Antibacterial and antibiofilm activities of zingerone and niosomal zingerone against methicillin-resistant Staphylococcus aureus (MRSA)
,
Abstract
Background and Objectives: Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of nosocomial and community acquired infections. Nanoparticles are considered as proper tools to overcome the therapeutic problem of antimicrobial-resistant infections because of the drug concentration increment at the desired location and protection from enzymatic degradation. The goal of this study was to evaluate the effect of the antibacterial and antibiofilm activities of zingerone and niosome containing zingerone against pre-formed biofilm of MRSA isolates.
Materials and Methods: 62 MRSA isolates cultured from patients with diabetic ulcers were investigated. Niosomes were synthesized and characterized by X- ray diffraction, zeta potential and scanning electron microscopy (SEM). The size of niosomal particles measured by SEM and zetasizer.
Results: The surface charge of prepared niosomes was about -37 mV. The effect of the zingerone and noisome containing zingerone was evaluated against biofilms of MRSA isolates. Also, the antibiofilm activity of prepared niosomes on gene expression of MRSA biofilms was evaluated using Real Time PCR. Our results demonstrated that the niosome containing zingerone had a diameter of 196.1 nm and a -37.3-mV zeta potential. Zingerone removed one and three-day old biofilms of MRSA at the concentration of 1000 µg/ml, while the zingerone-laoded niosomes removed 1, 3- and 5-days old biofilms at the concentration of 250 µg/ml, 250 µg/ml, and 500 µg/ml.
Conclusion: The results indicated that niosome containing zingerone eliminated MRSA and its biofilms faster compared with free zingerone and it suggested that zingerone-encapsulated niosomes could be considered as a promising treatment against MRSA and its biofilms.
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2. Petrelli D, Repetto A, D'Ercole S, Rombini S, Ripa S, Prenna M, et al. Analysis of meticillin-susceptible and meticillin-resistant biofilm-forming Staphylococcus aureus from catheter infections isolated in a large Italian hospital. J Med Microbiol 2008; 57: 364-372.
3. Shafiei M, Abdi-Ali A, Shahcheraghi F, Vali H, Shahbani Zahiri H, Akbari Noghabi K. Analysis of Pseudomonas aeruginosa PAO1 biofilm protein profile after exposure to n-butanolic Cyclamen coum extract alone and in combination with ciprofloxacin. Appl Biochem Biotechnol 2017; 182: 1444-1457.
4. Safaei M, Maleki H, Soleimanpour H, Norouzy A, Zahiri HS, Vali H, et al. Development of a novel method for the purification of C-phycocyanin pigment from a local cyanobacterial strain Limnothrix sp. NS01 and evaluation of its anticancer properties. Sci Rep 2019; 9: 9474.
5. Namvar AE, Asghari B, Ezzatifar F, Azizi G, Lari AR. Detection of the intercellular adhesion gene cluster (ica) in clinical Staphylococcus aureus isolates. GMS Hyg Infect Control 2013; 8: Doc03.
6. Gad GF, El-Feky MA, El-Rehewy MS, Hassan MA, Abolella H, El-Baky RM. Detection of icaA, icaD genes and biofilm production by Staphylococcus aureus and Staphylococcus epidermidis isolated from urinary tract catheterized patients. J Infect Dev Ctries 2009; 3: 342-351.
7. Vallet I, Olson JW, Lory S, Lazdunski A, Filloux A. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc Natl Acad Sci U S A 2001; 98: 6911-6916.
8. Choi Y-S, Kim C, Moon J-H, Lee J-Y. Removal and killing of multispecies endodontic biofilms by N-acetylcysteine. Braz J Microbiol 2018; 49: 184-188.
9. Tavano L, Gentile L, Oliviero Rossi C, Muzzalupo R. Novel gel-niosomes formulations as multicomponent systems for transdermal drug delivery. Colloids Surf B Biointerfaces 2013; 110: 281-288.
