Login Register Cart 0
Generic placeholder image

Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Letter Article

A Novel Brevinin2 HYba5 Peptide against Polymicrobial Biofilm of Staphylococcus aureus and Enterococcus faecalis

Author(s): Megha Periyappilly Radhakrishnan, Karthika Suryaletha, Iype Joseph, Sanil George and Sabu Thomas*

Volume 30, Issue 10, 2023

Published on: 10 October, 2023

Page: [795 - 805] Pages: 11

DOI: 10.2174/0109298665266332231001115508

Price: $65

Abstract

Background: Brevinin2 HYba5 (Peptide 29) is a novel cationic peptide identified from an endemic frog, Hydrophylax bahuvistara. Staphylococcus aureus and Enterococcus faecalis are troublesome biofilm-forming pathogens associated with nosocomial and community-acquired infections and contribute to the severity of infections associated with implanted devices and chronic wounds. Co-existence of both pathogens in biofilm mode contributes to an increased antibiotic resistance, treatment failure and hence persistent disease burden. Identifying a novel and stable, less toxic compound targeting multispecies biofilm with a lower probability of acquiring resistance in comparison to antibiotics is highly warranted.

Objective: Evaluate the activity of Brevinin2 HYba5 against S. aureus and E. faecalis mixed biofilm.

Methods: The anti-biofilm activity of peptide 29 was tested by Crystal violet assay, Confocal laser scanning Microscopy (CLSM) and MTT Assay. Cytotoxicity of the peptide was tested in RBC and L929 fibroblast cell line. Biofilm inhibitory activity of the peptide was evaluated at different temperatures, pH, serum and plasma concentrations. The antibiofilm potential of the peptide was tested against polymicrobial biofilm by Fluorescent in situ hybridisation (FISH) and plate counting on HiCromeTM UTI Agar media.

Results: The peptide 29 could inhibit biofilm formation of S. aureus and E. faecalis individually as well as in polymicrobial biofilm at 75 μM concentration. The peptide maintained its antibiofilm potential at different temperatures, serum and plasma concentrations. Activity of the peptide was high at acidic and neutral pH but found to get reduced towards alkaline pH. The peptide is nonhemolytic and does not exhibit significant cytotoxicity against the L929 fibroblast cell line (92.80% cell viability).

Conclusion: The biofilm inhibition property makes peptide 29 a promising candidate for the management of S. aureus and E. faecalis biofilm, especially in catheter-associated devices to prevent the initial colonization and thus can ease the burden of pathogenic biofilm-associated infections.

