Anaerobes in Biofilm-Based Healthcare-Associated Infections

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 830)


Anaerobic bacteria can cause an infection when they encounter a permissive environment within the host. These opportunistic pathogens are seldom recovered as single isolates but more frequently are involved in polymicrobial infections, together with other anaerobes or aerobes. Nowadays it’s known that some anaerobic bacteria are also able to grow as biofilm even if this feature and its role in the healthcare-associated infections (HAIs) are still poorly characterized. As consequence, the involvement of biofilm-forming anaerobic bacteria in infections related to healthcare procedures, including surgery and medical devices implantation, is underestimated.

The current knowledge on the role of biofilm-growing anaerobes in HAIs has been here reviewed, with particular reference to respiratory, intestinal, intra-abdominal, wound, and urogenital tract infections. Even if the data are still scarce, the ability to form biofilm of opportunistic anaerobic species and their possible role as causative agents of HAIs should alert even more clinicians and microbiologists on the need to search for anaerobes in clinical samples when their presence can be reasonably assumed.


Anaerobic Bacterium Clostridium Difficile Infection Prosthetic Joint Infection Polymicrobial Infection Anaerobic Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are indebted to Dr Paola Mastrantonio, Dr. Patrizia Spigaglia, Dr. Fabrizio Barbanti and Dr. Rita Cardines from the Istituto Superiore di Sanità, Rome, for their advices in cultivation, isolation and identification of anaerobes in clinical samples. The generous gift of Propionibacterium acnes clinical isolates by Professor Anna Maria Cuffini, University of Turin, is also gratefully acknowledged.


  1. Agbaht K, Diaz E, Munoz E et al (2007) Bacteremia in patients with ventilator-associated pneumonia is associated with increased mortality: a study comparing bacteremic vs. nonbacteremic ventilator-associated pneumonia. Crit Care Med 35:2064–2070PubMedGoogle Scholar
  2. Alberti C, Brun-Buisson C, Burchardi H et al (2002) Epidemiology of sepsis and infection in ICU patients from an international multicentre cohort study. Intensive Care Med 28:108–121PubMedGoogle Scholar
  3. Alling B, Brandberg A, Seeberg S et al (1973) Aerobic and anaerobic microbial flora in the urinary tract of geriatric patients during long-term care. J Infect Dis 127:34–39PubMedGoogle Scholar
  4. American Thoracic Society, Infectious Diseases Society of America (2005) Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am J Respir Crit Care Med 171:388–416Google Scholar
  5. Bahrani-Mougeot FK, Paster BJ, Coleman S et al (2007) Molecular analysis of oral and respiratory bacterial species associated with ventilator-associated pneumonia. J Clin Microbiol 45:1588–1593PubMedCentralPubMedGoogle Scholar
  6. Bansal C, Scott R, Stewart D et al (2005) Decubitus ulcers: a review of the literature. Int J Dermatol 44:805PubMedGoogle Scholar
  7. Bartlett JG (2012) Anaerobic bacterial infection of the lung. Anaerobe 18:235–239PubMedGoogle Scholar
  8. Bauer TT, Torres A, Ferrer R et al (2002) Biofilm formation in endotracheal tubes. Association between pneumonia and the persistence of pathogens. Monaldi Arch Chest Dis 57:84–87PubMedGoogle Scholar
  9. Bayston R, Ashraf W, Barker-Davies R et al (2007) Biofilm formation by Propionibacterium acnes on biomaterials in vitro and in vivo: impact on diagnosis and treatment. J Biomed Mater Res A 81:705–709PubMedGoogle Scholar
  10. Blango MG, Mulvey MA (2010) Persistence of uropathogenic Escherichia coli in the face of multiple antibiotics. Antimicrob Agents Chemother 54:1855–1863PubMedCentralPubMedGoogle Scholar
  11. Bowler PG, Duerden BI, Armstrong DG (2001) Wound microbiology and associated approaches to wound management. Clin Microbiol Rev 14(2):244–269PubMedCentralPubMedGoogle Scholar
