INTRODUCTION
Brucellosis is a zoonotic disease that causes significant losses in livestock productivity as well as negative impacts on public health worldwide.1 The disease is caused by various species of the genus Brucella spp.2 with B. melitensis, B. abortus, and B. suis considered the most important species in terms of human health.3 Globally, approximately half a million new cases of human brucellosis are recorded each year.4 Humans acquire infection through consumption of unpasteurized dairy products and uncooked meat or through direct contact with infected animals, placentas, or aborted fetuses.5
Clinically, human brucellosis is characterized by fever, fatigue, sweating, joint pain, headache, loss of appetite, muscular pain, lumbar pain, weight loss, and arthritis.5,6 The disease is insidious and can be severely debilitating, with acute febrile episodes frequently misdiagnosed as malaria.1 Treatment of brucellosis involves prolonged therapy with two or more antimicrobial drugs and delay in treatment can lead to long-term complications. Consequently, brucellosis imposes a significant economic burden on society through loss of workdays due to malaise and hospitalization of infected persons, as well as loss of income and healthcare costs.7 Dairy farmers, pastoralists, abattoir workers, animal health personnel, laboratory personnel, and other people involved in the livestock value chain are considered the highest occupational risk groups.8 Adequate knowledge of brucellosis is of significant importance among high-risk groups because knowledge empowers people to take protective measures at work and actively participate in disease control programs, thus greatly assisting in brucellosis control strategies.9
Limited studies have been conducted on brucellosis in humans in Eritrea to date. Early this century (2002), Omer et al. investigated the disease in a small number of occupational-exposed groups including dairy farmers (n = 130), veterinary personnel (n = 21), and pastoralists (n = 105) with reported seropositivity of 7.1%, 4.6%, and 3.0% in each group, respectively.10 More recently, in 2022, Efrem et al. reported 2.4% seroprevalence in livestock owners in Northern Red Sea region (n = 637).11 Fragmented clinical reports, laboratory diagnostic results, and serological tests in livestock owners also indicate the presence of brucellosis in humans in different areas of the county.12,13 However, there is lack of data on the level of knowledge and practices in different farming systems, including in the dairy-cattle-rearing community.
The objective of this study was therefore to determine the seroprevalence of brucellosis and the level of knowledge and risky practices in dairy cattle workers in Maekel and Debub regions, Eritrea. These regions constitute the most densely populated regions in terms of human and dairy cattle populations in Eritrea.
MATERIALS AND METHODS
Study design and area.
This cross-sectional, community-based study was conducted in dairy cattle owners and workers in Maekel and Debub regions of Eritrea between August 2021 and February 2022. Eritrea is located in the Horn of Africa, between latitudes 12°42′N and 18°2′N and longitudes 36°30′E to 43°20′E. The country is divided into six administrative regions: Anseba, Debub, Gash-Barka, Maekel, Southern Red Sea, and Northern Red Sea. Debub region is located in the southern part of the country. It is divided into 12 subregions, 217 administrative areas, and 886 villages. It comprises the second highest population of all regions. Maekel region is in the central part of the country and divided into four subregions, 59 administrative areas, and 89 villages. It is the smallest in size but has the third largest population of all regions in Eritrea.14,15
Sampling design and sample size.
Dairy cattle owners and workers from dairy farms managed under intensive and semi-intensive production systems in Maekel and Debub regions were the target of this study. The study was conducted simultaneously with another study that focused on prevalence of brucellosis and risk factors in dairy cattle on the same farms.16 The criteria for selecting the farms is described in detail in that article. Briefly, lists of dairy farms were obtained from the respective regional Ministry of Agriculture Veterinary Offices. From these, farms with more than four animals in the study areas were selected to participate, proportional to the number of farms in each region (i.e., 87 farms in Maekel; 127 farms in Debub). The mean and median herd size of the sampled farms was 15.1 and nine head of cattle, respectively (minimum five, maximum 158).
