FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Infect Immun / Model of Chronic Equine Endometritis Involving a Pseudomonas...
Infection and immunity2017; 85(12); e00332-17; doi: 10.1128/IAI.00332-17

Model of Chronic Equine Endometritis Involving a Pseudomonas aeruginosa Biofilm.

Abstract: Bacteria in a biofilm community have increased tolerance to antimicrobial therapy. To characterize the role of biofilms in equine endometritis, six mares were inoculated with -engineered strains isolated from equine uterine infections. Following establishment of infection, the horses were euthanized and the endometrial surfaces were imaged for luminescence to localize adherent -labeled bacteria. Samples from the endometrium were collected for cytology, histopathology, carbohydrate analysis, and expression of inflammatory cytokine genes. Tissue-adherent bacteria were present in focal areas between endometrial folds (6/6 mares). The Pel exopolysaccharide (biofilm matrix component) and cyclic di-GMP (biofilm-regulatory molecule) were detected in 6/6 mares and 5/6 mares, respectively, from endometrial samples with tissue-adherent bacteria ( < 0.05). A greater incidence ( 0.05) in the number of inflammatory cells in the endometrium between areas with and without tissue-adherent bacteria. Neutrophils were decreased ( < 0.05) in areas surrounding tissue-adherent bacteria compared to those in areas free of adherent bacteria. Gene expression of interleukin-10, an immune-modulatory cytokine, was significantly ( < 0.05) increased in areas of tissue-adherent bacteria compared to that in endometrium absent of biofilm. These findings indicate that produces a biofilm in the uterus and that the host immune response is modulated focally around areas with biofilm, but inflammation within the tissue is similar in areas with and without biofilm matrix. Future studies will focus on therapeutic options for elimination of bacterial biofilm in the equine uterus.
Copyright © 2017 Ferris et al.
Get Full Text
Publication Date: 2017-11-17 PubMed ID: 28970274PubMed Central: PMC5695105DOI: 10.1128/IAI.00332-17Google 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

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.

The research focuses on understanding the role of biofilms, specifically from Pseudomonas aeruginosa, in chronic equine endometritis and how it affects the immune response in horses. It also helps in identifying the possible solution for bacterial biofilm elimination.

Experiment and Methodology

  • In the experiment, six mares were infected with Pseudomonas aeruginosa that were previously isolated from equine uterine infections.
  • The mares were euthanized post-infection to examine the endometrial surfaces and locate the bacteria.
  • Tests were conducted to determine different aspects of the infection and bacterial growth, including cytology, histopathology, carbohydrate analysis, and assessment of inflammatory cytokine genes’ expression.

Results and Findings

  • The researchers found bacteria in specific areas between endometrial folds in all the mares.
  • They detected Pel exopolysaccharide, a component of the biofilm matrix, in all mares, while cyclic di-GMP, a molecule that controls biofilm creation, was found in 5 out of the 6 mares.
  • These findings were statistically significant and suggested that Pseudomonas aeruginosa creates a biofilm in the uterine environment.
  • Importantly, the researchers established that Bouin’s solution is more effective at detecting bacteria adherent to the endometrium than buffered formalin.

Immune Response and Inflammation

  • There was no significant difference in the number of inflammatory cells in the endometrium between areas with and without bacteria.
  • However, there was a reduction in neutrophils, a type of white blood cell, surrounding areas with bacteria compared to those without bacteria.
  • The gene expression of interleukin-10, an inflammation-modulating cytokine, was significantly increased in areas with adherent bacteria compared to those without.
  • This indicates that the host immune response is altered around areas with biofilm, although the inflammation response within the tissue maintains similarity in areas with and without biofilm matrix.

Implication for Future Studies

  • This research provides crucial insights into how biofilms contribute to chronic equine endometritis and its impact on the host’s immune response.
  • Future research will aim to explore therapeutic options for eliminating bacterial biofilm in the equine uterus.

