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Veterinary sciences2022; 9(8); doi: 10.3390/vetsci9080448

Analysis of 1840 Equine Intraocular Fluid Samples for the Presence of Anti-Leptospira Antibodies and Leptospiral DNA and the Correlation to Ophthalmologic Findings in Terms of Equine Recurrent Uveitis (ERU)-A Retrospective Study.

Abstract: In the equine clinic of the LMU in Munich, therapeutic vitrectomies have been routinely performed in horses for three decades. The vitreous samples obtained during vitrectomies were usually tested for anti-Leptospira antibodies and for more than 20 years also by PCR for leptospiral DNA. If the indication for surgery was ophthalmologically inconclusive, an aqueous humor was collected preoperatively and examined for evidence of leptospiral infection. In this study, medical records from 2002 to 2017 were analyzed. Records for 1387 eyes affected by equine recurrent uveitis (ERU) and 237 eyes affected by another type of uveitis met the inclusion criteria. A total of 216 samples from healthy eyes were used as controls. In 83% of intraocular samples from ERU eyes, antibody titers of 1:100 or higher were detectable by microscopic agglutination test (MAT). Similarly, 83% of intraocular samples had anti-Leptospira antibodies detected by ELISA. In 72% of the intraocular specimens, leptospiral DNA was detectable by PCR. No antibodies were detectable in the samples from eyes with another type of uveitis or in the samples from healthy eyes. A PCR was positive in only one sample from a healthy eye. These results with a very high number of intraocular specimens demonstrate the great importance of an intraocular leptospiral infection for ERU. It can be concluded that for a reliable diagnosis of intraocular leptospiral infection or to reliably exclude an infection multiple tests should be applied.
Publication Date: 2022-08-21 PubMed ID: 36006363PubMed Central: PMC9414351DOI: 10.3390/vetsci9080448Google Scholar: Lookup
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  • Journal Article

Summary

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The research article discusses a study conducted on horses spanning over a 15-year period (2002-2017), focusing on the correlation between intraocular Leptospira infection and equine recurrent uveitis (ERU). The study emphasizes the importance of multiple tests for a reliable diagnosis of intraocular Leptospira infection.

Research Methodology

  • The equine clinic of the LMU in Munich has processed therapeutic vitrectomies on horses for about 30 years. Vitreous samples, obtained during these procedures, traditionally underwent testing for anti-Leptospira antibodies and have been tested for the presence of Leptospira DNA via PCR for over 20 years.
  • In instances where the necessity for surgery was unclear based on ophthalmological findings, an aqueous humor was collected preoperatively and examined for signs of leptospiral infection.
  • The study leveraged medical records from 2002 to 2017 and used inclusion criteria to select 1387 eyes affected by ERU, 237 eyes impacted by other types of uveitis, and 216 samples from healthy eyes as controls.

Findings of the Study

  • A substantial proportion – 83%, of intraocular samples from ERU eyes displayed antibody titers of 1:100 or higher, detectable by the microscopic agglutination test (MAT). This was mirrored in the ELISA test results, where 83% of intraocular samples registered anti-Leptospira antibodies.
  • 72% of intraocular specimens showed the presence of leptospiral DNA as per PCR tests.
  • In contrast, no anti-Leptospira antibodies were detected in eyes affected by other types of uveitis or in samples collected from healthy eyes. An exception was one sample from a healthy eye which tested positive in PCR.

Research Conclusions

  • The study concluded that a substantial majority of ERU cases could potentially be linked to intraocular leptospiral infection according to a significant number of intraocular specimens.
  • The research recommends that for accurate diagnosis or reliable exclusion of intraocular leptospiral infection, practitioners should apply multiple testing methods.

