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Evidence and Significance of Biofilms in Chronic Wounds in Horses

  • Samantha J. WestgateEmail author
  • Steven L. Percival
  • Peter D. Clegg
  • Derek C. Knottenbelt
  • Christine A. Cochrane
Chapter
  • 1.3k Downloads
Part of the Springer Series on Biofilms book series (BIOFILMS, volume 6)

Abstract

Equine wounds have a high risk of becoming infected due to their environment. Infected wounds encompass diverse populations of microorganisms that fail to respond to antibiotic treatment, resulting in chronic non-healing wounds. In human wounds this has been attributed to the ability of bacteria to survive in a biofilm phenotypic state. Biofilms are known to delay wound healing, principally due to their recalcitrance towards antimicrobial therapies and components of the innate immune response. The presence of biofilms in equine wounds partly explains the reluctance of many lower limb wounds to heal. Non-healing limb wounds in horses are a well documented welfare and economic concern. Therefore, there is a need to develop future treatments in order to increase the healing rate, decrease the cost of treatment and reduce suffering associate with equine wounds.

Keywords

Minimum Inhibitory Concentration Chronic Wound Wound Healing Process Fluid Channel Bacterial Attachment 
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.

References

  1. Adam EN, Southwood LL (2006) Surgical and traumatic wound infections, cellulitis, and myositis in horses. Vet Clin North Am Equine Pract 22:335–361PubMedCrossRefGoogle Scholar
  2. Anderl JN, Franklin MJ, Stewart PS (2000) Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44:1818–1824PubMedCrossRefGoogle Scholar
  3. Apelqvist J, Larsson J, Agardh CD (1993) Long-term prognosis for diabetic patients with foot ulcers. J Intern Med 233:485–491PubMedCrossRefGoogle Scholar
  4. Araujo JC, Teran FC, Oliveira RA, Nour EAA, Montenegro MAP, Campos JR, Vazoller RF (2003) Comparison of hexamethyldisilazane and critical point drying treatments for SEM analysis of anaerobic biofilms and granular sludge. J Electron Microsc 52:429–433CrossRefGoogle Scholar
  5. Arciola CR, Campoccia D, Gamberini S, Cervellati M, Donati E, Montanaro L (2002) Detection of slime production by means of an optimised Congo red agar plate test based on a colourimetric scale in Staphylococcus epidermidis clinical isolates genotyped for ica locus. Biomaterials 23:4233–4239PubMedCrossRefGoogle Scholar
  6. Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production1. Plant Physiol 134:307–319PubMedCrossRefGoogle Scholar
  7. Bakker DJ (2000) Hyperbaric oxygen therapy and the diabetic foot. Diab/Metab Res Rev 16:S55–S58CrossRefGoogle Scholar
  8. Balaban N, Cirioni O, Giacometti A, Ghiselli R, Braunstein JB, Silvestri C, Mocchegiani F, Saba V, Scalise G (2007) Treatment of staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP. Antimicrob Agents Chemother 51:2226–2229PubMedCrossRefGoogle Scholar
  9. Baselga R, Albizu I, De La Cruz M, Del Cacho E, Barberan M, Amorena B (1993) Phase variation of slime production in Staphylococcus aureus: implications in colonization and virulence. Infect Immun 61:4857–4862PubMedGoogle Scholar
  10. Benn M, Hagelskjaer LH, Tvede M (1997) Infective endocarditis, 1984 through 1993: a clinical and microbiological survey. J Intern Med 242:15–22PubMedCrossRefGoogle Scholar
  11. Bertone AL (1996) Infectious arthritis. In: McIlraith CW, Trotter G (eds) Joint disease in the horse. WB Saunders, Philadelphia, pp 397–409Google Scholar
  12. Bjarnsholt T, Kirketerp-Møller K, Jensen PØ, Madsen KG, Phipps R, Krogfelt K, Høiby N, Givskov M (2008) Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen 16:2–10PubMedCrossRefGoogle Scholar
  13. Bjarnsholt T, Jenson PO, Fiandaca MJ, Pedersen J, Hansen CR, Andersen CB, Pressier T, Givskov M, Hoiby N (2009) Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 44:547–558PubMedCrossRefGoogle Scholar
  14. Bolister N, Basker M, Hodges NA, Marriott C (1991) The diffusion of beta-lactam antibiotics through mixed gels of cystic fibrosis-derived mucin and Pseudomonas aeruginosa alginate. J Antimicrob Chemother 27:285–293PubMedCrossRefGoogle Scholar
