دورية أكاديمية

An explanation for Terson syndrome at last: the glymphatic reflux theory.

التفاصيل البيبلوغرافية
العنوان: An explanation for Terson syndrome at last: the glymphatic reflux theory.
المؤلفون: Kumaria A; Department of Neurosurgery, Queen's Medical Centre, Nottingham University Hospitals NHS Trust, Derby Road, Nottingham, NG7 2UH, UK. Ashwin.Kumaria@doctors.org.uk., Gruener AM; School of Medicine, University of Nottingham, Nottingham, UK.; Department of Ophthalmology, Queen's Medical Centre, Nottingham University Hospitals NHS Trust, Nottingham, UK., Dow GR; Department of Neurosurgery, Queen's Medical Centre, Nottingham University Hospitals NHS Trust, Derby Road, Nottingham, NG7 2UH, UK., Smith SJ; Department of Neurosurgery, Queen's Medical Centre, Nottingham University Hospitals NHS Trust, Derby Road, Nottingham, NG7 2UH, UK.; School of Medicine, University of Nottingham, Nottingham, UK., Macarthur DC; Department of Neurosurgery, Queen's Medical Centre, Nottingham University Hospitals NHS Trust, Derby Road, Nottingham, NG7 2UH, UK.; School of Medicine, University of Nottingham, Nottingham, UK., Ingale HA; Department of Neurosurgery, Queen's Medical Centre, Nottingham University Hospitals NHS Trust, Derby Road, Nottingham, NG7 2UH, UK.
المصدر: Journal of neurology [J Neurol] 2022 Mar; Vol. 269 (3), pp. 1264-1271. Date of Electronic Publication: 2021 Jun 25.
نوع المنشور: Journal Article; Review
اللغة: English
بيانات الدورية: Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 0423161 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-1459 (Electronic) Linking ISSN: 03405354 NLM ISO Abbreviation: J Neurol Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Berlin ; New York, Springer-Verlag
مواضيع طبية MeSH: Intracranial Hypertension*/etiology , Subarachnoid Hemorrhage*/complications, Humans ; Intracranial Pressure ; Optic Nerve/diagnostic imaging ; Vitreous Hemorrhage/etiology
مستخلص: Terson Syndrome (TS) describes the presence of intraocular hemorrhage in patients with intracranial hemorrhage, typically subarachnoid hemorrhage. Despite TS being a well-defined and frequently occurring phenomenon, its pathophysiology remains controversial. This review will present the current understanding of TS, with view to describing a contemporary and more plausible pathomechanism of TS, given recent advances in ophthalmic science and neurobiology. Previously proposed theories include a sudden rise in intracranial pressure (ICP) transmitted to the optic nerve sheath leading to rupture of retinal vessels; or intracranial blood extending to the orbit via the optic nerve sheath. The origin of blood in TS is uncertain, but retinal vessels appear to be an unlikely source. In addition, an anatomical pathway for blood to enter the eye from the intracranial space remains poorly defined. An ocular glymphatic system has recently been described, drainage of which from the globe into intracranial glymphatics is reliant on the pressure gradient between intraocular pressure and intracranial pressure. The glymphatic pathway is the only extravascular anatomical conduit between the subarachnoid space and the retina. We propose that subarachnoid blood in skull base cisterns near the optic nerve is the substrate of blood in TS. Raised ICP causes it to be refluxed through glymphatic channels into the globe, resulting in intraocular hemorrhage. We herewith present glymphatic reflux as an alternative theory to explain the phenomenon of Terson Syndrome.
(© 2021. Springer-Verlag GmbH Germany, part of Springer Nature.)
References: Litten M (1881) Über Einige vom Allgemein-Klinischen Standpunkt aus Interessante Augenveränderungen. Berl Klin Wochenschr 18:23–27.
De TA (1900) l’hémorrhagie dans le corps vitre au cours de l’hémorrhagie cerebrale. Clin Ophthalmol 6:309–312.
