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Innovative next-generation therapies in combating multi-drug-resistant and multi-virulent Escherichia coli isolates: insights from in vitro, in vivo, and molecular docking studies

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Abstract

Despite notable advances in vaccine and antimicrobial therapies, treatment failure has been increasingly reported worldwide. Of note, multi-drug-resistant (MDR) Escherichia coli (E. coli) strains have a considerable share in the evolution of this crisis. So, current practice guidelines are directed towards complementary and alternative therapies. Therefore, we evaluated the antibacterial and antivirulence activities of curcumin, thymol, and eugenol essential oils (EOs) as well as EOs-EOs and EOs-antibiotics interactions on MDR and multi-virulent E. coli isolates. Unfortunately, MDR E. coli could be isolated with a prevalence rate of 95.6% (86/90). Additionally, the majority of our isolates harbored both fimH (95.6%) and ompA (91.1%) genes, and half of them (45/90) were multi-virulent. Interestingly, all the tested EOs, especially curcumin, exhibited inhibitory activities against all MDR and multi-virulent E. coli isolates. The addition of thymol enhanced the antibacterial activities of curcumin and eugenol. Moreover, the activities of piperacillin/tazobactam and imipenem were increased by adding any one of the tested EOs. Regarding the antivirulence activities of the tested EOs, the cell surfaces of treated E. coli isolates under transmission electron microscope (TEM) were uneven. The cells appeared damaged and lost their appendages. Furthermore, EOs strongly reduced the transcription of ompA and fimH genes. The antibacterial and antivirulence activities of the used EOs were confirmed by in silico and mice protection assays. Hereby, we introduced the promising uses of curcumin, thymol, and eugenol oils as complementary and alternative therapies for combating MDR and multi-virulent E. coli isolates.

Key points

• Our promising results confirmed that we were right for renewed interest of EOs.

• The EOs, especially curcumin, can be used to prevent treatment failure.

• We supposed a new pharmaceutical formulation of antibiotic powders dissolved in EOs.

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All data generated or analyzed during this study are included in the submitted manuscript.

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Acknowledgement

This research work was funded by Institutional Fund Projects under grant no. (IFPIP: 1562-166-1442). Therefore, the authors gratefully acknowledge technical and financial support from the Ministry of Education and King Abdulaziz University, DSR, Jeddah, Saudi Arabia.

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Author notes

  1. Mahmoud M. Bendary and Marwa I. Abdel-Hamid contributed equally as first author.

Authors and Affiliations

  1. Department of Natural Products, Faculty of Pharmacy, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    Mahmoud A. Elfaky

  2. Centre for Artificial Intelligence in Precision Medicines, King Abdulaziz University, Jeddah, 21589, Saudi Arabia

    Mahmoud A. Elfaky

  3. Department of Microbiology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, 44511, Egypt

    Marwa I. Abdel-Hamid

  4. Department of Microbiology, Faculty of Veterinary Medicine, Matrouh University, Matrouh, 51511, Egypt

    Eman Khalifa

  5. Department of Microbiology and Immunology, Faculty of Pharmacy, 6 October University, 6 October, Cairo, 12566, Egypt

    Walaa A. Alshareef

  6. Infection Control Unit, Zagazig University Hospital, Zagazig, 44511, Egypt

    Rasha A. Mosbah

  7. Department of Pharmacology, Faculty of Veterinary Medicine, Mansoura University, Mansoura, 35516, Egypt

    Sara T. Elazab

  8. Department of Pharmacy Practice, College of Pharmacy, Al Maarefa University, Ad Diriyah, 13713, Saudi Arabia

    Mohammed M. Ghoneim

  9. Pharmaceutical Chemistry Department, College of Pharmacy, Jouf University, Sakaka, Al-jouf, 72341, Saudi Arabia

    Mohammad M. Al-Sanea

  10. Department of Microbiology and Immunology, Faculty of Pharmacy, Port Said University, Port Said, 42511, Egypt

    Mahmoud M. Bendary

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Contributions

MMB, EK, MAE, MIA: conceived and designed the study and analyzed data. MMB, MIA WAA, RAM, STE: analyzed the data, wrote the first draft of this manuscript. MMB, MIA, STE, MAG, MAA: did the software and wrote the final version of the manuscript

Corresponding author

Correspondence to Mahmoud M. Bendary.

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Ethical statement

Performing the antimicrobial susceptibility testing was the main purpose for collecting the clinical samples, which were taken from the patients in both Zagazig and Port Said University hospitals during the routine work in their laboratories. Therefore, the sole aims for obtaining these clinical samples were the appropriate care for patients, diagnosis, and treatment. For that, the informed consents of the participants were required; meanwhile, the ethical approval to perform this work was not necessary. The animal experimental study (in vivo mice protection assay) was carried out following the National Institutes of Health guidelines for the Care and Use of Laboratory Animals and was approved by the Ethics of Animal Use in Research Committee (IACUC, Institutional Review Board) at Faculty of Veterinary Medicine, Zagazig University under the reference number (ZU-IACUC/2/F/2021) and in accordance with the ARRIVE guidelines, the UK Animals (Scientific Procedures) Act 1986 and related guidelines (ECAHZU, 23 August 2015).

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The authors declare no competing interests.

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Elfaky, M.A., Abdel-Hamid, M.I., Khalifa, E. et al. Innovative next-generation therapies in combating multi-drug-resistant and multi-virulent Escherichia coli isolates: insights from in vitro, in vivo, and molecular docking studies. Appl Microbiol Biotechnol 106, 1691–1703 (2022). https://doi.org/10.1007/s00253-022-11781-w

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