FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Theriogenology2007; 68(3); 403-412; doi: 10.1016/j.theriogenology.2007.04.038

Use of a low-volume uterine flush for diagnosing endometritis in chronically infertile mares.

Abstract: Low-volume uterine flush (n=401) was performed in 308 infertile mares to diagnose endometritis. Mares evaluated were either barren after three or more breedings or had two or more unsuccessful embryo recovery attempts during consecutive cycles. Culture results were compared with cytological and histological findings, efflux clarity and pH to substantiate that the micro-organisms recovered were truly pathogens. Cytological specimens were evaluated for presence of epithelial and inflammatory cells, bacteria, yeast and debris. Endometrial biopsies (n=110) were examined for the presence of neutrophils in the stratum compactum. Micro-organisms were recovered in 282/401 (70%) of low-volume flushes; E. coli was most frequently isolated (42.2%), followed by beta hemolytic Streptococcus (37.6%). Efflux clarity of 318 flushes was clear (n=109), cloudy (n=149), or mucoid (n=60). Isolation of micro-organisms was highly associated with cloudy and mucoid effluxes (P<0.001), debris on cytological specimens (P<0.001), increased efflux pH (P<0.003), and neutrophils on endometrial biopsy (P<0.01). E. coli was associated with debris on cytological smear (P<0.002), whereas beta hemolytic Streptococcus was associated with increased efflux pH (P<0.002). Using the presence of neutrophils in a tissue specimen as the "best standard" for diagnosing endometritis, the sensitivity of flush culture was 0.71 and for flush cytology was 0.8, whereas the specificity was 0.86 and 0.67, respectively. Neutrophils in uterine flushes under-reported inflammation; only 86/282 positive cultures were positive on cytology. The clinical estimate of a contaminated (false positive) flush culture was 11%, if a false positive was defined as positive culture with clear efflux and no debris or neutrophils on cytology (26/228). In conclusion, a low-volume uterine flush was a rapid, accurate method for identifying mares with chronic endometritis. When micro-organisms were recovered, endometritis was confirmed by efflux clarity, pH and cytological findings of debris, bacteria, or neutrophils. E. coli was most commonly isolated and it appeared to differ in pathogenicity from beta hemolytic Streptococcus.
Get Full Text
Publication Date: 2007-05-31 PubMed ID: 17543379DOI: 10.1016/j.theriogenology.2007.04.038Google 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
  • Evaluation Study
  • 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 study examined the use of a low-volume uterine flush to diagnose endometritis in mares that are chronically infertile. The researchers discovered that this method was a rapid and accurate way to identify endometritis, and that micro-organisms were a significant indicator of the condition.

Methodology of the Study

  • The researchers carried out low-volume uterine flushes on 308 infertile mares. These mares had either not conceived after three or more breeding attempts or had two or more unsuccessful attempts to recover embryos over consecutive cycles.
  • The team compared the results of the flushes with cytological and histological findings, the clarity and pH of any efflux, and biopsies of the endometrium.
  • Cytological samples were evaluated for the presence of epithelial and inflammatory cells, bacteria, yeast and debris. Endometrial biopsies were evaluated for the occurrence of neutrophils in the stratum compactum.

Findings of the Study

  • They found that micro-organisms were present in 70% (282/401) of the flushes. The most commonly isolated organism was E. coli (42.2%), followed by beta hemolytic Streptococcus (37.6%).
  • Isolation of these micro-organisms was significantly associated with cloudy or mucoid effluxes, debris as seen on cytology, a higher efflux pH, and the presence of neutrophils on endometrial biopsies.
  • When looking at individual organisms, E. coli was associated with debris as seen on cytological smear while beta hemolytic Streptococcus was associated with increased efflux pH.

Accuracy of the Low-Volume Uterine Flush

  • Using the presence of neutrophils in a tissue sample as the best diagnostic tool for endometritis, the researchers found that the flush culture had a sensitivity of 0.71 and a specificity of 0.86. The flush cytology had a sensitivity of 0.8 and a specificity of 0.67.
  • Overall, the clinical estimate of a contaminated, or false positive, flush culture was 11%. A false positive was defined as a positive culture with clear efflux and without neutrophils or debris on cytology.

Conclusion

  • The study concluded that a low-volume uterine flush is effective for diagnosing mares with chronic endometritis.
  • When micro-organisms were recovered from the flush, it was a strong indication of endometritis. This was confirmed by the efflux’s clarity and pH, as well as cytological findings of debris, bacteria, or neutrophils.
  • E. coli was the most commonly isolated organism and there seemed to be a difference in pathogenicity between E. coli and beta hemolytic Streptococcus.

