Research Article
BibTex RIS Cite

Antimicrobial activity of ozonated sunflower oil against Pseudomonas aeruginosa strains isolated from mares, and interactions with antimicrobial drugs

Year 2025, Volume: 12 Issue: 4, 808 - 819, 05.12.2025
https://doi.org/10.21448/ijsm.1606326

Abstract

Infectious endometritis in mares can result in reduced fertility, early embryonic loss, and general health decline, implicating extensive economic loss. Pseudomonas aeruginosa is an opportunistic pathogen that is among the most frequent bacterial pathogens associated with infectious endometritis in mares. Here we explored the antimicrobial potential of ozonated sunflower seed oil, compared to the conventional form (both widely explored for wound healing), against clinical isolates of Pseudomonas aeruginosa obtained from mares with endometritis. The effects of combining the oils with clinically relevant antimicrobial drugs were also investigated. The conventional form of the oil was active against the strains, whereas the ozonated oil was not. When combined with the antimicrobials, both oils significantly decreased the pharmacological activity of the drugs. This study opens doors for discussions on clinical protocols for treating fertility issues in mares, as well as bacterial resistance in the intrauterine environment.

Ethical Statement

We have no ethical issues to report in this paper.

Supporting Institution

No institution supported financially this study.

Thanks

No thanks to inform.

