Terson Syndrome

From EyeWiki



Terson Syndrome
Classification and external resources
DiseasesDB 32502


Disease

Fig. 1. Mutliple intraretinal and preretinal hemorrhages in a patient with Terson syndrome.[1]

Vitreous hemorrhage associated with subarachnoid hemorrhage (SAH) was first described by German ophthalmologist Moritz

Litten in 1881 and then in 1900 by French ophthalmologist Albert Terson [2] [3].

Terson syndrome is now recognized as intraocular hemorrhage associated with SAH, intracerebral hemorrhage, or traumatic brain injury [2]. Hemorrhage may be present in the vitreous, sub-hyaloid, or intraretina/sub-internal limiting membrane.

Epidemiology

Terson syndrome occurs in 8-19.3% of SAH [4][5][6][7][2], 9.1% of intracerebral hemorrhages and 3.1% of traumatic brain injury [2]. 5.5% of vitreous hemorrhages not caused by diabetes or trauma are caused by Terson syndrome [8].

Terson syndrome usually occurs in adults, but has been reported in children as young as 7 months [9][10]. It can be unilateral or bilateral [11].

Pathogenesis

Fig. 2. Early (A) and late (B) frames of a fluorescein angiogram showing leakage from the disc margin[12].

There are several possible pathophysiologic mechanisms for Terson syndrome. Subarachnoid blood may be directly transmitted forward through the optic nerve sheath [4][2]. More commonly, a sudden increase in intracranial pressure leads to rapid effusion of CSF into the optic nerve sheath. Then dilation of the retrobulbar optic nerve mechanically compresses the central retinal vein and 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 [13].

Fluorescein angiography has demonstrated a leakage site at the disc margin in a patient with Terson syndrome with vitreous hemorrhage. This suggests potential damage to the peripapillary retina induced by increased intracranial pressure transmitted through the optic nerve sheath [14].

Etiology

Terson syndrome has been reported to be caused by, or associated with multiple conditions associated with, a spike in intracranial pressure. These causes include carotid artery occlusion, cortical venous sinus thrombosis [15], moyamoya disease [16][17], epidural saline injection [18], intraarterial angiography, lumbosacral myelomeningocele and iaotrogenic bleeing during endoscopic third ventriculostomy [19].

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 [20] and two other studies found that anterior communicating artery aneurysms in particular are associated with a higher rate of Terson syndrome [21][22]. Other studies have shown no correlation between site of aneurysm and Terson syndrome [2] or a negative correlation between presence of anterior communicating artery aneurysm and Terson syndrome [23]. There is also no relationship between the location of the aneurysm and which eye is affected by Terson syndrome [2][20][24][25].

Clinical presentation

Fig. 3. Macular preretinal hemorrhage in a patient with Terson syndrome. [26]

Terson syndrome can present with dome-shaped hemorrhages in the macula [27]. A macular “double ring” sign may be seen with the inner ring caused sub-ILM hemorrhage and the outer ring caused by sub-hyaloid hemorrhage [28].

Although intraocular hemorrhages most frequently develop in the first hour after SAH [29], Terson syndrome can have a delayed onset, with reports of intraocular hemorrhage occurring up to 47 days after SAH [2][30].

Relationship to neurologic outcomes

Low Glasgow coma scale, high Hunt and Hesse grade, and high Fisher grade are associated with a higher incidence of Terson syndrome [2].

Neurological outcomes and mortality rate are worse in patients with SAH and Terson syndrome than patients with SAH alone [2] [20] [24][23][29][31]. In a study by Pfausler, mortality was 90% in pts with SAH and Terson syndrome and 10% in those with SAH without Terson syndrome [24]. In a study by Gutierrez Diaz, mortality was 50% when Terson syndrome was present, and 20% when absent [32].

Diagnosis

Fig. 4. B-scan showing vitreous hemorrhage in a patient with Terson syndrome[33].

Funduscopic exam is the gold standard for diagnosis of Terson syndrome. Loss of red reflex is seen in 20% of eyes with Terson syndrome[2].

B-scan may be used to confirm vitreous hemorrhage when no view to the funds is present (Fig. 4).

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 [34]. 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 Terson syndrome [35].

