Biofilm and Equine Limb Wounds.
Abstract: In chronic wounds in humans, biofilm formation and wound chronicity are linked, as biofilms contribute to chronic inflammation and delayed healing. Biofilms are aggregates of bacteria, and living as biofilms is the default mode of bacterial life; within these aggregates, the bacteria are protected from both antimicrobial substances and the immune response of the host. In horses, delayed healing is more commonly seen in limb wounds than body wounds. Chronic inflammation and hypoxia are the main characteristics of delayed wound healing in equine limbs, and biofilms might also contribute to this healing pattern in horses. However, biofilm formation in equine wounds has been studied to a very limited degree. Biofilms have been detected in equine traumatic wounds, and recent experimental models have shown that biofilms protract the healing of equine limb wounds. Detection of biofilms within wounds necessitates advanced techniques that are not available in routine diagnostic yet. However, infections with biofilm should be suspected in equine limb wounds not healing as expected, as they are in human wounds. Treatment should be based on repeated debridement and application of topical antimicrobial therapy.
Publication Date: 2021-09-27 PubMed ID: 34679846PubMed Central: PMC8532864DOI: 10.3390/ani11102825Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
- Journal Article
- Review
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research explores the link between biofilm formation and delayed wound healing in equines, specifically in limb wounds. The study suggests that biofilms, which are aggregates of bacteria, could contribute to chronic inflammation and slow healing process in horses.
Understanding Biofilm and its Link to Wound Chronicity
- The research highlights biofilms as a significant factor in wound chronicity. Biofilms are aggregates of bacteria that, when formed, can contribute to chronic inflammation and delayed healing in wounds. Bacteria in these formations are protected from both antimicrobial substances and a host’s immune response.
- The correlation between biofilming and chronic wounds is already established in humans. The study seeks to apply this understanding to equine health, specifically focusing on horse limb wounds.
Delayed Healing and Biofilms in Equine Limb Wounds
- A delay in wound healing is more common in equine limb wounds than those on the body. Chronic inflammation and hypoxia, a condition in which part of the body or a region of the body is deprived of adequate oxygen supply, are integral characteristics of this healing delay.
- The researchers suggest that biofilms could also contribute to this common healing pattern seen in horses.
- Advanced techniques are needed to detect biofilms in wounds. These techniques are not yet available in routine diagnostic procedures but are currently under active development and study.
Treatment of Biofilms in Equine Limb Wounds
- If biofilm formation is suspected in equine limb wounds, the treatment approach should involve repeated debridement, a medical procedure that removes infected, damaged, or dead tissue to improve the healing potential of the remaining healthy tissue.
- Application of topical antimicrobial therapy, a treatment aimed at killing or inhibiting the growth of microorganisms, is also advised.
- The presence of biofilm should be suspected especially in cases where equine limb wounds do not heal as anticipated. This suspicion is based on similar observations and treatment guidelines in human wound healing.
Cite This Article
APA
Jørgensen E, Bjarnsholt T, Jacobsen S.
(2021).
Biofilm and Equine Limb Wounds.
Animals (Basel), 11(10).
https://doi.org/10.3390/ani11102825 Publication
Researcher Affiliations
- Costerton Biofilm Center, Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark.
- Costerton Biofilm Center, Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2200 Copenhagen, Denmark.
- Department of Clinical Microbiology, Rigshospitalet, DK-2100 Copenhagen, Denmark.
- Department of Veterinary Clinical Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, DK-2630 Taastrup, Denmark.
Conflict of Interest Statement
The authors declare no conflict of interest.
References
This article includes 133 references
- Bundgaard L, Bendixen E, Sørensen M.A, Harman V.M, Beynon R.J, Petersen L.J, Jacobsen S. A selected reaction monitoring based analysis of acute phase proteins in interstitial fluids from experimental equine wounds healing by secondary intention.. Wound Repair Regen 2016;24:525–532.
- Celeste C.J, Deschene K, Riley C.B, Theoret C.L. Regional differences in wound oxygenation during normal healing in an equine model of cutaneous fibroproliferative disorder.. Wound Repair Regen 2010;19:89–97.
- Mustoe T. Understanding chronic wounds: A unifying hypothesis on their pathogenesis and implications for therapy.. Am. J. Surg. 2004;187:S65–S70.