Czorlich P, Skevas C, Knospe V, Vettorazzi E, Westphal M, Regelsberger J (2016) Terson’s syndrome—pathophysiologic considerations of an underestimated concomitant disease in aneurysmal subarachnoid hemorrhage. J Clin Neurosci 33:182–186. (PMID: 27452126)
Fountas KN, Kapsalaki EZ, Lee GP, Machinis TG, Grigorian AA, Robinson JS, Vergados I, Theodosiadis PG (2008) Terson hemorrhage in patients suffering aneurysmal subarachnoid hemorrhage: predisposing factors and prognostic significance. J Neurosurg 109(3):439–444. (PMID: 18759574)
Czorlich P, Skevas C, Knospe V, Vettorazzi E, Richard G, Wagenfeld L, Westphal M, Regelsberger J (2015) Terson syndrome in subarachnoid hemorrhage, intracerebral hemorrhage, and traumatic brain injury. Neurosurg Rev 38(1):129–136 (discussion 136). (PMID: 25173620)
Medele RJ, Stummer W, Mueller AJ, Steiger HJ, Reulen HJ (1998) Terson’s syndrome in subarachnoid hemorrhage and severe brain injury accompanied by acutely raised intracranial pressure. J Neurosurg 88(5):851–854. (PMID: 9576253)
Wang YM, Nudleman E, Vinocur D, Kuo DJ (2018) Terson syndrome before induction chemotherapy for acute lymphoblastic leukemia. J Pediatr Hematol Oncol 40(2):141–142. (PMID: 29200170)
Scheller J, Doroslovacki P (2015) Ruptured aneurysm and terson syndrome in a 1-month-old infant. Pediatr Neurol 52(6):653–654. (PMID: 26002054)
Monteagudo M, Doménech C, Segura T (2015) Terson syndrome and ocular ultrasound. Neurologia 30(2):133–134. (PMID: 23453591)
Jayasekera BA, Deniz K, Pereira EA, Chandra J, Cudlip SA (2012) Terson’s syndrome diagnosed by CT. Br J Neurosurg 26(6):919–920. (PMID: 22577848)
Reale C, Brigandì A, Gorgoglione N, Laganà A, Girlanda P (2020) Terson’s syndrome. Pract Neurol 20(2):163–164. (PMID: 31666299)
Stienen MN, Lücke S, Gautschi OP, Harders A (2012) Terson haemorrhage in patients suffering aneurysmal subarachnoid haemorrhage: a prospective analysis of 60 consecutive patients. Clin Neurol Neurosurg 114(6):535–538. (PMID: 22472353)
Joswig H, Epprecht L, Valmaggia C, Leschka S, Hildebrandt G, Fournier JY, Stienen MN (2016) Terson syndrome in aneurysmal subarachnoid hemorrhage-its relation to intracranial pressure, admission factors, and clinical outcome. Acta Neurochir 158(6):1027–1036. (PMID: 27038169)
Gress DR, Wintermark M, Gean AD (2013) A case of Terson syndrome and its mechanism of bleeding. J Neuroradiol 40(4):312–314. (PMID: 24095292)
Liu X, Yang L, Cai W, Gao L, Li Y (2020) Clinical features and visual prognostic indicators after vitrectomy for Terson syndrome. Eye 34(4):650–656. (PMID: 31455901)
Garweg JG, Koerner F (2009) Outcome indicators for vitrectomy in Terson syndrome. Acta Ophthalmol 87(2):222–226. (PMID: 18537934)
Kuhn F, Morris R, Witherspoon CD, Mester V (1998) Terson syndrome. Results of vitrectomy and the significance of vitreous hemorrhage in patients with subarachnoid hemorrhage. Ophthalmology 105(3):472–477. (PMID: 9499778)
Schultz PN, Sobol WM, Weingeist TA (1991) Long-term visual outcome in Terson syndrome. Ophthalmology 98(12):1814–1819. (PMID: 1775315)
Gutierrez Diaz A, Jimenez Carmena J, Ruano Martin F, Diaz Lopez P, Muñoz Casado MJ (1979) Intraocular hemorrhage in sudden increased intracranial pressure (Terson syndrome). Ophthalmologica 179(3):173–176. (PMID: 548854)
Pfausler B, Belcl R, Metzler R, Mohsenipour I, Schmutzhard E (1996) Terson’s syndrome in spontaneous subarachnoid hemorrhage: a prospective study in 60 consecutive patients. J Neurosurg 85(3):392–394. (PMID: 8751622)
McCarron MO, Alberts MJ, McCarron P (2004) A systematic review of Terson’s syndrome: frequency and prognosis after subarachnoid hemorrhage. J Neurol Neurosurg Psychiatry 75(3):491–493. (PMID: 149661731738971)
Sung W, Arnaldo B, Sergio C, Juliana S, Michel F (2011) Terson’s syndrome as a prognostic factor for mortality of spontaneous subarachnoid haemorrhage. Acta Ophthalmol 89(6):544–547. (PMID: 20003110)
Greenberg M (2016) Handbook of neurosurgery, 8th edn. Thieme Medical Publishers, pp 1158–1159.
Ren Y, Wu Y, Guo G (2018) Terson syndrome secondary to subarachnoid hemorrhage: a case report and literature review. World Neurosurg S1878-8750(18):32907–32913.
Garfinkle AM, Danys IR, Nicolle DA, Colohan AR, Brem S (1992) Terson’s syndrome: a reversible cause of blindness following subarachnoid hemorrhage. J Neurosurg 76(5):766–771. (PMID: 1564539)
Hedges TR Jr, Walsh FB (1955) Optic nerve sheath and subhyaloid hemorrhage as a complication of angiocardiography. AMA Arch Ophthalmol 54(3):425–427. (PMID: 13248305)
Walsh FB, Hedges TR Jr (1951) Optic nerve sheath hemorrhage. Am J Ophthalmol 34(4):509–527. (PMID: 14819178)
Manschot WA (1954) Subarachnoid hemorrhage; intraocular symptoms and their pathogenesis. Am J Ophthalmol 38(4):501–505. (PMID: 13197505)
Tildsley J, Srinivasan S (2009) Valsalva retinopathy. Postgrad Med J 85(1000):110. (PMID: 19329707)
Eneh A, Almeida D (2013) Valsalva hemorrhagic retinopathy during labour: a case report and literature review. Can J Ophthalmol 48(6):e145–e147. (PMID: 24314426)
Cai CX, Han IC (2017) Cough-induced valsalva retinopathy. Ophthalmol Retina 1(5):427. (PMID: 31047574)
Vanderlinden RG, Chisholm LD (1974) Vitreous hemorrhages and sudden increased intracranial pressure. J Neurosurg 41(2):167–176. (PMID: 4842785)
Gnanaraj L, Tyagi AK, Cottrell DG, Fetherston TJ, Richardson J, Stannard KP, Inglesby DV (2000) Referral delay and ocular surgical outcome in Terson syndrome. Retina 20(4):374–377. (PMID: 10950415)
Swallow CE, Tsuruda JS, Digre KB, Glaser MJ, Davidson HC, Harnsberger HR (1998) Terson syndrome: CT evaluation in 12 patients. AJNR Am J Neuroradiol 19(4):743–747. (PMID: 95766668337382)
Castaño-Duque CH, Pons-Irazazabal LC, López-Moreno JL (1997) Subarachnoid hemorrhage associated to subhyaloid hemorrhage: “Terson syndrome.” Rev Neurol 25(143):1081–1083. (PMID: 9280640)
Sakamoto M, Nakamura K, Shibata M, Yokoyama K, Matsuki M, Ikeda T (2010) Magnetic resonance imaging findings of Terson’s syndrome suggesting a possible vitreous hemorrhage mechanism. Jpn J Ophthalmol 54(2):135–139. (PMID: 20401562)
Fong AC, Schatz H (1993) Central retinal vein occlusion in young adults. Surv Ophthalmol 37(6):393–417. (PMID: 8516752)
Fahmy JA (1972) Vitreous haemorrhage in subarachnoid haemorrhage—Terson’s syndrome Report of a case with macular degeneration as a complication. Acta Ophthalmol 50(2):137–143.
