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Recent Advances in Understanding Biofilms of Mucosae

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Abstract

Extensive information on biofilm formation on different mucosal surfaces, particularly those of bacteria, have been accumulated. Different body sites such as body cavities, organs and tracts can become colonized by a variety of microbial species, but which are specific for the location. Biofilms of mucosae can aid colonization and contribute to pathogenesis, and are produced by microbial persistence on artificial abiotic surfaces which are implanted or by direct biofilm formation on biotic surfaces of tissues or organs. Such aspects of biofilms are discussed in this review.

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References

  • Abraham SN & Beachey EH (1985) Host defences against adhesion of bacteria to mucosal surfaces. Adv. Host Def. Mech. 4: 63–88

    Google Scholar 

  • Agarwal S (2000) Vesicoureteral reflux and urinary tract infections. Curr. Opin. Urol. 10: 587–592

    Google Scholar 

  • Allison DG (2003) Molecular architecture of the bio lm matrix. In: Lens P, Moran AP, Mahony T, Stoodley P & O'Flaherty V (Eds), Biofilms in Medicine,Industry and Environmental Biotechnology. Characteristics, Analysis and Control (pp 81–90). IWA Publishing, London, UK

    Google Scholar 

  • Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J & Hultgren SJ (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301: 105–107

    Google Scholar 

  • Asaria RH, Downie JA, McLauglin-Borlace L, Morlet N, Munro P & Charteris DG (1999) Biofilm on scleral explants with and without clinical infection. Retina 19: 447–450

    Google Scholar 

  • Austin JW, Sanders G, Kay WW & Collinson SK (1998) Thin aggregative mbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett.162: 295–301

    Google Scholar 

  • Blaser MJ (1998) Helicobacter pylori and gastric diseases. BMJ 16: 1507–1510

    Google Scholar 

  • Bos R, Mei HC & Busscher HJ (1995) A quantitative method to study co-adhesion of microorganisms in a parallel plate flow chamber.II.Analysis of the kinetics of co-adhesion. J. Microbiol. Meth. 23: 169–182

    Google Scholar 

  • Boxerbaum B (1980) Isolation of rapidly growing mycobacteria in patients with cystic brosis. J. Pediatr. 96: 689–691

    Google Scholar 

  • Brooks W, Demuth DR, Gil S & Lamont RJ (1997) Identi cation of Streptococcus gordonii SspB domain that mediates adhesion to Porphyromonas gingivalis. Infect. Immun. 65: 3753–3758

    Google Scholar 

  • Buhler T, Ballestero S, Desai M & Brown MR (1998) Generation of a reproducible nutrient-depleted bio lm of Escherichia coli and Burkholderia cepacia. J. Appl. Microbiol. 85: 457–462

    Google Scholar 

  • Busscher HJ van der Mei HC (2000) Initial microbial adhesion events: Mechanisms and implications.In: Allison DG, Gilbert P, Lappin-Scott HM & Wilson M (Eds), Community Structure and Co-operation in Biofilms, (pp 25–36). University Press, Cambridge, UK

    Google Scholar 

  • Cassels FJ & Wolf MK (1995) Colonization factors of diarrheagenic E. coli and their intestinal receptors. J. Ind. Microbiol. 15: 214–226

    Google Scholar 

  • Chart H, Spencer J, Smith HR & Rowe B (1997) Magnesium ions are required for Hep-2 cell adhesion by enteroaggregative strains of Escherichia coli O126:H27 and O44:H18. FEMS Microbiol. Lett. 148: 49–52

    Google Scholar 

  • Cheng K-J & Costerton JW (1980) Adherent rumen bacteria – their role in the digestion of plant material, urea and dead epithelial cells. In: Ruckebush Y & Thivend P (Eds) Digestion and Metabolism in the Ruminant (pp 227–250). Lancaster, UK

  • Cheng K-J, McAllister TA & Costerton JW (1995) Biofilms of the ruminant digestive tract. In: Lappin-Scott HM & Costerton JW (Eds) Microbial Biofilms (pp 221 –232). Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Choong S & Whitfield H (2000) Biofilms and their role in infections in urology. BJU Int. 86: 935–941

    Google Scholar 

  • Cole MF, Evans M, Fitzsimmons S, Johnson J, Pearce C, Sheridan MJ, Wientzen R & Bowden G (1994) Pioneer oral streptococci produce immunoglobulin A1 protease. Infect. Immun. 62: 2165–2168

    Google Scholar 

  • Conway PL (1995) Microbial ecology of the human large intestine. In: Gibson GR & McFarlane GT (Eds) Human Colonic Bacteria. Role in Nutrition, Physiology and Pathology (pp 1 –24). Boca Raton, FL: CRC Press

    Google Scholar 

  • Cornelissen CN & Sparling PF (1994) Iron piracy:acquisition of transferrin-bound iron by bacterial pathogens. Mol. Microbiol. 14: 843–850

    Google Scholar 

  • Costerton JW (1999) Introduction to bio lm. Int. J. Antimicrobial Agents 11: 217–221

    Google Scholar 

  • Costerton JW, Cheng K-J, Geesey GG, Ladd TI, Nickel JC, Dasgupta M & Marrie TJ (1987) Bacterial bio lms in nature and disease.Ann. Rev. Microbiol. 41: 435–464

    Google Scholar 

  • Cramton SE, Ulrich M, Gotz F & Doring G (2001) Anaerobic conditions induce expression of polysaccharide intercellular adhesion in Staphylococcus aureus and Staphylococcus epidermidis. Infect. Immun. 69: 4079–4085

