Carvacrol Essential Oil: A Natural Antibiotic against Zoonotic Multidrug-Resistant Staphylococcus Species Isolated from Diseased Livestock and Humans

Abstract

Staphylococcus species cause diseases in animals and humans. The prevalence and antimicrobial profiles of Staphylococcus spp. in animals and human samples in the Minya Governorate, Egypt, were determined, and resistance- and virulence-associated genes were observed in multidrug-resistant (MDR) isolates. Moreover, the antibacterial effect of carvacrol essential oil (EO) on the MDR isolates was studied. A total of 216 samples were aseptically collected from subclinically mastitic cow’s milk (n = 100), sheep abscesses (n = 25) and humans (n = 91). Out of 216 samples, a total of 154 single Staphylococcus species (71.3%) were isolated. The most frequent bacterial isolates were S. aureus (43%), followed by S. schleiferi (25%), S. intermedius (12%), S. xylosus (12%), S. haemolyticus (4.5%), S. epidermidis (2%) and S. aurecularis (1%). Haemolytic activity and biofilm production were detected in 77 and 47% of isolates, respectively. Antimicrobial susceptibility testing showed a high degree of resistance to the most commonly used antimicrobials in human and veterinary practices. The mecA, vanA, vanC1 and ermC resistance genes were detected in 93, 42, 83 and 13% of isolates, respectively. Moreover, hla, icaA and icaD virulence genes were detected in 50, 75 and 78% of isolates, respectively. Carvacrol effectively inhibited the growth of all tested isolates at concentrations of 0.1, 0.05 and 0.04% while a concentration of 0.03% inhibited 75% of isolates. Interestingly, some phenotypic changes were observed upon treatment with a carvacrol oil concentration of 0.03%. All the treated MDR Staphylococcus isolates changed from multidrug resistant to either susceptible or intermediately susceptible to 2–3 antimicrobials more than parental bacterial isolates. Real-time PCR was applied for the detection of the differential expression of mecA and vanC1 genes before and after treatment with carvacrol which revealed a mild reduction in both genes’ expression after treatment. Staphylococcus spp. Containing MDR genes are more likely to spread between humans and animals. From these results, carvacrol EO is a promising natural alternative to conventional antimicrobials for pathogens impacting human health and agriculture due to its potential antimicrobial effect on MDR pathogens; even in sub-lethal doses, carvacrol EO can affect their phenotypic properties and genes’ expression.

Carvacrol Selective Pressure Allows the Occurrence of Genetic Resistant Variants of Listeria monocytogenes EGD-e

“…Moreover, these natural antimicrobials are also under study as potential alternatives or enhancers to antibiotics treatment against multidrug-resistant (MDR) bacteria and the spread of AMR [ 12 ]. One of the most promising ICs as a food preservative is carvacrol due to its great antimicrobial properties against food-borne pathogens [ 37 ] and also against MDR bacteria [ 38 ]. This compound is mainly extracted from EOs of Origanum vulgare , Thymus vulgaris , and Thymbra capitata [ 39 , 40 ], and it is generally recognized as safe (GRAS) by the U.S. Food and Drug Administration [ 41 ].…”

Alternatives Therapeutic Approaches to Conventional Antibiotics: Advantages, Limitations and Potential Application in Medicine

“…Several studies have investigated the synergy between EOs components [ 223 , 224 ]. A variation between different outcomes was observed according to the test organism, antibiotic and essential oil tested [ 225 ]. The combination of two antimicrobial agents results in an antagonistic, indifferent, or synergistic effect, depending on the mechanisms exerted by each agent against the test organism, the characteristics of the test organism, and any chemical interactions between the two antimicrobial agents [ 226 ].…”

The mechanistic role of natural antimicrobials in preventing Staphylococcus aureus invasion of MAC-T cells using an in vitro mastitis model

“…The notorious pathogen, S. aureus , has earned its reputation for its persistent infections with low recovery rates, largely due to its ability to form biofilms, evade host immune responses, and reside within micro-abscesses [ 2 ]. Recent trends have also witnessed a surge in mastitis cases associated with coagulase-negative Staphylococci (CNS), capable of producing toxins and interacting with fibronectin-binding proteins (FnbA) [ 2 , 6 ]. FnbA and ClfA are adhesive proteins facilitating the pathogen’s engagement with bovine mammary epithelial cells, playing a pivotal role in biofilm genesis [ 7 ].…”

“…Additionally, ArlR is an integral part of the ArlRS signaling pathway, influencing both virulence determinants and antibiotic resistance by directly modulating subsequent gene expression [ 7 ]. The transmission of staphylococci frequently occurs between animals and humans with both populations exhibiting a significant presence of staphylococcus spp [ 6 ].…”

“…Notably, SCM, despite its covert nature, is the more common form and incurs greater economic losses than its clinical counterpart [ 4 ]. However, the implications of Staphylococci extend beyond the realm of bovine health as they are prominent nosocomial pathogens, with over 50 Staphylococcus spp and subspecies being implicated in bovine staphylococcal mastitis [ 6 ]. The transmission dynamics of resistance genes and direct zoonotic transmission raise public health concerns [ 9 ].…”