504
Views
7
CrossRef citations to date
0
Altmetric
Review

Bacterial biofilm-derived antigens: a new strategy for vaccine development against infectious diseases

, , ORCID Icon, & ORCID Icon
Pages 385-396 | Received 28 Apr 2020, Accepted 16 Feb 2021, Published online: 08 Mar 2021

References

  • Yin W, Wang Y, Liu L, et al. “Protective clothing” in extreme environments. Int J Mol Scien. 2019;20(14):3423.
  • Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol. 2010;8(9):623.
  • Bjarnsholt T, Alhede M, Eickhardt-Sorensen SR, et al. The in vivo biofilm. Trends Microbiol. 2013;21(9):466–474.
  • Kragh KN, Hutchison JB, Melaugh G, et al. Role of multicellular aggregates in biofilm formation. mBio. 2016;7(2):e00237–16.
  • Tremblay YDN, Labrie J, Chénier S, et al. Actinobacillus pleuropneumoniae grows as aggregates in the lung of pigs: is it time to refine our in vitro biofilm assays? Microb Biotechnol. 2017;10(4):756–760.
  • Carron MA, Tran VR, Sugawa C, et al. Identification of Helicobacter pylori biofilms in human gastric mucosa. J Gastrointest Surg. 2006;10(5):712–717.
  • Sanchez-Vizuete P, Orgaz B, Aymerich S, et al. Pathogens protection against the action of disinfectants in multispecies biofilms. Front Microbiol. 2015;6:705.
  • Hengge R. Linking bacterial growth, survival, and multicellularity - small signaling molecules as triggers and drivers. Curr Opin Microbiol. 2020;55:57–66.
  • Hathroubi S, Mekni MA, Domenico P, et al. Biofilms: microbial shelters against antibiotics. Microbial Drug Resist. 2017;23(2):147–156.
  • Peters BM, Jabra-Rizk MA, O’May GA, et al. Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev. 2012;25(1):193–213.
  • Willems HM, Xu Z, Peters BM. Polymicrobial biofilm studies: from basic science to biofilm control. Current Oral Health Reports. 2016;3(1):36–44.
  • Loera-Muro A, Jacques M, Avelar-González FJ, et al. Auxotrophic Actinobacillus pleuropneumoniae grows in multispecies biofilms without the need for nicotinamide-adenine dinucleotide (NAD) supplementation. BMC Microbiol. 2016;16(1):128.
  • Hall-Stoodley L, Stoodley P. Evolving concepts in biofilm infections. Cel Microbiol. 2009;11(7):1034–1043.
  • Lapointe C, Deschênes L, Ells TC, et al. Interactions between spoilage bacteria in tri-species biofilms developed under simulated meat processing conditions. Food Microbiol. 2019;82:515–522.
  • Kolenbrander PE, Palmer RJ Jr, Periasamy S, et al. Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol. 2010;8(7):471–480.
  • Liu W, Røder HL, Madsen JS, et al. Interspecific bacterial interactions are reflected in multispecies biofilm spatial organization. Front Microbiol. 2016;7:1366.
  • Yang L, Liu Y, Wu H, et al. Current understanding of multi-species biofilms. Int J Oral Sci. 2011;3(2):74–81.
  • Elias S, Banin E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 2012;36(5):990–1004.
  • Zhang P, Chen YP, Qiu JH, et al. Imaging the microprocesses in biofilm matrices. Trends Biotechnol. 2019;37(2):214–226.
  • 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(3):324–336.
  • Chan CL, Richter K, Wormald PJ, et al. Alloiococcus otitidis forms multispecies biofilm with Haemophilus influenzae: effects on antibiotic susceptibility and growth in adverse conditions. Front Cell Infect Microbiol. 2017;7:344.
  • Johani K, Malone M, Jensen S, et al. Microscopy visualisation confirms multi‐species biofilms are ubiquitous in diabetic foot ulcers. Int Wound J. 2017;14(6):1160–1169.
  • Gabrilska RA, Rumbaugh KP. Biofilm models of polymicrobial infection. Future Microbiol. 2015;10(12):1997–2015.
  • Bertesteanu S, Triaridis S, Stankovic M, et al. Polymicrobial wound infections: pathophysiology and current therapeutic approaches. Int J Pharm. 2014;463(2):119–126.
