Advertisement

Pathological Consequences of Reduced Cerebrospinal Fluid Pressure: Experimental Studies

  • Zheng Zhang
  • Jing Li
  • Xiaoxia Li
  • Ningli WangEmail author
Chapter
Part of the Modeling and Simulation in Science, Engineering and Technology book series (MSSET)

Abstract

It has been speculated that a low orbital cerebrospinal fluid pressure (CSFP) may perhaps play a role in the pathogenesis of glaucomatous optic neuropathy. To verify the hypothesis, we conducted a serial of experimental study on low-CSFP models of monkeys and rats. Our studies showed that a reduction in CSFP could result in the structural and physiological changes of optic nerve and some molecular biology reactions in the optic axons. We hope that our chapter will be helpful for the further research in the pathogenesis of glaucoma.

References

  1. 1.
    Morgan WH, Yu DY, Cooper RL, et al. The influence of cerebrospinal fluid pressure on the lamina cribrosa tissue pressure gradient. Invest Ophthalmol Vis Sci. 1995;36:1163–1172.Google Scholar
  2. 2.
    Morgan WH, Chauhan BC, Yu DY, et al. Optic disc movement with variations in intraocular and cerebrospinal fluid pressure. Invest Ophthalmol Vis Sci. 2002;43:3236–3242.Google Scholar
  3. 3.
    Jonas JB, Berenshtein E, Holbach L. Anatomic relationship between lamina cribrosa, intraocular space, and cerebrospinal fluid space. Invest Ophthalmol Vis Sci. 2003;44:5189–5195.CrossRefGoogle Scholar
  4. 4.
    Morgan WH, Yu DY, Balaratnasingam C. The role of cerebrospinal fluid pressure in glaucoma pathophysiology: the dark side of the optic disc. J Glaucoma. 2008;17:408–413.CrossRefGoogle Scholar
  5. 5.
    Berdahl JP, Allingham RR, Johnson DH. Cerebrospinal fluid pressure is decreased in primary open-angle glaucoma. Ophthalmology. 2008;115:763–768.CrossRefGoogle Scholar
  6. 6.
    Ren R, Jonas JB, Tian G, et al. Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology. 2010;117: 259–266.CrossRefGoogle Scholar
  7. 7.
    Hiraoka M, Inoue K, Ninomiya T, Takada M. Ischaemia in the Zinn-Haller circle and glaucomatous optic neuropathy in macaque monkeys. Br J Ophthalmol. 2012;96:597-603.CrossRefGoogle Scholar
  8. 8.
    Križaj D, Ryskamp DA, Tian N, et al. From mechanosensitivity to inflammatory responses: new players in the pathology of glaucoma. Curr Eye Res. 2014;39:105-119.CrossRefGoogle Scholar
  9. 9.
    Cherecheanu AP, Garhofer G, Schmidl D, Werkmeister R, Schmetterer L. Ocular perfusion pressure and ocular blood flow in glaucoma. Curr Opin Pharmacol. 2013;13:36-42.CrossRefGoogle Scholar
  10. 10.
    Leske MC. Ocular perfusion pressure and glaucoma: clinical trial and epidemiologic findings. Curr Opin Ophthalmol. 2009;20:73-78.CrossRefGoogle Scholar
  11. 11.
    Chrysostomou V, Rezania F, Trounce IA, Crowston JG. Oxidative stress and mitochondrial dysfunction in glaucoma. Curr Opin Pharmacol. 2013;13:12-15.CrossRefGoogle Scholar
  12. 12.
    Zhang Z, Liu D, Jonas JB, et al. Glaucoma and the Role of Cerebrospinal Fluid Dynamics. Invest Ophthalmol Vis Sci. 2015;56:6632.CrossRefGoogle Scholar
  13. 13.
    Zhang Z, Wu S, Jonas JB, et al. Dynein, kinesin and morphological changes in optic nerve axons in a rat model with cerebrospinal fluid pressure reduction: the Beijing Intracranial and Intraocular Pressure (iCOP) study. Acta Ophthalmol. 2016;94:266-75.CrossRefGoogle Scholar
  14. 14.
    Zhang Z, Liu D, Jonas JB, et al. Axonal Transport in the Rat Optic Nerve Following Short-Term Reduction in Cerebrospinal Fluid Pressure or Elevation in Intraocular Pressure. Invest Ophthalmol Vis Sci. 2015;56:4257-4266.CrossRefGoogle Scholar
  15. 15.
    Wangsa-Wirawan ND, Linsenmeier RA. Retinal oxygen: fundamental and clinical aspects. Arch Ophthalmol 2003; 121:547–557.CrossRefGoogle Scholar
