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Review

Foodborne ESKAPE Biofilms and Antimicrobial Resistance: lessons Learned from Clinical Isolates

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References

  • Pérez-Rodríguez F, Mercanoglu Taban B. A state-of-art review on multi-drug resistant pathogens in foods of animal origin: risk factors and mitigation strategies. Front Microbiol. 2019;10:2091. Available from: https://pubmed.ncbi.nlm.nih.gov/31555256
  • Borah D, Singh V, Gogoi B, et al. Prevalence of multidrug resistant (MDR) novel Enterococcus faecium strain VDR03 in broiler chicken meat samples collected from Dibrugarh Town, Assam (India). Res J Microbiol. 2016;11(4):126–132. .
  • Molechan C, Amoako DG, Abia ALK, et al. Molecular epidemiology of antibiotic-resistant Enterococcus spp. from the farm-to-fork continuum in intensive poultry production in KwaZulu-Natal, South Africa. Sci Total Environ. 2019;692:868–878.
  • Ge B, Domesle KJ, Gaines SA, et al. Prevalence and antimicrobial susceptibility of indicator organisms Escherichia coli and Enterococcus spp. Isolated from U.S. animal food, 2005–2011. Microorganisms. 2020;8(7):1–14. .
  • Chajęcka-Wierzchowska W, Zadernowska A, García-Solache M, Ready-to-eat dairy products as a source of multidrug-resistant Enterococcus strains: phenotypic and genotypic characteristics. J Dairy Sci. 2020;103:4068–4077. (5):.
  • Ercoli L, Gallina S, Nia Y, et al. Investigation of a Staphylococcal food poisoning outbreak from a Chantilly Cream Dessert, in Umbria (Italy). Foodborne Pathog Dis. 2017;14(7):407–413.
  • Davis GS, Waits K, Nordstrom L, et al. Intermingled Klebsiella pneumoniae populations between retail meats and human urinary tract infections. Clin Infect Dis. 2015;61:892–899.
  • Malta RCR, Ramos GL, Nascimento Dos Santos J, From food to hospital: we need to talk about Acinetobacter spp. Germs. 2020;10(3):210–217.
  • Algammal AM, Mabrok M, Sivaramasamy E, et al. Emerging MDR-Pseudomonas aeruginosa in fish commonly harbor oprL and toxA virulence genes and blaTEM, blaCTX-M, and tetA antibiotic-resistance genes. Sci Rep. 2020;10(1):15961.
  • McClung RP, Roth DM, Vigar M, et al. Waterborne disease outbreaks associated with environmental and undetermined exposures to water - United States, 2013–2014. MMWR Morb Mortal Wkly Rep. 2017;66(44):1222–1225.
  • Das A, Guha C, Biswas U, et al. Detection of emerging antibiotic resistance in bacteria isolated from subclinical mastitis in cattle in West Bengal. Vet World. 2017;10(5):517–520.
  • Hayman MM, Edelson-Mammel SG, Carter PJ, et al. Prevalence of Cronobacter spp. and Salmonella in milk powder manufacturing facilities in the United States. J Food Prot. 2020;83(10):1685–1692. .
  • Xu Z, Xie J, Soteyome T, et al. Polymicrobial interaction and biofilms between Staphylococcus aureus and Pseudomonas aeruginosa: an underestimated concern in food safety. Curr Opin Food Sci. 2019;26:57–64.
  • Bhardwaj AK, Vinothkumar K, Rajpara N. Bacterial quorum sensing inhibitors : attractive alternatives for control of infectious pathogens showing multiple drug resistance. Recent Pat Antiinfect Drug Discov. 2013;8(1):68–83.
  • Reardon S, Antibiotic resistance sweeping developing world. Nat News. 2014;509:141–142.
  • Mukherji R, Patil A, Prabhune A. Role of extracellular proteases in biofilm disruption of gram positive bacteria with special emphasis on Staphylococcus aureus biofilms. Enzym Eng. 2015;4:1–9.
  • Sharma D, Misba L, Khan AU. Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control. 2019;8(1):1–10.
  • Jamal M, Ahmad W, Andleeb S, et al. Bacterial biofilm and associated infections. J Chin Med Assoc. 2018;81(1):7–11.