Between one and four dairy cattle owners/workers from each farm volunteered for blood and data collection, for a total of 416 human participants from 214 farms. With this sample size, using EpiTools (https://epitools.ausvet.com.au/prevalencess), we calculated that we could estimate the true seroprevalence in humans with approximately 5% precision and 95% confidence. This assumed a worst-case scenario of 30% prevalence (based on 28.4% seropositivity in clinically suspected cases17), and combined sensitivity and specificity for Rose Bengal plate test (RBPT) and competitive ELISA (c-ELISA) of 83% and 100%, respectively (based on data reported by Godfroid et al.18 and combined using the formula by Thrusfield19). We elected to use a high (30%) expected prevalence for these calculations because previous estimates were 20 years old,10 and it was assumed that prevalence would have increased in the absence of disease control efforts.
Data and sample collection.
A questionnaire was designed to assess knowledge and risky practices related to brucellosis acquisition in humans (see supplemental material). Participants were asked if they had heard about brucellosis before, as well as sources of information, routes of transmission from animals to humans, clinical signs in infected animals and humans, and availability of treatment or vaccine. Participants were also asked if they consume milk and milk products, eat raw meat, and assist animals during parturition without protective equipment. The contents of the questionnaire were prepared using simple and easily understandable close-ended questions. The questionnaire was translated into the local language (Tigrinya) and pretested in 10 households before commencement of data collection, with adjustments made to improve clarity.
The authorities in the respective study region gave permission for the research to be conducted in the study areas. During the informed consent process, participants were advised that they could withdraw at any stage of the research and that all the information provided including any identifiable information would be kept confidential. Seven to ten ml of blood was collected from each participant from the median cubital vein using a plain vacutainer tube and double ended needle. Each blood sample was labeled using a unique code to maintain confidentiality. The sample tubes were set tilted on a table for about 12–18 hours at a room temperature and protected from direct sunlight to allow separation of the serum. Subsequently, separated serum was decanted into another tube pre-labeled with the same unique code. Serum samples were then transported in an ice box to the National Animal and Plant Health Laboratory (NAPHL), Ministry of Agriculture, Asmara for laboratory analysis.
Laboratory investigation.
Sera was screened for brucellosis antibody using the RBPT according to the kit manufacturer’s instructions (product code RAA0060; Animal Health and Veterinary Laboratory Agency, Surry, United Kingdom). Negative and positive controls for B. abortus and B. melitensis were included at the beginning of each testing session. All RBPT positive samples were subjected to confirmation using c-ELISA following procedures described by the kit manufacturer (INgezim Brucella Compac 2.0; Ingenasa, Madrid, Spain). Optical density (OD) of each well was read at 450-nm using a plate-reader machine. The result was deemed acceptable if the OD in negative controls wells (NC) was >1 and OD in positive controls wells (PC) was <0.35. The percentage of inhibition (PI) for each sample was calculated as follows: PI = 100 × [1 – (OD sample/OD negative control)]. Samples with PI ≥40% were considered positive for Brucella antibody, and samples were deemed negative if PI <40%.
STATISTICAL ANALYSES
Questionnaire data and laboratory results were coded and entered into Microsoft Excel and imported into SPSS version 23 for analysis. Estimated true prevalence using imperfect tests was calculated in Epitools (https://epitools.ausvet.com.au/trueprevalence) using the same parameters above. Sociodemographic background, knowledge, and self-reported practices were summarized using descriptive statistics (frequency and percentages). Knowledge score was calculated by allocating marks to each question. Participants who had never heard of brucellosis were given a score of zero. Participants who had heard of brucellosis were asked to answer an additional 12 questions consisting of a total of 20 marks. The normality distribution of knowledge score data was checked graphically with a histogram and using Kolmogorov–Smirnov tests. Because the data were not normally distributed, nonparametric tests (Mann–Whitney U test and Kruskal–Wallis tests) were used to explore differences in median knowledge score by demographic characteristics and engagement in risky practices. Associations between seropositivity and knowledge score and between seropositivity and risky practices were also examined using Mann–Whitney and chi-square tests, respectively. All associations were found to be nonsignificant, likely because of the low number of seropositives detected in the study (n = 5) (see Supplemental Materials).
RESULTS
Participant characteristics and seroprevalence.
