Special Cerebral and Cerebrospinal Features in Primary Open Angle Glaucoma and Normal Tension Glaucoma

Abstract

In addition to aqueous humour and blood, cerebrospinal fluid also plays an important part in the pathophysiology of primary open-angle glaucoma (POAG) and, in particular, normal-tension glaucoma (NTG). Apart from the important role of CSF pressure in papillary congestion, the composition of the CSF and its flow rate are relevant. CSF is in contact with the brain, the spinal canal and the optic nerve. In neurodegenerative disease, one potential pathophysiological factor, apart from an altered composition of the CSF, is a decrease in flow rate. Changes in CSF composition and flow rate have also been described in the perioptic subarachnoid space of the optic nerve in patients with normal tension glaucoma. Such findings indicate that primary open angle glaucoma and normal tension glaucoma especially, might be due to a neurodegenerative process.

Key words

normal tension glaucoma - cerebrospinal fluid - neurodegeneration - Alzheimer disease - primary open-angle glaucoma

• Literatur/References

• 1 Klein BE, Klein R, Sponsel WE. et al. Prevalence of glaucoma. The Beaver Dam Eye Study. Ophthalmology 1992; 99: 1499-1504
• 2 Cho HK, Kee C. Population-based glaucoma prevalence studies in Asians. Surv Ophthalmol 2014; 5: 434-447
• 3 Caprioli J, Spaeth GL. Comparison of the optic nerve head in high- and low-tension glaucoma. Arch Ophthalmol 1985; 103: 1145-1149
• 4 Cho HK, Kee C. Population-based glaucoma prevalence studies in Asians. Surv Ophthalmol 2014; 59: 434-447
• 5 Killer HE, Pircher A. Normal tension glaucoma: review of the current understanding and mechanisms of the pathogenesis. Eye (Lond) 2018; 32: 924-930
• 6 Mi XS, Yuan TF, So KF. The current research status of normal tension glaucoma. Clin Interv Aging 2014; 9: 1563-1571
• 7 Mastropasqua R, Fasanella V, Agnifili L. et al. Advance in the pathogenesis and treatment of normal-tension glaucoma. Prog Brain Res 2015; 221: 213-232
• 8 Mallick J, Devi L, Malik PK. et al. Update on normal tension glaucoma. J Ophthalmic Vis Res 2016; 11: 204-208
• 9 Collaborative Normal-Tension Glaucoma Study Group. The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Am J Ophthalmol 1998; 126: 498-505
• 10 Flammer J, Orgul S, Costa VP. et al. The impact of ocular blood flow in glaucoma. Prog Retin Eye Res 2002; 21: 359-393
• 11 Flammer J. The vascular concept of glaucoma. Surv Ophthalmol 1994; 38 (Suppl.) S3-S6
• 12 Pache M, Flammer J. A sick eye in a sick body? Systemic findings in patients with primary open angle glaucoma. Surv Ophthalmol 2006; 51: 179-212
• 13 Flammer J, Konieczka K. The discovery of the Flammer syndrome: a historical and personal perspective. EPMA J 2017; 8: 75-97
• 14 Kaeslin MA, Killer HE, Fuhrer CA. et al. Changes to the aqueous humor proteome during glaucoma. PLoS One 2016; 11: e0165314
• 15 Bauer G, Killer HE, Forrer A. et al. Lipocalin-like prostaglandin D synthase (L-PGDS) concentration in aqueous humour in patients with open-angle glaucoma. J Glaucoma 2014; 23: 164-168
• 16 Killer HE, Laeng HR, Flammer J. et al. Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations. Br J Ophthalmol 2003; 87: 777-781
• 17 Whedon JM, Glassey D. Cerebrospinal fluid stasis and its clinical significance. Altern Ther Health Med 2009; 15: 54-60
• 18 Silverberg GD, Mayo M, Saul T. et al. Alzheimerʼs disease, normal-pressure hydrocephalus, and senescent changes in CSF circulatory physiology: a hypothesis. Lancet Neurol 2003; 2: 506-511
• 19 Wostyn P, De Groot V, Van Dam D. et al. Senescent changes in cerebrospinal fluid circulatory physiology and their role in the pathogenesis of normal-tension glaucoma. Am J Ophthalmol 2013; 156: 5-14
