Effectiveness of co-cultured Myristica fragrans Houtt. seed extracts with commensal Staphylococcus epidermidis and its metabolites in antimicrobial activity and biofilm formation of skin pathogenic bacteria.
Antimicrobial peptides
Biofilm formation
Essential oil
Nutmeg
Short-chain fatty acids
Journal
BMC complementary medicine and therapies
ISSN: 2662-7671
Titre abrégé: BMC Complement Med Ther
Pays: England
ID NLM: 101761232
Informations de publication
Date de publication:
31 Oct 2024
31 Oct 2024
Historique:
received:
13
06
2024
accepted:
07
10
2024
medline:
1
11
2024
pubmed:
1
11
2024
entrez:
1
11
2024
Statut:
epublish
Résumé
Skin commensal bacteria (Staphylococcus epidermidis) can help defend against skin infections, and they are increasingly being recognized for their role in benefiting skin health. This study aims to demonstrate the activities that Myristica fragrans Houtt. seed extracts, crude extract (CE) and essential oil (EO), have in terms of promoting the growth of the skin commensal bacterium S. epidermidis and providing metabolites under culture conditions to disrupt the biofilm formation of the common pathogen Staphylococcus aureus. The culture supernatant obtained from a co-culture of S. epidermidis with M. fragrans Houtt. seed extracts in either CE or EO forms were analyzed using gas chromatography-mass spectrometry (GC-MS) and liquid chromatography tandem mass spectrometry (LC-MS/MS), in silico investigations, and applied to assess the survival and biofilm formation of S. aureus. The combination of commensal bacteria with M. fragrans Houtt. seed extract either CE or EO produced metabolic compounds such as short-chain fatty acids and antimicrobial peptides, contributing to the antimicrobial activity. This antimicrobial activity was related to downregulating key genes involved in bacterial adherence and biofilm development in S. aureus, including cna, agr, and fnbA. These findings suggest that using the culture supernatant of the commensal bacteria in combination with CE or EO may provide a potential approach to combat biofilm formation and control the bacterial proliferation of S. aureus. This may be a putative non-invasive therapeutic strategy for maintaining a healthy skin microbiota and preventing skin infections.
Sections du résumé
BACKGROUND
BACKGROUND
Skin commensal bacteria (Staphylococcus epidermidis) can help defend against skin infections, and they are increasingly being recognized for their role in benefiting skin health. This study aims to demonstrate the activities that Myristica fragrans Houtt. seed extracts, crude extract (CE) and essential oil (EO), have in terms of promoting the growth of the skin commensal bacterium S. epidermidis and providing metabolites under culture conditions to disrupt the biofilm formation of the common pathogen Staphylococcus aureus.
METHODS
METHODS
The culture supernatant obtained from a co-culture of S. epidermidis with M. fragrans Houtt. seed extracts in either CE or EO forms were analyzed using gas chromatography-mass spectrometry (GC-MS) and liquid chromatography tandem mass spectrometry (LC-MS/MS), in silico investigations, and applied to assess the survival and biofilm formation of S. aureus.
RESULTS
RESULTS
The combination of commensal bacteria with M. fragrans Houtt. seed extract either CE or EO produced metabolic compounds such as short-chain fatty acids and antimicrobial peptides, contributing to the antimicrobial activity. This antimicrobial activity was related to downregulating key genes involved in bacterial adherence and biofilm development in S. aureus, including cna, agr, and fnbA.
CONCLUSION
CONCLUSIONS
These findings suggest that using the culture supernatant of the commensal bacteria in combination with CE or EO may provide a potential approach to combat biofilm formation and control the bacterial proliferation of S. aureus. This may be a putative non-invasive therapeutic strategy for maintaining a healthy skin microbiota and preventing skin infections.
Identifiants
pubmed: 39482677
doi: 10.1186/s12906-024-04675-z
pii: 10.1186/s12906-024-04675-z
doi:
Substances chimiques
Plant Extracts
0
Anti-Bacterial Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
380Subventions
Organisme : The Fundamental Fund of Khon Kaen University
ID : PR65-1-Immune-001
Organisme : The Research and Academic Services, Khon Kaen University through Research Program Year 2022
ID : PR65-311 1-002
Informations de copyright
© 2024. The Author(s).
