Chapter 17 : Biofilms as Reservoirs for Disease

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There is concern that biofilms could act as reservoirs of pathogenic organisms due to the growth advantages and the protection from conventional means for controlling bacterial growth that biofilms provide. Given the importance of waterborne, nosocomial, and food-borne diseases, the widespread ability of bacteria to form biofilms, and the resistance characteristics of biofilms, an attempt has been made to synthesize the prevalence, disease characteristics, and biofilm-forming capacity of several important pathogens to present a picture of the present and emerging threat of biofilms to human health. Researchers selected organisms that have documented prevalence in the environment and in locations that allow ingestion or inhalation, documented ability to form biofilms, and ability to cause disease. Such microbes include the waterborne pathogens spp., , spp., and , and the food-borne pathogens spp., , and spp. In summary, biofilms act as reservoirs of disease in a wide variety of habitats, including natural surface waters, groundwater, drinking water systems, food surfaces, and food industry surfaces. The presence of pathogenic bacteria in biofilms is clearly a challenge for protecting public health given the changing demographics of the world population, the increase in immunocompromised individuals, and the continued problems with water and food quality in the world.

Citation: Flanders J, Yildiz F. 2004. Biofilms as Reservoirs for Disease, p 314-331. In Ghannoum M, O'Toole G (ed), Microbial Biofilms. ASM Press, Washington, DC. doi: 10.1128/9781555817718.ch17
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1. Advisory Committee on the Microbiological Safety of Food. 1993. Interim Report on Campylobacter. HMSO, London, United Kingdom.
2. Ali, A.,, M. H. Rashid,, and D. K. R. Karaolis. 2002. High-frequency rugose exopolysaccharide production by Vibrio cholerae. Appl. Environ. Microbiol. 68:57735778.
3. Anaissie, E. J.,, S. R. Penzak,, and M. C. Dignani. 2002. The hospital water supply as a source of nosocomial infections: a plea for action. Arch. Intern. Med. 162:14831492.
4. Armon, R.,, T. Starosvetzky,, T. Arbel,, and M. Green. 1997. Survival of Legionella pneumophila and Salmonella typhimurium in biofilm systems. Water Sci. Technol. 35:293.
5. Atlas, R. M. 1999. Legionella: from environmental habitats to disease pathology, detection and control. Environ. Microbiol. 1:283293.
6. Atlas, R. M.,, J. F. Williams,, and M. K. Huntington. 1995. Legionella contamination of dental-unit waters. Appl. Environ. Microbiol. 61: 12081213.
7. Barbeau, J.,, C. Gauthier,, and P. Payment. 1998. Biofilms, infectious agents, and dental unit waterlines: a review. Can. J. Microbiol. 44:10191028.
8. Barker, J.,, and S. F. Bloomfield. 2000. Survival of Salmonella in bathrooms and toilets in domestic homes following salmonellosis. J. Appl. Microbiol. 89:137144.
9. Benson, R. F.,, and B. S. Fields. 1998. Classification of the genus Legionella. Semin. Respir. Infect. 13: 9099.
10. Berendt, R. F.,, H. W. Young,, R. G. Allen,, and G. L. Knutsen. 1980. Dose-response of guinea pigs experimentally infected with aerosols of Legionella pneumophila. J. Infect. Dis. 141:186192.
11. Beuchat, L. R. 2002. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 4:413423.
12. Blackman, I. C.,, and J. F. Frank. 1996. Growth of Listeria monocytogenes as a biofilm on various foodprocessing surfaces. J. Food Prot. 59:827831.
13. Bomchil, N.,, P. Watnick,, and R. Kolter. 2003. Identification and characterization of a Vibrio cholerae gene, mbaA, involved in maintenance of biofilm architecture. J. Bacteriol. 185:13841390.
14. Brandi, G.,, M. Sisti,, F. Giardini,, G. F. Schiavano,, and A. Albano. 1999. Survival ability of cytotoxic strains of motile Aeromonas spp. in different types of water. Lett. Appl. Microbiol. 29:211215.
15. Bremer, P. J.,, I. Monk,, and C. M. Osborne. 2001. Survival of Listeria monocytogenes attached to stainless steel surfaces in the presence or absence of Flavobacterium spp. J. Food Prot. 64:13691376.