  • Ledwoch K, Dancer SJ, Otter JA, et al. Beware biofilm! dry biofilms containing bacterial pathogens on multiple healthcare surfaces; a multi-centre study. J Hospital Infect. 2018;100(3):e47–e56.
  • Burmølle M, Ren D, Bjarnsholt T, et al. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 2014;22(2):84–91.
  • Alves PM, Al-Badi E, Withycombe C, et al. Interaction between Staphylococcus aureus and Pseudomonas aeruginosa is beneficial for colonization and pathogenicity in a mixed biofilm. Pathog Dis. 2018;76(1):1.
  • Pastar I, Pastar I, Nusbaum AG, et al. Interactions of methicillin resistant Staphylococcus aureus USA300 and pseudomonas aeruginosa in polymicrobial wound. Infection. 2013;8:e56846.
  • Beaudoin T, Yau YCW, Stapleton PJ, et al. Staphylococcus aureus interaction with Pseudomonas aeruginosa biofilm enhances tobramycin resistance. NPJ Biofilms Microbiomes. 2017;3(1):25.
  • Lopes SP, Ceri H, Azevedo NF, et al. Antibiotic resistance of mixed biofilms in cystic fibrosis: impact of emerging microorganisms on treatment of infection. Int J Antimicrob Agents. 2012;40:260–263.
  • Weimer KE, Armbruster CE, Juneau RA, et al. Coinfection with Haemophilus influenzae promotes pneumococcal biofilm formation during experimental otitis media and impedes the progression of pneumococcal disease. J Infect Dis. 2010;202(7):1068–1075.
  • Jacques M, Aragon V, Tremblay YD. Biofilm formation in bacterial pathogens of veterinary importance. Anim Health Res Rev. 2010;11(2):97–121.
  • Conover MS, Mishra M, Extracellular DR. Extracellular DNA Is Essential for Maintaining Bordetella biofilm integrity on abiotic surfaces and in the upper respiratory tract of mice. PLoS ONE. 2011;6(2):e16861.
  • Ramírez-Castillo FY, Loera-Muro A, Vargas-Padilla ND, et al. Incorporation of Actinobacillus pleuropneumoniae in preformed biofilms by Escherichia coli isolated from drinking water of swine farms. Front Vet Sci. 2018;5:184.
  • Tremblay YD, Caron V, Blondeau A, et al. Biofilm formation by coagulase-negative staphylococci: impact on the efficacy of antimicrobials and disinfectants commonly used on dairy farms. Vet Microbiol. 2014;172(3–4):511–518.
  • Goetz C, Tremblay YDN, Lamarche D, et al. Coagulase-negative staphylococci species affect biofilm formation of other coagulase-negative and coagulase-positive staphylococci. J Dairy Sci. 2017;100(8):6454–6464.
  • Dufour S, Labrie J, Jacques M. The mastitis pathogens culture collection. Microbiol Resour Announc. 2019;8(15):e00133–19.
  • Bordi C, De Bentzmann S. Hacking into bacterial biofilms: a new therapeutic challenge. Ann Intensive Care. 2011;1(1):19.
  • Solano C, Echeverz M, Lasa I. Biofilm dispersion and quorum sensing. Curr Opin Microbiol. 2014;18:96–104.
  • Barriuso J, Martínez MJ. In silico analysis of the quorum sensing metagenome in environmental biofilm samples. Front Microbiol. 2018;9:1243.
  • Kendall MM, Cell-to-Cell SV. Signaling in Escherichia coli and Salmonella. EcoSal Plus. 2014;6(1):6.
  • Davis BM, Jensen R, Williams P, et al. The interaction of N-Acylhomoserine lactone quorum sensing signaling molecules with biological membranes: implications for inter-kingdom signaling. PLoS ONE. 2010;5(10):e13522.
  • Hardie KR, Heurlier K. Establishing bacterial communities by ‘word of mouth’: luxS and autoinducer 2 in biofilm development. Nat Rev Microbiol. 2008;6(8):635–643.
  • Papenfort K, Bassler BL. Quorum sensing signal-response systems in Gram-negative bacteria. Nat Rev Microbiol. 2016;14(9):576–588.
