RETINA

OPHTHALMIC PEARLS

Terson Syndrome:
Don’t Let It Go Unrecognized

T
erson syndrome (TS) is the
1A 1B
presence of any intraocular
hemorrhage, including vitreous,
subhyaloid, intraretinal, or subretinal
bleeding, in patients with intracranial
hemorrhage or traumatic brain injury.
The term originally referred only to
vitreous hemorrhage in the setting of a
subarachnoid hemorrhage (SAH), but
the definition has since been expanded.
Incidence. In part due to this change
in diagnostic criteria, estimates of the
incidence of TS vary. In a systematic re­ FUNDUS FINDINGS. Fundi of a 48-year-old woman who had an anterior communi-
view of SAH patients, McCarron et al. cating cerebral artery aneurysm, diffuse subarachnoid hemorrhage, and left inferior
reported a 13% incidence of TS among frontal ce­rebral hematoma. (1A) Right eye, showing intraretinal hemorrhages nasal
patients evaluated prospectively.1 Czor­ and superior to the disc. (1B) Left eye, showing a large area of preretinal hem-
lich et al. reported an incidence of 19% orrhage overlying the macula, subretinal hemorrhage along the superior arcade,
in patients with SAH, 9% in those with and intraretinal hemorrhage nasal to the disc. (Images, taken with a 20 D lens and
intracerebral hemorrhages, and 3% in iPhone 7 camera with flash, are inverted vertically and horizontally.)
patients with traumatic brain injury.2
The incidence of TS is significantly relatively high incidence of TS in pa­ al. reported an average of 5.2 months
higher in patients with greater impair­ tients with SAH, the syndrome remains between the time that a TS patient first
ment in consciousness (as indicated by underdiagnosed. One reason may be complained of ocular symptoms and
a low Glasgow Coma Scale) or more se­ that the patients who are most likely when an ophthalmology consultation
vere subarachnoid hemorrhage (based to have TS are also more likely to be occurred.5 This delay in diagnosis can
on either a high Hunt and Hess grade neurologically impaired and, therefore, lead to permanent visual impairment
or a high Fisher grade).2 TS is more limited in their ability to verbalize their and impede neurorehabilitation efforts.
likely to occur in patients who have had ocular complaints.2 In addition, given
prolonged episodes of unconsciousness the neurological acuity and severity of Pathophysiology
or elevated intracranial pressure3; and these patients’ conditions, an ocular The pathophysiology of TS is debat­
some, but not all, studies have observed examination may not be performed able, and multiple mechanisms have
a stronger association with anteriorly until other, more emergent, interven­ been proposed. The leading theory
located aneurysms.4 Although TS usually tions have been undertaken. suggests that an increase in intracra­
develops within hours of the neurolog­ Thus, referral of patients with TS nial pressure causes a rapid efflux of
ical event, it can occur days or weeks to ophthalmology is often delayed. cerebrospinal fluid or hemorrhage via
later.2 In a review of TS patients who later the optic nerve sheath into the orbit.
Delayed diagnoses. Despite the underwent vitrectomy, Gnanaraj et This, in turn, compresses the central
retinal vein, obstructing venous outflow
Bing Chiu, MD

