Letter to the Editor. Low ICP and normal tension glaucoma: optic nerve damage due to barotraumatic factors, failure of CSF dynamics, or both?

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  • 1 PC Sint-Amandus, Beernem, Belgium;
  • 2 Antwerp University Hospital, Antwerp, Belgium;
  • 3 Laboratory of Neurochemistry and Behavior, Institute Born-Bunge, University of Antwerp, Antwerp, Belgium;
  • 4 University of Groningen and University Medical Center Groningen, Groningen, The Netherlands;
  • 5 Ghent University Hospital, Ghent, Belgium;
  • 6 Middelheim General Hospital (ZNA), Antwerp, Belgium; and
  • 7 Kantonsspital Aarau, Aarau, Switzerland
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TO THE EDITOR: We read with great interest the article by Gallina et al.2 (Gallina P, Savastano A, Becattini E, et al: Glaucoma in patients with shunt-treated normal pressure hydrocephalus. J Neurosurg [epub ahead of print November 17, 2017. DOI: 10.3171/2017.5.JNS163062]). We appreciate the authors’ study and their efforts to explore the role of low intracranial pressure (ICP) in the pathogenesis of normal tension glaucoma (NTG). However, we feel that an issue described in their paper deserves further discussion.

As discussed by the authors, several studies have provided clinical evidence in support of the theory that reduced ICP may play a role in the pathogenesis of NTG.1 In line with this theory, they demonstrate that patients whose ICP has been lowered following ventriculoperitoneal shunt placement, as treatment for normal pressure hydrocephalus, are almost 40 times more likely to suffer from NTG than elderly Italian patients without hydrocephalus.2 The mechanisms most commonly proposed to explain the contribution of low ICP and thus a high trans–lamina cribrosa pressure difference (intraocular pressure − ICP) to glaucoma are direct strain on the lamina cribrosa, impairment of axonal transport, and altered blood flow.1 The authors cite one of our papers,10 which focused on the possible role of cerebrospinal fluid (CSF) circulatory dysfunction in NTG, and argue against our hypothesis stating that “the finding that NTG occurs in patients whose CSF clearance was forced more strongly by the sink action of the diversion does not support, as already noted, a pressure-independent pathogenetic hypothesis, which focuses on the accumulation of toxins at the level of the optic nerve due to failure of CSF dynamics.”2 For the reasons set forth below, we respectfully disagree with this statement.

Evidence in support of our viewpoint comes from a recent dog study by Hou et al.3 During CSF shunting from the brain ventricle, the intraventricular ICP gradually decreased in a linear fashion together with the optic nerve subarachnoid space (SAS) pressure.3 But when the ICP fell below a critical breakpoint, optic nerve SAS pressure remained constant despite further ICP decline.3 These authors interpreted this as a sign of CSF communication arrest between the intracranial and optic nerve SAS.3 Indeed, when ICP drops too low, the breakpoint is reached and CSF flow stops.3 This means that the ICP is too low for CSF to freely flow through the optic canal.3

Intriguingly, the findings by Hou et al.3 may bring together two seemingly very different theories of glaucoma pathogenesis. Berdahl and Allingham,1 as well as others,9 have suggested that the lower ICP reported in glaucoma patients could play a role in the pathogenesis of the disease through a higher pressure difference across the lamina cribrosa, influencing the physiology and pathophysiology of the optic nerve head. However, it should be noted that the clinical retrospective and prospective studies of CSF pressure in patients with glaucoma have taken the lumbar CSF pressure measurement as a surrogate for the retrolaminar CSF pressure1 and that the true CSF pressure behind the lamina cribrosa is not known.7 Furthermore, two recent studies did not confirm lower ICP in NTG patients.5,8 Killer et al.4 suggested that open-angle glaucoma may be due to the sequestration of CSF within the terminus of the optic nerve SAS, creating a stagnant region accumulating substances toxic to the adjacent optic nerve head. Wostyn et al.10 proposed that decreased ICP and an optic nerve sheath compartment syndrome could be seen as sequential steps in the disease process of NTG. The dog study by Hou et al.3 indeed suggests that if the ICP is too low, CSF flow from the intracranial SAS into the optic nerve SAS stops and CSF drainage from the optic nerve SAS is interrupted as well, creating a CSF compartment syndrome. Compartmentation of the optic nerve SAS seems to be associated with a narrower optic canal cross-sectional area in NTG patients.6

Given the above considerations and given that both the hydrostatic pressure and the dynamics of CSF may be of great importance for the physiological stability of the optic nerve,11 we believe that the pressure gradient with shear stress at the site of the lamina cribrosa may be accompanied by another mechanism, namely toxicity of non-recycled CSF around the optic nerve.