Cite This Article

APA
Geiger T, Gerhards H, Bjelica B, Mackenthun E, Wollanke B. (2022). Analysis of 1840 Equine Intraocular Fluid Samples for the Presence of Anti-Leptospira Antibodies and Leptospiral DNA and the Correlation to Ophthalmologic Findings in Terms of Equine Recurrent Uveitis (ERU)-A Retrospective Study. Vet Sci, 9(8). https://doi.org/10.3390/vetsci9080448

Publication

ISSN: 2306-7381
NlmUniqueID: 101680127
Country: Switzerland
Language: English
Volume: 9
Issue: 8

Researcher Affiliations

Geiger, Tobias
  • Clinic for Horses, University of Veterinary Medicine, 30559 Hanover, Germany.
Gerhards, Hartmut
  • Equine Clinic, Clinical Department, Ludwig-Maximilians-University (LMU), 85764 Oberschleissheim, Germany.
Bjelica, Bogdan
  • Department of Neurology, Hanover Medical School, 30625 Hanover, Germany.
Mackenthun, Elke
  • Equine Clinic at the Racetrack, An der Rennbahn 16, 76473 Iffezheim, Germany.
Wollanke, Bettina
  • Equine Clinic, Clinical Department, Ludwig-Maximilians-University (LMU), 85764 Oberschleissheim, Germany.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 73 references
  1. Wollanke B, Gerhards H, Ackermann K. Infectious uveitis in horses and new insights in its leptospiral biofilm-related pathogenesis.. Microorganisms 2022;10:387.
  2. Schwink KL. Equine uveitis.. Vet. Clin. N. Am. Equine Pract. 1992;8:557–574.
    doi: 10.1016/S0749-0739(17)30441-8pubmed: 1458329google scholar: lookup
  3. Gilger BC, Hollingsworth SR. Diseases of the uvea, uveitis, and recurrent uveitis.. In: Gilger B.C., editor. Equine Ophthalmology. 3rd ed. Wiley Blackwell; Ames, IA, USA: 2017. pp. 369–415.
  4. Baumgart A, Gerhards H. Characteristics of uveitis in horses with leopard coat color and potential use of cyclosporine A in its therapy in Germany.. Pferdeheilkunde 2014;30:626–632.
  5. Sandmeyer LS, Bauer BS, Feng CX, Grahn BH. Equine recurrent uveitis in western Canadian prairie provinces: A retrospective study (2002–2015). Can. Vet. J. 2017;58:717–722.
    pmc: PMC5501119pubmed: 28698690
  6. Grahn BH, Cullen CL. Equine phacoclastic uveitis: The clinical manifestations, light microscopic findings, and therapy of 7 cases.. Can. Vet. J. 2000;41:376–382.
    pmc: PMC1476266pubmed: 10816830
  7. Pinto NI, McMullen RJ Jr, Linder KE, Cullen JM, Gilger BC. Clinical, histopathological and immunohistochemical characterization of a novel equine ocular disorder: Heterochromic iridocyclitis with secondary keratitis in adult horses.. Vet. Ophthalmol. 2015;18:443–456.
    doi: 10.1111/vop.12234pubmed: 25399915google scholar: lookup
  8. Davidson HJ, Blanchard GL, Wheeler CA, Render JA. Anterior uveal melanoma, with secondary keratitis, cataract, and glaucoma, in a horse.. J. Am. Vet. Med. Assoc. 1991;199:1049–1050.
    pubmed: 1748609
  9. Bistner SI. Medullo-epithelioma of the iris and ciliary body in a horse.. Cornell Vet. 1974;64:588–595.
    pubmed: 4430185
  10. Barnett KC. Uveitis.. In: Barnett K.C., Crispin S.M., Lavach J.D., Matthews A.G., editors. Equine Ophthalmology—An Atlas and Text. 2nd ed. Saunders; Edinburgh, UK: 2004. pp. 191–197.