- Sørensen M.A, Pedersen L.J, Bundgaard L, Toft N, Jacobsen S. Regional disturbances in metabolism and blood flow in equine limb wounds healing with formation of exuberant granulation tissue.. Wound Repair Regen 2014;22:647–653.
- Uccioli L, Izzo V, Meloni M, Vainieri E, Ruotolo V, Giurato L. Non-healing foot ulcers in diabetic patients: General and local interfering conditions and management options with advanced wound dressings.. J. Wound Care 2015;24:35–42.
- Wilmink J.M, Stolk P.W.T, Van Weeren P.R, Barneveld A. Differences in second-intention wound healing between horses and ponies: Macroscopic aspects.. Equine Veter.-J. 1999;31:53–60.
- Bjarnsholt T, Kirketerp-Møller K, Jensen P, Madsen K.G, Phipps R.K, Krogfelt K.A, Høiby N, Givskov M. Why chronic wounds will not heal: A novel hypothesis.. Wound Repair Regen 2008;16:2–10.
- James G.A, Swogger E, Wolcott R, Pulcini E.D, Secor P, Sestrich J, Costerton J.W, Stewart P. Biofilms in chronic wounds.. Wound Repair Regen 2008;16:37–44.
- Malone M, Bjarnsholt T, McBain A.J, James G.A, Stoodley P, Leaper D, Tachi M, Schultz G, Swanson T, Wolcott R. The prevalence of biofilms in chronic wounds: A systematic review and meta-analysis of published data.. J. Wound Care 2017;26:20–25.
- Schultz G, Bjarnsholt T, James G.A, Leaper D.J, McBain A, Malone M, Stoodley P, Swanson T, Tachi M, Wolcott R.D. Consensus guidelines for the identification and treatment of biofilms in chronic nonhealing wounds.. Wound Repair Regen 2017;25:744–757.
- Cochrane C.A, Freeman K, Woods E, Welsby S, Percival S.L. Biofilm evidence and the microbial diversity of horse wounds.. Can. J. Microbiol. 2009;55:197–202.
- Van Hecke L, Hermans K, Haspeslagh M, Chiers K, Pint E, Boyen F, Martens A. A quantitative swab is a good non-invasive alternative to a quantitative biopsy for quantifying bacterial load in wounds healing by second intention in horses.. Veter.-J. 2017;225:63–68.
- Westgate S.J, Percival S.L, Knottenbelt D.C, Clegg P.D, Cochrane C.A. Microbiology of equine wounds and evidence of bacterial biofilms.. Veter.-Microbiol. 2011;150:152–159.
- König L, Klopfleisch R, Kershaw O, Gruber A.D. Prevalence of biofilms on surgical suture segments in wounds of dogs, cats, and horses.. Veter.-Pathol. 2014;52:295–297.
- König L.M, Klopfleisch R, Höper D, Gruber A.D. Next generation sequencing analysis of biofilms from three dogs with postoperative surgical site infection.. Int. Sch. Res. Not. 2014;2014:1–5.
- Swanson E.A, Freeman L.J, Seleem M.N, Snyder P.W. Biofilm-infected wounds in a dog.. J. Am. Veter.-Med. Assoc. 2014;244:699–707.
- Jørgensen E, Bay L, Bjarnsholt T, Bundgaard L, Sørensen M, Jacobsen S. The occurrence of biofilm in an equine experimental wound model of healing by secondary intention.. Veter. Microbiol. 2017;204:90–95.
- Jørgensen E, Bay L, Skovgaard L.T, Bjarnsholt T, Jacobsen S. An equine wound model to study effects of bacterial aggregates on wound healing.. Adv. Wound Care 2019;8:487–498.
- Cochrane C.A. Models in vivo of wound healing in the horse and the role of growth factors.. Veter.-Dermatol. 1997;8:259–272.
- Knottenbelt D.C. Equine wound management: Are there significant differences in healing at different sites on the body?. Veter. Dermatol. 1997;8:273–290.
- Lefebvre-Lavoie J, Lussier J.G, Theoret C.L. Profiling of differentially expressed genes in wound margin biopsies of horses using suppression subtractive hybridization.. Physiol. Genom. 2005;22:157–170.
