Terson Syndrome 

Updated: Sep 20, 2018
Author: Richard J Ou, MD, FACS; Chief Editor: Hampton Roy, Sr, MD 

Overview

Background

In 1881, Litten first described an intraretinal hemorrhage associated with subarachnoid hemorrhage in the German literature.[1] However, Terson's description of vitreous hemorrhage following subarachnoid hemorrhage in 1900 is now associated with this syndrome. Terson syndrome has now been more broadly applied to intraocular hemorrhages associated with other causes of rapidly increased intracranial pressure beyond subarachnoid hemorrhages.[2, 3, 4, 5, 6, 7, 8, 9]

Problem

Terson syndrome originally was defined by the occurrence of vitreous hemorrhage in association with subarachnoid hemorrhage. Terson syndrome now encompasses any intraocular hemorrhage associated with intracranial hemorrhage and elevated intracranial pressures. Intraocular hemorrhage includes the development of subretinal, retinal, preretinal, subhyaloidal, or vitreal blood. The classic presentation is in the subhyaloidal space.[10]

Epidemiology

Consecutive case series have reported an incidence of 17-28% of intraocular hemorrhage with subarachnoid hemorrhage. This association is statistically associated with the severity of the subarachnoid hemorrhage based on the Hunt-Hess classification system of subarachnoid hemorrhages.[11, 12] The incidence of vitreous hemorrhage is much lower (3%-13%).[13, 14, 15, 16] Papilledema and unconsciousness are both positively correlated with Terson syndrome.[17]

Etiology

Terson syndrome has been described most commonly in subarachnoid hemorrhages due to ruptured cerebral aneurysms. Although early studies attempted to link this syndrome with aneurysms of the anterior communicating artery, statistical analysis has not correlated it with a specific aneurysmal location.[18] Other reports include such causes as strangulation, trauma, hypertension, tumor, and perioperative and postoperative intracranial bleeding.[4, 14] Iatrogenic events resulting in rapidly increased intracranial pressure have also been reported.[6, 7]

Right eye of a 28-year-old female with subarachnoi Right eye of a 28-year-old female with subarachnoid hemorrhage 1 week after intracranial surgery.
Left eye of a 28-year-old female with subarachnoid Left eye of a 28-year-old female with subarachnoid hemorrhage 1 week after intracranial surgery.

Pathophysiology

The pathogenesis of Terson syndrome has been controversial. The earliest reports assumed that the intracerebral blood directly connected with the intraocular space through the lamina cribrosa. While electron microscopy of the optic nerve anatomy has not demonstrated a communication between the 2 spaces, one case report has demonstrated bilateral optic nerve sheath hemorrhages following rupture of an anterior choroidal artery aneurysm resulting in a Terson syndrome.[19] Pathological specimens have not shown any blood in the optic nerve sheath within 3 mm of the globe.

A 2010 postmortem retrospective series demonstrated areas of multifocal optic nerve hemorrhages, suggesting that the blood in the nerve sheath may originate from the vessels directly supplying the nerve rather than from the main inciting intracerebral source of bleeding.[10]

Another mechanism suggests that a sudden rise in the venous pressure caused by the intracerebral bleeding is transmitted to the eye and results in intraocular bleeding. However, experimental studies have shown that the intravenous pressures are not high enough to create an intraocular hemorrhage.[20]

The sudden rise in intracranial pressure is probably the primary inciting event in Terson syndrome. Intracranial pressure is transmitted through the optic nerve sheath to the swollen optic nerve head, which occludes the retinal and choroidal anastomoses at the level of the lamina cribrosa. The elevated venous pressure generated in the retinal venous system is assumed to rupture the superficial retinal vessels, resulting in intraocular hemorrhages.[21] A case report supports this theory by demonstrating peripapillary fluorescein leakage in a patient with vitreous hemorrhage secondary to a subarachnoid hemorrhage.[21]

A case series of Terson syndrome patients was analyzed with scanning laser ophthalmoscopy, which revealed blood spreading along vessels. The data, combined with SD-OCT results and intraoperative observations of those Terson syndrome patients, suggest that blood may enter the vitreous cavity around the retinal vessels surrounding the optic disc.[22] Because of these assumptions regarding the pathogenesis of the syndrome, the definition of Terson syndrome now includes any intraocular hemorrhage associated with intracranial bleeding and acutely increased intracranial pressure. Attempts have been made to correlate Terson syndrome with the intraocular hemorrhages seen in shaken baby syndrome because of the similarity in clinical findings in the eye and the brain, but acute tractional forces may be an additional factor contributing to the intraocular hemorrhage in the latter.