Cite This Article

APA
Ferris RA, McCue PM, Borlee GI, Glapa KE, Martin KH, Mangalea MR, Hennet ML, Wolfe LM, Broeckling CD, Borlee BR. (2017). Model of Chronic Equine Endometritis Involving a Pseudomonas aeruginosa Biofilm. Infect Immun, 85(12), e00332-17. https://doi.org/10.1128/IAI.00332-17

Publication

Infection and immunity
ISSN: 1098-5522
NlmUniqueID: 0246127
Country: United States
Language: English
Volume: 85
Issue: 12
PII: e00332-17

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.
Glapa, Kristina E
  • Department of Clinical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Martin, Kevin H
  • Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
Mangalea, Mihnea R
  • Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA.
Hennet, Margo L
  • Department of Clinical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Wolfe, Lisa M
  • Proteomics and Metabolomics Facility, Colorado State University, Fort Collins, Colorado, USA.
Broeckling, Corey D
  • Proteomics and Metabolomics Facility, 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

  • Animals
  • Biofilms / growth & development
  • Endometritis / microbiology
  • Endometritis / pathology
  • Endometrium / microbiology
  • Endometrium / pathology
  • Female
  • Genes, Reporter
  • Horse Diseases / microbiology
  • Horse Diseases / pathology
  • Horses
  • Luciferases / analysis
  • Luciferases / genetics
  • Pseudomonas Infections / microbiology
  • Pseudomonas Infections / pathology
  • Pseudomonas aeruginosa / genetics
  • Pseudomonas aeruginosa / physiology