References

  • Alam, S., Richi, F.T., Emon, N.U., Chowdhury, A.A., Hasan, C.M., & Haque, M.R. (2024). First-time report on compound isolation from two Colocasia species: Vegetable-derived bioactive metabolites and their medicinal potential. Frontiers in Pharmacology, 15, Article 1474706. https://doi.org/10.3389/fphar.2024.1474706
  • Borzyszkowska-Bukowska, J., Czub, J., Szczeblewski, P., & Laskowski, T. (2023). Antibiotic-sterol interactions provide insight into the selectivity of natural aromatic analogues of amphotericin B and their photoisomers. Scientific Reports, 13(1), 762. https://doi.org/10.1038/s41598-023-28036-x
  • Carneiro, G.F., Filho, A.B.S., & Carneiro, L.C. (2023). Endometrite em Éguas: Diagnóstico e tratamentos convencionais e/ou alternativos [Endometritis in mares: Diagnosis and conventional and/or alternative treatments]. Ciência Animal, 30(4), S1, 113–122.
  • Cota, B.B., Alves, J.C., Caux, A.A., Passagli, L.C., Castro, A.K., & Luz, T.C. (2024). Use of herbal medicinal products among patients in primary health care in a Brazilian southeastern city: Evidence from the Prover Project. Einstein (São Paulo), 22, eAO0827.
  • Da Costa, G.J., Dos Santos, R.M., Ceravolo, I.P., Freire, G.P., & Dias-Souza, M.V. (2023). Green tea (Camellia sinensis) extract is effective against biofilms of Staphylococcus aureus and Pseudomonas aeruginosa, and interferes with the activity of antimicrobial drugs. Current Functional Foods, 2(1), Article e190423216032. https://doi.org/10.2174/2666862901666230419092405
  • Da Silva-Álvarez, E., Gómez-Arrones, V., Martín-Cano, F.E., Gaitskell-Phillips, G., Ortiz-Rodríguez, J.M., Carrasco, J.J., Gil, M.C., Peña Vega, F.J., & Ortega Ferrusola, C. (2022). Endometrial area of the blood flow as a marker of endometritis in equine. Reproduction in Domestic Animals, 57(Suppl 5), 98–102. https://doi.org/10.1111/rda.14132
  • Dias, C.G., Leal, W. de S., & Dias-Souza, M.V. (2022). Interference of nutraceuticals on the activity of antibacterial drugs against clinical isolates of Staphylococcus aureus, Escherichia coli, and Pseudomonas aeruginosa. International Journal of Chemical and Biological Sciences, 4(2), 10-14. https://doi.org/10.33545/26646765.2022.v4.i2a.40
  • Dias, K.J.S.O., Miranda, G.M., Bessa, J.R., Araújo, A.C.J., Freitas, P.R., Almeida, R.S., Paulo, C.L.R., Neto, J.B.A., Coutinho, H.D.M., & Ribeiro-Filho, J. (2022). Terpenes as bacterial efflux pump inhibitors: A systematic review. Frontiers in Pharmacology, 13, 953982. https://doi.org/10.3389/fphar.2022.953982
  • Dias-Souza, M.V., Andrade, S., Aguiar, A.P., & Monteiro, A.S. (2013). Evaluation of antimicrobial and anti-biofilm activities of Anacardium occidentale stem bark extract. Journal of Natural Products, 26, 198–205.
  • Dias-Souza, M.V., Perpétuo, A.A., Santos, G.S., et al. (2023). Natural products in drug discovery: Meeting the urgency for new antimicrobials for human and veterinary use. AIMS Molecular Science, 10(1), 11–21. https://doi.org/10.3934/molsci.2023002
  • Dias-Souza, M.V., Santos, G.S., Perpétuo, A.A., Cota, B.B., & Ceravolo, I.P. (2024). Antimicrobial activity of Banisteriopsis argyrophylla and Davilla rugosa leaf extracts over human and veterinary clinical isolates of Staphylococcus aureus. Journal of Health Science, 26(3), 143–146.
  • Dos Santos, G.S., Perpétuo, A.A., & Dias Souza, M.V. (2023). Susceptibility of bacterial species isolated from mares to ozonated sunflower oil. International Journal of Secondary Metabolite, 10(1), 119–123. https://doi.org/10.21448/ijsm.1167867
  • Dos Santos, R.M., Pimenta, G., & Dias-Souza, M.V. (2015). Carotenoids and flavonoids can impair the effectiveness of some antimicrobial drugs against clinical isolates of Escherichia coli and Staphylococcus aureus. International Food Research Journal, 22(5), 1777–1782.
  • Dos Santos, R.M., Pimenta, G., Figueiredo, F.J.B., & Dias-Souza, M.V. (2016). Interference of flavonoids and carotenoids on the antimicrobial activity of some drugs against clinical isolates of Pseudomonas aeruginosa. International Food Research Journal, 23, 1268–1273.
  • Ferreira, J.C., Amaral, R.S., & Cintra, B.S. (2021). Ozonioterapia no tratamento auxiliar de éguas inférteis: Potencial angiogênico e antimicrobiano [Ozone therapy in the auxiliary treatment of infertile mares: Angiogenic and antimicrobial potential]. Revista Brasileira de Reprodução Animal, 45(4), 482–488.