16. Brennan, P. J.,, and H. Nikaido. 1995. The envelope of mycobacteria. Annu. Rev. Biochem. 64: 2963.
17. Brenner, F. W.,, R. G. Villar,, F. J. Angulo,, R. Tauxe,, and B. Swaminathan. 2000. Salmonella nomenclature. J. Clin. Microbiol. 38:24652467.
18. Buswell, C. M.,, Y. M. Herlihy,, C. W. Keevil,, and S. A. Leach,. 1997. The effect of aquatic biofilm structure on the survival of the enteric pathogen Campylobacter jejuni in water. In C. W. Keevil, , A. Godfree, , D. Holt, , and C. Dow (ed.), Biofilms in the Aquatic Environment. The Royal Society of Chemistry, Cambridge, United Kingdom.
19. Buswell, C. M.,, Y. M. Herlihy,, L. M. Lawrence,, J. T. McGuiggan,, P. D. Marsh,, C. W. Keevil,, and S. A. Leach. 1998. Extended survival and persistence of Campylobacter spp. in water and aquatic biofilms and their detection by immunofluorescent-antibody and -rRNA staining. Appl. Environ. Microbiol. 64:733741.
20. Carter, A. M.,, R. E. Pacha,, G. W. Clark,, and E. A. Williams. 1987. Seasonal occurrence of Campylobacter spp. in surface waters and their correlation with standard indicator bacteria. Appl. Environ. Microbiol. 53:523526.
21. Centers for Disease Control and Prevention. 2001. Legionellosis. Centers for Disease Control and Prevention, Atlanta, Ga.
22. Chauret, C.,, C. Volk,, R. Creason,, J. Jarosh,, J. Robinson,, and C. Warnes. 2001. Detection of Aeromonas hydrophila in a drinking-water distribution system: a field and pilot study. Can. J. Microbiol. 47:782786.
23. Chiavelli, D. A.,, J. W. Marsh,, and R. K. Taylor. 2001. The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl. Environ. Microbiol. 67:32203225.
24. Chopra, A. K.,, and C. W. Houston. 1999. Enterotoxins in Aeromonas-associated gastroenteritis. Microbes Infect. 1:11291137.
25. Colwell, R. R.,, A. Huq,, M. S. Islam,, K. M. A. Aziz,, M. Yunus,, N. H. Khan,, A. Mahmud,, R. B. Sack,, G. B. Nair,, J. Chakraborty,, D. A. Sack,, and E. Russek-Cohen. 2003. Reduction of cholera in Bangladeshi villages by simple filtration. Proc. Natl. Acad. Sci. USA 100: 10511055.
26. Colwell, R. R.,, and W. M. Spira,. 1992. The ecology of Vibrio cholerae, p. 107127. In D. Barua, and W. B. Greennough III (ed.), Cholera. Plenum Medical Books, New York, N.Y.
27. Costerton, J. W.,, Z. Lewandowski,, D. E. Caldwell,, D. R. Korber,, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:71145.
28. Croci, L.,, S. Di Pasquale,, L. Cozzi,, and L. Toti. 2001. Behavior of Aeromonas hydrophila in bottled mineral waters. J. Food Prot. 64:18361840.
29. Drenkard, E.,, and F. Ausubel. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416:740743.
30. Falkinham, J. O., III,, C. D. Norton, , and M. W. LeChevallier. 2001. Factors influencing numbers of Mycobacterium avium, Mycobacterium intracellulare, and other Mycobacteria in drinking water distribution systems. Appl. Environ. Microbiol. 67:12251231.
31. Faruque, S. M.,, M. J. Albert,, and J. J. Mekalanos. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol. Mol. Biol. Rev. 62:13011314.
32. Fields, B. S., 2002. The social life of Legionellae, p. 135142. In R. Marre et al. (ed.), Legionella. ASM Press, Washington, D.C.
33. French, A. L.,, D. A. Benator,, and F. M. Gordin. 1997. Nontuberculous mycobacterial infections. Med. Clin. N. Am. 81:361379.