- Hall-Stoodley L, Costerton J.W, Stoodley P. Bacterial biofilms: From the Natural environment to infectious diseases.. Nat. Rev. Genet. 2004;2:95–108.
- Cornforth D.M, Dees J.L, Ibberson C.B, Huse H.K, Mathiesen I.H, Kirketerp-Møller K, Wolcott R.D, Rumbaugh K.P, Bjarnsholt T, Whiteley M. Pseudomonas aeruginosa transcriptome during human infection.. Proc. Natl. Acad. Sci. USA. 2018;115:E5125–E5134.
- Bjarnsholt T, Alhede M, Alhede M, Eickhardt-Sørensen S.R, Moser C, Kühl M, Jensen P, Høiby N. The in vivo biofilm.. Trends Microbiol. 2013;21:466–474.
- Roberts A.E, Kragh K.N, Bjarnsholt T, Diggle S.P. The limitations of in vitro experimentation in understanding biofilms and chronic infection.. J. Mol. Biol. 2015;427:3646–3661.
- Haesler E, Swanson T, Ousey K, Carville K. Clinical indicators of wound infection and biofilm: Reaching international consensus.. J. Wound Care 2019;28:s4–s12.
- Bjarnsholt T. The role of bacterial biofilms in chronic infections.. APMIS 2013;121:1–58.
- Stewart P.S. Biophysics of biofilm infection.. Pathog. Dis. 2014;70:212–218.
- Flemming H.-C, Wingender J. The biofilm matrix.. Nat. Rev. Genet. 2010;8:623–633.
- Bjarnsholt T, Givskov M. The role of quorum sensing in the pathogenicity of the cunning aggressor Pseudomonas aeruginosa.. Anal. Bioanal. Chem. 2006;387:409–414.
- Jakobsen T.H, Bjarnsholt T, Jensen P.O, Givskov M, Høiby N. Targeting quorum sensing in Pseudomonas aeruginosa biofilms: Current and emerging inhibitors.. Future Microbiol. 2013;8:901–921.
- Singh R, Ray P. Quorum sensing-mediated regulation of staphylococcal virulence and antibiotic resistance.. Future Microbiol. 2014;9:669–681.
- Brackman G, Cos P, Maes L, Nelis H.J, Coenye T. Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo.. Antimicrob. Agents Chemother. 2011;55:2655–2661.
- Stewart P.S, Franklin M.J. Physiological heterogeneity in biofilms.. Nat. Rev. Genet. 2008;6:199–210.
- Stewart P.S. Antimicrobial tolerance in biofilms.. Microbiol. Spectr. 2015;3:3.
- Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms.. Int. J. Antimicrob. Agents. 2010;35:322–332.
- Ceri H, Olson M, Stremick C, Read R.R, Morck D, Buret A. The calgary biofilm device: New technology for rapid determination of antibiotic susceptibilities of bacterial biofilms.. J. Clin. Microbiol. 1999;37:1771–1776.
- Cerca N, Jefferson K, Oliveira R, Pier G.B, Azeredo J. Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state.. Infect. Immun. 2006;74:4849–4855.
- Archer N, Mazaitis M.J, Costerton J.W, Leid J.G, Powers M.E, Shirtliff M.E. Staphylococcus aureus biofilms: Properties, regulation, and roles in human disease.. Virulence 2011;2:445–459.
- Jensen P, Givskov M, Bjarnsholt T, Moser C. The immune system vs. Pseudomonas aeruginosa biofilms.. FEMS Immunol. Med Microbiol. 2010;59:292–305.
- Hoiby N, Koch C. Cystic fibrosis. 1. Pseudomonas aeruginosa infection in cystic fibrosis and its management.. Thorax 1990;45:881–884.
- James G.A, Zhao A.G, Usui M, Underwood R.A, Nguyen H, Beyenal H, deLancey Pulcini E, Agostinho D, Hunt A.A, Bernstein H.C. Microsensor and transcriptomic signatures of oxygen depletion in biofilms associated with chronic wounds.. Wound Repair Regen 2016;24:373–383.
- Grice E.A, Segre J.A. The skin microbiome.. Nat. Rev. Micro. 2011;9:244–253.
- Harrison J.J, Turner R.J, Marques L.L.R, Ceri H. Biofilms.. Am. Sci. 2005;93:508–515.