10. Aparajay P, Dev A. Functionalized niosomes as a smart delivery device in cancer and fungal infection. Eur J Pharm Sci 2022; 168: 106052.
11. Ahmad B, Rehman MU, Amin I, Ahmad SB, Farooq A, Muzamil S, et al. Zingerone (4-(4-hydroxy-3-methylphenyl) butan-2-one) protects against alloxan-induced diabetes via alleviation of oxidative stress and inflammation: probable role of NF-kB activation. Saudi Pharm J 2018; 26: 1137-1145.
12. Shamsabadi S, Nazer Y, Ghasemi J, Mahzoon E, Rahimi VB, Ajiboye BO, et al. Promising influences of zingerone against natural and chemical toxins: A comprehensive and mechanistic review. Toxicon 2023; 233: 107247.
13. Seth AK, Geringer MR, Nguyen KT, Agnew SP, Dumanian Z, Galiano RD, et al. Bacteriophage therapy for Staphylococcus aureus biofilm–infected wounds: a new approach to chronic wound care. Plast Reconstr Surg 2013; 131: 225-234.
14. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st Edition. J Clin Microbiol 2021; 59(12): e0021321.
15. Shafiei M, Abdi Ali A, Shahcheraghi F, Saboora A, Akbari Noghabi K. Eradication of Pseudomonas aeruginosa biofilms using the combination of n-butanolic cyclamen coum extract and ciprofloxacin. Jundishapur J Microbiol 2014; 7(2): e14358.
16. Kim M-H, Yamayoshi I, Mathew S, Lin H, Nayfach J, Simon SI. Magnetic nanoparticle targeted hyperthermia of cutaneous Staphylococcus aureus infection. Ann Biomed Eng 2013; 41: 598-609.
17. Antunes BP, Moreira AF, Gaspar VM, Correia IJ. Chitosan/arginine–chitosan polymer blends for assembly of nanofibrous membranes for wound regeneration. Carbohydr Polym 2015; 130: 104-112.
18. Zafari M, Adibi M, Chiani M, Bolourchi N, Barzi SM, Shams Nosrati MS, et al. Effects of cefazolin-containing niosome nanoparticles against methicillin-resistant Staphylococcus aureus biofilm formed on chronic wounds. Biomed Mater 2021; 16: 035001.
19. Shamkani F, Barzi SM, Badmasti F, Chiani M, Mirabzadeh E, Zafari M, et al. Enhanced anti-biofilm activity of the minocycline-and-gallium-nitrate using niosome wrapping against Acinetobacter baumannii in C57/BL6 mouse pneumonia model. Int Immunopharmacol 2023; 115: 109551.
20. Jacob S, Nair AB, Al-Dhubiab BE. Preparation and evaluation of niosome gel containing acyclovir for enhanced dermal deposition. J Liposome Res 2017; 27: 283-292.
21. Sabaeifard P, Abdi-Ali A, Soudi MR, Dinarvand R. Optimization of tetrazolium salt assay for Pseudomonas aeruginosa biofilm using microtiter plate method. J Microbiol Methods 2014; 105: 134-140.
22. Petit T, Puskar L. FTIR spectroscopy of nanodiamonds: Methods and interpretation. Diam Relat Mater 2018; 89: 52-66.
23. Faghihzadeh F, Anaya NM, Schifman LA, Oyanedel-Craver V. Fourier transform infrared spectroscopy to assess molecular-level changes in microorganisms exposed to nanoparticles. Nanotechnol Environ Eng 2016; 1: 1-16.
24. Wiegand I, Hilpert K, Hancock RE. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 2008; 3: 163-175.
25. Robertson J, McGoverin C, White JR, Vanholsbeeck F, Swift S. Rapid detection of Escherichia coli antibiotic susceptibility using live/dead spectrometry for lytic agents. Microorganisms 2021; 9: 924.
26. Thammawithan S, Siritongsuk P, Nasompag S, Daduang S, Klaynongsruang S, Prapasarakul N, et al. A biological study of anisotropic silver nanoparticles and their antimicrobial application for topical use. Vet Sci 2021; 8: 177.