• 20 Wostyn P, De Groot V, Van Dam D. et al. Glaucoma considered as an imbalance between production and clearance of neurotoxins. Invest Ophthalmol Vis Sci 2014; 55: 5351-5352
• 21 Killer HE, Jaggi GP, Flammer J. et al. The optic nerve: a new window into cerebrospinal fluid composition?. Brain 2006; 129: 1027-1030
• 22 Berdahl JP, Fautsch MP, Stinnett SS. et al. Intracranial pressure in primary open angle glaucoma, normal tension glaucoma, and ocular hypertension: a case-control study. Invest Ophthalmol Vis Sci 2008; 49: 5412-5418
• 23 Berdahl JP, Allingham RR, Johnson DH. Cerebrospinal fluid pressure is decreased in primary open-angle glaucoma. Ophthalmology 2008; 115: 763-768
• 24 Jonas JB, Wang N, Yang D. Translamina cribrosa pressure difference as potential element in the pathogenesis of glaucomatous optic neuropathy. Asia Pac J Ophthalmol (Phila) 2016; 5: 5-10
• 25 Liu KC, Fleischman D, Lee AG. et al. Current concepts of cerebrospinal fluid dynamics and the translaminar cribrosa pressure gradient: a paradigm of optic disk disease. Surv Ophthalmol 2020; 65: 48-66
• 26 Lenfeldt N, Koskinen LO, Bergenheim AT. et al. CSF pressure assessed by lumbar puncture agrees with intracranial pressure. Neurology 2007; 68: 155-158
• 27 Ren R, Jonas JB, Tian G. et al. Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology 2010; 117: 259-266
• 28 Fleischman D, Berdahl JP, Zaydlarova J. et al. Cerebrospinal fluid pressure decreases with older age. PLoS One 2012; 7: e52664
• 29 Linden C, Qvarlander S, Johannesson G. et al. Normal-tension glaucoma has normal intracranial pressure: a prospective study of intracranial pressure and intraocular pressure in different body positions. Ophthalmology 2018; 125: 361-368
• 30 Pircher A, Remonda L, Weinreb RN. et al. Translaminar pressure in Caucasian normal tension glaucoma patients. Acta Ophthalmol (Copenh) 2017; 95: e524-e531
• 31 Pircher A, Killer HE. TLP: a premature concept. Eye (Lond) 2016; 30: 166-167
• 32 Davson H. Physiology of the cerebrospinal Fluid. London: J & A Churchill Ltd.; 1967
• 33 Davson H, Welch K, Segal MB. et al. Physiology and Pathophysiology of the cerebrospinal Fluid. Edinburgh, UK: Churchill Livingstone; 1987
• 34 Dichiro G. Movement of the cerebrospinal fluid in human beings. Nature 1964; 204: 290-291
• 35 Guldbrandsen A, Vethe H, Fara Y. et al. In-depth characterization of the cerebrospinal fluid (CSF) proteome displayed through the CSF proteome resource (CSF-PR) Mol Cell. Proteomics 2014; 13: 3152-3163
• 36 Kant S, Stopa EG, Johanson CE. et al. Choroid plexus genes for CSF production and brain homeostasis are altered in Alzheimerʼs disease. Fluids Barriers CNS 2018; 15: 34 (2018)
• 37 Giorgio A, Zhang J, Costantino F. et al. Diffuse brain damage in normal tension glaucoma. Hum Brain Mapp 2017; 39: 532-541
• 38 Lai SW, Lin CL, Liao KF. Glaucoma may be a non-memory manifestation of Alzheimerʼs disease in older people. Int Psychogeriatr 2017; 29: 1-7
• 39 Kessing LV, Lopez AG, Andersen PK. et al. No increased risk of developing Alzheimer disease in patients with glaucoma. J Glaucoma 2007; 16: 47-51
• 40 Bayer AU, Ferrari F, Erb C. High occurrence rate of glaucoma among patients with Alzheimerʼs disease. Eur Neurol 2002; 47: 165-168
• 41 Tamura H, Kawakami H, Kanamoto T. et al. High frequency of open-angle glaucoma in Japanese patients with Alzheimerʼs disease. J Neurol Sci 2006; 246: 79-83
• 42 Bach-Holm D, Kessing SV, Mogensen U. et al. Normal tension glaucoma and Alzheimer disease: comorbidity?. Acta Ophthalmol 2012; 90: 683-685
• 43 Silverberg GD, Heit G, Huhn S. et al. The cerebrospinal fluid production rate is reduced in dementia of the Alzheimerʼs type. Neurology 2001; 57: 1763-1766