34. Garrec, N.,, F. Picard-Bonnaud,, and A. M. Pourcher. 2003. Occurrence of Listeria spp. and L. monocytogenes in sewage sludge used for land application: effect of dewatering, liming and storage in tank on survival of Listeria species. FEMS Immunol. Med. Microbiol. 35:275283.
35. Gavin, R.,, A. A. Rabaan,, S. Merino,, J. M. Tomacutes,, I. Gryllos,, and J. G. Shaw. 2002. Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol. Microbiol. 43:383397.
36. Gavriel, A. A.,, J. P. Landre,, and A. J. Lamb. 1998. Incidence of mesophilic Aeromonas within a public drinking water supply in north-east Scotland. J. Appl. Microbiol. 84:383392.
37. Gerstel, U.,, and U. Romling. 2001. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ. Microbiol. 3:638648.
38. Graham, S. M. 2002. Salmonellosis in children in developing and developed countries and populations. Curr. Opin. Infect. Dis. 15:507512.
39. Hall-Stoodley, L.,, and H. Lappin-Scott. 1998. Biofilm formation by the rapidly growing mycobacterial species Mycobacterium fortuitum. FEMS Microbiol. Lett. 168:7784.
40. Haugo, A. J.,, and P. I. Watnick. 2002. Vibrio cholerae CytR is a repressor of biofilm development. Mol. Microbiol. 45:471483.
41. Heller, R.,, C. Holler,, R. Sussmuth,, and K. O. Gundermann. 1998. Effect of salt concentration and temperature on survival of Legionella pneumophila. Lett. Appl. Microbiol. 26:6468.
42. Hood, M. A.,, and G. E. Ness. 1982. Survival of Vibrio cholerae and Escherichia coli in estuarine waters and sediments. Appl. Environ. Microbiol. 43:578584.
43. Hood, M. A.,, and P. A. Winter. 1997. Attachment of Vibrio cholerae under various environmental conditions and to selected substrates. FEMS Microbiol. Ecol. 22:215223.
44. Hunter, P.,, J. Colford,, M. LeChevallier,, S. Binder,, and P. Berger. 2001. Waterborne disease. Emerg. Infect. Dis. 7:544.
45. Huq, A.,, R. R. Colwell,, M. A. Chowdhury,, B. Xu,, S. M. Moniruzzaman,, M. S. Islam,, M. Yunus,, and M. J. Albert. 1995. Coexistence of Vibrio cholerae O1 and O139 Bengal in plankton in Bangladesh. Lancet 345:1249.
46. Huq, A.,, S. A. Huq,, D. J. Grimes,, M. O’Brien,, K. H. Chu,, J. M. Capuzzo,, and R. R. Colwell. 1986. Colonization of the gut of the blue crab (Callinectes sapidus) by Vibrio cholerae. Appl. Environ. Microbiol. 52:586588.
47. Huq, A.,, E. B. Small,, P. A. West,, M. I. Huq,, R. Rahman,, and R. R. Colwell. 1983. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl. Environ. Microbiol. 45: 275283.
48. Islam, M. S.,, B. S. Drasar,, and D. J. Bradley. 1989. Attachment of toxigenic Vibrio cholerae O1 to various freshwater plants and survival with a filamentous green alga, Rhizoclonium fontanum. J. Trop. Med. Hyg. 92:396401.
49. Islam, M. S.,, B. S. Drasar,, and D. J. Bradley. 1990. Long-term persistence of toxigenic Vibrio cholerae O1 in the mucilaginous sheath of a bluegreen alga, Anabaena variabilis. J. Trop. Med. Hyg. 93:133139.
50. Islam, M. S.,, B. S. Drasar,, and R. B. Sack. 1993. The aquatic environment as a reservoir of Vibrio cholerae: a review. J. Diarrhoeal Dis. Res. 11:197206.
51. Islam, M. S.,, Z. Rahim,, M. J. Alam,, S. Begum,, S. M. Moniruzzaman,, A. Umeda,, K. Amako,, M. J. Albert,, R. B. Sack,, A. Huq,, and R. R. Colwell. 1999. Association of Vibrio cholerae O1 with the cyanobacterium, Anabaena sp., elucidated by polymerase chain reaction and transmission electron microscopy. Trans. R. Soc. Trop. Med. Hyg. 93:3640.