Références
Carmona-Cruz S, Orozco-Covarrubias L, Sáez-de-Ocariz M. The human skin microbiome in selected cutaneous diseases. Front Cell Infect Microbiol. 2022;12:834135. https://doi.org/10.3389/fcimb.2022.834135 .
doi: 10.3389/fcimb.2022.834135
pubmed: 35321316
pmcid: 8936186
Christensen GJ, Brüggemann H. Bacterial skin commensals and their role as host guardians. Benef Microbes. 2014;5(2):201–15. https://doi.org/10.3920/BM2012.0062 .
doi: 10.3920/BM2012.0062
pubmed: 24322878
Liu Q, Liu Q, Meng H, Lv H, Liu Y, Liu J, et al. Staphylococcus epidermidis contributes to healthy maturation of the nasal microbiome by stimulating antimicrobial peptide production. Cell Host Microbe. 2020;27(1):6878. https://doi.org/10.1016/j.chom.2019.11.003 .
doi: 10.1016/j.chom.2019.11.003
Cheung GY, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence. 2021;12(1):547–69. https://doi.org/10.1080/21505594.2021.1878688 .
doi: 10.1080/21505594.2021.1878688
pubmed: 33522395
pmcid: 7872022
Gnanamani A, Hariharan P, PaulSatyaseela M. Staphylococcus aureus: Overview of bacteriology, clinical diseases, epidemiology, antibiotic resistance and therapeutic approach [Internet]. Frontiers in Staphylococcus aureus. InTech. 2017;4(28):10–5772. https://doi.org/10.5772/67338 .
doi: 10.5772/67338
Glatthardt T, Campos JC, Chamon RC, de Sá Coimbra TF, Rocha GD, de Melo MA, et al. Small molecules produced by commensal Staphylococcus epidermidis disrupt formation of biofilms by Staphylococcus aureus. Appl Environ Microbiol. 2020;86(5):e02539–19. https://doi.org/10.1128/AEM.02539-19 .
doi: 10.1128/AEM.02539-19
pubmed: 31862721
pmcid: 7028967
World Health Organization. 2020 antibacterial agents in clinical and preclinical development: an overview and analysis. 2021. https://www.who.int/publications/i/item/9789240021303 . Accessed on 16 Jan 2024.
Konwar AN, Hazarika SN, Bharadwaj P, Thakur D. Emerging nontraditional approaches to combat antibiotic resistance. Curr Microbiol. 2022;79(11):330. https://doi.org/10.1007/s00284-022-03029-7 .
doi: 10.1007/s00284-022-03029-7
pubmed: 36155858
pmcid: 9510247
Huang Y, Huang J, Chen Y. Alphahelical cationic antimicrobial peptides: relationships of structure and function. Protein Cell. 2010;1:143 – 52. https://doi.org/10.1007/s13238-010-0004-3
Subbalakshmi C, Nagaraj R, Sitaram N. Biological activities of C-terminal 15-residue synthetic fragment of melittin: design of an analog with improved antibacterial activity. FEBS Lett. 1999;448(1):62–6. https://doi.org/10.1016/S0014-5793(99)00328-2 .
doi: 10.1016/S0014-5793(99)00328-2
pubmed: 10217411
Jiang Z, Vasil AI, Hale JD, Hancock RE, Vasil ML, Hodges RS. Effects of net charge and the number of positively charged residues on the biological activity of amphipathic α-helical cationic antimicrobial peptides. Pept Sci. 2008;90(3):369–83. https://doi.org/10.1002/bip.20911 .
doi: 10.1002/bip.20911
Oren Z, Shai Y. A class of highly potent antibacterial peptides derived from pardaxin, a pore-forming peptide isolated from Moses sole fish Pardachirus marmoratus. Eur J Biochem. 1996;237(1):303–10. https://doi.org/10.1111/j.1432-1033.1996.0303n.x .
doi: 10.1111/j.1432-1033.1996.0303n.x
pubmed: 8620888
Tossi A, Sandri L, Giangaspero A. Amphipathic, α-helical antimicrobial peptides. Pept Sci. 2000;55(1):4–30. https://doi.org/10.1002/1097-0282(2000)55:1%3C4::AID-BIP30%3E3.0.CO;2-M .
doi: 10.1002/1097-0282(2000)55:1<4::AID-BIP30>3.0.CO;2-M
Chen Y, Mant CT, Farmer SW, Hancock RE, Vasil ML, Hodges RS. Rational design of α-helical antimicrobial peptides with enhanced activities and specificity/therapeutic index. J Biol Chem. 2005;280(13):12316–29. https://doi.org/10.1074/jbc.M413406200 .