References

This article includes 96 references
  1. Traub-Dargatz JL, Salman MD, Voss JL. Medical problems of adult horses, as ranked by equine practitioners.. J Am Vet Med Assoc 1991 May 15;198(10):1745-7.
    pubmed: 2071472
  2. 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.
    doi: 10.1111/j.1439-0531.2009.01485.xpubmed: 19660076google scholar: lookup
  3. Causey RC. Mucus and the mare: how little we know.. Theriogenology 2007 Aug;68(3):386-94.
    doi: 10.1016/j.theriogenology.2007.04.011pubmed: 17512579google scholar: lookup
  4. O'Toole G, Kaplan HB, Kolter R. Biofilm formation as microbial development.. Annu Rev Microbiol 2000;54:49-79.
    doi: 10.1146/annurev.micro.54.1.49pubmed: 11018124google scholar: lookup
  5. 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
  6. 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
  7. 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.
    pmc: PMC191585pubmed: 1510427doi: 10.1128/aac.36.7.1347google scholar: lookup
  8. 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
  9. 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
  10. 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.
    doi: 10.1186/1471-2180-6-53pmc: PMC1557402pubmed: 16768798google scholar: lookup
  11. 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
  12. 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
  13. Bjarnsholt T, Jensen PØ, Fiandaca MJ, Pedersen J, Hansen CR, Andersen CB, Pressler T, Givskov M, Høiby N. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients.. Pediatr Pulmonol 2009 Jun;44(6):547-58.
    doi: 10.1002/ppul.21011pubmed: 19418571google scholar: lookup
  14. Mustoe T. Understanding chronic wounds: a unifying hypothesis on their pathogenesis and implications for therapy.. Am J Surg 2004 May;187(5A):65S-70S.
    doi: 10.1016/S0002-9610(03)00306-4pubmed: 15147994google 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. 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
  17. 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
  18. 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
  19. 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
  20. Walters MC 3rd, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin.. Antimicrob Agents Chemother 2003 Jan;47(1):317-23.
    doi: 10.1128/AAC.47.1.317-323.2003pmc: PMC148957pubmed: 12499208google scholar: lookup
  21. Chiang WC, Pamp SJ, Nilsson M, Givskov M, Tolker-Nielsen T. The metabolically active subpopulation in Pseudomonas aeruginosa biofilms survives exposure to membrane-targeting antimicrobials via distinct molecular mechanisms.. FEMS Immunol Med Microbiol 2012 Jul;65(2):245-56.
    doi: 10.1111/j.1574-695X.2012.00929.xpubmed: 22251216google scholar: lookup
  22. Williamson KS, Richards LA, Perez-Osorio AC, Pitts B, McInnerney K, Stewart PS, Franklin MJ. Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population.. J Bacteriol 2012 Apr;194(8):2062-73.
    doi: 10.1128/JB.00022-12pmc: PMC3318454pubmed: 22343293google scholar: lookup
  23. 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
  24. Mann EE, Wozniak DJ. Pseudomonas biofilm matrix composition and niche biology.. FEMS Microbiol Rev 2012 Jul;36(4):893-916.
    doi: 10.1111/j.1574-6976.2011.00322.xpmc: PMC4409827pubmed: 22212072google scholar: lookup
  25. Byrd MS, Sadovskaya I, Vinogradov E, Lu H, Sprinkle AB, Richardson SH, Ma L, Ralston B, Parsek MR, Anderson EM, Lam JS, Wozniak DJ. Genetic and biochemical analyses of the Pseudomonas aeruginosa Psl exopolysaccharide reveal overlapping roles for polysaccharide synthesis enzymes in Psl and LPS production.. Mol Microbiol 2009 Aug;73(4):622-38.
    doi: 10.1111/j.1365-2958.2009.06795.xpmc: PMC4409829pubmed: 19659934google scholar: lookup
