Terson Syndrome

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 by Tahira Mathen, MD on November 1, 2014.

Disease Entity


Vitreous hemorrhage associated with subarachnoid hemorrhage was first described by German ophthalmologist Moritz Litten in 1881 and then in 1900 by French ophthalmologist Albert Terson[1] [2](Czorlich, Skevas).

Terson syndrome is now recognized as intraocular hemorrhage associated with subarachnoid hemorrhage, intracerebral hemorrhage, or traumatic brain injury [1](Czorlich). Hemorrhage may be present in the vitreous, sub-hyaloid, or intraretina/sub-internal limiting membrane.


Terson syndrome occurs in 8-19.3% of subarachnoid hemorrhages (Iulano, Michaelewska, Morris, Czorlich), 9.1% of intracerebral hemorrhages, and 3.1% of traumatic brain injury (Czorlich). 5.5% of vitreous hemorrhages not caused by diabetes or trauma are caused by Terson syndrome (Verbraeken).

Terson syndrome usually occurs in adults but has been reports in children as young as 7 months (Bhardwaj, Kapoor). It can be unilateral or bilateral (Ritland).


Subarachnoid blood may be transmitted forward through the optic nerve sheath. (Iuliano, Czorlich). A sudden increase in intracranial pressure leads to rapid effusion of CSF into the optic nerve sheath. Dilation of the retrobulbar optic nerve mechanically compresses the central retinal vein. Venous hypertension results in rupture of thin retinal vessels. This mechanism is consistent with the fact that Terson syndrome can be seen in patients without intracranial hemorrhage (Gress).

Fluorescein angiography has demonstrated a leakage site at the disc margin in a patient with TS with vitreous hemorrhage. This suggests damage to peripapillary retina induced by increased intracranial pressure transmitted through the optic nerve sheath (Ogawa).


Terson syndrome has been reported to be caused by or associated with multiple conditions associated with a spike in intracranial pressure including carotid artery occlusion, cortical venous sinus thrombosis (Takkar), moyamoya disease (Kim, Arakwawa), epidural saline injection (Naseri), intraarterial angiography, lumbosacral myelomeningocele, iaotregnic during endoscopic third ventriculostomy (Hoving).

Relationship to aneurysm site

There is conflicting data on aneurysm site in SAH and Terson syndrome. Fountas found that anterior circulation aneurysms are more likely to be associated with Terson syndrome (Fountas) and two other studies found that anterior communicating artery aneurysms in particular are associated with a higher rate of TS (Fahmy, Garfinkle). Other studies have shown no correlation between site of aneurysm and TS (Czorlich) or a negative correlation between presence of anterior communicating artery aneurysm and TS (Stienen). There is also no relationship between the location of the aneurysm and which eye is affected by Terson syndrome (Czorlich, Fahmy, Fountas, Pfausler, Sung).

Clinical Presentation

TS can present with dome-shaped hemorrhages in the macula (Friedman). A macular “double ring” sign. The inner ring is cause sub-ILM hemorrhage and the outer ring is caused by sub-hyaloid hemorrhage (Srinivasan).

Although intraocular hemorrhages most frequently develop in the first hour after SAH (Manschot), Terson syndrome can have a delayed onset, with reports of intraocular hemorrhage occurring up to 47 days after SAH (Vanderlinder, Czorlich).

Prognostic factors

Low Glasgow coma scale, high Hunt and Hesse grade, and high Fisher grade are associated with a higher incidence of Terson syndrome (Czorlich).

Neurological outcomes and mortality rate are worse in patients with SAH and Terson syndrome than patients with SAH alone (Czorlich, Fountas, Manschot, Pfausler, Shaw&Landers, Vanderlinden, Stienen). In a study by Pfausler, mortality was 90% in pts with SAH and TS and 10% in those with SAH without TS (Pfausler). In a study by Gutierrez Diaz, mortality was 50% when TS present, and 20% when absent (Gutierrez Diaz).


Funduscopic exam is the gold standard for diagnosis of Terson syndrome. Loss of red reflex is seen in 20% of eyes with Terson syndrome (Czorlich).

