Advertisement

Infection

, Volume 47, Issue 1, pp 13–23 | Cite as

A review on anti-adhesion therapies of bacterial diseases

  • Arezoo Asadi
  • Shabnam RazaviEmail author
  • Malihe Talebi
  • Mehrdad Gholami
Review
  • 248 Downloads

Abstract

Background

Infections caused by bacteria are a foremost cause of morbidity and mortality in the world. The common strategy of treating bacterial infections is by local or systemic administration of antimicrobial agents. Currently, the increasing antibiotic resistance is a serious and global problem. Since the most important agent for infection is bacteria attaching to host cells, hence, new techniques and attractive approaches that interfere with the ability of the bacteria to adhere to tissues of the host or detach them from the tissues at the early stages of infection are good therapeutic strategies.

Methods

All available national and international databanks were searched using the search keywords. Here, we review various approaches to anti-adhesion therapy, including use of receptor and adhesion analogs, dietary constituents, sublethal concentrations of antibiotics, and adhesion-based vaccines.

Results

Altogether, the findings suggest that interference with bacterial adhesion serves as a new means to fight infectious diseases.

Conclusion

Anti-adhesion-based therapies can be effective in prevention and treatment of bacterial infections, but further work is needed to elucidate underlying mechanisms.

Keywords

Adhesins Antibiotic resistance Infectious disease Anti-adhesion therapy 

Notes

Compliance with ethical standards

Conflict of interest

There are no conflicts of interest.