  26. Friedman L, Kolter R. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms.. Mol Microbiol 2004 Feb;51(3):675-90.
    doi: 10.1046/j.1365-2958.2003.03877.xpubmed: 14731271google scholar: lookup
  27. Matsukawa M, Greenberg EP. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development.. J Bacteriol 2004 Jul;186(14):4449-56.
    doi: 10.1128/JB.186.14.4449-4456.2004pmc: PMC438629pubmed: 15231776google scholar: lookup
  28. Linker A, Jones RS. A new polysaccharide resembling alginic acid isolated from pseudomonads.. J Biol Chem 1966 Aug 25;241(16):3845-51.
    pubmed: 5916397
  29. Harmsen M, Yang L, Pamp SJ, Tolker-Nielsen T. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal.. FEMS Immunol Med Microbiol 2010 Aug;59(3):253-68.
    doi: 10.1111/j.1574-695X.2010.00690.xpubmed: 20497222google scholar: lookup
  30. Yang L, Hengzhuang W, Wu H, Damkiaer S, Jochumsen N, Song Z, Givskov M, Høiby N, Molin S. Polysaccharides serve as scaffold of biofilms formed by mucoid Pseudomonas aeruginosa.. FEMS Immunol Med Microbiol 2012 Jul;65(2):366-76.
    doi: 10.1111/j.1574-695X.2012.00936.xpubmed: 22309122google scholar: lookup
  31. Ma L, Jackson KD, Landry RM, Parsek MR, Wozniak DJ. Analysis of Pseudomonas aeruginosa conditional psl variants reveals roles for the psl polysaccharide in adhesion and maintaining biofilm structure postattachment.. J Bacteriol 2006 Dec;188(23):8213-21.
    doi: 10.1128/JB.01202-06pmc: PMC1698210pubmed: 16980452google scholar: lookup
  32. Ghafoor A, Hay ID, Rehm BH. Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture.. Appl Environ Microbiol 2011 Aug;77(15):5238-46.
    doi: 10.1128/AEM.00637-11pmc: PMC3147449pubmed: 21666010google scholar: lookup
  33. Jennings LK, Storek KM, Ledvina HE, Coulon C, Marmont LS, Sadovskaya I, Secor PR, Tseng BS, Scian M, Filloux A, Wozniak DJ, Howell PL, Parsek MR. Pel is a cationic exopolysaccharide that cross-links extracellular DNA in the Pseudomonas aeruginosa biofilm matrix.. Proc Natl Acad Sci U S A 2015 Sep 8;112(36):11353-8.
    doi: 10.1073/pnas.1503058112pmc: PMC4568648pubmed: 26311845google scholar: lookup
  34. Chew SC, Kundukad B, Seviour T, van der Maarel JR, Yang L, Rice SA, Doyle P, Kjelleberg S. Dynamic remodeling of microbial biofilms by functionally distinct exopolysaccharides.. mBio 2014 Aug 5;5(4):e01536-14.
    doi: 10.1128/mBio.01536-14pmc: PMC4128364pubmed: 25096883google scholar: lookup
  35. Vasseur P, Vallet-Gely I, Soscia C, Genin S, Filloux A. The pel genes of the Pseudomonas aeruginosa PAK strain are involved at early and late stages of biofilm formation.. Microbiology (Reading) 2005 Mar;151(Pt 3):985-997.
    doi: 10.1099/mic.0.27410-0pubmed: 15758243google scholar: lookup
  36. Römling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger.. Microbiol Mol Biol Rev 2013 Mar;77(1):1-52.
    doi: 10.1128/MMBR.00043-12pmc: PMC3591986pubmed: 23471616google scholar: lookup
  37. Hickman JW, Tifrea DF, Harwood CS. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels.. Proc Natl Acad Sci U S A 2005 Oct 4;102(40):14422-7.
    doi: 10.1073/pnas.0507170102pmc: PMC1234902pubmed: 16186483google scholar: lookup
  38. Paul R, Weiser S, Amiot NC, Chan C, Schirmer T, Giese B, Jenal U. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain.. Genes Dev 2004 Mar 15;18(6):715-27.
    doi: 10.1101/gad.289504pmc: PMC387245pubmed: 15075296google scholar: lookup
  39. Christen M, Christen B, Folcher M, Schauerte A, Jenal U. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP.. J Biol Chem 2005 Sep 2;280(35):30829-37.
    doi: 10.1074/jbc.M504429200pubmed: 15994307google scholar: lookup
  40. Tischler AD, Camilli A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation.. Mol Microbiol 2004 Aug;53(3):857-69.
    doi: 10.1111/j.1365-2958.2004.04155.xpmc: PMC2790424pubmed: 15255898google scholar: lookup