  11. Kinde H, Mathews M, Ash L, St Leger J. Halicephalobus gingivalis (H. deletrix) infection in two horses in southern California.. J. Vet. Diagn. Investig. 2000;12:162–165.
    doi: 10.1177/104063870001200213pubmed: 10730949google scholar: lookup
  12. Wollanke B, Gerhards H, Schaffer E. Keratouveitis und Makrohaematurie bei einer Infektion mit Micronema deletrix bei einem Pferd.. Pferdeheilkunde 2000;16:23–29.
    doi: 10.21836/PEM20000102google scholar: lookup
  13. Tarancón I, Leiva M, Jose-Cunilleras E, Ríos J, Peña T. Ophthalmologic findings associated with Rhodococcus equi bronchopneumonia in foals.. Vet. Ophthalmol. 2019;22:660–665.
    doi: 10.1111/vop.12637pubmed: 30706641google scholar: lookup
  14. Gilger BC, Wilkie DA, Clode AB, McMullen RJ Jr, Utter ME, Komaromy AM, Brooks DE, Salmon JH. Long-term outcome after implantation of a suprachoroidal cyclosporine drug delivery device in horses with recurrent uveitis.. Vet. Ophthalmol. 2010;13:294–300.
  15. Launois T, González Hilarión LM, Barbe F, Leurquin C, Bihin B, Hontoir F, Dugdale A, Vandeweerd JM. Use of Intravitreal Injection of Gentamicin in 71 Horses With Equine Recurrent Uveitis.. J. Equine Vet. Sci. 2019;77:93–97.
    doi: 10.1016/j.jevs.2019.02.018pubmed: 31133325google scholar: lookup
  16. Kleinpeter A, Göpfert A, Köhler E, Brehm W. Intravitreal injection of low-dose gentamicin for the treatment of ERU-affected horses.. Tierarztl. Prax. Ausg. G Grosstiere Nutztiere 2019;47:25–34.
    doi: 10.1055/a-0816-7156pubmed: 30808028google scholar: lookup
  17. Fischer BM, McMullen RJ Jr, Reese S, Brehm W. Intravitreal injection of low-dose gentamicin for the treatment of recurrent or persistent uveitis in horses: Preliminary results.. BMC Vet. Res. 2019;15:29.
    doi: 10.1186/s12917-018-1722-7pmc: PMC6335700pubmed: 30651102google scholar: lookup
  18. Pinard C, Piètrement E, Macieira S, Tremblay D. Intravitreal injections of gentamicin for the treatment of Leptospira-associated equine recurrent uveitis; Proceedings of the 36th Annual Meeting of the ACVO; Nashville, TN, USA.. 12–15 October 2005.
  19. Neumann M, Ohnesorge B. The intravitreal gentamicin-injection for treatment of the equine recurrent uveitis (ERU)—status quo.. Pferdeheilkd.—Equine Med. 2021;37:302–311.
    doi: 10.21836/PEM20210312google scholar: lookup
  20. Wollanke B, Gerhards H, Brem S, Meyer P, Kopp H. Ätiologie der equinen rezidivierenden Uveitis (ERU): Autoimmunkrankheit oder intraokulare Leptospireninfektion [Etiology of equine recurrent uveitis (ERU): Autoimmune disease or intraocular leptospiral infection]. Pferdeheilkunde 2004;20:327–340.
    doi: 10.21836/PEM20040403google scholar: lookup
  21. Ackermann K, Kenngott R, Settles M, Gerhards H, Maierl J, Wollanke B. In Vivo Biofilm Formation of Pathogenic Leptospira spp. in the Vitreous Humor of Horses with Recurrent Uveitis.. Microorganisms 2021;9:1915.
  22. Dwyer AE, Crockett RS, Kalsow CM. Association of leptospiral seroreactivity and breed with uveitis and blindness in horses: 372 cases (1986–1993). J. Am. Vet. Med. Assoc. 1995;207:1327–1331.
    pubmed: 7591929
  23. Tóth J, Hollerieder J, Sótoni P. Augenheilkunde beim Pferd—Lehrbuch und Atlas.. Schattauer GmbH; Stuttgart, Germany: 2010.
