Terson Syndrome

Key Points at a Glance

Key Points of This Disease

• Terson syndrome is a general term for intraocular hemorrhage that occurs in association with subarachnoid hemorrhage (SAH).
• It occurs in 3–20% of SAH patients, with aneurysm rupture accounting for 80% of cases.
• Vitreous hemorrhage is the main feature, and sub-internal limiting membrane (sub-ILM) hemorrhage is a characteristic finding.
• Onset typically occurs 2–3 days after SAH, and diagnosis may be delayed by about 5 months.
• Spontaneous resolution of vitreous hemorrhage takes 19 months or more in about half of cases.
• Vitrectomy (PPV) performed within 90 days of onset can achieve good visual recovery (81% achieve 20/30 or better).
• The presence of Terson syndrome may be a poor prognostic indicator associated with increased mortality in SAH patients.

1. What is Terson syndrome?

Terson syndrome is a general term for intraocular hemorrhage secondary to intracranial hemorrhage, including subarachnoid hemorrhage (SAH). It was first named and described in 1900 by French ophthalmologist Albert Terson. ⁶⁾

The incidence is reported to be 3–20% of SAH patients, with a large difference depending on the reporting method: 13% in prospective studies and 3% in retrospective studies. ¹⁾ About 80% of SAH cases are due to ruptured cerebral aneurysms, and Terson syndrome also occurs in the majority of these cases. Intraocular hemorrhage is often observed 2–3 days after the onset of SAH.

Definition

Terson syndrome: A general term for intraocular hemorrhage that occurs in association with intracranial hemorrhage (mainly SAH). Includes vitreous hemorrhage, subinternal limiting membrane hemorrhage, and retinal hemorrhage.

Incidence

SAH complication rate: 3–20%. Varies by report for intracranial hemorrhage in general.

Timing of onset

2–3 days after SAH: It often takes several days for hemorrhage to spread into the eye. Diagnosis delay averages 5 months according to some reports.

Common background

Aneurysmal SAH: 80% of SAH is due to aneurysm rupture. Terson syndrome also mainly occurs in this context.

Q Can Terson syndrome occur in conditions other than subarachnoid hemorrhage?

A

Intraocular hemorrhage can also occur in various conditions that cause a rapid increase in intracranial pressure, such as intracerebral hemorrhage or traumatic head injury. However, the most frequent and classically described association is with SAH.

2. Main symptoms and clinical findings

Subjective symptoms

• Decreased visual acuity: Vitreous hemorrhage or macular hemorrhage impairs central vision. The severity ranges from mild blurring to severe vision loss.
• Floaters: Blood in the vitreous is perceived as floating objects.
• Visual field defects: Occur depending on the extent and location of the hemorrhage.

Immediately after the onset of severe SAH, impaired consciousness often precedes eye symptoms, so patients may report eye symptoms late. This often leads to a delay in diagnosis.

Clinical findings

Vitreous hemorrhage is the central pathology of Terson syndrome, but bleeding can involve multiple layers.

Type of hemorrhage	Characteristics	Location
Vitreous hemorrhage	Most common. Takes a long time to resolve.	Vitreous cavity
Sub-internal limiting membrane hemorrhage	Double ring sign. ERM formation after absorption	Sub-internal limiting membrane
Retinal hemorrhage	Appears as flame-shaped or dot hemorrhages	Intraretinal

Double ring sign is a characteristic fundus finding of sub-internal limiting membrane (ILM) hemorrhage. Blood accumulates under the ILM, and the dome-shaped elevated hemorrhage is observed as a double ring contour.

The following long-term complications have been reported:

• Epiretinal membrane (ERM): Forms in 15–78% of cases. An important sequela affecting visual prognosis.
• Retinal detachment (RD): Occurs in approximately 9% of cases.

Q What is the double ring sign?

A

It is a fundus finding in which blood accumulates under the internal limiting membrane, and the dome-shaped elevated hemorrhage appears as a double ring due to the outer and inner edges of the ILM. It is considered characteristic of sub-ILM hemorrhage in Terson syndrome.

3. Causes and Risk Factors

The underlying cause of Terson syndrome is the spread of hemorrhage into the eye due to a sudden increase in intracranial pressure.

Approximately 80% of SAH cases are caused by rupture of a cerebral aneurysm, with the remainder due to arteriovenous malformations or SAH of unknown cause.