  16. 16.
    Geirsdottir A, Hardarson SH, Olafsdottir OB, Stefánsson E. Retinal oxygen metabolism in exudative age-related macular degeneration. Acta Ophthalmologica 2014; 92: 27–33.CrossRefGoogle Scholar
  17. 17.
    Hardarson SH, Stefansson E. Retinal oxygen saturation is altered in diabetic retinopathy. Br J Ophthalmol 2012; 96:560–563.CrossRefGoogle Scholar
  18. 18.
    Hammer M, Heller T, Jentsch S, Dawczynski J, Schweitzer D, Peters S, et al. Retinal Vessel Oxygen Saturation under Flicker Light Stimulation in Patients with Nonproliferative Diabetic Retinopathy. Invest Ophthalmol Vis Sci 2012; 53: 4063–4068.CrossRefGoogle Scholar
  19. 19.
    Hardarson SH, Stefansson E. Oxygen saturation in central retinal vein occlusion. Am J Ophthalmol 2010; 150:871–875.CrossRefGoogle Scholar
  20. 20.
    Eliasdottir TS, Bragason D, Hardarson SH, Kristjansdottir G, Stefánsson E. Venous oxygen saturation is reduced and variable in central retinal vein occlusion. Graefes Arch Clin Exp Ophthalmol 2015;253:1653–1661.CrossRefGoogle Scholar
  21. 21.
    Hardarson SH, Stefánsson E. Oxygen saturation in branch retinal vein occlusion. Acta Ophthalmologica 2011; 90: 466–470.CrossRefGoogle Scholar
  22. 22.
    Tobe LA, Harris A, Schroeder A, Gerber A, Holland S, Amireskandari A, et al. Retinal oxygen saturation and metabolism: how does it pertain to glaucoma? An update on the application of retinal oximetry in glaucoma. Eur J Ophthalmol 2013; 23:465–472.CrossRefGoogle Scholar
  23. 23.
    Vandewalle E, Abegao Pinto L, Olafsdottir OB, De Clerck E, Stalmans P, Van Calster J, et al. Oximetry in glaucoma: correlation of metabolic change with structural and functional damage. Acta Ophthalmol 2014; 92:105–110.CrossRefGoogle Scholar
  24. 24.
    Hardarson SH, Harris A, Karlsson RA, Halldorsson GH, Kagemann L, Rechtman E, et al. Automatic retinal oximetry. Invest Ophthalmol Vis Sci 2006; 47:5011–5016.CrossRefGoogle Scholar
  25. 25.
    Hardarson SH. Protocol for Analysis of Oxymap T1 Oximetry Images. Reykjavik, Iceland: Oxymap;2011.Google Scholar
  26. 26.
    Jani PD, Mwanza J-C, Billow KB, Waters AM, Moyer S, Garg S. Normative values and predictors of retinal oxygen saturation. Retina 2014; 34: 394–401.CrossRefGoogle Scholar
  27. 27.
    Geirsdottir A, Palsson O, Hardarson SH, Olafsdottir OB, Kristjansdottir JV, Stefansson E. Retinal Vessel Oxygen Saturation in Healthy Individuals. Invest Ophthalmol Vis Sci 2012; 53: 5433–5442.CrossRefGoogle Scholar
  28. 28.
    Yip W, Siantar R, Perera SA, Milastuti N, Ho KK, Tan B, et al. Reliability and determinants of retinal vessel oximetry measurements in healthy eyes. Invest Ophthalmol Vis Sci 2014; 55:7104–7110.CrossRefGoogle Scholar
  29. 29.
    Mohan A, Dabir S, Yadav NK, Kummelil M, Kumar RS, Shetty R. Normative Database of Retinal Oximetry in Asian Indian Eyes. PLoS ONE 2015; 10: e0126179.CrossRefGoogle Scholar
  30. 30.
    Man REK, Sasongko MB, Kawasaki R, Noonan JE, Lo TC, Luu CD, et al. Associations of retinal oximetry in healthy young adults. Invest Ophthalmol Vis Sci 2014; 55:1763–1769.CrossRefGoogle Scholar
  31. 31.
    Türksever C, Orgül S, Todorova MG. Reproducibility of retinal oximetry measurements in healthy and diseased retinas. Acta Ophthalmol 2015; 93: e439–e445.CrossRefGoogle Scholar
  32. 32.
    Burgoyne CF, Downs JC. Premise and prediction-how optic nerve head biomechanics underlies the susceptibility and clinical behavior of the aged optic nerve head. J Glaucoma 2008,17(4):318-328.CrossRefGoogle Scholar
  33. 33.
    Fechtner RD, Weinreb RN. Mechanisms of optic nerve damage in primary open angle glaucoma. Surv Ophthalmol 1994, 39(1):23-42.CrossRefGoogle Scholar
  34. 34.