Presentation

The neurologic symptoms are related to intracranial bleeding. Reported visual acuities range from 20/20 to light perception, but they often are difficult to obtain secondary to the impaired neurologic status of the patient.[23] The degree of visual loss is related to the degree and extent of the intraocular hemorrhage.

The intraocular hemorrhage is often bilateral and superficial to the retina. Intraretinal or subretinal hemorrhages have been reported but are less frequent. However, these may be more difficult to diagnose in the setting of vitreous or subhyaloidal hemorrhage. Preretinal hemorrhage can develop into vitreous hemorrhage weeks after the initial inciting event.[10, 24, 25] The intraocular hemorrhage may be difficult to diagnose immediately because the ophthalmologist may be restricted from dilating the patient for neurologic monitoring. A decreased red reflex can be helpful in evaluating a patient who is comatose, and B-scan ultrasonography can further establish the extent of vitreous hemorrhage in lieu of a dilated funduscopic examination.

Indications

Strict guidelines for treatment have not been established by clinical studies. Patients have responded well to observation.[24, 26]

Assuming patients are stable enough for surgery following intracranial hemorrhage, indications for a vitrectomy include the following:

  • Nonclearing vitreous hemorrhage in patient who is monocular or dense binocular vitreous hemorrhage [27]
  • Retinal detachment with vitreous hemorrhage [27]
  • Prevention of amblyopia in pediatric patients [28]
  • Late complications of intraocular hemorrhage, such as epiretinal membrane formation (macular pucker) [29]
  • Occupational or rehabilitation necessity for rapidly cleared vision [30]

Vitrectomy has been shown to be effective in quickly and safely restoring vision in Terson syndrome, even in cases delayed months after the intracranial hemorrhage.[31] Better outcomes in the setting of Terson syndrome are seen in younger patients and when vitrectomy is performed sooner after the intracranial event.[27, 32]

Relevant Anatomy

The relevant anatomy in Terson syndrome includes the inner retinal vasculature, choroidal vasculature, chorioretinal anastomoses near the optic nerve head, and subarachnoid space surrounding the optic nerve.

Contraindications

Contraindications for a vitrectomy include a small intraocular hemorrhage with a high likelihood of spontaneous clearing or an intraocular hemorrhage that is already spontaneously clearing. Patients with Terson syndrome are often poor surgical candidates because of the severity of the intracranial hemorrhage and often do not survive the devastating event.

Prognosis

Patients presenting with Terson syndrome have more severe subarachnoid hemorrhages based on the Glasgow Coma Scale or Hunt-Hess scale. Reported mortality rates increase from 3- to 12-fold in these patients compared to those with subarachnoid hemorrhages without Terson syndrome.[26, 25, 14, 15, 16]

 

Workup

Approach Considerations

The criterion standard for diagnosis is dilated funduscopic examination in the setting of intracranial hemorrhage or another cause of rapidly increased intracranial pressure. The intraocular hemorrhage should be easily visible to the trained examiner. Terson syndrome should be strongly suspected in cases of severe subarachnoid hemorrhage.

Laboratory Studies

Terson syndrome can be diagnosed by its unique clinical presentation of simultaneous intracranial and intraocular hemorrhage. A thorough history must be obtained to rule out causes of preexisting intraocular hemorrhages (eg, diabetic retinopathy, age-related macular degeneration, sickle cell disease, intraocular tumor). In cases associated with trauma, a posterior vitreous detachment, retinal break, or retinal detachment also must be ruled out. Typically, laboratory studies are not critical in making the diagnosis.

Sickle cell preparation may be considered.

Glucose and HbA1c testing may be performed to rule out diabetes, if applicable.

Imaging Studies

Neuroimaging studies, including CT scan, MRI, or angiography, are necessary to document intracranial hemorrhage.

B-scan ultrasound may be necessary to determine the severity of vitreous hemorrhage and to rule out a retinal detachment if no view to the retina is possible, particularly in the setting of trauma.

CT scans have been shown to be inferior to B-scan ultrasonography in identifying intraocular hemorrhage.[33, 34]

Visually evoked potentials has been reported to identify Terson syndrome in a patient who was unable to communicate prior to a full dilated examination.[30]

Other Tests

Examination of the cerebrospinal fluid should be deferred to a neurologist.

Diagnostic Procedures

Both a history and a clinical examination are indicated to help diagnose this condition.