52. Janda, J. M.,, and S. L. Abbott. 1998. Evolving concepts regarding the genus Aeromonas: an expanding panorama of species, disease presentations, and unanswered questions. Clin. Infect. Dis. 27: 332344.
53. Jay, J. M. 1996. Prevalence of Listeria spp. in meat and poultry products. Food Control 7:209214.
54. Jones, K.,, and S. B. Bradshaw. 1997. Synergism in biofilm formation between Salmonella enteritidis and a nitrogen-fixing strain of Klebsiella pneumoniae. J. Appl. Microbiol. 82:663668.
55. Kaper, J. B.,, H. Lockman,, R. R. Colwell,, and S. W. Joseph. 1981. Aeromonas hydrophila: ecology and toxigenicity of isolates from an estuary. J. Appl. Bacteriol. 50:359377.
56. Karlyshev, A. V.,, M. V. McCrossan,, and B. W. Wren. 2001. Demonstration of polysaccharide capsule in Campylobacter jejuni using electron microscopy. Infect. Immun. 69:59215924.
57. Kersters, I.,, G. Huys,, H. Van Duffel,, M. Vancanneyt,, K. Kersters,, and W. Verstraete. 1996. Survival potential of Aeromonas hydrophila in freshwaters and nutrient-poor waters in comparison with other bacteria. J. Appl. Bacteriol. 80: 26676.
58. Kersters, I.,, D. Van Der Kooij,, G. Huys,, P. Janssen,, K. Kersters,, and W. Verstraete. 1995. Influence of temperature and process technology on the occurence of Aeromonas species and hygienic indicator organisms in drinking water production plants. Microb. Ecol. 30:203218.
59. Korhonen, L. K.,, and P. J. Martikainen. 1991a. Comparison of the survival of Campylobacter jejuni and Campylobacter coli in culturable form in surface water. Can. J. Microbiol. 37:530533.
60. Korhonen, L. K.,, and P. J. Martikainen. 1991b. Survival of Escherichia coli and Campylobacter jejuni in untreated and filtered lake water. J. Appl. Bacteriol. 71:37982.
61. Kuhn, I.,, G. Allestam,, G. Huys,, P. Janssen,, K. Kersters,, K. Krovacek,, and T. A. Stenstrom. 1997. Diversity, persistence, and virulence of Aeromonas strains isolated from drinking water distribution systems in Sweden. Appl. Environ. Microbiol. 63: 27082715.
62. Kumar, C. G.,, and S. K. Anand. 1998. Significance of microbial biofilms in food industry: a review. Int. J. Food Microbiol. 42:927.
63. Kusnetsov, J. M.,, P. J. Keskitalo,, H. E. Ahonen,, A. I. Tulkki,, I. T. Miettinen,, and P. J. Martikanen. 1994. Growth of Legionella and other heterotrophic bacteria in a circulating cooling water system exposed to ultraviolet irradiation. J. Appl. Bacteriol. 77:461466.
64. Lastovica, A. J.,, and M. B. Skirrow,. 2000. Clinical significance of Campylobacter and related species other than Campylobacter jejuni and C. coli, p. 139153. In I. Nachamkin, and M. J. Blaser (ed.), Campylobacter, 2nd ed. ASM Press, Washington, D.C.
65. Leclerc, H.,, L. Schwartzbrod,, and E. Dei-Cas. 2002. Microbial agents associated with waterborne diseases. Crit. Rev. Microbiol. 28:371409.
66. Leriche, V.,, and B. Carpentier. 2000. Limitation of adhesion and growth of Listeria monocytogenes on stainless steel surfaces by Staphylococcus sciuri biofilms. J. Appl. Microbiol. 88:594605.
67. Linton, D.,, A. V. Karlyshev,, and B. W. Wren. 2001. Deciphering Campylobacter jejuni cell surface interactions from the genome sequence. Curr. Opin. Microbiol. 4:3540.
68. Lipp, E. K.,, A. Huq,, and R. R. Colwell. 2002. Effects of global climate on infectious disease: the cholera model. Clin. Microbiol. Rev. 15:757770.