  12. Brant CQ, Silva Júnior MR, Siqueira ES et al (1996) Biliary and pancreatic stent blockage by bacterial biofilm: presentation of two cases. Braz J Med Biol Res 29:1455–1459PubMedGoogle Scholar
  13. Brazier JS (2006) Human infections with Fusobacterium necrophorum. Anaerobe 12:165–172PubMedGoogle Scholar
  14. Brook I (2002) Microbiology of polymicrobial abscesses and implications for therapy. J Antimicrob Chemother 50:805–810PubMedGoogle Scholar
  15. Brook I (2004a) Role of anaerobic bacteria in infections following tracheostomy, intubation, or the use of ventilatory tubes in children. Ann Otol Rhinol Laryngol 113:830–834PubMedGoogle Scholar
  16. Brook I (2004b) Urinary tract and genito-urinary suppurative infections due to anaerobic bacteria. Int J Urol 11:133–134PubMedGoogle Scholar
  17. Brook I (2008) Microbiology and management of abdominal infections. Dig Dis Sci 53:2585–2591PubMedGoogle Scholar
  18. Brook I, Frazier EH (1993) Significant recovery of non sporulating anaerobic rods from clinical specimens. Clin Infect Dis 16:476–480PubMedGoogle Scholar
  19. Brook I, Frazier EH (2000) Aerobic and anaerobic microbiology in intra abdominal infections associated with diverticulitis. J Med Microbiol 49:827–830PubMedGoogle Scholar
  20. Brook I, Myhal LA, Dorsey HC (1991) Encapsulation and pilus formation of Bacteroides sp. J Infect 25:251–257Google Scholar
  21. Brook I, Wexler HM, Goldstein EJ (2013) Antianaerobic antimicrobials: spectrum and susceptibility testing. Clin Microbiol Rev 26:526–546PubMedCentralPubMedGoogle Scholar
  22. Cairns S, Thomas JG, Hooper SJ et al (2011) Molecular analysis of microbial communities in endotracheal tube biofilms. PLoS One 6:e14759PubMedCentralPubMedGoogle Scholar
  23. Castillo AA, Lew SQ, Smith AM et al (1999) Peritoneal dialysis-associated peritonitis caused by Propioni-bacteria species. Am J Kidney Dis 33:E6Google Scholar
  24. Cek M, Tandoğdu Z, Wagenlehner F, et al. (2014) Healthcare-associated urinary tract infections in hospitalized urological patients – a global perspective: results from the GPIU studies 2003–2010. World J Urol 23 Jan 2014. [Epub ahead of print]Google Scholar
  25. Chao CT, Lee SY, Yang WS et al (2013) Peritoneal dialysis peritonitis by anaerobic pathogens: a retrospective case series. BMC Nephrol 14:111PubMedCentralPubMedGoogle Scholar
  26. Chenoweth CE, Saint S (2011) Urinary tract infections. Infect Dis Clin North Am 25:103–115PubMedGoogle Scholar
  27. Chlebicki MP, Safdar N (2008) Topical chlorhexidine for prevention of ventilator-associated pneumonia: a meta-analysis. Crit Care Med 35:595–602Google Scholar
  28. Choudhuri AH (2013) Ventilator-associated pneumonia: when to hold the breath? Int J Crit Illn Inj Sci 3:169–174PubMedCentralPubMedGoogle Scholar
  29. Chroneou A, Zias N, Beamis JF Jr et al (2007) Healthcare-associated pneumonia: principles and emerging concepts on management. Expert Opin Pharmacother 8:3117–3131PubMedGoogle Scholar
  30. Cobo J, Del Pozo JL (2011) Prosthetic joint infection: diagnosis and management. Expert Rev Anti Infect Ther 9:787–802PubMedGoogle Scholar
  31. Coenye T, Peeters E, Nelis HJ (2007) Biofilm formation by Propionibacterium acnes is associated with increased resistance to antimicrobial agents and increased production of putative virulence factors. Res Microbiol 158:386–392PubMedGoogle Scholar
  32. Costerton JW (2002) Anaerobic biofilm infections in cystic fibrosis. Mol Cell 10:699–700PubMedGoogle Scholar
  33. Dapa T, Unnikrishnan M (2013) Biofilm formation by Clostridium difficile. Gut Microbes 25:4Google Scholar
  34. Ðapa T, Leuzzi R, Ng YK et al (2013) Multiple factors modulate biofilm formation by the anaerobic pathogen Clostridium difficile. J Bacteriol 195:545–555PubMedCentralPubMedGoogle Scholar
  35. Dasgupta MK (2002) Biofilms and infection in dialysis patients. Semin Dial 15:338–346PubMedGoogle Scholar
  36. Dasgupta MK, Larabie M (2001) Biofilms in peritoneal dialysis. Perit Dial Int 21:S213–S217PubMedGoogle Scholar