  • WHO. WHO publishes list of bacteria for which new antibiotics are urgently needed. GENEVA; 2017:1–4. Available from: https://www.who.int/news-room/detail/27-02-2017-who-publishes-list-of-bacteria-for-which-new-antibiotics-are-urgently-needed.
  • Ma YX, Wang CY, Li YY, et al. Considerations and caveats in combating ESKAPE pathogens against nosocomial infections. Adv Sci. 2020;7(8):202000779. .
  • Mulani MS, Kamble EE, Kumkar SN, et al. Emerging strategies to combat ESKAPE pathogens in the era of antimicrobial resistance: a review. Front Microbiol. 2019;10. https://doi.org/10.3389/fmicb.2019.00539.
  • Zhen X, Lundborg CS, Sun X, et al. Economic burden of antibiotic resistance in ESKAPE organisms: a systematic review. Antimicrob Resist Infect Control. 2019;8(1). https://doi.org/10.1186/s13756-019-0590-7.
  • Pendleton JN, Gorman SP, Gilmore BF. Clinical relevance of the ESKAPE pathogens. Expert Rev Anti Infect Ther. 2013;11(3):297–308.
  • Wang Z, Qin RR, Huang L, et al. Risk Factors for Carbapenem-resistant Klebsiella pneumoniae infection and mortality of Klebsiella pneumoniae infection. Chin Med J (Engl). 2018;131(1):56–62. .
  • Marturano JE, Lowery TJ. ESKAPE pathogens in bloodstream infections are associated with higher cost and mortality but can be predicted using diagnoses upon admission. Open Forum Infect Dis. 2019;1–8.
  • Rice LB. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J Infect Dis. 2008;197(8):1079–1081.
  • Ross CL, Liang X, Liu Q, et al. Targeted protein engineering provides insights into binding mechanism and affinities of bacterial collagen adhesins. J Biol Chem. 2012;287(41):34856–34865. .
  • Sattari-Maraji A, Jabalameli F, Node Farahani N, et al. Antimicrobial resistance pattern, virulence determinants and molecular analysis of Enterococcus faecium isolated from children infections in Iran. BMC Microbiol. 2019;19(1):1–8. .
  • Qu Y, Locock K, Verma-Gaur J, et al. Searching for new strategies against polymicrobial biofilm infections: guanylated polymethacrylates kill mixed fungal/bacterial biofilms. J Antimicrob Chemother. 2016;71(2):413–421. .
  • Nabb DL, Song S, Kluthe KE, et al. Polymicrobial interactions induce multidrug tolerance in Staphylococcus aureus through energy depletion. Front Microbiol. 2019;10:1–12.
  • Giraffa G. Enterococci from foods. FEMS Microbiol Rev. 2002;26(2):163–171.
  • Oprea SF, Zervos MJ. Enterococcus and its association with foodborne illness. Foodborne Dis. 2007;157–174.
  • Arntzen MØ, Karlskås IL, Skaugen M, et al. Proteomic investigation of the response of Enterococcus faecalis V583 when cultivated in urine. PLoS One. 2015;10(4):1–17. .
  • Stępień-Pyśniak D, Hauschild T, Kosikowska U, et al. Biofilm formation capacity and presence of virulence factors among commensal Enterococcus spp from wild birds . Sci Rep 2019;9:1–7.
  • Ben Braïek O, Smaoui S. Enterococci: between emerging pathogens and potential probiotics. Biomed Res Int. 2019;2019:5938210.
  • Chajecka-Wierzchowska W, Zadernowska A, Łaniewska-Trokenheim Ł. Virulence factors of Enterococcus spp. presented in food. LWT - Food Sci Technol. 2017;75:670–676.
  • Carniol K, Gilmore MS. Extracellular protease activity in signal transduction, quorum-sensing, and extracellular protease. J Bacteriol. 2004;186(24):8161–8163.
  • Hancock LE, Perego M. The Enterococcus faecalis fsr two-component system controls biofilm development through production of gelatinase. J Bacteriol. 2004;186(17):5629–5639.
  • Ali L, Goraya MU, Arafat Y, et al. Molecular mechanism of quorum-sensing in Enterococcus faecalis: its role in virulence and therapeutic approaches. Int J Mol Sci. 2017;18(5):960.
