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Biofilms: Formation, drug resistance and alternatives to conventional approaches

Ruba Mirghani, Tania Saba, Hebba Khaliq and 11 more

AIMS Microbiology · 2022 · Review

doi:10.3934/microbiol.2022019

Abstract

<abstract> <p>Biofilms are aggregates of bacteria, in most cases, which are resistant usually to broad-spectrum antibiotics in their typical concentrations or even in higher doses. A trend of increasing multi-drug resistance in biofilms, which are responsible for emerging life-threatening nosocomial infections, is becoming a serious problem. Biofilms, however, are at various sensitivity levels to environmental factors and are versatile in infectivity depending on virulence factors. This review presents the fundamental information about biofilms: formation, antibiotic resistance, impacts on public health and alternatives to conventional approaches. Novel developments in micro-biosystems that help reveal the new treatment tools by sensing and characterization of biofilms will also be discussed. Understanding the formation, structure, physiology and properties of biofilms better helps eliminate them by the usage of appropriate antibiotics or their control by novel therapy approaches, such as anti-biofilm molecules, effective gene editing, drug-delivery systems and probiotics.</p> </abstract>

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    Schaudinn C, Gorur A, Keller D, et al. Periodontitis: an archetypical biofilm disease. J Am Dent Assoc. 2009;140:978-986.

    Not in our library10.14219/jada.archive.2009.0307

  133. 133.

    Naginyte M, Do T, Meade J, et al. Enrichment of periodontal pathogens from the biofilms of healthy adults. Sci Rep. 2019;9:5491.

    Not in our library10.1038/s41598-019-41882-y

  134. 134.

    Chandki R, Banthia P, Banthia R. Biofilms: A microbial home. J Indian Soc Periodontol. 2011;15:111-114.

    Not in our library10.4103/0972-124x.84377

  135. 135.

    Brady RA, Leid JG, Calhoun JH, et al. Osteomyelitis and the role of biofilms in chronic infection. FEMS Immunol Med Microbiol. 2008;52:13-22.

    Not in our library10.1111/j.1574-695x.2007.00357.x

  136. 136.
  137. 137.

    Rochford ETJ, Sabaté Brescó M, Zeiter S, et al. Monitoring immune responses in a mouse model of fracture fixation with and without Staphylococcus aureus osteomyelitis. Bone. 2016;83:82-92.

    Not in our library10.1016/j.bone.2015.10.014

  138. 138.

    Oates A, Bowling FL, Boulton AJM, et al. The visualization of biofilms in chronic diabetic foot wounds using routine diagnostic microscopy methods. J Diabetes Res. 2014;2014:153586.

    Not in our library10.1155/2014/153586

  139. 139.

    Clinton A, Carter T. Chronic wound biofilms: Pathogenesis and potential therapies. Lab Med. 2015;46:277-284.

    Not in our library10.1309/lmbnswkui4jpn7so

  140. 140.

    Bjarnsholt T. The role of bacterial biofilms in chronic infections. APMIS Suppl. 2013;1-51.

    Not in our library10.1111/apm.12099

  141. 141.

    Burmølle M, Thomsen TR, Fazli M, et al. Biofilms in chronic infections-a matter of opportunity-monospecies biofilms in multispecies infections. FEMS Immunol Med Microbiol. 2010;59:324-336.

    Not in our library10.1111/j.1574-695x.2010.00714.x

  142. 142.

    Percival SL, McCarty SM, Lipsky B. Biofilms and wounds: An overview of the evidence. Adv Wound Care. 2015;4:373-381.

    Not in our library10.1089/wound.2014.0557

  143. 143.
  144. 144.

    Høiby N, Ciofu O, Bjarnsholt T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol. 2010;5:1663-1674.

    Not in our library10.2217/fmb.10.125

  145. 145.

    Moreau-Marquis S, Stanton BA, O'Toole GA. Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm Pharmacol Ther. 2008;21:595-599.

    Not in our library10.1016/j.pupt.2007.12.001

  146. 146.

    Lalani T, Kanafani ZA, Chu VH, et al. Prosthetic valve endocarditis due to coagulase-negative staphylococci: findings from the international collaboration on endocarditis merged database. Eur J Clin Microbiol Infect Dis. 2006;25:365-368.

    Not in our library10.1007/s10096-006-0141-z

  147. 147.

    van Steenbergen TJM, van Winkelhoff AJ, de Graaff J. Pathogenic synergy: mixed infections in the oral cavity. Antonie van Leeuwenhoek. 1984;50:789-798.

    Not in our library10.1007/bf02386241

  148. 148.
  149. 149.
  150. 150.