Diagnosis may be delayed due to inability to dilate pupils due to need for neurologic monitoring. Patients may also have cognitive impairment that prevents them from verbalizing visual complaints or complying with visual testing (Ashrafi). Median time from visual symptoms to referral to an ophthalmologist was 5.2 months for unilateral cases and 4.9 months for bilateral cases in a series of 17 patients with TS (Gnanaraj).

Swallow investigated the use of orbital CT to indentify intraocular hemorrhage in patients with Terson syndrome. Retinal crescentic hyperdensities and retinal nodularity were seen in CT in two-thirds of patients with Terson (Swallow, Kim).


Proliferative vitreoretinopathy, preretinal fibrosis (van Rens), retinal detachment (9%), retinal folds/perimacular folds(20%) (Sharma)(Keithahn), and epiretinal membrane after Terson syndrome have been reported (Mena, Velikay, Kim, Garweg). 2 patients have also had macular holes which were found intraoperatively during PPV for VH (Rubowitz). Ghost cell glaucoma (4%) (Gnanaraj).

Epiretinal membrane is the most common sequelae of TS (Schultz). Epiretinal membranes have an incidence of 15-78% in eyes with Terson syndrome (Rubowitz, Yokoi, Sharma, Ritland, Schultz). Vitreous blood has been shown to cause ERMs in animal models, possibly by inducing glial proliferation and disruption of the ILM (Rubowitz, Sharma, Augsten).


Intraocular hemorrhage frequently resolves spontaneously. Kapoor). Vision loss is usually reversible but permanent impairment of vision can occur (Roux, Kapoor). Half of vitreous hemorrhage had not resolved after 19 months (Shaw and Landers 1975).

There is no consensus on optimal timing for vitrectomy in Terson syndrome. IOH can be observed for up to 3 months before considering pars plana vitrectomy (czorlich, fountas, augsten). If bilateral or in a young child at risk of amblyopia may proceed to surgery sooner (Garweg, Czorlich). Augsten recommend operating on withing 4-8 weeks after the injury in patients with bilateral TS (Augsten). In a study of 36 eyes with TS, eyes that were operated on within 90 days of occurrence of VH had better final VA than eyes that were operated on after 90 days (Garweg). Patients younger than 45 had better final VA than patients older than 45 (Garweg). Retinal detachment secondary to PVR developed in 4/36 patients between 6 and 27 months after PPV (Garweg).

In a study of 7 eyes of 6 patients that underwent pars plana vitrectomy for Terson syndrome, median VA went from HM to 20/25 and no complications were observed (czorlich). S/p PPV, Rapid visual improvement in 96% and better than 20/30 vision in 81% (Kuhn). 93% had final VA of 20/40 or better in a series of 15 eyes s/p PPV vfor VH (Sharma). (ILM peeling has also been used (Abdelkader)

There was no difference in final visual acuity between patients who were conservatively managed and thoser who underwent PPV. However, visual recovery was more rapid in the vitrectomy group despite these patients having denser vitreous hemorrhage (Schultz).

Intravitreal tpa and gas have been used for recalcitrant Terson syndrome (Seracarbasse, Kapoor).

One patient with Terson syndrome and premacular subhyaloid hemorrhage was treated with Nd-YAG to puncture the posterior hyaloids face and allow drainage of blood intot he vitreous. VA improved from 20/400 before treatment to 20/20 1 month after treatment (Ulbig).

Additional Resources

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Arakawa Y, Goto Y, Ishii A, Ueno Y, Kikuta K, Yoshizumi H, Katsuta H, Kenmochi S, Yamagata S. Terson syndrome caused by ventricular hemorrhage associated with moyamoya disease--case report. Neurol Med Chir (Tokyo). 2000 Sep;40(9):480-3.

Arroyo J.G., and Bula D.V.: Immunohistochemical study of the internal limiting membrane in Terson syndrome. Retina 2004; 24: pp. 155-157.

Ashrafi AN, Chakrabarti R, Laidlaw J. Terson syndrome: the need for fundoscopy in subarachnoid haemorrhage. Med J Aust. 2012 Aug 6;197(3):152.