Association with severity is an important clinical feature. SAH patients with Terson syndrome have significantly higher mortality compared to those without, with a systematic review reporting 43% vs 9% (odds ratio 4.8)¹⁾, another report 28.6% vs 2.0%²⁾, and a study linking ICP reporting an odds ratio of 45.0³⁾. Lower Glasgow Coma Scale (GCS) scores and higher Hunt and Hess and Fisher grades are associated with a higher likelihood of Terson syndrome^2,3).

Collaboration with Neurology and Neurosurgery

In SAH patients, ophthalmologic consultation is often delayed due to impaired consciousness. Collaboration with neurosurgery and neurology is important to perform systematic fundus examinations after recovery of consciousness. To prevent diagnostic delay, it is desirable to incorporate ophthalmologic follow-up into the plan from the time of SAH diagnosis.

4. Diagnosis and Examination Methods

The diagnosis of Terson syndrome is based on fundus findings. However, in severe SAH patients, initial fundus examination is often difficult due to impaired consciousness, and there are reports of an average delay of 5 months until diagnosis.

Main Examination Methods

• Fundus examination: Basic assessment includes confirmation of vitreous hemorrhage, sub-internal limiting membrane hemorrhage, and the double-ring sign. Detailed observation under mydriasis is required.
• B-mode ultrasonography: Useful when vitreous hemorrhage is severe and fundus observation is difficult. It can also confirm the presence of retinal detachment.
• CT scan: May show intraocular high-density areas (hemorrhage). However, sensitivity is low, and intraocular hemorrhage is recognized on CT in only about two-thirds of all cases.

Diagnostic Pitfalls

CT has low sensitivity for detecting Terson syndrome. If an SAH patient has visual abnormalities or floaters, a detailed ophthalmologic examination is necessary even if CT does not show intraocular hemorrhage.

Q When is the appropriate timing for ophthalmologic consultation during SAH treatment?

A

Fundus examination should be performed as soon as the patient becomes alert. In severe cases, fundus confirmation should be actively performed once treatment has stabilized. Delayed confirmation of fundus hemorrhage may lead to missing the optimal timing for vitrectomy. For details, see the section on Standard Treatment.

5. Standard Treatment

The treatment strategy for Terson syndrome is determined by the extent and location of hemorrhage, impact on vision, and the patient’s general condition.

Observation

Indications: Mild vitreous hemorrhage or retinal hemorrhage with minimal visual impairment.

Natural course: In about 50% of cases, vitreous hemorrhage resolution takes more than 19 months. Long-term follow-up is required.

Vitrectomy (PPV)

Indications: Visual impairment due to severe vitreous hemorrhage, complications such as ERM or RD, or when spontaneous resolution is unlikely.

Timing: Surgery within 90 days of onset is associated with better visual prognosis. In multiple case series, visual improvement was seen in 21/22 eyes postoperatively, and 16 of 20 eyes with preoperative vision ≤0.1 achieved postoperative vision ≥0.5. ⁴⁾ A multicenter study also showed significant improvement from logMAR 1.57 to 0.53. ⁵⁾

Other Options

YAG laser: YAG laser vitreolysis for blood clots on the posterior vitreous. Outpatient laser irradiation promotes dispersion of hemorrhage into the vitreous cavity.

Additional treatment based on course: If ERM formation or retinal detachment occurs, surgical treatment should be considered.

Outcomes of Vitrectomy (PPV)

The relationship between timing of PPV and postoperative visual acuity is shown below.

Timing of Surgery	Rate of Achieving Postoperative VA ≥20/30	Notes
Within 90 days	81%	Early surgery group
>90 days	Tendency to decrease	Late surgery group
Internal limiting membrane peeling	Effective for ERM prevention	Surgical options

Importance of surgical timing

Vitrectomy performed within 90 days of onset has been reported to have better visual prognosis. While prioritizing systemic management during the acute phase of SAH, multidisciplinary collaboration is important to avoid missing the window for ophthalmic intervention.

