FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / J Clin Microbiol / In Vitro Efficacy of Nonantibiotic Treatments on Biofilm Dis...
Journal of clinical microbiology2015; 54(3); 631-639; doi: 10.1128/JCM.02861-15

In Vitro Efficacy of Nonantibiotic Treatments on Biofilm Disruption of Gram-Negative Pathogens and an In Vivo Model of Infectious Endometritis Utilizing Isolates from the Equine Uterus.

Abstract: In this study, we evaluated the ability of the equine clinical treatments N-acetylcysteine, EDTA, and hydrogen peroxide to disrupt in vitro biofilms and kill equine reproductive pathogens (Escherichia coli, Pseudomonas aeruginosa, or Klebsiella pneumoniae) isolated from clinical cases. N-acetylcysteine (3.3%) decreased biofilm biomass and killed bacteria within the biofilms of E. coli isolates. The CFU of recoverable P. aeruginosa and K. pneumoniae isolates were decreased, but the biofilm biomass was unchanged. Exposure to hydrogen peroxide (1%) decreased the biofilm biomass and reduced the CFU of E. coli isolates, K. pneumoniae isolates were observed to have a reduction in CFU, and minimal effects were observed for P. aeruginosa isolates. Chelating agents (EDTA formulations) reduced E. coli CFU but were ineffective at disrupting preformed biofilms or decreasing the CFU of P. aeruginosa and K. pneumoniae within a biofilm. No single nonantibiotic treatment commonly used in equine veterinary practice was able to reduce the CFU and biofilm biomass of all three Gram-negative species of bacteria evaluated. An in vivo equine model of infectious endometritis was also developed to monitor biofilm formation, utilizing bioluminescence imaging with equine P. aeruginosa isolates from this study. Following infection, the endometrial surface contained focal areas of bacterial growth encased in a strongly adherent "biofilm-like" matrix, suggesting that biofilms are present during clinical cases of infectious equine endometritis. Our results indicate that Gram-negative bacteria isolated from the equine uterus are capable of producing a biofilm in vitro, and P. aeruginosa is capable of producing biofilm-like material in vivo.
Copyright © 2016, American Society for Microbiology. All Rights Reserved.
Get Full Text
Publication Date: 2015-12-30 PubMed ID: 26719448PubMed Central: PMC4768000DOI: 10.1128/JCM.02861-15Google 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.
LinkedInCopy
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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 study explores how various non-antibiotic treatments such as N-acetylcysteine, EDTA, and hydrogen peroxide affect the biofilms of Gram-negative bacteria that cause reproductive infections in horses. It also introduces a new in vivo model to observe biofilm formation in horses. However, none of these non-antibiotic methods were found to be completely effective against all three studied bacterial species.

Objective of the Study

  • The main aim of this study was to evaluate the in vitro effectiveness of non-antibiotic treatments (N-acetylcysteine, EDTA, and hydrogen peroxide) in disrupting biofilms and eliminating equine reproductive pathogens such as Escherichia coli, Pseudomonas aeruginosa, and Klebsiella pneumoniae.
  • In addition, an in vivo model of infectious endometritis was developed, using equine P. aeruginosa isolates, to study and monitor biofilm formation.

Procedure and Findings

  • The researchers discovered that a 3.3% concentration of N-acetylcysteine could decrease the biofilm biomass of E. coli and kill the bacteria within the biofilms. However, while it reduced the amount of recoverable P. aeruginosa and K. pneumoniae, it did not change their biofilm biomass.
  • Hydrogen peroxide (1%) was found to reduce both the biofilm biomass and the amount of recoverable E. coli and K. pneumoniae. However, its effects on P. aeruginosa were minimal.
  • The use of chelating agents such as EDTA formulations was able to reduce E. coli presence but had no effect on altering preformed biofilms or in decreasing the amount of P. aeruginosa and K. pneumoniae within a biofilm.
  • Regrettably, no single non-antibiotic treatment commonly used in equine veterinary practice was able to reduce both the amount of bacteria and the biofilm biomass for all three Gram-negative species evaluated in the study.

Development of an in vivo model

  • As a part of the study, an in vivo equine model of infectious endometritis was also created. This was done by infecting horses with P. aeruginosa and monitoring the formation of biofilms using bioluminescence imaging. The results provided evidence that biofilms are present during clinical cases of infectious equine endometritis.
  • This confirms that Gram-negative bacteria isolated from the equine uterus have the capability to produce a biofilm in vitro and, notably, that P. aeruginosa can produce biofilm-like material in vivo.

