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. 2023 Sep 15:13:1265027.
doi: 10.3389/fcimb.2023.1265027. eCollection 2023.

Partnering essential oils with antibiotics: proven therapies against bovine Staphylococcus aureus mastitis

Marwa I Abd El-Hamid  1 , Reham M El-Tarabili  2 , Mosa M Bahnass  3   4 , Mohammed Abdulrahman Alshahrani  5 , Ahmed Saif  6 , Khairiah Mubarak Alwutayd  7 , Fatmah Ahmed Safhi  7 , Abdallah Tageldein Mansour  8   9 , Noaf Abdullah N Alblwi  10 , Mohammed M Ghoneim  11 , Ayman Abo Elmaaty  12 , Helal F Al-Harthi  13 , Mahmoud M Bendary  14
Affiliations

Partnering essential oils with antibiotics: proven therapies against bovine Staphylococcus aureus mastitis

Marwa I Abd El-Hamid et al. Front Cell Infect Microbiol. .

Abstract

Introduction: There is an urgent need to develop therapeutic options for biofilm-producing Staphylococcus aureus (S. aureus). Therefore, the renewed interest in essential oils (EOs), especially carvacrol, linalool and eugenol, has attracted the attention of our research group.

Methods: Multidrug resistance and multivirulence profiles in addition to biofilm production of S. aureus strains isolated from cows with mastitis were evaluated using both phenotypic and genotypic methods. The antimicrobial and antibiofilm activities of EOs were tested using both in vitro and molecular docking studies. Moreover, the interactions between commonly used antibiotics and the tested EOs were detected using the checkerboard method.

Results: We found that all our isolates (n= 37) were biofilm methicillin resistant S. aureus (MRSA) producers and 40.5% were vancomycin resistant S. aureus (VRSA). Unfortunately, 73 and 43.2% of the recovered MRSA isolates showed multidrug resistant (MDR) and multivirulence patterns, respectively. The antimicrobial activities of the tested EOs matched with the phenotypic evaluation of the antibiofilm activities and molecular docking studies. Linalool showed the highest antimicrobial and antibiofilm activities, followed by carvacrol and eugenol EOs. Fortunately, synergistic interactions between the investigated EOs and methicillin or vancomycin were detected with fractional inhibitory concentration index (FICI) values ≤ 0.5. Moreover, the antimicrobial resistance patterns of 13 isolates changed to sensitive phenotypes after treatment with any of the investigated EOs. Treatment failure of bovine mastitis with resistant S. aureus can be avoided by combining the investigated EOs with available antimicrobial drugs.

Conclusion: We hope that our findings can be translated into a formulation of new pharmaceutical dosage forms against biofilm-producing S. aureus pathogens.

Keywords: MDR; MRSA; antibiofilm; carvacrol; eugenol; linalool.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Antimicrobial resistance patterns of MRSA (A) and VRSA (B) isolates.
Figure 2
Figure 2
Heat maps illustrating the distribution of phenotypic antimicrobial resistance, mecA, vanA and virulence genes and agr genotypes among MRSA (A) and VRSA (B) isolates. The blue and red colors represent the sensitivity and resistance to certain antimicrobial agent and the absence and presence of mecA, vanA and certain virulence gene and agr genotype, respectively. The recovered isolates are coded on the right of the heat map; M: mastitis milk. CFX: cefoxitin, AMP: ampicillin, AMC: amoxicillin-clavulanic acid, VA: vancomycin, E: erythromycin, C: chloramphenicol, SXT: sulfamethoxazole-trimethoprim, CIP: ciprofloxacin and CN: gentamycin, mecA: methicillin resistance encoding gene, vanA: vancomycin resistance encoding gene, sea: staphylococcal enterotoxin a gene, seb: staphylococcal enterotoxin b gene, sec: staphylococcal enterotoxin c gene, see: staphylococcal enterotoxin e gene, hla: alpha-hemolysin gene, hlb: beta-hemolysin gene, icaA: intercellular adhesion A gene, agr: accessory gene regulator gene.
Figure 3
Figure 3
The 3D protein positioning and 3D binding interactions of the tested essential oils with S. aureus biofilm associated protein; binding of carvacrol (A), linalool (B) and eugenol (C) with PDB entry of 7c7u.
See this image and copyright information in PMC

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