  37. Dawson LF, Valiente E, Faulds-Pain A et al (2012) Characterisation of Clostridium difficile biofilm formation, a role for Spo0A. PLoS One 7:e50527PubMedCentralPubMedGoogle Scholar
  38. Del Pozo JL, Patel R (2009) Clinical practice. Infection associated with prosthetic joints. N Engl J Med 361:787–794PubMedCentralPubMedGoogle Scholar
  39. Dempsey KE, Riggio MP, Lennon A et al (2007) Identification of bacteria on the surface of clinically infected and non-infected prosthetic hip joints removed during revision arthroplasties by 16S rRNA gene sequencing and by microbiological culture. Arthritis Res Ther 9:R46PubMedCentralPubMedGoogle Scholar
  40. Donelli G (2006) Vascular catheter-related infection and sepsis. Surg Infect 7:25–27Google Scholar
  41. Donelli G, Vuotto C (2014) Biofilm-based infections in long-term care facilities. Future Microbiol 9:175–188PubMedGoogle Scholar
  42. Donelli G, Guaglianone E, Di Rosa R et al (2007) Plastic biliary stent occlusion: factors involved and possible preventive approaches. Clin Med Res 5:53–60PubMedCentralPubMedGoogle Scholar
  43. Donelli G, Vuotto C, Cardines R et al (2012) Biofilm-growing intestinal anaerobic bacteria. FEMS Immunol Med Microbiol 65:318–325PubMedGoogle Scholar
  44. Donskey CJ, Chowdhry TK, Hecker MT et al (2000) Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients. N Engl J Med 343:1925–1932PubMedGoogle Scholar
  45. Dowd SE, Sun Y, Secor PR et al (2008) Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 8:43PubMedCentralPubMedGoogle Scholar
  46. Dryden MS (2010) Complicated skin and soft tissue infection. J Antimicrob Chemother 65:iii35–44PubMedGoogle Scholar
  47. Ebright JR (2005) Microbiology of chronic leg and pressure ulcers: clinical significance and implications for treatment. Nurs Clin North Am 40:207–216PubMedGoogle Scholar
  48. Edmiston CE Jr, Krepel CJ, Marks RM et al (2013) Microbiology of explanted suture segments from infected and non infected surgical patients. J Clin Microbiol 51:417–421PubMedCentralPubMedGoogle Scholar
  49. Edwards R, Harding KG (2004) Bacteria and wound healing. Curr Opin Infect Dis 17:91–96PubMedGoogle Scholar
  50. Ferrara AM (2006) Potentially multidrug-resistant non-fermentative Gram-negative pathogens causing nosocomial pneumonia. Int J Antimicrob Agents 27:183–195PubMedGoogle Scholar
  51. Finegold SM (1995a) Anaerobic infections in humans. Anaerobe 1:3–9PubMedGoogle Scholar
  52. Finegold SM (1995b) Overview of clinically important anaerobes. Clin Infect Dis 20:S205–S207Google Scholar
  53. Frank DN, Wilson SS, St Amand AL et al (2009) Culture-independent microbiological analysis of foley urinary catheter biofilms. PLoS One 4:e7811PubMedCentralPubMedGoogle Scholar
  54. García-López L, Fernández-Reyes LMJ, Criado-Illana MT et al (2012) Intraperitoneal administration of daptomycin in recurrent peritonitis with suspected biofilm. Nefrologia 32:139–142PubMedGoogle Scholar
  55. Genuit T, Bochicchio G, Napolitano LM et al (2001) Prophylactic chlorhexidine oral rinse decreases ventilator-associated pneumonia in surgical ICU patients. Surg Infect 2:5–18Google Scholar
  56. Gerding DN (1995) Foot infections in diabetic patients: the role of anaerobes. Clin Infect Dis 20(Suppl 2): 283–288Google Scholar
  57. Goldstein EJC, Snydman DR (2004) Intra-abdominal infections: review of the bacteriology, antimicrobial susceptibility and the role of ertapenem in their therapy. J Antimicrob Chemother 53:ii29–36PubMedGoogle Scholar
  58. Gorman SP, Adair CG, Mawhinney WM (1994) Incidence and nature of peritoneal catheter biofilm determined by electron and confocal laser scanning microscopy. Epidemiol Infect 112:551–559PubMedCentralPubMedGoogle Scholar
  59. Gould D (2013) Healthcare-associated respiratory tract infection. Nurs Stand 27:49–56PubMedGoogle Scholar
  60. Guaglianone E, Cardines R, Vuotto C et al (2010) Microbial biofilms associated with biliary stent clogging. FEMS Immunol Med Microbiol 59:410–420PubMedGoogle Scholar