Histologic Findings

Pathologic specimens of patients with Terson syndrome have shown abundant erythrocytes with occasional leukocytes in the vitreous, subhyaloidal and subinternal limiting membrane space, and retina. Clinical case reports have documented subretinal blood, but this is not as common. Epiretinal membranes examined in Terson syndrome show glial cells and basement membrane material.[10]

Staging

No staging currently exists.

 

Treatment

Medical Therapy

Spontaneously clearing vitreous hemorrhage or small intraocular hemorrhage is most common. Elevated head positioning with bed rest and avoidance of anticoagulation medications (eg, aspirin, nonsteroidal anti-inflammatory drugs [NSAIDs], warfarin) may be helpful. Resolution of symptoms may take months. One study demonstrated an average of 9 months for the clearance of such hemorrhages.

Surgical Therapy

In severe intracerebral hemorrhages, the condition is often fatal within days or weeks, thus precluding the opportunity for surgical intervention or even a complete dilated examination. In patients who survive the intracerebral bleed, a large vitreous hemorrhage that does not clear spontaneously may require a vitrectomy to facilitate clearing. In pediatric cases, the development of amblyopia is a consideration for early vitrectomy. A vitrectomy with possible epiretinal membrane peeling may be necessary for late complications (eg, macular pucker).

Preoperative Details

A complete dilated funduscopic examination is critical to evaluate the severity of the intraocular hemorrhage.

B-scan ultrasonography is useful for ruling out other pathology, including a retinal detachment that may not be visible in the setting of a vitreous hemorrhage.

Consult with a neurologist to approve of the patient's neurologic stability for surgery.

Intraoperative Details

Intervention with a vitrectomy is rarely needed in most patients who survive with Terson syndrome because of the spontaneous clearing of both the vitreous and the preretinal or subhyaloidal hemorrhage. Special consideration should be made for early intervention in those patients where amblyopia is concerned.

For long-standing vitreous hemorrhages of over 4- to 6-month duration without signs of progressive clearing, a core vitrectomy can be performed using the standard 3-port vitrectomy technique. In patients with loculated, nonclearing preretinal or subhyaloidal hemorrhage, the posterior hyaloid face can be incised and stripped away from the retinal surface with a bent microvitreoretinal (MVR) blade following a core vitrectomy.

The use of YAG laser photodisruption of the preretinal or posterior hyaloid membrane has been used for the treatment of subhyaloidal hemorrhages due to other mechanisms, but it is not recommended for patients with Terson syndrome because of the potential for the development of late-stage macular pucker or epiretinal membrane formation. This late complication of Terson syndrome is best addressed by posterior hyaloid membrane stripping using a bent MVR blade and excision of the peeled membrane with the vitrectomy instrument.

Postoperative Details

Avoid anticoagulation therapy.

Follow-up

Coordinate postoperative care with a neurologist.

Complications

The most common complication is the formation of epiretinal membranes, observed in 27-78% of patients with Terson syndrome. The subhyaloidal or subinternal limiting membrane space created by the intraocular hemorrhage may result in fibroblast or glial cell proliferation. The resulting macular pucker or epiretinal membrane formation may severely affect vision after the resolution of the hemorrhage and may become visually significant as late as 4 years after the resolution of the hemorrhage.

Other reported long-term complications include retinal pigment epithelium mottling, optic atrophy, macular holes, retinal folds, cystoid retinal changes, proliferative vitreoretinopathy, retinal detachment, and cataract formation.

Outcome and Prognosis

Terson syndrome has been correlated significantly in several studies with elevated morbidity and mortality when compared with subarachnoid hemorrhage without intraocular bleeding. Vitreous hemorrhage is associated with a 3- to 9-fold higher rate of mortality in comparison to other sites of intraocular bleeding in Terson syndrome.

Patients able to survive the neurologic complications usually have a favorable visual prognosis. In a study of 30 patients with Terson syndrome, over 83% of patients achieved a long-term visual acuity better than 20/50 following observation or a vitrectomy.[24] No statistical difference in final visual acuity was found between patients treated with observation or a vitrectomy.

The most common cause of persistent visual loss is epiretinal membrane formation as a late complication of Terson syndrome. A nonclearing vitreous hemorrhage in an infant may lead to amblyopia and warrants early vitrectomy.

Future and Controversies

Observation usually results in a favorable visual outcome for patients with Terson syndrome. Ophthalmic surgical intervention may be necessary to treat late complications (eg, macular epiretinal membranes). Immediate vitrectomy for intraocular hemorrhages is not recommended, except for patients with submacular hemorrhage, patients who are monocular with severe visual loss, or pediatric patients at risk for amblyopia.

The exact etiology of the mechanism of the intraocular blood remains to be elucidated definitively through histologic or experimental models.