  41. Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Cámara M, Williams P, Dow JM. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover.. Proc Natl Acad Sci U S A 2006 Apr 25;103(17):6712-7.
    doi: 10.1073/pnas.0600345103pmc: PMC1458946pubmed: 16611728google scholar: lookup
  42. Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S. The second messenger bis-(3'-5')-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa.. Mol Microbiol 2007 Aug;65(4):876-95.
    doi: 10.1111/j.1365-2958.2007.05817.xpubmed: 17645452google scholar: lookup
  43. Hay ID, Remminghorst U, Rehm BH. MucR, a novel membrane-associated regulator of alginate biosynthesis in Pseudomonas aeruginosa.. Appl Environ Microbiol 2009 Feb;75(4):1110-20.
    doi: 10.1128/AEM.02416-08pmc: PMC2643583pubmed: 19088322google scholar: lookup
  44. Kuchma SL, Connolly JP, O'Toole GA. A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa.. J Bacteriol 2005 Feb;187(4):1441-54.
    doi: 10.1128/JB.187.4.1441-1454.2005pmc: PMC545632pubmed: 15687209google scholar: lookup
  45. Starkey M, Hickman JH, Ma L, Zhang N, De Long S, Hinz A, Palacios S, Manoil C, Kirisits MJ, Starner TD, Wozniak DJ, Harwood CS, Parsek MR. Pseudomonas aeruginosa rugose small-colony variants have adaptations that likely promote persistence in the cystic fibrosis lung.. J Bacteriol 2009 Jun;191(11):3492-503.
    doi: 10.1128/JB.00119-09pmc: PMC2681918pubmed: 19329647google scholar: lookup
  46. Malone JG, Jaeger T, Spangler C, Ritz D, Spang A, Arrieumerlou C, Kaever V, Landmann R, Jenal U. YfiBNR mediates cyclic di-GMP dependent small colony variant formation and persistence in Pseudomonas aeruginosa.. PLoS Pathog 2010 Mar 12;6(3):e1000804.
    doi: 10.1371/journal.ppat.1000804pmc: PMC2837407pubmed: 20300602google scholar: lookup
  47. Licking E. Getting a grip on bacterial slime. Businessweek 13 September 1999, New York, NY.
  48. 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
  49. 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
  50. 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
  51. 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
  52. 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.
    doi: 10.1111/j.1439-0531.2010.01634.xpubmed: 20591061google scholar: lookup
  53. 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
  54. Ferris RA. Bacterial endometritis: a focus on biofilms. Clin Theriogenol 2014;6:315–319.
  55. Ferris RA, Wittstock SM, McCue PM, Borlee BR. Evaluation of biofilms in Gram-negative bacteria isolated from the equine uterus. J Equine Vet Sci 2014;34:121.
    doi: 10.1016/j.jevs.2013.10.082google scholar: lookup
  56. Ferris RA, McCue PM, Borlee GI, Loncar KD, Hennet ML, Borlee BR. 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 2016 Mar;54(3):631-9.
    doi: 10.1128/JCM.02861-15pmc: PMC4768000pubmed: 26719448google scholar: lookup
  57. Beehan DP, Wolfsdorf K, Elam J, Krekeler N, Paccamonti D, Lyle SK. The evaluation of biofilm-forming potential of Escherichia coli collected from the equine female reproductive tract. J Equine Vet Sci 2015;35:935–939.
    doi: 10.1016/j.jevs.2015.08.018google scholar: lookup
  58. Parham P. The immune system, 3rd ed. 2009, Garland Publishing, New York, NY.
  59. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes.. J Exp Med 1991 Nov 1;174(5):1209-20.
    doi: 10.1084/jem.174.5.1209pmc: PMC2119001pubmed: 1940799google scholar: lookup
  60. Guichelaar T, ten Brink CB, van Kooten PJ, Berlo SE, Broeren CP, van Eden W, Broere F. Autoantigen-specific IL-10-transduced T cells suppress chronic arthritis by promoting the endogenous regulatory IL-10 response.. J Immunol 2008 Feb 1;180(3):1373-81.
    doi: 10.4049/jimmunol.180.3.1373pubmed: 18209031google scholar: lookup
  61. 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