    Leske MC. Ocular perfusion pressure and glaucoma: clinical trial and epidemiologic findings. Curr Opin Ophthalmol 2009, 20(2):73-78.CrossRefGoogle Scholar
  35. 35.
    Schmidl D, Garhofer G, Schmetterer L. The complex interaction between ocular perfusion pressure and ocular blood flow - relevance for glaucoma. Exp Eye Res. 2011;93(2):141-55.CrossRefGoogle Scholar
  36. 36.
    Suh MH, Park KH, Kim H, Kim TW, Kim SW, Kim SY, Kim DM. Glaucoma progression after the first-detected optic disc hemorrhage by optical coherence tomography. J Glaucoma. 2012;21(6):358-66.CrossRefGoogle Scholar
  37. 37.
    Seidensticker F, Reznicek L, Mann T, Hübert I, Kampik A, Ulbig M, Hirneiss C, Neubauer AS, Kernt M. Assessment of β-zone peripapillary atrophy by optical coherence tomography and scanning laser ophthalmoscopy imaging in glaucoma patients. Clin Ophthalmol. 2014;8:1233-9.Google Scholar
  38. 38.
    Jia Y, Tan O, Tokayer J, Potsaid B, Wang Y, Liu JJ, Kraus MF, Subhash H, Fujimoto JG, Hornegger J, Huang D. Split-spectrum amplitude-decorrelation angiography with optical coherence tomography. Opt Express. 2012;20(4):4710-25.Google Scholar
  39. 39.
    Jia Y, Morrison JC, Tokayer J, Tan O, Lombardi L, Baumann B, Lu CD, Choi W, Fujimoto JG, Huang D. Quantitative OCT angiography of optic nerve head blood flow. Biomed Opt Express. 2012;3(12):3127-37.CrossRefGoogle Scholar
  40. 40.
    Wei E, Jia Y, Tan O, Potsaid B, Liu JJ, Choi W, Fujimoto JG, Huang D. Parafoveal retinal vascular response to pattern visual stimulation assessed with OCT angiography. PLoS One. 2013 Dec 2;8(12):e81343.CrossRefGoogle Scholar
  41. 41.
    Jia Y, Wei E, Wang X, Zhang X, Morrison JC, Parikh M, Lombardi LH, Gattey DM, Armour RL, Edmunds B, Kraus MF, Fujimoto JG, Huang D. Optical coherence tomography angiography of optic disc perfusion in glaucoma. Ophthalmology. 2014;121(7):1322-32.CrossRefGoogle Scholar
  42. 42.
    Jia Y, Bailey ST, Wilson DJ, Tan O, Klein ML, Flaxel CJ, Potsaid B, Liu JJ, Lu CD, Kraus MF, Fujimoto JG, Huang D. Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration. Ophthalmology. 2014;121(7):1435-44.CrossRefGoogle Scholar
  43. 43.
    Kuehlewein L, Sadda SR, Sarraf D. OCT angiography and sequential quantitative analysis of type 2 neovascularization after ranibizumab therapy. Eye (Lond). 2015;29(7):932-5.CrossRefGoogle Scholar
  44. 44.
    Yu J, Jiang C, Wang X, Zhu L, Gu R, Xu H, Jia Y, Huang D, Sun X. Macular perfusion in healthy Chinese: an optical coherence tomography angiogram study. Invest Ophthalmol Vis Sci. 2015;56(5):3212-7.CrossRefGoogle Scholar
  45. 45.
    Pechauer AD, Jia Y, Liu L, Gao SS, Jiang C, Huang D. Optical coherence tomography angiography of peripapillary retinal blood flow response to hyperoxia. Invest Ophthalmol Vis Sci. 2015;56(5):3287-91.CrossRefGoogle Scholar
  46. 46.
    Vrabec JP, Levin LA. The neurobiology of cell death in glaucoma. Eye (Lond). 2007;21(suppl 1):S11–S14.CrossRefGoogle Scholar
  47. 47.
    Johnson EC, Guo Y, Cepurna WO, Morrison JC. Neurotrophin roles in retinal ganglion cell survival: lessons from rat glaucoma models. Exp Eye Res. 2009;88:808–815.CrossRefGoogle Scholar
  48. 48.
    Pease ME, McKinnon SJ, Quigley HA, Kerrigan-Baumrind LA, Zack DJ. Obstructed axonal transport of BDNF and its receptor TrkB in experimental glaucoma. Invest Ophthalmol Vis Sci. 2000;41:764–774.Google Scholar
  49. 49.
    Martin KR, Quigley HA, Valenta D, Kielczewski J, Pease ME. Optic nerve dynein motor protein distribution changes with intraocular pressure elevation in a rat model of glaucoma. Exp Eye Res. 2006;83:255–262.CrossRefGoogle Scholar
  50. 50.
    Minckler DS, Bunt AH, Johanson GW. Orthograde and retrograde axoplasmic transport during acute ocular hypertension in the monkey. Invest Ophthalmol Vis Sci. 1977;16: 426–441.Google Scholar