References

  1. 1.
    Krachler AM, Orth K. Targeting the bacteria–host interface: strategies in anti-adhesion therapy. Virulence. 2013;4:284–94.Google Scholar
  2. 2.
    Signoretto C, Canepari P, Stauder M, Vezzulli L, Pruzzo C. Functional foods and strategies contrasting bacterial adhesion. Curr Opin Biotechnol. 2012;23:160–7.Google Scholar
  3. 3.
    Ofek I, Hasty DL, Sharon N. Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunol Med Microbiol. 2003;38:181–91.Google Scholar
  4. 4.
    Sharon N. Carbohydrates as future anti-adhesion drugs for infectious diseases. Biochim Biophys Acta (BBA) Gen Subj. 2006;1760:527–37.Google Scholar
  5. 5.
    Johnson-Henry KC, Pinnell LJ, Waskow AM, Irrazabal T, Martin A, Hausner M, et al. Short-chain fructo-oligosaccharide and inulin modulate inflammatory responses and microbial communities in Caco2-bbe cells and in a mouse model of intestinal injury. J Nutr. 2014;144:1725–33.Google Scholar
  6. 6.
    Bibel DJ, Aly R, Shinefield HR. Inhibition of microbial adherence by sphinganine. Can J Microbiol. 1992;38:983–5.Google Scholar
  7. 7.
    Sherman P, Boedeker E. Pilus-mediated interactions of the Escherichia coli strain RDEC-1 with mucosal glycoproteins in the small intestine of rabbits. Gastroenterology. 1987;93:734–43.Google Scholar
  8. 8.
    Pak J, Pu Y, Zhang Z-T, Hasty DL, Wu X-R. Tamm–Horsfall protein binds to type 1 fimbriated Escherichia coli and prevents E. coli from binding to uroplakin Ia and Ib receptors. J Biol Chem. 2001;276:9924–30.Google Scholar
  9. 9.
    Piotrowski J, Slomiany A, Murty V, Fekete Z, Slomiany B. Inhibition of Helicobacter pylori colonization by sulfated gastric mucin. Biochem Int. 1991;24:749–56.Google Scholar
  10. 10.
    Mulvey MA. Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol. 2002;4:257–71.Google Scholar
  11. 11.
    Cozens D, Read RC. Anti-adhesion methods as novel therapeutics for bacterial infections. Expert Rev Anti-infect Ther. 2012;10:1457–68.Google Scholar
  12. 12.
    Quintero-Villegas MI, Aam BB, Rupnow J, Sørlie M, Eijsink VG, Hutkins RW. Adherence inhibition of enteropathogenic Escherichia coli by chitooligosaccharides with specific degrees of acetylation and polymerization. J Agric Food Chem. 2013;61:2748–54.Google Scholar
  13. 13.
    Ofek I, Doyle RJ. Common themes in bacterial adhesion. Bacterial adhesion to cells and tissues. Springer, Berlin 1994, pp. 513–61.Google Scholar
  14. 14.
    Miörner H, Johansson G, Kronvall G. Lipoteichoic acid is the major cell wall component responsible for surface hydrophobicity of group A streptococci. Infect Immun. 1983;39:336–43.Google Scholar
  15. 15.
    Sharon N. Bacterial lectins, cell-cell recognition and infectious disease. FEBS Lett. 1987;217:145–57.Google Scholar
  16. 16.
    Cundell DR, Gerard NP, Craig G, Idanpaan-Heikkila I, Tuomanen EI. Streptococcus pneumoniae anchor to activated human cells by the receptor for platelet-activating factor. Nature. 1995;377:435.Google Scholar
  17. 17.
    Chen SL, Hung C-S, Xu J, Reigstad CS, Magrini V, Sabo A, et al. Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli: a comparative genomics approach. Proc Natl Acad Sci. 2006;103:5977–82.Google Scholar
  18. 18.
    Svensson A, Larsson A, Emtenäs H, Hedenström M, Fex T, Hultgren SJ, et al. Design and evaluation of pilicides: potential novel antibacterial agents directed against uropathogenic Escherichia coli. Chembiochem. 2001;2:915–8.Google Scholar
  19. 19.
    Pinkner JS, Bengtsson C, Edvinsson S, Cusumano CK, Rosenbaum E, Johansson LB, et al. Design and synthesis of fluorescent pilicides and curlicides: bioactive tools to study bacterial virulence mechanisms. Chem A Eur J. 2012;18:4522–32.Google Scholar