Cite This Article

APA
Ferris RA, McCue PM, Borlee GI, Loncar KD, Hennet ML, Borlee BR. (2015). In Vitro Efficacy of Nonantibiotic Treatments on Biofilm Disruption of Gram-Negative Pathogens and an In Vivo Model of Infectious Endometritis Utilizing Isolates from the Equine Uterus. J Clin Microbiol, 54(3), 631-639. https://doi.org/10.1128/JCM.02861-15

Publication

Journal of clinical microbiology
ISSN: 1098-660X
NlmUniqueID: 7505564
Country: United States
Language: English
Volume: 54
Issue: 3
Pages: 631-639

Researcher Affiliations

Ferris, Ryan A
  • Department of Clinical Sciences, Colorado State University, Fort Collins, Colorado, USA rferris@colostate.edu brad.borlee@colostate.edu.
McCue, Patrick M
  • Department of Clinical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Borlee, Grace I
  • Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
Loncar, Kristen D
  • Department of Clinical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Hennet, Margo L
  • Department of Clinical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Borlee, Bradley R
  • Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA rferris@colostate.edu brad.borlee@colostate.edu.

MeSH Terms

  • Acetylcysteine / pharmacology
  • Animals
  • Anti-Infective Agents / pharmacology
  • Biofilms / drug effects
  • Biofilms / growth & development
  • Biomass
  • Disease Models, Animal
  • Edetic Acid / pharmacology
  • Endometritis / drug therapy
  • Endometritis / microbiology
  • Female
  • Gram-Negative Bacteria / isolation & purification
  • Gram-Negative Bacteria / physiology
  • Horses
  • Hydrogen Peroxide / pharmacology
  • Luminescent Measurements
  • Microbial Viability / drug effects
  • Staining and Labeling / methods
  • Uterus / microbiology