- Lebeaux D, Ghigo J.-M. Management of biofilm-associated infections: What can we expect from recent research on biofilm lifestyles?. Med. Sci. 2012;28:727–739.
- Trampuz A, Zimmerli W. Diagnosis and treatment of implant-associated septic arthritis and osteomyelitis.. Curr. Infect. Dis. Rep. 2008;10:394–403.
- Wolcott R, Rhoads D, Bennett M, Wolcott B, Gogokhia L, Costerton J, Dowd S. Chronic wounds and the medical biofilm paradigm.. J. Wound Care 2010;19:45–53.
- Moser C, Pedersen H.T, Lerche C.J, Kolpen M, Line L, Thomsen K, Høiby N, Jensen P. Biofilms and host response—helpful or harmful.. APMIS 2017;125:320–338.
- Olson M, Ceri H, Morck D.W, Buret A.G, Read R.R. Biofilm bacteria: Formation and comparative susceptibility to antibiotics.. Can. J. Veter.-Res. 2002;66:86–92.
- Clutterbuck A, Woods E, Knottenbelt D, Clegg P, Cochrane C, Percival S. Biofilms and their relevance to veterinary medicine.. Veter.-Microbiol. 2007;121:1–17.
- Pedersen R.R, Krömker V, Bjarnsholt T, Dahl-Pedersen K, Buhl R, Jørgensen E. Biofilm research in bovine mastitis.. Front. Veter.-Sci. 2021;8.
- Wilmink J.M, Van Herten J, Van Weeren P.R, Barneveld A. Retrospective study of primary intention healing and sequestrum formation in horses compared to ponies under clinical circumstances.. Equine Veter.-J. 2010;34:270–273.
- Spaas J.H, Broeckx S, Van de Walle G, Polettini M. The effects of equine peripheral blood stem cells on cutaneous wound healing: A clinical evaluation in four horses.. Clin. Exp. Dermatol. 2013;38:280–284.
- Owen K.R, Singer E.R, Clegg P.D, Ireland J.L, Pinchbeck G.L. Identification of risk factors for traumatic injury in the general horse population of north-west England, Midlands and north Wales.. Equine Veter.-J. 2011;44:143–148.
- Agina O.A, Ihedioha J.I. Occurrence of wounds in Nigerian horses.. J. Appl. Anim. Welf. Sci. 2017;20:372–380.
- Theoret C.L, Bolwell C.F, Riley C. A cross-sectional survey on wounds in horses in New Zealand.. N. Z. Veter.-J. 2015;64:90–94.
- Theoret C.L, Wilmink J.M. Aberrant wound healing in the horse: Naturally occurring conditions reminiscent of those observed in man.. Wound Repair Regen. 2013;21:365–371.
- Textor J.A, Clark K.C, Walker N.J, Aristizobal F.A, Kol A, Lejeune S.S, Bledsoe A, Davidyan A, Gray S.N, Bohannon-Worsley L.K. Allogeneic stem cells alter gene expression and improve healing of distal limb wounds in horses.. Stem Cells Transl. Med. 2017;7:98–108.
- Gordillo G.M, Bernatchez S.F, Diegelmann R, Di Pietro L.A, Eriksson E, Hinz B, Hopf H, Kirsner R, Liu P, Parnell L.K. Preclinical models of wound healing: Is man the model? Proceedings of the wound healing society symposium.. Adv. Wound Care 2013;2:1–4.
- Harman R.M, Theoret C.L, Van De Walle G.R. The horse as a model for the study of cutaneous wound healing.. Adv. Wound Care 2019;10:381–399.
- Jacobs K.A, Leach D.H, Fretz P.B, Townsend H.G.G. Comparative aspects of the healing of excisional wounds on the leg and body of horses.. Veter.-Surg. 2008;13:83–90.
- Theoret C. Physiology of Wound Healing.. .
- Cochrane C.A, Pain R, Knottenbelt D.C. In-Vitro wound contraction in the horse: Differences between body and limb wounds.. Wounds 2003;15:175–181.
- Sardari K, Kazemi H, Emami M.R, Movasaghi A.R, Goli A.A. Role of collagen cross-linking on equine wound contraction and healing.. Comp. Haematol. Int. 2008;18:239–247.