  61. Guembe M, Martín-Rabadán P, Echenagusia A et al (2012) How should long-term tunneled central venous catheters be managed in microbiology laboratories in order to provide an accurate diagnosis of colonization? J Clin Microbiol 50:1003–1007PubMedCentralPubMedGoogle Scholar
  62. Han A, Zenilman JM, Melendez JH et al (2011) The importance of a multifaceted approach to characterizing the microbial flora of chronic wounds. Wound Repair Regen 19:532–541PubMedCentralPubMedGoogle Scholar
  63. Hanlon GW, Denyer SP, Hodges NA et al (2004) Biofilm formation and changes in bacterial cell surface hydrophobicity during growth in a CAPD model system. J Pharm Pharmacol 56:847–854PubMedGoogle Scholar
  64. Haslett TM, Isenberg HD, Hilton E et al (1988) Microbiology of indwelling central intravascular catheters. J Clin Microbiol 26:696–701PubMedCentralPubMedGoogle Scholar
  65. Hoffman BJ, Cunningham JT, Marsh WH et al (1994) An in vitro comparison of biofilm formation on various biliary stent materials. Gastrointest Endosc 40:581–583PubMedGoogle Scholar
  66. Hofstad T (1989) Virulence determinants in non-spore-forming anaerobic bacteria. Scand J Infect Dis 62:15–24Google Scholar
  67. Høgdall D, Hvolris JJ, Christensen L (2010) Improved detection methods for infected hip joint prostheses. APMIS 118:815–823PubMedGoogle Scholar
  68. Holmberg A, Lood R, Mörgelin M et al (2009) Biofilm formation by Propionibacterium acnes is a characteristic of invasive isolates. Clin Microbiol Infect 15:787–795PubMedGoogle Scholar
  69. Imirzalioglu C, Hain T, Chakraborty T et al (2008) Hidden pathogens uncovered: metagenomic analysis of urinary tract infections. Andrologia 40:66–71PubMedGoogle Scholar
  70. Jamal WY, Shahin M, Rotimi VO (2013) Comparison of two matrix-assisted laser desorption/ionization-time of flight (MALDI-TOF) mass spectrometry methods and API 20AN for identification of clinically relevant anaerobic bacteria. J Med Microbiol 62:540–544PubMedGoogle Scholar
  71. James GA, Swogger E, Wolcott R et al (2008) Biofilms in chronic wounds. Wound Repair Regen 16:37–44PubMedGoogle Scholar
  72. Jämsen E, Huhtala H, Puolakka T et al (2009) Risk factors for infection after knee arthroplasty: a register-based analysis of 43,149 cases. J Bone Joint Surg Am 91:38–47PubMedGoogle Scholar
  73. Jansen B, Goodman LP, Ruiten D (1993) Bacterial adherence to hydrophilic polymer-coated polyurethane stents. Gastrointest Endosc 39:670–673PubMedGoogle Scholar
  74. Japanese Society of Chemotherapy Committee on guidelines for treatment of anaerobic infections, Japanese Association for Anaerobic Infection Research (2011) Chapter 2-1. Anaerobic infections (individual fields): respiratory infections. J Infect Chemother 17:42–46Google Scholar
  75. Kathju S, Nistico L, Hall-Stoodley L et al (2009) Chronic surgical site infection due to suture-associated polymicrobial biofilm. Surg Infect (Larchmt) 10:457–461Google Scholar
  76. Kiernan M (2012) Reducing the risk surgical site infection. Nurs Times 108:12–14PubMedGoogle Scholar
  77. Knight CL, Surawicz CM (2013) Clostridium difficile infection. Med Clin North Am 97:523–536PubMedGoogle Scholar
  78. Koerner RJ (1997) Contribution of endotracheal tubes to the pathogenesis of ventilator-associated pneumonia. J Hosp Infect 35:83–89PubMedGoogle Scholar
  79. Kolenbrander PE, Palmer RJ Jr, Periasamy S et al (2010) Oral multispecies biofilm development and the key role of cell–cell distance. Nat Rev Microbiol 8:471–480PubMedGoogle Scholar
  80. La Scola B, Fournier PE, Raoult D (2011) Burden of emerging anaerobes in the MALDI-TOF and 16S rRNA gene sequencing era. Anaerobe 17:106–112PubMedGoogle Scholar
  81. Lazzarini L, Conti E, Ditri L et al (2004) Clostridial orthopedic infections: case reports and review of the literature. J Chemother 16:94–97PubMedGoogle Scholar
  82. Leung JW, Liu YL, Desta T et al (1998) Is there a synergistic effect between mixed bacterial infection in biofilm formation on biliary stents? Gastrointest Endosc 48:250–257PubMedGoogle Scholar