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 syndrome [36][16]. Thus CT may be useful to identify possible Terson syndrome prior to an eye exam.

Complications

Multiple complications have been reported after Terson syndrome. Epiretinal membrane is the most common sequelae of Terson syndrome, with an incidence of 15-78% [37][38][39][40][11]. Vitreous blood may cause ERMs by inducing glial proliferation and disruption of the ILM [37][41][38].

Retinal folds/perimacular folds occur in 20% of patients with Terson syndrome, retinal detachment occurs in 9%, and ghost cell glaucoma occurs in around 4% [37][42][35]. Proliferative vitreoretinopathy and preretinal fibrosis have also been reported after Terson syndrome [43][44][16][45]. Two patients have also been reported with macular holes, which were found intraoperatively during pars plana vitrectomy for vitreous hemorrhage [38].

Treatment and prognosis

Intraocular hemorrhage frequently resolves spontaneously [10]. Vision loss is usually reversible but permanent impairment of vision can occur [10][46]. It has been reported that about 50% of vitreous hemorrhages do not resolve after 19 months.

Fig. 5. Bilateral Terson syndrome before treatment (top images) and after bilateral pars plana vitrectomy with resolution of hemorrhage (bottom images)[47].

There is no consensus on optimal timing for vitrectomy in Terson syndrome. Vitreous hemorrhage can be observed for up to 3 months before considering pars plana vitrectomy [2][20][41]. This is supported by a study of 36 eyes with Terson syndrome in which eyes that were o

perated on within 90 days of occurrence of VH had better final VA than eyes that were operated on after 90 days [45]. If the hemorrhage is bilateral or occurs in a young child at risk of amblyopia, one may proceed with surgery sooner [2][45]. Augsten recommends operating within 4-8 weeks after the injury in patients with bilateral Terson syndrome [41].

Multiple studies have shown good outcomes after pars plana vitectomy. 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 [2]. In another study on PPV for Terson syndrome, 96% of patients had rapid visual improvement and 81% had better than 20/30 vision [48]. In a series of 15 eyes that underwent PPV for VH, 93% had final VA of 20/40 or better. [37]. ILM peeling has also been described in the surgical management of Terson syndrome [49].

Younger patients (<45 years old) who have PPV for Terson syndrome have better final visual acuity than older patients (>45 years old)[45].

Studies have shown no difference in final visual acuity between patients who were conservatively managed and those who underwent PPV. However, visual recovery was more rapid in the vitrectomy group despite these patients having denser vitreous hemorrhage [39].

Intravitreal tpa and gas have been used for recalcitrant Terson syndrome[50] [10].

One patient with Terson syndrome and premacular subhyaloid hemorrhage was treated with Nd-YAG to puncture the posterior hyaloid face and allow drainage of blood into the vitreous. VA improved from 20/400 before treatment to 20/20 one month after treatment [51].