  62. Percival SL, Knapp JS, Edyvean R, Wales DS. Biofilm development on stainless steel in mains water. Water Res 1998;32:243–253.
    doi: 10.1016/S0043-1354(97)00132-2google scholar: lookup
  63. 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
  64. 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
  65. 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
  66. Byrd MS, Pang B, Hong W, Waligora EA, Juneau RA, Armbruster CE, Weimer KE, Murrah K, Mann EE, Lu H, Sprinkle A, Parsek MR, Kock ND, Wozniak DJ, Swords WE. Direct evaluation of Pseudomonas aeruginosa biofilm mediators in a chronic infection model.. Infect Immun 2011 Aug;79(8):3087-95.
    doi: 10.1128/IAI.00057-11pmc: PMC3147566pubmed: 21646454google scholar: lookup
  67. Bjarnsholt T, Alhede M, Alhede M, Eickhardt-Sørensen SR, Moser C, Kühl M, Jensen PØ, Høiby N. The in vivo biofilm.. Trends Microbiol 2013 Sep;21(9):466-74.
    doi: 10.1016/j.tim.2013.06.002pubmed: 23827084google scholar: lookup
  68. Lebeaux D, Chauhan A, Rendueles O, Beloin C. From in vitro to in vivo Models of Bacterial Biofilm-Related Infections.. Pathogens 2013 May 13;2(2):288-356.
    doi: 10.3390/pathogens2020288pmc: PMC4235718pubmed: 25437038google scholar: lookup
  69. Lovewell RR, Patankar YR, Berwin B. Mechanisms of phagocytosis and host clearance of Pseudomonas aeruginosa.. Am J Physiol Lung Cell Mol Physiol 2014 Apr 1;306(7):L591-603.
    doi: 10.1152/ajplung.00335.2013pmc: PMC4116407pubmed: 24464809google scholar: lookup
  70. Mishra M, Byrd MS, Sergeant S, Azad AK, Parsek MR, McPhail L, Schlesinger LS, Wozniak DJ. Pseudomonas aeruginosa Psl polysaccharide reduces neutrophil phagocytosis and the oxidative response by limiting complement-mediated opsonization.. Cell Microbiol 2012 Jan;14(1):95-106.
    doi: 10.1111/j.1462-5822.2011.01704.xpmc: PMC4466118pubmed: 21951860google scholar: lookup
  71. Doig PA, McKnight JD, Miller RB. The use of endometrial biopsy in the infertile mare.. Can Vet J 1981 Mar;22(3):72-6.
    pmc: PMC1789874pubmed: 7026016
  72. 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
  73. Schurr MJ. Which bacterial biofilm exopolysaccharide is preferred, Psl or alginate?. J Bacteriol 2013 Apr;195(8):1623-6.
    doi: 10.1128/JB.00173-13pmc: PMC3624548pubmed: 23417492google scholar: lookup
  74. Valle J, Solano C, García B, Toledo-Arana A, Lasa I. Biofilm switch and immune response determinants at early stages of infection.. Trends Microbiol 2013 Aug;21(8):364-71.
    doi: 10.1016/j.tim.2013.05.008pubmed: 23816497google scholar: lookup
  75. Rybtke M, Hultqvist LD, Givskov M, Tolker-Nielsen T. Pseudomonas aeruginosa Biofilm Infections: Community Structure, Antimicrobial Tolerance and Immune Response.. J Mol Biol 2015 Nov 20;427(23):3628-45.
    doi: 10.1016/j.jmb.2015.08.016pubmed: 26319792google scholar: lookup
  76. Irie Y, Borlee BR, O'Connor JR, Hill PJ, Harwood CS, Wozniak DJ, Parsek MR. Self-produced exopolysaccharide is a signal that stimulates biofilm formation in Pseudomonas aeruginosa.. Proc Natl Acad Sci U S A 2012 Dec 11;109(50):20632-6.
    doi: 10.1073/pnas.1217993109pmc: PMC3528562pubmed: 23175784google scholar: lookup
  77. Kirisits MJ, Prost L, Starkey M, Parsek MR. Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms.. Appl Environ Microbiol 2005 Aug;71(8):4809-21.
    doi: 10.1128/AEM.71.8.4809-4821.2005pmc: PMC1183349pubmed: 16085879google scholar: lookup
  78. Hinrichs K, Cummings MR, Sertich PL, Kenney RM. Clinical significance of aerobic bacterial flora of the uterus, vagina, vestibule, and clitoral fossa of clinically normal mares.. J Am Vet Med Assoc 1988 Jul 1;193(1):72-5.
    pubmed: 3417532
  79. Ricketts SW. Bacterioloical examinations of the mare's cervix: techniques and interpretation of results.. Vet Rec 1981 Jan 17;108(3):46-51.
    doi: 10.1136/vr.108.3.46pubmed: 6789540google scholar: lookup