  83. Leung JW, Liu Y, Chan RC et al (2000) Early attachment of anaerobic bacteria may play an important role in biliary stent blockage. Gastrointest Endosc 52:725–729PubMedGoogle Scholar
  84. Levy PY, Fenollar F, Stein A et al (2008) Propionibacterium acnes postoperative shoulder arthritis: an emerging clinical entity. Clin Infect Dis 46:1884–1886PubMedGoogle Scholar
  85. Lo Vecchio A, Zacur GM (2012) Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options. Curr Opin Gastroenterol 28:1–9PubMedGoogle Scholar
  86. Luna CM, Sibila O, Agusti C et al (2009) Animal models of ventilator-associated pneumonia. Eur Respir J 33:182–188PubMedGoogle Scholar
  87. Lutz MF, Berthelot P, Fresard A et al (2005) Arthroplastic and osteosynthetic infections due to Propionibacterium acnes: a retrospective study of 52 cases, 1995–2002. Eur J Clin Microbiol Infect Dis 24:739–744PubMedGoogle Scholar
  88. Macfarlane S, Dillon JF (2007) Microbial biofilms in the human gastrointestinal tract. J Appl Microbiol 102:1187–1196PubMedGoogle Scholar
  89. Macfarlane S, Macfarlane GT (2006) Composition and metabolic activities of bacterial biofilms colonizing food residues in the human gut. Appl Environ Microbiol 72:6204–6211PubMedCentralPubMedGoogle Scholar
  90. Macfarlane S, Bahrami B, Macfarlane GT (2011) Mucosal biofilm communities in the human intestinal tract. Adv Appl Microbiol 75:111–143PubMedGoogle Scholar
  91. Macfarlane S, Woodmansey EJ, Macfarlane GT (2005) Colonization of mucin by human intestinal bacteria and establishment of biofilm communities in a two-stage continuous culture system. Appl Environ Microbiol 71(11):7483–7492PubMedCentralPubMedGoogle Scholar
  92. Mangram AJ, Horan TC, Pearson ML et al (1999) Guideline for prevention of surgical site infection, 1999. Centers for Disease Control and Prevention (CDC) Hospital Infection Control Practices Advisory Committee. Am J Infect Control 27:97–132PubMedGoogle Scholar
  93. Marik PE, Careau P (1999) The role of anaerobes in patients with ventilator-associated pneumonia and aspiration pneumonia: a prospective study. Chest 115:178–183PubMedGoogle Scholar
  94. Marsh PD (2004) Dental plaque as a microbial biofilm. Caries Res 38:204–211PubMedGoogle Scholar
  95. Marshall JC (2004) Intra-abdominal infections. Microbes Infect 6:1015–1025PubMedGoogle Scholar
  96. Martín-Rabadán P, Gijón P, Alcalá L et al (2008) Propionibacterium acnes is a common colonizer of intravascular catheters. J Infect 56:257–260PubMedGoogle Scholar
  97. Martins M, Rodrigues A, Pedrosa JM et al (2013) Update on the challenging role of biofilms in peritoneal dialysis. Biofouling 29:1015–1027PubMedGoogle Scholar
  98. Mastrantonio P, Pantosti A, Cerquetti M, Fiorentini C, Donelli G (1996) Clostridium difficile: an update on virulence mechanisms. Anaerobe 2:337–343PubMedGoogle Scholar
  99. Mazuski JE, Solomkin JS (2009) Intra-abdominal infections. Surg Clin North Am 89:421–437PubMedGoogle Scholar
  100. McAllister EW, Carey LC, Brady PG et al (1993) The role of polymeric surface smoothness of biliary stents in bacterial adherence, biofilm deposition, and stent occlusion. Gastrointest Endosc 39:422–425PubMedGoogle Scholar
  101. McCarthy J, Stingemore N (1999) Clostridium difficile infection of a prosthetic joint presenting 12 months after antibiotic-associated diarrhoea. J Infect 39:94–96PubMedGoogle Scholar
  102. McDowell A, Patrick S (2005) Evaluation of nonculture methods for the detection of prosthetic hip biofilms. Clin Orthop Relat Res 437:74–82PubMedGoogle Scholar
  103. Mermel LA, Farr BM, Sherertz RJ et al (2001) Guidelines for the management of intravascular catheter-related infections. Clin Infect Dis 32:1249–1272PubMedGoogle Scholar
  104. Mikamo H, Arakawa S, Fujiwara M et al (2011) Chapter 1-1. Anaerobic infections (General): epidemiology of anaerobic infections. J Infect Chemother 17:4–12Google Scholar