    Google Scholar 

  • Czeczulin JR, Balepur S, Hicks S, Phillips A, Hall R, Kothary MH, Navarro-Garcia F & Nataro JP (1997) Aggregative adherence mbria II, a second mbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect. Immun. 65: 4135–4145

    Google Scholar 

  • Czeczulin JR, Whittam TS, Henderson IR, Navarro-Garcia F & Nataro JP (1999) Phylogenetic analysis of enteroaggregative and diffusely adherent Escherichia coli. Infect. Immun. 67: 2692–2699

    Google Scholar 

  • Danese PN, Pratt LA, Dove SL & Kolter R (2000a) The outer membran eprotein,antigen 43,mediates cell-to-cell interactions within Escherichia coli biofilms. Mol. Microbiol. 37: 424–432

    Google Scholar 

  • Danese PN, Pratt LA & Kolter R (2000b) Exopolysaccharide production is required for development of Escherichia coli K-12 bio lm architecture. J. Bacteriol. 182: 3593–3596

    Google Scholar 

  • Davies DG (2000) Physiological events in biofilm formation.In: Allison DG, Gilbert P, Lappin-Scott HM & Wilson M (Eds) Community Structure and Co-operation in Biofilms (pp 37–52). Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Davies DG, Chakrabarty AM & Geesey GG (1993) Exopolysaccharide production in bio lms:substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl. Environ. Microbiol. 59: 1181–1186

    Google Scholar 

  • Davies GD, Parsek MR, Pearson JP, Iglewski BH, Costerton JW & Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295–298

    Google Scholar 

  • Davis JP, Chesney PJ, Wand P & LaVenture M (1980) Toxic shock syndrome:epidemiological features,recurrence, risk factors and presentation. N. Engl. J. Med. 303: 1429–1435

    Google Scholar 

  • de Bentzmann S, Plotkowski C & Puchelle E (1996) Receptors in the Pseudomonas aeruginosa adherence to injured and repairing airway epithelium. Am. J. Respir. Crit. Care Med. 154: S155–S162

    Google Scholar 

  • DeFlaun MF, Mrshall BM, Kulle E-P & Levy SP (1994) Tn5 insertion mutants of Pseudomonas fluorescens defective in adhesion to soli and seeds. Appl. Environ. Microbiol. 30: 2637–2642

    Google Scholar 

  • DeMaria TF, Prior RB, Briggs BR, Okasaki N & Lim DJ (1984a) Experimental otitis media with effusion following middle-ear inoculation of nonviable H. influenzae. Ann. Otol. Rhinol. Laryngol. 93: 52–56

    Google Scholar 

  • DeMaria TF, Prior RB, Briggs BR, Lim DJ & Birck HG (1984b) Endotoxin in middle-ear effusions from patients with chronic otitis media with effusion. J. Clin. Microbiol. 20: 15–17

    Google Scholar 

  • Dingman JR, Rayner MG, Mishra S, Zhang Y, Ehrlich MD, Post JC & Ehrlich GD (1998) Correlation between presence of viable bacteria and presence of endotoxin in middle-ear effusions. J. Clin. Microbiol. 36: 3417–3419

    Google Scholar 

  • Domingue GJ & Hellström WJG. (1998) Prostatitis. Clin. Microbiol. Rev. 11: 604–613

    Google Scholar 

  • Domingue PA, Sdahu K, Costerton JW, Bartlett K & Chow AW (1991) The human vagina: normal flora considered as an in situ tissue-associated,adherent biofilm. Genitourin. Med. 67: 226–231

    Google Scholar 

  • Donlan RM (2001a) Biofilm formation:a clinically relevant microbiological process. Clin, Infect. Dis. 33: 1387–1392

    Google Scholar 

  • Donlan RM (2001b) Biofilms and device-associated infections. Emerg. Infect. Dis. 7: 277–281

    Google Scholar 

  • Donlan RM & Costerton JW (2002) Biofilms: Survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15: 167–193

    Google Scholar 

  • Douglas LJ (2002) Medical importance of biofilms in Candida infections. Rev. Iberoam. Micol. 19: 139–143

    Google Scholar 

  • Douglas LJ (2003) Candida biofilms and their role in infection. Trends Microbiol. 11: 30–36

    Google Scholar 

  • Dumanski AJ, Hedelin H, Edin-Liljegren A, Beauchemin D & McLean RJ (1994) Unique ability of Proteus mirabilis capsule to enhance mineral growth in infectious urinary calculi. Infect. Immun. 62: 2998–3003

    Google Scholar 

  • Duncan SH, Richardson AJ, Kaul P, Holmes RP, Allison MJ & Stewart CS (2002) Oxalobacter formigenes and its potential role in human health. Appl. Environ. Microbiol. 68: 3841–3847

    Google Scholar 

  • Durack DY (1975) Experimental bacterial endocarditis IV. Structure and evolution of very early lesions. J. Pathol. 115: 81–89

    Google Scholar 

  • Durack DY & Beeson PB (1972) Experimental bacterial endocarditis II.Survival of bacteria in endocardial vegetations. Br. J. Pathol. 53: 50–53

    Google Scholar 

  • Ehrlich GD, Veeh R, Wang X, Costerton JW, Hayes JD, Hu FZ, Daigle BJ, Herich MD & Post JC (2002) Mucosal bio lm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287: 1710–1715

    Google Scholar 

  • Elder MJ & Morlet N (2002) Endophthalmitis. EPSWA, Endophthalmitis Population Study of Western Australia. Clin. Experiment. Ophthalmol. 30: 394–398