6. Pathophysiology and detailed mechanisms

Several hypotheses have been proposed regarding the mechanism of Terson syndrome. All share the common starting point of a sudden increase in intracranial pressure. In fact, ICP monitoring studies have shown that all cases with Terson syndrome had ICP > 20 cmH₂O (median 40 vs 15 cmH₂O), supporting that elevated intracranial pressure is central to the pathology. ^3,6)

Four main hypotheses

• Venous compression hypothesis: Increased intracranial pressure raises central venous pressure, leading to increased pressure in the central retinal vein and causing intraocular hemorrhage.
• Direct inflow hypothesis: Blood from SAH flows directly into the eye along the optic nerve sheath. There is an anatomical route for hemorrhage within the optic nerve sheath to penetrate into the eye.
• Virchow-Robin space hypothesis: Blood reaches the retina or vitreous via the perivascular spaces (Virchow-Robin spaces).
• Integrated hypothesis: Hemorrhage occurs through a combination of the above mechanisms.

Relationship with the Glymphatic System

In recent years, the relationship with the brain’s glymphatic system has attracted attention. The glymphatic system is a network of channels involved in waste removal in the brain, connecting to the optic nerve sheath and the Virchow-Robin spaces. Research suggests that acute pressure changes in the glymphatic pathway due to SAH may contribute to the spread of blood into the eye.

7. Latest Research and Future Perspectives (Research Stage Reports)

For Patients: Please Read Carefully

The following content is currently at the research stage or under clinical trial and is not standard treatment available at general hospitals. It is reference information for professionals regarding future medical developments.

Glymphatic System Research

Research is progressing on the pathway of blood migration from the intracranial space to the eye via the glymphatic system. If this pathway is confirmed, it may lead to the prevention of Terson syndrome and the development of early diagnostic markers.

Optimization of PPV Timing

Based on the finding that PPV performed within 90 days of onset leads to better visual outcomes, studies are ongoing to establish more precise criteria for surgical timing. The challenge is to establish a protocol for early surgical intervention within the limits allowed by the patient’s general condition.

Significance of Internal Limiting Membrane Peeling

It has been reported that simultaneous peeling of the internal limiting membrane (ILM peeling) during PPV may prevent postoperative ERM formation. Whether ILM peeling should be standardized in Terson syndrome, where the incidence of ERM is as high as 15–78%, is still under investigation.

Q Does Terson syndrome resolve on its own?

A

In about half of cases, vitreous hemorrhage does not resolve for 19 months or longer. Even when long-term observation is chosen in expectation of spontaneous resolution, attention must be paid to complications such as epiretinal membrane and retinal detachment. If visual acuity is significantly affected, vitrectomy should be considered. For details, see the section on Standard Treatments.

Q Can vision recover in Terson syndrome?

A

When vitrectomy is performed early, it has been reported that 81% of patients recover visual acuity of 20/30 or better. However, prognosis differs if epiretinal membrane or retinal detachment is present. Surgery within 90 days of onset is associated with a good prognosis.

References

1. McCarron MO, Alberts MJ, McCarron P. A systematic review of Terson’s syndrome: frequency and prognosis after subarachnoid haemorrhage. J Neurol Neurosurg Psychiatry. 2004;75(3):491-493. PMID: 14966173. ¹⁾
2. Fountas KN, Kapsalaki EZ, Lee GP, et al. Terson hemorrhage in patients suffering aneurysmal subarachnoid hemorrhage: predisposing factors and prognostic significance. J Neurosurg. 2008;109(3):439-444. PMID: 18759574. ²⁾
3. Joswig H, Epprecht L, Valmaggia C, et al. Terson syndrome in aneurysmal subarachnoid hemorrhage—its relation to intracranial pressure, admission factors, and clinical outcome. Acta Neurochir (Wien). 2016;158(6):1027-1036. PMID: 27038169. ³⁾
4. Ritland JS, Syrdalen P, Eide N, Vatne HO, Øvergaard R. Outcome of vitrectomy in patients with Terson syndrome. Acta Ophthalmol Scand. 2002;80(2):172-175. PMID: 11952484. ⁴⁾
5. Nazarali S, Kherani I, Hurley B, et al. Outcomes of vitrectomy in Terson syndrome: a multicenter Canadian perspective. Retina. 2020;40(7):1325-1330. PMID: 31145391. ⁵⁾
6. Aboulhosn R, Raju B, Jumah F, et al. Terson’s syndrome, the current concepts and management strategies: a review of literature. Clin Neurol Neurosurg. 2021;210:107008. PMID: 34775364. ⁶⁾