References

This article includes 65 references
  1. Causey RC. Making sense of equine uterine infections: the many faces of physical clearance.. Vet J 2006 Nov;172(3):405-21.
    doi: 10.1016/j.tvjl.2005.08.005pubmed: 16169264google scholar: lookup
  2. Riddle WT, LeBlanc MM, Stromberg AJ. Relationships between uterine culture, cytology and pregnancy rates in a Thoroughbred practice.. Theriogenology 2007 Aug;68(3):395-402.
    doi: 10.1016/j.theriogenology.2007.05.050pubmed: 17583785google scholar: lookup
  3. Frontoso R, De Carlo E, Pasolini MP, van der Meulen K, Pagnini U, Iovane G, De Martino L. Retrospective study of bacterial isolates and their antimicrobial susceptibilities in equine uteri during fertility problems.. Res Vet Sci 2008 Feb;84(1):1-6.
    doi: 10.1016/j.rvsc.2007.02.008pubmed: 17434193google scholar: lookup
  4. LeBlanc MM, Causey RC. Clinical and subclinical endometritis in the mare: both threats to fertility.. Reprod Domest Anim 2009 Sep;44 Suppl 3:10-22.
    pubmed: 19660076doi: 10.1111/j.1439-0531.2009.01485.xgoogle scholar: lookup
  5. LeBlanc MM. Advances in the diagnosis and treatment of chronic infectious and post-mating-induced endometritis in the mare.. Reprod Domest Anim 2010 Jun;45 Suppl 2:21-7.
    pubmed: 20591061doi: 10.1111/j.1439-0531.2010.01634.xgoogle scholar: lookup
  6. LeBlanc MM. The current status of antibiotic use in equine reproduction. Equine Vet Educ 21:156–167.
    doi: 10.2746/095777308X357621google scholar: lookup
  7. Jefferson KK, Goldmann DA, Pier GB. Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms.. Antimicrob Agents Chemother 2005 Jun;49(6):2467-73.
    doi: 10.1128/AAC.49.6.2467-2473.2005pmc: PMC1140491pubmed: 15917548google scholar: lookup
  8. Brown MR, Allison DG, Gilbert P. Resistance of bacterial biofilms to antibiotics: a growth-rate related effect?. J Antimicrob Chemother 1988 Dec;22(6):777-80.
    doi: 10.1093/jac/22.6.777pubmed: 3072331google scholar: lookup
  9. Anwar H, Strap JL, Costerton JW. Establishment of aging biofilms: possible mechanism of bacterial resistance to antimicrobial therapy.. Antimicrob Agents Chemother 1992 Jul;36(7):1347-51.
    doi: 10.1128/AAC.36.7.1347pmc: PMC191585pubmed: 1510427google scholar: lookup
  10. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms.. Lancet 2001 Jul 14;358(9276):135-8.
    doi: 10.1016/S0140-6736(01)05321-1pubmed: 11463434google scholar: lookup
  11. Borriello G, Werner E, Roe F, Kim AM, Ehrlich GD, Stewart PS. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms.. Antimicrob Agents Chemother 2004 Jul;48(7):2659-64.
    doi: 10.1128/AAC.48.7.2659-2664.2004pmc: PMC434183pubmed: 15215123google scholar: lookup
  12. Shah D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K. Persisters: a distinct physiological state of E. coli.. BMC Microbiol 2006 Jun 12;6:53.
    pmc: PMC1557402pubmed: 16768798doi: 10.1186/1471-2180-6-53google scholar: lookup
  13. Jensen ET, Kharazmi A, Lam K, Costerton JW, Høiby N. Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms.. Infect Immun 1990 Jul;58(7):2383-5.
    pmc: PMC258823pubmed: 2114367doi: 10.1128/iai.58.7.2383-2385.1990google scholar: lookup
  14. Thurlow LR, Hanke ML, Fritz T, Angle A, Aldrich A, Williams SH, Engebretsen IL, Bayles KW, Horswill AR, Kielian T. Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo.. J Immunol 2011 Jun 1;186(11):6585-96.
    doi: 10.4049/jimmunol.1002794pmc: PMC3110737pubmed: 21525381google scholar: lookup
  15. Anderl JN, Franklin MJ, Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin.. Antimicrob Agents Chemother 2000 Jul;44(7):1818-24.
    doi: 10.1128/AAC.44.7.1818-1824.2000pmc: PMC89967pubmed: 10858336google scholar: lookup
  16. Anderl JN, Zahller J, Roe F, Stewart PS. Role of nutrient limitation and stationary-phase existence in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin.. Antimicrob Agents Chemother 2003 Apr;47(4):1251-6.
