In pastoral environments characterized by close human-animal interactions, Staphylococcus aureus has emerged as a zoonotic concern of public health importance due to the prevalence of multidrug-resistant microorganisms. It has long been recognized as a significant concern in terms of public health (1). This bacterium, which exhibits a positive Gram stain, displays a vast geographic dispersion, as evidenced by investigations conducted in diverse regions across the globe (1, 2). The frequency of food products contaminated with S. aureus varies, with cereals having the highest frequency and meat and bean products having the lowest. The hospital and community settings have been the sites of methicillin-resistant S. aureus (MRSA) strains, with several dominant clones reported in various countries (3, 4). Antibiotic-resistant genotypes and host epidemiology have combined to cause the spread of community-associated MRSA lineages, changing the transmission dynamics and resulting in sustained transmission in regional population centers (1, 5).

In addition to causing zoonotic diseases, it can lead to mastitis, bacteremia, and food-borne poisoning in humans (1, 6). Staphylococcal enterotoxins are a prominent source of food-borne outbreaks that are frequently linked to S. aureus (5, 7). Since S. aureus frequently co-occurs with humans, care must be taken to lower the possibility of contamination when preparing food. The presence of biofilm-related medical equipment infections is also a significant issue. Currently, methicillin-resistant S. aureus infections have become endemic worldwide (1, 2, 7).

Research has indicated a significant frequency of S. aureus colonization among employees in various work environments, such as bakeries, pig farms, fire departments, and healthcare facilities (4). Investigations into the presence of S. aureus in cows, their handlers, and their immediate environment have also revealed a diversity of clonal lineages and suggested a potential route of transmission between handlers and cows (4, 8). As it has been pointed out in the different studies, there is a potential occupational contact with swine, such as that experienced by hog slaughterhouse workers, influences nasal S. aureus colonization (9, 10). Among the antibiotic resistance genes, variations in lineage distribution and virulence factors of S. aureus have been studied in pig workers compared to non-workers. Due to their close contact with livestock treated with antibiotics, pig workers are at higher risk of carrying antibiotic-resistant S. aureus (11). Methicillin-susceptible S. aureus (MSSA) strains with variable virulence factors and antibiotic-resistance genes have been detected in swine populations (11, 12). Furthermore, research on the epidemiology and genetic relatedness of the mecA gene in S. aureus strains isolated from pets, contact persons with pets, and veterinary clinical environments has revealed the increasing prevalence of methicillin-resistant S. aureus (MRSA) strains at animal-human-environment interfaces (5).

Staphylococcal Cassette Chromosome mec (SCCmec) is indeed a critical genetic element responsible for the multidrug resistance in S. aureus strains, particularly methicillin-resistant S. aureus (MRSA). SCCmec is a mobile genetic element that carries the mecA gene, which encodes penicillin-binding protein 2a (PBP2a). PBP2a has a low affinity for β-lactam antibiotics, including methicillin and other β-lactam antibiotics, rendering the bacteria resistant to these drugs (13). Methicillin-resistant S. aureus is connected to hospitals, and the population is most commonly associated with type IV SCCmec elements, which are categorized into 15 categories (14). The whole-genome sequence of the SCCmec IVd (2B) subtype, one of several subtypes of SCCmec type IV strains, is still missing (13). Additionally, S. aureus has multiple transmissible genes, including plasmids and transposons. These genes spread antibiotic resistance genes between S. aureus strains that confer resistance to various antibiotics through mechanisms like enzymatic inactivation, altered target sites, and reduced intracellular drug accumulation (15). Little is known about the processes that facilitate the acquisition of foreign genes and the dynamics of their transfer between hosts (16).

Workers may be susceptible to colonization by S. aureus in a variety of work contexts. There is a high incidence of S. aureus colonization among healthcare workers (HCWs) in several nations, including Indonesia (17), Portugal (18), Ecuador (19), and Nigeria (20). Healthcare professionals who have previously worked in a hospital with a positive MRSA colonization history are at risk for S. aureus colonization (21), and other risk factors include not practicing hand hygiene, being male, being older, not washing your hands well, having a wound or skin infection, and recently using antibiotics (22–24).