69. Mallory, L. M.,, B. Austin,, and R. R. Colwell. 1977. Numerical taxonomy and ecology of oligotrophic bacteria isolated from the estuarine environment. Can. J. Microbiol. 23:733750.
70. Marras, T. K.,, and C. L. Daley. 2002. Epidemiology of human pulmonary infection with nontuberculous mycobacteria. Clin. Chest Med. 23:553567.
71. Martinez, A.,, S. Torello,, and R. Kolter. 1999. Sliding motility in mycobacteria. J. Bacteriol. 181: 73317338.
72. Mary, P.,, G. Buchet,, C. Defives,, and J. P. Hornez. 2001. Growth and survival of clinical vs. environmental species of Aeromonas in tap water. Int. J. Food Microbiol. 69:191198.
73. Merino, S.,, R. Gavin,, M. Altarriba,, L. Izquierdo,, M. E. Maguire,, and J. M. Tomas. 2001. The MgtE Mg2+ transport protein is involved in Aeromonas hydrophila adherence. FEMS Microbiol. Lett. 198:189195.
74. Merino, S.,, X. Rubires,, A. Aguilar,, and J. M. Tomas. 1997. The role of flagella and motility in the adherence and invasion to fish cell lines by Aeromonas hydrophila serogroup O:34 strains. FEMS Microbiol. Lett. 151:213217.
75. Mizunoe, Y.,, S. N. Wai,, A. Takade,, and S.-I. Yoshida. 1999. Isolation and characterization of rugose form of Vibrio cholerae O139 strain MO10. Infect. Immun. 67:958963.
76. Morgan, D. R.,, P. C. Johnson,, H. L. DuPont,, T. K. Satterwhite,, and L. V. Wood. 1985. Lack of correlation between known virulence properties of Aeromonas hydrophila and enteropathogenicity for humans. Infect. Immun. 50:6265.
77. Morris, J. G.,, M. B. Sztein,, E. W. Rice,, J. P. Nataro,, and G. A. Losonsky. 1996. Vibrio cholera O1 can assume a chlorine resistant rugoose survival form that is virulent for humans. J. Infect. Dis. 174:13641368.
78. Murga, R.,, T. S. Forster,, E. Brown,, J. M. Pruckler,, B. S. Fields,, and R. M. Donlan. 2001. Role of biofilms in the survival of Legionella pneumophila in a model potable-water system. Microbiology 147:31213126.
79. National Center for Infectious Diseases. 2000. Surveillance for Foodborne Disease Outbreaks: United States, 1993-1997. Centers for Disease Control, Atlanta, Ga.
80. Norwood, D. E.,, and A. Gilmour. 2001. The differential adherence capabilities of two Listeria monocytogenes strains in monoculture and multispecies biofilms as a function of temperature. Lett. Appl. Microbiol. 33:320324.
81. Olson, B. H.,, and L. A. Nagy. 1984. Microbiology of potable water. Adv. Appl. Microbiol. 30:73132.
82. Palmer, C. J.,, G. F. Bonilla,, B. Roll,, C. Paszko-Kolva,, L. R. Sangermano,, and R. S. Fujioka. 1995. Detection of Legionella species in reclaimed water and air with the EnviroAmp Legionella PCR kit and direct fluorescent antibody staining. Appl. Environ. Microbiol. 61:407412.
83. Palmer, C. J.,, Y. L. Tsai,, C. Paszko-Kolva,, C. Mayer,, and L. R. Sangermano. 1993. Detection of Legionella species in sewage and ocean water by polymerase chain reaction, direct fluorescent-antibody, and plate culture methods. Appl. Environ. Microbiol. 59:36183624.
84. Park, S. R.,, W. G. Mackay,, and D. C. Reid. 2001. Helicobacter sp. recovered from drinking water biofilm sampled from a water distribution system. Water Res. 35:16241626.
85. Parkhill, J.,, B. W. Wren,, K. Mungall,, J. M. Ketley,, C. Churcher,, D. Basham,, T. Chillingworth,, R. M. Davies,, T. Feltwell,, S. Holroyd,, K. Jagels,, A. V. Karlyshev,, S. Moule,, M. J. Pallen,, C. W. Penn,, M. A. Quail,, M. A. Rajandream,, K. M. Rutherford,, A. H. van Vliet,, S. Whitehead,, and B. G. Barrell. 2000. The genome sequence of the foodborne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665668.