    Hall-Stoodley L, Stoodley P, Kathju S, et al. Towards diagnostic guidelines for biofilm-associated infections. FEMS Immunol Med Microbiol. 2012;65:127-145.

    Not in our library10.1111/j.1574-695x.2012.00968.x

  151. 151.

    Olson ME, Ceri H, Morck DW, et al. Biofilm bacteria: formation and comparative susceptibility to antibiotics. Can J Vet Res. 2002;66:86-92.

    Not in our library

  152. 152.

    Mosaddad SA, Tahmasebi E, Yazdanian A, et al. Oral microbial biofilms: an update. Eur J Clin Microbiol Infect Dis. 2019;38:2005-2019.

    Not in our library10.1007/s10096-019-03641-9

  153. 153.

    Fair RJ, Tor Y. Antibiotics and bacterial resistance in the 21st century. Perspect Med Chem. 2014;6:25-64.

    Not in our library10.4137/pmc.s14459

  154. 154.

    Hedberg M, Nord CE. Beta-lactam resistance in anaerobic bacteria: a review. J Chemother. 1996;8:3-16.

    Not in our library10.1179/joc.1996.8.1.3

  155. 155.

    Macià MD, Rojo-Molinero E, Oliver A. Antimicrobial susceptibility testing in biofilm-growing bacteria. Clin Microbiol Infect. 2014;20:981-990.

    Not in our library10.1111/1469-0691.12651

  156. 156.

    Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother. 2001;45:999.

    Not in our library10.1128/aac.45.4.999-1007.2001

  157. 157.
  158. 158.
  159. 159.

    Wozniak DJ, Wyckoff TJ, Starkey M, et al. Alginate is not a significant component of the extracellular polysaccharide matrix of PA14 and PAO1 Pseudomonas aeruginosa biofilms. Proc Natl Acad Sci U S A. 2003;100:7907-7912.

    Not in our library10.1073/pnas.1231792100

  160. 160.

    Madsen JS, Burmølle M, Hansen LH, et al. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol. 2012;65:183-195.

    Not in our library10.1111/j.1574-695x.2012.00960.x

  161. 161.

    Lister PD, Wolter DJ, Hanson ND. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin Microbiol Rev. 2009;22:582-610.

    Not in our library10.1128/cmr.00040-09

  162. 162.

    Wilton M, Charron-Mazenod L, Moore R, et al. Extracellular DNA acidifies biofilms and induces aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2015;60:544-553.

    Not in our library10.1128/aac.01650-15

  163. 163.
  164. 164.

    Heilmann C, Hartleib J, Hussain MS, et al. The multifunctional Staphylococcus aureus autolysin aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect Immunol. 2005;73:4793-4802.

    Not in our library10.1128/iai.73.8.4793-4802.2005

  165. 165.

    Heilmann C, Hussain M, Peters G, et al. Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol. 1997;24:1013-1024.

    Not in our library10.1046/j.1365-2958.1997.4101774.x

  166. 166.

    Ch'ng JH, Chong KKL, Lam LN, et al. Biofilm-associated infection by enterococci. Nat Rev Microbiol. 2019;17:82-94.

    Not in our library10.1038/s41579-018-0107-z

  167. 167.
  168. 168.
  169. 169.

    Schilcher K, Horswill AR. Staphylococcal biofilm development: Structure, regulation, and treatment strategies. Microbiol Mol Biol Rev. 2020;84:e00026-19.

    Not in our library10.1128/mmbr.00026-19

  170. 170.
  171. 171.
  172. 172.
  173. 173.
  174. 174.

    Ramos-Vivas J, Chapartegui-González I, Fernández-Martínez M, et al. Biofilm formation by multidrug resistant Enterobacteriaceae strains isolated from solid organ transplant recipients. Sci Rep. 2019;9:8928.

    Not in our library10.1038/s41598-019-45060-y

  175. 175.
  176. 176.

    Smani Y, McConnell MJ, Pachón J, et al. Role of fibronectin in the adhesion of Acinetobacter baumannii to host cells. PLoS One. 2012;7:e33073.

    Not in our library10.1371/journal.pone.0033073

  177. 177.

    Gaddy JA, Tomaras AP, Actis LA. The Acinetobacter baumannii 19606 OmpA protein plays a role in biofilm formation on abiotic surfaces and in the interaction of this pathogen with eukaryotic cells. Infect Immun. 2009;77:3150-3160.

    Not in our library10.1128/iai.00096-09

  178. 178.
  179. 179.

