Multidrug-Resistant Staphylococcus aureus Strains Thrive in Dairy and Beef Production, Processing, and Supply Lines in Five Geographical Areas in Ethiopia

Simple Summary Monitoring and surveillance of food-borne pathogens and their antimicrobial resistance (AMR) in the food supply chain are fundamental for reducing food-borne hazards. Staphylococcus aureus is praised globally for readily acquiring AMR and causing foodborne illnesses. Studies are scarce on its reservoirs, hiding places, and routes of entry to the food supply chain in low-income countries. This study aimed to identify ecologies where S. aureus and its AMR strains are abundant in dairy and beef production and processing lines in five geographical areas in central Oromia in Ethiopia to guide whether food (meat and milk) is produced, handled, and moved in a safe and hygienic supply system. We found that S. aureus was prevalent, higher in dairy farms than in abattoirs. Its prevalence varied among 10 ecologies (10 sample sources) but did not vary among 5 locations. All isolates (100%) harbored AMR. The number of ineffective antimicrobial classes against them was high (range = 1–9; median = 5), indicating multidrug resistance (MDR) was prevalent. The abundance of MDR S. aureus varied between 5 locations and 10 ecologies, but the highest was in slaughter lines. Most isolates had different AMR patterns, indicating the isolates were phenotypically unrelated. We also detected some isolates with identical AMR patterns in different ecologies, suggesting their movement between ecologies or their ubiquitous presence in many ecologies. Overall, MDR S. aureus is abundant in a broader geographical area in central Oromia, contaminating milk, meat, equipment, and workers, demanding prompt regulations and operations on personnel safety, hygiene practices, and a comprehensive investigation of control. Abstract Livestock, farms, abattoirs, and food supply systems can become the source of foodborne pathogens, including S. aureus, in the absence of monitoring, general hygienic practices, and control. Studies are scarce on reservoirs (hiding places) and routes of entry of S. aureus into the food supply chain in Ethiopia. To fill these gaps, we evaluated the role of cows (milk), meat, equipment, and food handlers on the abundance and AMR of S. aureus in five geographical areas in central Oromia, Ethiopia. We isolated S. aureus from 10 different ecologies per area in 5 areas and tested their sensitivity to 14 antimicrobials of 9 different classes. We ranked the 5 areas and 10 ecologies by computing their multiple AMR index (MARI) at a cut-off value of 0.2 to determine ‘high-risk’ ecologies for AMR. We recorded as MDR if an isolate had resistance to ≥3 antimicrobial classes. We used a circos diagram to analyze if isolates with identical AMR patterns were shared between different ecologies. S. aureus is prevalent in central Oromia (16.1–18.3%), higher in dairy farms than in abattoirs, and varied among 10 ecologies (p < 0.001) but not among 5 areas (p > 0.05). Of the 92 isolates, 94.6% were penicillin-resistant. Their AMR prevalence was above 40% for 9 of 14 antimicrobials. All isolates (100%) had AMR in at least one antimicrobial class (range = 1–9; median = 5), indicating MDR was prevalent. The prevalence of MDR S. aureus varied (p < 0.05) among areas and 10 ecologies; the highest was in slaughter lines. All isolates had a MARI of >0.2, indicating drug overuse, and S. aureus’s AMR burden is high in central Oromia. Dairy farms had higher MARI values (0.44) than abattoirs (0.39). Of 10 ecologies, the highest and lowest MARI values were in the beef supply chain, i.e., slaughter line (0.67) and butcher’s hand (0.25). Of the 68 different AMR patterns by 92 isolates against 14 antimicrobials, 53 patterns (77.9%) were unique to individual isolates, indicating they were phenotypically dissimilar. MDR S. aureus was widespread in central Oromia in dairy and meat supply chains, contaminating milk, meat, equipment, and workers in farm and abattoir settings. In the absence of strict regulations and interventions, MDR S. aureus can be disseminated from these epicenters to the public.