    doi: 10.1128/AAC.47.4.1251-1256.2003pmc: PMC152508pubmed: 12654654google scholar: lookup
  17. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections.. Science 1999 May 21;284(5418):1318-22.
    doi: 10.1126/science.284.5418.1318pubmed: 10334980google scholar: lookup
  18. Donlan RM. Biofilm elimination on intravascular catheters: important considerations for the infectious disease practitioner.. Clin Infect Dis 2011 Apr 15;52(8):1038-45.
    doi: 10.1093/cid/cir077pubmed: 21460321google scholar: lookup
  19. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms.. Clin Microbiol Rev 2002 Apr;15(2):167-93.
    doi: 10.1128/CMR.15.2.167-193.2002pmc: PMC118068pubmed: 11932229google scholar: lookup
  20. Mah TF, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents.. Trends Microbiol 2001 Jan;9(1):34-9.
    doi: 10.1016/S0966-842X(00)01913-2pubmed: 11166241google scholar: lookup
  21. Licking E. Getting a grip on bacterial slime. Business Week 13 September:98–100.
  22. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. Microbial biofilms.. Annu Rev Microbiol 1995;49:711-45.
    doi: 10.1146/annurev.mi.49.100195.003431pubmed: 8561477google scholar: lookup
  23. Archibald LK, Gaynes RP. Hospital-acquired infections in the United States. The importance of interhospital comparisons.. Infect Dis Clin North Am 1997 Jun;11(2):245-55.
    doi: 10.1016/S0891-5520(05)70354-8pubmed: 9187945google scholar: lookup
  24. Potera C. Forging a link between biofilms and disease.. Science 1999 Mar 19;283(5409):1837, 1839.
    doi: 10.1126/science.283.5409.1837pubmed: 10206887google scholar: lookup
  25. Westgate SJ, Percival SL, Knottenbelt DC, Clegg PD, Cochrane CA. Microbiology of equine wounds and evidence of bacterial biofilms.. Vet Microbiol 2011 May 12;150(1-2):152-9.
    doi: 10.1016/j.vetmic.2011.01.003pubmed: 21273008google scholar: lookup
  26. Swidsinski A, Verstraelen H, Loening-Baucke V, Swidsinski S, Mendling W, Halwani Z. Presence of a polymicrobial endometrial biofilm in patients with bacterial vaginosis.. PLoS One 2013;8(1):e53997.
    doi: 10.1371/journal.pone.0053997pmc: PMC3540019pubmed: 23320114google scholar: lookup
  27. van Baar BL. Characterisation of bacteria by matrix-assisted laser desorption/ionisation and electrospray mass spectrometry.. FEMS Microbiol Rev 2000 Apr;24(2):193-219.
    doi: 10.1016/S0168-6445(99)00036-4pubmed: 10717314google scholar: lookup
  28. Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A. The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms.. J Clin Microbiol 1999 Jun;37(6):1771-6.
    pmc: PMC84946pubmed: 10325322doi: 10.1128/jcm.37.6.1771-1776.1999google scholar: lookup
  29. Borlee BR, Goldman AD, Murakami K, Samudrala R, Wozniak DJ, Parsek MR. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix.. Mol Microbiol 2010 Feb;75(4):827-42.
    doi: 10.1111/j.1365-2958.2009.06991.xpmc: PMC2847200pubmed: 20088866google scholar: lookup
  30. Tetz GV, Artemenko NK, Tetz VV. Effect of DNase and antibiotics on biofilm characteristics.. Antimicrob Agents Chemother 2009 Mar;53(3):1204-9.
    doi: 10.1128/AAC.00471-08pmc: PMC2650517pubmed: 19064900google scholar: lookup
  31. Quinn GA, Maloy AP, Banat MM, Banat IM. A comparison of effects of broad-spectrum antibiotics and biosurfactants on established bacterial biofilms.. Curr Microbiol 2013 Nov;67(5):614-23.
    doi: 10.1007/s00284-013-0412-8pubmed: 23783562google scholar: lookup
  32. Sieuwerts S, de Bok FA, Mols E, de vos WM, Vlieg JE. A simple and fast method for determining colony forming units.. Lett Appl Microbiol 2008 Oct;47(4):275-8.
    doi: 10.1111/j.1472-765X.2008.02417.xpubmed: 18778376google scholar: lookup
  33. Gores-Lindholm AR, LeBlanc MM, Causey R, Hitchborn A, Fayrer-Hosken RA, Kruger M, Vandenplas ML, Flores P, Ahlschwede S. Relationships between intrauterine infusion of N-acetylcysteine, equine endometrial pathology, neutrophil function, post-breeding therapy, and reproductive performance.. Theriogenology 2013 Aug;80(3):218-27.