- Davidson J.M, Yu F, Opalenik S.R. Splinting strategies to overcome confounding wound contraction in experimental animal models.. Adv. Wound Care 2013;2:142–148.
- Mogford J.E, Mustoe T.A. Experimental models of wound healing.. .
- Wilmink J.M, Weeren P.R, Stolk P.W.T, Mil F.N, Barneveld A. Differences in second-intention wound healing between horses and ponies: Histological aspects.. Equine Veter.-J. 1999;31:61–67.
- Bodaan C.J, Wise L.M, Wakelin K, Stuart G.S, Real N.C, Mercer A, Riley C, Theoret C. Short-term treatment of equine wounds with orf virus IL-10 and VEGF-E dampens inflammation and promotes repair processes without accelerating closure.. Wound Repair Regen. 2016;24:966–980.
- Beidler S.K, Douillet C.D, Berndt D.F, Keagy B.A, Rich P.B, Marston W.A. Inflammatory cytokine levels in chronic venous insufficiency ulcer tissue before and after compression therapy.. J. Vasc. Surg. 2009;49:1013–1020.
- Diegelmann R.F, Evans M.C. Wound healing: An overview of acute, fibrotic and delayed healing.. Front. Biosci. 2004;9:283–289.
- Jørgensen E, Hjerpe F.B, Hougen H.P, Bjarnsholt T, Berg L.C, Jacobsen S. Histologic changes and gene expression patterns in biopsy specimens from bacteria-inoculated and noninoculated excisional body and limb wounds in horses healing by second intention.. Am. J. Veter.-Res. 2020;81:276–284.
- Schreml S, Szeimies R, Prantl L, Karrer S, Landthaler M, Babilas P. Oxygen in acute and chronic wound healing.. Br. J. Dermatol. 2010;163:257–268.
- Jull A.B, Arroll B, Parag V, Waters J. Pentoxifylline for treating venous leg ulcers.. Cochrane Database Syst. Rev. 2012;12:CD001733.
- Beidler S.K, Douillet C.D, Berndt D.F, Keagy B.A, Rich P.B, Marston W.A. Multiplexed analysis of matrix metalloproteinases in leg ulcer tissue of patients with chronic venous insufficiency before and after compression therapy.. Wound Repair Regen. 2008;16:642–648.
- Hanson R.R. Complications of equine wound management and dermatologic surgery.. Veter.-Clin. N. Am. Equine Pract. 2008;24:663–696.
- Serra R, Grande R, Butrico L, Rossi A, Settimio U.F, Caroleo B, Amato B, Gallelli L, de Franciscis S. Chronic wound infections: The role of Pseudomonas aeruginosa and Staphylococcus aureus.. Expert Rev. Anti-infective Ther. 2015;13:605–613.
- Kirketerp-Møller K, Jensen P, Fazli M.M, Madsen K.G, Pedersen J, Moser C, Tolker-Nielsen T, Høiby N, Givskov M, Bjarnsholt T. Distribution, organization, and ecology of bacteria in chronic wounds.. J. Clin. Microbiol. 2008;46:2717–2722.
- Seth A.K, Geringer M.R, Hong S.J, Leung K.P, Mustoe T.A, Galiano R.D. In vivo modeling of biofilm-infected wounds: A review.. J. Surg. Res. 2012;178:330–338.
- Pastar I, Stojadinovic O, Yin N.C, Ramirez H, Nusbaum A.G, Sawaya A, Patel S.B, Khalid L, Isseroff R.R, Tomic-Canic M. Epithelialization in wound healing: A comprehensive review.. Adv. Wound Care 2014;3:445–464.
- Trøstrup H, Thomsen K, Calum H, Hoiby N, Moser C. Animal models of chronic wound care: The application of biofilms in clinical research.. Chronic Wound Care Manag. Res. 2016;3:123–132.
- Sullivan T.P, Eaglstein W.H, Davis S.C, Mertz P. The pig as a model for human wound healing.. Wound Repair Regen. 2001;9:66–76.
- Meyer W, Schwarz R, Neurand K. The skin of domestic mammals as a model for human skin, with speical reference to the domestic pig.. Curr. Probl. Dermatol. 1978;7:39–52.