  • Rao RM, Pasha SN, Sowdhamini R. Genome-wide survey and phylogeny of S-ribosylhomocysteinase (LuxS) enzyme in bacterial genomes. BMC Genomics. 2016;17(1):742.
  • Defoirdt T. Quorum-Sensing systems as targets for antivirulence therapy. Trends Microbiol. 2018;26(4):313–328.
  • LaSarre B, Federle MJ. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev. 2013;77:73–111.
  • Thompson JA, Oliveira RA, Xavier KB. Chemical conversations in the gut microbiota. Gut Microbes. 2016;7(2):163–170.
  • Ren Y, Li S, Wu Z, et al. The influences of Bacillus subtilis on the virulence of Aeromonas hydrophila and expression of luxS gene of both bacteria under co-cultivation. Curr Microbiol. 2017;74(6):718–724.
  • Wang X, Li X, Ling J. Streptococcus gordonii luxS/autoinducer-2 quorum-sensing system modulates the dual-species biofilm formation with Streptococcus mutans. J Basic Microbiol. 2017;57:605–616.
  • Moreira CG, Sperandio V. The epinephrine/norepinephrine/autoinducer-3 interkingdom signaling system in Escherichia coli O157:H7. Adv Exp Med Biol. 2016;874:247–261.
  • Hengge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol. 2009;7(4):263–273.
  • Srivastava D, Waters CM. A tangled web: regulatory connections between quorum sensing and cyclic Di-GMP. J Bacteriol. 2012;194(17):4485–4493.
  • Krasteva PV, Giglio KM, Sondermann H. Sensing the messenger: the diverse ways that bacteria signal through c-di-GMP. Protein Sci. 2012;21(7):929–948.
  • Pécastaings S, Allombert J, Lajoie B, et al. New insights into Legionella pneumophila biofilm regulation by c-di-GMP signaling. Biofouling. 2016;32(8):935–948.
  • Hochstrasser R, Kessler A, Sahr T, et al. The pleiotropic Legionella transcription factor LvbR links the Lqs and c-di-GMP regulatory networks to control biofilm architecture and virulence. Environ Microbiol. 2019;21(3):1035–1053.
  • Flores-Valdez MA. Vaccines directed against microorganisms or their products present during biofilm lifestyle: can we make a translation as a broad biological model to Tuberculosis? Front Microbiol. 2016;7:14.
  • Koo H, Allan RN, Howlin RP, et al. Targeting microbial biofilms: current and prospective therapeutic strategies. Nat Rev Microbiol. 2017;15(12):740–755.
  • Hathroubi S, Loera-Muro A, Guerrero-Barrera AL, et al. Actinobacillus pleuropneumoniae biofilms: role in pathogenicity and potential impact for vaccination development. Anim Health Res Rev. 2018;19(1):17–30.
  • Collado R, Prenafeta A, González-González L, et al. Probing vaccine antigens against bovine mastitis caused by Streptococcus uberis. Vaccine. 2016;34(33):3848–3854.
  • Chen S, Hao H, Zhao P, et al. Differential immunoreactivity to bovine convalescent serum between Mycoplasma bovis biofilms and planktonic cells revealed by comparative immunoproteomic analysis. Front Microbiol. 2018;9:379.
  • Loera-Muro A, Angulo C. New trends in innovative vaccine development against Actinobacillus pleuropneumoniae. Vet Microbiol. 2018;217:66–75.
  • Franklin MJ, Chang C, Akiyama T, et al. New technologies for studying biofilms. Microbiol Spectr. 2015;3(4):4.
  • Mitsuwan W, Olaya-Abril A, Calderon-Santiago M, et al. Integrated proteomic and metabolomic analysis reveals that rhodomyrtone reduces the capsule in Streptococcus pneumoniae. Sci Rep. 2017;7(1):2715.
  • Favre L, Ortalo-Magne A, Pichereaux C, et al. Metabolome and proteome changes between biofilm and planktonic phenotypes of the marine bacterium Pseudoalteromonas lipolytica TC8. Biofouling. 2018;34(2):132–148.
  • Khan MM, Chattagul S, Tran BQ, et al. Temporal proteomic profiling reveals changes that support Burkholderia biofilms. Pathog Dis. 2019;77(2).