Because S. aureus has a high incidence of antimicrobial resistance, it presents substantial clinical danger in Africa. Methicillin-resistant S. aureus (MRSA) is a contributing factor to hospital-associated and community-associated infections in Africa. Africa has yielded several clonal complexes (CCs), demonstrating the diversity of the clonal spread of MRSA across the continent. The three most frequently used MRSA strains are the ST5-IV [2B], ST8-IV [2B], and ST88-IV [2B] clones (3). Many CCs have MRSA that is Panton-Valentine leukocidin (PVL)-positive meticillin-resistant S. aureus and the frequency of PVL-positive MRSA varies from 0 to 77% in Africa (25). Inducible clindamycin resistance in S. aureus isolates varies from 2.9 to 44% in Africa; MRSA strains have a greater incidence of this resistance (26). Regarding the significance of antibiotic resistance in S. aureus, routine screening, prudent clindamycin usage, and molecular identification of resistance genes are advised (24, 27, 28). Kenyan community-associated MRSA (CA-MRSA) strains have been characterized by whole-genome sequencing, which has led to the discovery of rare sequence types (STs), such as ST7460 and ST7635 (28). Different spa types and clonal complexes have been identified by combining DNA microarray and spa typing to characterize S. aureus isolates from South Africa and Nigeria (3, 25, 29, 30).

Studies show that S. aureus is prevalent in a variety of contexts and is a major concern in Ethiopia. The country has a 23% overall pooled apparent prevalence of S. aureus in milk and meat samples according to a comprehensive study and meta-analysis (31). Another study that examined lines of cattle abattoirs revealed that 35.5% of the isolates were Staphylococcus, and 13.6% of those isolates were S. aureus (32). S. aureus is the most often isolated bacterium in burn wound infections, with an overall incidence of 57.8% (33). Methicillin-resistant S. aureus (MRSA) and other various strains were identified by molecular analysis of S. aureus isolates, underscoring the possibility of pandemic strains in the nation (34). Additionally, samples of cottage cheese and yoghourt included Staphylococcus species, with an overall prevalence of 14.3% and a specific prevalence of 22 and 6.5% in the former and yoghourt, respectively (35). Numerous researchers have examined the status of bacteria and the risk factors that are connected to the interface between personnel, animals, and working equipment, with a focus on Ethiopia (36–38). These results highlight the need for better sanitation habits, antibiotic stewardship, and public education to lower the prevalence of drug-resistant S. aureus infections in Ethiopia.

Thus, to support successful preventative and control initiatives, it is imperative to understand the general occurrence, multidrug resistance rate, and potential risk factors for S. aureus at the workers-animal-working utensils interface at the national level. Accordingly, this meta-analysis aimed to gather the available data and estimate the pooled prevalence of S. aureus and its antimicrobial resistance at the workers-animal-working interface in Ethiopia.

The PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analysis) checklist (39) was used to conduct this review.

Staphylococcus species are prevalent foodborne bacterial pathogens that cause food poisoning in humans when ingested in contaminated foods, including dairy products. The organisms can gain access to raw milk and milk products either by direct excretion from udders with clinical and subclinical staphylococcal mastitis or by contamination from food handlers. The primary aim of interest in this meta-analysis was to estimate the pooled prevalence of S. aureus in livestock, livestock-associated workers, and working equipment interfaces in Ethiopia. Our meta-analysis revealed that there was a 22% pooled prevalence of S. aureus in the worker-animal and equipment interfaces. The significant increase in the incidence of this pathogen is alarming both for dairy farms and for public health.