Disclosures

The authors report no conflict of interest.

References

  • 1

    Berdahl JP, Allingham RR: Intracranial pressure and glaucoma. Curr Opin Ophthalmol 21:106111, 2010

  • 2

    Gallina P, Savastano A, Becattini E, Orlandini S, Scollato A, Rizzo S, : Glaucoma in patients with shunt-treated normal pressure hydrocephalus. J Neurosurg [epub ahead of print November 17, 2017. DOI: 10.3171/2017.5.JNS163062]

    • Search Google Scholar
    • Export Citation
  • 3

    Hou R, Zhang Z, Yang D, Wang H, Chen W, Li Z, : Intracranial pressure (ICP) and optic nerve subarachnoid space pressure (ONSP) correlation in the optic nerve chamber: the Beijing Intracranial and Intraocular Pressure (iCOP) study. Brain Res 1635:201208, 2016

    • Search Google Scholar
    • Export Citation
  • 4

    Killer HE, Jaggi GP, Flammer J, Miller NR: Is open-angle glaucoma caused by impaired cerebrospinal fluid circulation: around the optic nerve? Clin Exp Ophthalmol 36:308311, 2008

    • Search Google Scholar
    • Export Citation
  • 5

    Lindén C, Qvarlander S, Jóhannesson G, Johansson E, Östlund F, Malm J, : Normal-tension glaucoma has normal intracranial pressure: a prospective study of intracranial pressure and intraocular pressure in different body positions. Ophthalmology 125:361368, 2018

    • Search Google Scholar
    • Export Citation
  • 6

    Pircher A, Montali M, Berberat J, Remonda L, Killer HE: The optic canal: a bottleneck for cerebrospinal fluid dynamics in normal-tension glaucoma? Front Neurol 8:47, 2017

    • Search Google Scholar
    • Export Citation
  • 7

    Pircher A, Montali M, Berberat J, Remonda L, Killer HE: Relationship between the optic nerve sheath diameter and lumbar cerebrospinal fluid pressure in patients with normal tension glaucoma. Eye (Lond) 31:13651372, 2017

    • Search Google Scholar
    • Export Citation
  • 8

    Pircher A, Remonda L, Weinreb RN, Killer HE: Translaminar pressure in Caucasian normal tension glaucoma patients. Acta Ophthalmol 95:e524e531, 2017

    • Search Google Scholar
    • Export Citation
  • 9

    Ren R, Jonas JB, Tian G, Zhen Y, Ma K, Li S, : Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology 117:259266, 2010

    • Search Google Scholar
    • Export Citation
  • 10

    Wostyn P, De Groot V, Van Dam D, Audenaert K, De Deyn PP: Senescent changes in cerebrospinal fluid circulatory physiology and their role in the pathogenesis of normal-tension glaucoma. Am J Ophthalmol 156:514, 14.e1–14.e2, 2013

    • Search Google Scholar
    • Export Citation
  • 11

    Zhang Z, Liu D, Jonas JB, Wu S, Kwong JM, Zhang J, : Glaucoma and the role of cerebrospinal fluid dynamics. Invest Ophthalmol Vis Sci 56:6632, 2015 (Letter)

    • Search Google Scholar
    • Export Citation
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  • 1 University of Florence, Italy; and
  • 2 University Hospital “Ospedali Riuniti” of Trieste, Italy

Response

We are pleased regarding the letter by Wostyn et al. because it gives us the possibility of critically checking our contention that a lowering of ICP underlies optic nerve damage in shunted normal pressure hydrocephalus. Those results support the role of changes in intraocular pressure and ICP gradient across the lamina cribrosa in the pathophysiology of NTG.20