  20. 20.
    Hartlova A, Cerveny L, Hubalek M, Krocova Z, Stulik J. Membrane rafts: a potential gateway for bacterial entry into host cells. Microbiol Immunol. 2010;54:237–45.Google Scholar
  21. 21.
    Svensson M, Frendeus B, Butters T, Platt F, Dwek R, Svanborg C. Glycolipid depletion in antimicrobial therapy. Mol Microbiol. 2003;47:453–61.Google Scholar
  22. 22.
    Margalit M, Ash N, Zimran A, Halkin H. Enzyme replacement therapy in the management of longstanding skeletal and soft tissue salmonella infection in a patient with Gaucher’s disease. Postgrad Med J. 2002;78:564–5.Google Scholar
  23. 23.
    Bernbom N, Jørgensen RL, Ng Y, Meyer R, Kingshott P, Vejborg RM, et al. Bacterial adhesion to stainless steel is reduced by aqueous fish extract coatings. Biofilms. 2006;3:25–36.Google Scholar
  24. 24.
    Chen L, Wen Y-m. The role of bacterial biofilm in persistent infections and control strategies. Int J Oral Sci. 2011;3:66.Google Scholar
  25. 25.
    Svensson M, Platt FM, Svanborg C. Glycolipid receptor depletion as an approach to specific antimicrobial therapy. FEMS Microbiol Lett. 2006;258:1–8.Google Scholar
  26. 26.
    Okuda K, Hanada N, Usui Y, Takeuchi H, Koba H, Nakao R, et al. Inhibition of Streptococcus mutans adherence and biofilm formation using analogues of the SspB peptide. Arch Oral Biol. 2010;55:754–62.Google Scholar
  27. 27.
    Moon HW, Bunn TO. Vaccines for preventing enterotoxigenic Escherichia coli infections in farm animals. Vaccine. 1993;11:213–20.Google Scholar
  28. 28.
    Sharon N, Ofek I. Safe as mother’s milk: carbohydrates as future anti-adhesion drugs for bacterial diseases. Glycoconj J. 2000;17:659–64.Google Scholar
  29. 29.
    Bouckaert J, Berglund J, Schembri M, De Genst E, Cools L, Wuhrer M, et al. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Mol Microbiol. 2005;55:441–55.Google Scholar
  30. 30.
    Jiang X, Abgottspon D, Kleeb S, Rabbani S, Scharenberg M, Wittwer M, et al. Antiadhesion therapy for urinary tract infections. A balanced PK/PD profile proved to be key for success. J Med Chem. 2012;55:4700–13.Google Scholar
  31. 31.
    Vanwetswinkel S, Volkov AN, Sterckx YG, Garcia-Pino A, Buts L, Vranken WF, et al. Study of the structural and dynamic effects in the FimH adhesin upon α-d-heptyl mannose binding. J Med Chem. 2014;57:1416–27.Google Scholar
  32. 32.
    Almant M, Moreau V, Kovensky J, Bouckaert J, Gouin SG. Clustering of Escherichia coli type-1 fimbrial adhesins by using multimeric heptyl α-d-Mannoside probes with a carbohydrate core. Chem A Eur J. 2011;17:10029–38.Google Scholar
  33. 33.
    Chemani C, Imberty A, de Bentzmann S, Pierre M, Wimmerová M, Guery BP, et al. Role of LecA and LecB lectins in Pseudomonas aeruginosa-induced lung injury and effect of carbohydrate ligands. Infect Immun. 2009;77:2065–75.Google Scholar
  34. 34.
    Ukkonen P, Varis K, Jernfors M, Herva E, Jokinen J, Ruokokoski E, et al. Treatment of acute otitis media with an antiadhesive oligosaccharide: a randomised, double-blind, placebo-controlled trial. Lancet. 2000;356:1398–402.Google Scholar
  35. 35.
    Lillehoj EP, Kim BT, Kim KC. Identification of Pseudomonas aeruginosa flagellin as an adhesin for Muc1 mucin. Am J Physiol Lung Cell Mol Physiol. 2002;282:L751-L6.Google Scholar
  36. 36.
    Ma J, Hunjan M, Smith R, Lehner T. Specificity of monoclonal antibodies in local passive immunization against Streptococcus mutans. Clin Exp Immunol. 1989;77:331.Google Scholar
  37. 37.
    Munro GH, Evans P, Todryk S, Buckett P, Kelly CG, Lehner T. A protein fragment of streptococcal cell surface antigen I/II which prevents adhesion of Streptococcus mutans. Infect Immun. 1993;61:4590–8.Google Scholar