Table 1 shows the characteristics of participants, by brucellosis serostatus. Of 416 participants, 8 (1.9%) were seropositive for brucellosis by RBPT, of whom five were confirmed by c-ELISA. Thus, the apparent and true individual-level prevalence was 1.2% (95% CI: 0.05–2.8%) and 1.4% (95% CI: 0.6–3.4%), respectively. All individuals came from different farms; apparent farm-level prevalence was five of 214 (2.3%). Of 416 participants tested across both regions, two of 175 (1.1%) from Maekel were seropositive and three of 241 (1.2%) from Debub were seropositive.
Demographic characteristics and brucellosis serostatus of dairy farm owners and workers in Maekal and Debub regions, Eritrea (N = 416)
| Variable | Total Samples, n (%) | c-ELISA Positive, n (%) |
|---|---|---|
| Region | ||
| Maekel | 175 (42.1) | 2 (1.1) |
| Debub | 241 (57.9) | 3 (1.2) |
| Age in years | ||
| 18–30 | 147 (35.3) | 3 (2.0) |
| 31–50 | 154 (37) | 2 (1.3) |
| >50 | 115 (27.6) | 0 (0.0) |
| Gender | ||
| Male | 310 (74.5) | 4 (1.3) |
| Female | 106 (25.5) | 1 (0.9) |
| Educational level | ||
| Illiterate (0) | 40 (9.6) | 0 (0.0) |
| Primary (1–5) | 89 (21.4) | 1 (1.1) |
| Junior and secondary (6–12) | 250 (60.1) | 3 (1.2) |
| Higher education (>12) | 37 (8.9) | 1 (2.7) |
| Relation of respondent to household | ||
| Family member | 268 (64.4) | 2 (0.7) |
| Farm worker | 148 (35.6) | 3 (2.0) |
| Years working in dairy farming | ||
| ≤10 | 231 (55.8) | 5 (2.2) |
| 11–30 | 164 (39.6) | 0 (0.0) |
| >30 | 19 (4.6) | 0 (0.0) |
| No. of household members | ||
| 1–5 | 154 (37.0) | 2 (1.3) |
| 6–10 | 196 (47.1) | 2 (1.0) |
| 11–20 | 66 (15.9) | 1 (1.5) |
| Total | 416 | 5 (1.2) |
Brucellosis knowledge of participants.
Brucellosis knowledge of participants is summarized in the supplemental material. Nearly half of the participants (206/416; 49.5%) had never heard of brucellosis before. Of 210 participants (50.5%) who had heard of brucellosis, respondents stated that they had heard of brucellosis from television (123/210; 59%), friends/relatives (65/210; 31%), and radio (34/210; 16%); through community awareness-raising programs (20/210; 9.5%); and/or from newspapers (2/210; 1%). The great majority (196/210; 94%) of these participants knew that animals can be infected with brucellosis. Animal species that were identified as being infected with brucellosis were cattle (192/210; 91%), sheep/goats (142/210; 67%), and camels (47/210; 22%). Respondents correctly identified several clinical signs of brucellosis in animals including abortion (113/210; 54%), repeat breeding (25/210; 12%), loss of milk production (21/210; 10%), infertility (10/210; 5%), retained placenta (10/210; 5%), and epididymitis (4/210; 2%). However, 41% (86/210) of participants did not know any clinical sign of brucellosis in animals. Nearly 85% (178/210) of respondents indicated that brucellosis can be transmitted from animals to humans by eating raw meat or drinking raw milk. More than half (110/210; 52%) answered that brucellosis can be transmitted to humans through direct contact with contaminated fluids and tissues from animals with brucellosis. Brucellosis symptoms and clinical signs in humans were recognized by some participants and included joint and back pain (74/210; 35%), fever (46/210; 22%), weakness (36/210; 17%), and headache (20/210; 10%). However, 49% (103/210) did not know any symptoms of brucellosis in humans. Most (181/210; 86%) respondents answered that brucellosis can be medically treated in humans, and 70% (146/210) knew that a vaccine against brucellosis in animals is available.
Self-reported practices.