The arguments by Wostyn et al. descend from experimental findings in dogs,7 in which CSF circulation at the level of the optic nerve SAS is halted when ICP falls below a critical breakpoint value. According to Hou et al.,7 this would involve CSF segregation, thus preventing the supply of nutrients to, and the disposal of waste molecules from, the so-called optic nerve chamber.10,11 Wostyn et al. disputed that these findings would put into question our inference that the failure of CSF dynamics cannot explain the occurrence of NTG in precisely those patients with lower opening pressure valve values, where CSF clearance was forced by the stronger sink action of the diversion. Consequently, we argued that a pressure-independent pathogenetic hypothesis based on the accumulation of toxins at the level of the optic nerve due to CSF circulation failure21 cannot apply to our data because a higher CSF clearance would prevent stagnation of CSF.

Admittedly, because of the obvious anatomical-physiological differences, it is difficult to straightforwardly translate the results obtained in dogs into human beings. However, dogs have been widely used to study CSF hydrodynamics since the classic work of Dandy and Blackfan.4 Therefore, it was tempting to play along, and we noted that our NTG patients underwent a lowering of ICP within the ICP-dependent zone identified by Hou et al.,7 where the intraventricular values decreased linearly with optic nerve SAS pressure. As a consequence, our patients experienced optic nerve damage even though the hypothetical arrest of communication between the intracranial and optic nerve SAS would not have occurred yet.

Recent anatomical evidence supports the notion that free circulation of CSF within the optic canal in humans may be hampered,16,17 leading to compartmentalization of the SAS within the canalicular portion and the accumulation of toxins, possibly causing NTG.11 Liugan et al.16 revealed the fibrous components within the optic canal and their relationship with the optic nerve SAS, which are suggestive of a valve mechanism at work in CSF sequestration.12 A bony bottleneck responsible for CSF circulatory dysfunction was advocated by Pircher et al.,17 who showed that the optic canal, as measured in the coronal plane at the orbital opening, is smaller in NTG patients than in controls. These results were paralleled by MRI data showing lower CSF flow between the intracranial cavity and optic nerve SAS in NTG patients compared to that in healthy controls.3 Overall, these findings shift the anatomical-physiological site of NTG pathogenesis far from the lamina cribrosa, the structure where an increased pressure gradient between the intraocular and intracranial compartments would act and damage the optic nerve.20 Moreover, Wostyn et al. put forward two recent studies14,18 that reported no ICP decrease, as measured by lumbar puncture, in white NTG patients, suggesting that the current view20 of the trans–lamina cribrosa gradient hypothesis should at least be reconsidered. However, Pircher et al.18 performed a retrospective study without a control group, which limits the generalizability of their results. Moreover, these studies14,18 share two more weaknesses: 1) lumbar CSF pressure is not accurate enough to extrapolate ICP around the optic nerve,9 and 2) both involved white patients—which could explain the discrepancy between their results and those of Ren et al.,19 who studied an Asian population. Nonetheless, recent advances in ultrasound technology have allowed higher-resolution images of the optic nerve SAS to be generated, enabling more detailed measurements and increased power to predict CSF pressure at that level.15 Liu et al. demonstrated that NTG patients had a significant smaller optic nerve SAS than healthy controls, a finding that was indicative of lower CSF pressure and suggestive of an abnormally high trans–lamina cribrosa pressure difference in the NTG group.15