- Klein P, Sojka M, Kucera J, Matonohova J, Pavlik V, Nemec J, Kubickova G, Slavkovsky R, Szuszkiewicz K, Danek P. A porcine model of skin wound infected with a polybacterial biofilm.. Biofouling 2018;34:226–236.
- Ganesh K, Sinha M, Mathew-Steiner S.S, Das A.K, Roy S, Sen C.K. Chronic wound biofilm model.. Adv. Wound Care 2015;4:382–388.
- Snyder R.J, Bohn G, Hanft J, Harkless L, Kim P, Lavery L, Schultz G, Wolcott R. Wound biofilm: Current perspectives and strategies on biofilm disruption and treatments.. Wounds 2017;29:S1–S17.
- Westgate S.J, Percival S.L, Knottenbelt D.C, Clegg P.D, Cochrane C.A. Chronic equine wounds: What is the role of infection and biofilms.. Wounds 2010;22:138–145.
- Bischofberger A.S, Dart C.M, Perkins N.R, Kelly A, Jeffcott L, Dart A.J. The effect of short- and long-term treatment with manuka honey on second intention healing of contaminated and noncontaminated wounds on the distal aspect of the forelimbs in horses.. Veter.-Surg. 2012;42:154–160.
- Hopf H.W, Rollins M.D. Wounds: An overview of the role of oxygen.. Antioxid. Redox Signal. 2007;9:1183–1192.
- Alhede M, Bjarnsholt T, Jensen P, Phipps R.K, Moser C, Christophersen L, Christensen L.D, Van Gennip M, Parsek M, Høiby N. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes.. Microbiology 2009;155:3500–3508.
- Nadzir N.A.A, Zakaria Z, Adzahan N.M, Mayaki A.M. Antibiotic susceptibilities of biofilm producing bacteria isolated from horse wounds.. Explor. Anim. Med. Res. 2020;10:42–49.
- Johani K, Malone M, Jensen S, Gosbell I, Dickson H, Hu H, Vickery K. Microscopy visualisation confirms multi-species biofilms are ubiquitous in diabetic foot ulcers.. Int. Wound J. 2017;14:1160–1169.
- Barker J.C, Khansa I, Gordillo G.M. A formidable foe is sabotaging your results: What you should know about biofilms and wound healing.. Plast. Reconstr. Surg. 2017;139:1184e–1194e.
- Percival S, Vuotto C, Donelli G, Lipsky B.A. Biofilms and wounds: An identification algorithm and potential treatment options.. Adv. Wound Care 2015;4:389–397.
- Thomsen T.R, Aasholm M.S, Rudkjøbing V.B, Saunders A.M, Bjarnsholt T, Givskov M, Kirketerp-Møller K, Nielsen P.H. The bacteriology of chronic venous leg ulcer examined by culture-independent molecular methods.. Wound Repair Regen. 2010;18:38–49.
- Price L.B, Liu C.M, Frankel Y.M, Melendez J.H, Aziz M, Buchhagen J, Contente-Cuomo T, Engelthaler D.M, Keim P.S, Ravel J. Macroscale spatial variation in chronic wound microbiota: A cross-sectional study.. Wound Repair Regen. 2010;19:80–88.
- Xu Y, Moser C, Abu Al-Soud W, Sørensen S, Høiby N, Nielsen P.H, Thomsen T.R. Culture-dependent and -independent investigations of microbial diversity on urinary catheters.. J. Clin. Microbiol. 2012;50:3901–3908.
- Høiby N, Bjarnsholt T, Moser C, Bassi G, Coenye T, Donelli G, Hall-Stoodley L, Holá V, Imbert C, Kirketerp-Møller K. ESCMID guideline for the diagnosis and treatment of biofilm infections 2014.. Clin. Microbiol. Infect. 2015;21:S1–S25.
- Hill K, Davies C, Wilson M, Stephens P, Harding K, Thomas D. Molecular analysis of the microflora in chronic venous leg ulceration.. J. Med. Microbiol. 2003;52:365–369.
- Penterman J, Nguyen D, Anderson E, Staudinger B.J, Greenberg E.P, Lam J.S, Singh P.K. Rapid evolution of culture-impaired bacteria during adaptation to biofilm growth.. Cell Rep. 2014;6:293–300.