  105. Murphy EC, Frick IM (2013) Gram-positive anaerobic cocci – commensals and opportunistic pathogens. FEMS Microbiol Rev 37:520–553PubMedGoogle Scholar
  106. Nagy E (2010) Anaerobic infections: update on treatment considerations. Drugs 70:841–858PubMedGoogle Scholar
  107. National Collaborating Centre for Women’s and Children’s Health (2008) Surgical site infection: prevention and treatment of surgical site infection. Clinical guideline. RCOG Press, LondonGoogle Scholar
  108. Nessim SJ, Nisenbaum R, Bargman JM et al (2012) Microbiology of peritonitis in peritoneal dialysis patients with multiple episodes. Perit Dial Int 32:316–321PubMedCentralPubMedGoogle Scholar
  109. Nichols RL, Florman S (2001) Clinical presentations of soft-tissue infections and surgical site infections. Clin Infect Dis 33:84–93Google Scholar
  110. O’Grady NP, Alexander M, Dellinger EP et al (2002) Guidelines for the prevention of intravascular catheter-related infections. Centers for disease control and prevention. MMWR Recomm Rep 51:1–29PubMedGoogle Scholar
  111. Passerini L, Lam K, Costerton JW et al (1992) Biofilms on indwelling vascular catheters. Crit Care Med 20:665–673PubMedGoogle Scholar
  112. Percival SL, Hill KE, Williams DW et al (2012) A review of the scientific evidence for biofilms in wounds. Wound Repair Regen 20:647–657PubMedGoogle Scholar
  113. Perkins SD, Woeltje KF, Angenent LT (2010) Endotracheal tube biofilm inoculation of oral flora and subsequent colonization of opportunistic pathogens. Int J Med Microbiol 300:503–511PubMedGoogle Scholar
  114. Pihl M, Davies JR, Johansson AC et al (2013) Bacteria on catheters in patients undergoing peritoneal dialysis. Perit Dial Int 33:51–59PubMedCentralPubMedGoogle Scholar
  115. Pneumatikos IA, Dragoumanis CK, Bouros DE (2009) Ventilator-associated pneumonia or endotracheal tube-associated pneumonia? Anesthesiology 110:673–680PubMedGoogle Scholar
  116. Portillo ME, Corvec S, Borens O et al (2013) Propionibacterium acnes: an underestimated pathogen in implant-associated infections. Biomed Res Int 2013:804391PubMedCentralPubMedGoogle Scholar
  117. Probert HM, Gibson GR (2002) Bacterial biofilms in the human gastrointestinal tract. Curr Issues Intest Microbiol 3:23–27PubMedGoogle Scholar
  118. Pumbwe L, Skilbeck CA, Nakano V et al (2007) Bile salts enhance bacterial co-aggregation, bacterial-intestinal epithelial cell adhesion, biofilm formation and antimicrobial resistance of Bacteroides fragilis. Microb Pathog 43:78–87PubMedGoogle Scholar
  119. Ramage G, Tunney MM, Patrick S et al (2003) Formation of Propionibacterium acnes biofilms on orthopaedic biomaterials and their susceptibility to antimicrobials. Biomaterials 24:3221–3227PubMedGoogle Scholar
  120. Robert R, Grollier G, Doré P et al (1999) Nosocomial pneumonia with isolation of anaerobic bacteria in ICU patients: therapeutic considerations and outcome. J Crit Care 14:114–119PubMedGoogle Scholar
  121. Roberts AP, Mullany P (2010) Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev Anti Infect Ther 8:1441–1450PubMedGoogle Scholar
  122. Sapico FL, Wideman PA, Finegold SM (1976) Aerobic and anaerobic bladder urine flora of patients with indwelling urethral catheters. Urology 7:382–384PubMedGoogle Scholar
  123. Sartelli M, Catena F, Ansaloni L et al (2012) Complicated intra-abdominal infections in Europe: a comprehensive review of the CIAO study. World J Emerg Surg 7:36PubMedCentralPubMedGoogle Scholar
  124. Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Med 31:107–133Google Scholar
  125. Scheithauer BK, Wos-Oxley ML, Ferslev B et al (2009) Characterization of the complex bacterial communities colonizing biliary stents reveals a host-dependent diversity. ISME J 3:797–807PubMedGoogle Scholar
  126. Sendi P, Zimmerli W (2011) Challenges in periprosthetic knee-joint infection. Int J Artif Organs 34:947–956PubMedGoogle Scholar
  127. Shuman EK, Chenoweth CE (2010) Recognition and prevention of healthcare-associated urinary tract infections in the intensive care unit. Crit Care Med 38:S373–S379PubMedGoogle Scholar