  15. Bowler PG (2003) The 105 bacterial growth guidelines: reassessing its clinical relevance in wound healing. Ost Wound Manag 49:44–53Google Scholar
  16. Brady RA, Leid JG, Kofonow J, Costerton JW, Shirtliff ME (2007) Immunoglobulins to surface-associated biofilm immunogens provide a novel means of visualization of methicillin-resistant Staphylococcus aureus biofilms. Appl Environ Microbiol 73:6612–6619PubMedCrossRefGoogle Scholar
  17. Brenner K, Karig DK, Weiss R, Arnold FH (2007) Engineered bidirectional communication mediates a consensus in a microbial biofilm consortium. Proc Natl Acad Sci USA 104:17300–17304PubMedCrossRefGoogle Scholar
  18. Broadley KN, Aquino AM, Woodward SC, Buckley-Sturrock A, Sato Y, Rifkin DB, Davidson JM (1989) Monospecific antibodies implicate basic fibroblast growth factor in normal wound repair. Lab Investig 61:571–575PubMedGoogle Scholar
  19. Brooun A, Songhua L, Lewis K (2000) A dose-response study of antibiotic resistance in Pseudamonas aeruginosa biofilms. Antimicrob Agents Chemother 44:640–646PubMedCrossRefGoogle Scholar
  20. Burton E, Yakandawala N, LoVetri K, Madhyastha MS (2007) A microplate spectrofluorometric assay for bacterial biofilms. J Ind Microbiol Biotechnol 34:1–4PubMedCrossRefGoogle Scholar
  21. Busscher HJ, Free RH, Van Weissenbruch R, Albers FWJ, Van Der Mei HC (2000) Preliminary observations on influence of dairy products on biofilm removal from silicone rubber voice prostheses in vitro. J Dairy Sci 83:641–647PubMedCrossRefGoogle Scholar
  22. Carter CA, Jolly DG, Worden CE, Hendren DG, Kane CJM (2003) Platelet-rich plasma gel promotes differentiation and regeneration during equine wound healing. Exp Mol Pathol 74:224–255CrossRefGoogle Scholar
  23. Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A (1999) The calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776PubMedGoogle Scholar
  24. Chavakis T, Hussain M, Kanse SM (2002) Staphylococcus aureus extracellular adherence protein serves as an anti-inflammatory factor by inhibiting the recruitment of host leukocytes. Nat Med 8:687–693PubMedCrossRefGoogle Scholar
  25. Chen X, Stewart PS (2000) Biofilm removal caused by chemical treatments. Water Res 34:4229–4233CrossRefGoogle Scholar
  26. Chincholikar DA, Pal RB (2002) Study of fungal and bacterial infections of the diabetic foot. Indian J Pathol Microbiol 45:15–22PubMedGoogle Scholar
  27. Clark RAF (1985) Cutaneous tissue repair: basic biological considerations. J Am Acad Dermatol 13:701–725PubMedCrossRefGoogle Scholar
  28. Clutterbuck AL, Cochrane CA, Dolman J, Percival SL (2007a) Evaluating antibiotics for use in medicine using a poloxamer biofilm model. Ann Clin Microbiol Antimicrob 6:2PubMedCrossRefGoogle Scholar
  29. Clutterbuck AL, Woods EJ, Knottenbelt DC, Clegg PD, Cochrane CA, Percival SL (2007b) Biofilms and their relevance to veterinary medicine. Vet Microbiol 121:1–17PubMedCrossRefGoogle Scholar
  30. Cochrane CA (1997) Models in vivo of wound healing in the horse and the role of growth factors. Vet Dermatol 8:259–272CrossRefGoogle Scholar
  31. Cochrane CA, Pain R, Knottenbelt DK (2003) In-vitro wound contraction in the horse: differences between body and limb wounds. Wounds 15:175–181Google Scholar
  32. Cochrane CA, Freeman K, Woods E, Welsby S, Percival SL (2009) Biofilm evidence and the microbial diversity of horse wounds. Can J Microbiol 55:197–202PubMedCrossRefGoogle Scholar
  33. Collins MN, Friend TH, Jousan FD, Chen SC (2000) Effect of density on displacement, falls, injuries and orientation during horse transportation. Appl Anim Behav Sci 67:169–179PubMedCrossRefGoogle Scholar
  34. Costerton JW (1999) Introduction to biofilm. Int J Antimicrob Agents 11:217–221PubMedCrossRefGoogle Scholar
  35. Costerton JW, Steward PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284(5418):1318–1322PubMedCrossRefGoogle Scholar
  36. Cruse PJ, Foord R (1980) The epidemiology of wound infection. A 10-year prospective study of 62,939 wounds. Surg Clin North Am 60:27–40PubMedGoogle Scholar