and subsequently rupturing the smaller

EYENET MAGAZINE   •   35
acute elevation in intracranial pressure early as 1 week after onset.9 Thus, it is important for TS be recog­
can increase orbital venous pressure, Imaging. It can be challenging to nized early, not only for its prognostic
leading to backflow of blood through identify this pathology by funduscopy significance and impact on patients’
the retinal veins.7 A third theory sug­ if the view is obscured by vitreous hem­ neurorehabilitation efforts, but also
gests that the intraocular hemorrhages orrhage; in such cases, other modalities, because its complications may lead to
may be the result of direct extension such as B-scan ultrasonography, should permanent vision loss if left untreated.
of blood from the subarachnoid space be considered to aid in the diagnosis.
itself via the optic nerve sheath.8 In a study of patients with SAH, B-scan Key Points
Although the exact etiology remains ultrasonography was 100% sensitive • When medically stable, patients
unknown, an association with intra­ and specific for identifying vitreous with intracerebral and subarachnoid
cranial pressure has been supported by or preretinal hemorrhages and 44% hemorrhages should receive a prompt
Czorlich et al., who found that patients sensitive for identifying intraretinal funduscopic exam to evaluate for TS.
with TS were more likely to have had hemorrhages. Head CT scans, in con­ • B-scan ultrasonography or CT head
periods of elevated intracranial pres­ trast, were 60% sensitive for detecting scan can be used as to screen for TS.
sure greater than 25 mm Hg.3 preretinal hemorrhages and 32% sen­ • Early vitrectomy should be consid­
sitive for any intraocular hemorrhage.4 ered in patients with severe vision loss
Symptoms Thus, these modalities may be viable or bilateral hemorrhages and in young
The symptoms reported by TS patients screening options. children at risk for amblyopia.
can vary widely, depending on the de­ • The presence of TS is associated
gree and location of the hemorrhage as Management and Outcomes with a worse neurological prognosis
well as the individual’s neurological sta­ Ophthalmologic. The ophthalmic prog­ and higher risk of mortality.
tus. Many patients, especially those who nosis for TS patients is quite good.
are most neurologically compromised, Many intraocular hemorrhages resolve 1 McCarron MO et al. J Neurol Neurosurg Psychi-
may not be able to perceive or com­ spontaneously over several months. atry. 2004;75(3):491-493.
municate ocular complaints. In such For those that do not, vitrectomy has 2 Czorlich P et al. Neurosurg Rev. 2015;38(1):129-
cases, prompt diagnosis depends on the been successful in improving visual 136.
primary physician’s first being aware outcomes.5,10 3 Czorlich P et al. J Clin Neurosci. 2016;33:182-186.
of the possibility of Terson syndrome In a series of 25 TS eyes undergoing 4 Bauerle J et al. J Neuroimaging. 2016;26(2):247-
and then arranging for evaluation by an vitrectomy, 88% of eyes achieved 20/30 252.
ophthalmologist. Patients who are able vision or better.5 A study of 44 vitrecto­ 5 Gnanaraj L et al. Retina. 2000;20(4):374-377.
to describe their symptoms typically mized TS eyes found that patients who 6 Manschot WA. Am J Ophthalmol. 1954;38(4):
report an acute decrease in vision in 1 underwent early vitrectomy (within 90 501-505.
or both eyes in the setting of a recent days of vitreous hemorrhage) achieved 7 Weingeist TA et al. Ophthalmology. 1986;93(11):
severe headache or head trauma. better visual outcomes than those who 1435-1442.
were operated on after 3 months.11 8 Gress DR et al. J Neuroradiol. 2013;40(4):312-
Diagnosis Thus, many experts advocate for early 314.
Given the notable incidence of TS in vitrectomy, especially in cases of bi­ 9 Ko F, Knox DL. Ophthalmology. 2010;117(7):
patients with intracranial hemorrhage, lateral vitreous hemorrhages, dense 1423-1429.e1422.
SAH, or traumatic brain injury—espe­ unilateral hemorrhage, or hemorrhages 10 Schultz PN et al. Ophthalmology. 1991;98(12):
cially in patients with a loss of con­ in young children.5,7,9,10 1814-1819.
sciousness or low initial Glasgow Coma The other types of retinal pathology 11 Garweg JG, Koerner F. Acta Ophthalmol. 2009;
Scale—screening for TS is important associated with TS, including retinal 87(2):222-226.
once the patient is medically stable.2,3 detachment and macular holes, can also
Fundus examination. Funduscopy have profound effects on vision if not Dr. Rowlands and Dr. Chiu are residents in
is the gold standard for detecting and promptly recognized and treated.9 ophthalmology at NYU Langone Health, in New
diagnosing TS. Hemorrhages involving Neurological and systemic. In terms York. Dr. Schuman is professor and chairman of
multiple intraocular layers may be seen; of neurological and survival outcomes, ophthalmology, and professor of neuroscience
they can manifest as a “double ring” the prognosis for these patients is and physiology at NYU Langone Health, and
sign, in which blood is present below notably poor. In a systematic review of professor of electrical and computer engineering
the internal limiting membrane and outcomes in SAH, patients with TS had at NYU Tandon School of Engineering. Relevant
posterior hyaloid.9 Patients may also a risk of mortality almost 5 times higher financial disclosures: None.
have a loss of the red reflex. than that of patients with SAH alone For full disclosures, view this article at aao.org/
TS has been linked with develop­ (50% vs. 11%, respectively, among pa­ eyenet.
ment of macular holes, epiretinal tients studied prospectively).1 Further­
membranes, retinal folds, proliferative more, TS patients who do survive have MORE ONLINE. See this article
vitreoretinopathy, retinal detachment, significantly lower Glasgow scales at 3 at aao.org/eyenet for brain
and optic nerve sheath hemorrhage as months than SAH patients without TS.2 imaging of the patient in Fig. 1.

36  •   N O V E M B E R 2018