    Google Scholar 

  • el-Shoura SM (1995) Helicobacter pylori: I. Ultrastructural sequences of adherence,attachment,and penetration into the gastric mucosa. Ultrastruct. Pathol. 19: 323–333

    Google Scholar 

  • Ferrer J (2000) Vaginal candidosis:epidemiological and etiological factors. Int. J. Gynaecol. Obstet. 71(Suppl 1): S21–S27

    Google Scholar 

  • Field LH, Underwood JL & Berry LJ (1984) The role of gut flora and animal passage in the colonization of adult mice with Campylobacter jejuni. J. Med.Microbiol. 17: 59–66

    Google Scholar 

  • Finlay BB & Falkow S (1997) Common themes in microbial pathogenicity revisited. Microbiol. Mol. Biol. Rev. 61: 136–169

    Google Scholar 

  • Fitzsimmons S, Evans M, Pearce C, Sheridan MJ, Wientzen R, Bowden G & Cole MF (1996) Clonal diversity of Streptococcus mitis biovar 1 isolates from the oral cavity of human neonates. Clin. Diagn. Lab. Immunol. 3: 517–522

    Google Scholar 

  • Flint HJ (1997) The rumen microbial ecosystem –some recent developments. Trends Microbiol. 5: 483–488

    Google Scholar 

  • Frandsen EV, Pedrazzoli V & Kilian M (1991) Ecology of viridans streptococci in the oral cavity and pharynx. Oral Microbiol. Immunol. 6: 129–133

    Google Scholar 

  • Fulcher TP, Dart JK, McLaughlin-Borlace L, Howes R, Matheson M & Cree I (2001) Demonstration of bio lm in infectious crystalline keratopathy using ruthenium red and electron microscopy. Ophthalmology 108: 1088–1092

    Google Scholar 

  • Fuller R & Gibson GR (1997) Modi cation of the intestinal microflora using probiotics and prebiotics. Scand. J. Gastroenterol. 222(Suppl.): 28–31

    Google Scholar 

  • Garrett ES, Perlegas D & Wozniak DJ (1999) Negative control of flagellum synthesis in Pseudomonas aeruginosa is modulated by the alternative sigma factor AlgT (AlgU). J.Bacteriol. 181: 7401–7404

    Google Scholar 

  • Gavin R, Rabaan AA, Merino S, Tomás J, Gryllos I & Shaw JG (2002) Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43: 383–397

    Google Scholar 

  • Geisenberger O, Givskov M, Riedel K, Høiby N, Tümmler B & Eberl L (2000) Production of N-acyl-L-homoserine lactones by P. aeruginosa isolates from chronic lung infections associated with cystic brosis. FEMS Microbiol. Lett. 184: 273–278

    Google Scholar 

  • Gibney EM & Goldfarb DS (2003) The association of nephrolithiasis with cystic brosis. Am. J. Kidney Dis. 42: 1–11

    Google Scholar 

  • Gleeson MJ & Griffith DP (1993) Struvite calculi. Br. J. Urol. 71: 503–511

    Google Scholar 

  • Govan JRW & Deretic V (1996) Microbial pathogenesis in cystic brosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60: 539–574

    Google Scholar 

  • Graf J, Dunlap PV & Ruby EG (1994) Effect of transpositioninduced motility mutations on colonization of the host light organ by Vibrio sheria. J.Bacteriol. 30: 6986–6991

    Google Scholar 

  • Gupta K, Hillier SL, Hooton TM, Roberts PL & Stamm WE (2000) Effects of contraceptive method on the vaginal microbial flora:a prospective evaluation. J. Infect. Dis. 181: 595–601

    Google Scholar 

  • Habash M Reid G (1999) Microbial biofilms: Their development and signi cance for medical device-related infections. J. Clin. Pharmacol. 39: 887–898

    Google Scholar 

  • Häußler S, Tümmler B, Weissbrodt H, Rohde M & Steinmetz I (1999) Small-colony variants of Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Clin. Infect. Dis. 29: 621–625

    Google Scholar 

  • Häußler S, Ziegler I, Löttel A, von Götz F, Rohde M, Wehmhöhner D, Saravanamuthu S, Tümmler B & Steinmetz I (2003) Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic brosis lung infection. J. Med. Microbiol. 52: 295–301

    Google Scholar 

  • Heilmann C, Hussain M, Peters G & Götz F (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol. Microbiol. 24: 1013–1124

    Google Scholar 

  • Hicks S, Candy DC & Phillips AD (1996) Adhesion of enteroaggregative Escherichia coli to formalin-xed intestinal and ureteric epithelia from children. J. Med. Microbiol. 44: 362–371

    Google Scholar 

  • Hirose K, Isogai E, Mizugai H, Ueda I (1996) Adhesion of Porphyromonas gingivalis fimbriae to human gingival cell line Ca9-22. Oral Microbiol. Immunol. 11: 402–406

    Google Scholar 

  • Høiby N, Espersen F, Fomsgaard A, Giwercman B, Jensen ET, Johansen HK, Koch C, Kronborg G, Pedersen SS & Pressler T (1994) Biofilm,foreign bodies and chronic infections. Ugeskr. Laeger 156: 5998–6005

    Google Scholar 

  • Holt SC, Kesavalu L, Walker S & Genco CA (2000) Virulence factors of Porphyromonas gingivalis. Peridontol. 20: 168–238

    Google Scholar 

  • Hooton TM, Stapleton AE, Roberts PL, Winter C, Scholes D, Bavendam T & Stamm WE (1999) Perineal anatomy and urine-voiding characteristics or young women with and without recurrent urinary tract infections. Clin. Infect. Dis. 29: 1600–1601