• 44 Attier-Zmudka J, Sérot JM, Balédent O. et al. Decreased Cerebrospinal Fluid Flow Is Associated with Cognitive Deficit in Elderly Patients. Front Aging Neurosci 2019; 11: 87
• 45 Boye D, Montali M, Miller NR. et al. Flow dynamics of cerebrospinal fluid between the intracranial cavity and the subarachnoid space of the optic nerve measured with a diffusion magnetic resonance imaging sequence in patients with normal tension glaucoma. Clin Exp Ophthalmol 2018; 46: 511-518
• 46 Nakada T, Kwee IL. Fluid Dynamics Inside the Brain Barrier: Current Concept of Interstitial Flow, Glymphatic Flow, and Cerebrospinal Fluid Circulation in the Brain. Neuroscientist 2019; 25: 155-166
• 47 Killer HE, Laeng HR, Groscurth P. Lymphatic capillaries in the meninges of the human optic nerve. J Neuroophthalmol 1999; 19: 222-228
• 48 Killer HE, Jaggi GP, Miller NR. et al. Does immunohistochemistry allow easy detection of lymphatics in the optic nerve sheath?. J Histochem Cytochem 2008; 56: 1087-1092
• 49 Killer HE, Jaggi GP, Flammer J. et al. Cerebrospinal fluid dynamics between the intracranial and the subarachnoid space of the optic nerve. Is it always bidirectional?. Brain 2007; 130: 514-520
• 50 Killer HE, Miller NR, Flammer J. et al. Cerebrospinal fluid exchange in the optic nerve in normal-tension glaucoma. Br J Ophthalmol 2012; 96: 544-548
• 51 Pircher A, Neutzner A, Montali M. et al. Lipocalin-type Prostaglandin D Synthase Concentration Gradients in the Cerebrospinal Fluid in Normal-tension Glaucoma Patients with Optic Nerve Sheath Compartmentation. Eye Brain 2021; 13: 89-97
• 52 Reiber H. Dynamics of brain-derived proteins in cerebrospinal fluid. Clin Chim Acta 2001; 310: 173-186
• 53 Tumani H, Nau R, Felgenhauer K. Beta-trace protein in cerebrospinal fluid: a blood-CSF barrier-related evaluation in neurological diseases. Ann Neurol 1998; 44: 882-889
• 54 Maesaka JK, Sodam B, Palaia T. et al. Prostaglandin D2 synthase: apoptotic factor in alzheimer plasma, inducer of reactive oxygen species, inflammatory cytokines and dialysis dementia. J Nephropathol 2013; 2: 166-180
• 55 Ragolia L, Palaia T, Frese L. et al. Prostaglandin D2 synthase induces apoptosis in PC12 neuronal cells. Neuroreport 2001; 12: 2623-2628
• 56 Link H, Olsson JE. Beta-trace protein concentration in CSF in neurological disorders. Acta Neurol Scand 1972; 48: 57-68
• 57 Jaggi GP, Harlev M, Ziegler U. et al. Cerebrospinal fluid segregation optic neuropathy: an experimental model and a hypothesis. Br J Ophthalmol 2010; 94: 1088-1109
• 58 Andrews RM, Griffiths PG, Johnson M. et al. Histochemical localisation of mitochondrial enzyme activity in human optic nerve and retina. Br J Ophthalmol 1999; 83: 231-235
• 59 Pircher A, Montali M, Berberat J. et al. The optic canal: a bottleneck for cerebrospinal fluid dynamics in normal-tension glaucoma?. Front Neurol 2017; 8: 47
• 60 Mathieu E, Gupta N, Ahari A. et al. Evidence for Cerebrospinal Fluid Entry Into the Optic Nerve via a Glymphatic Pathway. Invest Ophthalmol Vis Sci 2017; 58: 4784-4791
• 61 Wostyn P, De Groot V, Van Dam D. et al. The First Histologic Evidence of a Paravascular Pathway Within the Optic Nerve. Invest Ophthalmol Vis Sci 2018; 59: 1717
• 62 Mader TH, Gibson CR, Pass AF. et al. Optic disc edema, globe flattening, choroidal folds, and hyperopic shifts observed in astronauts after long-duration space flight. Ophthalmology 2011; 118: 2058-2069
• 63 Mader TH, Gibson CR, Pass AF. et al. Optic disc edema in an astronaut after repeat long-duration space flight. J Neuroophthalmol 2013; 33: 249-255
• 64 Lee AG, Mader TH, Gibson CR. et al. Space flight-associated neuro-ocular syndrome (SANS). Eye (Lond) 2018; 32: 1164-1167