In fact, the pathophysiology of NTG remains incompletely understood. Both the barometric and the CSF dynamics failure hypotheses are supported by bodies of evidence. Intriguingly, Wostyn et al. propose a reconciliation between the two theories and advance a stepwise nature for the disease. Wishing to follow the advice from Wostyn et al., we plan to check the possible concomitance of some features supporting the CSF compartment syndrome at the optic nerve SAS in our normal pressure hydrocephalus patients whose ICP was lowered by a CSF shunt. We will simply look at possible differences in the size of the optic canal17 between NTG and no-NTG groups. If the mechanism involved in NTG occurrence in these patients is related to the lowering of ICP, as we have argued, a narrowing of the optic canal should not be expected. Indeed, the trans–lamina cribrosa pressure difference hypothesis assumes free communication between the intracranial CSF spaces and the lamina cribrosa, which is, in fact, posteriorly displaced in NTG,13 while a canalicular bottleneck would limit the transmission of ICP through the SAS. It is worth noting that severe papilledema and poor visual function were associated with a larger optic canal in 69 patients with idiopathic intracranial hypertension,2 while a smaller size was associated with the less affected side in 8 patients with asymmetrical papilledema.1 Further clinical studies may also assess possible age differences among NTG patients in relation to optic canal size. In this regard, it has been shown that optic canal volume decreases with aging.6 Pircher et al.17 could not detect a significant correlation between optic canal size and age in either the NTG group or the control group. However, it should be noted that their samples were dimensionally inadequate to appreciate small effect sizes. For the sake of speculation, we considered the data of Pircher et al.17 and found that their youngest (age < 60 years) NTG patients had a smaller optic canal size than those measured in their oldest (age > 80 years) NTG patients. The opposite was true for their controls, in whom the size of the optic canal of the oldest subjects was narrower than that measured in the youngest group. These inverse correlations between NTG and controls were especially valid for males. Therefore, the question is far from being settled, especially if ethnic differences come into play. Notably, optic canal measurements in Chinese patients showed larger cross-sectional areas compared to those in whites.8,17 Nevertheless, if an anatomical narrowing of the optic canal predisposes to an impairment of CSF flow in the optic nerve SAS, which can now be assessed in a noninvasive manner,3 CSF compartmentalization would occur early. As a consequence, the damage to the optic nerve would appear in the absence of intracranial hypotension, which is an age-related process.5 On the other hand, in the presence of a relatively large optic canal, NTG occurrence might be expected to be a process related to aging. In this light, the temporal dimension and anatomical interindividual variation at the level of the optic canal may ultimately make someone more liable to either barometric damage at the lamina cribrosa or to stagnation of toxic substances within the compartmentalized optic canal SAS. Undoubtedly, much experimental and clinical knowledge is still needed to understand which one of these mechanisms underlies NTG and if they operate together or alternatively.

References

  • 1

    Bidot S, Bruce BB, Saindane AM, Newman NJ, Biousse V: Asymmetric papilledema in idiopathic intracranial hypertension. J Neuroophthalmol 35:3136, 2015

    • Search Google Scholar
    • Export Citation
  • 2

    Bidot S, Clough L, Saindane AM, Newman NJ, Biousse V, Bruce BB: The optic canal size is associated with the severity of papilledema and poor visual function in idiopathic intracranial hypertension. J Neuroophthalmol 36:120125, 2016

    • Search Google Scholar
    • Export Citation
  • 3

    Boye D, Montali M, Miller NR, Pircher A, Gruber P, Killer HE, : 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 [epub ahead of print], 2017

    • Search Google Scholar
    • Export Citation
  • 4

    Dandy WE, Blackfan KD: An experimental and clinical study of internal hydrocephalus. JAMA 61:22162217, 1913

  • 5

    Fleischman D, Berdahl JP, Zaydlarova J, Stinnett S, Fautsch MP, Allingham RR: Cerebrospinal fluid pressure decreases with older age. PLoS One 7:e52664, 2012

    • Search Google Scholar
    • Export Citation
  • 6

    Friedrich RE, Bruhn M, Lohse C: Cone-beam computed tomography of the orbit and optic canal volumes. J Craniomaxillofac Surg 44:13421349, 2016

    • Search Google Scholar
    • Export Citation
  • 7

    Hou R, Zhang Z, Yang D, Wang H, Chen W, Li Z, : Intracranial pressure (ICP) and optic nerve subarachnoid space pressure (ONSP) correlation in the optic nerve chamber: the Beijing Intracranial and Intraocular Pressure (iCOP) study. Brain Res 1635:201208, 2016

    • Search Google Scholar
    • Export Citation
  • 8

    Jiang PF, Dai XY, Lv Y, Liu S, Mu XY: Imaging study on the optic canal using sixty four-slice spiral computed tomography. Int J Clin Exp Med 8:2124721251, 2015

