Planta Med 2024; 90(14): 1080-1096
DOI: 10.1055/a-2416-8584
Biological and Pharmacological Activity
Original Papers

Evaluation of Antimicrobial Activity of Selected Plant Extracts against Staphylococcus Strains Isolated from Wound Infections

Anna Pietruczuk-Padzik
1   Department of Pharmaceutical Microbiology and Bioanalysis, Medical University of Warsaw, Warsaw, Poland
5   Center for Preclinical Research, Medical University of Warsaw, Warsaw, Poland
,
Milena Śliwińska
2   Studentsʼ Scientific Association at the Department of Pharmaceutical Microbiology and Bioanalysis, Medical University of Warsaw, Warsaw, Poland
,
Marta Mainka
3   Department of Pharmaceutical Biology, Medical University of Warsaw, Warsaw, Poland
,
Monika E. Czerwińska
4   Department of Biochemistry and Pharmacogenomics, Medical University of Warsaw, Warsaw, Poland
5   Center for Preclinical Research, Medical University of Warsaw, Warsaw, Poland
,
Weronika Skowrońska
3   Department of Pharmaceutical Biology, Medical University of Warsaw, Warsaw, Poland
,
3   Department of Pharmaceutical Biology, Medical University of Warsaw, Warsaw, Poland
› Institutsangaben
The project was carried out with the use of CePT infrastructure financed by the European Regional Development Fund within the Operational Program “Innovative economy” for 2007 – 2013. The authors would like to thank Dr. Joanna Stefańska for her financial support.

Abstract

Wound infections are a significant medical problem, with Staphylococcus species being one of the most common etiological factors. Treatment is complex due to bacterial antibiotic resistance and the ability to form a biofilm. The aim of this study was to determine the drug susceptibility of the clinical isolates of Staphylococcus species obtained from wound infections, assess their ability to form a biofilm in vitro, evaluate the level of extracellular slime synthesis, and test the antistaphylococcal properties of selected plant extracts against plate-cultured bacteria and activity against mature biofilms. A total of 20 Staphylococcus strains were evaluated. The antibiotic susceptibility and sensitivity of the strains to the tested extracts were determined using the disc diffusion method. The production of extracellular bacterial slime was assessed using Congo Red agar plates. The biofilm formation and the effect of plant extracts on the biofilm layer were examined using the MTT method on polystyrene microtiter plates. Diverse drug susceptibility profiles, slime production ability, and in vitro biofilm formation were observed among the tested strains. It was found that aqueous extracts from the Serpylli herba, Arctii lappae folium, Taraxaci folium, and Galii aparini herba showed antibacterial activity against some of the tested strains. In contrast, their antibiofilm activity was not confirmed. Among all tested preparations, the most promising antimicrobial extracts in both planktonic cultures and biofilm were Thymus serpyllum herb and Taraxacum officinale leaf extracts. These results allowed us to conclude their potential application in medicine to support the treatment of challenging wound conditions.