  37. Dahm AM, De Bruin A, Limat A, VON Tscharner C, Wyder M, Suter MM (2002) Cultivation and characterisation of primary and subcultured equine keratinocytes. Equine Vet J 34:114–120PubMedCrossRefGoogle Scholar
  38. Darby I, Gabbiani G (1990) Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Investig 63:21–29PubMedGoogle Scholar
  39. Darveau RP, McFall-Ngai M, Ruby E, Miller S, Mangan DF (2003) Host tissues may actively respond to beneficial microbes. ASM News 69:86–191Google Scholar
  40. Davies DG, 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 280:295–298PubMedCrossRefGoogle Scholar
  41. Davis SC, Ricotti C, Cazzaniga A, Welsh E, Eaglstein WH, Mertz PM (2008) Microscopic and physiological evidence forbiofilm-associated wound colonisation in vivo. Wound Repair Regen 16:23–29PubMedCrossRefGoogle Scholar
  42. De Kievit TR, Parkins MD, Gilllis RJ, Srikumar R, Ceri H, Poole K, Iglewski BH, Storey DG (2001) Multidrug efflux pumps: expression patterns and contribution to antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 45:1761–1770PubMedCrossRefGoogle Scholar
  43. DeBeer D, Srinivasan R, Stewart PS (1994) Direct measurement of chlorine penetration into biofilms during disinfection. Appl Environ Microbiol 60:4339–4344Google Scholar
  44. DeRossi R, Coelho ACAO, Mello GS, Frazílio FO, Leal CRB, Facco GG, Brum KB (2009) Effects of platelet-rich plasma gel on skin healing in surgical wound in horses. Acta Cir Bras 24:276–281PubMedCrossRefGoogle Scholar
  45. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890PubMedGoogle Scholar
  46. Donlan RM (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17:66–72PubMedCrossRefGoogle Scholar
  47. Dorsett-Martin WA, Wysocki AB (2008) Rat models of skin wound healing. In: Conn PM (ed) Sourcebook of models for biomedical research. Humana, Totowa, NJ, pp 631–638CrossRefGoogle Scholar
  48. Elliot M (2001) Cushing’s disease: a new approach to therapy in equine and canine patients. Br Homeopath J 90:33–36CrossRefGoogle Scholar
  49. Fazli M, Bjarnsholt T, Kirketerp-Møller K, Jørgensen B, Andersen AS, Krogfelt K, Givskov M, Tolker-Nielsen T (2009) Non-RNAdon distribution of Pseudamonas aeruginoa and Staphylococcus aureus in chronic wounds. J Clin Microbiol. doi: 10.1128/JCM.01395-09
  50. Fexby S, Bjarnsholt T, Ostrup JP (2007) Biological Trojan horse: antigen 43 provides specific bacterial uptake and survival in human neutrophils. Infect Immun 75:30–34PubMedCrossRefGoogle Scholar
  51. Frank S, Hubner G, Breier G, Longaker MT, Greenhalgh DG, Werner S (1995) Regulation of vascular endothelial growth factor expression in cultured keratonocytes, implications for normal and impaired wound healing. Am Soc Biochem Mol Biol 270:12607–12613Google Scholar
  52. Fratesi SE, Lynch FL, Kirkland BL, Brown LR (2004) Effects of SEM preparation techniques on the appearance of bacteria and biofilms in the Carter Sandstone. J Sed Res 74:858–867CrossRefGoogle Scholar
  53. Galuppo LD, Pascoe JR, Jang SS, Willits NH, Greenman SL (1999) Evaluation of iodophor skin preparation techniques and factors influencing drainage from ventral midline incisions in horses. J Am Vet Med Assoc 215:969Google Scholar
  54. Gay CC, Lording PM (1980) Peritonitis in horses associated with Actinobacillus equuli. Aust Vet J 56:296–300PubMedCrossRefGoogle Scholar
  55. Golovlev EL (2002) The mechanism of formation of Pseudomonas aeruginosa biofilm, a type of structured population. Mikrobiologiia 71:293–300PubMedGoogle Scholar
  56. Goodrich LR (2006) Osteomyelitis in horses. Vet Clin North Am Equine Pract 22:389–417PubMedCrossRefGoogle Scholar
  57. Graham DY (1999) Antibiotic resistance in Helicobacter pylori: implications for therapy. Gastroenterology 117:1032–1033CrossRefGoogle Scholar
  58. Greiling D, Clark RAF (1997) Fibronectin provides a conduit for fibroblast transmigration from collagenous stroma into fibrin clot provisional matrix. J Cell Sci 110:861–870PubMedGoogle Scholar
  59. Griffiths DA, Simpson RA, Shorey BA, Speller DCE, Williams NB (2003) Single-dose preoperative antibiotic prophylaxis in gastrointestinal surgery. Lancet 308:325–328CrossRefGoogle Scholar