    Google Scholar 

  • Huber B, Riedel K, Hentzer M, Heydron A, Gotschlich A, Givskov M, Molin S & Eberl L (2001) The cep quorumsensing system of Burkholderia cepacia H111 controls bio lm formation and swarming motility. Microbiology 147: 2517–2528

    Google Scholar 

  • Hume EB, Stapleton F & Willcox MD (2003) Evasion of cellular ocular defenses by contact lens isolates of Serratia marcescens. Eye Contact Lens 29: 108–112

    Google Scholar 

  • Isles A, MacLusky I, Corey M, Gold R, Prober C, Fleming P & Levison H (1984) Pseudomonas cepacia infection in cystic brosis:an emerging problem. J. Pediatr. 104: 206–221

    Google Scholar 

  • Jansen HJ, Hart CA, Rhodes JM, Saunders JR & Smalley JW (1999) A novel mucin-sulfatase activity found in Burkholderia cepacia and Pseudomonas aeruginosa. J. Med. Microbiol. 48: 551–557

    Google Scholar 

  • Joly V, Pangon B, Vallois J-M, Abel L, Brion N, Bure A, Chau NP, Contrepois A & Carbon C (1987) Value of antibiotic levels in serum and cardiac vegetations for predicting antibacterial effect of ceftriaxone in experimental Escherichia coli endocarditis. Antimicrob. Agents Chemother. 31: 1632–1639

    Google Scholar 

  • Kaitwatcharachai C, Silpapojakul K, Jitsurong S & Kal nauwakul S (2000) An outbreak of Burkholderia cepacia bacteremia in haemodialysis patients:An epidemiologic and molecular study. Am. J. Kidney Dis. 36: 199–204

    Google Scholar 

  • Kawashima M, Hanada N, Hamada T, Tagami J & Senpuku H (2003) Real-time interaction of oral streptococci with human salivary components. Oral Microbiol. Immunol. 18: 220–225

    Google Scholar 

  • Kilian M, Reinholdt J, Lomholt H, Poulsen K & Frandsen EVG (1996) Biological signi cance of IgA1 proteases in bacterial colonization and pathogenesis:critical evaluation of experimental evidence. APMIS 104: 321–338

    Google Scholar 

  • Koch C & Høiby N (1993) Pathogenesis of cystic fibrosis. Lancet 341: 1065–1069

    Google Scholar 

  • Kolenbrander PE, Andersen RN, Kazmerzak KM Palmer Jr RJ (2000) Coaggregation and coadhesion in oral biofilms. In: Allison DG, Gilbert P, Lappin-Scott HM & Wilson M (Eds) Community Structure and Cooperation in Biofilms (pp 65–85). Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Kontani M, Ono H, Shibata H, Okamura Y, Tanaka T, Fujiwara T, Kimura S & Hamada S (1996) Cysteine protease of Porphyromonas gingivalis 381 enhances binding of mbriae to cultured human broblasts and matrix proteins. Infect. Immun. 64: 756–762

    Google Scholar 

  • Korber DR, Lawrence JR & Caldwell DE (1994) Effect of motility on surface colonization and reproductive success of Pseudomonas fluorescens in dual-dilution continuous culture and batch culture systems. Appl. Environ. Microbiol. 30: 1421–1429

    Google Scholar 

  • Kuramitsu HK (1998) Proteases of Porphyromonas gingivalis: What don't they do? Oral. Microbiol. Immunol. 13: 263–270

    Google Scholar 

  • Kwak C, Jeong BC, Kim HK, Kim EC, Chox MS & Kim HH (2003) Molecular epidemiology of fecal Oxalobacter formigenes in healthy adults living in Seoul, Korea. J Endourol. 17: 239–243

    Google Scholar 

  • Lamont RJ & Jenkinson HF (1998) Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Bio. Rev. 62: 1244–1263

    Google Scholar 

  • Lamont RJ & Jenkinson HF (2000) Subgingival colonization by Porphyromonas gingivalis. Oral. Microbiol. Immunol. 15: 341–349

    Google Scholar 

  • Lamont RJ, Hersey SG & Rosan B (1992) Characterization of the adherence of Porphyromonas (Bacteroides )gingivalis to oral streptococci. Oral. Microbiol. Immunol. 7: 193–197

    Google Scholar 

  • Lamont RJ, Gil S, Demuth DR, Malamud D & Rosan B (1994) Molecules of Streptococcus gordonii that bind to Porphyromonas gingivalis. Microbiology 140: 867–872

    Google Scholar 

  • Lawrence JR, Delaquis PJ, Korber DR & Caldwell DE (1987) Behavior of Pseudomonas fluorescens within the hydrodynamic boundary layers of surface microenvironments. Microb. Ecol. 30: 1–14

    Google Scholar 

  • Leid JG, Costerton JW, Shirtliff ME, Gilmore MS & Engelbert M (2002) Immunology of Staphylococcal biofilm infections in the eye: new tools to study bio lm endophthalmitis. DNA Cell. Biol. 21: 405–413

    Google Scholar 

  • Lewenza S, Conway B, Greenberg EP & Sokol PA (1999) Quorum sensing in Burkholderia cepacia: identification of the LuxRI homologs CepIR. J. Bacteriol. 181: 748–756

    Google Scholar 

  • Li J, Ellen RP, Hoover CJ & Felton JR (1991) Association of proteases of Porphyromonas (Bacteroides) gingivalis with its adhesion to Actinomyces viscosus. J. Dent. Res. 70: 82–86