  38. 38.
    Krachler AM, Mende K, Murray C, Orth K. In vitro characterization of multivalent adhesion molecule 7-based inhibition of multidrug-resistant bacteria isolated from wounded military personnel. Virulence. 2012;3:389–99.Google Scholar
  39. 39.
    Lalezari JP, Henry K, O’hearn M, Montaner JS, Piliero PJ, Trottier B, et al. Enfuvirtide, an HIV-1 fusion inhibitor, for drug-resistant HIV infection in North and South America. N Engl J Med. 2003;348:2175–85.Google Scholar
  40. 40.
    Kumar Malik D, Baboota S, Ahuja A, Hasan S, Ali J. Recent advances in protein and peptide drug delivery systems. Curr Drug Deliv. 2007;4:141–51.Google Scholar
  41. 41.
    Eucker TP, Konkel ME. The cooperative action of bacterial fibronectin-binding proteins and secreted proteins promote maximal Campylobacter jejuni invasion of host cells by stimulating membrane ruffling. Cell Microbiol. 2012;14:226–38.Google Scholar
  42. 42.
    Kelly CG, Lehner T. Peptide inhibitors of Streptococcus mutans in the control of dental caries. Int J Pept Res Ther. 2007;13:517–23.Google Scholar
  43. 43.
    Labrecque J, Bodet C, Chandad F, Grenier D. Effects of a high-molecular-weight cranberry fraction on growth, biofilm formation and adherence of Porphyromonas gingivalis. J Antimicrob Chemother. 2006;58:439–43.Google Scholar
  44. 44.
    Burger O, Weiss E, Sharon N, Tabak M, Neeman I, Ofek I. Inhibition of Helicobacter pylori adhesion to human gastric mucus by a high-molecular-weight constituent of cranberry juice. Crit Rev Food Sci Nutr. 2002;42:279–84.Google Scholar
  45. 45.
    Wizemann TM, Adamou JE, Langermann S. Adhesins as targets for vaccine development. Emerg Infect Dis. 1999;5:395.Google Scholar
  46. 46.
    Klemm P, Vejborg RM, Hancock V. Prevention of bacterial adhesion. Appl Microbiol Biotechnol. 2010;88:451–9.Google Scholar
  47. 47.
    Ghosh S, Chakraborty K, Nagaraja T, Basak S, Koley H, Dutta S, et al. An adhesion protein of Salmonella enterica serovar Typhi is required for pathogenesis and potential target for vaccine development. Proc Natl Acad Sci. 2011;108:3348–53.Google Scholar
  48. 48.
    Bravo D, Blondel CJ, Hoare A, Leyton L, Valvano MA, Contreras I. Type IV B pili are required for invasion but not for adhesion of Salmonella enterica serovar Typhi into BHK epithelial cells in a cystic fibrosis transmembrane conductance regulator-independent manner. Microbial Pathog. 2011;51:373–7.Google Scholar
  49. 49.
    Langermann S, Palaszynski S, Barnhart M, Auguste G, Pinkner JS, Burlein J, et al. Prevention of mucosal Escherichia coli infection by FimH-adhesin-based systemic vaccination. Science. 1997;276:607–11.Google Scholar
  50. 50.
    Greco D, Salmaso S, Mastrantonio P, Giuliano M, Tozzi AE, Anemona A, et al. A controlled trial of two acellular vaccines and one whole-cell vaccine against pertussis. N Engl J Med. 1996;1996:341–9.Google Scholar
  51. 51.
    Poolman JT, Hallander HO. Acellular pertussis vaccines and the role of pertactin and fimbriae. Expert Rev Vaccines. 2007;6:47–56.Google Scholar
  52. 52.
    Briles DE, Ades E, Paton JC, Sampson JS, Carlone GM, Huebner RC, et al. Intranasal immunization of mice with a mixture of the pneumococcal proteins PsaA and PspA is highly protective against nasopharyngeal carriage of Streptococcus pneumoniae. Infect Immun. 2000;68:796–800.Google Scholar
  53. 53.
    Arrecubieta C, Matsunaga I, Asai T, Naka Y, Deng MC, Lowy FD. Vaccination with clumping factor A and fibronectin binding protein A to prevent Staphylococcus aureus infection of an aortic patch in mice. J Infect Dis. 2008;198:571–5.Google Scholar