doi: 10.1074/jbc.M413406200
pubmed: 15677462
Bahar AA, Ren D. Antimicrobial peptides. Pharmaceuticals. 2013;6(12):1543–75. https://doi.org/10.3390/ph6121543 .
doi: 10.3390/ph6121543
pubmed: 24287494
pmcid: 3873676
Otto M. Bacterial evasion of antimicrobial peptides by biofilm formation. In: Shafer WM, editors. Antimicrobial peptides and human disease. Current topics in microbiology and immunology, vol 306. Springer, Berlin: Heidelberg; 2006. pp. 251-8. https://doi.org/10.1007/3-540-29916-5_10
Shu M, Wang Y, Yu J, Kuo S, Coda A, Jiang Y, et al. Fermentation of Propionibacterium acnes, a commensal bacterium in the human skin microbiome, as skin probiotics against methicillinresistant Staphylococcus aureus. PLoS ONE. 2013;8(2):e55380. https://doi.org/10.1371/journal.pone.0055380 .
doi: 10.1371/journal.pone.0055380
pubmed: 23405142
pmcid: 3566139
Huang TY, Jiang YE, Scott DA. Culturable bacteria in the entire acne lesion and short-chain fatty acid metabolites of Cutibacterium acnes and Staphylococcus epidermidis isolates. Biochem Biophys Res Commun. 2022;622:45–9. https://doi.org/10.1016/j.bbrc.2022.06.068 .
doi: 10.1016/j.bbrc.2022.06.068
pubmed: 35843093
Asgarpanah J, Kazemivash N. Phytochemistry and pharmacologic properties of Myristica fragrans Hoyutt.: a review. Afr J Biotechnol. 2012;11(65):12787–93. https://doi.org/10.5897/ajb12.1043 .
doi: 10.5897/ajb12.1043
Van Gils C, Cox PA. Ethnobotany of nutmeg in the Spice Islands. J Ethnopharmacol. 1994;42(2):117–. https://doi.org/10.1016/0378-8741(94)90105-8 . 24.
doi: 10.1016/0378-8741(94)90105-8
pubmed: 8072304
Ashokkumar K, Simal-Gandara J, Murugan M, Dhanya MK, Pandian A. Nutmeg (Myristica fragrans Houtt.) Essential oil: a review on its composition, biological, and pharmacological activities. Phytother Res. 2022;36(7):2839–51. https://doi.org/10.1002/ptr.7491 .
doi: 10.1002/ptr.7491
pubmed: 35567294
pmcid: 9541156
Dzotam JK, Kuete V. Myristica fragrans as a potential source of antibacterial agents. In: Victor K, editor. Adv Bot Res. Academic; 2023. pp. 213–37. https://doi.org/10.1016/bs.abr.2022.08.017 .
Jaiswal P, Kumar P, Singh VK, Singh DK. Biological effects of Myristica fragrans. Annu Rev Biomed Sci. 2009;11:21–9. https://doi.org/10.5016/1806-8774.2009v11p21 .
doi: 10.5016/1806-8774.2009v11p21
Naeem N, Rehman R, Mushtaq A, Ghania JB. Nutmeg: a review on uses and biological properties. Int J Chem Biochem Sci. 2016;9:107–10.
Ansory HM, Fitriani IN, Nilawatii A. Chemical separation and antibacterial activity of nutmeg seed essential oil against Shigella sp. and Escherichia coli ATCC 25922. IOP conf ser: Mater Sci Eng. IOP Publishing; 2020. p. 012005. https://doi.org/10.1088/1757-899X/846/1/012005 .
Gupta AD, Bansal VK, Babu V, Maithil N. Chemistry, antioxidant and antimicrobial potential of nutmeg (Myristica fragrans Houtt). J Genet Eng Biotechnol. 2013;11(1):25–31. https://doi.org/10.1016/j.jgeb.2012.12.001 .
doi: 10.1016/j.jgeb.2012.12.001
Matulyte I, Jekabsone A, Jankauskaite L, Zavistanaviciute P, Sakiene V, Bartkiene E, et al. The essential oil and hydrolats from Myristica fragrans seeds with magnesium aluminometasilicate as excipient: antioxidant, antibacterial, and antiinflammatory activity. Foods. 2020;9(1):37. https://doi.org/10.3390/foods9010037 .
doi: 10.3390/foods9010037
pubmed: 31906495
pmcid: 7022514
Morita T, Jinno K, Kawagishi H, Arimoto Y, Suganuma H, Inakuma T, et al. Hepatoprotective effect of myristicin from nutmeg (Myristica fragrans) on lipopolysaccharide/dgalactosamineinduced liver injury. J Agric Food Chem. 2003;51(6):1560–5. https://doi.org/10.1021/jf020946n .