  51. 51.
    Johansson JO. Inhibition of retrograde axoplasmic transport in rat optic nerve by increased IOP in vitro. Invest Ophthalmol Vis Sci. 1983;24:1552–1558.Google Scholar
  52. 52.
    Abbott CJ, Choe TE, Lusardi TA, Burgoyne CF, Wang L, Fortune B. Evaluation of retinal nerve fiber layer thickness and axonal transport 1 and 2 weeks after 8 hours of acute intraocular pressure elevation in rats. Invest Ophthalmol Vis Sci. 2014;55: 674–687.CrossRefGoogle Scholar
  53. 53.
    Zhang S, Wang H, Lu Q, et al. Detection of early neuron degeneration and accompanying glial responses in the visual pathway in a rat model of acute intraocular hypertension. Brain research 2009;1303:131-143.CrossRefGoogle Scholar
  54. 54.
    Sapienza A, Raveu AL, Reboussin E, et al. Bilateral neuroinflammatory processes in visual pathways induced by unilateral ocular hypertension in the rat. Journal of neuroinflammation 2016;13:44.Google Scholar
  55. 55.
    Mac Nair CE, Schlamp CL, Montgomery AD, Shestopalov VI, Nickells RW. Retinal glial responses to optic nerve crush are attenuated in Bax-deficient mice and modulated by purinergic signaling pathways. Journal of neuroinflammation 2016;13:93.Google Scholar
  56. 56.
    Sun D, Qu J, Jakobs TC. Reversible reactivity by optic nerve astrocytes. Glia 2013;61:1218-1235.CrossRefGoogle Scholar
  57. 57.
    Dai Y, Sun X, Yu X, Guo W, Yu D. Astrocytic responses in the lateral geniculate nucleus of monkeys with experimental glaucoma. Veterinary ophthalmology 2012;15:23-30.CrossRefGoogle Scholar
  58. 58.
    Tehrani S, Davis L, Cepurna WO, et al. Astrocyte Structural and Molecular Response to Elevated Intraocular Pressure Occurs Rapidly and Precedes Axonal Tubulin Rearrangement within the Optic Nerve Head in a Rat Model. PloS one 2016;11:e0167364.CrossRefGoogle Scholar
  59. 59.
    Trost A, Motloch K, Bruckner D, et al. Time-dependent retinal ganglion cell loss, microglial activation and blood-retina-barrier tightness in an acute model of ocular hypertension. Experimental eye research 2015;136:59-71.CrossRefGoogle Scholar
  60. 60.
    Ramirez AI, Salazar JJ, de Hoz R, et al. Macro- and microglial responses in the fellow eyes contralateral to glaucomatous eyes. Progress in brain research 2015;220:155-172.Google Scholar
  61. 61.
    Tezel G, Fourth APORICWG. The role of glia, mitochondria, and the immune system in glaucoma. Investigative ophthalmology & visual science 2009;50:1001-1012.Google Scholar
  62. 62.
    Wang X, Su J, Ding J, et al. alpha-Aminoadipic acid protects against retinal disruption through attenuating Muller cell gliosis in a rat model of acute ocular hypertension. Drug design, development and therapy 2016;10:3449-3457.Google Scholar
  63. 63.
    Xue LP, Lu J, Cao Q, Hu S, Ding P, Ling EA. Muller glial cells express nestin coupled with glial fibrillary acidic protein in experimentally induced glaucoma in the rat retina. Neuroscience 2006;139:723-732.CrossRefGoogle Scholar
  64. 64.
    Kim EJ, Pellman B, Kim JJ. Stress effects on the hippocampus: a critical review. Learning & memory 2015;22:411-416.Google Scholar
  65. 65.
    Butenko O, Dzamba D, Benesova J, et al. The increased activity of TRPV4 channel in the astrocytes of the adult rat hippocampus after cerebral hypoxia/ischemia. PloS one 2012;7:e39959.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Zheng Zhang
    • 1
    • 2
  • Jing Li
    • 2
  • Xiaoxia Li
    • 2
  • Ningli Wang
    • 1
    • 2
    Email author
  1. 1.Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, Beijing Ophthalmology and Visual Sciences Key LaboratoryBeijingChina
  2. 2.Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical UniversityBeijingChina

Personalised recommendations