  • García-González, A., Velasco, J., Velasco, L., & Ruiz-Méndez, M.V. (2021). Characterization of press and solvent extraction oils from new sunflower seeds with modified phytosterol compositions. Journal of the Science of Food and Agriculture, 101(1), 101–109. https://doi.org/10.1002/jsfa.10619
  • Gil-Miranda, A., Macnicol, J., Orellana-Guerrero, D., Samper, J.C., & Gomez, D.E. (2024). Reproductive tract microbiota of mares. Veterinary Sciences, 11(7), Article 324. https://doi.org/10.3390/vetsci11070324
  • Guimarães, T.P., Carvalheira, J., & Rocha, A. (2012). Conception rate, uterine infection, and embryo quality after artificial insemination and natural breeding with a stallion carrier of Pseudomonas aeruginosa: A case report. Acta Veterinaria Scandinavica, 54(1), Article 20. https://doi.org/10.1186/1751-0147-54-20
  • Ito, Y., Nagasawa, M., Koyama, K., Ito, K., & Kikusui, T. (2024). Comparative analysis based on shared amplicon sequence variants reveals that cohabitation influences gut microbiota sharing between humans and dogs. Frontiers in Veterinary Science, 11, Article 1417461. https://doi.org/10.3389/fvets.2024.1417461
  • Kanokmedhakul, K., Kanokmedhakul, S., & Phatchana, R. (2005). Biological activity of anthraquinones and triterpenoids from Prismatomeris fragrans. Journal of Ethnopharmacology, 100(2), 284–288. https://doi.org/10.1016/j.jep.2005.03.015
  • Kim, D.Y., & Choi, B.Y. (2019). Costunolide: A bioactive sesquiterpene lactone with diverse therapeutic potential. International Journal of Molecular Sciences, 20(12), Article 2926. https://doi.org/10.3390/ijms20122926
  • Kim, J.H., Dong, J., Le, B.H., Lonergan, Z.R., Gu, W., Girke, T., Zhang, W., Newman, D.K., & Martins-Green, M. (2024). Pseudomonas aeruginosa activates quorum sensing, antioxidant enzymes, and type VI secretion in response to oxidative stress to initiate biofilm formation and wound chronicity. Antioxidants, 13(6), Article 655. https://doi.org/10.3390/antiox13060655
  • Köhne, M., Kuhlmann, M., Tönißen, A., Martinsson, G., & Sieme, H. (2020). Diagnostic and treatment practices of equine endometritis: A questionnaire. Frontiers in Veterinary Science, 7, Article 547. https://doi.org/10.3389/fvets.2020.00547
  • Landolsi, C., Salem-Berrabah, O.B., Feki, M., Harrabi, S., & Hosseinian, F. (2024). Unsaponifiable compounds and phenols content, antioxidant and antitrypsin activities of Prunus persica kernel oil. Journal of Oleo Science, 73(6), 865 874. https://doi.org/10.5650/jos.ess24027
  • Lestari, S., Kurnia, D., Mayanti, T., & Heliawati, L. (2024). Antimicrobial activities of stigmasterol from Piper crocatum in vitro and in silico. Journal of Chemistry, 2024, Article 2935516. https://doi.org/10.1155/2024/2935516
  • Levison, M.E., & Levison, J.H. (2009). Pharmacokinetics and pharmacodynamics of antibacterial agents. Infectious Disease Clinics of North America, 23(4), 791 815. https://doi.org/10.1016/j.idc.2009.06.008
  • Li, H.Y., Yang, W.Q., Zhou, X.Z., Shao, F., Shen, T., Guan, H.Y., Zheng, J., & Zhang, L.M. (2022). Antibacterial and antifungal sesquiterpenoids: Chemistry, resource, and activity. Biomolecules, 12(9), Article 1271. https://doi.org/10.3390/biom12091271
  • Morris, L.H.A., McCue, P.M., & Aurich, C. (2020). Equine endometritis: A review of challenges and new approaches. Reproduction, 160(5), R95 R110. https://doi.org/10.1530/REP-19-0478
  • Nakonechna, K., Ilko, V., Berčíková, M., Vietoris, V., Panovská, Z., & Doležal, M. (2024). Nutritional, utility, and sensory quality and safety of sunflower oil on the Central European market. Agriculture, 14(4), Article 536. https://doi.org/10.3390/agriculture14040536
  • Nocera, F.P., Maurizi, L., Masullo, A., Nicoletti, M., Conte, A.L., Brunetti, F., De Martino, L., Zagaglia, C., & Longhi, C. (2023a). Genotypic and phenotypic characterization of Escherichia coli isolates recovered from the uterus of mares with fertility problems. Animals, 13(10), 1639. https://doi.org/10.3390/ani13101639
  • Nocera, F.P., Pizzano, F., Masullo, A., Cortese, L., & De Martino, L. (2023b). Antimicrobial resistant Staphylococcus species colonization in dogs, their owners, and veterinary staff of the Veterinary Teaching Hospital of Naples, Italy. Pathogens, 12(8), 1016. https://doi.org/10.3390/pathogens12081016