    • Search Google Scholar
    • Export Citation
  • 9

    Killer HE: Compartment syndromes of the optic nerve and open-angle glaucoma. J Glaucoma 22 (5 Suppl 5):S19S20, 2013

  • 10

    Killer HE, Jaggi GP, Flammer J, Miller NR: Is open-angle glaucoma caused by impaired cerebrospinal fluid circulation: around the optic nerve? Clin Experiment Ophthalmol 36:308311, 2008

    • Search Google Scholar
    • Export Citation
  • 11

    Killer HE, Laeng HR, Flammer J, Groscurth P: Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations. Br J Ophthalmol 87:777781, 2003

    • Search Google Scholar
    • Export Citation
  • 12

    Killer HE, Pircher A: Reduced free communication of the subarachnoid space within the optic canal in the human. Am J Ophthalmol 183:164165, 2017

    • Search Google Scholar
    • Export Citation
  • 13

    Li L, Bian A, Cheng G, Zhou Q: Posterior displacement of the lamina cribrosa in normal-tension and high-tension glaucoma. Acta Ophthalmol 94:e492e500, 2016

    • Search Google Scholar
    • Export Citation
  • 14

    Lindén C, Qvarlander S, Jóhannesson G, Johansson E, Östlund F, Malm J, : Normal-tension glaucoma has normal intracranial pressure: a prospective study of intracranial pressure and intraocular pressure in different body positions. Ophthalmology 125:361368, 2018

    • Search Google Scholar
    • Export Citation
  • 15

    Liu H, Yang D, Ma T, Shi W, Zhu Q, Kang J, : Measurement and associations of the optic nerve subarachnoid space in normal tension and primary open-angle glaucoma. Am J Ophthalmol 186:128137, 2018

    • Search Google Scholar
    • Export Citation
  • 16

    Liugan M, Xu Z, Zhang M: Reduced free communication of the subarachnoid space within the optic canal in the human. Am J Ophthalmol 179:2531, 2017

    • Search Google Scholar
    • Export Citation
  • 17

    Pircher A, Montali M, Berberat J, Remonda L, Killer HE: The optic canal: a bottleneck for cerebrospinal fluid dynamics in normal-tension glaucoma? Front Neurol 8:47, 2017

    • Search Google Scholar
    • Export Citation
  • 18

    Pircher A, Remonda L, Weinreb RN, Killer HE: Translaminar pressure in Caucasian normal tension glaucoma patients. Acta Ophthalmol 95:e524e531, 2017

    • Search Google Scholar
    • Export Citation
  • 19

    Ren R, Jonas JB, Tian G, Zhen Y, Ma K, Li S, : Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology 117:259266, 2010

    • Search Google Scholar
    • Export Citation
  • 20

    Siaudvytyte L, Januleviciene I, Daveckaite A, Ragauskas A, Bartusis L, Kucinoviene J, : Literature review and meta-analysis of translaminar pressure difference in open-angle glaucoma. Eye (Lond) 29:12421250, 2015

    • Search Google Scholar
    • Export Citation
  • 21

    Wostyn P, De Groot V, Van Dam D, Audenaert K, De Deyn PP: Senescent changes in cerebrospinal fluid circulatory physiology and their role in the pathogenesis of normal-tension glaucoma. Am J Ophthalmol 156:514, 14.e1–14.e2, 2013

    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Contributor Notes

Correspondence Peter Wostyn: wostyn.peter@skynet.be.

INCLUDE WHEN CITING Published online May 4, 2018; DOI: 10.3171/2017.11.JNS172939.

Disclosures The authors report no conflict of interest.