  24. Szemes P, Gerhards H. Study on the prevalence of equine recurrent uveitis in the Cologne-Bonn area.. Prakt. Tierarzt. 2000;81:408–420.
  25. Alexander CS, Keller H. Ätiologie und Vorkommen der periodischen Augenentzündung des Pferdes im Raum Berlin [Etiology and occurrence of periodic eye inflammation of horses in the area of Berlin]. Tierarztl. Prax. 1990;18:623–627.
    pubmed: 2080508
  26. Sandmeyer LS, Kingsley NB, Walder C, Archer S, Leis ML, Bellone RR, Bauer BS. Risk factors for equine recurrent uveitis in a population of Appaloosa horses in western Canada.. Vet. Ophthalmol. 2020;23:515–525.
    doi: 10.1111/vop.12749pubmed: 32086865google scholar: lookup
  27. Gerhards H, Wollanke B. Surgical treatment of equine recurrent uveitis: Trans-pars-plana vitrectomy in horses.. In: Gilger B.C., editor. Equine Ophthalmology. 1st ed. Elsevier Saunders; St. Louis, MO, USA: 2005. pp. 314–319.
  28. Wollanke B, Gerhards H, Schinagl C. Results of 654 trans-pars plana vitrectomies of equine eyes with recurrent uveitis—follow-up until 18 years after surgery.. Pferdeheilkd.—Equine Med. 2021;37:204–214.
    doi: 10.21836/PEM20210301google scholar: lookup
  29. Baake EI, Borstel M.v., Rohn K, Boeve MH, Ohnesorge B. Long-term ophthalmologic examinations of eyes with equine recurrent uveitis after pars plana vitrectomy.. Pferdeheilkd.—Equine Med. 2019;35:220–233.
    doi: 10.21836/PEM20190303google scholar: lookup
  30. Von Borstel M, Von Oppen T, Glitz F, Fruhauf B, Deegen E, Boeve M, Ohnesorge B. Long-term results of pars-plana (double-port) vitrectomy in equine recurrent uveitis.. Pferdeheilkunde 2005;21:13–18.
    doi: 10.21836/PEM20050102google scholar: lookup
  31. Frühauf B, Ohnesorge B, Deegen E, Boevé M. Surgical management of equine recurrent uveitis with single port pars plana vitrectomy.. Vet. Ophthalmol. 1998;1:137–151.
  32. Baake EI, von Borstel M, Rohn K, Ohnesorge B. Detection of intraocular leptospiral DNA, antibodies and Leptospira spp. in horses with equine recurrent uveitis in different laboratories.. Pferdeheilkunde 2016;32:346–356.
    doi: 10.21836/PEM20160407google scholar: lookup
  33. Von Borstel MV, Oey L, Strutzberg-Minder K, Boeve MH, Ohnesorge B. Direct and indirect detection of leptospires in vitreal samples of horses with ERU.. Pferdeheilkunde 2010;26:219–225.
    doi: 10.21836/PEM20100217google scholar: lookup
  34. Toemoerdy E, Haessig M, Spiess BM. The outcome of pars plana vitrectomy in horses with equine recurrent uveitis with regard to the presence or absence of intravitreal antibodies against various serovars of Leptospira interrogans.. Pferdeheilkunde 2010;26:251–254.
    doi: 10.21836/PEM20100222google scholar: lookup
  35. Dorrego-Keiter E, Tóth J, Dikker L, Sielhorst J, Schusser GF. Detection of leptospira by culture of vitreous humor and detection of antibodies against leptospira in vitreous humor and serum of 225 horses with equine recurrent uveitis.. Berl. Munch. Tierarztl. Wochenschr. 2016;129:209–215.
    pubmed: 27344913
  36. Voelter K, Vial Z, Pot SA, Spiess BM. Leptospiral antibody prevalence and surgical treatment outcome in horses with Equine Recurrent Uveitis (ERU) in Switzerland.. Vet. Ophthalmol. 2020;23:648–658.