Moteki Y, Niimi Y, Okada Y, Kawamata T (2018) Ruptured vertebral artery dissecting aneurysm as a risk factor for ocular symptoms accompanied with subarachnoid hemorrhage. World Neurosurg 116:e505–e512. (PMID: 29758373)
Baker ML, Hand PJ, Tange D (2008) Terson’s syndrome in spontaneous spinal subarachnoid hemorrhage. J Clin Neurosci 15(3):313–316. (PMID: 18191572)
Pagani-Estévez GL, Chen JJ, Watson JC, Leavitt JA (2016) Acute vision loss secondary to epidural blood patch: terson syndrome. Reg Anesth Pain Med 41(2):164–168. (PMID: 26735156)
Ogawa T, Kitaoka T, Dake Y, Amemiya T (2001) Terson syndrome: a case report suggesting the mechanism of vitreous hemorrhage. Ophthalmology 108(9):1654–1656. (PMID: 11535467)
Anderson DR, Hoyt WF (1969) Ultrastructure of intraorbital portion of human and monkey optic nerve. Arch Ophthalmol 82(4):506–530. (PMID: 4981187)
Anderson DR (1969) Ultrastructure of human and monkey lamina cribrosa and optic nerve head. Arch Ophthalmol 82(6):800–814. (PMID: 4982225)
Michalewska Z, Michalewski J, Nawrocki J (2010) Possible methods of blood entrance in Terson syndrome. Ophthalmic Surg Laser Imaging. https://doi.org/10.3928/15428877-20101031-15. (PMID: 10.3928/15428877-20101031-15)
Da Mesquita S, Fu Z, Kipnis J (2018) The meningeal lymphatic system: a new player in neurophysiology. Neuron 100(2):375–388. (PMID: 303596036268162)
Jessen NA, Munk AS, Lundgaard I, Nedergaard M (2015) The glymphatic system: a beginner’s guide. Neurochem Res 40(12):2583–2599. (PMID: 259473694636982)
Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA, Nagelhus EA, Nedergaard M (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4(147):147ra111. (PMID: 228966753551275)
Rasmussen MK, Mestre H, Nedergaard M (2018) The glymphatic pathway in neurological disorders. Lancet Neurol 17(11):1016–1024. (PMID: 303538606261373)
Tamura R, Yoshida K, Toda M (2019) Current understanding of lymphatic vessels in the central nervous system. Neurosurg Rev. https://doi.org/10.1007/s10143-019-01133-0. (PMID: 10.1007/s10143-019-01133-031781985)
Mestre H, Mori Y, Nedergaard M (2020) The brain’s glymphatic system: current controversies. Trends Neurosci 43(7):458–466. https://doi.org/10.1016/j.tins.2020.04.003. (PMID: 10.1016/j.tins.2020.04.003324237647331945)
Sandrone S, Moreno-Zambrano D, Kipnis J, van Gijn J (2019) A (delayed) history of the brain lymphatic system. Nat Med 25(4):538–540. https://doi.org/10.1038/s41591-019-0417-3. (PMID: 10.1038/s41591-019-0417-330948855)
Eide PK, Ringstad G (2015) MRI with intrathecal MRI gadolinium contrast medium administration: a possible method to assess glymphatic function in human brain. Acta Radiol Open 4(11):2058460115609635. (PMID: 266341474652208)
Louveau A, Herz J, Alme MN, Salvador AF, Dong MQ, Viar KE, Herod SG, Knopp J, Setliff JC, Lupi AL, Da Mesquita S, Frost EL, Gaultier A, Harris TH, Cao R, Hu S, Lukens JR, Smirnov I, Overall CC, Oliver G, Kipnis J (2018) CNS lymphatic drainage and neuroinflammation are regulated by meningeal lymphatic vasculature. Nat Neurosci 21(10):1380–1391. (PMID: 302248106214619)
Ahn JH, Cho H, Kim JH, Kim SH, Ham JS, Park I, Suh SH, Hong SP, Song JH, Hong YK, Jeong Y, Park SH, Koh GY (2019) Meningeal lymphatic vessels at the skull base drain cerebrospinal fluid. Nature 572(7767):62–66. (PMID: 31341278)
Denniston AK, Keane PA (2015) Paravascular pathways in the eye: is there an 'ocular glymphatic system'? Invest Ophthalmol Vis Sci 56(6):3955–3956. (PMID: 26087361)
Wostyn P, Van Dam D, Audenaert K, Killer HE, De Deyn PP, De Groot V (2015) A new glaucoma hypothesis: a role of glymphatic system dysfunction. Fluids Barriers CNS 29(12):16.
Mathieu E, Gupta N, Ahari A, Zhou X, Hanna J, Yücel YH (2017) Evidence for cerebrospinal fluid entry into the optic nerve via a glymphatic pathway. Invest Ophthalmol Vis Sci 58(11):4784–4791. (PMID: 28973323)
Goel M, Picciani RG, Lee RK, Bhattacharya SK (2010) Aqueous humor dynamics: a review. Open Ophthalmol J 3(4):52–59.
Wang X, Lou N, Eberhardt A, Yang Y, Kusk P, Xu Q, Förstera B, Peng S, Shi M, Ladrón-de-Guevara A, Delle C, Sigurdsson B, Xavier ALR, Ertürk A, Libby RT, Chen L, Thrane AS, Nedergaard M (2020) An ocular glymphatic clearance system removes β-amyloid from the rodent eye. Sci Transl Med 12(536):eaaw3210. (PMID: 322136287356596)
Jacobsen HH, Ringstad G, Jørstad ØK, Moe MC, Sandell T, Eide PK (2019) The human visual pathway communicates directly with the subarachnoid space. Invest Ophthalmol Vis Sci 60(7):2773–2780. (PMID: 31247084)
Wostyn P, De Groot V, Van Dam D, Audenaert K, De Deyn PP, Killer HE (2016) The glymphatic system: a new player in ocular diseases? Invest Ophthalmol Vis Sci 57(13):5426–5427. (PMID: 27768786)
Wostyn P, Killer HE, De Deyn PP (2017) Glymphatic stasis at the site of the lamina cribrosa as a potential mechanism underlying open-angle glaucoma. Clin Exp Ophthalmol 45(5):539–547. (PMID: 28129671)
Mathieu E, Gupta N, Paczka-Giorgi LA, Zhou X, Ahari A, Lani R, Hanna J, Yücel YH (2018) Reduced cerebrospinal fluid inflow to the optic nerve in glaucoma. Invest Ophthalmol Vis Sci 59(15):5876–5884. (PMID: 30543343)
Davoodi-Bojd E, Ding G, Zhang L, Li Q, Li L, Chopp M, Zhang Z, Jiang Q (2019) Modeling glymphatic system of the brain using MRI. Neuroimage 188:616–627. (PMID: 30578928)
Eide PK, Ringstad G (2019) In vivo imaging of molecular clearance from human entorhinal cortex: a possible method for preclinical testing of dementia. Gerontol Geriatr Med 28(5):2333721419889739.
Ringstad G, Vatnehol SAS, Eide PK (2017) Glymphatic MRI in idiopathic normal pressure hydrocephalus. Brain 140(10):2691–2705. (PMID: 289693735841149)
Potts MB, Wu AC, Rusinak DJ, Kesavabhotla K, Jahromi BS (2018) Seeing floaters: a case report and literature review of intraventricular migration of silicone oil tamponade material for retinal detachment. World Neurosurg 115:201–205. (PMID: 29678701)
Fangtian D, Rongping D, Lin Z, Weihong Y (2005) Migration of intraocular silicone into the cerebral ventricles. Am J Ophthalmol 140(1):156–158. (PMID: 16038670)
Eller AW, Friberg TR, Mah F (2000) Migration of silicone oil into the brain: a complication of intraocular silicone oil for retinal tamponade. Am J Ophthalmol 129(5):685–688. https://doi.org/10.1016/s0002-9394(00)00368-8 (PMID: 10844074). (PMID: 10.1016/s0002-9394(00)00368-810844074)
Lenck S, Radovanovic I, Nicholson P, Hodaie M, Krings T, Mendes-Pereira V (2018) Idiopathic intracranial hypertension: the veno glymphatic connections. Neurology 91(11):515–522. (PMID: 30201744)
Bezerra MLS, Ferreira ACAF, de Oliveira-Souza R (2018) Pseudotumor cerebri and glymphatic dysfunction. Front Neurol 16(8):734.
Denniston AK, Keane PA, Aojula A, Sinclair AJ, Mollan SP (2017) The ocular glymphatic system and idiopathic intracranial hypertension: Author Response to “hypodense holes and the ocular glymphatic system”. Invest Ophthalmol Vis Sci. 58(2):1134–1136. https://doi.org/10.1167/iovs.17-21479. (PMID: 10.1167/iovs.17-2147928196227)
Quah BL, Munusamy T, Watts C (2019) Primary central nervous system lymphoma. In: Kirollos RW, Helmy A, Thomson S, Hutchinson PJA (eds) Oxford textbook of neurological surgery, Oxford University Press.
Gündüz K, Pulido JS, McCannel CA, O’Neill BP (2006) Ocular manifestations and treatment of central nervous system lymphomas. Neurosurg Focus 21(5):E9–E10. (PMID: 17134125)
Coupland SE, Chan CC, Smith J (2009) Pathophysiology of retinal lymphoma. Ocul Immunol Inflamm 17(4):227–237. https://doi.org/10.1080/09273940903168696. (PMID: 10.1080/09273940903168696196579752769503)
Chan CC, Haen SP, Möhle R, Zierhut M (2016) Primary intraocular lymphoma. In: Zierhut M, Pavesio C, Ohno S, Orefice F, Rao N (eds) Intraocular inflammation. Springer, Berlin. https://doi.org/10.1007/978-3-540-75387-2_147. (PMID: 10.1007/978-3-540-75387-2_147)
Eichler AF, Batchelor TT (2006) Primary central nervous system lymphoma: presentation, diagnosis and staging. Neurosurg Focus 21(5):E15. https://doi.org/10.3171/foc.2006.21.5.16. (PMID: 10.3171/foc.2006.21.5.1617134117)
Küker W, Nägele T, Korfel A et al (2005) Primary central nervous system lymphomas (PCNSL): MRI features at presentation in 100 patients. J Neurooncol 72(2):169–177. https://doi.org/10.1007/s11060-004-3390-7. (PMID: 10.1007/s11060-004-3390-715925998)
Kawasaki K, Wakabayashi K, Koizumi T, Tanaka R, Takahashi H (2002) Spinal cord involvement of primary central nervous system lymphomas: histopathological examination of 14 autopsy cases. Neuropathology 22(1):13–18. https://doi.org/10.1046/j.0919-6544.2002.00421.x. (PMID: 10.1046/j.0919-6544.2002.00421.x12030410)
Kumaria A, Teale A, Kulkarni GV, Ingale HA, Macarthur DC, Robertson IJA (2018) Glioblastoma multiforme metastatic to lung in the absence of intracranial recurrence: case report. Br J Neurosurg. https://doi.org/10.1080/02688697.2018.1529296 (published online ahead of print: 19 Nov 2018). (PMID: 10.1080/02688697.2018.15292963045100530451005)
Madsen JR, Egnor M, Zou R (2006) Cerebrospinal fluid pulsatility and hydrocephalus: the fourth circulation. Clin Neurosurg 53:48–52. (PMID: 17380738)
فهرسة مساهمة: Keywords: Glymphatic system; Intraocular hemorrhage; Subarachnoid hemorrhage; Terson syndrome
تواريخ الأحداث: Date Created: 20210625 Date Completed: 20220222 Latest Revision: 20220222
رمز التحديث: 20231215
DOI: 10.1007/s00415-021-10686-4
PMID: 34170402
قاعدة البيانات: MEDLINE
الوصف
تدمد:1432-1459
DOI:10.1007/s00415-021-10686-4