  • Okafor, C.E., Ijoma, I.K., Igboamalu, C.A., Ezebalu, C.E., Eze, C.F., Osita-Chikeze, J.C., Uzor, C.E., & Ekwuekwe, A.L. (2024). Secondary metabolites, spectra characterization, and antioxidant correlation analysis of the polar and nonpolar extracts of Bryophyllum pinnatum (Lam) Oken. Biotechnologia, 105(2), 121 136. https://doi.org/10.5114/bta.2024.139752
  • Poli, A., Marangoni, F., Corsini, A., et al. (2021). Phytosterols, cholesterol control, and cardiovascular disease. Nutrients, 13(8), 2810. https://doi.org/10.3390/nu13082810
  • Prete, C.D., Nocera, F.P., Piegari, G., Palumbo, V., Martino, L., Cocchia, N., Paciello, O., Montano, C., & Pasolini, M.P. (2024). Use of cytobrush for bacteriological and cytological diagnosis of endometritis in mares. Veterinary World, 17(2), 398 406. https://doi.org/10.14202/vetworld.2024.398-406
  • Salehi, B., Rescigno, A., Dettori, T., Calina, D., Docea, A.O., Singh, L., Cebeci, F., Özçelik, B., Bhia, M., Dowlati Beirami, A., Sharifi-Rad, J., Sharopov, F., Cho, W.C., & Martins, N. (2020). Avocado-soybean unsaponifiables: A panoply of potentialities to be exploited. Biomolecules, 10(1), 130. https://doi.org/10.3390/biom10010130
  • Silva, J.S. da, Zilly, A., Silva, R.M.M. da, Librelotto, C.S., & Ferreira, H. (2021). Avaliação da atividade antibacteriana do óleo de girassol: Respaldo para a enfermagem. Research, Society and Development, 10(9), e8710917941. https://doi.org/10.33448/rsd-v10i9.17941
  • Spring, O. (2021). Sesquiterpene lactones in sunflower oil. LWT, https://doi.org/10.1016/j.lwt.2021.111047
  • Travagli, V., & Iorio, E.L. (2023). The biological and molecular action of ozone and its derivatives: State-of-the-art, enhanced scenarios, and quality insights. International Journal of Molecular Sciences, 24(10), 8465. https://doi.org/10.3390/ijms24108465
  • Ugazio, E., Tullio, V., Binello, A., Tagliapietra, S., & Dosio, F. (2020). Ozonated oils as antimicrobial systems in topical applications. Their characterization, current applications, and advances in improved delivery techniques. Molecules (Basel, Switzerland), 25(2), 334. https://doi.org/10.3390/molecules25020334
  • Uttu, A.J., Sallau, M.S., Ibrahim, H., & Iyun, O.R.A. (2022). Isolation, characterization, and docking studies of campesterol and β-sitosterol from Strychnos innocua (Delile) root bark. Journal of Taibah University Medical Sciences, 18(3), 566 578. https://doi.org/10.1016/j.jtumed.2022.12.003
  • Virendra, A., Gulavane, S.U., Ahmed, Z.A., Reddy, R., Chaudhari, R.J., Gaikwad, S.M., Shelar, R.R., Ingole, S.D., Thorat, V.D., Khanam, A., & Khan, F.A. (2024). Metagenomic analysis unravels novel taxonomic differences in the uterine microbiome between healthy mares and mares with endometritis. Veterinary Medicine and Science, 10(2), e1369. https://doi.org/10.1002/vms3.1369
  • Welz, A.N., Emberger-Klein, A., & Menrad, K. (2018). Why people use herbal medicine: Insights from a focus-group study in Germany. BMC Complementary and Alternative Medicine, 18, 92. https://doi.org/10.1186/s12906-018-2160-6
  • Zhao, K., Jiang, Y., Dev, K., He, X., Sharma, V., & Pang, X. (2024). Terpenoids as principal bioactive compound of Cissampelos oppositifolia essential oils: Enhancing synergistic efficacy with conventional antibiotics. Frontiers in Cellular and Infection Microbiology, 14, 1481656. https://doi.org/10.3389/fcimb.2024.1481656
There are 43 citations in total.

Details

Primary Language English
Subjects Pharmaceutical Microbiology
Journal Section Research Article
Authors

Arthur Azevedo Perpétuo This is me 0000-0002-3863-8718

Gabriel Souza Dos Santos This is me 0000-0002-2801-0214

Marcus Vinícius Dias Souza 0000-0001-5723-5095

Submission Date December 28, 2024
Acceptance Date May 9, 2025
Early Pub Date September 1, 2025
Publication Date December 5, 2025
Published in Issue Year 2025 Volume: 12 Issue: 4

Cite

APA Azevedo Perpétuo, A., Souza Dos Santos, G., & Dias Souza, M. V. (2025). Antimicrobial activity of ozonated sunflower oil against Pseudomonas aeruginosa strains isolated from mares, and interactions with antimicrobial drugs. International Journal of Secondary Metabolite, 12(4), 808-819. https://doi.org/10.21448/ijsm.1606326
International Journal of Secondary Metabolite

e-ISSN: 2148-6905