    doi: 10.1111/vop.12767pubmed: 32352624google scholar: lookup
  37. Wollanke B, Rohrbach BW, Gerhards H. Serum and vitreous humor antibody titers in and isolation of Leptospira interrogans from horses with recurrent uveitis.. J. Am. Vet. Med. Assoc. 2001;219:795–800.
    doi: 10.2460/javma.2001.219.795pubmed: 11561656google scholar: lookup
  38. Geiger T, Gerhards H, Wollanke B. Detection of Anti-LipL32 Antibodies in Serum Samples from Horses with Chronic Intraocular Infection with Leptospira spp.. Pathogens 2021;10:1325.
    doi: 10.3390/pathogens10101325pmc: PMC8537251pubmed: 34684272google scholar: lookup
  39. Loibl JK, Gerhards H, Brem S, Wollanke B. Improving the laboratory diagnosis of leptospiral uveitis in horses by using an indirect ELISA for the detection of antibodies against Leptospira spp. in intraocular samples.. Pferdeheilkunde—Equine Med. 2018;34:267–277.
    doi: 10.21836/PEM20180308google scholar: lookup
  40. Gesell S. Doctoral Thesis. Ludwig-Maximilians-University (LMU); Munich, Germany: 2004. [(accessed on 25 June 2022)]. [Is there an Asymptomatic Intraocular Leptospiral Infection in Horses?] Gibt es eine Asymptomatische Intraokulare Leptospireninfektion beim Pferd? Available online: https://edoc.ub.uni-muenchen.de/2527/1/Gesell_Stefan.pdf.. .
    doi: 10.5282/edoc.2527google scholar: lookup
  41. Kettner H. Doctoral Thesis. Ludwig-Maximilians-University; Munich, Germany: 1997. Untersuchungen zur klinischen Epizootiologie und Diagnostik der Leptospireninfektion beim Pferd. [Studies On the Clinical Epizootiology and Diagnosis of Leptospiral Infection in the Horse]. .
  42. Richter K, Lange S. Methods for evaluating diagnosis.. Internist. 1997;38:325–336.
    doi: 10.1007/s001080050044pubmed: 9213571google scholar: lookup
  43. Landis JR, Koch GG. The measurement of observer agreement for categorical data.. Biometrics 1977;33:159–174.
    doi: 10.2307/2529310pubmed: 843571google scholar: lookup
  44. Gsell O, Rehsteiner K, Verrey F. Iridocyclitis als Spätfolge von Leptospirosis Pomona (Schweinehüterkrankheit). Agglutinin- und Lymphozytose-Befund im Kammerwasser [Iridocyclitis as a late sequela of Leptospirosis Pomona (porter’s disease): Agglutinin and lymphocytosis in the aqueous humor]. Ophthalmologica 1946;112:320–334.
    doi: 10.1159/000300399pubmed: 20293718google scholar: lookup
  45. Hartwigk H, Stoebbe E. Kultureller Nachweis von Leptospiren bei Hund und Pferd.. Berl. Munch. Tierarztl. Wschr. 1952;65:212–214.
  46. Kemenes F, Surján J, Vizy L. Leptospira as the cause of periodic ophthalmia in horses.. Magyar Allatorvosok Lapja 1960;15:253–257.
  47. Williams RD, Morter RL, Freeman MJ, Lavignette AM. Experimental chronic uveitis. Ophthalmic signs following equine leptospirosis.. Investig. Ophthalmol. 1971;10:948–954.
    pubmed: 5128770
  48. Gelatt KN, Peiffer RL Jr, Gwin RM, Williams LW. The status of equine ophthalmology.. J. Equine Med. Surg. 1977;1:13–19.
  49. Goldmann H, Witmer R. Antibodies in the aqueous humor.. Ophthalmologica 1954;127:323–330.
    doi: 10.1159/000301976pubmed: 13176931google scholar: lookup