    Poulsen LK, Ballard G, Stahl DA. Use of rRNA fluorescence in situ hybridization for measuring the activity of single cells in young and established biofilms. Appl Environ Microbiol. 1993;59:1354-1360.

    Not in our library10.1128/aem.59.5.1354-1360.1993

  180. 180.

    Sternberg C, Christensen BB, Johansen T, et al. Distribution of bacterial growth activity in flow-chamber biofilms. Appl Environ Microbiol. 1999;65:4108-4117.

    Not in our library10.1128/aem.65.9.4108-4117.1999

  181. 181.

    Mitchison JM. Enzyme synthesis in synchronous cultures. Science. 1969;165:657-663.

    Not in our library10.1126/science.165.3894.657

  182. 182.

    Gilbert P, Maira-Litran T, McBain AJ, et al. The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol. 2002;46:202-256.

    Not in our library10.1016/s0065-2911(02)46005-5

  183. 183.

    Walters MC, Roe F, Bugnicourt A, et al. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother. 2003;47:317-323.

    Not in our library10.1128/aac.47.1.317-323.2003

  184. 184.

    Tresse O, Jouenne T, Junter GA. The role of oxygen limitation in the resistance of agar-entrapped, sessile-like Escherichia coli to aminoglycoside and beta-lactam antibiotics. J Antimicrob Chemother. 1995;36:521-526.

    Not in our library10.1093/jac/36.3.521

  185. 185.

    Hall CW, Mah TF. Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev. 2017;41:276-301.

    Not in our library10.1093/femsre/fux010

  186. 186.

    Zheng Z, Stewart PS. Growth limitation of Staphylococcus epidermidis in biofilms contributes to rifampin tolerance. Biofilms. 2004;1:31-35.

    Not in our library10.1017/s1479050503001042

  187. 187.

    Mah TFC, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 2001;9:34-39.

    Not in our library10.1016/s0966-842x(00)01913-2

  188. 188.
  189. 189.

    Shih PC, Huang CT. Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. J Antimicrob Chemother. 2002;49:309-314.

    Not in our library10.1093/jac/49.2.309

  190. 190.

    Algburi A, Comito N, Kashtanov D, et al. Control of biofilm formation: Antibiotics and beyond. Appl Environ Microbiol. 2017;83:e02508-02516.

    Not in our library10.1128/aem.02508-16

  191. 191.
  192. 192.

    Klemm P, Vejborg RM, Hancock V. Prevention of bacterial adhesion. Appl Microbiol Biotechnol. 2010;88:451-459.

    Not in our library10.1007/s00253-010-2805-y

  193. 193.

    Veerachamy S, Yarlagadda T, Manivasagam G, et al. Bacterial adherence and biofilm formation on medical implants: A review. Proc Inst Mech Eng, Part H. 2014;228:1083-1099.

    Not in our library10.1177/0954411914556137

  194. 194.

    Chow JY, Yang Y, Tay SB, et al. Disruption of biofilm formation by the human pathogen Acinetobacter baumannii using engineered quorum-quenching lactonases. Antimicrob Agents Chemother. 2014;58:1802-1805.

    Not in our library10.1128/aac.02410-13

  195. 195.
  196. 196.
  197. 197.

    Gil C, Solano C, Burgui S, et al. Biofilm matrix exoproteins induce a protective immune response against Staphylococcus aureus biofilm infection. Infect Immun. 2014;82:1017-1029.

    Not in our library10.1128/iai.01419-13

  198. 198.

    Jiang Q, Jin Z, Sun B. MgrA negatively regulates biofilm formation and detachment by repressing the expression of psm operons in Staphylococcus aureus. Appl Environ Microbiol. 2018;84.

    Not in our library10.1128/aem.01008-18

  199. 199.
  200. 200.

    Gallant CV, Daniels C, Leung JM, et al. Common beta-lactamases inhibit bacterial biofilm formation. Mol Microbiol. 2005;58:1012-1024.

    Not in our library10.1111/j.1365-2958.2005.04892.x

  201. 201.

    Reza A, Sutton JM, Rahman KM. Effectiveness of efflux pump inhibitors as biofilm disruptors and resistance breakers in Gram-Negative (ESKAPEE) bacteria. Antibiotics (Basel,Switz). 2019;8:229.

    Not in our library10.3390/antibiotics8040229

  202. 202.

    Ciofu O, Rojo-Molinero E, Macià MD, et al. Antibiotic treatment of biofilm infections. APMIS. 2017;125:304-319.

    Not in our library10.1111/apm.12673

  203. 203.

    Brooun A, Liu S, Lewis K. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother. 2000;44:640-646.

    Not in our library10.1128/aac.44.3.640-646.2000

  204. 204.

    Danese PN. Antibiofilm Approaches: Prevention of Catheter Colonization. Chem Biol. 2002;9:873-880.

    Not in our library10.1016/s1074-5521(02)00192-8

  205. 205.

    Flemming HC, Ridgway H, Flemming HC, Murthy PS, Venkatesan R, et al. Biofilm control: Conventional and alternative approaches. Marine and Industrial Biofouling. 2009;103-117.

    Not in our library10.1007/978-3-540-69796-1_5

  206. 206.

    Sambanthamoorthy K, Gokhale AA, Lao W, et al. Identification of a novel benzimidazole that inhibits bacterial biofilm formation in a broad-spectrum manner. Antimicrob Agents Chemother. 2011;55:4369.

    Not in our library10.1128/aac.00583-11

  207. 207.

    Dinicola S, De Grazia S, Carlomagno G, et al. N-acetylcysteine as powerful molecule to destroy bacterial biofilms. A systematic review. Eur Rev Med Pharmacol Sci. 2014;18:2942-2948.

    Not in our library

  208. 208.

    Abraham NM, Lamlertthon S, Fowler VG, et al. Chelating agents exert distinct effects on biofilm formation in Staphylococcus aureus depending on strain background: role for clumping factor B. J Med Microbiol. 2012;61:1062-1070.

    Not in our library10.1099/jmm.0.040758-0

  209. 209.

    Antoci V, Adams CS, Parvizi J, et al. The inhibition of Staphylococcus epidermidis biofilm formation by vancomycin-modified titanium alloy and implications for the treatment of periprosthetic infection. Biomaterials. 2008;29:4684-4690.

    Not in our library10.1016/j.biomaterials.2008.08.016

  210. 210.

    Ma Y, Chen M, Jones JE, et al. Inhibition of Staphylococcus epidermidis biofilm by trimethylsilane plasma coating. Antimicrob Agents Chemother. 2012;56:5923-5937.

    Not in our library10.1128/aac.01739-12

  211. 211.

    Sanyasi S, Majhi RK, Kumar S, et al. Polysaccharide-capped silver nanoparticles inhibit biofilm formation and eliminate multi-drug-resistant bacteria by disrupting bacterial cytoskeleton with reduced cytotoxicity towards mammalian cells. Sci Rep. 2016;6:24929.

    Not in our library10.1038/srep24929

  212. 212.

    AshaRani PV, Low Kah Mun G, Hande MP, et al. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano. 2009;3:279-290.

    Not in our library10.1021/nn800596w

  213. 213.

    Raie DS, Mhatre E, Thiele M, et al. Application of quercetin and its bio-inspired nanoparticles as anti-adhesive agents against Bacillus subtilis attachment to surface. Mater Sci Eng, C. 2017;70:753-762.

    Not in our library10.1016/j.msec.2016.09.038

  214. 214.

    Hume EB, Baveja J, Muir B, et al. The control of Staphylococcus epidermidis biofilm formation and in vivo infection rates by covalently bound furanones. Biomaterials. 2004;25:5023-5030.

    Not in our library10.1016/j.biomaterials.2004.01.048

  215. 215.

    Li H, Bao H, Bok KX, et al. High durability and low toxicity antimicrobial coatings fabricated by quaternary ammonium silane copolymers. Biomater Sci. 2016;4:299-309.

    Not in our library10.1039/c5bm00353a

  216. 216.

    Trentin DS, Silva DB, Frasson AP, et al. Natural green coating inhibits adhesion of clinically important bacteria. Sci Rep. 2015;5:8287.

    Not in our library10.1038/srep08287

  217. 217.
  218. 218.

    Tran PL, Lowry N, Campbell T, et al. An organoselenium compound inhibits Staphylococcus aureus biofilms on hemodialysis catheters in vivo. Antimicrob Agents Chemother. 2012;56:972-978.

    Not in our library10.1128/aac.05680-11

  219. 219.

    Zhao X, Zhao F, Wang J, et al. Biofilm formation and control strategies of foodborne pathogens: food safety perspectives. RSC Adv. 2017;7:36670-36683.

    Not in our library10.1039/c7ra02497e

  220. 220.

    de Sousa DG, Harvey LA, Dorsch S, et al. Interventions involving repetitive practice improve strength after stroke: a systematic review. J Physiother. 2018;64:210-221.

    Not in our library10.1016/j.jphys.2018.08.004

  221. 221.

    Chappell TC, Nair NU. Engineered lactobacilli display anti-biofilm and growth suppressing activities against Pseudomonas aeruginosa. npj Biofilms Microbiomes. 2020;6:48.

    Not in our library10.1038/s41522-020-00156-6

  222. 222.
  223. 223.

    Bendaoud M, Vinogradov E, Balashova NV, et al. Broad-spectrum biofilm inhibition by Kingella kingae exopolysaccharide. J Bacteriol Res. 2011;193:3879-3886.

    Not in our library10.1128/jb.00311-11

  224. 224.

    Mi L, Licina GA, Jiang S. Nonantibiotic-Based Pseudomonas aeruginosa biofilm inhibition with osmoprotectant analogues. ACS Sustainable Chem Eng. 2014;2:2448-2453.

    Not in our library10.1021/sc500468a

  225. 225.

    Kuang X, Chen V, Xu X. Novel approaches to the control of oral microbial biofilms. BioMed Res Int. 2018;2018:6498932.

    Not in our library10.1155/2018/6498932

  226. 226.

    Chen H, Zhang B, Weir MD, et al. S. mutans gene-modification and antibacterial resin composite as dual strategy to suppress biofilm acid production and inhibit caries. J Dent. 2020;93:103278.

    Not in our library10.1016/j.jdent.2020.103278

  227. 227.

    Pires DP, Melo LDR, Vilas Boas D, et al. Phage therapy as an alternative or complementary strategy to prevent and control biofilm-related infections. Curr Opin Microbiol. 2017;39:48-56.

    Not in our library10.1016/j.mib.2017.09.004

  228. 228.
  229. 229.

    Pires DP, Vilas Boas D, Sillankorva S, et al. Phage therapy: a step forward in the treatment of Pseudomonas aeruginosa infections. J Virol. 2015;89:7449-7456.

    Not in our library10.1128/jvi.00385-15

  230. 230.

    Fu W, Forster T, Mayer O, et al. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother. 2010;54:397-404.

    Not in our library10.1128/aac.00669-09

  231. 231.
  232. 232.

    Singh VK, Mishra A, Jha B. Anti-quorum sensing and anti-biofilm activity of delftia tsuruhatensis extract by attenuating the quorum sensing-controlled virulence factor production in Pseudomonas aeruginosa. Front Cell Infect Microbiol. 2017;7.

    Not in our library10.3389/fcimb.2017.00337

  233. 233.
  234. 234.

    Kalaiarasan E, Thirumalaswamy K, Harish BN, et al. Inhibition of quorum sensing-controlled biofilm formation in Pseudomonas aeruginosa by quorum-sensing inhibitors. Microb Pathog. 2017;111:99-107.

    Not in our library10.1016/j.micpath.2017.08.017

  235. 235.

    Bulman ZP, Ly NS, Lenhard JR, et al. Influence of rhlR and lasR on polymyxin pharmacodynamics in Pseudomonas aeruginosa and implications for quorum sensing inhibition with azithromycin. Antimicrob Agents Chemother. 2017;61.

    Not in our library10.1128/aac.00096-16

  236. 236.

    Maura D, Rahme LG. Pharmacological inhibition of the Pseudomonas aeruginosa MvfR quorum-sensing system interferes with biofilm formation and potentiates antibiotic-mediated biofilm disruption. Antimicrob Agents Chemother. 2017;61.

    Not in our library10.1128/aac.01362-17

  237. 237.

    Stenvang M, Dueholm MS, Vad BS, et al. Epigallocatechin gallate remodels overexpressed functional amyloids in Pseudomonas aeruginosa and increases biofilm susceptibility to antibiotic treatment*. J Biol Chem. 2016;291:26540-26553.

    Not in our library10.1074/jbc.m116.739953

  238. 238.

    Guo Q, Wei Y, Xia B, et al. Identification of a small molecule that simultaneously suppresses virulence and antibiotic resistance of Pseudomonas aeruginosa. Sci Rep. 2016;6:19141.

    Not in our library10.1038/srep19141

  239. 239.

    Freire MO, Devaraj A, Young A, et al. A bacterial-biofilm-induced oral osteolytic infection can be successfully treated by immuno-targeting an extracellular nucleoid-associated protein. Mol Oral Microbiol. 2017;32:74-88.

    Not in our library10.1111/omi.12155

  240. 240.

    Sun D, Accavitti MA, Bryers JD. Inhibition of biofilm formation by monoclonal antibodies against Staphylococcus epidermidis RP62A accumulation-associated protein. Clin Diagn Lab Immunol. 2005;12:93-100.

    Not in our library10.1128/cdli.12.1.93-100.2005

  241. 241.

    Estellés A, Woischnig AK, Liu K, et al. A high-affinity native human antibody disrupts biofilm from Staphylococcus aureus bacteria and potentiates antibiotic efficacy in a mouse implant infection model. Antimicrob Agents Chemother. 2016;60:2292-2301.

    Not in our library10.1128/aac.02588-15

  242. 242.

    Hall AE, Domanski PJ, Patel PR, et al. Characterization of a protective monoclonal antibody recognizing Staphylococcus aureus MSCRAMM protein clumping factor A. Infect Immun. 2003;71:6864-6870.

    Not in our library10.1128/iai.71.12.6864-6870.2003

  243. 243.

    Visai L, Xu Y, Casolini F, et al. Monoclonal antibodies to CNA, a collagen-binding microbial surface component recognizing adhesive matrix molecules, detach Staphylococcus aureus from a collagen substrate. J Biol Chem. 2000;275:39837-39845.

    Not in our library10.1074/jbc.m005297200

  244. 244.

    Rennermalm A, Li YH, Bohaufs L, et al. Antibodies against a truncated Staphylococcus aureus fibronectin-binding protein protect against dissemination of infection in the rat. Vaccine. 2001;19:3376-3383.

    Not in our library10.1016/s0264-410x(01)00080-9

  245. 245.

    Belyi Y, Rybolovlev I, Polyakov N, et al. Staphylococcus aureus surface protein G is an immunodominant protein and a possible target in an anti-biofilm drug development. Open Microbiol J. 2018;12:94-106.

    Not in our library10.2174/1874285801812010094

  246. 246.

    Haghighat S, Siadat SD, Sorkhabadi SM, et al. Cloning, expression and purification of autolysin from methicillin-resistant Staphylococcus aureus: potency and challenge study in Balb/c mice. Mol Immunol. 2017;82:10-18.

    Not in our library10.1016/j.molimm.2016.12.013

  247. 247.

    Nair N, Vinod V, Suresh MK, et al. Amidase, a cell wall hydrolase, elicits protective immunity against Staphylococcus aureus and S. epidermidis. Int J Biol Macromol. 2015;77:314-321.

    Not in our library10.1016/j.ijbiomac.2015.03.047

  248. 248.

    Varrone JJ, de Mesy Bentley KL, Bello-Irizarry SN, et al. Passive immunization with anti-glucosaminidase monoclonal antibodies protects mice from implant-associated osteomyelitis by mediating opsonophagocytosis of Staphylococcus aureus megaclusters. J Orthop Res. 2014;32:1389-1396.

    Not in our library10.1002/jor.22672

  249. 249.

    van den Berg S, Bonarius HP, van Kessel KP, et al. A human monoclonal antibody targeting the conserved Staphylococcal antigen IsaA protects mice against Staphylococcus aureus bacteremia. Int J Med Microbiol. 2015;305:55-64.

    Not in our library10.1016/j.ijmm.2014.11.002

  250. 250.

    Liu B, Park S, Thompson CD, et al. Antibodies to Staphylococcus aureus capsular polysaccharides 5 and 8 perform similarly in vitro but are functionally distinct in vivo. Virulence. 2017;8:859-874.

    Not in our library10.1080/21505594.2016.1270494

  251. 251.

    Weisman LE. Antibody for the prevention of neonatal noscocomial Staphylococcal infection: a review of the literature. Arch Pediatr. 2007;14 Suppl 1:S31-34.

    Not in our library10.1016/s0929-693x(07)80008-x

  252. 252.

    Raafat D, Otto M, Reppschläger K, et al. Fighting Staphylococcus aureus biofilms with monoclonal antibodies. Trends Microbiol. 2019;27:303-322.

    Not in our library10.1016/j.tim.2018.12.009

  253. 253.

    Freire-Moran L, Aronsson B, Manz C, et al. Critical shortage of new antibiotics in development against multidrug-resistant bacteria-time to react is now. Drug Resist Updat. 2011;14:118-124.

    Not in our library10.1016/j.drup.2011.02.003

  254. 254.

    Banerjee M, Moulick S, Bhattacharya KK, et al. Attenuation of Pseudomonas aeruginosa quorum sensing, virulence and biofilm formation by extracts of Andrographis paniculata. Microb Pathog. 2017;113:85-93.

    Not in our library10.1016/j.micpath.2017.10.023

  255. 255.

    Zhang L, Bao M, Liu B, et al. Effect of andrographolide and its analogs on bacterial infection: A review. Pharmacology. 2020;105:123-134.

    Not in our library10.1159/000503410

  256. 256.

    Rasool U, SP, Parveen A, et al. Efficacy of andrographis paniculata against extended spectrum β-lactamase (ESBL) producing E. coli. BMC Complementary Altern Med. 2018;18:244-244.