    Google Scholar 

  • Licht TR, Christensen BB, Krogfelt KA & Molin S (1999) Plasmid transfer in the animal intestine and other dynamic bacterial populations: the role of community structure and environment. Microbiology 145: 2615–5622

    Google Scholar 

  • LiPuma JJ, Spilker JT, Gill LH, Campbell III PW & Mahenthiralingam E (2001) Disproportionate distribution of Burkholderia cepacia complex species and transmissibility markers in cystic fibrosis. Am. J. Respir. Care Med. 164: 92–96

    Google Scholar 

  • Livornese LL & Korzeniowski OM (1992) Pathogenesis of infective endocarditis. In: Kaye D (Ed.) Infective Endocarditis, 2nd Edn (pp 19–35). Raven Press, New York, NY

    Google Scholar 

  • Lowrance JH, Hasty DL & Simpson WA (1988) Adherence of Streptococcus sanguis to conformationally speci c determinants in fibronectin. Infect. Immun. 56: 2279–2285

    Google Scholar 

  • Lyczak JB, Cannon CL & Pier GB (2002) Lung infections associated with cystic fibrosis. Clin. Microbiol. Rev. 15: 194–222

    Google Scholar 

  • Macfarlane S, Hopkins MJ & Macfarlane GT (2000) Bacterial growth and metabolism on surfaces in the large intestine. Microb. Ecol. Health Dis. 2: 64–72

    Google Scholar 

  • Mackay WG, Gribbon LT, Barer MR & Reid DC (1999) Biofilms in drinking water systems:a possible reservoir for Helicobacter pylori. J. Appl. Microbiol. Symp. Suppl. 85: 52S–59S

    Google Scholar 

  • Macpherson AJ, Martinic MM & Harris N (2002) The functions of mucosal T cells in containing the indigenous commensal flora of the intestine. Cell Mol. Life Sci. 59: 2088–2096

    Google Scholar 

  • Marsh PD (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149: 279–294

    Google Scholar 

  • Marsh PD & Bowden GHW. (2000) Microbial community interactions in biofilms. In: Allison DG, Gilbert P, LappinScott HM & Wilson M (Eds) Community Structure and Cooperation in Biofilms (pp 167–198). Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Marsh PD & Bradshaw DJ (1997) Physiological approaches to the control of oral biofilms. Adv. Dent. Res. 11: 176–185

    Google Scholar 

  • Marsh PD & Martin MV (1999) In Oral Microbiology, 4th Edn, Oxford, Wright

    Google Scholar 

  • Mathee K, Ciofu O, Sternberg C, Lindum PW, Campbell JIA., Jensen P, Givskov M, Ohman DE, Molin S, Høiby N & Kharazmi A (1999) Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide:a mechanism for virulence activation in the cystic brosis lung. Microbiology 145: 1349–1357

    Google Scholar 

  • May TB, Shinabarger D, Maharai R, Kato J, Chu L, DeVault JD, Roychoudhury S, Zielinski NA, Berry A, Rothmel RK, Misra TK & Chakrabarty AM (1991) Alginate synthesis by Pseudomonas aeruginosa: a key pathogenic factor in chronic pulmonary infections of cystic brosis patients. Clin. Microbiol. Rev. 4: 191–206

    Google Scholar 

  • McCarter L & Silverman M (1990) Surface-induced swarmer cell differentiation of Vibrio parahaemolyticus. Mol. Micro biol. 4: 1057–1062

    Google Scholar 

  • McFarlane GT & McFarlane S (1997) Human colonic microbiota:physiology and metabolic potential of intestinal bacteria. Scand. J. Gastroenterol. 222(Suppl.): 3–9

    Google Scholar 

  • McLaughlin-Borlace L, Stapleton F, Matheson M & Dart JK (1998) Bacterial bio lm on contact lenses and lens storage cases in wearers with microbial keratitis. J. Appl. Microbiol. 84: 827–838

    Google Scholar 

  • McLean RJC, Lawrence JR, Korber DR & Caldwell DE (1991) Proteus mirabilis biofilm protection against struvite crystal dissolution and its implications in struvite urolithiasis. J.Urol. 146: 1138–1142

    Google Scholar 

  • Mills AL Powelson DK (1996) Bacterial interactions with surfaces in soil. In: Fletcher M (Ed.) Bacterial Adhesion: Molecular and Ecological Diversity (pp 25 –57). John Wiley & Sons, New York

    Google Scholar 

  • Milnes AR, Bowden GH, Gates D & Tate R (1993) Predominant cultivable microorganisms on the tongue of pre-school children.Microb. Ecol. Health Dis. 6: 229–235

    Google Scholar 

  • Miyanaga Y (1997) A new perspective in ocular infection and the role of antibiotics. Ophthalmologica 211(Suppl.1): 9–14

    Google Scholar 

  • Monif GR Carson HJ (1998) Female genital tract bacterial coisolates with Candida albicans in patients without clinical vaginitis. Infect. Dis. Obstet. Gynecol. 6: 52–56

    Google Scholar 

  • Moore KN, Day RA & Albers M (2002) Pathogenesis of urinary tract infections:a review. J. Clin. Nurs. 11: 568–574

    Google Scholar 

  • Moran AP (2001) Molecular structure,biosynthesis and pathogenic roles of Helicobacter pylori lipopolysaccharides. In: Mobley H, Mendz G & Hazell S (Eds) Helicobacter pylori: Physiology and Genetics (pp 81–95). ASM Press, Washington DC

    Google Scholar 

  • Moran AP & Ljungh Å (2003) Physico-chemical properties of the biofilm matrix. In: Lens P, Moran AP, Mahony T, Stoodley P & O'Flaherty V (Eds) Biofilms in Medicine, Industry and Environmental Biotechnology. Characteristics, analysis and control (pp 81–90). IWA Publishing, London, UK