  • 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(1):94–106. eCollection 2018
  • Fattahian Y, Rasooli I, Mousavi Gargari SL, et al. Protection against Acinetobacter baumannii infection via its functional deprivation of biofilm associated protein (Bap). Microb Pathog. 2011;51(6):402–406.
  • Skerniškytė J, Karazijaitė E, Deschamps J, et al. Blp1 protein shows virulence-associated features and elicits protective immunity to Acinetobacter baumannii infection. BMC Microbiol. 2019;19(1):259.
  • Flores-Mireles AL, Pinkner JS, Caparon MG, et al. EbpA vaccine antibodies block binding of Enterococcus faecalis to fibrinogen to prevent catheter-associated bladder infection in mice. Sci Transl Med. 2014;6(254):254ra127.
  • Novotny LA, Adams LD, Kang DR, et al. Epitope mapping immunodominant regions of the PilA protein of Nontypeable Haemophilus influenzae (NTHI) to facilitate the design of two novel chimeric vaccine candidates. Vaccine. 2009;28(1):279–289.
  • Novotny LA, Jurcisek JA, Ward MO, et al. Antibodies against the majority subunit of type IV pili disperse nontypeable H aemophilus influenzae biofilms in a LuxS-dependent manner and confer therapeutic resolution of experimental otitis media. Mol Microbiol. 2015;96(2):276–292.
  • Novotny LA, Brockman KL, Mokrzan EM, et al. Biofilm biology and vaccine strategies for otitis media due to nontypeable Haemophilus influenzae. J Pediatr Infect Dis. 2019;14(2):69–77.
  • Ysebaert C, Denoël P, Weynants V, et al. A protein e-pila fusion protein shows vaccine potential against nontypeable Haemophilus influenzae in mice and chinchillas. Infect Immun. 2019;87(8):e00345–19.
  • De Gouw D, Serra DO, De Jonge MI, et al. The vaccine potential of Bordetella pertussis biofilm-derived membrane proteins. Emerg Microbes Infect. 2014;3(8):e58.
  • McKenney D, Pouliot KL, Wang Y, et al. Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science. 1999;284(5419):1523–1527.
  • Mckenney D, Pouliot K, Wang Y, et al. Vaccine potential of poly-1-6 beta-D-N-succinylglucosamine, an immunoprotective surface polysaccharide of Staphylococcus aureus and Staphylococcus epidermidis. J Biotechnol. 2000;83(1–2):37–44.
  • 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(3):1017–1029.
  • Gogoi-Tiwari J, Williams V, Waryah CB, et al. Comparative studies of the immunogenicity and protective potential of biofilm vs planktonic Staphylococcus aureus vaccine against bovine mastitis using non-invasive mouse mastitis as a model system. Biofouling. 2015;31(7):543–554.
  • Pérez MM, Prenafeta A, Valle J, et al. Protection from Staphylococcus aureus mastitis associated with poly-N-acetyl β-1, 6 glucosamine specific antibody production using biofilm-embedded bacteria. Vaccine. 2009;27(17):2379–2386.
  • Prenafeta A, March R, Foix A, et al. Study of the humoral immunological response after vaccination with a Staphylococcus aureus biofilm-embedded bacterin in dairy cows: possible role of the exopolysaccharide specific antibody production in the protection from Staphylococcus aureus induced mastitis. Vet Immunol Immunopathol. 2010;134(3–4):208–217.
  • Goodman SD, Obergfell KP, Jurcisek JA, et al. Biofilms can be dispersed by focusing the immune system on a common family of bacterial nucleoid-associated proteins. Mucosal Immunol. 2011;4(6):625–637.
  • Brandstetter KA, Jurcisek JA, Goodman SD, et al. Antibodies directed against integration host factor mediate biofilm clearance from Nasopore. Laryngoscope. 2013 11;123(11):2626–2632.
  • Gustave JE, Jurcisek JA, McCoy KS, et al. Targeting bacterial integration host factor to disrupt biofilms associated with cystic fibrosis. J Cys Fibros. 2013;12(4):384–389.
  • Brockson ME, Novotny LA, Mokrzan EM, et al. Evaluation of the kinetics and mechanism of action of anti-integration host factor-mediated disruption of bacterial biofilms. Mol Microbiol. 2014;93(6):1246–1258.