  60. Grinnell F (1992) Wound repair, keratinocyte activation and integrin modulation. J Cell Sci 101:1–5PubMedGoogle Scholar
  61. Hadi R, Vickery K, Deva A, Charlton T (2010) Biofilm removal by medical device cleaners: comparison of two bioreactor detection assays. J Hosp Infect 74:160–167PubMedCrossRefGoogle Scholar
  62. Hall MJR, Wall R (1995) Myiasis of humans and domestic animals. Adv Parasitol 35:257–334PubMedCrossRefGoogle Scholar
  63. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108PubMedCrossRefGoogle Scholar
  64. Harrison-Balastra C, Cazzaniga AL, Davis SC, Mertz PM (2003) A wound-isolated Pseudomonas aeruginosa grows a biofilm in vitro within 10 hours and is visualized by light microscopy. J Dermatol Surg 29:1–5CrossRefGoogle Scholar
  65. Hausner M, Wuertz S (1999) High rates of conjugation in bacterial biofilms as determined by quantitative in situ analysis. Appl Environ Miocrobiol 65:3710–3713Google Scholar
  66. Hendrickson D, Virgin J (2005) Factors that affect equine wound repair. Vet Clin Equine 21:33–44CrossRefGoogle Scholar
  67. Hernandez J, Hawkins DL (2001) Training failure among yearling horses. Am J Vet Res 62:1418–1422PubMedCrossRefGoogle Scholar
  68. Hoiby N, Krogh JH, Moser C, Song Z, Ciofu O, Kharazmi A (2001) Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect 3:23–35PubMedCrossRefGoogle Scholar
  69. Hoyle BD, Jass J, Costerton JW (1990) The biofilm glycocalyx as a resistance factor. J Antimicrob Chemother 26:1–5PubMedCrossRefGoogle Scholar
  70. Hyde JA, Darouiche RO, Costerton LW (1998) Strategies for prophylaxis against prosthetic valve endocarditis: a review article. J Heart Valve Dis 7:316–326PubMedGoogle Scholar
  71. Ivnitsky H, Katz I, Minz D, Volvovic G, Shimoni E, Kesselman E, Semiat R, Dosoretz CG (2007) Bacterial community composition and structure of biofilms developing on nanofiltration membranes applied to wastewater treatment. Water Res 41:3924–3935PubMedCrossRefGoogle Scholar
  72. Izano EA, Wang H, Ragunath C, Ramasubbu N, Kaplan JB (2007) Detachment and Killing of Aggregatibacter actinomycetemcomitans biofilms by dispersin B and SDS. J Dent Res 86:618–622PubMedCrossRefGoogle Scholar
  73. James GA, Swogger E, Wolcott R, Pulcini ED, Secor P, Sestrich J, Costerton JW, Stewart PS (2008) Biofilms in chronic wounds. Wound Repair Regen 16:37–44PubMedCrossRefGoogle Scholar
  74. Johnson D (1990) The effect of continuous passive motion on wound-healing and joint mobility after knee arthroplasty. J Bone Joint Surg Am 72:421–426PubMedGoogle Scholar
  75. Johnson P, Hayman J, Quek T (2007) Consensus recommendations for the diagnosis, treatment and control of Mycobacterium ulcerans infection (Bairnsdale or Buruli ulcer) in Victoria, Australia. Med J Aust 186:64–68PubMedGoogle Scholar
  76. Kaeberlein T, Lewis K, Epstein SS (2002) “Uncultivable” microorganisms in pure culture in simulated natural environment. Science 296:1127–1129PubMedCrossRefGoogle Scholar
  77. Kania RE, Lamers GEM, Vonk JM, Dorpmans E, Struik J, Huy PT, Hiemstra P, Bloemberg GV, Grote JJ (2008) Characterization of mucosal biofilms on human adenoid tissues. Laryngoscope 118:128–134PubMedCrossRefGoogle Scholar
  78. Kingsley A (2001) A reactive approach to wound infection. Nurs Stand 15:50–58PubMedGoogle Scholar
  79. Kipnis E, Sawa T, Wiener-Kronish J (2006) Targeting mechanisms of Pseudomonas aeruginosa pathogenesis. Me´ Malad Infect 36:78–91CrossRefGoogle Scholar
  80. Kirker KR, Secor PR, James GA, Fleckman P, Olerud JE, Stewart PS (2009) Loss of viability and induction of apoptosis in human keratinocytes exposed to Staphylococcus aureus biofilms in vitro. Wound Repair Regen 17:690–699PubMedCrossRefGoogle Scholar
  81. Knottenbelt DC (1997) Equine wound management: are there significant differences in healing at different sites on the body? Vet Dermatol 8:273–290CrossRefGoogle Scholar
  82. Knottenbelt DC (2003) Handbook of equine wound management. WB Saunders, LiverpoolGoogle Scholar
  83. Knottenbelt DC (2007) Handbook of equine wound management. WB Saunders, ChinaGoogle Scholar
  84. Knubben JM, Furst A, Gygax L, Stauffacher M (2008) Bite and kick injuries in horses: prevalence, risk factors and prevention. Equine Vet J 40:219–223PubMedCrossRefGoogle Scholar
  85. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ (2002) Communication among oral bacteria. Microb Mol Biol Rev 66:486–505CrossRefGoogle Scholar
  86. Kumar S, Leaper DJ (2005) Classification and management of acute wounds. Surgery 23:47–51Google Scholar
  87. Lagendijk EL, Validov S, Lamers GEM, de Weert S, Bloemberg GV (2009) Genetic tools for tagging Gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS Microbiol Lett 305:81–90CrossRefGoogle Scholar
  88. Lambers H, Piessens S, Bloem A (2006) Natural skin surface pH is on average below 5, which is beneficial for its resident flora. Int J Cosmet Sci 28:359–370PubMedCrossRefGoogle Scholar
  89. Landry RM, An D, Hupp JT, Singh PK, Parsek MR (2006) Musin-Pseudomonas aeruginosa interactions promote biofilm formation and antibiotic resistance. Mol Microbiol 59:142–151PubMedCrossRefGoogle Scholar
  90. Lee YK, Lim CY, Teng WL, Ouwehand AC, Tuomola EM, Salminen S (2000) Quantitative approach in the study of adhesion of lactic acid bacteria to intestinal cells and their competition with Enterobacteria. Appl Environ Microbiol 66:3692–3697PubMedCrossRefGoogle Scholar
  91. Lefebvre-Lavoie J, Lussier JG, Theoret CL (2005) Profiling of differentially expressed genes in wound margin biopsies of horses using suppression subtractive hybridization. Physiol Genomics 22:157–170PubMedCrossRefGoogle Scholar
  92. Leid JG, Shirtliff ME, Costerton JW, Stoodley AP (2002) Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun 70:6339–6345PubMedCrossRefGoogle Scholar
  93. Leigh DA, Simmons K, Norman E (1974) Bacterial flora of the appendix fossa in appendicitis and postoperative wound infection. J Clin Path 27:997–1000PubMedCrossRefGoogle Scholar
  94. Lewandowski L, Stoodley AP, Roe F, (1995) Internal mass transport in heterogeneous biofilms: recent advances. In: NACE International Annual Conference and Corrosion Show, HoustonGoogle Scholar
  95. Lindsay D, Von Holy A (2006) Bacterial biofilms within the clinical setting. What healthcare professionals should know. J Hosp Infect 64:313–325PubMedCrossRefGoogle Scholar
  96. Lipsky Benjamin A, Hoey C (2009) Clinical practice: topical antimicrobial therapy for treating chronic wounds. Clin Infect Dis 49:1541–1549PubMedCrossRefGoogle Scholar
  97. Little B, Wagner P, Ray R, Pope R, Scheetz R (1991) Biofilms: an ESEM evaluation of artifacts introduced during SEM preparation. J Ind Microbiol Biotechnol 8:213–221Google Scholar
  98. Loo CY, Corliss DA, Ganeshkumar N (2000) Streptococcus gordonii biofilm formation: identification of genes that code for biofilm phenotypes. Am J Microbiol 182:1374–1382Google Scholar
  99. Lu TK, Collins JJ (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci USA 104:111CrossRefGoogle Scholar
  100. MacDonald DG, Morley PS, Bailey JV, Barber SM, Fretz PB (1994) An examination of the occurrence of surgical wound infection following equine orthopaedic surgery (1981–1990). Equine Vet J 6:323–326CrossRefGoogle Scholar
  101. Mair TS, Smith LJ (2005) Survival and complication rates in 300 horses undergoing surgical treatment of colic. Part 2: Short-term complications. Equine Vet J 37:303–309PubMedCrossRefGoogle Scholar
  102. Malic S, Hill KE, Hayes A, Percival SL, Thomas DW, Williams DW (2009) Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA FISH). Microbiology 155:2603–2611PubMedCrossRefGoogle Scholar
  103. Mangold S, Harneit K, Rohwerder T, Claus G, Sand W (2008) Novel combination of atomic force microscopy and epifluorescence microscopy for visualization of leaching bacteria on pyrite. Appl Environ Microbiol 74:410–415PubMedCrossRefGoogle Scholar
  104. Marrie TJ, Costerton JW (1984) Scanning and transmission electron microscopy of in situ bacterial colonization of intravenous and intraarterial catheters. J Clin Microbiol 19(5):687–693PubMedGoogle Scholar
  105. Marrie TJ, Nelligan J, Costerton JW (1982) A scanning and transmission electron microscopic study of an infected endocardial pacemaker lead. Circulation 66:1339–1341PubMedCrossRefGoogle Scholar
  106. Mateo M, Maestre J, Aguilar L, Giménez M, Granizo J, Prieto J (2008) Strong slime production is a marker of clinical significance in Staphylococcus epidermidis isolated from intravascular catheters. Eur J Clin Microbiol Infect Dis 27:311–314PubMedCrossRefGoogle Scholar
  107. Merckoll P, Jonassen TØ, Vad ME, Jeansson SL, Melby KK (2009) Bacteria, biofilm and honey: a study of the effects of honey on ‘planktonic’ and biofilm-embedded chronic wound bacteria. Scand J Infect Dis 41:341–347PubMedCrossRefGoogle Scholar
  108. Mertz PM (2003) Cutaneous biofilms: friend or foe? Wounds 15:129–132Google Scholar
  109. Mertz AJ, Forest KT (2002) Bacterial surphase motility: slime trails, grappling hooks and nozzles. Curr Microbiol 12:297–303Google Scholar
  110. Morris NS, Stickler DJ, McLean RJ (1999) The development of bacterial biofilms on indwelling urethral catheters. World J Urol 17:345–350PubMedCrossRefGoogle Scholar
  111. Nadell CD, Xavier JB, Levin SA, Foster KR (2008) The evolution of quorum sensing in bacterial biofilms. PLoS Biol 6:14CrossRefGoogle Scholar
  112. Nadell CD, Xavier JB, Foster KR (2009) The sociobiology of biofilms. FEMS Microbiol Rev 33:206–224PubMedCrossRefGoogle Scholar
  113. Nakada T, Saito Y, Chikenji M, Koda S, Higuchi M, Kawata K, Ishida S, Takahashi S, Kondo S, Kubota Y, Kubota I, Shimizu Y (2006) Therapeutic outcome of hyperbaric oxygen and basic fibroblast growth factor on intractable skin ulcer in legs: preliminary report. Plast Reconstr Surg 117:646–651PubMedCrossRefGoogle Scholar
  114. Neu TR (1996) Significance of bacterial surface-active compounds in interactions of bacteria with interfaces. Microbiol Rev 60:151–166PubMedGoogle Scholar
  115. Nguyen TT, Gilpin DA, Meyer DA (1996) Current treatment of severely burned patients. Ann Surg 223:14–25PubMedCrossRefGoogle Scholar
  116. Nichols WW, Dorrington SM, Slack MP, Walmsley HL (1988) Inhibition of tobramycin diffusion by binding to alginate. Antimicrob Agents Chemother 32:518–523PubMedGoogle Scholar
  117. O’Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461PubMedCrossRefGoogle Scholar
  118. O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79PubMedCrossRefGoogle Scholar
  119. Parsek MR, Greenberg EP (2005) Sociomicrobiology: the connection between quorum sensing and biofilms. Trends Microbiol 13:27–33PubMedCrossRefGoogle Scholar
  120. Percival SL, Cochrane CA (2010) MMP and microbial enzymes. In: Percival SL, Cutting K (eds) Microbiology of wound. CRC, New YorkCrossRefGoogle Scholar
  121. Phillips P, Sampson E, Yang O, Antonelli P, Progulske-Fox A, Schultz G (2008) Bacterial biofilms in wounds. Wound Heal South Afr 1:10–12Google Scholar
  122. 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 181:5993–6002PubMedGoogle Scholar
  123. Proudman CJ, Smith JE, Edwards GB, French NP (2002) Long-term survival of equine surgical colic cases. Part 1. Patterns of mortality and morbidity. Equine Vet J 34:432–437PubMedCrossRefGoogle Scholar
  124. Rather PN (2005) Swarmer cell differentiation in Proteus mirabilis. Environ Microbiol 7:1065–1073PubMedCrossRefGoogle Scholar
  125. Rhoads DD, Wolcott RD, Percival SL (2008) Biofilms in wounds: management strategies. J Woundcare 17:502–508Google Scholar
  126. Rice SA, Koh KS, Queck SY, Labbate M, Lam KW, Kjelleberg S (2005) Biofilm formation and sloughing in Serratia marcescens are controlled by quorum sensing and nutrient cues. J Bacteriol 187:3477–3485PubMedCrossRefGoogle Scholar
  127. Rivera AE, Spencer JM (2007) Clinical aspects of full-thickness wound healing. Clin Dermatol 25:39–48PubMedCrossRefGoogle Scholar
  128. Roberts IS (1996) The biochemistry and genetics of capsular polysacharide production in bacteria. Annu Rev Microbiol 50:285–315PubMedCrossRefGoogle Scholar
  129. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184:1140–1154PubMedCrossRefGoogle Scholar
  130. Schaudinn C, Carr G, Gorur A, Jaramillo D, Costerton JW, Webster P (2009) Imaging of endodontic biofilms by combined microscopy (FISH/cLSM – SEM). J Microsc 235:124–127PubMedCrossRefGoogle Scholar
  131. Schierle CF, Garza MDl, Mustoe TA, Galiano RD (2009) Staphylococcal biofilms impair wound healing by delaying reepithelialization in a murine cutaneous wound model. Wound Repair Regen 17:354–359PubMedCrossRefGoogle Scholar
  132. Schreml S, Szeimies RM, Karrer S, Heinlin J, Landthaler M, Babilas P (2009) The impact of the pH value on skin integrity and cutaneous wound healing. J Eur Acad Dermatol Venereol 24:373–378PubMedCrossRefGoogle Scholar
  133. Schwartz AJ, Wilson DA, Keegan KG (2002) Factors regulating collagen synthesis and degredation during second-intension healing of wounds in the thoracic region and distal aspect of the forelimb of horses. Am J Vet Clin 63:1564–1570CrossRefGoogle Scholar
  134. Sen CK (2009) Wound healing essentials: let there be oxygen. Wound Repair Regen 17:1–18PubMedCrossRefGoogle Scholar
  135. Sepandj F, Ceri H, Gibb A, Read R, Olson M (2007) Minimum inhibitory concentration versus minimum biofilm eliminating concentration in evaluation of antibiotic sensitivity of enterococci causing peritonitis. Perit Dial Int 27:464–468PubMedGoogle Scholar
  136. Serralta VW, Harrison-Balestra C, Cazzaniga AL (2001) Lifestyles of bacteria in wounds: presence of biofilms? Wounds 13:29–34Google Scholar
  137. Sherman RA, Morrison S, Ng D (2007) Maggot debridement therapy for serious horse wounds – a survey of practitioners. Vet J 174:86–91PubMedCrossRefGoogle Scholar
  138. Singer II, Kawka DM, Kazazis DM, Clark RAF (1984) The in vivo codistribution of fibronectin and actin firers in granulation tissue: immunofluorescence and electron microscopic studies of the fibronexus at the myofibroblast surface. J Cell Biol 98:2091PubMedCrossRefGoogle Scholar
  139. Singer ER, Saxby F, French NP (2003) A retrospective case-control study of horse falls in the sport of horse trials and three-day eventing. Equine Vet J 35:139–145PubMedCrossRefGoogle Scholar
  140. Singh PK, Schaefer AL, Parsek MR, Moninger TO, Welsh MJ, Greenberg EP (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407:762–764PubMedCrossRefGoogle Scholar
  141. Slovis N (2008) Review of equine hyperbaric medicine. J Equine Vet Sci 28:760–767CrossRefGoogle Scholar
  142. Smith MA, Ross MW (2002) Postoperative infection with Actinobacillus spp. in horses: 10 cases (1995–2000). J Am Vet Med Assoc 221:1306–1310PubMedCrossRefGoogle Scholar
  143. Stevens N, Tharmabala M, Dillane T, Greene CM, O’Gara JP, Humphreys H (2008) Biofilm and the role of the ica operon and aap in Staphylococcus epidermidis isolates causing neurosurgical meningitis. Clin Microbiol Infect 14:719–722PubMedCrossRefGoogle Scholar
  144. Stewart PS, Franklin MJ (2008) Physiological heterogeneity in biofilms. Nat Rev Micro 6:199–210CrossRefGoogle Scholar
  145. Stoodley P, Wilson S, Hall-Stoodley L, Boyle JD, Lappin-Scott HM, Costerton JW (2001) Growth and detachment of cell clusters from mature mixed-species biofilms. Appl Environ Microbiol 67:5608–5613PubMedCrossRefGoogle Scholar
  146. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209PubMedCrossRefGoogle Scholar
  147. Sun Y, Dowd SE, Smith E, Rhoads DD, Wolcott RD (2008) In vitro multispecies Lubbock chronic wound biofilm model. Wound Repair Regen 16:805–813PubMedCrossRefGoogle Scholar
  148. Theoret CL, Barber SM, Moyana TN, Gordon JR (2001) Expression of transforming growth factor β1 and β3, and basic fibroblast growth factor in full-thickness skin wounds of equine limbs and thorax. Vet Surg 30(3):269–277PubMedCrossRefGoogle Scholar
  149. Trostle SS, Peavey CL, King DS, Hartmann FA (2001) Treatment of methicillin-resistant Staphylococcus epidermidis infection following repair of an ulnar fracture and humeroradial joint luxation in a horse. J Am Vet Med Assoc 4:554–559, 527CrossRefGoogle Scholar
  150. Tuomanen E, Cozens R, Tosch W, Zak O, Tomasz A (1986) The rate of killing of Escherichia coli by β-lactam antibiotics is strictly proportional to the rate of bacterial growth. J Gen Microbiol 132:1297–1304PubMedGoogle Scholar
  151. Van der Kolk JH (1997) Equine Cushing’s disease. Equine Vet Educ 9:209–214CrossRefGoogle Scholar
  152. Vasseur PB, Levy J, Dowd E (1988) Surgical wound infection rates in dogs and cats: data from a teaching hospital. Vet Surg Clin N Am 17:60–64CrossRefGoogle Scholar
  153. Waring GH (2003) Agonistic behaviour. In: Waring GH (ed) Horse behaviour. Noyes/William Andrew, New York, pp 253–269Google Scholar
  154. Watnick P, Kolter R (2000) Biofilm: city of microbes. J Bacteriol 182:2675–2679PubMedCrossRefGoogle Scholar
  155. Webster P, Wu S, Webster S, Rich KA, McDonald K (2004) Ultrastructural preservation of biofilms formed by non-typeable Haemophilus influenzae. Biofilms 1:165–182CrossRefGoogle Scholar
  156. Westgate SJ, Percival SL, Knottenbelt DC, Clegg PD, Cochrane CA (2010) Chronic equine wounds: what is the role of infection and biofilms? Wounds 22:138–145Google Scholar
  157. White R, Cutting K (2008) Critical colonisation of chronic wounds: microbial mechanisms. Wounds 4:70–78Google Scholar
  158. Williams P (2007) Quorum sensing, communication and cross-kingdom signalling in the bacterial world. Microbiology 153:3923–3938PubMedCrossRefGoogle Scholar
  159. Wilmink JM, Van Weeren PR (2005) Second-intention repair in the horse and pony and management of exuberant granulation tissue. Vet Clin North Am Equine Pract 21:15–32PubMedCrossRefGoogle Scholar
  160. Wilmink JM, Nederbragt H, Van Weeren PR, Stilk PW, Barneveld A (2001) Differences in wound contraction between horses and ponies: the in vitro contraction capability of fibroblasts. Equine Vet J 33:499–505PubMedCrossRefGoogle Scholar
  161. Wilmink JM, Herten J, Weeren PR, Barneveld A (2002) Retrospective study of primary intention healing and sequestrum formation in horses compared to ponies under clinical circumstances. Equine Vet J 34:270–273PubMedCrossRefGoogle Scholar
  162. Wilmink JM, Van Den Boom R, Van Weeren PR, Barneveld A (2006) The modified Meek technique as a novel method for skin grafting in horses: evaluation of acceptance, wound contraction and closure in chronic wounds. Equine Vet J 38:324–329PubMedCrossRefGoogle Scholar
  163. Wimpenny JWT, Colasanti RA (1997) A unifying hypothesis for the structure of microbial films based on cellular automation models. FEMS Microb Ecol 22:1–16CrossRefGoogle Scholar
  164. Wolcott RD, Rhoads DD (2008) A study of biofilm-based wound management in subjects with critical limb ischaemia. J Wound Care 17:145–155PubMedGoogle Scholar
  165. Wuertz S, Okabe S, Hausner M (2004) Microbial communities and their interactions in biofilm systems: an overview. Water Sci Technol 49:327–336PubMedGoogle Scholar
  166. Xavier JB, Foster KR (2007) Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA 104:876–881PubMedCrossRefGoogle Scholar
  167. Ymele-Leki P, Ross JM (2007) Erosion from Staphylococcus aureus biofilms grown under physiologically relevant fluid shear forces yields bacterial cells with reduced avidity to collagen. Appl Environ Microbiol 73:1834–1841PubMedCrossRefGoogle Scholar
  168. Zhang TC, Bishop PL (1996) Evaluation of substrate and pH effects in a nitrifying biofilm. Water Environ Res 68:1107–1115CrossRefGoogle Scholar
  169. Zyl N, Rayner SG (2008) Penetrating thoracic injury with associated abdominal visceral involvement in a mare. Equine Vet Educ 20:414–417CrossRefGoogle Scholar
  170. Zyl AV, Daniel J, Wayne J, McCowan C, Malik R, Jelfs P, Lavender CJ, Fyfe JA (2010) Mycobacterium ulcerans infections in two horses in south-eastern Australia. Aust Vet J 88:101–106PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  • Samantha J. Westgate
    • 1
    Email author
  • Steven L. Percival
    • 2
  • Peter D. Clegg
    • 3
  • Derek C. Knottenbelt
    • 1
  • Christine A. Cochrane
    • 4
  1. 1.Faculty of Health and Life Sciences, Department of musculoskeletal BiologyUniversity of LiverpoolNestonUK
  2. 2.Department of Pathology, Medical SchoolWest Virginia UniversityMorgantownUSA
  3. 3.Department of Musculoskeletal BiologyUniversity of LiverpoolNestonUK
  4. 4.Faculty of Health and Life Sciences, Institute of Ageing and Chronic DiseaseUniversity of LiverpoolNestonUK

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