    Google Scholar 

  • Moran AP & Prendergast MM (2001) Molecular mimicry in Campylobacter jejuni and Helicobacter pylori lipopolysaccharides. J. Autoimmun. 16: 241–256

    Google Scholar 

  • Moran AP, Prendergast MM & Appelmelk BJ (1996) Molecular mimicry of host structures by bacterial lipopolysaccharides and its contribution to disease. FEMS Immunol. Med. Microbiol. 16: 105–115

    Google Scholar 

  • Morris NS, Stickler DJ McLean RJ (1999) The development of bacterial bio lms on indwelling urethral catheters. World J.Urol. 17: 345–350

    Google Scholar 

  • Murphy TF & Kirkham C (2002) Biofilm formation by nontypable Haemophilus influenzae: Strain variability,outer membrane antigen expression and role of pili.BMC Microbiol. 2: 7

    Google Scholar 

  • Nataro JP & Kaper JB (1998) Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142–201

    Google Scholar 

  • Nataro JP, Yikang D, Cookson S, Cravioto A, Savarino SJ, Guers LD, Levine MM & Tacket CO (1995) Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J. Infect. Dis. 171: 465–468

    Google Scholar 

  • Nataro JP, Hicks S, Phillips AD, Vial PA & Sears CL (1996) T84 cells in culture as a model for enteroaggregative Escherichia coli pathogenesis. Infect. Immun. 64: 4761–4768

    Google Scholar 

  • Nataro JP, Steiner T & Guerrant RL (1998) Enteroaggregative Escherichia coli. Emerg. Infect. Dis. 4: 251–261

    Google Scholar 

  • Nickel JC (1990) The battle of the bladder: the pathogenesis and treatment of uncomplicated cystitis. Int. Urogynecol. J. 1: 218–222

    Google Scholar 

  • Nickel JC (1998) Bacterial bio lms in urology. Infect. Urol. 11: 169–175

    Google Scholar 

  • Nickel JC Costerton JW (1992) Coagulase-negative staphylococcus in chronic prostatitis. J. Urol. 147: 398–401

    Google Scholar 

  • Nickel JC & Costerton JW (1993) Bacterial localization in antibiotic-refractory chronic bacterial prostatitis. Prostate 23: 107–114

    Google Scholar 

  • Nickel JC, Olson M, McLean RJ, Grant SK & Costerton JW (1987) An ecological study of infected urinary stone genesis in an animal model. Br. J. Urol. 59: 21–30

    Google Scholar 

  • Nickel JC, Olson ME, Barabas A, Benediktsson H, Dasgupta MK & Costerton JW (1990) Pathogenesis of chronic bacterial prostatitis in animal model. Br. J. Urol. 66: 47–54

    Google Scholar 

  • Nickel JC, Costerton JW, McLean RJC.& Olson M (1994) Bacterial biofilms: influence on the pathogenesis, diagnosis, and treatment of urinary tract infections. J. Antimicrob. Chemother. 33 (Suppl A): 31–41

    Google Scholar 

  • Nielsen AT, Toker-Niesen T, Barken KB & Molin S (2000) Role of commensal relationship on the spatial structure of a surface-attached microbial consortium. Environ. Microbiol. 2: 59–68

    Google Scholar 

  • Oelschlaeger TA, Dobrindt U & Hacker J (2002) Virulence factors of uropathogens. Curr. Opin. Urol. 12: 33–38

    Google Scholar 

  • Oliver A, Caton R, Campo P, Baquero F & Blazquez J (2000) High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288: 1251–1254

    Google Scholar 

  • O'Toole GA & Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295–304

    Google Scholar 

  • Park SR, Mackay WG & Reid DC (2001) Helicobacter sp. recovered from drinking water bio lm sampled from a water distribution system. Water Res. 35: 1624–1626

    Google Scholar 

  • Pearce C, Bowden GH, Evans M, Fitzsimmons SP, Johnson J, Sheridan MJ, Wientzen R & Cole MF (1995) Identification of pioneer viridans streptococci in the oral cavity of human neonates. J. Med. Microbiol. 42: 67–72

    Google Scholar 

  • Pier GB, Grout M, Zaidi TS, Olsen JC, Johnson LG, Yankaskas JR & Goldberg JB (1996) Role of mutant CFTR in hypersusceptibility of cystic brosis patients to lung infections. Science 271: 64–67

    Google Scholar 

  • Post JC (2001) Direct evidence of bacterial biofilms in otitis media. Laryngoscope 111: 2083–2094

    Google Scholar 

  • Potera C (1999) Forging a link between biofilms and disease. Science 283: 1837–1838

    Google Scholar 

  • Pratt LA & Kolter R (1998) Genetic analysis of Escherichia coli bio lm formation: roles of flagella,motility,chemotaxis and type I pili. Mol. Microbiol. 30: 285–293

    Google Scholar 

  • Prigent-Combaret C, Vidal O, Dorel C & Lejeune P (1999) Abiotic surface sensing and biofilm dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181: 5993–6002

    Google Scholar 

  • Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejejune P & Dorel C (2000) Developmental pathway for biofilm formation in curli-producing Escherichia coli strains:role of flagella, curli and colanic acid. Environ.Microbiol. 2: 450–464

    Google Scholar 

  • Purevdorj BL & Stoodley P (2003) The role of cell signalling in biofilm development. In: Lens P, Moran AP, Mahony T, Stoodley P & O'Flaherty V (Eds) Biofilms in Medicine, Industry and Environmental Biotechnology.Characteristics, analysis and control (pp 81–90). IWA Publishing, London, UK