Additional Resources

References

  1. AAO One Network Images. one.aao.org/images/terson-syndrome
  2. 2.00 2.01 2.02 2.03 2.04 2.05 2.06 2.07 2.08 2.09 2.10 2.11 2.12 2.13 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.
  3. 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.
  4. 4.0 4.1 Iuliano L, Fogliato G, Codenotti M. Intrasurgical imaging of subinternal limiting membrane blood diffusion in terson syndrome. Case Rep Ophthalmol Med. 2014;2014:689793.
  5. 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.
  6. Morris R., Kuhn F., and Witherspoon C.D.: Hemorrhagic macular cysts. Ophthalmology 1994; 101: 1.
  7. 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.
  8. 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.
  9. 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.
  10. 10.0 10.1 10.2 10.3 Kapoor S. Terson syndrome: an often overlooked complication of subarachnoid hemorrhage. World Neurosurg. 2014 Jan;81(1):e4.
  11. 11.0 11.1 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.
  12. 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.
  13. Gress DR, Wintermark M, Gean AD. A case of Terson syndrome and its mechanism of bleeding. J Neuroradiol. 2013 Oct;40(4):312-4.
  14. 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.
  15. 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.
  16. 16.0 16.1 16.2 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.
  17. 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.
  18. Naseri A, Blumenkranz MS, Horton JC. Terson's syndrome following epidural saline injection. Neurology. 2001 Jul 24;57(2):364.
  19. 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.
  20. 20.0 20.1 20.2 20.3 Fountas KN, Kapsalaki EZ, Lee GP, et al. Terson hemorrhage in patients suffering aneurysmal subarachnoid hemorrhage: predisposing factors and prognostic significance. J Neurosurg. 2008 Sep;109(3):439-44.
  21. Fahmy JA. Vitreous haemorrhage in subarachnoid haemorrhage--Terson's syndrome. Report of a case with macular degeneration as a complication. Acta Ophthalmol (Copenh). 1972;50(2):137-43.
  22. Garfinkle AM, Danys IR, Nicolle DA, Colohan AR, Brem S. Terson's syndrome: a reversible cause of blindness following subarachnoid hemorrhage. J Neurosurg. 1992 May;76(5):766-71.
  23. 23.0 23.1 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.
  24. 24.0 24.1 24.2 Pfausler B, Belcl R, Metzler R, Mohsenipour I, Schmutzhard E. Terson's syndrome in spontaneous subarachnoid hemorrhage: a prospective study in 60 consecutive patients. J Neurosurg. 1996 Sep;85(3):392-4.
  25. Sung W, Arnaldo B, Sergio C, Juliana S, Michel F. Terson's syndrome as a prognostic factor for mortality of spontaneous subarachnoid haemorrhage. Acta Ophthalmol. 2011 Sep;89(6):544-7.
  26. AAO One Network Images. one.aao.org/images/preretinal-hemorrhage-2
  27. Friedman S.M., and Margo C.E. Bilateral subinternal limiting membrane hemorrhage with Terson syndrome. Am J Ophthalmol 1997; 124: pp. 850-851.
  28. 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.
  29. 29.0 29.1 Manschot WA. Subarachnoid hemorrhage. Intraocular symptoms and their pathogenesis. Am J Ophthalmol. 1954;38:501-505.
  30. Vanderlinden RG & Chisholm LD (1974): Vitreous hemorrhages and sudden increased intracranial pressure. J Neurosurg 41: 167–176.
  31. Shaw HE Jr & Landers MB III (1975): Vitreous hemorrhage after intracranial hemorrhage. Am J Ophthalmol 80: 207–213.
  32. Gutierrez Diaz A, Jimenez Carmena J, Ruano Martin F, Diaz Lopez P, Muñoz Casado MJ. Intraocular hemorrhage in sudden increased intracranial pressure (Terson syndrome). Ophthalmologica. 1979;179(3):173-6.
  33. 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.
  34. Ashrafi AN, Chakrabarti R, Laidlaw J. Terson syndrome: the need for fundoscopy in subarachnoid haemorrhage. Med J Aust. 2012 Aug 6;197(3):152.
  35. 35.0 35.1 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.
  36. 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.
  37. 37.0 37.1 37.2 37.3 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.
  38. 38.0 38.1 38.2 Rubowitz A, Desai U. Nontraumatic macular holes associated with Terson syndrome. Retina. 2006 Feb;26(2):230-2.
  39. 39.0 39.1 Schultz PN, Sobol WM, Weingeist TA. Long-term visual outcome in Terson syndrome. Ophthalmology. 1991 Dec;98(12):1814-9.
  40. 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.
  41. 41.0 41.1 41.2 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.
  42. Keithahn M.A., Bennett S.R., Cameron D., and Mieler W.F.: Retinal folds in Terson syndrome. Ophthalmology 1993; 100: pp. 1187-1190.
  43. 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.
  44. 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.
  45. 45.0 45.1 45.2 45.3 Garweg JG, Koerner F. Outcome indicators for vitrectomy in Terson syndrome. Acta Ophthalmol. 2009 Mar;87(2):222-6.
  46. 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.
  47. Schultz PN, Sobol WM, Weingeist TA. Long-term visual outcome in Terson syndrome. Ophthalmology. 1991 Dec;98(12):1814-9. 
  48. 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.
  49. Abdelkader E, Lois N. Internal limiting membrane peeling in vitreo-retinal surgery. Surv Ophthalmol. 2008 Jul-Aug;53(4):368-96.
  50. 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.
  51. 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.