  • Mohamed JA, Huang DB. Biofilm formation by enterococci. J Med Microbiol. 2007;56(12):1581–1588.
  • Hashem YA, Amin HM, Essam TM, et al. Biofilm formation in enterococci: genotype-phenotype correlations and inhibition by vancomycin. Sci Rep. 2017;7(1):1–12.
  • Hendrickx APA, Van Luit-Asbroek M, Schapendonk CME, et al. SgrA, a nidogen-binding LPXTG surface adhesin implicated in biofilm formation, and EcbA, a collagen binding MSCRAMM, are two novel adhesins of hospital-acquired Enterococcus faecium. Infect Immun. 2009;77(11):5097–5106. .
  • Ali SA, Bin-Asif H, Hasan KA, et al. Molecular assessment of virulence determinants, hospital associated marker (IS16gene) and prevalence of antibiotic resistance in soil borne Enterococcus species. Microb Pathog. 2017 [ cited 2020 Mar 23];105:298–306.
  • Toledo-arana A, Valle J, Solano C, et al. The enterococcal surface protein, esp, is involved in Enterococcus faecalis biofilm formation. Society. 2001;67:4538–4545. Available from: https://aem.asm.org/content/67/10/4538.short%0A
  • Strateva T, Atanasova D, Savov E, et al. Incidence of virulence determinants in clinical Enterococcus faecalis and Enterococcus faecium isolates collected in Bulgaria. Brazilian J Infect Dis. 2016;20(2):127–133.
  • Top J, Paganelli FL, Zhang X, et al. The Enterococcus faecium enterococcal biofilm regulator, ebrb, regulates the esp operon and is implicated in biofilm formation and intestinal colonization. PLoS One. 2013;8(5):1–13. .
  • Yang Y, Li W, Hou B, et al. Quorum sensing LuxS/autoinducer-2 inhibits Enterococcus faecalis biofilm formation ability. J Appl Oral Sci. 2018;26:e20170566.
  • Grace D, Fetsch A. Staphylococcus aureus —A foodborne pathogen. Staphylococcus Aureus. 2018. Elsevier Inc. https://doi.org/10.1016/B978-0-12-809671-0.00001-2.
  • Jhalka K, Smith TC, Thapaliya D. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Environ Res. 2016;150:528–540.
  • Clarke SR, Foster SJ, Clarke SR, et al. Surface adhesins of Staphylococcus aureus. Adv Microb Physiol. 2006.
  • Kalia VC. Quorum sensing vs quorum quenching: a battle with no end in sight. Kalia VC, editor. Springer: 2015.
  • Kirmusaoglu S. Staphylococcal biofilms: pathogenicity, mechanism and regulation of biofilm formation by quorum-sensing system and antibiotic resistance mechanisms of biofilm-embedded microorganisms. In: Dharumadurai D, Nooruddin T, editors. Microbial Biofilms - Importance and Applications. IntechOpen. DOI: https://doi.org/10.5772/62943.
  • Yu D, Zhao L, Xue T, et al. Staphylococcus aureus autoinducer-2 quorum sensing decreases biofilm formation in an icaR-dependent manner. BMC Microbiol. 2012;12(1):1.
  • Askarian F, Ajayi C, Hanssen AM, et al. The interaction between Staphylococcus aureus SdrD and desmoglein 1 is important for adhesion to host cells. Sci Rep. 2016;6(1):1–11. .
  • Riley LW. Extraintestinal foodborne pathogens. Annu Rev Food Sci Technol. 2020;11(1):275–294.
  • Hartantyo SHP, Chau ML, Koh TH, et al. Foodborne Klebsiella Pneumoniae: virulence potential, antibiotic resistance, and risks to food safety. J Food Prot. 2020;83(7):1096–1103. .
  • Calbo E, Freixas N, Xercavins M, et al. Foodborne nosocomial outbreak of SHV1 and CTX-M-15-producing Klebsiella pneumoniae: epidemiology and control. Clin Infect Dis. 2011;52(6):743–749. .
  • Zheng JX, Lin ZW, Chen C, et al. Biofilm formation in Klebsiella pneumoniae bacteremia strains was found to be associated with CC23 and the presence of wcaG. Front Cell Infect Microbiol. 2018;8:8.
  • Ce´cilia A, Balestrino D, Lucile R, et al. Quorum sensing affects biofilm formation through lipopolysaccharide synthesis in Klebsiella pneumoniae. Res Microbiol. 2010;161(7):595–603. .
  • Balestrino D, Haagensen JAJ, Rich C, et al. Characterization of type 2 quorum sensing in Klebsiella pneumoniae and relationship with biofilm formation. J Bacteriol. 2005;187(8):2870–2880. .
  • Berne C, Ducret A, Gail H, et al. Adhesins involved in attachment to abiotic surfaces by Gram- negative bacteria. Microbiol Spectr. 2015;3(4):1–45. .
  • Schroll C, Barken KB, Krogfelt KA, et al. Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formation. BMC Microbiol. 2010;10(1):179.
  • Lavender HF, Jagnow JR, Clegg S. Biofilm formation in vitro and virulence in vivo of mutants of Klebsiella pneumoniae. Infect Immun. 2004;72(8):4888–4890.
  • Di Martino P, Cafferini N, Joly B, et al. Klebsiella pneumoniae type 3 pili facilitate adherence and biofilm formation on abiotic surfaces. Res Microbiol. 2003;154(1):9–16. .
  • Lin CT, Lin TH, Wu CC, et al. CRP-Cyclic AMP regulates the expression of type 3 fimbriae via cyclic di-GMP in Klebsiella pneumoniae. PLoS One. 2016;11:1–19.
  • Gaddy J, Actis L. Regulation of Acinetobacter baumannii biofilm formation Jennifer. Future Microbiol. 2009;23:1–7.
  • De Amorim AMB, Nascimento JDS. Acinetobacter: an underrated foodborne pathogen? J Infect Dev Ctries. 2017;11(2):111–114.
  • Meliani A, Bensoltane A. Review of Pseudomonas attachment and biofilm formation in food industry. Poultry, Fish Wildl Sci. 2015;03:1–7.
  • Raposo A, Pérez E, De Faria CT, et al. Food spoilage by Pseudomonas spp.—An overview [Internet]. Foodborne Pathog Antibiot Resist. 2016;41–71. https://doi.org/10.1002/9781119139188.ch3
  • Papaioannou E, Utari PD, Quax WJ. Choosing an appropriate infection model to study quorum sensing inhibition in Pseudomonas infections. Int J Mol Sci. 2013;14:19309–19340.
  • El-shaer S, Shaaban M, Barwa R, et al. Control of quorum sensing and virulence factors of Pseudomonas aeruginosa using phenylalanine arginyl b -naphthylamide. J Med Microbiol. 2016;65(10):1194–1204.
  • Ganesh PS, Rai VR. Alternative strategies to regulate quorum sensing and biofilm formation of pathogenic Pseudomonas by quorum sensing Inhibitors of Diverse Origins. In: Kalia VC, editor. Biotechnol Appl Quor Sens Inhib. Springer Nature; 2018. p. 33–61.
  • Philip D, David W. Alginate oligosaccharide-induced modification of the lasI-lasR and rhlI-rhlR quorum sensing systems in Pseudomonas aeruginosa. 2018.
  • Yang Y, Xu Z, Zhang Y, et al. A new quorum-sensing inhibitor attenuates virulence and decreases antibiotic resistance in Pseudomonas aeruginosa. J Microbiol. 2012;50(6):987–993. .
  • Lee J, Zhang L. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein Cell. 2014;6(1):26–41.
  • Chuang SK, Vrla GD, Fröhlich KS, et al. Surface association sensitizes Pseudomonas aeruginosa to quorum sensing. Nat Commun. 2019;10(1). https://doi.org/10.1038/s41467-019-12153-1
  • Turkina MV, Vikström E. Bacteria-host crosstalk: sensing of the quorum in the context of Pseudomonas aeruginosa Infections. J Innate Immun. 2019;11(3):263–279.
  • Chanda W, Joseph TP, Padhiar AA, et al. Combined effect of linolenic acid and tobramycin on Pseudomonas aeruginosa biofilm formation and quorum sensing. Exp Ther Med. 2017;14(5):4328–4338. .
  • Chemani C, Imberty A, De Bentzmann S, et al. Role of LecA and LecB lectins in Pseudomonas aeruginosa-induced lung injury and effect of carbohydrate ligands. Infect Immun. 2009;77(5):2065–2075. .