    doi: 10.1016/j.theriogenology.2013.03.026pubmed: 23623166google scholar: lookup
  34. Leblanc MM, McKinnon AO. Breeding the problem mare. p 2620–2642.
  35. Youngquist RS, Blanchard TL, Lapin D, Klein W. The effects of EDTA-Tris infusion on the equine endometrium.. Theriogenology 1984 Nov;22(5):593-9.
    doi: 10.1016/0093-691X(84)90059-1pubmed: 16725992google scholar: lookup
  36. Maestre JR, Mateo M, Méndez ML, Aguilar L, Gimenez MJ, Alou L, Coronel P, Granizo JJ, Prieto J. In vitro interference of beta-lactams with biofilm development by prevalent community respiratory tract isolates.. Int J Antimicrob Agents 2010 Mar;35(3):274-7.
    doi: 10.1016/j.ijantimicag.2009.10.020pubmed: 20031375google scholar: lookup
  37. DeShazer D, Woods DE. Broad-host-range cloning and cassette vectors based on the R388 trimethoprim resistance gene.. Biotechniques 1996 May;20(5):762-4.
    pubmed: 8723912doi: 10.2144/96205bm05google scholar: lookup
  38. Choi KH, Gaynor JB, White KG, Lopez C, Bosio CM, Karkhoff-Schweizer RR, Schweizer HP. A Tn7-based broad-range bacterial cloning and expression system.. Nat Methods 2005 Jun;2(6):443-8.
    doi: 10.1038/nmeth765pubmed: 15908923google scholar: lookup
  39. Choi KH, Schweizer HP. mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa.. Nat Protoc 2006;1(1):153-61.
    doi: 10.1038/nprot.2006.24pubmed: 17406227google scholar: lookup
  40. López CM, Rholl DA, Trunck LA, Schweizer HP. Versatile dual-technology system for markerless allele replacement in Burkholderia pseudomallei.. Appl Environ Microbiol 2009 Oct;75(20):6496-503.
    doi: 10.1128/AEM.01669-09pmc: PMC2765137pubmed: 19700544google scholar: lookup
  41. Choi KH, Mima T, Casart Y, Rholl D, Kumar A, Beacham IR, Schweizer HP. Genetic tools for select-agent-compliant manipulation of Burkholderia pseudomallei.. Appl Environ Microbiol 2008 Feb;74(4):1064-75.
    doi: 10.1128/AEM.02430-07pmc: PMC2258562pubmed: 18156318google scholar: lookup
  42. Hinrichs K, Spensley MS, McDonough PL. Evaluation of progesterone treatment to create a model for equine endometritis.. Equine Vet J 1992 Nov;24(6):457-61.
    doi: 10.1111/j.2042-3306.1992.tb02876.xpubmed: 1459059google scholar: lookup
  43. James GA, Swogger E, Wolcott R, Pulcini Ed, Secor P, Sestrich J, Costerton JW, Stewart PS. Biofilms in chronic wounds.. Wound Repair Regen 2008 Jan-Feb;16(1):37-44.
    doi: 10.1111/j.1524-475X.2007.00321.xpubmed: 18086294google scholar: lookup
  44. Saye DE. Recurring and antimicrobial-resistant infections:considering the potential role of biofilms in clinical practice.. Ostomy Wound Manage 2007 Apr;53(4):46-8, 50, 52 passim.
    pubmed: 17449916
  45. Davis SC, Ricotti C, Cazzaniga A, Welsh E, Eaglstein WH, Mertz PM. Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo.. Wound Repair Regen 2008 Jan-Feb;16(1):23-9.
    doi: 10.1111/j.1524-475X.2007.00303.xpubmed: 18211576google scholar: lookup
  46. Lindsay D, von Holy A. Bacterial biofilms within the clinical setting: what healthcare professionals should know.. J Hosp Infect 2006 Dec;64(4):313-25.
    doi: 10.1016/j.jhin.2006.06.028pubmed: 17046102google scholar: lookup
  47. Percival SL, Knapp JS, Edyvean R, Wales DS. Biofilm development on stainless steel in mains water. Water Res 32:243–253.
    doi: 10.1016/S0043-1354(97)00132-2google scholar: lookup
  48. ten Cate JM. Biofilms, a new approach to the microbiology of dental plaque.. Odontology 2006 Sep;94(1):1-9.
    doi: 10.1007/s10266-006-0063-3pubmed: 16998612google scholar: lookup
  49. Ghosh A, Borst L, Stauffer SH, Suyemoto M, Moisan P, Zurek L, Gookin JL. Mortality in kittens is associated with a shift in ileum mucosa-associated enterococci from Enterococcus hirae to biofilm-forming Enterococcus faecalis and adherent Escherichia coli.. J Clin Microbiol 2013 Nov;51(11):3567-78.
    doi: 10.1128/JCM.00481-13pmc: PMC3889735pubmed: 23966487google scholar: lookup