  50. Witmer RH. Ätiologische Diagnostik der Uveitis. I. Klinische und experimentelle Ergebnisse an Mensch und Tier [Etiological diagnosis of uveitis. I. Clinical and experimental results in man and animal]. Albrecht Von Graefes Arch. Ophthalmol. 1955;156:235–260.
    doi: 10.1007/BF00684419pubmed: 13248800google scholar: lookup
  51. Zwierzchowski J. Klinik und Therapie der Leptospirosen der Haus- und Nutztiere.. In: Kathe J., Mochmann H., editors. Leptospiren und Leptospirosen. Volume I. Gustav Fischer Verlag; Jena, Germany: 1967. pp. 79–137.
  52. Witmer R. Clinical implications of aqueous humor studies in uveitis.. Am. J. Ophthalmol. 1978;86:39–44.
    doi: 10.1016/0002-9394(78)90012-0pubmed: 354395google scholar: lookup
  53. Remky H, Kuchle HJ, Vollberchtshausen R. Quantitative serological studies in suspected toxoplasmosis of the eye.. Klin. Monatsbl. Augenheilkd. Augenarztl. Fortbild. 1957;130:794–800.
    pubmed: 13482145
  54. Dussaix E, Cerqueti PM, Pontet F, Bloch-Michel E. New approaches to the detection of locally produced antiviral antibodies in the aqueous of patients with endogenous uveitis.. Ophthalmologica 1987;194:145–149.
    doi: 10.1159/000309752pubmed: 3302799google scholar: lookup
  55. De Visser L. Proefschrift. Utrecht University; Utrecht, The Netherlands: 2009. [(accessed on 20 August 2022)]. Infectious Uveitis—New Developments in Etiology and Pathogenesis, Chapter 1: Etiology and Diagnosis of Infectious Uveitis. Intraocular Fluid Analysis. Available online: https://dspace.library.uu.nl/handle/1874/36951.. .
  56. Pleyer U, Ruokonen P. Aqueous humor analysis: A diagnostic tool in intraocular inflammation.. Klin. Monbl. Augenheilkd. 2010;227:953–960.
    doi: 10.1055/s-0029-1245927pubmed: 21157665google scholar: lookup
  57. de Groot-Mijnes JD, de Visser L, Zuurveen S, Martinus RA, Völker R, ten Dam-van Loon NH, de Boer JH, Postma G, de Groot RJ, van Loon AM. Identification of new pathogens in the intraocular fluid of patients with uveitis.. Am. J. Ophthalmol. 2010;150:628–636.
    doi: 10.1016/j.ajo.2010.05.015pmc: PMC7093850pubmed: 20691420google scholar: lookup
  58. Rothova A, de Boer JH, Ten Dam-van Loon NH, Postma G, de Visser L, Zuurveen SJ, Schuller M, Weersink AJ, van Loon AM, de Groot-Mijnes JD. Usefulness of aqueous humor analysis for the diagnosis of posterior uveitis.. Ophthalmology 2008;115:306–311.
    doi: 10.1016/j.ophtha.2007.05.014pubmed: 17669497google scholar: lookup
  59. De Groot-Mijnes JD, De Visser L, Rothova A, Schuller M, Van Loon AM, Weersink AJ. Rubella virus is associated with fuchs heterochromic iridocyclitis.. Am. J. Ophthalmol. 2006;141:212–214.
    doi: 10.1016/j.ajo.2005.07.078pubmed: 16387009google scholar: lookup
  60. Robert-Gangneux F, Binisti P, Antonetti D, Brezin A, Yera H, Dupouy-Camet J. Usefulness of immunoblotting and Goldmann-Witmer coefficient for biological diagnosis of toxoplasmic retinochoroiditis.. Eur. J. Clin. Microbiol. Infect. Dis. 2004;23:34–38.
    doi: 10.1007/s10096-003-1048-6pubmed: 14669070google scholar: lookup