Augsten R, Königsdörffer E, Strobel J. Surgical approach in terson syndrome: vitreous and retinal findings. Eur J Ophthalmol. 2000 Oct-Dec;10(4):293-6.

Bhardwaj G., Jacobs M.B., Moran K.T., and Tan K.: Terson syndrome with ipsilateral severe hemorrhagic retinopathy in a 7-month-old child. J AAPOS 2010; 14: pp. 441-443

Czorlich P, Skevas C, Knospe V, et al. Terson syndrome in subarachnoid hemorrhage, intracerebral hemorrhage, and traumatic brain injury. Neurosurg Rev. Epub 2014 Aug 31.

Friedman S.M., and Margo C.E.: Bilateral subinternal limiting membrane hemorrhage with Terson syndrome. Am J Ophthalmol 1997; 124: pp. 850-851.

Garweg JG, Koerner F. Outcome indicators for vitrectomy in Terson syndrome. Acta Ophthalmol. 2009 Mar;87(2):222-6.

Gnanaraj L, Tyagi AK, Cottrell DG, Fetherston TJ, Richardson J, Stannard KP, Inglesby DV. Referral delay and ocular surgical outcome in Terson syndrome. Retina. 2000;20(4):374-7.

Gress DR, Wintermark M, Gean AD. A case of Terson syndrome and its mechanism of bleeding. J Neuroradiol. 2013 Oct;40(4):312-4.

Hedges TR Jr. Mechanism of Terson Syndrome. Ophthalmology. 1992 May;99(5):647.

Hoving EW, Rahmani M, Los LI, Renardel de Lavalette VW. Bilateral retinal hemorrhage after endoscopic third ventriculostomy: iatrogenic Terson syndrome. J Neurosurg. 2009 May;110(5):858-60.

Iuliano L, Fogliato G, Codenotti M. Intrasurgical imaging of subinternal limiting membrane blood diffusion in terson syndrome. Case Rep Ophthalmol Med. 2014;2014:689793.

Kapoor S. Terson syndrome: an often overlooked complication of subarachnoid hemorrhage. World Neurosurg. 2014 Jan;81(1):e4.

Keithahn M.A., Bennett S.R., Cameron D., and Mieler W.F.: Retinal folds in Terson syndrome. Ophthalmology 1993; 100: pp. 1187-1190

Kim HS, Lee SW, Sung SK, Seo EK. Terson syndrome caused by intraventricular hemorrhage associated with moyamoya disease. J Korean Neurosurg Soc. 2012 Jun;51(6):367-9.

Kuhn F, Morris R, Witherspoon CD, Mester V. Terson syndrome. Results of vitrectomy and the significance of vitreous hemorrhage in patients with subarachnoid hemorrhage. Ophthalmology. 1998 Mar;105(3):472-7.

Mena O.J., Paul I., and Reichard R.R.: Ocular findings in raised intracranial pressure: a case of Terson syndrome in a 7-month-old infant. Am J Forensic Med Pathol 2011; 32: pp. 55-57.

Michalewska Z, Michalewski J, Nawrocki J. Possible methods of blood entrance in Terson syndrome. Ophthalmic Surg Lasers Imaging. 2010 Nov-Dec;41 Suppl:S42-9.

Mills MD. Terson syndrome. Ophthalmology. 1998 Dec;105(12):2161-3.

Monteagudo M, Doménech C, Segura T. Terson syndrome and ocular ultrasound. Neurologia. 2013 Feb 28. pii: S0213-4853(13)00006-6.

Morris R., Kuhn F., and Witherspoon C.D.: Hemorrhagic macular cysts. Ophthalmology 1994; 101: pp.

Morris R., Kuhn F., Witherspoon C.D., et al: Hemorrhagic macular cysts in Terson's syndrome and its implications for macular surgery. Dev Ophthalmol 1997; 29: pp. 44-54.

Ogawa T, Kitaoka T, Dake Y, Amemiya T. Terson syndrome: a case report suggesting the mechanism of vitreous hemorrhage. Ophthalmology. 2001 Sep;108(9):1654-6.

