Evaluation of anti-biofilm and anti-virulence effect of zinc sulfate on Staphylococcus aureus isolates.
Biofilms
/ drug effects
Staphylococcus aureus
/ drug effects
Zinc Sulfate
/ pharmacology
Anti-Bacterial Agents
/ pharmacology
Microbial Sensitivity Tests
Virulence
/ drug effects
Virulence Factors
/ genetics
Humans
Staphylococcal Infections
/ microbiology
Hemolysis
/ drug effects
Drug Synergism
Gene Expression Regulation, Bacterial
/ drug effects
Staphylococcus aureus
Anti-biofilm
Anti-virulence
Synergistic effect
Zinc sulfate
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
28 10 2024
28 10 2024
Historique:
received:
14
03
2024
accepted:
04
10
2024
medline:
29
10
2024
pubmed:
29
10
2024
entrez:
29
10
2024
Statut:
epublish
Résumé
Staphylococcus aureus produces a plethora of virulence factors to invade and establish infections in the host system, and biofilms are more resistant to antibiotics than planktonic cells. In this study, we aimed to investigate the anti-virulence and anti-biofilm potentials of zinc sulfate against S. aureus isolates. The synergistic effect of zinc sulfate in combination with antibiotics on S. aureus was characterized using the checkerboard method. The influence of zinc sulfate on biofilm formation and virulence factors production by S. aureus was experimentally assessed. RT-qPCR was used to investigate the effect of zinc sulfate on the expression of biofilm-related genes. Zinc sulfate exhibited good antibacterial activity against S. aureus with a MIC of 128 µg/ml against all tested isolates. Also, the findings indicate a synergistic effect of a combination of zinc sulfate and antibiotics against the tested isolates. Zinc sulfate at 256 µg/ml concentration inhibited biofilm formation for all isolates. The expression of biofilm-related genes was significantly repressed in zinc sulfate-treated bacteria compared to untreated cells. Zinc sulfate could inhibit the hemolytic ability of S. aureus. Moreover, zinc sulfate-treated bacteria exhibited a significant decrease in coagulase and catalase activity relative to control untreated S. aureus. Our results support that zinc sulfate is a potential antimicrobial and anti-virulence agent against S. aureus infections.
Identifiants
pubmed: 39468094
doi: 10.1038/s41598-024-75317-0
pii: 10.1038/s41598-024-75317-0
doi:
Substances chimiques
Zinc Sulfate
7733-02-0
Anti-Bacterial Agents
0
Virulence Factors
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
25747Informations de copyright
© 2024. The Author(s).
Références
Taylor, T. A. & Unakal C. G. Staphylococcus aureus infection. (2017).
Lister, J. L. & Horswill, A. R. Staphylococcus aureus biofilms: Recent developments in biofilm dispersal. Front. Cell. Infect. Microbiol. 4, 178. https://doi.org/10.3389/fcimb.2014.00178 (2014).
doi: 10.3389/fcimb.2014.00178
pubmed: 25566513
pmcid: 4275032
Sedarat, Z. & Taylor-Robinson, A. W. Biofilm formation by pathogenic bacteria: Applying a Staphylococcus aureus model to appraise potential targets for therapeutic intervention. Pathogens 11 https://doi.org/10.3390/pathogens11040388 (2022).
Halebeedu Prakash, P., Rajan, V. & Gopal, S. Predominance of SCCmec types IV and V among biofilm producing device-associated Staphylococcus aureus strains isolated from tertiary care hospitals in Mysuru, India. Enferm Infecc Microbiol. Clin. 35, 229–235. https://doi.org/10.1016/j.eimc.2016.09.005 (2017).
doi: 10.1016/j.eimc.2016.09.005
pubmed: 27825734
Roohani, N., Hurrell, R., Kelishadi, R. & Schulin, R. Zinc and its importance for human health: An integrative review. J. Res. Med. Sci. 18, 144–157 (2013).
pubmed: 23914218
pmcid: 3724376
Boone, C. B., Buhl, C. & Stone, K. D. Zinc sulfate general fact sheet. National Pesticide Information Center, Oregon State University Extension Services. http://npic.orst.edu/factsheets/znso4gen.html (2012).