  61. De Groot-Mijnes JD, Rothova A, Van Loon AM, Schuller M, Ten Dam-Van Loon NH, De Boer JH, Schuurman R, Weersink AJ. Polymerase chain reaction and Goldmann-Witmer coefficient analysis are complimentary for the diagnosis of infectious uveitis.. Am. J. Ophthalmol. 2006;141:313–318.
    doi: 10.1016/j.ajo.2005.09.017pubmed: 16458686google scholar: lookup
  62. Wollanke B. Habilitation Thesis. Ludwig-Maximilians-University (LMU); Munich, Germany: 2002. Equine Recurrent Uveitis (ERU) as an Intraocular Leptospirosis.. .
  63. Halliwell RE, Brim TA, Hines MT, Wolf D, White FH. Studies on equine recurrent uveitis. II: The role of infection with Leptospira interrogans serovar pomona.. Curr. Eye Res. 1985;4:1033–1040.
    doi: 10.3109/02713688509003348pubmed: 3877614google scholar: lookup
  64. Gilger BC, Salmon JH, Yi NY, Barden CA, Chandler HL, Wendt JA, Colitz CM. Role of bacteria in the pathogenesis of recurrent uveitis in horses from the southeastern United States.. Am. J. Vet. Res. 2008;69:1329–1335.
    doi: 10.2460/ajvr.69.10.1329pubmed: 18828691google scholar: lookup
  65. Sauvage AC, Monclin SJ, Elansary M, Hansen P, Grauwels MF. Detection of intraocular Leptospira spp. by real-time polymerase chain reaction in horses with recurrent uveitis in Belgium.. Equine Vet. J. 2019;51:299–303.
    doi: 10.1111/evj.13012pubmed: 30144314google scholar: lookup
  66. Malalana F, Blundell RJ, Pinchbeck GL, McGowan CM. The role of Leptospira spp. in horses affected with recurrent uveitis in the UK.. Equine Vet. J. 2017;49:706–709.
    doi: 10.1111/evj.12683pmc: PMC5655720pubmed: 28321895google scholar: lookup
  67. Stein-Streilein J. Mechanisms of immune privilege in the posterior eye.. Int. Rev. Immunol. 2013;32:42–56.
    doi: 10.3109/08830185.2012.740535pubmed: 23360157google scholar: lookup
  68. Zhou R, Caspi RR. Ocular immune privilege.. F1000 Biol. Rep. 2010;2:3.
    doi: 10.3410/B2-3pmc: PMC2948372pubmed: 20948803google scholar: lookup
  69. Grisanti S. Immune privilege of the eye.. Ophthalmologe 1998;95:124–135.
    doi: 10.1007/s003470050250pubmed: 9545793google scholar: lookup
  70. Lavach JD. Large Animal Ophthalmology.. C. W. Mosby Company; St. Louis, MO, USA: 1990. Periodic ophthalmia; pp. 162–171.
  71. Pearce JW, Galle LE, Kleiboeker SB, Turk JR, Schommer SK, Dubielizig RR, Mitchell WJ, Moore CP, Giuliano EA. Detection of Leptospira interrogans DNA and antigen in fixed equine eyes affected with end-stage equine recurrent uveitis.. J. Vet. Diagn. Investig. 2007;19:686–690.
    doi: 10.1177/104063870701900611pubmed: 17998558google scholar: lookup
  72. Dorrego-Keiter E, Tóth J, Dikker L, Sielhorst J, Schusser G. Long-term results of pars plana vitrectomy in relationship to leptospiral antibody detection in vitreous humor in 118 horses with equine recurrent uveitis (ERU). Pferdeheilkunde 2017;33:112–118.
    doi: 10.21836/PEM20170201google scholar: lookup
  73. Thibeaux R, Soupé-Gilbert ME, Kainiu M, Girault D, Bierque E, Fernandes J, Bähre H, Douyère A, Eskenazi N, Vinh J. The zoonotic pathogen Leptospira interrogans mitigates environmental stress through cyclic-di-GMP-controlled biofilm production.. NPJ Biofilms Microbiomes 2020;6:24.
    doi: 10.1038/s41522-020-0134-1pmc: PMC7293261pubmed: 32532998google scholar: lookup