27. Gopalakrishnan S, Gupta A, Makabenta JMV, Park J, Amante JJ, Chattopadhyay AN, et al. Ultrasound‐enhanced antibacterial activity of polymeric nanoparticles for eradicating bacterial biofilms. Adv Healthc Mater 2022; 11(21): e2201060.
28. Allkja J, van Charante F, Aizawa J, Reigada I, Guarch-Perez C, Vazquez-Rodriguez JA, et al. Interlaboratory study for the evaluation of three microtiter plate-based biofilm quantification methods. Sci Rep 2021; 11: 13779.
29. Atshan SS, Shamsudin MN, Karunanidhi A, Van Belkum A, Lung LT, Sekawi Z, et al. Quantitative PCR analysis of genes expressed during biofilm development of methicillin resistant Staphylococcus aureus (MRSA). Infect Genet Evol 2013; 18: 106-112.
30. Afreen U, Fahelelbom KM, Shah SNH, Ashames A, Almas U, Khan SA, et al. Formulation and evaluation of niosomes-based chlorpheniramine gel for the treatment of mild to moderate skin allergy. J Exp Nanosci 2022; 17: 467-495.
31. Hosseini M, Shapouri Moghaddam A, Derakhshan S, Hashemipour SMA, Hadadi-Fishani M, Pirouzi A, et al. Correlation between biofilm formation and antibiotic resistance in MRSA and MSSA isolated from clinical samples in Iran: a systematic review and meta-analysis. Microb Drug Resist 2020; 26: 1071-1080.
32. Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 2021; 12: 547-569.
33. Tocco I, Zavan B, Bassetto F, Vindigni V. Nanotechnology-based therapies for skin wound regeneration. J Nanomater 2012; 2012: 11.
34. Hedayati Ch M, Abolhassani Targhi A, Shamsi F, Heidari F, Salehi Moghadam Z, Mirzaie A, et al. Niosome‐encapsulated tobramycin reduced antibiotic resistance and enhanced antibacterial activity against multidrug‐resistant clinical strains of Pseudomonas aeruginosa. J Biomed Mater Res A 2021; 109: 966-980.
35. Shah P, Goodyear B, Dholaria N, Puri V, Michniak-Kohn B. Nanostructured non-ionic surfactant carrier-based gel for topical delivery of desoximetasone. Int J Mol Sci 2021; 22: 1535.
36. Ahmad B, Rehman MU, Amin I, Arif A, Rasool S, Bhat SA, et al. A review on pharmacological properties of zingerone (4-(4-Hydroxy-3-methoxyphenyl)-2-butanone). ScientificWorldJournal 2015; 2015: 816364.
37. Madsen JS, Burmølle M, Hansen LH, Sørensen SJ. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol 2012; 65: 183-195.
38. Abdelaziz AA, Elbanna TE, Sonbol FI, Gamaleldin NM, El Maghraby GM. Optimization of niosomes for enhanced antibacterial activity and reduced bacterial resistance: in vitro and in vivo evaluation. Expert Opin Drug Deliv 2015; 12: 163-180.
39. Junyaprasert VB, Teeranachaideekul V, Supaperm T. Effect of charged and non-ionic membrane additives on physicochemical properties and stability of niosomes. AAPS PharmSciTech 2008; 9: 851-859.
40. Khan DH, Bashir S, Figueiredo P, Santos HA, Khan MI, Peltonen L. Process optimization of ecological probe sonication technique for production of rifampicin loaded niosomes. J Drug Deliv Technol 2019; 50: 27-33.
41. Barakat HS, Kassem MA, El-Khordagui LK, Khalafallah NM. Vancomycin-eluting niosomes: a new approach to the inhibition of staphylococcal biofilm on abiotic surfaces. AAPS PharmSciTech 2014; 15: 1263-1274.
