Skip to main content

Advertisement

SpringerLink
Log in

Terson syndrome in subarachnoid hemorrhage, intracerebral hemorrhage, and traumatic brain injury

  • Original Article
  • Published:
Neurosurgical Review Aims and scope Submit manuscript

Abstract

This prospective trial was designed to evaluate the incidence of Terson syndrome in patients suffering from subarachnoid hemorrhage, intracerebral hemorrhage, or traumatic brain injury and whether consequences necessarily derive from the intraocular hemorrhage itself. Two ophthalmologic examinations were performed to identify patients with Terson syndrome. Data on initial Glasgow Coma Scale, Hunt and Hess and Fisher grades, aneurysm site and diameter, and volume of hemorrhage in intracerebral hemorrhage patients were correlated to the location and course of Terson syndrome. Follow-up was performed after 3 months, including clinical and ophthalmologic investigations. The data showed that 16 of 83 subarachnoid hemorrhage patients (19.3 %), 2 of 22 intracerebral hemorrhage patients (9.1 %), and 1 of 32 traumatic brain injury patients (3.1 %) suffered from Terson syndrome. Low Glasgow Coma Scale (p = 0.002), high Hunt and Hess grade (p < 0.001), and high Fisher grade (p = 0.002) were found to be associated with a higher incidence of Terson syndrome. The neurological outcome in subarachnoid hemorrhage patients suffering from Terson syndrome was worse compared with that of subarachnoid hemorrhage patients without Terson syndrome (p = 0.005), and vitrectomy was performed in seven eyes of six patients due to poor visual acuity. Terson syndrome is underestimated in patients with subarachnoid hemorrhage and a rare pathology in intracerebral hemorrhage as well as in traumatic brain injury patients. Spontaneous regression of the intraocular hemorrhage may be seen, but in half of the patients, vitrectomy is necessary to prevent permanent visual deterioration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Arakawa Y, Goto Y, Ishii A, Ueno Y, Kikuta K, Yoshizumi H et al (2000) Terson syndrome caused by ventricular hemorrhage associated with moyamoya disease. Neurol Med Chir (Tokyo) 40:480–483

    Article  CAS  Google Scholar 

  2. Augsten R, Konigsdorffer E (2007) Terson syndrome—a contribution to the timing of operation for pars plana vitrectomy. Klin Monbl Augenheilkd 224:674–677, German

    Article  CAS  PubMed  Google Scholar 

  3. Baker ML, Hand PJ, Tange D (2008) Terson’s syndrome in spontaneous spinal subarachnoid haemorrhage. J Clin Neurosci 15:313–316

    Article  PubMed  Google Scholar 

  4. Castren JA (1963) Pathogenesis and treatment of Terson-syndrome. Acta Ophthalmol 41:430–434

    Article  CAS  Google Scholar 

  5. Fahmy JA (1973) Fundal haemorrhages in ruptured intracranial aneurysms I. Material, frequency and morphology. Acta Ophthalmol (Copenh) 51:289–298

    Article  CAS  Google Scholar 

  6. Fountas KN, Kapsalaki EZ, Lee GP, Machinis TG, Grigorian AA, Robinson JS et al (2008) Terson hemorrhage in patients suffering aneurysmal subarachnoid hemorrhage: predisposing factors and prognostic significance. J Neurosurg 109:439–444

    Article  PubMed  Google Scholar 

  7. Frizzel RT, Kuhn F, Morris R, Quinn C, Fisher WS III (1997) Screening for ocular hemorrhages in patients with ruptured cerebral aneurysms: a prospective study of 99 patients. Neurosurgery 41:529–533, Discussion 33–34

    Google Scholar 

  8. Garfinkle AM, Danys IR, Nicolle DA, Colohan AR, Brem S (1992) Terson’s syndrome: a reversible cause of blindness following subarachnoid hemorrhage. J Neurosurg 76:766–771

    Article  CAS  PubMed  Google Scholar 

  9. Gauntt CD, Sherry RG, Kannan C (2007) Terson syndrome with bilateral optic nerve sheath hemorrhage. J Neuroophthalmol 27(3):193–194

    Article  PubMed  Google Scholar 

  10. Gibran S, Mirza K, Kinsella F (2002) Unilateral vitreous haemorrhage secondary to caudal epidural injection: a variant of Terson’s syndrome. Br J Ophthalmol 86:353–354

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Hegdes TR Jr, Walsh FB (1955) Optic nerve sheath and subhyaloid hemorrhage as a complication of angiocardiography. AMA Arch Ophthalmol 54:425–427

    Article  Google Scholar 

  12. Hoving EW, Rahmani M, Los LI, Renardel de Lavalette VW (2009) Bilateral retinal hemorrhage after endoscopic third ventriculostomy: iatrogenic Terson syndrome. J Neurosurg 100:858–860