  • 1

    Berdahl JP, Allingham RR: Intracranial pressure and glaucoma. Curr Opin Ophthalmol 21:106111, 2010

  • 2

    Gallina P, Savastano A, Becattini E, Orlandini S, Scollato A, Rizzo S, : Glaucoma in patients with shunt-treated normal pressure hydrocephalus. J Neurosurg [epub ahead of print November 17, 2017. DOI: 10.3171/2017.5.JNS163062]

    • Search Google Scholar
    • Export Citation
  • 3

    Hou R, Zhang Z, Yang D, Wang H, Chen W, Li Z, : Intracranial pressure (ICP) and optic nerve subarachnoid space pressure (ONSP) correlation in the optic nerve chamber: the Beijing Intracranial and Intraocular Pressure (iCOP) study. Brain Res 1635:201208, 2016

    • Search Google Scholar
    • Export Citation
  • 4

    Killer HE, Jaggi GP, Flammer J, Miller NR: Is open-angle glaucoma caused by impaired cerebrospinal fluid circulation: around the optic nerve? Clin Exp Ophthalmol 36:308311, 2008

    • Search Google Scholar
    • Export Citation
  • 5

    Lindén C, Qvarlander S, Jóhannesson G, Johansson E, Östlund F, Malm J, : Normal-tension glaucoma has normal intracranial pressure: a prospective study of intracranial pressure and intraocular pressure in different body positions. Ophthalmology 125:361368, 2018

    • Search Google Scholar
    • Export Citation
  • 6

    Pircher A, Montali M, Berberat J, Remonda L, Killer HE: The optic canal: a bottleneck for cerebrospinal fluid dynamics in normal-tension glaucoma? Front Neurol 8:47, 2017

    • Search Google Scholar
    • Export Citation
  • 7

    Pircher A, Montali M, Berberat J, Remonda L, Killer HE: Relationship between the optic nerve sheath diameter and lumbar cerebrospinal fluid pressure in patients with normal tension glaucoma. Eye (Lond) 31:13651372, 2017

    • Search Google Scholar
    • Export Citation
  • 8

    Pircher A, Remonda L, Weinreb RN, Killer HE: Translaminar pressure in Caucasian normal tension glaucoma patients. Acta Ophthalmol 95:e524e531, 2017

    • Search Google Scholar
    • Export Citation
  • 9

    Ren R, Jonas JB, Tian G, Zhen Y, Ma K, Li S, : Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology 117:259266, 2010

    • Search Google Scholar
    • Export Citation
  • 10

    Wostyn P, De Groot V, Van Dam D, Audenaert K, De Deyn PP: Senescent changes in cerebrospinal fluid circulatory physiology and their role in the pathogenesis of normal-tension glaucoma. Am J Ophthalmol 156:514, 14.e1–14.e2, 2013

    • Search Google Scholar
    • Export Citation
  • 11

    Zhang Z, Liu D, Jonas JB, Wu S, Kwong JM, Zhang J, : Glaucoma and the role of cerebrospinal fluid dynamics. Invest Ophthalmol Vis Sci 56:6632, 2015 (Letter)

    • Search Google Scholar
    • Export Citation
  • 1

    Bidot S, Bruce BB, Saindane AM, Newman NJ, Biousse V: Asymmetric papilledema in idiopathic intracranial hypertension. J Neuroophthalmol 35:3136, 2015

    • Search Google Scholar
    • Export Citation
  • 2

    Bidot S, Clough L, Saindane AM, Newman NJ, Biousse V, Bruce BB: The optic canal size is associated with the severity of papilledema and poor visual function in idiopathic intracranial hypertension. J Neuroophthalmol 36:120125, 2016

    • Search Google Scholar
    • Export Citation
  • 3

    Boye D, Montali M, Miller NR, Pircher A, Gruber P, Killer HE, : 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 [epub ahead of print], 2017

    • Search Google Scholar
    • Export Citation
  • 4

    Dandy WE, Blackfan KD: An experimental and clinical study of internal hydrocephalus. JAMA 61:22162217, 1913

  • 5

    Fleischman D, Berdahl JP, Zaydlarova J, Stinnett S, Fautsch MP, Allingham RR: Cerebrospinal fluid pressure decreases with older age. PLoS One 7:e52664, 2012

    • Search Google Scholar
    • Export Citation
  • 6

    Friedrich RE, Bruhn M, Lohse C: Cone-beam computed tomography of the orbit and optic canal volumes. J Craniomaxillofac Surg 44:13421349, 2016