    Not in our library10.1186/s12906-018-2312-8

  257. 257.

    Carrol DH, Chassagne F, Dettweiler M, et al. Antibacterial activity of plant species used for oral health against Porphyromonas gingivalis. PLoS One. 2020;15:e0239316.

    Not in our library10.1371/journal.pone.0239316

  258. 258.
  259. 259.

    Liu G, Xiang H, Tang X, et al. Transcriptional and functional analysis shows sodium houttuyfonate-mediated inhibition of autolysis in Staphylococcus aureus. Molecules (Basel,Switz). 2011;16:8848-8865.

    Not in our library10.3390/molecules16108848

  260. 260.

    Zhou J, Bi S, Chen H, et al. Anti-Biofilm and antivirulence activities of metabolites from plectosphaerella cucumerina against Pseudomonas aeruginosa. Front Microbiol. 2017;8:769.

    Not in our library10.3389/fmicb.2017.00769

  261. 261.

    Rabin N, Zheng Y, Opoku-Temeng C, et al. Agents that inhibit bacterial biofilm formation. Future Med Chem. 2015;7:647-671.

    Not in our library10.4155/fmc.15.7

  262. 262.

    Xiang H, Cao F, Ming D, et al. Aloe-emodin inhibits Staphylococcus aureus biofilms and extracellular protein production at the initial adhesion stage of biofilm development. Appl Microbiol Biotechnol. 2017;101:6671-6681.

    Not in our library10.1007/s00253-017-8403-5

  263. 263.

    Jakobsen TH, van Gennip M, Phipps RK, et al. Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Antimicrob Agents Chemother. 2012;56:2314-2325.

    Not in our library10.1128/aac.05919-11

  264. 264.

    Balcázar JL, Vendrell D, de Blas I, et al. Characterization of probiotic properties of lactic acid bacteria isolated from intestinal microbiota of fish. Aquaculture. 2008;278:188-191.

    Not in our library10.1016/j.aquaculture.2008.03.014

  265. 265.

    Didinen BI, Onuk EE, Metin S, et al. Identification and characterization of lactic acid bacteria isolated from rainbow trout (Oncorhynchus mykiss, Walbaum 1792), with inhibitory activity against Vagococcus salmoninarum and Lactococcus garvieae. Aquacult Nutr. 2018;24:400-407.

    Not in our library10.1111/anu.12571

  266. 266.

    Ben Taheur F, Kouidhi B, Fdhila K, et al. Anti-bacterial and anti-biofilm activity of probiotic bacteria against oral pathogens. Microb Pathog. 2016;97:213-220.

    Not in our library10.1016/j.micpath.2016.06.018

  267. 267.

    Lee DK, Park SY, An HM, et al. Antimicrobial activity of Bifidobacterium spp. isolated from healthy adult Koreans against cariogenic microflora. Arch Oral Biol. 2011;56:1047-1054.

    Not in our library10.1016/j.archoralbio.2011.03.002

  268. 268.

    Schwendicke F, Horb K, Kneist S, et al. Effects of heat-inactivated Bifidobacterium BB12 on cariogenicity of Streptococcus mutans in vitro. Arch Oral Biol. 2014;59:1384-1390.

    Not in our library10.1016/j.archoralbio.2014.08.012

  269. 269.

    Suzuki N, Yoneda M, Hatano Y, et al. Enterococcus faecium WB2000 inhibits biofilm formation by oral cariogenic Streptococci. Int J Dent. 2011;2011:834151.

    Not in our library10.1155/2011/834151

  270. 270.

    Sassone-Corsi M, Raffatellu M. No vacancy: how beneficial microbes cooperate with immunity to provide colonization resistance to pathogens. J immunol. 2015;194:4081-4087.

    Not in our library10.4049/jimmunol.1403169

  271. 271.

    Tuomola EM, Ouwehand AC, Salminen SJ. The effect of probiotic bacteria on the adhesion of pathogens to human intestinal mucus. FEMS Immunol Med Microbiol. 1999;26:137-142.

    Not in our library10.1111/j.1574-695x.1999.tb01381.x

  272. 272.

    Yan F, Polk DB. Probiotics and immune health. Curr Opin Gastroenterol. 2011;27:496-501.

    Not in our library10.1097/mog.0b013e32834baa4d

  273. 273.

    Hegarty JW, Guinane CM, Ross RP, et al. Bacteriocin production: a relatively unharnessed probiotic trait? F1000Res. 2016;5:2587.

    Not in our library10.12688/f1000research.9615.1

  274. 274.