    Article  Google Scholar 

  13. Kim HS, Lee SW, Sung SK, Seo EK (2012) Terson syndrome caused by intraventricular hemorrhage associated with moyamoya disease. J Korean Neurosurg Soc 51:367–369

    Article  PubMed Central  PubMed  Google Scholar 

  14. 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 105:472–477

    Article  CAS  PubMed  Google Scholar 

  15. Litten M (1881) Ueber Einige von Allgemein-Klinischen Standpunkt aus Interessante Augenveränderungen. Berl Klin Wochenschr 18:23–27, German

    Google Scholar 

  16. Manschot WA (1954) Subarachnoid hemorrhage. Intraocular symptoms and their pathogenesis. Am J Ophthalmol 38:501–505

    Article  CAS  PubMed  Google Scholar 

  17. 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 88:851–854

    Article  CAS  PubMed  Google Scholar 

  18. Mena OJ, Paul I, Reichard RR (2011) Ocular findings in raised intracranial pressure: a case of Terson syndrome in a 7-month-old infant. Am J Forensic Med Pathol 32:55–57

    Article  PubMed  Google Scholar 

  19. Muller PJ, Deck JH (1974) Intraocular and optic nerve sheath hemorrhage in cases of sudden intracranial hypertension. J Neurosurg 41:160–166

    Article  CAS  PubMed  Google Scholar 

  20. Naseri A, Blumenkranz MS, Horton JC (2001) Terson’s syndrome following epidural saline injection. Neurology 57:364

    Article  CAS  PubMed  Google Scholar 

  21. Ogawa T, Kitaoka T, Dake Y, Amemiya T (2001) Terson syndrome. A case report suggesting the mechanism of vitreous hemorrhage. Ophthalmology 108:1654–1656

    Article  CAS  PubMed  Google Scholar 

  22. 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 85:392–394

    Article  CAS  PubMed  Google Scholar 

  23. Shaw HE Jr, Landers MB III (1975) Vitreous hemorrhage after intracranial hemorrhage. Am J Ophthalmol 80:207–213

    Article  PubMed  Google Scholar 

  24. Shaw HE Jr, Landers MB III, Syndor CF (1977) The significance of intraocular hemorrhages due to subarachnoid hemorrhage. An Ophthalmol 9:1403–1405

    Google Scholar 

  25. Stiebel-Kalish H, Turtel LS, Kupersmith MJ (2004) The natural history of nontraumatic subarachnoid hemorrhage-related intraocular hemorrhages. Retina 24:36–40

    Article  PubMed  Google Scholar 

  26. Stienen MN, Lücke S, Gautschi OP, Harders A (2012) Terson hemorrhage in patients suffering aneurysmal subarachnoid hemorrhage: a prospective analysis of 60 consecutive patients. Clin Neurol Neurosurg 114:535–538

    Article  PubMed  Google Scholar 

  27. 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 89:544–547

    Article  PubMed  Google Scholar 

  28. Swallow CE, Tsuruda JS, Digre KB, Glaser MJ, Davidson HC, Harnsberger HR (1998) Terson syndrome: CT evaluation in 12 patients. AJNR Am J Neuroradiol 19:743–747

    CAS  PubMed  Google Scholar 

  29. Takkar A, Kesav P, Lal V, Gupta A (2013) Terson syndrome in cortical venous sinus thrombosis. Neurology 81:e40–e41

    Article  PubMed  Google Scholar 

  30. Terson A (1900) De ĺhemorrhagie dans le corps vitre au cours de ĺhemorrhagie cerebrale. Clin Ophthalmol 6:309–312

    Google Scholar 

  31. Toosi SH, Malton M (1987) Terson’s syndrome-significance of ocular findings. Ann Ophthalmol 19:7–12

    CAS  PubMed  Google Scholar 

  32. Vanderlinden RG, Chisholm LD (1974) Vitreous hemorrhages and sudden increased intracranial pressure. J Neurosurg 41:167–176

    Article  CAS  PubMed  Google Scholar 

  33. Walsh FB, Hedges TR (1951) Optic nerve sheath hemorrhage. Am J Ophthalmol 34:509–527

    Article  CAS  PubMed  Google Scholar 

  34. Weaver RG, Davis CH (1961) Subhyaloid hemorrhage. Am J Ophthalmol 52:257–259

    Article  CAS  PubMed  Google Scholar 

  35. Wietholter S, Steube D, Stotz HP (1998) Terson syndrome: a frequently missed opthalmologic complication in subarachnoid hemorrhage. Zentralbl Neurochir 59:166–170

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the nursing staff and ward physicians in the department of intensive care at our medical center for their patience and support of the study. We also would like to express our deep gratitude to all enrolled patients and their legal representatives for making this study possible.