Publikationsverlauf

Eingereicht: 24. April 2024

Angenommen nach Revision: 09. September 2024

Artikel online veröffentlicht:
10. Oktober 2024

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  • References

  • 1 Najm A, Javed SA, Al Bratty M, Alhazmi HA. Modern approaches in the discovery and development of plant-based natural products and their analogues as potential therapeutic agents. Molecules 2022; 27: 349
  • 2 Nasim N, Sandeep IS, Mohanty S. Plant-derived natural products for drug discovery: Current approaches and prospects. Nucleus (Calcutta) 2022; 65: 399-411
  • 3 Bodeker C, Bodeker G, Ong CK, Grundy CK, Burford G, Shein K. WHO Global Atlas of Traditional, Complementary and Alternative Medicine. Geneva, Switzerland: World Health Organization; 2005
  • 4 Cheesman MJ, Ilanko A, Blonk B, Cock IE. Developing new antimicrobial therapies: Are synergistic combinations of plant extracts/compounds with conventional antibiotics the solution?. Pharmacogn Rev 2017; 11: 57-72
  • 5 Puca V, Marulli RZ, Grande R, Vitale I, Niro A, Molinaro G, Prezioso S, Muraro R, Di Giovanni P. Microbial species isolated from infected wounds and antimicrobial resistance analysis: Data emerging from a three-years retrospective study. Antibiotics (Basel) 2021; 24: 1162
  • 6 Malka M, Krakowiecki A, Chojak M, Pławski M, Wądołek M, Wołowicz A, Dyczewska A, Paź A, Pawlik K, Grzela T. The pathogen isolates in chronic wound infections in Poland. Pol J Microbiol 2023; 72: 133-142
  • 7 Hrynyshyn A, Simões M, Borges A. Biofilms in surgical site infections: Recent advances and novel prevention and eradication strategies. Antibiotics (Basel) 2022; 7: 69
  • 8 Percival SL, McCarty SM, Lipsky B. Biofilms and wounds: An overview of the evidence. Adv Wound Care (New Rochelle) 2015; 4: 373-381
  • 9 Sharifi-Rad M, Iriti M, Sharifi-Rad M, Gibbons S, Sharifi-Rad J. Anti-methicillin-resistant Staphylococcus aureus (MRSA) activity of Rubiaceae, Fabaceae and Poaceae plants: A search for new sources of useful alternative antibacterials against MRSA infections. Cell Mol Biol 2016; 62: 39-45
  • 10 Herman A, Herman AP. Herbal products for treatment of burn wounds. J Burn Care Res 2020; 41: 457-465
  • 11 Ali SI, Gopalakrishnan B, Venkatesalu V. Pharmacognosy, phytochemistry and pharmacological properties of Achillea millefolium L.: a review. Phytother Res 2017; 31: 1140-1161
  • 12 Givol O, Kornhaber R, Visentin D, Cleary M, Haik J, Harats M. A systematic review of Calendula officinalis extract for wound-healing. Wound Repair Regen 2019; 27: 548-561
  • 13 Qian L, Zhou Y, Teng Z, Du CL, Tian C. Preparation and antibacterial activity of oligosaccharides derived from dandelion. Int J Biol Macromol 2014; 64: 392-394
  • 14 Chan YS, Chan YS, Cheng LN, Wu JH, Chan E, Kwan YW, Lee SM, Leung GP, Yu PH, Chan SW. A review of the pharmacological effects of Arctium lappa (burdock). Inflammopharmacology 2011; 19: 245-254
  • 15 Mainka M, Czerwińska ME, Osińska E, Ziaja M, Bazylko A. Screening of antioxidative properties and inhibition of inflammation-linked enzymes by aqueous and ethanolic extracts of plants traditionally used in wound healing in Poland. Antioxidants (Basel) 2021; 10: 698
  • 16 European Medicines Agency. European Union herbal monograph on Achillea millefolium L., herba Final–Revision 1. Accessed on 28 August 2023 at https://www.ema.europa.eu/en/documents/herbal-opinion/draft-european-union-herbal-monograph-achillea-millefolium-l-herba-revision-1_en.pdf
  • 17 European Medicines Agency. Community herbal monograph on Arctium lappa L., radix. Accessed on 28 August 2023 at https://www.ema.europa.eu/en/documents/herbal-monograph/final-community-herbal-monograph-arctium-lappa-l-radix_en.pdf
  • 18 Skowrońska W, Granica S, Dziedzic M, Kurkowiak J, Ziaja M, Bazylko A. Arctium lappa and Arctium tomentosum, sources of Arctii radix: comparison of anti-lipoxygenase and antioxidant activity as well as the chemical composition of extracts from aerial parts and from roots. Plants 2021; 10: 78
  • 19 Jarić S, Mitrović M, Pavlović P. Review of ethnobotanical, phytochemical, and pharmacological study of Thymus serpyllum L. Evid Based Complement Alternat Med 2015; 2015: 101978
  • 20 Ivasenko S, Orazbayeva P, Skalicka-Wozniak K, Ludwiczuk A, Marchenko A, Ishmuratova M, Poleszak E, Korona-Glowniak I, Akhmetova S, Karilkhan I, Loseva I. Antimicrobial activity of ultrasonic extracts of two chemotypes of Thymus serpyllum L. of central Kazakhstan and their polyphenolic profiles. Maced J Med Sci 2021; 9: 61-67
  • 21 Jovanović AA, Djordjević VB, Petrović PM, Pljevljakušić DS, Zdunić GM, Šavikin KP, Bugarski BM. The influence of different extraction conditions on polyphenol content, antioxidant and antimicrobial activities of wild thyme. J Appl Res Med Aromat Plants 2021; 25: 1-7