  • Crouzet M, Claverol S, Lomenech AM, et al. Pseudomonas aeruginosa cells attached to a surface display a typical proteome early as 20 minutes of incubation. PLoS One. 2017;12(7):1–24. .
  • Cambronel M, Tortuel D, Biaggini K, et al. Epinephrine affects motility, and increases adhesion, biofilm and virulence of Pseudomonas aeruginosa H103. Sci Rep. 2019;9(1):1–8. .
  • Amorim AMB, Nascimento Dos S J. A highlight for non-Escherichia coli and Non-Salmonella sp. Enterobacteriaceae in dairy foods contamination. Front Microbiol. 2017;8:2011–2014.
  • Culler HF, Couto SCF, Higa JS, et al. Role of SdiA on biofilm formation by atypical enteropathogenic Escherichia coli. Genes (Basel). 2018;9(5):253. .
  • Rodrigues ME, Gomes F, Celia R. Candida spp./bacteria mixed biofilms. J Fungi. 2020;6:1–29.
  • Keehoon L, Kang-Mu L, Donggeun Kim SSY. Molecular determinants of the thickened matrix in a dual-species. Appl Environ Microbiol. 2017;83:1–15.
  • Nair N, Biswas R, Götz F, et al. Impact of Staphylococcus aureus on pathogenesis in polymicrobial infections. Infect Immun. 2014;82(6):2162–2169. .
  • Alves PM, Al-Badi E, Withycombe C, et al. Interaction between Staphylococcus aureus and Pseudomonas aeruginosa is beneficial for colonisation and pathogenicity in a mixed biofilm. Pathog Dis. 2018;76(1):76.
  • Peters BM, Ovchinnikova ES, Krom BP, et al. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology. 2012;158:2975–2986. (12):.
  • Demuyser L, Jabra-Rizk MA, Van Dijck P. Microbial cell surface proteins and secreted metabolites involved in multispecies biofilms. Pathog Dis. 2014;70(3):219–230.
  • Ch’ng J-H, Chong KKL, Lam LN, et al. Biofilm-associated infection by enterococci. Nat Rev Microbiol. 2019;17(2):82–94.
  • Childers BM, Van Laar TA, You T, et al. MrkD 1P from Klebsiella pneumoniae strain IA565 allows for coexistence with pseudomonas aeruginosa and protection from protease-mediated biofilm detachment. Infect Immun. 2013;81(11):4112–4120. .
  • Wang Y-C, Huang T-W, Yang Y-S, et al. Biofilm formation is not associated with worse outcome in Acinetobacter baumannii bacteraemic pneumonia. Sci Rep. 2018;8(1):7289.
  • Scoffield JA, Duan D, Zhu F, et al. A commensal Streptococcus hijacks a Pseudomonas aeruginosa exopolysaccharide to promote biofilm formation. PLoS Pathog. 2017;13(4):e1006300–e1006300.
  • Stoodley P, Sidhu S, Nistico L, et al. Kinetics and morphology of polymicrobial biofilm formation on polypropylene mesh. FEMS Immunol Med Microbiol. 2012;65(2):283–290.
  • Wang B, Tan X, Du R, et al. Bacterial composition of biofilms formed on dairy-processing equipment. Prep Biochem Biotechnol. 2019;49(5):477–484.
  • Ciofu O, Tolker-Nielsen T. Tolerance and resistance of pseudomonas aeruginosabiofilms to antimicrobial agents-How P. aeruginosa can escape antibiotics. Front Microbiol. 2019;10. https://doi.org/10.3389/fmicb.2019.00913
  • Hall CW, Mah TF. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev. 2017;41(3):276–301.
  • Liao YT, Kuo SC, Lee YT, et al. Sheltering effect and indirect pathogenesis of carbapenem-resistant Acinetobacter baumannii in polymicrobial infection. Antimicrob Agents Chemother. 2014;58(7):3983–3990. .
  • Anderl JN, Franklin MJ, Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother. 2000;44(7):1818–1824.
  • Poudyal B, Sauer K. The ABC of biofilm drug tolerance: the MerR-like regulator brlr is an activator of ABC transport systems, with PA1874-77 contributing to the tolerance of Pseudomonas aeruginosa biofilms to tobramycin. Antimicrob Agents Chemother. 2018;62.