    Google Scholar 

  • Rahman NU, Meng MV & Stoller ML (2003) Infections and urinary stone disease. Curr. Pharm. Des. 9: 975–981

    Google Scholar 

  • Rainey PB & Travisano M (1998) Adaptive radiation in a heterogeneous environment. Nature 394: 69–72

    Google Scholar 

  • Rayner MG, Zhang Y, Gorry MC, Chen Y, Post JC & Ehrlich GD (1998) Evidence of bacterial metabolic activity in culturenegative otitis media with effusion. Clin. Invest. 279: 296–299

    Google Scholar 

  • Reid G (2001) Probiotic agents to protect the urogenital tract against infection. Am. J. Clin. Nutr. 73(Suppl.2): 437S–443S

    Google Scholar 

  • Reid G, Bruce AW, Cook RL & Llano M (1990) Effect on urogenital flora of antibiotic therapy for urinary tract infection. Scand. J. Infect. Dis. 22: 43–47

    Google Scholar 

  • Riedel K, Hentzer M, Geisenberger O, Huber B, Steidel A, Wu H, Høiby N, Givskov M, Molin S & Eberl L (2001) N-Acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147: 3249–3262

    Google Scholar 

  • Roberts RB (1992) Pathogenesis of infective endocarditis. In: Kaye D (Ed) Infective Endocarditis, 2nd edn (pp 191 –208). Raven Press, New York, NY

    Google Scholar 

  • Roland PS (2002) Chronic suppurative otitis media:A clinical overview. Ear Nose Throat J. 81: 8–10

    Google Scholar 

  • Saiman L & Prince A (1993) Pseudomonas aeruginosa pili binfd to asialoGM1 which is increased on the surface of cysic brosis epithelial cells. J. Clin. Invest. 92: 1875–1880

    Google Scholar 

  • Saiman L, Cacalano G & Prince A (1990) Pseudomonas cepacia adherence to respiratory epithelial cells is enhanced by Pseudomonas aeruginosa. Infect. Immun. 58: 2578–2584

    Google Scholar 

  • Salminen S & Salminen E (1997) Lactulose,lactic acid bacteria, intestinal microecology and mucosal protection. Scand. J. Gastroenterol. 222(Suppl.): 45–48

    Google Scholar 

  • Sandkvist M, Overbye LM, Hough LM, Morales VM, Bagdasarian M, Koomey M, DiRita VJ & Bagdasarian M (1997) General secretion pathway (eps )genes required for toxin secretion and outer membrane biogenesis in Vibrio cholerae. J. Bacteriol. 179: 6994–7003

    Google Scholar 

  • Sauer K & Camper AK (2001) Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J. Bacteriol. 183: 6579–6589

    Google Scholar 

  • Schmitz W, Nolde A, Marklein G & Hesse A (1993) In vitro studies of encrustations on catheters,a model of infection stone formation. Cells Mater. 3: 1–10

    Google Scholar 

  • Schwab U, Leigh M, Ribeiro C, Yankaskas J, Burns K, Gilligan P, Sokol P & Boucher R (2002) Patterns of epithelial cell invasion by different species of the Burkholderia cepacia complex in well-differentiated human airway epithelia. Infect. Immun. 70: 4547–4555

    Google Scholar 

  • Sethi S & Murphy TF (2001) Bacterial infection in chronic obstructive pulmonary disease in 2000.A state of the art review. Clin. Microbiol. Rev. 14: 336–363

    Google Scholar 

  • Sheikh J, Hicks S, Dall'Angol M, Phillips AD & Nataro JP (2001) Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol. Microbiol. 41: 983–997

    Google Scholar 

  • Siebers A & Finlay BB (1996) M cells and the pathogenesis of mucosal and systemic infections. Trends Microbiol. 4: 22–29

    Google Scholar 

  • Speer AG, Cotton PB, Rode J, Seddon AM, Neal CR, Holton J & Costerton JW (1988) Biliary stent blockage with bacterial bio lm.A light and electron microscopy study. Ann. Intern. Med. 108: 46–53

    Google Scholar 

  • Speradino V, Mellies JL, Nguyen W, Shin S & Kaper JB (1999) Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohaemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 96: 15196–15201

    Google Scholar 

  • Stark MR, Gerwig GJ, Pitman RS, Potts LF, Williams NA, Greenman J, Weinzweig IP, Hirst TR & Millar MR (1999) Biofilm formation by Helicobacter pylori. Lett. Appl. Microbiol. 28: 121–126

    Google Scholar 

  • Steiner TS, Lima AA, Nataro JP & Guerrant RL (1998) Enteroaggregative Escherichia coli produce intestinal in flammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J. Infect. Dis. 177: 88–96

    Google Scholar 

  • Stenfors LE & Raisanen S (1988) Quantification of bacteria in middle ear effusions. Acta Otolaryngol.(Stockholm) 106: 435–440

    Google Scholar 

  • Stickler DJ, King JB, Winters C & Morris SL (1993) Blockage of urethral catheters by bacterial biofilms. J. Infect. 27: 133–135

    Google Scholar 

  • Stiles GL & Friesinger GC (1980) Bacterial endocarditis with aortic regurgitation: implicants of embolism. South. Med. J. 73: 582–586

    Google Scholar 

  • Sugita J, Yokoi N, Fullwood NJ, Quantock AJ, Takada Y, Nakamura Y & Kinoshita S (2001) The detection of bacteria and bacterial bio lms in punctal plug holes. Cornea 20: 362–365