42. Rahimipour S, Salahinejad E, Sharifi E, Nosrati H, Tayebi L. Structure, wettability, corrosion and biocompatibility of nitinol treated by alkaline hydrothermal and hydrophobic functionalization for cardiovascular applications. Appl Surf Sci 2020; 506: 144657.
43. Kashef MT, Saleh NM, Assar NH, Ramadan MA. The antimicrobial activity of ciprofloxacin-loaded niosomes against ciprofloxacin-resistant and biofilm-forming Staphylococcus aureus. Infect Drug Res 2020; 13: 1619-1629.
2. Petrelli D, Repetto A, D'Ercole S, Rombini S, Ripa S, Prenna M, et al. Analysis of meticillin-susceptible and meticillin-resistant biofilm-forming Staphylococcus aureus from catheter infections isolated in a large Italian hospital. J Med Microbiol 2008; 57: 364-372.
3. Shafiei M, Abdi-Ali A, Shahcheraghi F, Vali H, Shahbani Zahiri H, Akbari Noghabi K. Analysis of Pseudomonas aeruginosa PAO1 biofilm protein profile after exposure to n-butanolic Cyclamen coum extract alone and in combination with ciprofloxacin. Appl Biochem Biotechnol 2017; 182: 1444-1457.
4. Safaei M, Maleki H, Soleimanpour H, Norouzy A, Zahiri HS, Vali H, et al. Development of a novel method for the purification of C-phycocyanin pigment from a local cyanobacterial strain Limnothrix sp. NS01 and evaluation of its anticancer properties. Sci Rep 2019; 9: 9474.
5. Namvar AE, Asghari B, Ezzatifar F, Azizi G, Lari AR. Detection of the intercellular adhesion gene cluster (ica) in clinical Staphylococcus aureus isolates. GMS Hyg Infect Control 2013; 8: Doc03.
6. Gad GF, El-Feky MA, El-Rehewy MS, Hassan MA, Abolella H, El-Baky RM. Detection of icaA, icaD genes and biofilm production by Staphylococcus aureus and Staphylococcus epidermidis isolated from urinary tract catheterized patients. J Infect Dev Ctries 2009; 3: 342-351.
7. Vallet I, Olson JW, Lory S, Lazdunski A, Filloux A. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc Natl Acad Sci U S A 2001; 98: 6911-6916.
8. Choi Y-S, Kim C, Moon J-H, Lee J-Y. Removal and killing of multispecies endodontic biofilms by N-acetylcysteine. Braz J Microbiol 2018; 49: 184-188.
9. Tavano L, Gentile L, Oliviero Rossi C, Muzzalupo R. Novel gel-niosomes formulations as multicomponent systems for transdermal drug delivery. Colloids Surf B Biointerfaces 2013; 110: 281-288.
10. Aparajay P, Dev A. Functionalized niosomes as a smart delivery device in cancer and fungal infection. Eur J Pharm Sci 2022; 168: 106052.
11. Ahmad B, Rehman MU, Amin I, Ahmad SB, Farooq A, Muzamil S, et al. Zingerone (4-(4-hydroxy-3-methylphenyl) butan-2-one) protects against alloxan-induced diabetes via alleviation of oxidative stress and inflammation: probable role of NF-kB activation. Saudi Pharm J 2018; 26: 1137-1145.
12. Shamsabadi S, Nazer Y, Ghasemi J, Mahzoon E, Rahimi VB, Ajiboye BO, et al. Promising influences of zingerone against natural and chemical toxins: A comprehensive and mechanistic review. Toxicon 2023; 233: 107247.
13. Seth AK, Geringer MR, Nguyen KT, Agnew SP, Dumanian Z, Galiano RD, et al. Bacteriophage therapy for Staphylococcus aureus biofilm–infected wounds: a new approach to chronic wound care. Plast Reconstr Surg 2013; 131: 225-234.
14. Humphries R, Bobenchik AM, Hindler JA, Schuetz AN. Overview of changes to the clinical and laboratory standards institute performance standards for antimicrobial susceptibility testing, M100, 31st Edition. J Clin Microbiol 2021; 59(12): e0021321.