  50. Olson ME, Ceri H, Morck DW, Buret AG, Read RR. Biofilm bacteria: formation and comparative susceptibility to antibiotics.. Can J Vet Res 2002 Apr;66(2):86-92.
    pmc: PMC226988pubmed: 11989739
  51. Zhao T, Liu Y. N-acetylcysteine inhibit biofilms produced by Pseudomonas aeruginosa.. BMC Microbiol 2010 May 12;10:140.
    doi: 10.1186/1471-2180-10-140pmc: PMC2882372pubmed: 20462423google scholar: lookup
  52. Quah SY, Wu S, Lui JN, Sum CP, Tan KS. N-acetylcysteine inhibits growth and eradicates biofilm of Enterococcus faecalis.. J Endod 2012 Jan;38(1):81-5.
    doi: 10.1016/j.joen.2011.10.004pubmed: 22152626google scholar: lookup
  53. Dinicola S, De Grazia S, Carlomagno G, Pintucci JP. N-acetylcysteine as powerful molecule to destroy bacterial biofilms. A systematic review.. Eur Rev Med Pharmacol Sci 2014 Oct;18(19):2942-8.
    pubmed: 25339490
  54. Olofsson AC, Hermansson M, Elwing H. N-acetyl-L-cysteine affects growth, extracellular polysaccharide production, and bacterial biofilm formation on solid surfaces.. Appl Environ Microbiol 2003 Aug;69(8):4814-22.
    doi: 10.1128/AEM.69.8.4814-4822.2003pmc: PMC169071pubmed: 12902275google scholar: lookup
  55. Perumal PK, Wand ME, Sutton JM, Bock LJ. Evaluation of the effectiveness of hydrogen-peroxide-based disinfectants on biofilms formed by Gram-negative pathogens.. J Hosp Infect 2014 Aug;87(4):227-33.
    doi: 10.1016/j.jhin.2014.05.004pubmed: 24957804google scholar: lookup
  56. Stewart PS, Roe F, Rayner J, Elkins JG, Lewandowski Z, Ochsner UA, Hassett DJ. Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms.. Appl Environ Microbiol 2000 Feb;66(2):836-8.
    doi: 10.1128/AEM.66.2.836-838.2000pmc: PMC91906pubmed: 10653761google scholar: lookup
  57. Orrù G, Del Nero S, Tuveri E, Laura Ciusa M, Pilia F, Erriu M, Orrù G, Liciardi M, Piras V, Denotti G. Evaluation of antimicrobial-antibiofilm activity of a hydrogen peroxide decontaminating system used in dental unit water lines.. Open Dent J 2010 Jul 20;4:140-6.
    doi: 10.2174/1874210601004010140pmc: PMC2948419pubmed: 21113279google scholar: lookup
  58. Brown CD, Zitelli JA. A review of topical agents for wounds and methods of wounding. Guidelines for wound management.. J Dermatol Surg Oncol 1993 Aug;19(8):732-7.
    doi: 10.1111/j.1524-4725.1993.tb00417.xpubmed: 8349913google scholar: lookup
  59. Vaara M. Agents that increase the permeability of the outer membrane.. Microbiol Rev 1992 Sep;56(3):395-411.
    pmc: PMC372877pubmed: 1406489doi: 10.1128/mr.56.3.395-411.1992google scholar: lookup
  60. Nikaido H, Vaara M. Molecular basis of bacterial outer membrane permeability.. Microbiol Rev 1985 Mar;49(1):1-32.
    pmc: PMC373015pubmed: 2580220doi: 10.1128/mr.49.1.1-32.1985google scholar: lookup
  61. Leive L. The barrier function of the gram-negative envelope.. Ann N Y Acad Sci 1974 May 10;235(0):109-29.
    doi: 10.1111/j.1749-6632.1974.tb43261.xpubmed: 4212391google scholar: lookup
  62. Hancock RE. Alterations in outer membrane permeability.. Annu Rev Microbiol 1984;38:237-64.
    doi: 10.1146/annurev.mi.38.100184.001321pubmed: 6093683google scholar: lookup
  63. Leive L. Release of lipopolysaccharide by EDTA treatment of E. coli.. Biochem Biophys Res Commun 1965 Nov 22;21(4):290-6.
    doi: 10.1016/0006-291X(65)90191-9pubmed: 4159978google scholar: lookup
  64. Kite P, Eastwood K, Sugden S, Percival SL. Use of in vivo-generated biofilms from hemodialysis catheters to test the efficacy of a novel antimicrobial catheter lock for biofilm eradication in vitro.. J Clin Microbiol 2004 Jul;42(7):3073-6.
    doi: 10.1128/JCM.42.7.3073-3076.2004pmc: PMC446317pubmed: 15243062google scholar: lookup
  65. Yi L, Wang Y, Ma Z, Zhang H, Li Y, Zheng JX, Yang YC, Fan HJ, Lu CP. Biofilm formation of Streptococcus equi ssp. zooepidemicus and comparative proteomic analysis of biofilm and planktonic cells.. Curr Microbiol 2014 Sep;69(3):227-33.
    doi: 10.1007/s00284-014-0574-zpubmed: 24696150google scholar: lookup