- O’Meara S, Nelson E.A, Golder S, Dalton J.E, Craig D, Iglesias C. Systematic review of methods to diagnose infection in foot ulcers in diabetes.. Diabet. Med. 2006;23:341–347.
- Gardner S.E, Frantz R.A, Saltzman C.L, Hillis S, Park H, Scherubel M. Diagnostic validity of three swab techniques for identifying chronic wound infection.. Wound Repair Regen. 2006;14:548–557.
- Rondas A.A.L.M, Schols J.M.G.A, Halfens R.J.G, Stobberingh E.E. Swab versus biopsy for the diagnosis of chronic infected wounds.. Adv. Ski. Wound Care. 2013;26:211–219.
- Levine N.S, Lindberg R.B, Mason A.D, Pruitt B.A. The quantitative swab culture and smear: A quick, simple method for determining the number of viable aerobic bacteria on open wounds.. J. Trauma Inj. Infect. Crit. Care. 1976;16:89–94.
- Bonham P.A. Swab cultures for diagnosing wound infections: A literature review and clinical guideline.. J. Wound Ostomy Cont. Nurs. 2009;36:389–395.
- Saegeman V, Flamaing J, Muller J, Peetermans W.E, Stuyck J, Verhaegen J. Clinical evaluation of the Copan ESwab for methicillin-resistant Staphylococcus aureus detection and culture of wounds.. Eur. J. Clin. Microbiol. Infect. Dis. 2011;30:943–949.
- Kalan L.R, Meisel J.S, Loesche M, Horwinski J, Soaita I, Chen X, Uberoi A, Gardner S.E, Grice E.A. Strain- and species-level variation in the microbiome of diabetic wounds is associated with clinical outcomes and therapeutic efficacy.. Cell Host Microbe. 2019;25:641–655.e5.
- Wolcott R.D, Hanson J.D, Rees E.J, Koenig L.D, Phillips C, Wolcott R.A, Cox S.B, White J.S. Analysis of the chronic wound microbiota of 2,963 patients by 16S rDNA pyrosequencing.. Wound Repair Regen. 2015;24:163–174.
- Burmølle M, Thomsen T.R, Fazli M.M, Dige I, Christensen L, Homøe P, Tvede M, Nyvad B, Tolker-Nielsen T, Givskov M. Biofilms in chronic infections—A matter of opportunity—Monospecies biofilms in multispecies infections.. FEMS Immunol. Med. Microbiol. 2010;59:324–336.
- Malic S, Hill K.E, Hayes A, Percival S, Thomas D, Williams D. Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA FISH). Microbiology 2009;155:2603–2611.
- Jacobsen S. Topical Wound Treatments and Wound-Care Products.. .
- Coenye T, Kjellerup B, Stoodley P, Bjarnsholt T. The future of biofilm research—Report on the ‘2019 Biofilm Bash’.. Biofilm 2019;2:100012.
- Nakagami G, Schultz G, Kitamura A, Minematsu T, Akamata K, Suga H, Kurita M, Hayashi C, Sanada H. Rapid detection of biofilm by wound blotting following sharp debridement of chronic pressure ulcers predicts wound healing: A preliminary study.. Int. Wound J. 2019;17:191–196.
- Ashrafi M, Novak-Frazer L, Bates M, Baguneid M, Alonso-Rasgado T, Xia G, Rautemaa-Richardson R, Bayat A. Validation of biofilm formation on human skin wound models and demonstration of clinically translatable bacteria-specific volatile signatures.. Sci. Rep. 2018;8:9431.
- Dowd S, Wolcott R, Kennedy J, Jones C, Cox S. Molecular diagnostics and personalised medicine in wound care: Assessment of outcomes.. J. Wound Care 2011;20:232–239.
- Howell-Jones R.S, Wilson M.J, Hill K.E, Howard A.J, Price P.E, Thomas D. A review of the microbiology, antibiotic usage and resistance in chronic skin wounds.. J. Antimicrob. Chemother. 2005;55:143–149.
- Lipsky B.A, Berendt A.R, Cornia P.B, Pile J.C, Peters E.J.G, Armstrong D.G, Deery H.G, Embil J.M, Joseph W.S, Karchmer A.W. Executive summary: 2012 infectious diseases society of america clinical practice guideline for the diagnosis and treatment of diabetic foot infectionsa.. Clin. Infect. Dis. 2012;54:1679–1684.