Authors’ contributions

PC, VK, and JR conceived and designed the study. PC, CS, VK, and LW acquired the data. PC, CS, EV, and LW analyzed and interpreted the data. PC, GR, LW, MW, and JR revised the article critically for important intellectual content. PC, CS, MW, and JR gave the final approval of the version to be published.

Conflict of interest

The authors have no personal financial interest in any of the materials or devices described in this article.

Ethical standards

The study was approved by the ethics committee of the medical council of the state of Hamburg and has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Written consent was obtained by each patient or their legal representative prior to any ophthalmologic examination.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, University Medical Center Hamburg-Eppendorf, Martinistr. 52, 20246, Hamburg, Germany

    Patrick Czorlich, Manfred Westphal & Jan Regelsberger

  2. Department of Ophthalmology, University Medical Center Hamburg-Eppendorf, Martinistr. 52, 20246, Hamburg, Germany

    Christos Skevas, Volker Knospe, Gisbert Richard & Lars Wagenfeld

  3. Department of Medical Biometry and Epidemiology, University Medical Center Hamburg-Eppendorf, Martinistr. 52, 20246, Hamburg, Germany

    Eik Vettorazzi

Authors
  1. Patrick Czorlich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christos Skevas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Volker Knospe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eik Vettorazzi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gisbert Richard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lars Wagenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manfred Westphal
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jan Regelsberger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrick Czorlich.

Additional information

Comments

Konstantinos N. Fountas, Larisa, Greece

The presence of blood in the vitreous body of the orbit is known as Terson hemorrhage. This pathological condition was firstly described in 1881, by Moritz Litten, a German physician [1]. However, this clinico-pathological entity was described in detail and reported in the literature by Albert Terson in a monograph, in 1900 [2]. Since that initial report, numerous publications have outlined the various anatomical locations of intraocular hemorrhages, which may be preretinal, retinal, subretinal, hyaloidal, subhyaloidal, and/or intra-vitreous, and have clearly defined its strong association with a sudden increase of the intracranial pressure. Thus, Terson hemorrhages have been reported to be present in patients suffering spontaneous or traumatic subarachnoid hemorrhage, severe head injuries, or venous sinus thrombosis.

Although the causative relationship of Terson hemorrhage and aneurysmal subarachnoid hemorrhage (aSAH) has been reported in several recent clinical series, the actual occurrence of Terson hemorrhages among patients with aSAH remains still ill defined. Furthermore, the morbidity associated with Terson hemorrhages is generally underestimated in patients suffering aSAH. Moreover, the prognostic significance of Terson hemorrhage in patients with aSAH has not been adequately explored.

Czorlich et al. [3] in their current, well-designed, prospective study are examining systematically the actual incidence of Terson hemorrhage among patients suffering spontaneous SAH, and SAH of aneurysmal origin. The authors are exploring in their cohort the potential role of the severity and the extent of the initial subarachnoid hemorrhage and also the anatomic location of the ruptured aneurysm in the development of Terson hemorrhages. In addition, they study the prognostic role of Terson hemorrhages in the overall outcome of patients suffering aSAH.

But, Czorlich et al. [3] have not limited their study to SAH patients only. They examine the incidence of Terson hemorrhages in two other groups of neurosurgical patients with special interest: patients suffering from intracranial but subarachnoid hemorrhage and also patients with closed head injuries. They provide an initial approach in the occurrence of Terson hemorrhages in these two extremely common clinico-pathological entities, which definitely require further studying in the near future. Their work may well serve as a stimulus for additional clinical research in this field, and their current data could constitute the basis for better understanding of the underlying pathophysiologic mechanism in Terson hemorrhages.

References

1. Litten M. Ueber Einige vom Allgemein-Klinischen Standpunkt aus Interessante Augenveränderungen. Berl Klin Wochenschr 1881;18: 23–7

2. Terson A. De l’hémorrhagie dans le corps vitre au cours de l’hémorrhagie cerebrale. Clin Ophthalmol 1900;6: 309–12

3. Czorlich P., Skevas C., Knospe V., Vettorazzi E., Gisbert R., Wagenfeld L, et al. Terson syndrome in subarachnoid hemorrhage, intracerebral hemorrhage, and traumatic brain injury. Neurosurg Rev 2014;

Patrick Czorlich and Christos Skevas contributed equally.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Czorlich, P., Skevas, C., Knospe, V. et al. Terson syndrome in subarachnoid hemorrhage, intracerebral hemorrhage, and traumatic brain injury. Neurosurg Rev 38, 129–136 (2015). https://doi.org/10.1007/s10143-014-0564-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10143-014-0564-4

Keywords

Search

Navigation