86. Pedro-Botet, M. L.,, J. E. Stout,, and V. L. Yu. 2002. Legionnaires’ disease contracted from patient homes: the coming of the third plague? Eur. J. Clin. Microbiol. Infect. Dis. 21:699705.
87. Percival, S.,, J. Walker,, and P. Hunter. 2000. Microbes and public health significance, p. 105141. Microbiological Aspects of Biofilms and Drinking Water. CRC Press, Boca Raton, Fla.
88. Recht, J.,, and R. Kolter. 2001. Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J. Bacteriol. 183:57185724.
89. Recht, J.,, A. Martinez,, S. Torello,, and R. Kolter. 2000. Genetic analysis of sliding motility in Mycobacterium smegmatis. J. Bacteriol. 182:43484351.
90. Riffard, S.,, S. Douglass,, T. Brooks,, S. Springthorpe,, L. G. Filion,, and S. A. Sattar. 2001. Occurrence of Legionella in groundwater: an ecological study. Water Sci. Technol. 43:99102.
91. Rocourt, J. 1996. Taxonomy of the Listeria genus and typing of L. monocytogenes. Pathol. Biol. 44: 749756.
92. Rocourt, J.,, P. BenEmbarek,, H. Toyofuku,, and J. Schlundt. 2003. Quantitative risk assessment of Listeria monocytogenes in ready-to-eat foods: the FAO/WHO approach. FEMS Immunol. Med. Microbiol. 35:263267.
93. Rogers, J.,, A. B. Dowsett,, P. J. Dennis,, J. V. Lee,, and C. W. Keevil. 1994. Influence of temperature and plumbing material selection on biofilm formation and growth of Legionella pneumophila in a model potable water system containing complex microbial flora. Appl. Environ. Microbiol. 60:15851592.
94. Romling, U. 2001. Genetic and phenotypic analysis of multicellular behavior in Salmonella typhimurium. Methods Enzymol. 336:4859.
95. Romling, U.,, Z. Bian,, M. Hammar,, W. D. Sierralta,, and S. Normark. 1998a. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180:722731.
96. Romling, U.,, and M. Rohde. 1999. Flagella modulate the multicellular behavior of Salmonella typhimurium on the community level. FEMS Microbiol.Lett. 180:91102.
97. Romling, U.,, M. Rohde,, A. Olsen,, S. Normark,, and J. Reinkoster. 2000. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol. Microbiol. 36:1023.
98. Romling, U.,, W. D. Sierralta,, K. Eriksson,, and S. Normark. 1998b. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol. Microbiol. 28:249264.
99. Rusin, P. A.,, J. B. Rose,, C. N. Haas,, and C. P. Gerba. 1997. Risk assessment of opportunistic bacterial pathogens in drinking water. Rev. Environ. Contam. Toxicol. 152:5783.
100. Salvat, G.,, M. T. Toquin,, Y. Michel,, and P. Colin. 1995. Control of Listeria monocytogenes in the delicatessen industries: the lessons of a listeriosis outbreak in France. Int. J. Food Microbiol. 25: 7581.
101. Schulze-Robbecke, R.,, C. Feldmann,, R. Fischeder,, B. Janning,, M. Exner,, and G. Wahl. 1995. Dental units: an environmental study of sources of potentially pathogenic mycobacteria. Tuber. Lung Dis. 76:318323.
102. Schulze-Robbecke, R.,, B. Janning,, and R. Fischeder. 1992. Occurrence of mycobacteria in biofilm samples. Tuber. Lung Dis. 73:141144.
103. Skirrow, M.,, and M. Blaser,. 1992. Clinical and epidemiological considerations. In I. Nachamkin, , M. Blaser, , and L. Tomkins (ed.), Camylobacter jejuni, Current Status and Future Trends. American Society for Microbiology, Washington, D.C.
104. Smith, D. L.,, A. D. Harris,, J. A. Johnson,, E. K. Silbergeld, , and J. G. Morris, Jr. 2002. Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc. Natl. Acad. Sci. USA 99:64346439.