Citations

This article has been cited 22 times.
  1. Nocera FP, Maurizi L, Masullo A, Nicoletti M, Conte AL, Brunetti F, De Martino L, Zagaglia C, Longhi C. Genotypic and Phenotypic Characterization of Escherichia coli Isolates Recovered from the Uterus of Mares with Fertility Problems. Animals (Basel) 2023 May 14;13(10).
    doi: 10.3390/ani13101639pubmed: 37238068google scholar: lookup
  2. Nesse LL, Osland AM, Vestby LK. The Role of Biofilms in the Pathogenesis of Animal Bacterial Infections. Microorganisms 2023 Feb 28;11(3).
    doi: 10.3390/microorganisms11030608pubmed: 36985183google scholar: lookup
  3. Zhao Y, Zhu Y, Liu B, Mi J, Li N, Zhao W, Wu R, Holyoak GR, Li J, Liu D, Zeng S, Wang Y. Antimicrobial Susceptibility of Bacterial Isolates from Donkey Uterine Infections, 2018-2021. Vet Sci 2022 Feb 5;9(2).
    doi: 10.3390/vetsci9020067pubmed: 35202320google scholar: lookup
  4. Morrell JM, Rocha A. A Novel Approach to Minimising Acute Equine Endometritis That May Help to Prevent the Development of the Chronic State. Front Vet Sci 2021;8:799619.
    doi: 10.3389/fvets.2021.799619pubmed: 35071389google scholar: lookup
  5. Borlee GI, Lakin SM, Kapuscinski ML, Abdo Z, Stenglein MD, McCue PM, Borlee BR. Complete Genome Sequences of Eight Streptococcus equi subsp. zooepidemicus Strains Isolated from Mares in Estrus with Endometritis. Microbiol Resour Announc 2021 Jul;10(26):e0132120.
    doi: 10.1128/MRA.01321-20pubmed: 34197198google scholar: lookup
  6. Wang L, Zhang K, Zhang K, Zhang J, Fu J, Li J, Wang G, Qiu Z, Wang X, Li J. Antibacterial Activity of Cinnamomum camphora Essential Oil on Escherichia coli During Planktonic Growth and Biofilm Formation. Front Microbiol 2020;11:561002.
    doi: 10.3389/fmicb.2020.561002pubmed: 33304322google scholar: lookup
  7. Nunes TSBS, Rosa LM, Vega-Chacón Y, Mima EGO. Fungistatic Action of N-Acetylcysteine on Candida albicans Biofilms and Its Interaction with Antifungal Agents. Microorganisms 2020 Jun 30;8(7).
    doi: 10.3390/microorganisms8070980pubmed: 32629850google scholar: lookup
  8. Canisso IF, Segabinazzi LGTM, Fedorka CE. Persistent Breeding-Induced Endometritis in Mares - a Multifaceted Challenge: From Clinical Aspects to Immunopathogenesis and Pathobiology. Int J Mol Sci 2020 Feb 20;21(4).
    doi: 10.3390/ijms21041432pubmed: 32093296google scholar: lookup
  9. Vestby LK, Grønseth T, Simm R, Nesse LL. Bacterial Biofilm and its Role in the Pathogenesis of Disease. Antibiotics (Basel) 2020 Feb 3;9(2).
    doi: 10.3390/antibiotics9020059pubmed: 32028684google scholar: lookup
  10. Mangalea MR, Luna EK, Ziegle J, Chang C, Bosco-Lauth AM, Bowen RA, Leach JE, Borlee BR. Complete Genome Sequence of Pandoraea pnomenusa TF-18, a Multidrug-Resistant Organism Isolated from the Rhizosphere of Rice (Oryza sativa L. subsp. japonica). Microbiol Resour Announc 2020 Jan 2;9(1).
    doi: 10.1128/MRA.01008-19pubmed: 31896624google scholar: lookup
  11. Pollini S, Di Pilato V, Landini G, Di Maggio T, Cannatelli A, Sottotetti S, Cariani L, Aliberti S, Blasi F, Sergio F, Rossolini GM, Pallecchi L. In vitro activity of N-acetylcysteine against Stenotrophomonas maltophilia and Burkholderia cepacia complex grown in planktonic phase and biofilm. PLoS One 2018;13(10):e0203941.
    doi: 10.1371/journal.pone.0203941pubmed: 30273348google scholar: lookup