Oo T, Saiboonjan B, Srijampa S, Srisrattakarn A, Sutthanut K, Tavichakorntrakool R, et al. Inhibition of bacterial efflux pumps by crude extracts and essential oil from Myristica fragrans Houtt. (nutmeg) seeds against methicillinresistant Staphylococcus aureus. Molecules. 2021;26(15):4662. https://doi.org/10.3390/molecules26154662 .
doi: 10.3390/molecules26154662
pubmed: 34361815
pmcid: 8348620
Al-Mariri A, Safi M. In vitro antibacterial activity of several plant extracts and oils against some gram-negative bacteria. Iran J Med Sci. 2014;39(1):36.
pubmed: 24453392
pmcid: 3895893
Weinstein M. M100 Performance standards for Antimicrobial susceptibility testing. J Serv Mark. 2021;59(12):e00213–21.
Su P, Henriksson A, Nilsson C, Mitchell H. Synergistic effect of green tea extract and probiotics on the pathogenic bacteria, Staphylococcus aureus and Streptococcus pyogenes. World J Microbiol Biotechnol. 2008;24:1837–42. https://doi.org/10.1007/s11274-008-9682x .
doi: 10.1007/s11274-008-9682x
Roytrakul S, Jaresitthikunchai J, Phaonakrop N, Charoenlappanit S, Thaisakun S, Kumsri N, Arpornsuwan T. Secretomic changes of amyloid beta peptides on Alzheimer’s disease related proteins in differentiated human SH-SY5Y neuroblastoma cells. PeerJ. 2024;12:e17732. https://doi.org/10.7717/peerj.17732 . PMID: 39035166; PMCID: PMC11260076.
doi: 10.7717/peerj.17732
pubmed: 39035166
pmcid: 11260076
Sakarin S, Rungsipipat A, Roytrakul S, Jaresitthikunchai J, Phaonakrop N, Charoenlappanit S, et al. Proteomic analysis of pulmonary arteries and lung tissues from dogs affected with pulmonary hypertension secondary to degenerative mitral valve disease. PLoS ONE. 2024;19(1):e0296068. https://doi.org/10.1371/journal.pone.0296068 .
doi: 10.1371/journal.pone.0296068
pubmed: 38181036
pmcid: 10769092
Waghu FH, Gopi L, Barai RS, Ramteke P, Nizami B, Idicula-Thomas S. CAMP: Collection of sequences and structures of antimicrobial peptides. Nucleic Acids Res. 2014;42(D1):D1154-8.
Yu HH, Song YJ, Yu HS, Lee NK, Paik HD. Investigating the antimicrobial and antibiofilm effects of cinnamaldehyde against Campylobacter spp. using cell surface characteristics. J Food Sci. 2020;85(1):157–64. https://doi.org/10.1111/1750-3841.14989 .
doi: 10.1111/1750-3841.14989
pubmed: 31909483
Turkey AM, Barzani KK, Suleiman AA, Abed JJ. Molecular assessment of accessory gene regulator (agr) quorum sensing system in biofilm forming Staphylococcus aureus and study of the effect of silver nanoparticles on agr system. Iran J Microbiol. 2018;10(1):14.
pubmed: 29922414
pmcid: 6004638
Arciola CR, Campoccia D, Gamberini S, Baldassarri L, Montanaro L. Prevalence of cna fnbA and fnbB adhesin genes among Staphylococcus aureus isolates from orthopedic infections associated to different types of implant. FEMS Microbiol Lett. 2005;246(1):81–6. https://doi.org/10.1016/j.femsle.2005.03.035 .
doi: 10.1016/j.femsle.2005.03.035
pubmed: 15869965
Arciola CR, Baldassarri L, Montanaro L. Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. J Clin Microbiol. 2001;39(6):2151–6. https://doi.org/10.1128/jcm.39.6.2151-2156.2001 .