15. Shafiei M, Abdi Ali A, Shahcheraghi F, Saboora A, Akbari Noghabi K. Eradication of Pseudomonas aeruginosa biofilms using the combination of n-butanolic cyclamen coum extract and ciprofloxacin. Jundishapur J Microbiol 2014; 7(2): e14358.
16. Kim M-H, Yamayoshi I, Mathew S, Lin H, Nayfach J, Simon SI. Magnetic nanoparticle targeted hyperthermia of cutaneous Staphylococcus aureus infection. Ann Biomed Eng 2013; 41: 598-609.
17. Antunes BP, Moreira AF, Gaspar VM, Correia IJ. Chitosan/arginine–chitosan polymer blends for assembly of nanofibrous membranes for wound regeneration. Carbohydr Polym 2015; 130: 104-112.
18. Zafari M, Adibi M, Chiani M, Bolourchi N, Barzi SM, Shams Nosrati MS, et al. Effects of cefazolin-containing niosome nanoparticles against methicillin-resistant Staphylococcus aureus biofilm formed on chronic wounds. Biomed Mater 2021; 16: 035001.
19. Shamkani F, Barzi SM, Badmasti F, Chiani M, Mirabzadeh E, Zafari M, et al. Enhanced anti-biofilm activity of the minocycline-and-gallium-nitrate using niosome wrapping against Acinetobacter baumannii in C57/BL6 mouse pneumonia model. Int Immunopharmacol 2023; 115: 109551.
20. Jacob S, Nair AB, Al-Dhubiab BE. Preparation and evaluation of niosome gel containing acyclovir for enhanced dermal deposition. J Liposome Res 2017; 27: 283-292.
21. Sabaeifard P, Abdi-Ali A, Soudi MR, Dinarvand R. Optimization of tetrazolium salt assay for Pseudomonas aeruginosa biofilm using microtiter plate method. J Microbiol Methods 2014; 105: 134-140.
22. Petit T, Puskar L. FTIR spectroscopy of nanodiamonds: Methods and interpretation. Diam Relat Mater 2018; 89: 52-66.
23. Faghihzadeh F, Anaya NM, Schifman LA, Oyanedel-Craver V. Fourier transform infrared spectroscopy to assess molecular-level changes in microorganisms exposed to nanoparticles. Nanotechnol Environ Eng 2016; 1: 1-16.
24. Wiegand I, Hilpert K, Hancock RE. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 2008; 3: 163-175.
25. Robertson J, McGoverin C, White JR, Vanholsbeeck F, Swift S. Rapid detection of Escherichia coli antibiotic susceptibility using live/dead spectrometry for lytic agents. Microorganisms 2021; 9: 924.
26. Thammawithan S, Siritongsuk P, Nasompag S, Daduang S, Klaynongsruang S, Prapasarakul N, et al. A biological study of anisotropic silver nanoparticles and their antimicrobial application for topical use. Vet Sci 2021; 8: 177.
27. Gopalakrishnan S, Gupta A, Makabenta JMV, Park J, Amante JJ, Chattopadhyay AN, et al. Ultrasound‐enhanced antibacterial activity of polymeric nanoparticles for eradicating bacterial biofilms. Adv Healthc Mater 2022; 11(21): e2201060.
28. Allkja J, van Charante F, Aizawa J, Reigada I, Guarch-Perez C, Vazquez-Rodriguez JA, et al. Interlaboratory study for the evaluation of three microtiter plate-based biofilm quantification methods. Sci Rep 2021; 11: 13779.
29. Atshan SS, Shamsudin MN, Karunanidhi A, Van Belkum A, Lung LT, Sekawi Z, et al. Quantitative PCR analysis of genes expressed during biofilm development of methicillin resistant Staphylococcus aureus (MRSA). Infect Genet Evol 2013; 18: 106-112.