  54. 54.
    Schuchat A, Hilger T, Zell E, Farley MM, Reingold A, Harrison L, et al. Active bacterial core surveillance of the emerging infections program network. Emerg Infect Dis. 2001;7:92.Google Scholar
  55. 55.
    Maiden MC, Stuart JM, Group UMC. Carriage of serogroup C meningococci 1 year after meningococcal C conjugate polysaccharide vaccination. Lancet. 2002;359:1829–30.Google Scholar
  56. 56.
    Evans CM, Pratt CB, Matheson M, Vaughan TE, Findlow J, Borrow R, et al. Nasopharyngeal colonization by Neisseria lactamica and induction of protective immunity against N. meningitidis. Clin Infect Dis. 2011;52:70–7.Google Scholar
  57. 57.
    Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell. 1997;91:511–20.Google Scholar
  58. 58.
    Zhang C, Zhang W. Escherichia coli K88ac fimbriae expressing heat-labile and heat-stable (STa) toxin epitopes elicit antibodies that neutralize cholera toxin and STa toxin and inhibit adherence of K88ac fimbrial E. coli. Clin Vaccine Immunol. 2010;17:1859–67.Google Scholar
  59. 59.
    Sheth H, Glasier L, Ellert N, Cachia P, Kohn W, Lee K, et al. Development of an anti-adhesive vaccine for Pseudomonas aeruginosa targeting the C-terminal region of the pilin structural protein. Biomed Pept Proteins Nucl Acids 1995;1:141–8.Google Scholar
  60. 60.
    Arciola CR, Speziale P, Montanaro L. Perspectives on DNA vaccines. Targeting staphylococcal adhesins to prevent implant infections. Int J Artif Organs. 2009;32:635–41.Google Scholar
  61. 61.
    Therrien R, Lacasse P, Grondin G, Talbot BG. Lack of protection of mice against Staphylococcus aureus despite a significant immune response to immunization with a DNA vaccine encoding collagen-binding protein. Vaccine. 2007;25:5053–61.Google Scholar
  62. 62.
    Rogers TJ, Paton JC. Therapeutic strategies for Shiga toxin-producing Escherichia coli infections. Expert Rev Anti-Infect Ther. 2009;7:683–6.Google Scholar
  63. 63.
    Pinkner JS, Remaut H, Buelens F, Miller E, Åberg V, Pemberton N, et al. Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc Natl Acad Sci. 2006;103:17897–902.Google Scholar
  64. 64.
    Eidam O, Dworkowski FS, Glockshuber R, Grütter MG, Capitani G. Crystal structure of the ternary FimC–FimFt–FimDN complex indicates conserved pilus chaperone–subunit complex recognition by the usher FimD. FEBS Lett. 2008;582:651–5.Google Scholar
  65. 65.
    Ton-That H, Schneewind O. Anchor structure of staphylococcal surface proteins IV. Inhibitors of the cell wall sorting reaction. J Biol Chem. 1999;274:24316–20.Google Scholar
  66. 66.
    Mortensen NP, Fowlkes JD, Maggart M, Doktycz MJ, Nataro JP, Drusano G, et al. Effects of sub-minimum inhibitory concentrations of ciprofloxacin on enteroaggregative Escherichia coli and the role of the surface protein dispersin. Int J Antimicrob Agents. 2011;38:27–34.Google Scholar
  67. 67.
    Wojnicz D, Jankowski S. Effects of subinhibitory concentrations of amikacin and ciprofloxacin on the hydrophobicity and adherence to epithelial cells of uropathogenic Escherichia coli strains. Int J Antimicrob Agents. 2007;29:700–4.Google Scholar
  68. 68.
    Fonseca A, Sousa J. Effect of antibiotic-induced morphological changes on surface properties, motility and adhesion of nosocomial Pseudomonas aeruginosa strains under different physiological states. J Appl Microbiol. 2007;103:1828–37.Google Scholar
  69. 69.
    Roberts DE, Read RC, Cole PJ, Wilson R. Haemophilus influenzae infection of human respiratory mucosa in low concentrations of antibiotics. Am Rev Respir Dis. 1993;148:201–7.Google Scholar