Self-reported practices of participants are summarized in the supplemental material. Of 416 participants, 96% (n = 400) reported that they consume boiled/pasteurized milk. Most of them (290/416; 70%) explained that yoghurt is commonly made from raw milk and is further processed to butter and buttermilk for home consumption and sale. Participants indicated that cheese was not processed at home; if any exists, it was produced in dairy processing plants. Only a small proportion (31/416; 7.5%) had the habit of eating raw meat, and it was stated to happen only rarely on holidays. The majority (311/416; 75%) of respondents stated that they assisted animals during parturition, and most (189/311; 61%) stated that they did not wear protective gear.
Comparison of knowledge score by demographic characteristics and engagement in risky practices.
Overall brucellosis knowledge score of participants was low (mean score of 6.53/20; median of 1, interquartile range [IQR]: 0–12.5). Significant differences existed in median knowledge score by demographic characteristics (Table 2). Knowledge score was higher in participants from Maekel region (P <0.001), older participants (P = 0.035), those with higher educational attainment (P = 0.001), and those with more years of experience working in dairy farming (P = 0.001). In contrast, knowledge score was lower in farm workers (versus family members; P = 0.016). No significant differences in knowledge score existed between participants who engaged in potential risky practices including drinking yoghurt produced from raw milk (P = 0.874), eating raw meat (P = 0.197), and assisting calving animals without wearing protective gloves (P = 0.100), compared with those who did not engage in such practices (not shown).
Median brucellosis knowledge score of dairy workers in Maekal and Debub regions, Eritrea, by demographic characteristics (N = 416)
| Variable | Median Value of Knowledge Score | P-Value |
|---|---|---|
| Region | ||
| Maekel | 11 | <0.001 |
| Debub | 0 | |
| Age | ||
| 18–30 | 0 | 0.035 |
| 31–50 | 3.5 | |
| >50 | 10 | |
| Gender | ||
| Male | 0 | 0.767 |
| Female | 5.5 | |
| Educational level | ||
| Illiterate (0) | 0 | 0.001 |
| Primary (1–5) | 0 | |
| Junior and secondary (6–2) | 2.5 | |
| Higher education (>12) | 11 | |
| Relation of respondent to household | ||
| Family member | 7.5 | 0.016 |
| Farm worker | 0 | |
| Years in working in dairy farming | ||
| ≤10 | 0 | 0.001 |
| 11–30 | 9 | |
| >30 | 10 | |
| No. of household members | ||
| 1–5 | 0 | 0.922 |
| 6–10 | 5 | |
| 11–20 | 0 |
P-values comparing knowledge score between categories were derived using Mann–Whitney U test for two samples and Kruskal–Wallis test for three or more samples.
DISCUSSION
This study is one of few to assess the seroprevalence of brucellosis and associated knowledge and practices related to brucellosis in dairy farmers and workers in Eritrea. The overall apparent seroprevalence of brucellosis in dairy farmers in this study (1.2%) was lower than reported 20 years previously in a study of dairy farm workers around the capital city, Asmara (7%).10 It was also slightly lower than reported more recently in livestock owners in Northern Red Sea region (2.4%).11 Interestingly, the current study in humans was simultaneously carried out with a seroprevalence survey of dairy cattle on the same farms where the prevalence was found to be low; 1.2% and 1.1% in cattle in Maekal and Debub regions, respectively.16 Simultaneous sampling of humans and animals is uncommon in brucellosis research and is a strength of this study. The findings agree with the common understanding that the epidemiology of brucellosis among humans largely reflects the epidemiology in animals.20
Nearly half of the dairy cattle farmers in the present study had never heard of brucellosis before. Comparable observations have been reported in South Africa where more than 40% of farmers had not heard about brucellosis.21 In contrast, in neighboring Ethiopia, more than 90% of dairy farm workers had never heard about brucellosis.22 Similar findings have been reported in India and Tajikistan.23,24 Shortage of health facilities, inadequate veterinary services, shortage of personal protective gear, lack of training on the rearing and handling of animals and lack of health education programs have previously been reported as the major contributors to the low level of awareness/knowledge among dairy farmers.25
Of the farmers who had heard about brucellosis, most answered that they acquired the information through mass media (television and radio). Most likely this high proportion was linked with the brucellosis-related information broadcasted on weekly basis for several months in the years 2020–2021 (Eri-TV-programs 2020/21). Nowadays, Eri-TV and radio are the most accessible and commonly consumed mass media by almost all ages and sexes in the country. Hence, it is important that the concerned authorities and experts continue to use the mass media to convey and educate the community about this disease. In particular, most farmers in this study had poor knowledge of clinical signs of brucellosis in animals and humans. This is an important finding and suggests that farmers may not recognize brucellosis when it occurs in their herd, nor may they attribute signs they experience to the disease. This knowledge gap could be targeted in future mass media campaigns.
