Prevalence and molecular characteristics of Staphylococcus aureus in raw milk and milk products in Ethiopia: a systematic review and meta-analysis

Abstract

Abstract Background Staphylococcus aureus is an important opportunistic pathogen of raw milk and milk products, and the enterotoxins cause food poisoning. Milk and milk products are important reservoirs of enterotoxin-producing S. aureus. The aims of this systematic review were to estimate the pooled prevalence of S. aureus, including methicillin-resistant Staphylococcus aureus (MRSA), and to summarize their molecular characteristics, assess the potential sources of S. aureus contamination in bulk milk and analyse the antimicrobial resistance patterns of the isolates. Methods Following Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, we searched publicly available scientific online databases and search engines: PubMed, Research for Life, African Journal Online (AJOL), and Google Scholar. In addition, the reference lists of the identified studies were manually checked for relevant literature. A random effects model using the DerSimonian method was used to compute pooled prevalence estimates, and the data were transformed using variance stabilizing Freeman-Tukey double arcsine transformation. Results A total of 38 studies were included in this systematic review. The pooled prevalence of S. aureus was highest in raw cow milk (30.7%), followed by camel milk (19.3%), goat milk (13.6%) and pasteurized milk (3.8%). The pooled prevalence of S. aureus in locally produced soft cheese (ayib) and traditional fermented milk (ergo) was 18.6% and 14.9%, respectively. The pooled prevalence of MRSA in milk and milk products was 0.73%. In this study, 58.9% of S. aureus isolates recovered from milk and milk products harbored at least one type of enterotoxin gene. Raw milk of the three species (cow, goat and camel) showed the highest S. aureus pooled prevalence rate at processing plants (50.3%), followed by milk collection centers (MCCs) (47.1%), selling points (34.5%), farm bulk milk (25.8%), milking buckets (24.8%) and udder milk (20.3%). Water for washing milking utensils (39.3%) was more contaminated than swab samples from farm workers’ nares (31.5%), milkers’ hands (25.9%), MCCs containers (23.8%), bulk tanks (20.4%), udders (15.6%), milking buckets (14.2%) and towels (10%). S. aureus isolates were highly resistant to penicillin G (92%), followed by ampicillin (82%) and amoxicillin (62.6%). The pooled multidrug resistance (MDR) was high (62.1%). Conclusion This systematic review revealed a high and increasing level of S. aureus contamination of raw milk from udder to MCCs or processing plants. Enterotoxin genes and MRSA were reported in milk, milk products and samples from farm workers. S. aureus showed resistance to different antimicrobial agents, with β-lactams showing the highest pooled antimicrobial resistance and the level of MDR was high. The results of this study indicated that the consumption of raw milk and milk products may predispose consumers to staphylococcal food poisoning. Application of good hygiene and handling practices across the dairy value chain starting from farm, udder health, milk cooling, heat treatment of milk before drinking and rational use of antibiotics in veterinary medicine can reduce the potential health risks from S. aureus and MRSA contamination of milk and milk products.