The sub-analysis revealed that the pooled prevalence of S. aureus at the animal-worker-equipment interface was greater in dairy farm sources, which accounted for 23%, than in abattoir settings, which accounted for 18%. This result contradicted the findings reported by Abunna et al. (55), who reported a greater proportion of S. aureus (53.2%) in a slaughterhouse where the percentage of S. aureus was slightly greater than that in a dairy farm (44.8%). Another contradictory result was found in the study by Gizaw et al. (56), in which the occurrence of S. aureus was significantly greater in meat samples (22.7%) and considerably lower in dairy farms (11.7%) in Ethiopia. According to Tibebu et al. (23), the overall prevalence of S. aureus was estimated to be 21.46%. Of these, 25.53% were derived from cow milk, 10% from udder swabs, and 19.23% from hand swabs. On the other hand, Marami et al. (40) reported that 74% of udder milk samples, 72% of udder swabs, and 83% of milker hand swabs were positive for S. aureus.

The potential causes for this variation may stem from the inadequate management practices employed by dairy farms and their workers, as well as the insufficient attention given to dairy farms in Ethiopia. These discrepancies could arise from the use of various research methods employed in different studies conducted by multiple researchers. Another possible factor could be attributed to the characteristics of the samples, such as the presence of meat or milk, which may or may not favor the growth and proliferation of S. aureus. Moreover, the protocols for processing samples in terms of abattoir settings and dairy farms could introduce significant variations in the proportion of the pathogen in different sampling units. Like other contradictory studies in Ethiopia, the present study depicted a contrary notion in Turkey, as it was reported that meat product samples (48.7%) had a significantly greater prevalence than milk and dairy products (23.2%), implying a widespread distribution of S. aureus among diversified food items (57). A converse result might be that the Turkish dairy management system receives great attention throughout the milk and milk product processing chain and provides better treatment options for the pathogen. Moreover, this difference could be attributed to the diverse isolation and identification methods of the agent across different geographical areas as well as to global climatic changes.

The present discovery also indicated that the occurrence of S. aureus was greater in human workers (25%) than in animals (23%). The pooled prevalence of S. aureus in animals was significantly greater (23%) than that in the study conducted by Marami (40), which revealed that the prevalence of the pathogen in animals was 13.9%. Furthermore, the occurrence of S. aureus in animal workers was also found to be greater (25%) than that in Mekuria’s study (42), which reported a 15.5% prevalence of S. aureus in milk samples from dairy cows and nasal swabs of farm workers in selected dairy farms around Addis Ababa, Ethiopia. Similarly, our study demonstrated a higher result than the finding documented by Lewis and James (58), where the proportion of S. aureus accounted for 17.2% of the cattle, food chain, and human infections in Bishoftu, Ethiopia. However, this meta-analysis result was lower than that of Bendahou et al. (59, 60), who reported that 40% of S. aureus isolates were found in dairy products in North Morocco. The lower prevalence of S. aureus in the current study compared to the study in northern Morocco could be attributed to the direct collection of milk samples from cows’ udders before contact with milking utensils in this study, which may have reduced the prevalence of S. aureus (40).

Risk factors, Tibebu et al. (23) study on S. aureus in milk linked the bacteria to various possible factors, including milker age, community awareness of S. aureus, antiseptic use before and after milking, barn drainage systems, management systems, prior exposure to mastitis, and the use of drying towels for each udder separately. Only prior mastitis exposure (p < 0.05) from these linked factors to the agent had a statistically significant association with the prevalence of S. aureus. In Addition, Marami et al. (40) reported that Staphylococcus species isolates from dairy cows and smallholders were common in Central Ethiopia. The authors attempted to correlate the disease’s prevalence with several variables, including site town, breed, farm type, cow age, parity, lactation stage, blind test, eating lesion, tick infestation, floor type, and towel usage. Overall, the results of the univariate logistic regression analysis indicated that there was no significant correlation between any of the research variables in cows and the isolation of Staphylococcus. Additional research has evaluated the prevalence of this organism in relation to potential risk variables, such as sex, age, farm duty, job experience of the attendees/owners, and parity and lactation status of the cow (41). Carriage of staphylococci in the nasal passages and hands of the milkers are also potential sources of staphylococci in milk.

