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Endolymphatic sac involvement in bacterial meningitis

  • Otology
  • Published:
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Abstract

The commonest sequelae of bacterial meningitis are related to the inner ear. Little is known about the inner ear immune defense. Evidence suggests that the endolymphatic sac provides some protection against infection. A potential involvement of the endolymphatic sac in bacterial meningitis is largely unaccounted for, and thus the object of the present study. A well-established adult rat model of Streptococcus pneumoniae meningitis was employed. Thirty adult rats were inoculated intrathecally with Streptococcus pneumoniae and received no additional treatment. Six rats were sham-inoculated. The rats were killed when reaching terminal illness or on day 7, followed by light microscopy preparation and PAS-Alcian blue staining. The endolymphatic sac was examined for bacterial invasion and leukocyte infiltration. Neither bacteria nor leukocytes infiltrated the endolymphatic sac during the first days. Bacteria invaded the inner ear through the cochlear aquaduct. On days 5–6, the bacteria invaded the endolymphatic sac through the endolymphatic duct subsequent to invasion of the vestibular endolymphatic compartment. No evidence of direct bacterial invasion of the sac through the meninges was found. Leukocyte infiltration of the sac occurred prior to bacterial invasion. During meningitis, bacteria do not invade the endolymphatic sac through the dura, but solely through the endolymphatic duct, following the invasion of the vestibular system. Leukocyte infiltration of the sac occurs prior to, as well as concurrent with bacterial invasion. The findings support the endolymphatic sac as part of an innate immune defense system protecting the inner ear from infection.

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References

  1. Rasmussen N, Johnsen NJ, Bohr VA (1991) Otologic sequelae after pneumococcal meningitis: a survey of 164 consecutive cases with a follow-up of 94 survivors. Laryngoscope 101:876–882

    Article  CAS  PubMed  Google Scholar 

  2. Worsøe L, Cayé-Thomasen P, Brandt CT, Thomsen J, Østergaard C (2010) Factors associated with the occurrence of hearing loss after pneumococcal meningitis. Clin Infect Dis 51(8):917–924

    Article  PubMed  Google Scholar 

  3. Cushing SL, Papsin BC, Rutka JA et al (2009) Vestibular end-organ and balance deficits after meningitis and cochlear implantation in children correlate poorly with functional outcome. Otol Neurotol 30(4):488–495

    Article  PubMed  Google Scholar 

  4. Zingler VC, Weintz E, Jahn K et al (2009) Causative factors, epidemiology, and follow-up of bilateral vestibulopathy. Ann NY Acad Sci 1164:505–508

    Article  PubMed  Google Scholar 

  5. Merchant SN, Gopen Q (1996) A human temporal bone study of acute bacterial meningogenic labyrinthitis. Am J Otol 17:375–385

    CAS  PubMed  Google Scholar 

  6. Bhatt S, Halpin C, Hsu W et al (1991) Hearing loss and pneumococcal meningitis: an animal model. Laryngoscope 101:1285–1292

    Article  CAS  PubMed  Google Scholar 

  7. Caye-Thomasen P, Worsoe L, Brandt CT et al (2009) Routes, dynamics, and correlates of cochlear inflammation in terminal and recovering experimental meningitis. Laryngoscope 119(8):1560–1570

    Article  PubMed  Google Scholar 

  8. Osborne MP, Comis SD, Tarlow MJ, Stephen J (1995) The cochlear lesion in experimental bacterial meningitis of the rabbit. Int J Exp Pathol 76:317–330

    PubMed Central  CAS  PubMed  Google Scholar 

  9. Brandt CT, Cayé-Thomasen P, Lund SP, Worsøe L, Ostergaard C, Frimodt-Møller N, Espersen F, Thomsen J, Lundgren JD (2006) Hearing loss and cochlear damage in experimental pneumococcal meningitis, with special reference to the role of neutrophil granulocytes. Neurobiol Dis 23(2):300–311

    Article  CAS  PubMed  Google Scholar 

  10. Winter AJ, Comis SD, Osborne MP, Tarlow MJ, Stephen J, Andrew PW, Hill J, Mitchell TJ (1997) A role for pneumolysin but not neuraminidase in the hearing loss and cochlear damage induced by experimental pneumococcal meningitis in guinea pigs. Infect Immun 65(11):4411–4418

    PubMed Central  CAS  PubMed  Google Scholar 

  11. Møller MN, Brandt CT, Ostergaard C, Caye-Thomasen P (2013) Bacterial invasion of the inner ear during pneumococcal meningitis. Accepted Otol Neurotol

  12. Hausler R, Toupet M, Guidetti G, Basseres F, Montandon P (1987) Menière’s disease in children. Am J Otolaryngol 8(4):187–193

    Article  CAS  PubMed  Google Scholar 

  13. Tomiyama S, Harris JP (1986) The endolymphatic sac: its importance in inner ear immune responses. Laryngoscope 96:685–691

    Article  CAS  PubMed  Google Scholar 

  14. Tomiyama S, Harris JP (1987) The role of the endolymphatic sac in inner ear immunity. Acta Otolaryngol (Stockh) 103:182–188

    Article  Google Scholar 

  15. Gloddek B, Arnold W (1998) The endolymphatic sac receives antigenetic information from the organs of the mucosa-associated lymphatic system. Acta Otolaryngol 118(3):333–336

    Article  CAS  PubMed  Google Scholar 

  16. Rask-Andersen H, Stahle J (1980) Immunodefence of the inner ear? Lymphocyte-macrophage interaction in the endolymphatic sac. Acta Otolaryngol 89(3–4):283–294