  12. Ferris RA, McCue PM, Borlee GI, Glapa KE, Martin KH, Mangalea MR, Hennet ML, Wolfe LM, Broeckling CD, Borlee BR. Model of Chronic Equine Endometritis Involving a Pseudomonas aeruginosa Biofilm. Infect Immun 2017 Dec;85(12).
    doi: 10.1128/IAI.00332-17pubmed: 28970274google scholar: lookup
  13. Mazzuchini MP, Canisso IF. The Apparent pH Stability of Antibiotic Preparations Used for Uterine Infusions in Mares. Animals (Basel) 2026 Jan 26;16(3).
    doi: 10.3390/ani16030382pubmed: 41681363google scholar: lookup
  14. Köhne M, Hüsch R, Peh E, Hirnet J, Tönissen A, Müsken M, Plötz M, Kittler S, Sieme H. Newly isolated bacteriophages show efficacy and phage-antibiotic synergy in vitro against the equine genital pathogens Klebsiella pneumoniae and Pseudomonas aeruginosa. BMC Vet Res 2025 Oct 3;21(1):568.
    doi: 10.1186/s12917-025-04989-1pubmed: 41044673google scholar: lookup
  15. Yáñez Ramil U, Jezierska S, Krupa M, Bogado Pascottini O. Fundamentals of microbiome-based therapies for reproductive tract inflammatory diseases in domestic animals. Anim Reprod 2025;22(3):e20250030.
    doi: 10.1590/1984-3143-AR2025-0030pubmed: 40933872google scholar: lookup
  16. Hardefeldt L, Thomas K, Page S, Norris J, Browning G, El Hage C, Stewart A, Gilkerson J, Muscatello G, Verwilghen D, van Galen G, Bauquier J, Cuming R, Reynolds B, Whittaker C, Wilkes E, Clulow J, Burden C, Begg L. Antimicrobial prescribing guidelines for horses in Australia. Aust Vet J 2025 Dec;103(12):781-889.
    doi: 10.1111/avj.70003pubmed: 40903020google scholar: lookup
  17. Köhne M, Hüsch R, Tönissen A, Schmidt M, Müsken M, Böttcher D, Hirnet J, Plötz M, Kittler S, Sieme H. Isolation and characterization of bacteriophages specific to Streptococcus equi subspecies zooepidemicus and evaluation of efficacy ex vivo. Front Microbiol 2024;15:1448958.
    doi: 10.3389/fmicb.2024.1448958pubmed: 39529671google scholar: lookup
  18. Mazzuchini MP, Lisboa FP, de Castro JI, Alvarenga MA, Segabinazzi LGTM, Canisso IF. In vitro antimicrobial activity of non-traditional therapies for infectious endometritis in mares. Equine Vet J 2025 Jul;57(4):1118-1126.
    doi: 10.1111/evj.14423pubmed: 39431554google scholar: lookup
  19. Leynaud V, Jousserand NP, Lucas MN, Cavalié L, Motta JP, Oswald É, Lavoué R. Adjunctive intravesical EDTA-tromethamine treatment of a biofilm-associated recurrent Escherichia coli cystitis in a dog. Can Vet J 2024 Sep;65(9):886-893.
    pubmed: 39219609
  20. Novello G, Souza FF, Canisso IF. Platelet-Rich Plasma Proteome of Mares Susceptible to Persistent-Breeding-Induced Endometritis Differs from Resistant Mares. Animals (Basel) 2024 Jul 18;14(14).
    doi: 10.3390/ani14142100pubmed: 39061562google scholar: lookup
  21. Zhang X, Gao Y, Mai Z, Li Y, Wang J, Zhao X, Zhang Y. Untargeted Metabolomic Analysis Reveals Plasma Differences between Mares with Endometritis and Healthy Ones. Animals (Basel) 2024 Jun 29;14(13).
    doi: 10.3390/ani14131933pubmed: 38998045google scholar: lookup
  22. Heil BA, van Heule M, Thompson SK, Kearns TA, Oberhaus EL, King G, Daels P, Dini P, Sones JL. Effect of Sampling Method on Detection of the Equine Uterine Microbiome during Estrus. Vet Sci 2023 Nov 8;10(11).
    doi: 10.3390/vetsci10110644pubmed: 37999467google scholar: lookup
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.