- Robson M.C, Edstrom L.E, Krizek T.J, Groskin M.G. The efficacy of systemic antibiotics in the treatment of granulating wounds.. J. Surg. Res. 1974;16:299–306.
- McCullough C.J, Wheeler M.H, Neale M.L, Heard G.E. The influence of penicillin on experimental wound contamination with staphylococci: Studies with chromic catgut and monofilament nylon closure.. BJS 1977;64:120–124.
- Wolcott R, Rumbaugh K, James G, Schultz G, Phillips P, Yang Q, Watters C, Stewart P, Dowd S. Biofilm maturity studies indicate sharp debridement opens a time-dependent therapeutic window.. J. Wound Care 2010;19:320–328.
- Malone M, Swanson T. Biofilm-based wound care: The importance of debridement in biofilm treatment strategies.. Br. J. Community Nurs. 2017;22:S20–S25.
- Edwards J, Stapley S. Debridement of diabetic foot ulcers.. Cochrane Database Syst. Rev. 2010;2010:CD003556.
- Elraiyah T, Domecq J.P, Prutsky G, Tsapas A, Nabhan M, Frykberg R.G, Hasan R, Firwana B, Prokop L.J, Murad M.H. A systematic review and meta-analysis of débridement methods for chronic diabetic foot ulcers.. J. Vasc. Surg. 2016;63:37S–45S.e2.
- Skärlina E.M, Wilmink J.M, Fall N, Gorvy D.A. Effectiveness of conventional and hydrosurgical debridement methods in reducing Staphylococcus aureus inoculation of equine musclein vitro.. Equine Veter.-J. 2014;47:218–222.
- Schwarzer S, James G, Goeres D, Bjarnsholt T, Vickery K, Percival S, Stoodley P, Schultz G, Jensen S, Malone M. The efficacy of topical agents used in wounds for managing chronic biofilm infections: A systematic review.. J. Infect. 2019;80:261–270.
- Freeman S.L, Ashton N.M, Elce Y.A, Hammond A, Hollis A.R, Quinn G. BEVA primary care clinical guidelines: Wound management in the horse.. Equine Veter.-J. 2020;53:18–29.
- Bjarnsholt T, Alhede M, Jensen P, Nielsen A.K, Johansen H.K, Homøe P, Høiby N, Givskov M, Kirketerp-Møller K. Antibiofilm properties of acetic acid.. Adv. Wound Care 2015;4:363–372.
- Bradley B.H, Cunningham M. Biofilms in chronic wounds and the potential role of negative pressure wound therapy: An integrative review.. J. Wound Ostomy Cont. Nurs. 2013;40:143–149.
- Li T, Zhang L, Han L, Wang G, Yin P, Li Z, Zhang L, Guoqi W, Liu D, Tang P. Early application of negative pressure wound therapy to acute wounds contaminated with Staphylococcus aureus: An effective approach to preventing biofilm formation.. Exp. Ther. Med. 2016;11:769–776.
- Bjarnsholt T, Tolker-Nielsen T, Høiby N, Givskov M. Interference of Pseudomonas aeruginosa signalling and biofilm formation for infection control.. Expert Rev. Mol. Med. 2010;12:e11.
- Burian E.A, Sabah L, Kirketerp-Møller K, Ibstedt E, Fazli M.M, Gundersen G. The safety and antimicrobial properties of stabilized hypochlorous acid in acetic acid buffer for the treatment of acute wounds—A human pilot study and in vitro data.. Int. J. Low. Extrem. Wounds. 2021.
- Bourély C, Cazeau G, Jarrige N, Leblond A, Madec J, Haenni M, Gay E. Antimicrobial resistance patterns of bacteria isolated from dogs with otitis.. Epidemiol. Infect. 2019;147:e121.
- Woo K.Y, Sibbald R.G. A cross-sectional validation study of using NERDS and STONEES to assess bacterial burden.. Ostomy Wound Manag. 2009;55:40.
- Haalboom M, Blokhuis-Arkes M.H, Beuk R.J, Klont R, Guebitz G, Heinzle A, Van Der Palen J. Wound swab and wound biopsy yield similar culture results.. Wound Repair Regen. 2018;26:192–199.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists