“Dual-pressure theory” in pathogenesis of glaucomatous optic neuropathy from the Beijing intracranial and intraocular pressure study

Ying Cheng , Mayinuer Yusufu , Robert N. Weinreb , Ningli Wang

Eye & ENT Research ›› 2024, Vol. 1 ›› Issue (1) : 11 -19.

PDF (431KB)
Eye & ENT Research ›› 2024, Vol. 1 ›› Issue (1) : 11 -19. DOI: 10.1002/eer3.3
REVIEW ARTICLE

“Dual-pressure theory” in pathogenesis of glaucomatous optic neuropathy from the Beijing intracranial and intraocular pressure study

Author information +
History +
PDF (431KB)

Abstract

The mechanical theory of glaucoma indicates that high intraocular pressure (IOP) leads to glaucomatous optic nerve damage. However, nearly half of primary openangle glaucoma patients with normal intraocular pressure also exhibit progression of what appears to be glaucomatous optic nerve damage. Our earlier prospective study identified for the first time that the relatively low intracranial pressure (ICP) is also an important risk factor for progressive glaucomatous injury of normal-tension glaucoma. When considering the results of studies in nonhuman primates, clinical research, large-scale natural-population studies, and basic laboratory investigations, a new understanding of the pathophysiology of glaucoma, the “Dual-Pressure Theory”, has been proposed. This theory states that “either high IOP or low ICP contributes to increasing the translaminar cribrosa pressure difference; it is the pressure difference rather than the IOP alone that results in the glaucomatous optic neuropathy”. Here, we provide a systematic introduction to Dual-Pressure Theory relating to glaucoma, the form of a research map, an outline of basic laboratory investigations, the main methodology, and research updates.

Keywords

dual-pressure theory / intracranial pressure / intraocular pressure / primary open-angle glaucoma / translaminar cribrosa pressure difference

Cite this article

Download citation ▾
Ying Cheng, Mayinuer Yusufu, Robert N. Weinreb, Ningli Wang. “Dual-pressure theory” in pathogenesis of glaucomatous optic neuropathy from the Beijing intracranial and intraocular pressure study. Eye & ENT Research, 2024, 1(1): 11-19 DOI:10.1002/eer3.3

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Chen H, Cho KS, Vu THK, et al. Commensal microflora-induced T cell responses mediate progressive neurodegeneration in glaucoma. Nat Commun. 2018;9(1):3209.

[2]

Leung DYL, Tham CC. Normal-tension glaucoma: current concepts and approaches-a review. Clin Exp Ophthalmol. 2022;50(2):247-259.

[3]

Fan X, Ying Y, Zhai R, et al. The characteristics of fundus micro-vascular alterations in the course of glaucoma: a narrative review. Ann Transl Med. 2022;10(9):527.

[4]

Miao Y, Zhao GL, Cheng S, Wang Z, Yang XL. Activation of retinal glial cells contributes to the degeneration of ganglion cells in experimental glaucoma. Prog Retin Eye Res. 2023;93:101169.

[5]

Yang H, Reynaud J, Lockwood H, et al. The connective tissue phenotype of glaucomatous cupping in the monkey eye -clinical and research implications. Prog Retin Eye Res. 2017;59:1-52.

[6]

Ren R, Jonas JB, Tian G, et al. Cerebrospinal fluid pressure in glaucoma: a prospective study. Ophthalmology. 2010;117(2):259-266.

[7]

Wang N, Xie X, Yang D, et al. Orbital cerebrospinal fluid space in glaucoma: the Beijing intracranial and intraocular pressure (iCOP) study. Ophthalmology. 2012;119(10):2065-2073.

[8]

Jonas JB, Wang N, Yang D, Ritch R, Panda-Jonas S. Facts and myths of cerebrospinal fluid pressure for the physiology of the eye. Prog Retin Eye Res. 2015;46:67-83.

[9]

Wang N. Intraocular and Intracranial Pressure Gradient in Glaucoma; 2019.

[10]

Chen MJ. Normal tension glaucoma in Asia: epidemiology, pathogenesis, diagnosis, and management. Taiwan J Ophthalmol. 2020;10(4):250-254.

[11]

Cho H-K, Kee C. Population-based glaucoma prevalence studies in Asians. Surv Ophthalmol. 2014;59(4):434-447.

[12]

Zhao J, Solano MM, Oldenburg CE, et al. Prevalence of normaltension glaucoma in the Chinese population: a systematic review and meta-analysis. Am J Ophthalmol. 2019;199:101-110.

[13]

Berdahl JP, Fautsch MP, Stinnett SS, Allingham RR. Intracranial pressure in primary open angle glaucoma, normal tension glaucoma, and ocular hypertension: a case-control study. Invest Ophthalmol Vis Sci. 2008;49(12):5412-5418.

[14]

Zhang Z, Yang D, Sang J, et al. Reproducibility of macular, retinal nerve fiber layer, and ONH measurements by OCT in Rhesus monkeys: the Beijing Intracranial and Intraocular Pressure (iCOP) Study. Invest Ophthalmol Vis Sci. 2012;53(8):4505-4509.

[15]

Yang D, Fu J, Hou R, et al. Optic neuropathy induced by experimentally reduced cerebrospinal fluid pressure in monkeys. Invest Ophthalmol Vis Sci. 2014;55(5):3067-3073.

[16]

Liang Q, Liu X. [Mechanism study on trans-lamina cribrosa pressure difference correlated with optic neuropathy in glaucoma]. Zhonghua Yan Ke Za Zhi. 2014;50(10):798-800.

[17]

Jonas JB, Wang N, Wang YX, et al. Body height, estimated cerebrospinal fluid pressure and open-angle glaucoma. The Beijing Eye Study 2011. PLoS One. 2014;9(1):e86678.

[18]

Jonas JB, Nangia V, Wang N, et al. Trans-lamina cribrosa pressure difference and open-angle glaucoma. The central India eye and medical study. PLoS One. 2013;8(12):e82284.

[19]

Lee SH, Kwak SW, Kang EM, et al. Estimated trans-lamina cribrosa pressure differences in low-teen and high-teen intraocular pressure normal tension glaucoma: the Korean national health and nutrition examination Survey. PLoS One. 2016;11(2):e0148412.

[20]

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(3):266-275.

[21]

SHAARAWY and TAREK. Glaucoma -Medical Diagnosis and Therapy -Expert Consult Premium Edition -2-volume Set.

[22]

Wareham LK, Calkins DJ. The neurovascular unit in glaucomatous neurodegeneration. Front Cell Dev Biol. 2020;8:452.

[23]

Alarcon-Martinez L, Shiga Y, Villafranca-Baughman D, et al. Neurovascular dysfunction in glaucoma. Prog Retin Eye Res. 2023;97:101217.

[24]

Schwarz TL. Mitochondrial trafficking in neurons. Cold Spring Harb Perspect Biol. 2013;5(6):a011304.

[25]

Dias MS, Luo X, Ribas VT, Petrs-Silva H, Koch JC. The role of axonal transport in glaucoma. Int J Mol Sci. 2022;23(7):3935.

[26]

Liu H, Prokosch V. Energy metabolism in the inner retina in health and glaucoma. Int J Mol Sci. 2021;22(7):3689.

[27]

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(8):4257-4266.

[28]

Zhang Z, Wu S, Liu K, et al. Time-dependent effects of reduced cerebrospinal fluid pressure on optic nerve retrograde axonal transport. Invest Ophthalmol Vis Sci. 2020;61(5):6.

[29]

Lin D, Wu S, Cheng Y, et al. Early proteomic characteristics and changes in the optic nerve head, optic nerve, and retina in a rat model of ocular hypertension. Mol Cell Proteomics. 2023;22(11):100654.

[30]

Guidoboni G, Harris A, Cassani S, et al. Intraocular pressure, blood pressure, and retinal blood flow autoregulation: a mathematical model to clarify their relationship and clinical relevance. Invest Ophthalmol Vis Sci. 2014;55(7):4105-4118.

[31]

Mann C, et al. Morphological and quantitative changes in retinal and optic nerve vessels in experimental glaucoma model with elevated IOP for 7 Weeks. Klin Monbl Augenheilkd. 2019;236(7):871-876.

[32]

Tian J, Xie Y, Li M, et al. The relationship between nailfold microcirculation and retinal microcirculation in healthy subjects. Front Physiol. 2020;11:880.

[33]

Konieczka K, Ritch R, Traverso CE, et al. Flammer syndrome. Epma J. 2014;5(1):11.

[34]

Flammer J, Konieczka K, Flammer AJ. The primary vascular dysregulation syndrome: implications for eye diseases. Epma J. 2013;4(1):14.

[35]

Flammer J, Konieczka K. The discovery of the Flammer syndrome: a historical and personal perspective. Epma J. 2017;8(2):75-97.

[36]

Konieczka K, Choi HJ, Koch S, Fankhauser F, Schoetzau A, Kim DM. Relationship between normal tension glaucoma and Flammer syndrome. Epma J. 2017;8(2):111-117.

[37]

Liu L, Li X, Killer HE, Cao K, Li J, Wang N. Changes in retinal and choroidal morphology after cerebrospinal fluid pressure reduction: a Beijing iCOP study. Sci China Life Sci. 2019;62(2):268-271.

[38]

Liu X, Khodeiry MM, Lin D, et al. The association of acute cerebrospinal fluid pressure reduction with choroidal thickness. Curr Eye Res. 2021;46(8):1193-1200.

[39]

Amerasinghe N, Aung T, Cheung N, et al. Evidence of retinal vascular narrowing in glaucomatous eyes in an Asian population. Invest Ophthalmol Vis Sci. 2008;49(12):5397-5402.

[40]

Kim JM, Sae Kim M, Ju Jang H, Ho Park K, Caprioli J. The association between retinal vessel diameter and retinal nerve fiber layer thickness in asymmetric normal tension glaucoma patients. Invest Ophthalmol Vis Sci. 2012;53(9):5609-5614.

[41]

Ramirez AI, de Hoz R, Salobrar-Garcia E, et al. The role of microglia in retinal neurodegeneration: alzheimer’s disease, Parkinson, and glaucoma. Front Aging Neurosci. 2017;9:214.

[42]

Pless ML. The eye as a window to the brain. Ann Acad Med Singapore. 2023;52(2):60-61.

[43]

Mao Y, Yang D, Li J, et al. Finite element analysis of trans-lamina cribrosa pressure difference on optic nerve head biomechanics: the Beijing Intracranial and Intraocular Pressure Study. Sci China Life Sci. 2020;63(12):1887-1894.

[44]

Oikawa K, Ver Hoeve JN, Teixeira LBC, et al. Sub-region-Specific optic nerve head glial activation in glaucoma. Mol Neurobiol. 2020;57(6):2620-2638.

[45]

Li XX, Zhang Z, Zeng HY, et al. Selective early glial reactivity in the visual pathway precedes axonal loss, following short-term cerebrospinal fluid pressure reduction. Invest Ophthalmol Vis Sci. 2018;59(8):3394-3404.

[46]

Cheng Y, Wu S, Yan X, et al. Human PrO370Leu mutant myocilin induces the phenotype of open-angle glaucoma in transgenic mice. Cell Mol Neurobiol. 2023;43(5):2021-2033.

[47]

Cheng Y, Lin D, Wu S, et al. Cerebrospinal fluid pressure reduction induces glia-mediated retinal inflammation and leads to retinal ganglion cell injury in rats. Mol Neurobiol. 2023;60(10):5770-5788.

[48]

Oikawa K, Teixeira LB, Keikhosravi A, Eliceiri KW, McLellan GJ. Microstructure and resident cell-types of the feline optic nerve head resemble that of humans. Exp Eye Res. 2021;202:108315.

[49]

Hopkins AA, Murphy R, Irnaten M, Wallace DM, Quill B, O’Brien C. The role of lamina cribrosa tissue stiffness and fibrosis as fundamental biomechanical drivers of pathological glaucoma cupping. Am J Physiol Cell Physiol. 2020;319(4):C611-C623.

[50]

Choi HJ, Sun D, Jakobs TC. Astrocytes in the optic nerve head express putative mechanosensitive channels. Mol Vis. 2015;21:749-766.

[51]

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(11):e0167364.

[52]

Li Q, Cheng Y, Zhang S, Sun X, Wu J. TRPV4-induced Müller cell gliosis and TNF-α elevation-mediated retinal ganglion cell apoptosis in glaucomatous rats via JAK2/STAT3/NF-κB pathway. J Neuroinflammation. 2021;18(1):271.

[53]

Michalick L, Erfinanda L, Weichelt U, van der Giet M, Liedtke W, Kuebler WM. Transient receptor potential vanilloid 4 and serum glucocorticoid-regulated kinase 1 are critical mediators of lung injury in overventilated mice in vivo. Anesthesiology. 2017;126(2):300-311.

[54]

Wan Y, Wang H, Fan X, et al. Mechanosensitive channel PiezO1 is an essential regulator in cell cycle progression of optic nerve head astrocytes. Glia. 2023;71(5):1233-1246.

[55]

Cheng Y, Ren T, Wang N. Biomechanical homeostasis in ocular diseases: a mini-review. Front Public Health. 2023;11:1106728.

[56]

Xie X, Zhang X, Fu J, et al. Noninvasive intracranial pressure estimation by orbital subarachnoid space measurement: the Beijing Intracranial and Intraocular Pressure (iCOP) study. Crit Care. 2013;17(4):R162.

[57]

Ren R, Wang N, Zhang X, Tian G, Jonas JB. Cerebrospinal fluid pressure correlated with body mass index. Graefes Arch Clin Exp Ophthalmol. 2012;250(3):445-446.

[58]

Jonas JB, Wang N. Association between arterial blood pressure, cerebrospinal fluid pressure and intraocular pressure in the pathophysiology of optic nerve head diseases. Clin Exp Ophthalmol. 2012;40(4):e233-e234.

[59]

Li Z, Yang Y, Lu Y, et al. Intraocular pressure vs intracranial pressure in disease conditions: a prospective cohort study (Beijing iCOP study). BMC Neurol. 2012;12(1):66.

[60]

Zhang Q, Zhang Y, Xin C, et al. Determinants of maximum cup depth in non-glaucoma and primary open-angle glaucoma subjects: a population-based study. Eye (Lond). 2020;34(5):892-900.

[61]

Geeraerts T. Noninvasive surrogates of intracranial pressure: another piece added with magnetic resonance imaging of the cerebrospinal fluid thickness surrounding the optic nerve. Crit Care. 2013;17(5):187.

[62]

Zhang Y, Cao K, Pang R, et al. Non-invasive intracranial pressure estimation using ultrasonographic measurement of area of optic nerve subarachnoid space. Br J Ophthalmol. 2023;107(11):1716-1721.

[63]

Shinojima A. Possible factors associated with spaceflight-associated neuro-ocular syndrome. JAMA Ophthalmol. 2020;138(2):172-173.

[64]

Eklund A, Jóhannesson G, Johansson E, et al. The pressure difference between eye and brain changes with posture. Ann Neurol. 2016;80(2):269-276.

[65]

Xie Y, Yang D, Huang AS, et al. Retinal microvasculature is a potential biomarker for acute mountain sickness. Sci China Life Sci. 2023;66(6):1290-1302.

[66]

Pang R, Lin D, Di X, et al. Reference values for trans-laminar cribrosa pressure difference and its association with systemic biometric factors. Eye (Lond). 2023;37(11):2240-2245.

[67]

Berdahl JP, Fleischman D, Zaydlarova J, Stinnett S, Allingham RR, Fautsch MP. Body mass index has a linear relationship with cerebrospinal fluid pressure. Invest Ophthalmol Vis Sci. 2012;53(3):1422-1427.

[68]

Pasquale LR, Willett WC, Rosner BA, Kang JH. Anthropometric measures and their relation to incident primary open-angle glaucoma. Ophthalmology. 2010;117(8):1521-1529.

[69]

Newman-Casey PA, Talwar N, Nan B, Musch DC, Pasquale LR, Stein JD. The potential association between postmenopausal hormone use and primary open-angle glaucoma. JAMA Ophthalmol. 2014;132(3):298-303.

[70]

Vajaranant TS, Grossardt BR, Maki PM, et al. Risk of glaucoma after early bilateral oophorectomy. Menopause. 2014;21(4):391-398.

[71]

Hetemäki N, Mikkola TS, Tikkanen MJ, et al. Adipose tissue estrogen production and metabolism in premenopausal women. J Steroid Biochem Mol Biol. 2021;209:105849.

[72]

Zhao T, Liu S, Zhang R, et al. Global burden of vitamin A deficiency in 204 countries and territories from 1990-2019. Nutrients. 2022;14(5):950.

[73]

Ramdas WD, Wolfs RCW, Kiefte-de Jong JC, et al. Nutrient intake and risk of open-angle glaucoma: the Rotterdam Study. Eur J Epidemiol. 2012;27(5):385-393.

[74]

Giaconi JA, Yu F, Stone KL, et al. The association of consumption of fruits/vegetables with decreased risk of glaucoma among older African-American women in the study of osteoporotic fractures. Am J Ophthalmol. 2012;154(4):635-644.

[75]

Yoserizal M, Hirooka K, Yoneda M, et al. Associations of nutrient intakes with glaucoma among Japanese Americans. Medicine (Baltim). 2019;98(49):e18314.

[76]

Pang R, Feng S, Cao K, et al. Association of serum retinol concentration with normal-tension glaucoma. Eye (Lond). 2022;36(9):1820-1825.

[77]

Zhang J, Wu S, Wang N. Trans-lamina cribrosa pressure difference activates mechanical stress signal transduction to induce glaucomatous optic neuropathy: a hypothesis. In: Wang N, ed. Intraocular and Intracranial Pressure Gradient in Glaucoma. Springer;2019:179-183.

[78]

Wang N. Road map for the pathogenesis of glaucomatous optic neuropathy. In: Wang N, ed. Intraocular and Intracranial Pressure Gradient in Glaucoma. Springer;2019:3-7.

RIGHTS & PERMISSIONS

2024 The Authors. Eye & ENT Research published by John Wiley & Sons Australia, Ltd on behalf of Higher Education Press.

AI Summary AI Mindmap
PDF (431KB)

1168

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/