doi: 10.1128/jcm.39.6.2151-2156.2001
pubmed: 11376050
pmcid: 88104
Battaglia M, GarrettSinha LA. Staphylococcus xylosus and Staphylococcus aureus as commensals and pathogens on murine skin. Lab Anim Res. 2023;39(1):18. https://doi.org/10.1186/s42826-023-00169-0 .
doi: 10.1186/s42826-023-00169-0
pubmed: 37533118
pmcid: 10394794
Nurxat N, Wang L, Wang Q, Li S, Jin C, Shi Y, et al. Commensal Staphylococcus epidermidis defends against Staphylococcus aureus through SaeRS two-component system. ACS Omega. 2023;8(20):17712–8. https://doi.org/10.1021/acsomega.3c00263 .
doi: 10.1021/acsomega.3c00263
pubmed: 37251147
pmcid: 10210170
O’GARA JP, Humphreys H. Staphylococcus epidermidis biofilms: importance and implications. J Med Microbiol. 2001;50(7):582–7.
doi: 10.1099/0022-1317-50-7-582
pubmed: 11444767
Lima RK, Cardoso MD, Andrade MA, Guimarães PL, Batista LR, Nelson DL. Bactericidal and antioxidant activity of essential oils from Myristica fragrans Houtt and Salvia microphylla HBK. J Am Oil Chem Soc. 2012;89(3):523–8. https://doi.org/10.1007/s11746-011-1938-1 .
doi: 10.1007/s11746-011-1938-1
Kusuma SAF, Ronato, Baitariza A. Effect of nutmeg seeds extracts (Myristica fragrans Houtt) on Staphylococcus aureus and Staphylococcus epidermidis. World J Pharm Res. 2019;101–9. https://doi.org/10.20959/wjpr20199-15493 .
Taguri T, Tanaka T, Kouno I. Antibacterial spectrum of plant polyphenols and extracts depending upon hydroxyphenyl structure. Biol Pharm Bull. 2006;29(11):2226–35. https://doi.org/10.1248/bpb.29.2226 .
doi: 10.1248/bpb.29.2226
pubmed: 17077519
Lamas A, Regal P, Vázquez B, Cepeda A, Franco CM. Short chain fatty acids commonly produced by gut microbiota influence Salmonella enterica motility, biofilm formation, and gene expression. Antibiotics. 2019;8(4):265. https://doi.org/10.3390/antibiotics8040265 .
doi: 10.3390/antibiotics8040265
pubmed: 31847278
pmcid: 6963744
Idrees M, Sawant S, Karodia N, Rahman A. Staphylococcus aureus biomorphologyhology, genetics, pathogenesis and treatment strategies. Int J Environ Res Public Health. 2021;18(14):7602. https://doi.org/10.3390/ijerph18147602 .
O’Gara JP. Ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett. 2007;270(2):179–88. https://doi.org/10.1111/j.1574-6968.2007.00688.x .
doi: 10.1111/j.1574-6968.2007.00688.x
pubmed: 17419768
Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun. 1999;67(10):5427–33. https://doi.org/10.1128/iai.67.10.5427-5433.1999 .
doi: 10.1128/iai.67.10.5427-5433.1999
pubmed: 10496925
pmcid: 96900
Azmi K, Qrei W, Abdeen Z. Screening of genes encoding adhesion factors and biofilm production in methicillin resistant strains of Staphylococcus aureus isolated from Palestinian patients. BMC Genomics. 2019;20:1–2. https://doi.org/10.1186/s12864-019-5929-1 .
doi: 10.1186/s12864-019-5929-1
Chen Q, Xie S, Lou X, Cheng S, Liu X, Zheng W, et al. Biofilm formation and prevalence of adhesion genes among Staphylococcus aureus isolates from different food sources. MicrobiologyOpen. 2020;9(1):e00946. https://doi.org/10.1002/mbo3.946 .
doi: 10.1002/mbo3.946
pubmed: 31769202
Sinha B, Francois P, Que YA, Hussain M, Heilmann C, Moreillon P, et al. Heterologously expressed Staphylococcus aureus fibronectinbinding proteins are sufficient for invasion of host cells. Infect Immun. 2000;68(12):6871–8. https://doi.org/10.1128/iai.68.12.6871-6878.2000 .