Drinking raw milk is an important risk factor for acquiring brucellosis infection in humans. Presence and viability of Brucella species in dairy products is influenced by various intrinsic and extrinsic factors such as temperature, moisture content, pH, storage condition, age, and type of dairy product.26 It is generally recommended that all milk for human consumption should be boiled or pasteurized at high temperatures to kill Brucella spp. If pasteurization facilities are not available, the milk should be heated to a minimum temperature of 80 to 85°C and held at that level for at least 30 minutes.1 In this study, most participants stated that they drink only boiled or pasteurized milk. This is a good preventive measure and likely contributes to the low observed seroprevalence in the study areas. This contrasts with a study of livestock owners in the Northern Red Sea region of Eritrea, where most respondents (77.8%) reported that they never boiled milk before drinking or selling.11 These regional differences may be important for designing appropriately targeted messaging campaigns. Notably, participants in the current study did report that yoghurt was commonly made from raw milk, and it was further processed to butter and buttermilk for home consumption and sale. This is a risky practice and custom, highlighting the need to target people engaged in downstream milk processing in education campaigns in addition to primary producers.
Most participants in this study assisted their animals during parturition and did not wear protective gear while doing so. This finding is consistent with a previous study conducted in Eritrea11 and is similar to another in Egypt.27 The results are, however, in contrast to a study conducted in Jordan,26 where nearly half of the respondents indicated that they wore gloves for protection. In Eritrea, this risky practice could be partly explained by the fact that participants cannot easily find such protective equipment in their vicinity. This constraint should be recognized by concerned extension workers who are advised to explore and find solutions.
Higher knowledge scores were observed for participants from Maekel region than Debub, probably because of the relatively longer history of dairy farming in Maekel region, where more studies have been conducted. Hence dairy owners and other stakeholders involved in the dairy chain and residing in Maekel region could have been exposed to better information about brucellosis. Three demographic factors (increasing age, educational level, and number of years in dairy cattle work) showed a significant positive association with higher knowledge score. This likely reflects cumulative exposure to information and associated learning through various sources.
There are some limitations of this study. First, the study excluded farms owning fewer than five animals. Therefore, the findings cannot be generalized to small farms. Our aim was to measure seroprevalence, and as such we applied serological tests at a single point in time. We cannot comment on whether any of the seropositive participants had active brucellosis infection or whether participants who were seronegative had been exposed in the past. The small number of seropositives also prohibited detailed analysis of risk factors using multivariable analysis. Further, the kits that were used for serological screening and confirmation in humans in this study were developed for use in animals. We did not undertake a full evaluation of these tests; however, basic validation was performed using control sera before application of the tests to human samples in this study. We also used the same cutoff value as established in other studies that used a c-ELISA kit developed and validated for livestock as a confirmatory test in humans.28,29 Finally, potential biases could also have arisen if the questions were misinterpreted by the farmers. Every effort was taken to prevent this by pretesting the questionnaire.
CONCLUSION
In conclusion, the prevalence of brucellosis in dairy cattle owners and workers in Maekel and Debub regions of Eritrea was low. Participants had low levels of knowledge on brucellosis and engaged in practices that posed potential risks related to the disease. Dairy cattle owners and workers, and the communities in the study areas in general, need to be educated on brucellosis and related risky practices and preventive methods. Concerned authorities and extension workers should make every effort to expand access of dairy owners and workers to protective equipment including gloves.
Supplemental Materials
ACKNOWLEDGMENTS
We acknowledge the Ministry of Agriculture, State of Eritrea, for supplying the data collection materials and the laboratory facilities for analysis. We also appreciate the support of the Ministry of Agriculture, Animal Production and Veterinary Offices in Maekel and Debub regions for their permission and assistance during data collection.
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