Almuhayawi, M. S. et al. Staphylococcus aureus induced wound infections which antimicrobial resistance, methicillin- and vancomycin-resistant: Assessment of emergence and cross sectional study. Infect. Drug Resist. 16, 5335–5346. https://doi.org/10.2147/IDR.S418681 (2023).
Tsige, Y. et al. Prevalence of methicillin-resistant Staphylococcus aureus and associated risk factors among patients with wound infection at referral hospital, Northeast Ethiopia. J. Pathogens. 2020 (3168325). https://doi.org/10.1155/2020/3168325 (2020).
Abdelraheem, W., Abdelraheem & Zaki, S. Phenotypic and genotypic detection of biofilm formation and methicillin resistance among Staphylococcus aureus isolates. J. Microbes Infect. Dis. 2, 485–496. https://doi.org/10.21608/mid.2021.80188.1163 (2021).
doi: 10.21608/mid.2021.80188.1163
Abdelraheem, W. M., Khairy, R. M. M., Zaki, A. I. & Zaki, S. H. Effect of ZnO nanoparticles on methicillin, vancomycin, linezolid resistance and biofilm formation in Staphylococcus aureus isolates. Ann. Clin. Microbiol. Antimicrob. 20, 54. https://doi.org/10.1186/s12941-021-00459-2 (2021).
doi: 10.1186/s12941-021-00459-2
pubmed: 34419054
pmcid: 8379777
Ahmed, E. F., Rasmi, A. H., Darwish, A. M. A. & Gad, G. F. M. Prevalence and resistance profile of bacteria isolated from wound infections among a group of patients in upper Egypt: A descriptive cross-sectional study. BMC Res. Notes. 16, 106. https://doi.org/10.1186/s13104-023-06379-y (2023).
doi: 10.1186/s13104-023-06379-y
pubmed: 37337258
pmcid: 10280819
Saeed, A. et al. Incidence of vancomycin resistant phenotype of the methicillin resistant Staphylococcus aureus isolated from a tertiary care hospital. Antibiotics. 9 (1), 3 (2020).
doi: 10.3390/antibiotics9010003
Ghoniem, E. M., Moteleb, T. M. A., Hassan, H. A. & Khalil, H. A. E. R. Characterization of vancomycin-resistant Staphylococcus aureus in the National Liver Institute. Menoufia Med. J. 27(4):825 (2014).
Abdelghafar, A., Yousef, N. & Askoura, M. Zinc oxide nanoparticles reduce biofilm formation, synergize antibiotics action and attenuate Staphylococcus aureus virulence in host; An important message to clinicians. BMC Microbiol. 22, 244. https://doi.org/10.1186/s12866-022-02658-z (2022).
doi: 10.1186/s12866-022-02658-z
pubmed: 36221053
pmcid: 9552502
Sahal, G. et al. Antifungal and biofilm inhibitory effect of Cymbopogon citratus (lemongrass) essential oil on biofilm forming by Candida tropicalis isolates; An in vitro study. J. Ethnopharmacol. 246, 112188. https://doi.org/10.1016/j.jep.2019.112188 (2020).
doi: 10.1016/j.jep.2019.112188
pubmed: 31470085
Neopane, P., Nepal, H. P., Shrestha, R., Uehara, O. & Abiko, Y. In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance. Int. J. Gen. Med. 11, 25–32. https://doi.org/10.2147/ijgm.S153268 (2018).