  70. 70.
    Balagué C, Fernández L, Pérez J, Grau R. Effect of ciprofloxacin on adhesive properties of non-P mannose-resistant uropathogenic Escherichia coli isolates. J Antimicrob Chemother. 2003;51:401–4.Google Scholar
  71. 71.
    Rasigade JP, Moulay A, Lhoste Y, Tristan A, Bes M, Vandenesch F, et al. Impact of sub-inhibitory antibiotics on fibronectin-mediated host cell adhesion and invasion by Staphylococcus aureus. BMC Microbiol. 2011;11:263.Google Scholar
  72. 72.
    Cars O. Pharmacokinetics of antibiotics in tissues and tissue fluids: a review. Scand J Infect Dis. 1991;74:23–33.Google Scholar
  73. 73.
    Liu Y, Pinzón-Arango PA, Gallardo-Moreno AM, Camesano TA. Direct adhesion force measurements between E. coli and human uroepithelial cells in cranberry juice cocktail. Mol Nutr Food Res. 2010;54:1744–52.Google Scholar
  74. 74.
    Toivanen M, Huttunen S, Lapinjoki S, Tikkanen-Kaukanen C. Inhibition of adhesion of Neisseria meningitidis to human epithelial cells by berry juice polyphenolic fractions. Phytother Res. 2011;25:828–32.Google Scholar
  75. 75.
    Yamanaka A, Kimizuka R, Kato T, Okuda K. Inhibitory effects of cranberry juice on attachment of oral streptococci and biofilm formation. Mol Oral Microbiol. 2004;19:150–4.Google Scholar
  76. 76.
    Kontiokari T, Sundqvist K, Nuutinen M, Pokka T, Koskela M, Uhari M. Randomised trial of cranberry-lingonberry juice and Lactobacillus GG drink for the prevention of urinary tract infections in women. BMJ. 2001;322:1571.Google Scholar
  77. 77.
    Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS. Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J Nutr. 2005;135:1304–7.Google Scholar
  78. 78.
    Coppa GV, Zampini L, Galeazzi T, Facinelli B, Ferrante L, Capretti R, et al. Human milk oligosaccharides inhibit the adhesion to Caco-2 cells of diarrheal pathogens: Escherichia coli, Vibrio cholerae, and Salmonella fyris. Pediatr Res. 2006;59:377–82.Google Scholar
  79. 79.
    Newburg DS, Ruiz-Palacios GM, Morrow AL. Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr. 2005;25:37–58.Google Scholar
  80. 80.
    Parker P, Sando L, Pearson R, Kongsuwan K, Tellam RL, Smith S. Bovine Muc1 inhibits binding of enteric bacteria to Caco-2 cells. Glycoconj J. 2010;27:89–97.Google Scholar
  81. 81.
    Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P, et al. Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol. 2008;125:286–92.Google Scholar
  82. 82.
    Focareta A, Paton JC, Morona R, Cook J, Paton AW. A recombinant probiotic for treatment and prevention of cholera. Gastroenterology. 2006;130:1688–95.Google Scholar
  83. 83.
    Lievin V, Peiffer I, Hudault S, Rochat F, Brassart D, Neeser J, et al. Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut. 2000;47:646–52.Google Scholar
  84. 84.
    Kailasapathy K, Chin J. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol. 2000;78:80.Google Scholar
  85. 85.
    Moshiri M, Dallal MMS, Rezaei F, Douraghi M, Sharifi L, Noroozbabaei Z, et al. The effect of lactobacillus acidophilus PTCC 1643 on cultured intestinal epithelial cells infected with Salmonella enterica serovar Enteritidis. Osong Public Health Res Perspect. 2017;8:54.Google Scholar
  86. 86.
    Cecioni S, Imberty A, Vidal S. Glycomimetics versus multivalent glycoconjugates for the design of high affinity lectin ligands. Chem Rev. 2014;115:525–61.Google Scholar
  87. 87.
    Roberts PA, Huebinger RM, Keen E, Krachler A-M, Jabbari S. Predictive modelling of a novel anti-adhesion therapy to combat bacterial colonisation of burn wounds. arXiv preprint arXiv:170807062. 2017.Google Scholar
  88. 88.