Next »
Graphical Abstract

[1]
She, P.; Zhou, L.; Li, S.; Liu, Y.; Xu, L.; Chen, L.; Luo, Z.; Wu, Y. Synergistic microbicidal effect of auranofin and antibiotics against planktonic and biofilm-encased Staphylococcus aureus and Enterococcus faecalis. Front. Microbiol., 2019, 10, 2453.
[http://dx.doi.org/10.3389/fmicb.2019.02453] [PMID: 31708908]
[2]
Cheung, G.Y.C.; Bae, J.S.; Otto, M. Pathogenicity and virulence of Staphylococcus aureus. Virulence, 2021, 12(1), 547-569.
[http://dx.doi.org/10.1080/21505594.2021.1878688] [PMID: 33522395]
[3]
Fiore, E.; Van Tyne, D.; Gilmore, M.S. Pathogenicity of Enterococci. Microbiol. Spectr., 2019, 7(4), 7.4.9..
[http://dx.doi.org/ 10.1128/microbiolspec.GPP3-0053-2018] [PMID: 31298205]
[4]
Kulkarni, A.P.; Nagvekar, V.C.; Veeraraghavan, B.; Warrier, A.R.; Ts, D.; Ahdal, J.; Jain, R. Current perspectives on treatment of Gram-positive infections in India: What is the way forward? Interdiscip. Perspect. Infect. Dis., 2019, 2019, 1-8.
[http://dx.doi.org/10.1155/2019/7601847] [PMID: 31080476]
[5]
Murray, C.J.L.; Ikuta, K.S.; Sharara, F.; Swetschinski, L.; Robles Aguilar, G.; Gray, A.; Han, C.; Bisignano, C.; Rao, P.; Wool, E.; Johnson, S.C.; Browne, A.J.; Chipeta, M.G.; Fell, F.; Hackett, S.; Haines-Woodhouse, G.; Kashef, H.B.H.; Kumaran, E.A.P.; McManigal, B.; Achalapong, S.; Agarwal, R.; Akech, S.; Albertson, S.; Amuasi, J.; Andrews, J.; Aravkin, A.; Ashley, E.; Babin, F-X.; Bailey, F.; Baker, S.; Basnyat, B.; Bekker, A.; Bender, R.; Berkley, J.A.; Bethou, A.; Bielicki, J.; Boonkasidecha, S.; Bukosia, J.; Carvalheiro, C.; Castañeda-Orjuela, C.; Chansamouth, V.; Chaurasia, S.; Chiurchiù, S.; Chowdhury, F.; Clotaire Donatien, R.; Cook, A.J.; Cooper, B.; Cressey, T.R.; Criollo-Mora, E.; Cunningham, M.; Darboe, S.; Day, N.P.J.; De Luca, M.; Dokova, K.; Dramowski, A.; Dunachie, S.J.; Duong Bich, T.; Eckmanns, T.; Eibach, D.; Emami, A.; Feasey, N.; Fisher-Pearson, N.; Forrest, K.; Garcia, C.; Garrett, D.; Gastmeier, P.; Giref, A.Z.; Greer, R.C.; Gupta, V.; Haller, S.; Haselbeck, A.; Hay, S.I.; Holm, M.; Hopkins, S.; Hsia, Y.; Iregbu, K.C.; Jacobs, J.; Jarovsky, D.; Javanmardi, F.; Jenney, A.W.J.; Khorana, M.; Khusuwan, S.; Kissoon, N.; Kobeissi, E.; Kostyanev, T.; Krapp, F.; Krumkamp, R.; Kumar, A.; Kyu, H.H.; Lim, C.; Lim, K.; Limmathurotsakul, D.; Loftus, M.J.; Lunn, M.; Ma, J.; Manoharan, A.; Marks, F.; May, J.; Mayxay, M.; Mturi, N.; Munera-Huertas, T.; Musicha, P.; Musila, L.A.; Mussi-Pinhata, M.M.; Naidu, R.N.; Nakamura, T.; Nanavati, R.; Nangia, S.; Newton, P.; Ngoun, C.; Novotney, A.; Nwakanma, D.; Obiero, C.W.; Ochoa, T.J.; Olivas-Martinez, A.; Olliaro, P.; Ooko, E.; Ortiz-Brizuela, E.; Ounchanum, P.; Pak, G.D.; Paredes, J.L.; Peleg, A.Y.; Perrone, C.; Phe, T.; Phommasone, K.; Plakkal, N.; Ponce-de-Leon, A.; Raad, M.; Ramdin, T.; Rattanavong, S.; Riddell, A.; Roberts, T.; Robotham, J.V.; Roca, A.; Rosenthal, V.D.; Rudd, K.E.; Russell, N.; Sader, H.S.; Saengchan, W.; Schnall, J.; Scott, J.A.G.; Seekaew, S.; Sharland, M.; Shivamallappa, M.; Sifuentes-Osornio, J.; Simpson, A.J.; Steenkeste, N.; Stewardson, A.J.; Stoeva, T.; Tasak, N.; Thaiprakong, A.; Thwaites, G.; Tigoi, C.; Turner, C.; Turner, P.; van Doorn, H.R.; Velaphi, S.; Vongpradith, A.; Vongsouvath, M.; Vu, H.; Walsh, T.; Walson, J.L.; Waner, S.; Wangrangsimakul, T.; Wannapinij, P.; Wozniak, T.; Young Sharma, T.E.M.W.; Yu, K.C.; Zheng, P.; Sartorius, B.; Lopez, A.D.; Stergachis, A.; Moore, C.; Dolecek, C.; Naghavi, M. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet, 2022, 399(10325), 629-655.
