal owners about the risk of this practice and the lack of access to protective clothing such as gloves. If humans assist animals without the use of personal protective equipment and handle aborted tissue and retained placenta incorrectly, human contamination may increase, and brucellosis may spread farther.29
Approximately 98% of the respondents disposed of aborted fetuses by either feeding them to dogs or depositing them in open landfills. This finding is higher than the 55.5% reported in Egypt.30 Feeding aborted fetuses to dogs may increase the transmission and persistence of infection in the flock since dogs could play a role in the mechanical transmission of the infection when they drag aborted material across the ground.31 Additionally, discarding aborted materials into open landfills and waterways increases the chance of disease transmission to animals and humans.32
The majority of the respondents (89.1%) were consuming raw milk, which is greater than the 79% reported in Kenya26 but lower than the 94.5% reported in districts in southern region3 and the 97.6% reported in Afar region33 of Ethiopia. The findings revealed that the consumption of raw milk, which is a known risk factor for animal-to-human brucellosis transmission, is high in the area. This could be because owners of animals believe that raw goat milk tastes better and has therapeutic benefits, such as aphrodisiac qualities.26
The level of owners’ knowledge, attitudes and practices toward brucellosis were found to be independently associated with the education level of the respondents (P < .001), which is in line with findings reported in Saudi Arabia.27 The findings demonstrated that inadequate education is a significant factor linked to poor understanding of brucellosis and that education has broader implications for health-related awareness and perceptions. This finding is consistent with existing research in health education, which demonstrates that a higher level of education tends to equip individuals with improved access to information and a greater ability to understand and retain health-related knowledge.34,35
The seropositivity of small ruminant brucellosis was significantly lower in owners who had appropriate (good) practices than in their counterparts. This finding is consistent with reports in Mali, Kenya, and Jordan,35-37 but seropositivity was not associated with knowledge or attitudes. These findings indicate that knowledge and attitudes without proper practices are not sufficient to reduce the transmission of brucellosis. Therefore, improving owners’ practices related to aborted fetuses and fetal membrane management, the consumption of pasteurized or boiled milk and cooked meat, the use of personal protective equipment while assisting delivery, and the maintenance of personal and environmental hygiene are crucial for reducing brucellosis in both animals and humans.
Limitations of the study
Although parallel tests are preferable for all samples, which could help to explore the concordance of MRBPT and I-ELISA, owing to financial constraints in the purchase of I-ELISA kits for all samples, only those positive samples with MRBPT were checked using I-ELISA. Despite the fact that a pilot study involving thirty participants was conducted and efforts were made to ensure that participants understood the questions before responding, the honesty and recall ability of individuals were not independently assessed due to a lack of standardized instruments. A thorough understanding of participants’ brucellosis-related knowledge, attitudes, and practices may be hampered by the use of quantitative methods that dichotomize data into binary categories. Importantly, both qualitative and quantitative methodologies should be used in future research.
Conclusions
According to the current serosurvey investigation, small ruminant brucellosis is moderately prevalent in the study area, and sex was significantly associated with brucellosis seropositivity. The knowledge, attitudes and practices of animal owners toward brucellosis were found to be low, and educational level was found to be significantly associated with this low level of owners’ knowledge, attitudes and practices. The seropositivity of sheep and goats was significantly associated with owner practices; hence, poor practices were positively associated with the seropositivity of animals. Therefore, brucellosis is a public health threat in the Garowe district; however, it is important to encourage behavioral changes concerning the handling of animals and discharges during abortion and parturition, and the consumption of pasteurized/boiled milk and cooked meat is equally important. In addition, comprehensive epidemiological investigations employing one health approach are necessary to identify and characterize the circulating species of Brucella in humans and livestock to determine the transmission dynamics of the organism.
Acknowledgements
The authors would like to acknowledge the animal owners who participated in this study and the Garowe Laboratory staff and management for allowing us to conduct all the laboratory activities and providing the necessary reagents and technical support.
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CRediT Authorship Contribution Statement
Mustafe Mohamed Bile: Writing original draft, Conceptualization, Methodology Data curation, Ambachew Motbaynor Wubaye: Writing – review and editing, Writing – original draft, Formal analysis, Methodology, Yihenew Getahun Ambaw: Writing – review and editing, Formal analysis, Data curation, Shihun Shimelis: Writing – review and editing, Conceptualization, and Supervision. Simegnew Adugna Kallu: Conceptualization, Methodology, Formal analysis, Supervision.
Data Availability Statement
All the raw data generated, analyzed, and presented in this article are available from the corresponding author upon reasonable request.
Ethics Statement
This research was approved by Haramaya University, College of Veterinary Medicine Ethics Committee (Ref. No: HU/IEC/21/2017/2022). Each participant who decided to participate in this study provided written informed consent, and the information collected was kept confidential and utilized solely for this research.