    Gholami M, Chirani AS, Razavi S, Falak R, Irajian G. Immunogenicity of a fusion protein containing PilQ and disulfide turn region of PilA from Pseudomonas aeruginosa in mice. Lett Appl Microbiol. 2017;65:439–445.Google Scholar
  89. 89.
    Campana R, Casettari L, Ciandrini E, Illum L, Baffone W. Chitosans inhibit the growth and the adhesion of Klebsiella pneumoniae and Escherichia coli clinical isolates on urinary catheters. Int J Antimicrob Agents. 2017;50:135–41.Google Scholar
  90. 90.
    Huttunen S, Toivanen M, Liu C, Tikkanen-Kaukanen C. Novel anti-infective potential of salvianolic acid B against human serious pathogen Neisseria meningitidis. BMC Res Notes. 2016;9:25.Google Scholar
  91. 91.
    Raie DS, Mhatre E, Thiele M, Labena A, El-Ghannam G, Farahat LA, 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;70:753–62.Google Scholar
  92. 92.
    Heana NY, Othmanb SNAM, Basarb N, Jemona K. Antibiofilm and antiadhesion activities of Phaleria macrocarpa against oral Streptococcus mutans. J Teknol. 2015;77:31–35.Google Scholar
  93. 93.
    Miladi H, Mili D, Slama RB, Zouari S, Ammar E, Bakhrouf A. Antibiofilm formation and anti-adhesive property of three mediterranean essential oils against a foodborne pathogen Salmonella strain. Microbial Pathog. 2016;93:22–31.Google Scholar
  94. 94.
    Amerighi F, Valeri M, Donnarumma D, Maccari S, Moschioni M, Taddei A, et al. Identification of a monoclonal antibody against pneumococcal pilus 1 ancillary protein impairing bacterial adhesion to human epithelial cells. J Infect Dis. 2015;213:516–22.Google Scholar
  95. 95.
    Gupta D, Sarkar S, Sharma M, Thapa B, Chakraborti A. Inhibition of enteroaggregative Escherichia coli cell adhesion in-vitro by designed peptides. Microbial Pathog. 2016;98:23–31.Google Scholar
  96. 96.
    Boukerb AM, Rousset A, Galanos N, Mear J-B, Thepaut M, Grandjean T, et al. Antiadhesive properties of glycoclusters against Pseudomonas aeruginosa lung infection. J Med Chem. 2014;57:10275–89.Google Scholar
  97. 97.
    Kaspar KL, Howell AB, Khoo C. Ex vivo anti-adhesion activity of a proanthocyanidin standardized cranberry powder beverage. FASEB J. 2013;27:1079.42-.42.Google Scholar
  98. 98.
    Fessele C, Lindhorst TK. Effect of aminophenyl and aminothiahexyl α-d-glycosides of the manno-, gluco-, and galacto-series on type 1 fimbriae-mediated adhesion of Escherichia coli. Biology. 2013;2:1135–49.Google Scholar
  99. 99.
    Asha MK, Debraj D, Edwin JR, Srikanth H, Muruganantham N, Dethe SM, et al. In vitro anti-Helicobacter pylori activity of a flavonoid rich extract of Glycyrrhiza glabra and its probable mechanisms of action. J Ethnopharmacol. 2013;145:581–6.Google Scholar
  100. 100.
    Sumitomo T, Nakata M, Yamaguchi M, Terao Y, Kawabata S. S-carboxymethylcysteine inhibits adherence of Streptococcus pneumoniae to human alveolar epithelial cells. J Med Microbiol. 2012;61:101–8.Google Scholar
  101. 101.
    Stauder M, Papetti A, Mascherpa D, Schito AM, Gazzani G, Pruzzo C, et al. Antiadhesion and antibiofilm activities of high molecular weight coffee components against Streptococcus mutans. J Agric Food Chem. 2010;58:11662–6.Google Scholar
  102. 102.
    Howell AB, Botto H, Combescure C, Blanc-Potard A-B, Gausa L, Matsumoto T, et al. Dosage effect on uropathogenic Escherichia coli anti-adhesion activity in urine following consumption of cranberry powder standardized for proanthocyanidin content: a multicentric randomized double blind study. BMC Infect Dis. 2010;10:94.Google Scholar
  103. 103.
    Burkholder KM, Bhunia AK. Salmonella enterica serovar Typhimurium adhesion and cytotoxicity during epithelial cell stress is reduced by Lactobacillus rhamnosus GG. Gut Pathog. 2009;1:14.Google Scholar