105. Solano, C.,, B. Garcia,, J. Valle,, C. Berasain,, J. M. Ghigo,, C. Gamazo,, and I. Lasa. 2002. Genetic analysis of Salmonella enteritidis biofilm formation: critical role of cellulose. Mol. Microbiol. 43: 793808.
106. Stanley, K.,, R. Cunningham,, and K. Jones. 1998. Isolation of Campylobacter jejuni from groundwater. J. Appl. Microbiol. 85:187191.
107. Stark, R. M.,, G. J. Gerwig,, R. S. Pitman,, L. F. Potts,, N. A. Williams,, J. Greenman,, I. P. Weinzweig,, T. R. Hirst,, and M. R. Millar. 1999. Biofilm formation by Helicobacter pylori. Lett. Appl. Microbiol. 28:121126.
108. Stewart, P. S. 2002. Mechanisms of antibiotic resistance in bacterial biofilms. Int. J. Med. Microbiol. 292:107113.
109. Stone, B. J.,, and Y. A. Kwaik. 1998. Expression of multiple pili by Legionella pneumophila: identification and characterization of a type IV pilin gene and its role in adherence to mammalian and protozoan cells. Infect. Immun. 66:17681775.
110. Stoodley, P.,, S. Wilson,, L. Hall-Stoodley,, J. D. Boyle,, H. M. Lappin-Scott,, and J. W. Costerton. 2001. Growth and detachment of cell clusters from mature mixed-species biofilms. Appl. Environ. Microbiol. 67:56085613.
111. Stout, J. E.,, and V. L. Yu. 1997. Legionellosis. N. Engl. J. Med. 337:682687.
112. Surman, S.,, L. Morton,, A. Skinner,, R. Fitzgeorge,, and C. Keevil,. 1997. Growth of Legionella pneumophila is not dependent on intracellular replication. In C. W. Keevil, , A. Godfree, , D. Holt, , and C. Dow (ed.) , Biofilms in the Aquatic Environment. Royal Society of Chemistry, Cambridge, United Kingdom.
113. Szewzyk, U.,, R. Szewzyk,, W. Manz,, and K. H. Schleifer. 2000. Microbiological safety of drinking water. Annu. Rev. Microbiol. 54:81127.
114. Tamplin, M. L.,, A. L. Gauzens,, A. Huq,, D. A. Sack,, and R. R. Colwell. 1990. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl. Environ. Microbiol. 56:19771980.
115. Thornley, J. P.,, J. G. Shaw,, I. Gryllos,, and A. Eley. 1997. Virulence properties of clinically significant Aeromonas species. Rev. Med. Microbiol. 43: 6172.
116. Trachoo, N.,, and J. F. Frank. 2002. Effectiveness of chemical sanitizers against Campylobacter jejunicontaining biofilms. J. Food Prot. 65:11171121.
117. Trachoo, N.,, J. F. Frank,, and N. J. Stern. 2002. Survival of Campylobacter jejuni in biofilms isolated from chicken houses. J. Food. Prot. 65:11101116.
118. Tsai, G. J.,, F. C. Tsai,, and Z. L. Kong. 1997. Effects of temperature, medium composition, pH, salt and dissolved oxygen on haemolysin and cytotoxin production by Aeromonas hydrophila isolated from oyster. Int. J. Food Microbiol. 38:111116.
119. Turnock, L. L.,, E. B. Somers,, N. G. Faith,, C. J. Czuprynski,, and W. A. Lee. 2002. The effects of prior growth as a biofilm on the virulence of Salmonella typhimurium for mice. Comp. Immunol. Microbiol. Infect. Dis. 25:4348.
120. Tyndall, R. L., , R. E. Hand, Jr.,, R. C. Mann, , C. Evans, , and R. Jernigan. 1985. Application of flow cytometry to detection and characterization of Legionella spp. Appl. Environ. Microbiol. 49:852857.
121. U.S. Food and Drug Administration. 1992 . Foodborne Pathogenic Microorganisms and Natural Toxins Handbook: Salmonella. [Online.] U.S. Food and Drug Administration, Washington, D.C. http://www.cfsan.fda.gov/~mow/chap1.html.