[http://dx.doi.org/10.1016/S0140-6736(21)02724-0] [PMID: 35065702]
[6]
Jabbari, S.S.M.; Pormohammad, A.; Hashemi, A.; Lak, P. Global prevalence of antibiotic resistance in blood-isolated Enterococcus faecalis and Enterococcus faecium: A systematic review and meta-analysis. Infect. Drug Resist., 2019, 12, 2713-2725.
[http://dx.doi.org/10.2147/IDR.S206084] [PMID: 31564921]
[7]
Gomes, F.I.A.; Teixeira, P.; Azeredo, J.; Oliveira, R. Effect of farnesol on planktonic and biofilm cells of Staphylococcus epidermidis. Curr. Microbiol., 2009, 59(2), 118-122.
[http://dx.doi.org/10.1007/s00284-009-9408-9] [PMID: 19365686]
[8]
Qu, Y.; Locock, K.; Verma-Gaur, J.; Hay, I.D.; Meagher, L.; Traven, A. Searching for new strategies against polymicrobial biofilm infections: Guanylated polymethacrylates kill mixed fungal/bacterial biofilms. J. Antimicrob. Chemother., 2016, 71(2), 413-421.
[http://dx.doi.org/10.1093/jac/dkv334] [PMID: 26490013]
[9]
Stoodley, P.; Sidhu, S.; Nistico, L.; Mather, M.; Boucek, A.; Hall-Stoodley, L.; Kathju, S. Kinetics and morphology of polymicrobial biofilm formation on polypropylene mesh. FEMS Immunol. Med. Microbiol., 2012, 65(2), 283-290.
[http://dx.doi.org/10.1111/j.1574-695X.2012.00948.x] [PMID: 22364207]
[10]
Nguyen, L.T.; Haney, E.F.; Vogel, H.J. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol., 2011, 29(9), 464-472.
[http://dx.doi.org/10.1016/j.tibtech.2011.05.001] [PMID: 21680034]
[11]
Di Somma, A.; Moretta, A.; Canè, C.; Cirillo, A.; Duilio, A. Antimicrobial and antibiofilm peptides. Biomolecules, 2020, 10(4), 652.
[http://dx.doi.org/10.3390/biom10040652] [PMID: 32340301]
[12]
Radhakrishnan, M.P.; Suryaletha, K.; Shankar, A.; Savithri, A.V.; George, S.; Thomas, S. Insights into peptide mediated antibiofilm treatment in chronic wound: A bench to bedside approach. Curr. Protein Pept. Sci., 2021, 22(1), 50-59.
[http://dx.doi.org/10.2174/1389203721666201103084727] [PMID: 33143623]
[13]
Teixeira, V.; Feio, M.J.; Bastos, M. Role of lipids in the interaction of antimicrobial peptides with membranes. Prog. Lipid Res., 2012, 51(2), 149-177.
[http://dx.doi.org/10.1016/j.plipres.2011.12.005] [PMID: 22245454]
[14]
Huang, Y.; Huang, J.; Chen, Y. Alpha-helical cationic antimicrobial peptides: Relationships of structure and function. Protein Cell, 2010, 1(2), 143-152.
[http://dx.doi.org/10.1007/s13238-010-0004-3] [PMID: 21203984]
[15]
Hancock, R.E.W.; Chapple, D.S. Peptide Antibiotics. Antimicrob. Agents Chemother., 1999, 43(6), 1317-1323.
[http://dx.doi.org/10.1128/AAC.43.6.1317] [PMID: 10348745]
[16]
Shai, Y.; Oren, Z. From “carpet” mechanism to de-novo designed diastereomeric cell-selective antimicrobial peptides. Peptides, 2001, 22(10), 1629-1641.
[http://dx.doi.org/10.1016/S0196-9781(01)00498-3] [PMID: 11587791]
[17]
Rotem, S.; Mor, A. Antimicrobial peptide mimics for improved therapeutic properties. Biochim. Biophys. Acta Biomembr., 2009, 1788(8), 1582-1592.
[http://dx.doi.org/10.1016/j.bbamem.2008.10.020] [PMID: 19028449]
[18]
Malik, E.; Dennison, S.; Harris, F.; Phoenix, D. pH dependent antimicrobial peptides and proteins, their mechanisms of action and potential as therapeutic agents. Pharmaceuticals (Basel), 2016, 9(4), 67.