Cite This Article

APA
LeBlanc MM, Magsig J, Stromberg AJ. (2007). Use of a low-volume uterine flush for diagnosing endometritis in chronically infertile mares. Theriogenology, 68(3), 403-412. https://doi.org/10.1016/j.theriogenology.2007.04.038

Publication

Theriogenology
ISSN: 0093-691X
NlmUniqueID: 0421510
Country: United States
Language: English
Volume: 68
Issue: 3
Pages: 403-412

Researcher Affiliations

LeBlanc, Michelle M
  • Rood and Riddle Equine Hospital, and Department of Statistics, University of Kentucky, Lexington, KY 40506-0027, USA. Mleblanc@roodandriddle.com
Magsig, Joshua
    Stromberg, Arnold J

      MeSH Terms

      • Animals
      • Bacteria / isolation & purification
      • Chronic Disease
      • Cytodiagnosis / veterinary
      • Diagnostic Techniques, Obstetrical and Gynecological / veterinary
      • Endometritis / diagnosis
      • Endometritis / microbiology
      • Endometritis / veterinary
      • Endometrium / cytology
      • Endometrium / microbiology
      • Female
      • Horse Diseases / diagnosis
      • Horse Diseases / microbiology
      • Horses
      • Hydrogen-Ion Concentration
      • Infertility, Female / diagnosis
      • Infertility, Female / microbiology
      • Infertility, Female / veterinary
      • Neutrophils / cytology
      • Sensitivity and Specificity
      • Uterus / cytology
      • Uterus / microbiology