    Article  CAS  PubMed  Google Scholar 

  17. Kastenbauer S, Klein M, Koedel U, Pfister HW (2001) Reactive nitrogen species contribute to blood-labyrinth barrier disruption in suppurative labyrinthitis complicating experimental pneumococcal meningitis in the rat. Brain Res 904(2):208–217

    Article  CAS  PubMed  Google Scholar 

  18. Brandt CT, Lundgren JD, Lund SP, Frimodt-Møller N, Christensen T, Benfield T, Espersen F, Hougaard DM (2004) Attenuation of the bacterial load in blood by pretreatment with granulocyte-colony-stimulating factor protects rats from fatal outcome and brain damage during Streptococcus pneumoniae meningitis. Østergaard CInfect Immun 72(8):4647–4653

    Article  CAS  Google Scholar 

  19. Leib SL, Kim YSM, Ferriero DM, Tauber MG (1996) Neuroprotective effect of excitatory amino acid antagonist kynurenic acid in experimental bacterial meningitis. J Infect Dis 173:166–171

    Article  CAS  PubMed  Google Scholar 

  20. Fusaro RM, Goltz RW (1960) A comparative study of the periodic acid-schiff and alcian blue stains. J Invest Dermatol 35:305–307

    Article  CAS  PubMed  Google Scholar 

  21. Salt AN, Rask-Andersen H (2004) Responses of the endolymphatic sac to perilymphatic injections and withdrawals: evidence for the presence of a one-way valve. Hear Res 191(1–2):90–100

    Article  PubMed  Google Scholar 

  22. Kugelberg E, Gollan B, Tang CM (2008) Mechanisms in Neisseria meningitidis for risistance against complement-mediated killing. Vaccine 26(6):I34–I39

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Southwick FS, Purich DL (1996) Intracellular pathogenesis of listeriosis. N Engl J Med 334:770–776

    Article  CAS  PubMed  Google Scholar 

  24. Satoh H, Firestein GS, Billings PB, Harris JP, Keithley EM (2003) Proinflammatory cytokine expression in the endolymphatic sac during inner ear inflammation. J Assoc Res Otolaryngol 4(2):139–147

    Article  PubMed Central  PubMed  Google Scholar 

  25. Rask-Andersen H, Danckwardt-Lillieström N, Friberg U, House W (1991) Lymphocyte-macrophage activity in the human endolymphatic sac. Acta Otolaryngol Suppl 485:15–17

    Article  CAS  PubMed  Google Scholar 

  26. Møller MN, Caye-Tomasen P, Qvortrup K (2013) Oxygenated fixation demonstrates novel and improved ultrastructural features of the human endolymphatic sac. Laryngoscope 123(8):1967–1975. doi:10.1002/lary.23929

    Article  PubMed  Google Scholar 

  27. Altermatt HJ, Gebbers J, Müller C, Laissue J, Arnold W (1992) Immunohistochemical characterization of the human endolymphatic sac and its associated cell populations. Acta Otolaryngol (stockh) 112:299–305

    CAS  Google Scholar 

  28. Friis M, Martin-Bertelsen T, Friis-Hansen L, Winther O, Henao R, Sørensen MS, Qvortrup K (2011) Gene expression of the endolymphatic sac. Acta Otolaryngol 131(12):1257–1263 Epub 2011 Oct 23

    Article  CAS  PubMed  Google Scholar 

  29. Wackym PA, Friberg U, Linthicum FH Jr, Bagger-Sjöback D, Bui HT, Hofman F, Rask-Andersen H (1987) Human endolymphatic sac: morphologic evidence of immunologic function. Ann Otol Rhinol Laryngol 96(3 Pt 1):276–281

    CAS  PubMed  Google Scholar 

  30. Yeo SW, Gottteschilch S, Harris JP, Keithley EM (1995) Antigen diffusion from the perilymphatic space of the cochlea. Laryngoscope 105:623–628

    Article  CAS  PubMed  Google Scholar 

  31. Yimtae K, Song H, Billings P, Harris JP, Keithley EM (2001) Connection between the inner ear and the lymphatic system. Laryngoscope 111:1631–1635

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

All financial support for this work was funded solely through public institutional funds.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Oto-Rhino-Laryngology, Head and Neck Surgery, University Hospital Rigshospitalet/Gentofte, 2100, Copenhagen, Denmark

    Martin Nue Møller & Per Caye-Thomasen

  2. Department of Infectious Diseases, Copenhagen University Hospital Hvidovre, Kettegård Alle 30, 2650, Hvidovre, Denmark

    Christian Brandt

  3. Department of Clinical Microbiology, Copenhagen University Hospital Hvidovre, Kettegård Alle 30, 2650, Hvidovre, Denmark

    Christian Østergaard

  4. The Faculty of Health and Medical Sciences, University of Copenhagen, Copenhagen, Denmark

    Per Caye-Thomasen

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  1. Martin Nue Møller
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  2. Christian Brandt
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  4. Per Caye-Thomasen
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Correspondence to Martin Nue Møller.

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Møller, M.N., Brandt, C., Østergaard, C. et al. Endolymphatic sac involvement in bacterial meningitis. Eur Arch Otorhinolaryngol 272, 843–851 (2015). https://doi.org/10.1007/s00405-014-2884-y

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  • DOI: https://doi.org/10.1007/s00405-014-2884-y

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