  • Novotny LA, Jurcisek JA, Goodman SD, et al. Monoclonal antibodies against DNA-binding tips of DNABII proteins disrupt biofilms in vitro and induce bacterial clearance in vivo. EBio Med. 2016;10:33–44.
  • 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(1):74–88.
  • Novotny LA, Goodman SD, Bakaletz LO. Redirecting the immune response towards immunoprotective domains of a DNABII protein resolves experimental otitis media. NPJ Vaccines. 2019;4(1):43.
  • Bailey MT, Lauber CL, Novotny LA, et al. Immunization with a biofilm-disrupting nontypeable haemophilus influenzae vaccine antigen did not alter the gut microbiome in chinchillas, unlike oral delivery of a broad-spectrum antibiotic commonly used for otitis media. mSphere. 2020;5(2):e00296–20.
  • Harris JB. Cholera: immunity and prospects in vaccine development. J Infect Dis. 2018;218(suppl_3):S141–S146.
  • Berk V, Fong JC, Dempsey GT, et al. Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science. 2012;337(6091):236–239.
  • Chupácová J, Borghi E, Morace G, et al. Anti-biofilm activity of antibody directed against surface antigen complement receptor 3-related protein-comparison of Candida albicans and Candida dubliniensis. Pathog Dis. 2018;76(1):76.
  • Latasa C, Echeverz M, García B, et al. Evaluation of a Salmonella strain lacking the secondary messenger c-di-GMP and RpoS as a live oral vaccine. PLoS ONE. 2016;11(8):e0161216.
  • Brady RA, O’May GA, Leid JG, et al. Resolution of Staphylococcus aureus biofilm infection using vaccination and antibiotic treatment. Infect Immun. 2011;79(4):1797–1803.
  • Harro JM, Achermann Y, Freiberg JA, et al. Clearance of Staphylococcus aureus from in vivo models of chronic infection by immunization requires both planktonic and biofilm antigens. Infect Immun. 2019;IAI.00586–19. DOI:10.1128/IAI.00586-19
  • Azad IS, Shankar KM, Mohan CV, et al. Biofilm vaccine of Aeromonas hydrophila– standardization of dose and duration for oral vaccination of carps. Fish Shellfish Immunol. 1999;9(7):519–528.
  • Vinay TN, Ray AK, Avunje S, et al. Vibrio harveyi biofilm as immunostimulant candidate for high-health pacific white shrimp, Penaeus vannamei farming. Fish Shellfish Immunol. 2019;95:498–505.
  • Ram MK, Naveen Kumar BT, Poojary SR, et al. Evaluation of biofilm of Vibrio anguillarum for oral vaccination of asian seabass, lates calcarifer (BLOCH, 1790). Fish Shellfish Immunol. 2019;94:746–751.
  • Shahrooei M, Hira V, Khodaparast L, et al. Vaccination with SesC decreases Staphylococcus epidermidis biofilm formation. Infect Immun. 2012;80(10):3660–3668.
  • Theoret JR, Cooper KK, Zekarias B, et al. The campylobacter jejuni dps homologue is important for in vitro biofilm formation and cecal colonization of poultry and may serve as a protective antigen for vaccination. Clin Vaccine Immunol. 2012;19(9):1426–1431.
  • Huang L, Xu QA, Liu C, et al. Anti-caries DNA vaccine-induced secretory immunoglobulin A antibodies inhibit formation of Streptococcus mutans biofilms in vitro. Acta Pharmacol Sin. 2013;34(2):239–346.
  • Yan L, Zhang L, Ma H, et al. A Single B-repeat of staphylococcus epidermidis accumulation-associated protein induces protective immune responses in an experimental biomaterial-associated infection mouse model. Clin Vaccine Immunol. 2014;21(9):1206–12014.
  • Badmasti F, Ajdary S, Bouzari S, et al. Immunological evaluation of OMV(PagL)+Bap(1-487aa) and AbOmpA(8-346aa)+Bap(1-487aa) as vaccine candidates against Acinetobacter baumannii sepsis infection. Mol Immunol. 2015;67(2):552–558.
  • 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.