    • Search Google Scholar
    • Export Citation
  • 7

    Hou R, Zhang Z, Yang D, Wang H, Chen W, Li Z, : Intracranial pressure (ICP) and optic nerve subarachnoid space pressure (ONSP) correlation in the optic nerve chamber: the Beijing Intracranial and Intraocular Pressure (iCOP) study. Brain Res 1635:201208, 2016

    • Search Google Scholar
    • Export Citation
  • 8

    Jiang PF, Dai XY, Lv Y, Liu S, Mu XY: Imaging study on the optic canal using sixty four-slice spiral computed tomography. Int J Clin Exp Med 8:2124721251, 2015

    • Search Google Scholar
    • Export Citation
  • 9

    Killer HE: Compartment syndromes of the optic nerve and open-angle glaucoma. J Glaucoma 22 (5 Suppl 5):S19S20, 2013

  • 10

    Killer HE, Jaggi GP, Flammer J, Miller NR: Is open-angle glaucoma caused by impaired cerebrospinal fluid circulation: around the optic nerve? Clin Experiment Ophthalmol 36:308311, 2008

    • Search Google Scholar
    • Export Citation
  • 11

    Killer HE, Laeng HR, Flammer J, Groscurth P: Architecture of arachnoid trabeculae, pillars, and septa in the subarachnoid space of the human optic nerve: anatomy and clinical considerations. Br J Ophthalmol 87:777781, 2003

    • Search Google Scholar
    • Export Citation
  • 12

    Killer HE, Pircher A: Reduced free communication of the subarachnoid space within the optic canal in the human. Am J Ophthalmol 183:164165, 2017

    • Search Google Scholar
    • Export Citation
  • 13

    Li L, Bian A, Cheng G, Zhou Q: Posterior displacement of the lamina cribrosa in normal-tension and high-tension glaucoma. Acta Ophthalmol 94:e492e500, 2016

    • Search Google Scholar
    • Export Citation
  • 14

    Lindén C, Qvarlander S, Jóhannesson G, Johansson E, Östlund F, Malm J, : Normal-tension glaucoma has normal intracranial pressure: a prospective study of intracranial pressure and intraocular pressure in different body positions. Ophthalmology 125:361368, 2018

    • Search Google Scholar
    • Export Citation
  • 15

    Liu H, Yang D, Ma T, Shi W, Zhu Q, Kang J, : Measurement and associations of the optic nerve subarachnoid space in normal tension and primary open-angle glaucoma. Am J Ophthalmol 186:128137, 2018

    • Search Google Scholar
    • Export Citation
  • 16

    Liugan M, Xu Z, Zhang M: Reduced free communication of the subarachnoid space within the optic canal in the human. Am J Ophthalmol 179:2531, 2017

    • Search Google Scholar
    • Export Citation
  • 17

    Pircher A, Montali M, Berberat J, Remonda L, Killer HE: The optic canal: a bottleneck for cerebrospinal fluid dynamics in normal-tension glaucoma? Front Neurol 8:47, 2017

    • Search Google Scholar
    • Export Citation
  • 18

    Pircher A, Remonda L, Weinreb RN, Killer HE: Translaminar pressure in Caucasian normal tension glaucoma patients. Acta Ophthalmol 95:e524e531, 2017

    • Search Google Scholar
    • Export Citation
  • 19

    Ren R, Jonas JB, Tian G, Zhen Y, Ma K, Li S, : Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology 117:259266, 2010

    • Search Google Scholar
    • Export Citation
  • 20

    Siaudvytyte L, Januleviciene I, Daveckaite A, Ragauskas A, Bartusis L, Kucinoviene J, : Literature review and meta-analysis of translaminar pressure difference in open-angle glaucoma. Eye (Lond) 29:12421250, 2015

    • Search Google Scholar
    • Export Citation
  • 21

    Wostyn P, De Groot V, Van Dam D, Audenaert K, De Deyn PP: Senescent changes in cerebrospinal fluid circulatory physiology and their role in the pathogenesis of normal-tension glaucoma. Am J Ophthalmol 156:514, 14.e1–14.e2, 2013

    • Search Google Scholar
    • Export Citation

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