  • Gabrilska RA, Rumbaugh KP. Biofilm models of polymicrobial infection. Future Microbiol. 2015;10(12):1997–2015.
  • Neopane P, Nepal HP, Shrestha R, et al. In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance. Int J Gen Med. 2018;11:25–32.
  • Tanner W, Atkinson-Dunn R, Goel R, et al. Horizontal transfer of the blaNDM-1 gene to Pseudomonas aeruginosa and Acinetobacter baumannii in biofilms. FEMS Microbiol Lett. 2017;364(8):364.
  • Guilhen C, Forestier C, Balestrino D. Biofilm dispersal: multiple elaborate strategies for dissemination of bacteria with unique properties. Mol Microbiol. 2017;105(2):188–210.
  • Rafii F. Antimicrobial resistance in clinically important biofilms. World J Pharmacol. 2015;4(1):31.
  • Penesyan A, Nagy SS, Kjelleberg S, et al. Rapid microevolution of biofilm cells in response to antibiotics. Npj Biofilms Microbiomes. 2019;5(1). Available from: https://doi.org/http://dx.doi.org/10.1038/s41522-019-0108-3
  • Chambers JR, Cherny KE, Sauer K. Susceptibility of Pseudomonas aeruginosa dispersed cells to antimicrobial agents is dependent on the dispersion cue and class of the antimicrobial agent used. Antimicrob Agents Chemother. 2017;61(12):1–18.
  • Gernot LM, Tanja Z, Simone K. Analysis and characterization of Staphylococcus aureus small colony variants isolated from cystic fibrosis patients in Austria. Curr Microbiol. 2016;72(5):606–611.
  • Fux C, Wilson S, Stoodley P. Detachment characteristics and oxacillin resistance of Staphyloccocus aureus biofilm emboli in an in vitro catheter infection model. J Bacteriol. 2004;186(14):4486–4491.
  • Guilhen C, Miquel S, Charbonnel N, et al. Colonization and immune modulation properties of Klebsiella pneumoniae biofilm-dispersed cells. Npj Biofilms Microbiomes. 2019;5(1). https://doi.org/10.1038/s41522-019-0098-1.
  • Chua SL, Liu Y, Kuok J, et al. lifestyles. Nat Commun. 2014;5:1–12.
  • Pettigrew MM, Marks LR, Kong Y, et al. Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection. Infect Immun. 2014;82(11):4607–4619. .
  • Merghni A, Ben Nejma M, Dallel I, et al. High potential of adhesion to biotic and abiotic surfaces by opportunistic Staphylococcus aureus strains isolated from orthodontic appliances. Microb Pathog. 2016;91:61–67.
  • Struve C, Bojer M, Krogfelt KA. Characterization of Klebsiella pneumoniae type 1 fimbriae by detection of phase variation during colonization and infection and impact on virulence. Infect Immun. 2008;76:4055–4065. Available from: https://pubmed.ncbi.nlm.nih.gov/18559432
  • Wilksch JJ, Yang J, Clements A, et al. MrkH, a Novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating Type 3 fimbriae expression. PLOS Pathog. 2011;7(8):e1002204.
  • Pakharukova N, Tuittila M, Paavilainen S, et al. Structural basis for Acinetobacter baumannii biofilm formation. Proc Natl Acad Sci U S A. 2018;115(21):5558–5563. .
  • Weidensdorfer M, Ishikawa M, Hori K, et al. The Acinetobacter trimeric autotransporter adhesin Ata controls key virulence traits of Acinetobacter baumannii. Virulence. 2019;10(1):68–81.
  • Dueholm MS, Søndergaard MT, Nilsson M, et al. Expression of Fap amyloids in Pseudomonas aeruginosa, P . fluorescens, and P. putida results in aggregation and increased biofilm formation. Microbiologyopen. 2013;2(3):365–382.
  • Silva VO, Soares LO, Silva Júnior A, et al. Biofilm formation on biotic and abiotic surfaces in the presence of antimicrobials by Escherichia coli Isolates from cases of bovine mastitis. Appl Environ Microbiol. 2014;80:6136–6145. (19).

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