    Google Scholar 

  • Surette MG, Miller MB & Bassler BJ (1999) Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: A new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. USA 96: 1639–1644

    Google Scholar 

  • Theilade E (1990) Factors controlling the microflora of the healthy mouth. In: Hill MJ & Marsh PD (Eds) Human Microbial Ecology (pp 1–56). CRC Press, Inc., Boca Raton, Fla

    Google Scholar 

  • Thelin KH & Taylor RK (1996) Toxin-coregulated pilus,but not mannose-sensitive hemagglutinin,is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect. Immun. 64: 2853–2856

    Google Scholar 

  • Trachoo N, Frank JF & Stern NJ (2002) Survival of Campylobacter jejuni in bio lms isolated from chicken houses. J. Food Prot. 65: 1110–1116

    Google Scholar 

  • Troxel SA, Sidhu H, Kaul P & Low RK (2003) Intestinal Oxalobacter formigenes colonization in calcium oxalate stone formers and its relation to urinary oxalate. J. Endourol. 17: 173–176

    Google Scholar 

  • Tunkel AR & Mandell GL (1992) Pathogenesis of infective endocarditis. In: Kaye D (Ed) Infective Endocarditis, 2nd edn (pp 85–97). Raven Press, New York, NY

    Google Scholar 

  • Ulrich M, Ramphal R, Guay CM, DesJardins D & Pier GB (1998) Localization of Staphylococcus aureus in infected airways of patients with cystic brosis and in a cell culture model of S.aureus adherence. Am. J. Respir. Cell Mol. Biol. 19: 83–91

    Google Scholar 

  • van Bijsterveld OP & Jager GV (1996) Infectious diseases of the conjunctiva and cornea. Curr. Opin. Ophthalmol. 7: 65–70

    Google Scholar 

  • Velraeds MCM, Van der Mei HC, Reid G & Busscher HJ (1996) Inhibition of initial adhesion of uropathogenic Enterococcus faecalis by biosurfactants from Lactobacillus isolates. Appl. Environ. Microbiol. 62: 1958–1963

    Google Scholar 

  • Victoria JM, Kalapothakis E, Silva Jd Jde F & Gomez RS (2003) Helicobacter pylori DNA in recurrent aphthous stomatitis. J. Oral. Pathol. Med. 32: 219–223

    Google Scholar 

  • Vidal O, Longin R, Prigent-Combaret C, Dorel C, Hooreman M & Lejeune P (1998) Isolation of an Escherichia coli K-12 mutant strain able to form bio lms on inert surfaces: Involvement of a new omp R allele that increases curli expression. J. Bacteriol. 30: 2442–2449

    Google Scholar 

  • Wanke CA, Cronan S, Goss C, Chadee K & Guerrant RL (1990) Characterization of binding of Escherichia coli strains which are enteropathogens to small-bowel mucin. Infect. Immun. 58: 794–800

    Google Scholar 

  • Watnick PI & Kolter R (1999) Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34: 586–595

    Google Scholar 

  • Watnick PI, Fullner KJ & Kolter R (1999) A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J. Bacteriol. 181: 3606–3609

    Google Scholar 

  • Watnick PI, Laurino CM, Klose KE, Croal L & Kolter R (2001) The absence of a flagellum to altered colony morphology, biofi lm development and virulence in Vibrio chole rae O139. Mol. Microbiol. 39: 223–235

    Google Scholar 

  • Weinberg A, Belton CM, Park Y & Lamont RJ (1997) Role of mbriae in Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 65: 313–316

    Google Scholar 

  • Weimer PJ (1998) Manipulating ruminal fermentation:A microbial ecological perspective. J. Anim. Sci. 76: 3114–3122

    Google Scholar 

  • Wilson M (2001) Bacterial bio lms and human disease. Sci. Prog. 84: 235–254

    Google Scholar 

  • Wilson M, Reddi K & Henderson B (1996) Cytokine-inducing components of periodontopathogenic bacteria. J. Periodont. Res. 31: 393–407

    Google Scholar 

  • Wise GJ (2001) Genitourinary fungal infections:A therapeutic conundrum. Expert Opin.Pharmacother. 2: 1211–1226

    Google Scholar 

  • Withers HL & Nordstrom K (1998) Quorum-sensing acts at initiation of chromosomal replication in Escherichia coli. Proc. Natl. Acad. Sci. USA 95: 15694–15699

    Google Scholar 

  • Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, Birrer P, Bellon G, Berger J, Weiss T, Botzenhart K, Yankaskas JR, Randell S, Boucher RC & Döring G (2002) Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic brosis patients. J. Clin. Invest. 109: 317–325

    Google Scholar 

  • Xie H, Cook GS, Costerton JW, Bruce G, Rose TM & Lamont RJ (2000) Intergeneric communication in dental plaque biofilms. J. Bacteriol. 182: 7067–7069

    Google Scholar 

  • Xu KD, McFeters GA & Stewart PS (2000) Biofilm resistance to antimicrobial agents. Microbiology 146: 547–549

    Google Scholar 

  • Zegans ME, Becker HI, Budzik J & O'Toole G (2002) The role of bacterial biofilms in ocular infections. DNA Cell. Biol. 21: 415–420

    Google Scholar 

  • Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL & Mekalanos JJ (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99: 3129–3134

    Google Scholar 

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    A.P. Moran & H. Annuk

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Moran, A., Annuk, H. Recent Advances in Understanding Biofilms of Mucosae. Re/Views in Environmental Science and Bio/Technology 2, 121–140 (2003). https://doi.org/10.1023/B:RESB.0000040462.36578.54

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