  104. 104.
    Daglia M, Stauder M, Papetti A, Signoretto C, Giusto G, Canepari P, et al. Isolation of red wine components with anti-adhesion and anti-biofilm activity against Streptococcus mutans. Food Chem. 2010;119:1182–8.Google Scholar
  105. 105.
    Sinclair HR, Kemp F, de Slegte J, Gibson GR, Rastall RA. Carbohydrate-based anti-adhesive inhibition of Vibrio cholerae toxin binding to GM1-OS immobilized into artificial planar lipid membranes. Carbohydr Res. 2009;344:1968–74.Google Scholar
  106. 106.
    McEwan NA, Rème CA, Gatto H, Nuttall TJ. Monosaccharide inhibition of adherence by Pseudomonas aeruginosa to canine corneocytes. Vet Dermatol. 2008;19:221–5.Google Scholar
  107. 107.
    Rosentritt M, Hahnel S, Gröger G, Mühlfriedel B, Bürgers R, Handel G. Adhesion of Streptococcus mutans to various dental materials in a laminar flow chamber system. J Biomed Mater Res Part B Appl Biomater. 2008;86:36–44.Google Scholar
  108. 108.
    Gkana EN, Doulgeraki AI, Chorianopoulos NG, Nychas G-JE. Anti-adhesion and anti-biofilm potential of organosilane nanoparticles against foodborne pathogens. Front Microbiol. 2017;8:1295.Google Scholar
  109. 109.
    Orooji Y, Faghih M, Razmjou A, Hou J, Moazzam P, Emami N, et al. Nanostructured mesoporous carbon polyethersulfone composite ultrafiltration membrane with significantly low protein adsorption and bacterial adhesion. Carbon. 2017;111:689–704.Google Scholar
  110. 110.
    Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ. Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol. 2015;13:269.Google Scholar
  111. 111.
    Xiao J, Dufrêne YF. Optical and force nanoscopy in microbiology. Nat Microbiol. 2016;1:16186.Google Scholar
  112. 112.
    Tao Y, Pinzón-Arango PA, Howell AB, Camesano TA. Oral consumption of cranberry juice cocktail inhibits molecular-scale adhesion of clinical uropathogenic Escherichia coli. J Med Food. 2011;14:739–45.Google Scholar
  113. 113.
    Herman-Bausier P, Valotteau C, Pietrocola G, Rindi S, Alsteens D, Foster TJ, et al. Mechanical strength and inhibition of the Staphylococcus aureus collagen-binding protein Cna. mBio. 2016;7:e01529-16.Google Scholar
  114. 114.
    Valotteau C, Prystopiuk V, Pietrocola G, Rindi S, Peterle D, De Filippis V, et al. Single-cell and single-molecule analysis unravels the multifunctionality of the Staphylococcus aureus collagen-binding protein Cna. ACS Nano. 2017;11:2160–70.Google Scholar
  115. 115.
    Neto C, Penndorf K, Feldman M, Meron-Sudai S, Zakay-Rones Z, Steinberg D, et al. Characterization of non-dialyzable constituents from cranberry juice that inhibit adhesion, co-aggregation and biofilm formation by oral bacteria. Food Funct. 2017;8:1955–65.Google Scholar
  116. 116.
    Leshem R, Maharshak I, Jacob EB, Ofek I, Kremer I. The effect of nondialyzable material (NDM) cranberry extract on formation of contact lens biofilm by Staphylococcus epidermidis. Investig Ophthalmol Vis Sci. 2011;52:4929–34.Google Scholar
  117. 117.
    Sattin S, Bernardi A. Glycoconjugates and glycomimetics as microbial anti-adhesives. Trends Biotechnol. 2016;34:483–95.Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018
corrected publication 2018

Authors and Affiliations

  • Arezoo Asadi
    • 1
  • Shabnam Razavi
    • 1
    Email author
  • Malihe Talebi
    • 1
  • Mehrdad Gholami
    • 2
  1. 1.Department of Microbiology, Faculty of MedicineIran University of Medical SciencesTehranIran
  2. 2.Department of Microbiology and Virology, Faculty of MedicineMazandaran University of Medical SciencesSariIran

Personalised recommendations