122. Vance, R. E.,, J. Zhu,, and J. J. Mekalanos. 2003. A constitutively active variant of the quorumsensing regulator LuxO affects protease production and biofilm formation in Vibrio cholerae. Infect. Immun. 71:25712576.
123. Vatanyoopaisarn, S.,, A. Nazli,, C. E. R. Dodd,, C. E. D. Rees,, and W. M. Waites. 2000. Effect of flagella on initial attachment of Listeria monocytogenes to stainless steel. Appl. Environ. Microbiol. 66: 860863.
124. von Reyn, C.,, R. Waddell,, T. Eaton,, R. Arbeit,, J. Maslow,, T. Barber,, R. Brindle,, C. Gilks,, J. Lumio,, and J. Lahdevirta. 1993. Isolation of Mycobacterium avium complex from water in the United States, Finland, Zaire, and Kenya. J. Clin. Microbiol. 31:32273230.
125. von Reyn, C. F.,, J. N. Maslow,, T. W. Barber, , J. O. Falkinham, III,, and R. D. Arbeit. 1994. Persistent colonisation of potable water as a source of Mycobacterium avium infection in AIDS. Lancet 343:11371141.
126. Wadowsky, R. M.,, and R. B. Yee. 1985. Effect of non-Legionellaceae bacteria on the multiplication of Legionella pneumophila in potable water. Appl. Environ. Microbiol. 49:12061210.
127. Walker, S. J.,, P. Archer,, and J. G. Banks. 1990. Growth of Listeria monocytogenes at refrigeration temperatures. J. Appl. Bacteriol. 68:157162.
128. Wallace, R. J., Jr.,, J. M. Musser, , S. I. Hull, , V. A. Silcox, , L. C. Steele, , G. D. Forrester, , A. Labidi, , and R. K. Selander. 1989. Diversity and sources of rapidly growing mycobacteria associated with infections following cardiac surgery. J. Infect. Dis. 159:708716.
129. Watnick, P. I.,, and R. Kolter. 1999. Steps in the development of a Vibrio cholerae El Tor biofilm. Mol. Microbiol. 34:586595.
130. Watnick, P. I., , C. M. Lauriano, , K. E. Klose, , L. Croal, , and R. Kolter. 2001. The absence of a flagellum leads to altered colony morphology, biofilm development and virulence in Vibrio cholerae O139. Mol. Microbiol. 39:223235.
131. Whiteley, M.,, E. Brown,, and R. J. C. McLean. 1997. An inexpensive chemostat apparatus for the study of microbial biofilms. J. Microbiol. Methods 30:125132.
132. Williams, J. F.,, J. A. Molinari,, and N. Andrews. 1996. Microbial contamination of dental unit waterlines: origins and characteristics. Compend. Contin. Educ. Dent. 17:538540.
133. Wuertz, S.,, R. Spaeth,, A. Hinderberger,, T. Griebe,, H. C. Flemming,, and P. A. Wilderer. 2001. A new method for extraction of extracellular polymeric substances from biofilms and activated sludge suitable for direct quantification of sorbed metals. Water Sci. Technol. 43:2531.
134. Yildiz, F. H.,, N. A. Dolganov,, and G. K. Schoolnik. 2001. VpsR, a member of the response regulators of the two-component regulatory systems, is required for expression of vps biosynthesis genes and EPS(ETr)-associated phenotypes in Vibrio cholerae O1 El Tor. J. Bacteriol. 183:17161726.
135. Yildiz, F. H.,, and G. K. Schoolnik. 1999. Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc. Natl. Acad. Sci. USA 96: 40284033.
136. Zacheus, O. M.,, and P. J. Martikainen. 1994. Occurence of Legionella in hot water distribution systems of Finnish apartment buildings. Can. J. Microbiol. 40:993999.
137. Zhu, J.,, M. B. Miller,, R. E. Vance,, M. Dziejman,, B. L. Bassler,, and J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:31293134.
138. Zogaj, X.,, M. Nimtz,, M. Rohde,, W. Bokranz,, and U. Romling. 2001. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol. Microbiol. 39:14521463.

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