  128. Smith DM, Snow DE, Rees E et al (2010) Evaluation of the bacterial diversity of pressure ulcers using bTEFAP pyrosequencing. BMC Med Genomics 3:41PubMedCentralPubMedGoogle Scholar
  129. Song Z, Borgwardt L, Høiby N et al (2013) Prosthesis infections after orthopedic joint replacement: the possible role of bacterial biofilms. Orthop Rev (Pavia) 5:65–71Google Scholar
  130. Spigaglia P, Barbanti F, Mastrantonio P, European Study Group on Clostridium difficile (ESGCD) (2011) Multidrug resistance in European clostridium difficile clinical isolates. J Antimicrob Chemother 66:2227–2234PubMedGoogle Scholar
  131. Spronk PE (2007) Positive blood cultures or Gram-negative pathogens with ventilator-associated pneumonia: what’s the real killer? Crit Care Med 35:2215–2216PubMedGoogle Scholar
  132. Sproule-Willoughby KM, Stanton MM, Rioux KP et al (2010) In vitro anaerobic biofilms of human colonic microbiota. J Microbiol Methods 83:296–301PubMedGoogle Scholar
  133. Su S, Hassett DJ (2012) Anaerobic Pseudomonas aeruginosa and other obligately anaerobic bacterial biofilms growing in the thick airway mucus of chronically infected cystic fibrosis patients: an emerging paradigm or “old hat”? Expert Opin Ther Targets 16:859–873PubMedGoogle Scholar
  134. Sung JJ (1995) Bacterial biofilm and clogging of biliary stents. J Ind Microbiol 15:152–155PubMedGoogle Scholar
  135. Tano E, Melhus A (2011) Evaluation of three swab transport systems for the maintenance of clinically important bacteria in simulated mono- and polymicrobial samples. APMIS 119:198–203PubMedGoogle Scholar
  136. Thomson CH (2011) Biofilms: do they affect wound healing? Int Wound J 8:63–67PubMedGoogle Scholar
  137. Troidle L, Finkelstein F (2006) Treatment and outcome of CPD-associated peritonitis. Ann Clin Microbiol Antimicrob 5:6PubMedCentralPubMedGoogle Scholar
  138. Tunney MM, Patrick S, Gorman SP et al (1998) Improved detection of infection in hip replacements. A currently underestimated problem. J Bone Joint Surg Br 80:568–572PubMedGoogle Scholar
  139. Tunney MM, Patrick S, Curran MD et al (1999) Detection of prosthetic hip infection at revision arthroplasty by immunofluorescence microscopy and PCR amplification of the bacterial 16S rRNA gene. J Clin Microbiol 37:3281–3290PubMedCentralPubMedGoogle Scholar
  140. Tunney MM, Dunne N, Einarsson G et al (2007) Biofilm formation by bacteria isolated from retrieved failed prosthetic hip implants in an in vitro model of hip arthroplasty antibiotic prophylaxis. J Orthop Res 25:2–10PubMedGoogle Scholar
  141. Ulrich M, Beer I, Braitmaier P et al (2010) Relative contribution of Prevotella intermedia and Pseudomonas aeruginosa to lung pathology in airways of patients with cystic fibrosis. Thorax 65:978–984PubMedGoogle Scholar
  142. van Berkel AM, van Marle J, Groen AK et al (2005) Mechanisms of biliary stent clogging: confocal laser scanning and scanning electron microscopy. Endoscopy 37:729–734PubMedGoogle Scholar
  143. Van Wamel WJ, Hendrickx AP, Bonten MJ et al (2007) Growth condition-dependent Esp expression by Enterococcus faecium affects initial adherence and biofilm formation. Infect Immun 75:924–931PubMedCentralPubMedGoogle Scholar
  144. Vandecandelaere I, Matthijs N, Van Nieuwerburgh F et al (2012) Assessment of microbial diversity in biofilms recovered from endotracheal tubes using culture dependent and independent approaches. PLoS One 7:e38401PubMedCentralPubMedGoogle Scholar
  145. Verger C, Chesneau AM, Thibault M et al (1987) Biofilm on Tenckhoff catheters: a possible source for peritonitis. Perit Dial Int 7:174–178Google Scholar
  146. Wang X, Lunsdorf H, Ehren I et al (2010) Characteristics of biofilms from urinary tract catheters and presence of biofilm-related components in Escherichia coli. Curr Microbiol 60:446–453PubMedGoogle Scholar
  147. Ward KH, Olson ME, Lam K et al (1992) Mechanism of persistent infection associated with peritoneal implants. J Med Microbiol 36:406–413PubMedGoogle Scholar