  80. Ricketts SW, Mackintosh ME. Role of anaerobic bacteria in equine endometritis.. J Reprod Fertil Suppl 1987;35:343-51.
    pubmed: 3479588
  81. 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
  82. Rodeheaver GT, Pettry D, Thacker JG, Edgerton MT, Edlich RF. Wound cleansing by high pressure irrigation.. Surg Gynecol Obstet 1975 Sep;141(3):357-62.
    pubmed: 808870
  83. Fry DE. Pressure Irrigation of Surgical Incisions and Traumatic Wounds.. Surg Infect (Larchmt) 2017 May Jun;18(4):424-430.
    doi: 10.1089/sur.2016.252pubmed: 28437197google scholar: lookup
  84. Anglen J, Apostoles PS, Christensen G, Gainor B, Lane J. Removal of surface bacteria by irrigation.. J Orthop Res 1996 Mar;14(2):251-4.
    doi: 10.1002/jor.1100140213pubmed: 8648503google scholar: lookup
  85. Bahrs C, Schnabel M, Frank T, Zapf C, Mutters R, von Garrel T. Lavage of contaminated surfaces: an in vitro evaluation of the effectiveness of different systems.. J Surg Res 2003 Jun 1;112(1):26-30.
    doi: 10.1016/S0022-4804(03)00150-1pubmed: 12873429google scholar: lookup
  86. Santander J, Martin T, Loh A, Pohlenz C, Gatlin DM, Curtiss R. Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence.. Microbiology (Reading) 2013 Jul;159(Pt 7):1471-1486.
    doi: 10.1099/mic.0.066639-0pmc: PMC4085987pubmed: 23676433google scholar: lookup
  87. Irie Y, Parsek MR. LC/MS/MS-based quantitative assay for the secondary messenger molecule, c-di-GMP.. Methods Mol Biol 2014;1149:271-9.
    doi: 10.1007/978-1-4939-0473-0_22pubmed: 24818912google scholar: lookup
  88. MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, MacCoss MJ. Skyline: an open source document editor for creating and analyzing targeted proteomics experiments.. Bioinformatics 2010 Apr 1;26(7):966-8.
    doi: 10.1093/bioinformatics/btq054pmc: PMC2844992pubmed: 20147306google scholar: lookup
  89. Broccardo CJ, Schauer KL, Kohrt WM, Schwartz RS, Murphy JP, Prenni JE. Multiplexed analysis of steroid hormones in human serum using novel microflow tile technology and LC-MS/MS.. J Chromatogr B Analyt Technol Biomed Life Sci 2013 Sep 1;934:16-21.
    doi: 10.1016/j.jchromb.2013.06.031pmc: PMC4391816pubmed: 23891914google scholar: lookup
  90. Shrivastava A, Gupta VB. Methods for the determination of limit of detection and limit of quantitation of the analytical methods. Chron Young Sci 2011;2:21.
    doi: 10.4103/2229-5186.79345google scholar: lookup
  91. Ferris RA, Bohn A, McCue PM. Equine endometrial cytology: collection techniques and interpretation. Equine Vet Educ 2015;27:316–322.
    doi: 10.1111/eve.12280google scholar: lookup
  92. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction.. BMC Bioinformatics 2012 Jun 18;13:134.
    doi: 10.1186/1471-2105-13-134pmc: PMC3412702pubmed: 22708584google scholar: lookup
  93. Hraha TH, Doremus KM, McIlwraith CW, Frisbie DD. Autologous conditioned serum: the comparative cytokine profiles of two commercial methods (IRAP and IRAP II) using equine blood.. Equine Vet J 2011 Sep;43(5):516-21.
    doi: 10.1111/j.2042-3306.2010.00321.xpubmed: 21496084google scholar: lookup
  94. Klein C, Rutllant J, Troedsson MH. Expression stability of putative reference genes in equine endometrial, testicular, and conceptus tissues.. BMC Res Notes 2011 Apr 12;4:120.
    doi: 10.1186/1756-0500-4-120pmc: PMC3083352pubmed: 21486450google scholar: lookup
  95. Dascanio J, Tschetter J, Gray A, Bridges K. Use of quantitative real-time polymerase chain reaction to examine endometrial tissue. Anim Reprod Sci 2006;94:254–258.
    doi: 10.1016/j.anireprosci.2006.04.008google scholar: lookup
  96. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR.. Nucleic Acids Res 2001 May 1;29(9):e45.
    pmc: PMC55695pubmed: 11328886doi: 10.1093/nar/29.9.e45google scholar: lookup