    Corcoran BM, Stanton C, Fitzgerald GF, et al. Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol. 2005;71:3060-3067.

    Not in our library10.1128/aem.71.6.3060-3067.2005

  275. 275.

    Vuotto C, Longo F, Donelli G. Probiotics to counteract biofilm-associated infections: promising and conflicting data. Int J Oral Sci. 2014;6:189-194.

    Not in our library10.1038/ijos.2014.52

  276. 276.

    Fang K, Jin X, Hong SH. Probiotic Escherichia coli inhibits biofilm formation of pathogenic E. coli via extracellular activity of DegP. Sci Rep. 2018;8:4939.

    Not in our library10.1038/s41598-018-23180-1

  277. 277.

    Jaffar N, Ishikawa Y, Mizuno K, et al. Mature biofilm degradation by potential probiotics: Aggregatibacter actinomycetemcomitans versus LactoBacillus spp. PLoS One. 2016;11:e0159466.

    Not in our library10.1371/journal.pone.0159466

  278. 278.
  279. 279.

    Hertzberger R, Arents J, Dekker Henk L, et al. H2O2 production in species of the LactoBacillus acidophilus group: a central role for a novel NADH-Dependent flavin reductase. Appl Environ Microbiol. 2014;80:2229-2239.

    Not in our library10.1128/aem.04272-13

  280. 280.
  281. 281.
  282. 282.

    Barzegari A, Kheyrolahzadeh K, Hosseiniyan Khatibi SM, et al. The battle of probiotics and their derivatives against biofilms. Infect Drug Resist. 2020;13:659-672.

    Not in our library10.2147/idr.s232982

  283. 283.
  284. 284.

    Tan L, Fu J, Feng F, et al. Engineered probiotics biofilm enhances osseointegration via immunoregulation and anti-infection. Sci Adv. 2020;6:eaba5723.

    Not in our library10.1126/sciadv.aba5723

  285. 285.

    Carvalho FM, Teixeira-Santos R, Mergulhão FJM, et al. The use of probiotics to fight biofilms in medical devices: A systematic review and meta-analysis. Microorganisms. 2020;9.

    Not in our library10.3390/microorganisms9010027

  286. 286.

    Gholizadeh P, Aghazadeh M, Asgharzadeh M, et al. Suppressing the CRISPR/Cas adaptive immune system in bacterial infections. Eur J Clin Microbiol Infect Dis. 2017;36:2043-2051.

    Not in our library10.1007/s10096-017-3036-2

  287. 287.

    Yao R, Liu D, Jia X, et al. CRISPR-Cas9/Cas12a biotechnology and application in bacteria. Synth Syst Biotechnol. 2018;3:135-149.

    Not in our library10.1016/j.synbio.2018.09.004

  288. 288.

    Jiang W, Bikard D, Cox D, et al. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol. 2013;31:233-239.

    Not in our library10.1038/nbt.2508

  289. 289.

    Goren M, Yosef I, Qimron U. Sensitizing pathogens to antibiotics using the CRISPR-Cas system. Drug Resist Updat. 2017;30:1-6.

    Not in our library10.1016/j.drup.2016.11.001

  290. 290.

    Touchon M, Charpentier S, Pognard D, et al. Antibiotic resistance plasmids spread among natural isolates of Escherichia coli in spite of CRISPR elements. Microbiology (Reading). 2012;158:2997-3004.

    Not in our library10.1099/mic.0.060814-0

  291. 291.

    Hale CR, Majumdar S, Elmore J, et al. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol Cell. 2012;45:292-302.

    Not in our library10.1016/j.molcel.2011.10.023

  292. 292.

    Bikard D, Euler CW, Jiang W, et al. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat Biotechnol. 2014;32:1146-1150.

    Not in our library10.1038/nbt.3043

  293. 293.
  294. 294.

    Gholizadeh P, Köse Ş, Dao S, et al. How CRISPR-Cas system could be used to combat antimicrobial resistance. Infect Drug Resist. 2020;13:1111-1121.

    Not in our library10.2147/idr.s247271

  295. 295.
  296. 296.

    Gong T, Tang B, Zhou X, et al. Genome editing in Streptococcus mutans through self-targeting CRISPR arrays. Mol Oral Microbiol. 2018;33:440-449.

    Not in our library10.1111/omi.12247

  297. 297.

    Garrido V, Piñero-Lambea C, Rodriguez-Arce I, et al. Engineering a genome-reduced bacterium to eliminate Staphylococcus aureus biofilms in vivo. Mol Syst Biol. 2021;17:e10145.

    Not in our library10.15252/msb.202010145

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