The prevalence and extent of antimicrobial resistance in veterinary medicine are experiencing a in the global. The spread of staphylococci that are resistant to antimicrobial agents poses a challenge to both human and animal health professionals. It is crucial to monitor and surveil foodborne pathogens and their resistance to antimicrobials in the food supply chain to effectively reduce the risks associated with food-borne hazards. In the present meta-analysis, the collective prevalence of multidrug-resistant strains was 27% in various sampling units on dairy farms and abattoirs. Our findings revealed a significantly lower prevalence than that reported in previous studies conducted in Egypt, with rates of 100, 74, and 80% reported by Seedy et al. (61), Gizaw et al. (56), and Balta et al. (62), respectively. In Korea, Moon et al. (63) reported a prevalence rate of 79%, while Beyene et al.(48)reported a rate of 34.9% in Ethiopia. However, our findings indicated a greater prevalence than that reported in other studies conducted in Ethiopia, such as the 10.42% reported by Tibebu et al. (23) and 16% by Buna et al. (36). This is a result of repeated therapeutic or indiscriminate use of these antibiotics on dairy farms and in humans for the treatment of infections.

The high prevalence of multidrug resistance of S. aureus can be attributed to the frequent use of antimicrobials, particularly microorganisms that produce β-lactamase, which inactivates penicillin and related antibiotics. The use of disinfectants containing heavy metals in washing milking equipment could potentially induce antimicrobial resistance in bacteria. It is possible to increase antimicrobial resistance via various ecological settings, by administering subtherapeutic doses, subdose antibiotics in animal feed and water, administering them at the wrong time, and administering them using the wrong route (which impacts bioavailability) (64).

The introduction and propagation of low-grade medications within a nation can also present significant obstacles (65). Additionally, the presence of antimicrobial residues in milk can contribute to the development of antimicrobial resistance in pathogens, which can then be transmitted to different individuals upon consumption (66). The abundance of multidrug-resistant Staphylococcus sp. have been found in milk from farms, meat from abattoirs, equipment, and humans poses a risk to public health.

To effectively control these pathogens at the national level in Ethiopia, veterinary professionals should provide health-related training to para-professionals, such as livestock keepers, attendants, milkers, hygiene workers, and milk collectors. To achieve optimal health outcomes for humans, animals, and the environment, national action plans should prioritize efforts to reduce antimicrobial resistance from livestock to the environment and the community.

The present meta-analysis revealed that the pooled prevalence of S. aureus at the animal-worker-working equipment interface was 22% in Ethiopia. Overall, 25, 23, and 19% of the pathogens were distributed in humans, animals, and working facilities/utensils, respectively. The current meta-analysis also revealed an overall MDR rate of 27% in different sampling units. And, the highest frequency of MRSA isolates was recorded found in the Dairy farm settings (44%). The sub-pooled results also revealed substandard practices for milk, meat, personnel, and equipment hygiene in dairy farms and abattoirs when handling, storing, and processing foods originating from livestock. The contamination rates of food of animal origin (milk and meat), personnel, and working equipment by S. aureus are approximately equal, indicating that this particular pathogen is present and circulating at the interface where humans, animals, and working utensils interact. Additionally, it can serve as a useful marker for inadequate hygiene practices and compromised animal food safety. In particular, the frequent cleaning of abattoir workers’ and milkers’ hands could be a contributing factor to the relatively low prevalence of S. aureus in abattoirs. The higher pooled prevalence of S. aureus in dairy farms, abattoir settings, and workers in this meta-analysis indicates its serious economic, animal welfare, food safety and public health problems and its association with livestock for its transmission between animals and humans in livestock farm settings. Thus, improving hygienic measures on dairy farms and working equipment as well as within abattoirs must be effective in safeguarding the public from the risk of staphylococcal food poisoning and acquiring MDR isolates. Additionally, future research should consider identifying Staphylococcus enterotoxins from milk and meat and genes responsible for AMR in Ethiopia.