  148. Weickert U, Venzke T, König J et al (2001) Why do bilioduodenal plastic stents become occluded? A clinical and pathological investigation on 100 consecutive patients. Endoscopy 33:786–790PubMedGoogle Scholar
  149. Weickert U, Zimmerling S, Eickhoff A et al (2009) A comparative scanning electron microscopic study of biliary and pancreatic stents. Z Gastroenterol 47:347–350PubMedGoogle Scholar
  150. Weinacht KG, Roche H, Krinos CM et al (2004) Tyrosine site-specific recombinases mediate DNA inversions affecting the expression of outer surface proteins of Bacteroides fragilis. Mol Microbiol 53:1319–1330PubMedGoogle Scholar
  151. Werarak P, Kiratisin P, Thamlikitkul V (2010) Hospital-acquired pneumonia and ventilator-associated pneumonia in adults at Siriraj Hospital: etiology, clinical outcomes, and impact of antimicrobial resistance. J Med Assoc Thai 93:S126–S138PubMedGoogle Scholar
  152. Wiegand PN, Nathwani D, Wilcox MH et al (2012) Clinical and economic burden of Clostridium difficile infection in Europe: a systematic review of healthcare-facility-acquired infection. J Hosp Infect 81:1–14PubMedGoogle Scholar
  153. Wildeboer-Veloo AC, Harmsen HJ, Welling GW et al (2007) Development of 16S rRNA-based probes for the identification of Gram-positive anaerobic cocci isolated from human clinical specimens. Clin Microbiol Infect 13:985–992PubMedGoogle Scholar
  154. Wolcott R, Cutting KF, Dowd SE (2008) Surgical site infections: biofilms, dehiscence and delayed healing. Wounds UK 4:4Google Scholar
  155. Wolcott RD, Gontcharova V, Sun Y et al (2009) Bacterial diversity in surgical site infections: not just aerobic cocci anymore. J Wound Care 18:317–323PubMedGoogle Scholar
  156. Worlitzsch D, Rintelen C, Böhm K et al (2009) Antibiotic-resistant obligate anaerobes during exacerbations of cystic fibrosis patients. Clin Microbiol Infect 15:454–460PubMedGoogle Scholar
  157. Wybo I, Van den Bossche D, Soetens O et al (2014) Fourth Belgian multicentre survey of antibiotic susceptibility of anaerobic bacteria. J Antimicrob Chemother 69:155–161PubMedCentralPubMedGoogle Scholar
  158. Zappe B, Graf S, Ochsner PE et al (2008) Propionibacterium spp. in prosthetic joint infections: a diagnostic challenge. Arch Orthop Trauma Surg 128:1039–1046PubMedGoogle Scholar
  159. Zeller V, Ghorbani A, Strady C et al (2007) Propionibacterium acnes: an agent of prosthetic joint infection and colonization. J Infect 55:119–124PubMedGoogle Scholar
  160. Zhang H, Tsang TK, Jack CA et al (2002) Role of bile mucin in bacterial adherence to biliary stents. J Lab Clin Med 139:28–34PubMedGoogle Scholar
  161. Zijnge V, Ammann T, Thurnheer T et al (2012) Subgingival biofilm structure. Front Oral Biol 15:1–16PubMedGoogle Scholar
  162. Zimmerli W, Moser C (2012) Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunol Med Microbiol 65:158–168PubMedGoogle Scholar
  163. Zingg W, Sax H, Inan C et al (2009) Hospital-wide surveillance of catheter-related bloodstream infection: from the expected to the unexpected. J Hosp Infect 73:41–46PubMedGoogle Scholar
  164. Zoetendal EG, von Wright A, Vilpponen-Salmela T et al (2002) Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from faeces. Appl Environ Microbiol 68:3401–3407PubMedCentralPubMedGoogle Scholar
  165. Zolfaghari PS, Wyncoll DL (2011) The tracheal tube: gateway to ventilator-associated pneumonia. Crit Care 15:310PubMedCentralPubMedGoogle Scholar
  166. Zulkowski K, Langemo D, Posthauer M, National Pressure Ulcer Advisory Panel (2005) Coming to consensus on deep tissue injury. Adv Skin Wound Care 18:28–29PubMedGoogle Scholar
  167. Zur KB, Mandell DL, Gordon RE et al (2004) Electron microscopic analysis of biofilm on endotracheal tubes removed from intubated neonates. Otolaryngol Head Neck Surg 130:407–414PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Microbial Biofilm LaboratoryFondazione Santa Lucia IRCCSRomeItaly

Personalised recommendations