O’Neill E, Pozzi C, Houston P, Humphreys H, Robinson DA, Loughman A, et al. A novel Staphylococcus aureus biofilm phenotype mediated by the fibronectin-binding proteins, FnBPA and FnBPB. J Bacteriol. 2008;190(11):3835–50. https://doi.org/10.1128/jb.00167-08 .
doi: 10.1128/jb.00167-08
pubmed: 18375547
pmcid: 2395027
Smeltzer MS, Gillaspy AF, Pratt FL Jr, Thames MD, Iandolo JJ. Prevalence and chromosomal map location of Staphylococcus aureus adhesin genes. Gene. 1997;196(1–2):249–59. https://doi.org/10.1016/S0378-1119(97)00237-0 .
doi: 10.1016/S0378-1119(97)00237-0
pubmed: 9322764
Moormeier DE, Bayles KW. Staphylococcus aureus biofilm: a complex developmental organism. Mol Microbiol. 2017;104(3):365–76. https://doi.org/10.1111/mmi.13634 .
doi: 10.1111/mmi.13634
pubmed: 28142193
pmcid: 5397344
Lister JL, Horswill AR. Staphylococcus aureus biofilms: recent developments in biofilm dispersal. Front Cell Infect Microbiol. 2014;4:178. https://doi.org/10.3389/fcimb.2014.00178 .
doi: 10.3389/fcimb.2014.00178
pubmed: 25566513
pmcid: 4275032
Peschel A, Otto M. Phenol-soluble modulins and staphylococcal infection. Nat Rev Microbiol. 2013;11(10):667–73. https://doi.org/10.1038/nrmicro3110 .
doi: 10.1038/nrmicro3110
pubmed: 24018382
pmcid: 4780437
Saggu SK, Jha G, Mishra PC. Enzymatic degradation of biofilm by metalloprotease from Microbacterium sp. SKS10. Front Bioeng Biotechnol. 2019;7:192. https://doi.org/10.3389/fbioe.2019.00192 .
doi: 10.3389/fbioe.2019.00192
pubmed: 31448272
pmcid: 6692633
Queck SY, JamesonLee M, Villaruz AE, Bach TH, Khan BA, Sturdevant DE, et al. RNAIIIindependent target gene control by the agr quorumsensing system: insight into the evolution of virulence regulation in Staphylococcus aureus. Mol Cell. 2008;32(1):150–8. https://doi.org/10.1016/j.molcel.2008.08.005 .
Amrutha B, Sundar K, Shetty PH. Effect of organic acids on biofilm formation and quorum signaling of pathogens from fresh fruits and vegetables. Microb Pathog. 2017;111:156–62. https://doi.org/10.1016/j.micpath.2017.08.042 .
doi: 10.1016/j.micpath.2017.08.042
pubmed: 28867627
Ansari JM, Abraham NM, Massaro J, Murphy K, Smith-Carpenter J, Fikrig E. Anti-biofilm activity of a self-aggregating peptide against Streptococcus mutans. Front Microbiol. 2017;8:252915. https://doi.org/10.3389/fmicb.2017.00488 .
doi: 10.3389/fmicb.2017.00488
Brancatisano FL, Maisetta G, Di Luca M, Esin S, Bottai D, Bizzarri R, et al. Inhibitory effect of the human liver-derived antimicrobial peptide hepcidin 20 on biofilms of polysaccharide intercellular adhesin (PIA)-positive and PIA-negative strains of Staphylococcus epidermidis. Biofouling. 2014;30(4):435–46. https://doi.org/10.1080/08927014.2014.888062 .
doi: 10.1080/08927014.2014.888062
pubmed: 24645694
Overhage J, Campisano A, Bains M, Torfs EC, Rehm BH, Hancock RE. Human host defense peptide LL-37 prevents bacterial biofilm formation. InfectImmun. 2008;76(9):4176–82. https://doi.org/10.1128/iai.00318-08 .
doi: 10.1128/iai.00318-08
Yasir M, Willcox MD, Dutta D. Action of antimicrobial peptides against bacterial biofilms. Materials. 2018;11(12):2468. https://doi.org/10.3390/ma11122468 .
doi: 10.3390/ma11122468
pubmed: 30563067
pmcid: 6317029
Lee JH, Cho HS, Joo SW, Chandra Regmi S, Kim JA, Ryu CM, et al. Diverse plant extracts and transresveratrol inhibit biofilm formation and swarming of Escherichia coli O157: H7. Biofouling. 2013;29(10):1189–203. https://doi.org/10.1080/08927014.2013.832223 .
doi: 10.1080/08927014.2013.832223
pubmed: 24067082