Citations

This article has been cited 14 times.
  1. 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
  2. Ding X, Cui X, Shi J, Cheng X, Yao D, Gao Y, Zhang Y. Construction of a model of endometritis in domestic rabbits using equine-derived pathogens and evaluation of therapeutic effect of sensitive drugs.. Front Vet Sci 2023;10:1064522.
    doi: 10.3389/fvets.2023.1064522pubmed: 36846263google scholar: lookup
  3. Holyoak GR, Premathilake HU, Lyman CC, Sones JL, Gunn A, Wieneke X, DeSilva U. The healthy equine uterus harbors a distinct core microbiome plus a rich and diverse microbiome that varies with geographical location.. Sci Rep 2022 Aug 30;12(1):14790.
    doi: 10.1038/s41598-022-18971-6pubmed: 36042332google scholar: lookup
  4. Lu S, Tao T, Su Y, Hu J, Zhang L, Wang G, Li X, Guo X. Whole Genome Sequencing and CRISPR/Cas9 Gene Editing of Enterotoxigenic Escherichia coli BE311 for Fluorescence Labeling and Enterotoxin Analyses.. Int J Mol Sci 2022 Jul 6;23(14).
    doi: 10.3390/ijms23147502pubmed: 35886856google scholar: lookup
  5. 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
  6. Hsu I, Hsu L, Dorjee S, Hsu CC. Bacterial colonization at caesarean section defects in women of secondary infertility: an observational study.. BMC Pregnancy Childbirth 2022 Feb 18;22(1):135.
    doi: 10.1186/s12884-022-04471-ypubmed: 35180844google scholar: lookup
  7. Díaz-Bertrana ML, Deleuze S, Pitti Rios L, Yeste M, Morales Fariña I, Rivera Del Alamo MM. Microbial Prevalence and Antimicrobial Sensitivity in Equine Endometritis in Field Conditions.. Animals (Basel) 2021 May 20;11(5).
    doi: 10.3390/ani11051476pubmed: 34065566google 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. Yan S, Wu G. Can Biofilm Be Reversed Through Quorum Sensing in Pseudomonas aeruginosa?. Front Microbiol 2019;10:1582.
    doi: 10.3389/fmicb.2019.01582pubmed: 31396166google scholar: lookup
  11. Zhu H, Li W, Wang Z, Chen J, Ding M, Han L. TREM-1 deficiency attenuates the inflammatory responses in LPS-induced murine endometritis.. Microb Biotechnol 2019 Nov;12(6):1337-1345.
    doi: 10.1111/1751-7915.13467pubmed: 31365951google scholar: lookup
  12. Al-Kass Z, Eriksson E, Bagge E, Wallgren M, Morrell JM. Bacteria detected in the genital tract, semen or pre-ejaculatory fluid of Swedish stallions from 2007 to 2017.. Acta Vet Scand 2019 May 30;61(1):25.
    doi: 10.1186/s13028-019-0459-zpubmed: 31146786google scholar: lookup
  13. Kern ZT, Jacob ME, Gilbertie JM, Vaden SL, Lyle SK. Characteristics of Dogs with Biofilm-Forming Escherichia Coli Urinary Tract Infections.. J Vet Intern Med 2018 Sep;32(5):1645-1651.
    doi: 10.1111/jvim.15231pubmed: 30084122google scholar: lookup
  14. Tosaki K, Kojima H, Akama S, Ootake Y, Inoue K, Katsuda K, Shibahara T. Bovine esophageal and glossal ulceration associated with Pseudomonas aeruginosa and Fusobacterium spp. in a 10-month-old Holstein heifer.. J Vet Med Sci 2018 Jul 18;80(7):1174-1178.
    doi: 10.1292/jvms.17-0616pubmed: 29806628google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.