[http://dx.doi.org/10.3390/ph9040067] [PMID: 27809281]
[19]
O’Toole, G.A. Microtiter dish biofilm formation assay. J. Vis. Exp., 2011, 30(47), 2437.
[PMID: 21307833]
[20]
Vineeth Kumar, T.P.V.K.; Asha, R.; Shyla, G.; George, S. Identification and characterization of novel host defense peptides from the skin secretion of the fungoid frog, Hydrophylax bahuvistara (Anura: Ranidae). Chem. Biol. Drug Des., 2018, 92(2), 1409-1418.
[http://dx.doi.org/10.1111/cbdd.12937] [PMID: 28072492]
[21]
Suryaletha, K.; John, J.; Radhakrishnan, M.P.; George, S.; Thomas, S. Metataxonomic approach to decipher the polymicrobial burden in diabetic foot ulcer and its biofilm mode of infection. Int. Wound J., 2018, 15(3), 473-481.
[http://dx.doi.org/10.1111/iwj.12888] [PMID: 29356343]
[22]
Mshana, R.N.; Tadesse, G.; Abate, G.; Miörner, H. Use of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide for rapid detection of rifampin-resistant Mycobacterium tuberculosis. J. Clin. Microbiol., 1998, 36(5), 1214-1219.
[http://dx.doi.org/10.1128/JCM.36.5.1214-1219.1998] [PMID: 9574679]
[23]
Tavanti, A.; Maisetta, G.; Del Gaudio, G.; Petruzzelli, R.; Sanguinetti, M.; Batoni, G.; Senesi, S. Fungicidal activity of the human peptide hepcidin 20 alone or in combination with other antifungals against Candida glabrata isolates. Peptides, 2011, 32(12), 2484-2487.
[http://dx.doi.org/10.1016/j.peptides.2011.10.012] [PMID: 22015266]
[24]
Horiuchi, N.; Nakagawa, K.; Sasaki, Y.; Minato, K.; Fujiwara, Y.; Nezu, K.; Ohe, Y.; Saijo, N. In vitro antitumor activity of mitomycin C derivative (RM-49) and new anticancer antibiotics (FK973) against lung cancer cell lines determined by tetrazolium dye (MTT) assay. Cancer Chemother. Pharmacol., 1988, 22(3), 246-250.
[http://dx.doi.org/10.1007/BF00273419] [PMID: 2842080]
[25]
Lawson, T.S.; Connally, R.E.; Iredell, J.R.; Vemulpad, S.; Piper, J.A. Detection of Staphylococcus aureus with a fluorescence in situ hybridization that does not require lysostaphin. J. Clin. Lab. Anal., 2011, 25(2), 142-147.
[http://dx.doi.org/10.1002/jcla.20448] [PMID: 21438009]
[26]
Hermie, J.M.; Harmsen, P.; Elfferich, F.; Schut, G.W.; Welling, A. 16S rRNA-targeted probe for detection of lactobacilli and Enterococci in faecal samples by Fluorescent in situ Hybridization. Microb. Ecol. Health Dis., 1999, 11(1), 3-12.
[27]
Shinde, S.; Lee, L.H.; Chu, T. Inhibition of biofilm formation by the synergistic action of EGCG-S and antibiotics. Antibiotics (Basel), 2021, 10(2), 102.
[http://dx.doi.org/10.3390/antibiotics10020102] [PMID: 33494273]
[28]
Thomas, P.; Vineeth Kumar, T.V.; Reshmy, V.; Kumar, K.S.; George, S. A mini review on the antimicrobial peptides isolated from the genus Hylarana (Amphibia: Anura) with a proposed nomenclature for amphibian skin peptides. Mol. Biol. Rep., 2012, 39(6), 6943-6947.
[http://dx.doi.org/10.1007/s11033-012-1521-3] [PMID: 22307792]
[29]
Gautier, R.; Douguet, D.; Antonny, B.; Drin, G. HELIQUEST: A web server to screen sequences with specific α-helical properties. Bioinformatics, 2008, 24(18), 2101-2102.
[http://dx.doi.org/10.1093/bioinformatics/btn392] [PMID: 18662927]
[30]
Maisetta, G.; Vitali, A.; Scorciapino, M.A.; Rinaldi, A.C.; Petruzzelli, R.; Brancatisano, F.L.; Esin, S.; Stringaro, A.; Colone, M.; Luzi, C.; Bozzi, A.; Campa, M.; Batoni, G. pH-dependent disruption of Escherichia coli ATCC 25922 and model membranes by the human antimicrobial peptides hepcidin 20 and 25. FEBS J., 2013, 280(12), 2842-2854.