Rheinboldt M, Francis K, Parrish D, Harper D, Blase J. Terson syndrome in conjunction with ruptured intracranial aneurysm and penetrating intracranial injury: a review of two cases. Emerg Radiol. 2014 Apr;21(2):215-8.

Ritland JS, Syrdalen P, Eide N, Vatne HO, Øvergaard R. Outcome of vitrectomy in patients with Terson syndrome. Acta Ophthalmol Scand. 2002 Apr;80(2):172-5.

Roux F.X., Panthier J.N., Tanghe Y.M., Gallina P., Oswald A.M., Mérienne L., and Cioloca C.: Terson's syndrome and intraocular complications in meningeal hemorrhages (26 cases) [in French]. Neurochirurgie 1991; 37: pp. 6-11.

Rubowitz A, Desai U. Nontraumatic macular holes associated with Terson syndrome. Retina. 2006 Feb;26(2):230-2.

Serracarbassa P.D., Rodrigues L.D., and Rodrigues J.R.: Tissue plasminogen activator and intravitreal gas for the treatment of Terson's syndrome: case report. Arq Bras Oftalmol 2009; 72: pp. 403-405.

Schultz PN, Sobol WM, Weingeist TA. Long-term visual outcome in Terson syndrome. Ophthalmology. 1991 Dec;98(12):1814-9.

Sharma T, Gopal L, Biswas J, Shanmugam MP, Bhende PS, Agrawal R, Shetty NS, Sanduja N. Results of vitrectomy in Terson syndrome. Ophthalmic Surg Lasers. 2002 May-Jun;33(3):195-9.

Srinivasan S, Kyle G. Subinternal limiting membrane and subhyaloid haemorrhage in Terson syndrome: the macular 'double ring' sign. Eye (Lond). 2006 Sep;20(9):1099-101.

Stienen MN, Lücke S, Gautschi OP, Harders A. Terson haemorrhage in patients suffering aneurysmal subarachnoid haemorrhage: a prospective analysis of 60 consecutive patients. Clin Neurol Neurosurg. 2012 Jul;114(6):535-8.

Swallow CE, Tsuruda JS, Digre KB, Glaser MJ, Davidson HC, Harnsberger HR. Terson syndrome: CT evaluation in 12 patients. AJNR Am J Neuroradiol. 1998 Apr;19(4):743-7.

Takkar A, Kesav P, Lal V, Gupta A. Teaching NeuroImages: Terson syndrome in cortical venous sinus thrombosis. Neurology. 2013 Aug 6;81(6):e40-1.

Ulbig MW, Mangouritsas G, Rothbacher HH, Hamilton AM, McHugh JD. Long-term results after drainage of premacular subhyaloid hemorrhage into the vitreous with a pulsed Nd:YAG laser. Arch Ophthalmol. 1998 Nov;116(11):1465-9.

Velikay M., Datlinger P., Stolba U., Wedrich A., Binder S., and Hausmann N.: Retinal detachment with severe proliferative vitreoretinopathy in Terson syndrome. Ophthalmology 1994; 101: pp. 35-37

Verbraeken H, Van Egmond J. Non-diabetic and non-oculotraumatic vitreous haemorrhage treated by pars plana vitrectomy. Bull Soc Belge Ophtalmol. 1999;272:83-9.

Yokoi M, Kase M, Hyodo T, Horimoto M, Kitagawa F, Nagata R. Epiretinal membrane formation in Terson syndrome. Jpn J Ophthalmol. 1997 May-Jun;41(3):168-73.

  1. 1.0 1.1 Czorlich P, Skevas C, Knospe V, et al. Terson syndrome in subarachnoid hemorrhage, intracerebral hemorrhage, and traumatic brain injury. Neurosurg Rev. Epub 2014 Aug 31.
  2. Skevas C, Czorlich P,Knospe V, et al. Terson's syndrome--rate and surgical approach in patients with subarachnoid hemorrhage: a prospective interdisciplinary study. Ophthalmology. 2014 Aug;121(8):1628-33.