30. Afreen U, Fahelelbom KM, Shah SNH, Ashames A, Almas U, Khan SA, et al. Formulation and evaluation of niosomes-based chlorpheniramine gel for the treatment of mild to moderate skin allergy. J Exp Nanosci 2022; 17: 467-495.
31. Hosseini M, Shapouri Moghaddam A, Derakhshan S, Hashemipour SMA, Hadadi-Fishani M, Pirouzi A, et al. Correlation between biofilm formation and antibiotic resistance in MRSA and MSSA isolated from clinical samples in Iran: a systematic review and meta-analysis. Microb Drug Resist 2020; 26: 1071-1080.
32. Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 2021; 12: 547-569.
33. Tocco I, Zavan B, Bassetto F, Vindigni V. Nanotechnology-based therapies for skin wound regeneration. J Nanomater 2012; 2012: 11.
34. Hedayati Ch M, Abolhassani Targhi A, Shamsi F, Heidari F, Salehi Moghadam Z, Mirzaie A, et al. Niosome‐encapsulated tobramycin reduced antibiotic resistance and enhanced antibacterial activity against multidrug‐resistant clinical strains of Pseudomonas aeruginosa. J Biomed Mater Res A 2021; 109: 966-980.
35. Shah P, Goodyear B, Dholaria N, Puri V, Michniak-Kohn B. Nanostructured non-ionic surfactant carrier-based gel for topical delivery of desoximetasone. Int J Mol Sci 2021; 22: 1535.
36. Ahmad B, Rehman MU, Amin I, Arif A, Rasool S, Bhat SA, et al. A review on pharmacological properties of zingerone (4-(4-Hydroxy-3-methoxyphenyl)-2-butanone). ScientificWorldJournal 2015; 2015: 816364.
37. Madsen JS, Burmølle M, Hansen LH, Sørensen SJ. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol 2012; 65: 183-195.
38. Abdelaziz AA, Elbanna TE, Sonbol FI, Gamaleldin NM, El Maghraby GM. Optimization of niosomes for enhanced antibacterial activity and reduced bacterial resistance: in vitro and in vivo evaluation. Expert Opin Drug Deliv 2015; 12: 163-180.
39. Junyaprasert VB, Teeranachaideekul V, Supaperm T. Effect of charged and non-ionic membrane additives on physicochemical properties and stability of niosomes. AAPS PharmSciTech 2008; 9: 851-859.
40. Khan DH, Bashir S, Figueiredo P, Santos HA, Khan MI, Peltonen L. Process optimization of ecological probe sonication technique for production of rifampicin loaded niosomes. J Drug Deliv Technol 2019; 50: 27-33.
41. Barakat HS, Kassem MA, El-Khordagui LK, Khalafallah NM. Vancomycin-eluting niosomes: a new approach to the inhibition of staphylococcal biofilm on abiotic surfaces. AAPS PharmSciTech 2014; 15: 1263-1274.
42. Rahimipour S, Salahinejad E, Sharifi E, Nosrati H, Tayebi L. Structure, wettability, corrosion and biocompatibility of nitinol treated by alkaline hydrothermal and hydrophobic functionalization for cardiovascular applications. Appl Surf Sci 2020; 506: 144657.
43. Kashef MT, Saleh NM, Assar NH, Ramadan MA. The antimicrobial activity of ciprofloxacin-loaded niosomes against ciprofloxacin-resistant and biofilm-forming Staphylococcus aureus. Infect Drug Res 2020; 13: 1619-1629.
| Files | ||
| Issue | Vol 16 No 3 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i3.15794 | |
| Keywords | ||
| Niosomes; Zingerone; Biofilm; Methicillin resistant Staphylococcus aureus | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Larijanian L, Shafiei M, Ghasemi Pirbalouti A, Ferdousi A, Chiani M. Antibacterial and antibiofilm activities of zingerone and niosomal zingerone against methicillin-resistant Staphylococcus aureus (MRSA). Iran J Microbiol. 2024;16(3):366-375.