  • 22 Fan M, Zhang X, Song H, Zhang Y. Dandelion (Taraxacum Genus): A Review of Chemical Constituents and Pharmacological Effects. Molecules 2023; 28: 5022
  • 23 Grauso L, Emrick S, de Falco B, Lanzotti V, Bonanomi G. Common dandelion: A review of its botanical, phytochemical and pharmacological profiles. Phytochem Rev 2019; 18: 1115-1132
  • 24 Schütz K, Kammerer DR, Carle R, Schieber A. Characterization of phenolic acids and flavonoids in dandelion (Taraxacum officinale WEB. ex WIGG.) root and herb by high-performance liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 2005; 19: 179-186
  • 25 Shafeie N, Naini AT, Jahromi HK. Comparison of different concentrations of Calendula officinalis gel on cutaneous wound-healing. Biomed Pharmacol J 2015; 8: 979-992
  • 26 Nicolaus C, Junghanns S, Hartmann A, Murillo R, Ganzera M, Merfort I. In vitro studies to evaluate the wound-healing properties of Calendula officinalis extracts. J Ethnopharmacol 2017; 196: 94-103
  • 27 Ilina T, Skowrońska W, Kashpur N, Granica S, Bazylko A, Kovalyova A, Goryacha O, Koshovyi O. Immunomodulatory activity and phytochemical profile of infusions from cleavers herb. Molecules 2020; 25: 3721
  • 28 The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 13.1, 2023. Accessed on 28 August 2023 at: http://www.eucast.org
  • 29 Kant V, Kumar D, Prasad R, Gopal A, Pathak NN, Kumar P, Tandan SK. Combined effect of substance P and curcumin on cutaneous wound-healing in diabetic rats. J Surg Res 2017; 212: 130-145
  • 30 Jones RE, Foster DS, Longaker MT. Management of chronic wounds–2018. JAMA 2018; 320: 1481-1482
  • 31 Roy R, Tiwari M, Donelli G, Tiwari V. Strategies for combating bacterial biofilms: A focus on anti-biofilm agents and their mechanisms of action. Virulence 2018; 9: 522-554
  • 32 Frazee BW, Lynn J, Charlebois ED, Lambert L, Lowery D, Perdreau-Remington F. High prevalence of methicillin-resistant Staphylococcus aureus in emergency department skin and soft tissue infections. Ann Emerg Med 2005; 45: 311-320
  • 33 Tang Y, Lou Z, Rahman MR, Al-Hajj DN, Wang H. Chemical composition and anti-biofilm activity of burdock (Arctium lappa L Asteraceae) leaf fractions against Staphylococcus aureus . Trop J Pharm Res 2014; 13: 1933-1939
  • 34 Kernou ON, Azzouz Z, Madani K, Rijo P. Application of rosmarinic acid with its derivatives in the treatment of microbial pathogens. Molecules 2023; 28: 4243
  • 35 The European Committee on Antimicrobial Susceptibility Testing. Antimicrobial susceptibility testing. EUCAST disc diffusion method. Version 11.0, 2023. Accessed on 28 August 2023 at: http://www.eucast.org
  • 36 Freeman DJ, Falkiner FR, Keane CT. New method for detecting slime production by coagulase negative staphylococci. J Clin Pathol 1989; 42: 872-874
  • 37 Stepanović S, Vuković D, Hola V, Bonaventura G, Djukic S, Irkovic IC, Ruzicka F. Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 2007; 115: 891-899
  • 38 Jovanović AA, Verica B, Ðordević VB, Gordana M, Zdunić GM, Pljevljakušić DS, Šavikin KP, Godevac DM, Bugarski BM. Optimization of the extraction process of polyphenols from Thymus serpyllum L. herb using maceration, heat- and ultrasound-assisted techniques. Sep Purif Technol 2017; 179: 369-380
  • 39 Clifford M, Jaganath I, Ludwig I, Crozier A. Chlorogenic acids and the acyl-quinic acids: Discovery, biosynthesis, bioavailability and bioactivity. Nat Prod Rep 2017; 34: 1391-1421
  • 40 Geng P, Sun J, Zhang M, Li X, Harnly J, Chen P. Comprehensive characterization of C-glycosyl flavones in wheat (Triticum aestivum L.) germ using UPLC-PDA-ESI/HRMSn and mass defect filtering. J Mass Spectrom 2016; 51: 914-930
  • 41 Jiménez-López J, Ruiz-Medina A, Ortega-Barrales P, Llorent-Martínez E. Rosa rubiginosa and Fraxinus oxycarpa herbal teas: characterization of phytochemical profiles by liquid chromatography-mass spectrometry, and evaluation of the antioxidant activity. New J Chem 2017; 41: 7681-7688
  • 42 Ribas-Agustí A, Gratacós-Cubarsí M, Sarraga C, Garcia-Regueiro JA, Castellari M. Analysis of eleven phenolic compounds including novel p-coumaroyl derivatives in lettuce (Lactuca sativa L.) by ultra-high-performance liquid chromatography with photodiode array and mass spectrometry detection. Phytochem Anal 2011; 22: 555-563
  • 43 Serrano C, Villena G, Rodríguez E, Calsino B, Ludeña M, Ccana-Ccapatinta G. Phytochemical analysis for ten Peruvian Mentheae (Lamiaceae) by liquid chromatography associated with high resolution mass spectrometry. Sci Rep 2023; 13: 10714
  • 44 Xu M, Han J, Li H, Fan L, Liu A, Guo D. Analysis on the stability of total phenolic acids and salvianolic acid B from Salvia miltiorrhiza by HPLC and HPLC-MSn . Nat Prod Commun 2008; 3: 669-676