[http://dx.doi.org/10.1111/febs.12288] [PMID: 23587102]
[31]
Batoni, G.; Maisetta, G.; Lisa Brancatisano, F.; Esin, S.; Campa, M. Use of antimicrobial peptides against microbial biofilms: Advantages and limits. Curr. Med. Chem., 2011, 18(2), 256-279.
[http://dx.doi.org/10.2174/092986711794088399] [PMID: 21110801]
[32]
Jorge, P.; Lourenço, A.; Pereira, M.O. New trends in peptide-based anti-biofilm strategies: A review of recent achievements and bioinformatic approaches. Biofouling, 2012, 28(10), 1033-1061.
[http://dx.doi.org/10.1080/08927014.2012.728210] [PMID: 23016989]
[33]
Di Luca, M.; Maccari, G.; Nifosì, R. Treatment of microbial biofilms in the post-antibiotic era: Prophylactic and therapeutic use of antimicrobial peptides and their design by bioinformatics tools. Pathog. Dis., 2014, 70(3), 257-270.
[http://dx.doi.org/10.1111/2049-632X.12151] [PMID: 24515391]
[34]
Ferreira, A.A.; Tette, P.A.S.; Mendonça, R.C.S.; Soares, A.S.; Carvalho, M.M.D. Detection of exopolysaccharide production and biofilm-related genes in Staphylococcus spp. isolated from a poultry processing plant. Food Sci. Technol. (Campinas), 2014, 34(4), 710-716.
[http://dx.doi.org/10.1590/1678-457X.6446]
[35]
Høiby, N.; Ciofu, O.; Johansen, H.K.; Song, Z.; Moser, C.; Jensen, P.Ø.; Molin, S.; Givskov, M.; Tolker-Nielsen, T.; Bjarnsholt, T. The clinical impact of bacterial biofilms. Int. J. Oral Sci., 2011, 3(2), 55-65.
[http://dx.doi.org/10.4248/IJOS11026] [PMID: 21485309]
[36]
Pletzer, D.; Hancock, R.E.W. Antibiofilm peptides: Potential as broad-spectrum agents. J. Bacteriol., 2016, 198(19), 2572-2578.
[http://dx.doi.org/10.1128/JB.00017-16] [PMID: 27068589]
[37]
Wolfmeier, H.; Pletzer, D.; Mansour, S.C.; Hancock, R.E.W. New perspectives in biofilm eradication. ACS Infect. Dis., 2018, 4(2), 93-106.
[http://dx.doi.org/10.1021/acsinfecdis.7b00170] [PMID: 29280609]
[38]
Chauhan, A.; Lebeaux, D.; Ghigo, J.M.; Beloin, C. Full and broad-spectrum in vivo eradication of catheter-associated biofilms using gentamicin-EDTA antibiotic lock therapy. Antimicrob. Agents Chemother., 2012, 56(12), 6310-6318.
[http://dx.doi.org/10.1128/AAC.01606-12] [PMID: 23027191]
[39]
Bose, B.; Downey, T.; Ramasubramanian, A.K.; Anastasiu, D.C. Identification of distinct characteristics of antibiofilm peptides and prospection of diverse Sources for efficacious sequences. Front. Microbiol., 2022, 12, 783284.
[http://dx.doi.org/10.3389/fmicb.2021.783284] [PMID: 35185814]
[40]
Andrea, A.; Molchanova, N.; Jenssen, H. Antibiofilm peptides and peptidomimetics with focus on surface immobilization. Biomolecules, 2018, 8(2), 27.
[http://dx.doi.org/10.3390/biom8020027] [PMID: 29772735]
[41]
Wei, H.; Xie, Z.; Tan, X.; Guo, R.; Song, Y.; Xie, X.; Wang, R.; Li, L.; Wang, M.; Zhang, Y. Temporin-like peptides show antimicrobial and anti-biofilm activities against Streptococcus mutans with reduced hemolysis. Molecules, 2020, 25(23), 5724.
[http://dx.doi.org/10.3390/molecules25235724] [PMID: 33291521]
[42]
Abou Alaiwa, M.H.; Reznikov, L.R.; Gansemer, N.D.; Sheets, K.A.; Horswill, A.R.; Stoltz, D.A.; Zabner, J.; Welsh, M.J. pH modulates the activity and synergism of the airway surface liquid antimicrobials β-defensin-3 and LL-37. Proc. Natl. Acad. Sci. USA, 2014, 111(52), 18703-18708.