      Citations

      This article has been cited 24 times.
      1. Scarlet D, Malama E, Fischer S, Knutti B, Bollwein H. Relationship between Clinical Uterine Findings, Therapy, and Fertility in the Mare. Vet Sci 2023 Mar 29;10(4).
        doi: 10.3390/vetsci10040259pubmed: 37104414google scholar: lookup
      2. Parrilla Hernández S, Franck T, Munaut C, Feyereisen É, Piret J, Farnir F, Reigner F, Barrière P, Deleuze S. Characterization of Myeloperoxidase in the Healthy Equine Endometrium. Animals (Basel) 2023 Jan 21;13(3).
        doi: 10.3390/ani13030375pubmed: 36766264google scholar: lookup
      3. Asadi B, Seyedasgari F, Ashrafi Tamai I, Yarmohammadi M, Ebadi R, Kim E, Barin A. Isolated Bacteria from the Uteri of Camels with Different Reproductive Backgrounds: A Study on Sampling Methodology, Prevalence, and Clinical Significance. Vet Sci 2023 Jan 5;10(1).
        doi: 10.3390/vetsci10010039pubmed: 36669039google scholar: lookup
      4. Li J, Zhu Y, Mi J, Zhao Y, Holyoak GR, Yi Z, Wu R, Wang Z, Zeng S. Endometrial and vaginal microbiome in donkeys with and without clinical endometritis. Front Microbiol 2022;13:884574.
        doi: 10.3389/fmicb.2022.884574pubmed: 35979491google scholar: lookup
      5. D'Agostino A, Di Palma T, Cecchini Gualandi S, Boni R. Fluorescence Spectroscopy for the Diagnosis of Endometritis in the Mare. Animals (Basel) 2022 Apr 29;12(9).
        doi: 10.3390/ani12091157pubmed: 35565583google scholar: lookup
      6. Weber KS, Wagener K, Blanco M, Bauersachs S, Bollwein H. A comparative analysis of the intrauterine transcriptome in fertile and subfertile mares using cytobrush sampling. BMC Genomics 2021 May 22;22(1):377.
        doi: 10.1186/s12864-021-07701-3pubmed: 34022808google scholar: lookup
      7. Salemi Z, Rezaie A, Goorani Nejad S, Mohammadian B. Histopathological and cytological analyses of endometrium in water buffaloes (Bubalus bubalis) to detect estrus and endometritis. Vet Res Forum 2020 Fall;11(4):409-414.
        doi: 10.30466/vrf.2019.92037.2226pubmed: 33643595google scholar: lookup
      8. Wojtysiak K, Ryszka W, Stefaniak T, Król J, Kozdrowski R. Changes in the Secretion of Anti-Inflammatory Cytokines and Acute-Phase Proteins in the Uterus after Artificial Insemination in the Mare. Animals (Basel) 2020 Dec 19;10(12).
        doi: 10.3390/ani10122438pubmed: 33352707google scholar: lookup
      9. Köhne M, Kuhlmann M, Tönißen A, Martinsson G, Sieme H. Diagnostic and Treatment Practices of Equine Endometritis-A Questionnaire. Front Vet Sci 2020;7:547.
        doi: 10.3389/fvets.2020.00547pubmed: 32984410google scholar: lookup
      10. Quartuccio M, Cristarella S, Medica P, Fazio E, Mazzullo G, Rifici C, Liotta L, Satué K. Endometrial Cytology During the Different Phases of the Estrous Cycle in Jennies: New Evidences. Animals (Basel) 2020 Jun 19;10(6).
        doi: 10.3390/ani10061062pubmed: 32575538google scholar: lookup
      11. 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
      12. Skive B, Rohde M, Molinari G, Braunstein TH, Bojesen AM. Streptococcus equi subsp. zooepidemicus Invades and Survives in Epithelial Cells. Front Cell Infect Microbiol 2017;7:465.
        doi: 10.3389/fcimb.2017.00465pubmed: 29164073google scholar: lookup
      13. Sikora M, Król J, Nowak M, Stefaniak T, Aubertsson G, Kozdrowski R. The usefulness of uterine lavage and acute phase protein levels as a diagnostic tool for subclinical endometritis in Icelandic mares. Acta Vet Scand 2016 Sep 7;58(1):50.
        doi: 10.1186/s13028-016-0233-4pubmed: 27604098google scholar: lookup
      14. Siemieniuch MJ, Szóstek AZ, Gajos K, Kozdrowski R, Nowak M, Okuda K. Type of Inflammation Differentially Affects Expression of Interleukin 1β and 6, Tumor Necrosis Factor-α and Toll-Like Receptors in Subclinical Endometritis in Mares. PLoS One 2016;11(5):e0154934.
        doi: 10.1371/journal.pone.0154934pubmed: 27152525google scholar: lookup
      15. Buczkowska J, Kozdrowski R, Nowak M, Raś A, Staroniewicz Z, Siemieniuch MJ. Comparison of the biopsy and cytobrush techniques for diagnosis of subclinical endometritis in mares. Reprod Biol Endocrinol 2014 Apr 4;12:27.
        doi: 10.1186/1477-7827-12-27pubmed: 24708825google scholar: lookup
      16. Kalpokas I, Perdigón F, Rivero R, Talmon M, Sartore I, Viñoles C. Effect of a povidone-iodine intrauterine infusion on progesterone levels and endometrial steroid receptor expression in mares. Acta Vet Scand 2010 Dec 16;52(1):66.
        doi: 10.1186/1751-0147-52-66pubmed: 21162724google scholar: lookup
      17. Fehin B, Scott CJ, Arango-Sabogal JC, de Mestre AM, Mouncey R. Associations between endometrial swab bacteriology and cytology findings and live foal rates in Thoroughbred broodmares in the United Kingdom. Equine Vet J 2026 Mar;58(2):348-358.
        doi: 10.1111/evj.70086pubmed: 40888035google scholar: lookup
      18. Carvalho IB, Branco S, Laranjo M, Queiroga MC, Bettencourt E. Characteristics of the Mare-Uterine-Culture-Based Bacterial Composition Using Practical Clinical Evaluation Methods. Pathogens 2025 Apr 7;14(4).
        doi: 10.3390/pathogens14040357pubmed: 40333165google scholar: lookup
      19. Scholtz M, Guthrie AJ, Newton R, Schulman ML. Review of Pseudomonas aeruginosa and Klebsiella pneumoniae as venereal pathogens in horses. Equine Vet J 2025 May;57(3):587-597.
        doi: 10.1111/evj.14201pubmed: 39103748google scholar: lookup
      20. Prete CD, Nocera FP, Piegari G, Palumbo V, Martino L, Cocchia N, Paciello O, Montano C, Pasolini MP. Use of cytobrush for bacteriological and cytological diagnosis of endometritis in mares. Vet World 2024 Feb;17(2):398-406.
        doi: 10.14202/vetworld.2024.398-406pubmed: 38595673google scholar: lookup
      21. Virendra A, Gulavane SU, Ahmed ZA, Reddy R, Chaudhari RJ, Gaikwad SM, Shelar RR, Ingole SD, Thorat VD, Khanam A, Khan FA. Metagenomic analysis unravels novel taxonomic differences in the uterine microbiome between healthy mares and mares with endometritis. Vet Med Sci 2024 Mar;10(2):e1369.
        doi: 10.1002/vms3.1369pubmed: 38357732google 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
      23. Thomson P, García P, Río CD, Castro R, Núñez A, Miranda C. Antimicrobial Resistance and Extended-Spectrum Beta-Lactamase Genes in Enterobacterales, Pseudomonas and Acinetobacter Isolates from the Uterus of Healthy Mares. Pathogens 2023 Sep 8;12(9).
        doi: 10.3390/pathogens12091145pubmed: 37764953google scholar: lookup
      24. Tukia E, Hallman I, Penttilä M, Hänninen S, Kareskoski M. RNA in situ hybridization of Escherichia coli in equine endometrial biopsies. Front Vet Sci 2023;10:1186051.
        doi: 10.3389/fvets.2023.1186051pubmed: 37360403google scholar: lookup
      Subscribe to our newsletter
      Join 99,928 horse owners like you who receive our email updates on horse health and nutrition.