doi: 10.2147/ijgm.S153268
pubmed: 29403304
pmcid: 5779313
Karki, S., Lamichhane, S. A., Maharjan, J., Sharma, A. & Rajbhandari, L. Biofilm formation and detection of icaD Gene in Staphylococcus aureus isolated from clinical specimens. Open. Microbiol. J. 13 (1), 12–17 (2019).
doi: 10.2174/1874285801913010230
Bimanand, L., Jalilian, T. M., Sadeghifard, F. A., Ghafourian, N. & Mahdavi, S. Z. Association between biofilm production, adhesion genes and drugs resistance in different SCCmec types of methicillin resistant Staphylococcus aureus strains isolated from several major hospitals of Iran. Iran. J. Basic Med. Sci. 21(4), 400 (2018).
Muniza Qayyum, B. & Ahmad Syed Nawazish-1-Hussain, Jamila Iqbal & Khan, A. H. The antimicrobial activity of different zinc salts. Proc. S.Z.P.G.M.I 12, 8–12 (1998).
Dalia, A. & Al-Saedi, F. Antibacterial effect of different concentrations of zinc sulfate on multidrug resistant pathogenic bacteria. Sys Rev. Pharm. 11, 282288 (2020).
Pati, R. et al. A. Topical application of zinc oxide nanoparticles reduces bacterial skin infection in mice and exhibits antibacterial activity by inducing oxidative stress response and cell membrane disintegration in macrophages. Nanomedicine. 10 (6), 1195–1208 (2014).
doi: 10.1016/j.nano.2014.02.012
pubmed: 24607937
Fatima, T., Abdul Rahim, H., Lin, Z. B., Qamar, Z. & C. W. & Zinc: A precious trace element for oral health care? J. Pak. Med. Assoc. 66, 1019–1023 (2016).
pubmed: 27524540
Phan, T. N., Buckner, T., Sheng, J., Baldeck, J. D. & Marquis, R. E. Physiologic actions of zinc related to inhibition of acid and alkali production by oral streptococci in suspensions and biofilms. Oral Microbiol. Immunol. 19, 31–38. https://doi.org/10.1046/j.0902-0055.2003.00109.x (2004).
doi: 10.1046/j.0902-0055.2003.00109.x
pubmed: 14678472
Almoudi, M. M., Hussein, A. S., Abu Hassan, M. I. & Mohamad Zain, N. A systematic review on antibacterial activity of zinc against Streptococcus mutans. Saudi Dent. J. 30, 283–291. https://doi.org/10.1016/j.sdentj.2018.06.003 (2018).
doi: 10.1016/j.sdentj.2018.06.003
pubmed: 30202164
pmcid: 6128804
Cheesbrough, M. District laboratory practice in tropical countries, part 2. Interactive effects of copper. Cambridge University Press, UK, Chap. (3), 63–70. (45) (Cheloni, G., Marti, E. & Slaveykova, V. I.) (2016).
CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 32nd Ed. (Clinical and Laboratory Standards Institute, 2022).
MoDBAoAAAG, C. L. S. I. Clinical and Laboratory Standard Institute Vol. 19(18). (1999).
Bellio, P., Fagnani, L., Nazzicone, L. & Celenza, G. New and simplified method for drug combination studies by checkerboard assay. MethodsX. 8, 101543. https://doi.org/10.1016/j.mex.2021.101543 (2021).
doi: 10.1016/j.mex.2021.101543
pubmed: 34754811
pmcid: 8563647
Stepanovic, S. et al. Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS. 115, 891–899. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x (2007).
doi: 10.1111/j.1600-0463.2007.apm_630.x
pubmed: 17696944
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402–408 https://doi.org/10.1006/meth.2001.1262 (2001).
Rauf, M. A. et al. Biomimetically synthesized ZnO nanoparticles attain potent antibacterial activity against less susceptible S. aureus skin infection in experimental animals. RSC Adv. 7, 36361–36373. https://doi.org/10.1039/C7RA05040B (2017).
doi: 10.1039/C7RA05040B