[http://dx.doi.org/10.1073/pnas.1422091112] [PMID: 25512526]
[43]
Foulston, L.; Elsholz, A.K.W.; DeFrancesco, A.S.; Losick, R. The extracellular matrix of Staphylococcus aureus biofilms comprises cytoplasmic proteins that associate with the cell surface in response to decreasing pH. MBio, 2014, 5(5), e01667-e14.
[http://dx.doi.org/10.1128/mBio.01667-14] [PMID: 25182325]
[44]
Aoi, W.; Marunaka, Y. Importance of pH homeostasis in metabolic health and diseases: Crucial role of membrane proton transport. BioMed Res. Int., 2014, 2014, 1-8.
[http://dx.doi.org/10.1155/2014/598986] [PMID: 25302301]
[45]
Dostert, M.; Belanger, C.R.; Hancock, R.E.W. Design and assessment of anti-biofilm peptides: Steps toward clinical application. J. Innate Immun., 2019, 11(3), 193-204.
[http://dx.doi.org/10.1159/000491497] [PMID: 30134244]
[46]
Kao, P.H.N.; Ch’ng, J.H.; Chong, K.L.K. Enterococcus faecalis and Staphylococcus aureus mixed species infection attenuates pathogen-specific neutrophil responses and impairs bacterial clearance. BioRxiv, 2022, 17, 2022-05.
[47]
Ch’ng, J.H.; Muthu, M.; Chong, K.K.L.; Wong, J.J.; Tan, C.A.Z.; Koh, Z.J.S.; Lopez, D.; Matysik, A.; Nair, Z.J.; Barkham, T.; Wang, Y.; Kline, K.A. Heme cross-feeding can augment Staphylococcus aureus and Enterococcus faecalis dual species biofilms. ISME J., 2022, 16(8), 2015-2026.
[http://dx.doi.org/10.1038/s41396-022-01248-1] [PMID: 35589966]
[48]
Costa, G.A.; Rossatto, F.C.P.; Medeiros, A.W.; Correa, A.P.F.; Brandelli, A.; Frazzon, A.P.G.; Motta, A.D.S.D. Evaluation antibacterial and antibiofilm activity of the antimicrobial peptide P34 against Staphylococcus aureus and Enterococcus faecalis. An. Acad. Bras. Cienc., 2018, 90(1), 73-84.
[http://dx.doi.org/10.1590/0001-3765201820160131] [PMID: 29424388]
[49]
Batoni, G.; Maisetta, G.; Esin, S. Therapeutic potential of antimicrobial peptides in polymicrobial biofilm-associated infections. Int. J. Mol. Sci., 2021, 22(2), 482.
[http://dx.doi.org/10.3390/ijms22020482] [PMID: 33418930]
[50]
Francolini, I.; Donelli, G. Prevention and control of biofilm-based medical-device-related infections. FEMS Immunol. Med. Microbiol., 2010, 59(3), 227-238.
[http://dx.doi.org/10.1111/j.1574-695X.2010.00665.x] [PMID: 20412300]
[51]
Lim, K.; Chua, R.R.Y.; Ho, B.; Tambyah, P.A.; Hadinoto, K.; Leong, S.S.J. Development of a catheter functionalized by a polydopamine peptide coating with antimicrobial and antibiofilm properties. Acta Biomater., 2015, 15, 127-138.
[http://dx.doi.org/10.1016/j.actbio.2014.12.015] [PMID: 25541344]
[52]
Mishra, B.; Basu, A.; Chua, R.R.Y.; Saravanan, R.; Tambyah, P.A.; Ho, B.; Chang, M.W.; Leong, S.S.J. Site specific immobilization of a potent antimicrobial peptide onto silicone catheters: Evaluation against urinary tract infection pathogens. J. Mater. Chem. B Mater. Biol. Med., 2014, 2(12), 1706-1716.
[http://dx.doi.org/10.1039/c3tb21300e] [PMID: 32261400]
[53]
Shrestha, L.B.; Baral, R.; Khanal, B. Comparative study of antimicrobial resistance and biofilm formation among Gram-positive uropathogens isolated from community-acquired urinary tract infections and catheter-associated urinary tract infections. Infect. Drug Resist., 2019, 12, 957-963.
[http://dx.doi.org/10.2147/IDR.S200988] [PMID: 31118702]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy