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

Marwa I Abd El-Hamid; Reham M El-Tarabili; Mosa M Bahnass; Mohammed Abdulrahman Alshahrani; Ahmed Saif; Khairiah Mubarak Alwutayd; Fatmah Ahmed Safhi; Abdallah Tageldein Mansour; Noaf Abdullah N Alblwi; Mohammed M Ghoneim; Ayman Abo Elmaaty; Helal F Al-Harthi; Mahmoud M Bendary

doi:10.3389/fcimb.2023.1265027

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

Front Cell Infect Microbiol. 2023 Sep 15:13:1265027. doi: 10.3389/fcimb.2023.1265027. eCollection 2023.

Authors

Affiliations

¹ Department of Microbiology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt.
² Department of Bacteriology, Immunology and Mycology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, Egypt.
³ Department of Animal Medicine (Infectious Diseases), Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt.
⁴ Department of Clinical Laboratory Sciences, Applied Medical Sciences College, Najran University, Najran, Saudi Arabia.
⁵ Department of Clinical Laboratory Sciences, Faculty of Applied Medical Sciences, Najran University, Najran, Saudi Arabia.
⁶ Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, King Khalid University, Abha, Saudi Arabia.
⁷ Department of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.
⁸ Animal and Fish Production Department, College of Agricultural and Food Sciences, King Faisal University, Al-Ahsa, Saudi Arabia.
⁹ Fish and Animal Production Department, Faculty of Agriculture, Alexandria University, Alexandria, Egypt.
¹⁰ Al Hadithah General Hospital, Al-Qurayyat, Saudi Arabia.
¹¹ Department of Pharmacy Practice, College of Pharmacy, Al Maarefa University, Riyadh, Saudi Arabia.
¹² Medicinal Chemistry Department, Faculty of Pharmacy, Port Said University, Port Said, Egypt.
¹³ Biology Department, Turabah University College, Taif University, Taif, Saudi Arabia.
¹⁴ Department of Microbiology and Immunology, Faculty of Pharmacy, Port Said University, Port Said, Egypt.

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Anti-Bacterial Agents / pharmacology
Anti-Bacterial Agents / therapeutic use
Cattle
Eugenol
Female
Mastitis, Bovine* / drug therapy
Methicillin-Resistant Staphylococcus aureus* / genetics
Microbial Sensitivity Tests
Molecular Docking Simulation
Oils, Volatile* / pharmacology
Oils, Volatile* / therapeutic use
Staphylococcal Infections* / drug therapy
Staphylococcal Infections* / veterinary
Staphylococcus aureus

Substances

Anti-Bacterial Agents
carvacrol
linalool
Oils, Volatile
Eugenol

Grants and funding

Princess Nourah bint Abdulrahman University Researchers Supporting Project Number PNURSP2023R318, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia. Moreover, this work was supported by the Deanship of Scientific Research, Vice Presidency for Graduate Studies and Scientific Research, King Faisal University, Saudi Arabia [GRANT4,029]