  • Gogoi-Tiwari J, Williams V, Waryah CB, et al. Intramammary immunization of pregnant mice with Staphylococcal protein A reduces the post-challenge mammary gland bacterial load but not pathology. PLoS ONE. 2016;11(2):e0148383.
  • Sun Y, Yang Y, Zhou D, et al. Flagellin-rPAc vaccine inhibits biofilm formation but not proliferation of S. mutans. Hum Vaccin Immunother. 2016;12(11):2847–2854.
  • Yi L, Wang Y, Ma Z, et al. Identification and characterization of a Streptococcus equi ssp. zooepidemicus immunogenic GroEL protein involved in biofilm formation. Vet Res. 2016;47(1):50.
  • Den Reijer PM, Sandker M, Snijders SV, et al. Combining in vitro protein detection and in vivo antibody detection identifies potential vaccine targets against Staphylococcus aureus during osteomyelitis. Med Microbiol Immunol. 2017;206(1):11–22.
  • Flores-Valdez MA, Pedroza-Roldán C, Aceves-Sánchez MJ, et al. The BCGΔBCG1419c vaccine candidate reduces lung pathology, IL-6, TNF-α, and IL-10 during chronic TB infection. Front Microbiol. 2018;9:1281.
  • Medrano-Díaz CL, Vega-González A, Ruiz-Baca E, et al. Moonlighting proteins induce protection in a mouse model against Candida species. Microb Pathog. 2018;124:21–29.
  • Mirzaei B, Mousavi SF, Babaei R, et al. Synthesis of conjugated PIA–rSesC and immunological evaluation against biofilm-forming Staphylococcus epidermidis. J Med Microbiol. 2019;68(5):791–802.
  • Mokrzan EM, Novotny LA, Brockman KL, et al. Antibodies against the majority subunit (PilA) of the type iv pilus of nontypeable Haemophilus influenzae disperse Moraxella catarrhalis from a dual-species biofilm. MBio. 2019;9:e02423–18.
  • Asha A, Nayak DK, Shankar KM, et al. Antigen expression in biofilm cells of Aeromonas hydrophila employed in oral vaccination of fish. Fish Shellfish Immunol. 2004;16(3):429–436.
  • Nayak DK, Asha A, Shankar KM, et al. Evaluation of biofilm of Aeromonas hydrophila for oral vaccination of Clarias batrachus–A carnivore model. Fish Shellfish Immunol. 2004;16(5):613–619.
  • Krupesha Sharma SR, Shankar KM, Sathyanarayana ML, et al. Evaluation of immune response and resistance to diseases in tiger shrimp, Penaeus monodon fed with biofilm of Vibrio alginolyticus. Fish Shellfish Immunol. 2010;29(5):724–732.
  • Siriyappagouder P, Shankar KM, Naveen Kumar BT, et al. Evaluation of biofilm of Aeromonas hydrophila for oral vaccination of Channa striatus. Fish Shellfish Immunol. 2014;41(2):581–585.
  • Collado R, Montbrau C, Sitjà M, et al. Study of the efficacy of a Streptococcus uberis mastitis vaccine against an experimental intramammary infection with a heterologous strain in dairy cows. J Dairy Sci. 2018;101(11):10290–10302.
  • Gholami SA, Goli HR, Haghshenas MR, et al. Evaluation of polysaccharide intercellular adhesion (PIA) and glycerol teichoic acid (Gly-TA) arisen antibodies to prevention of biofilm formation in Staphylococcus aureus and Staphylococcus epidermidis strains. BMC Res Notes. 2019;12(1):691.
  • Vasileiou NGC, Cripps PJ, Ioannidi KS, et al. Experimental study for evaluation of the efficacy of a biofilm-embedded bacteria-based vaccine against Staphylococcus chromogenes-associated mastitis in sheep. Vet Microbiol. 2019;239:108480.
  • Vasileiou NGC, Chatzopoulos DC, Cripps PJ, et al. Evaluation of efficacy of a biofilm-embedded bacteria-based vaccine against staphylococcal mastitis in sheep-A randomized, placebo-controlled field study. J Dairy Sci. 2019;102(10):9328–9344.
  • Hathroubi S, Zerebinski J, Ottemann KM. Helicobacter pylori biofilm involves a multigene stress-biased response, including a structural role for flagella. mBio. 2018;9(5):e01973–18.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.