Intraocular hemorrhage in the setting of a subarachnoid hemorrhage was first described by Litten in 1881.1 In 1900, Terson subsequently described vitreous hemorrhage associated with subarachnoid hemorrhage.2 Terson syndrome is now more broadly defined as the syndrome of vitreous hemorrhage and/or retinal hemorrhage occurring in the setting of intracranial hemorrhage.3,4 Intraocular hemorrhage occurs in 17% of adults with subarachnoid hemorrhage from ruptured cerebral aneurysms.5 However, intraocular hemorrhage occurs in less than 8% of pediatric cases of intracranial hemorrhage not resulting from abusive head trauma.6 By definition, Terson syndrome occurs in the setting of an intracranial hemorrhage; however, other inciting events including meningoencephalitis and intrathecal anesthesia during a retrobulbar block may cause a Terson-like syndrome with hemorrhagic retinopathy without frank intracranial hemorrhage.7,8 To the best of our knowledge, herein we report the first described case of a unilateral Terson-like syndrome occurring in the setting of a perinatal stroke.
A 2-month-old male was referred for abnormal red reflex and left esotropia from nonclearing vitreous hemorrhage in his left eye first observed at 2 weeks of life. He was delivered at 37 weeks via emergent Caesarean section and briefly required chest compressions for neonatal cardiac arrest and positive pressure ventilation for meconium aspiration, respiratory distress, and hypoxia. He suffered a neonatal stroke secondary to congenital supraclinoid occlusion of the left internal carotid artery (ICA) with occlusion of the left middle cerebral artery (Figure 1). Magnetic resonance (MR) imaging (MRI)/MR angiography also revealed hypoplastic left vertebral artery, right-sided inferior frontal lobe, and parietal lobe infarcts, and left hemispheric cortical vein thrombosis, indicating cerebral venous stasis. Both MRI and computed tomography angiography excluded intracranial hemorrhage. A septic work up including blood and cerebrospinal fluid (CSF) cultures was negative despite the presence of bloody CSF. Thrombophilia testing was negative at 1 week and 6 months after the stroke event. Other developmental anomalies included a two-vessel cord, left renal agenesis, and fetal lung immaturity despite 37 weeks gestational age. Atelectasis from meconium aspiration and pulmonary hypertension were observed during the first week of life.
(A) T2-weighted turbo spin-echo magnetic resonance image (MRI) of the brain from the fifth day of life showing left hemispheric cerebral edema with midline shift. There was Wallerian degeneration of the left cerebral peduncle and pons consistent with prior increased intracranial pressure with herniation. The patient had supraclinoid occlusion of the left internal carotid artery (ICA) extending from the ophthalmic segment to the carotid terminus with occlusion of the left middle cerebral artery and high-grade stenosis of the left cervical ICA. (B) Magnetic resonance angiography reconstruction demonstrating severe reduction in flow in the left internal carotid artery (black arrows) and absent flow in the left middle cerebral artery (white arrowhead). The left vertebral artery was also hypoplastic (black arrowheads) (C) Susceptibility weighted imaging MRI demonstrating multifocal areas of low intensity signal in the left globe consistent with intraocular hemorrhage (white arrows). Asymmetric left-sided cavernous sinus hypointensity favors ipsilateral venous stasis or thrombosis (gray arrow). The lack of subarachnoid, subdural, or cortical hemorrhage was also confirmed by computed tomography angiography.
On ophthalmic examination, vision was central, steady, and maintained in the right eye and blink to light in the left eye. He had a normal anterior exam bilaterally and a normal right fundus. Dense vitreous hemorrhage (Figure 2) obscured view of the fundus in the left eye. B-scan ultrasonography confirmed dense vitreous hemorrhage emanating from submacular hemorrhage. Due to concern for deprivation amblyopia, the patient underwent lens-sparing vitrectomy (Figure 3). Intraoperatively, multifocal subretinal hemorrhages were noted along vortex veins and in the macula. Posoperatively, the lens remained clear and the retina remained attached in the left eye. Visual acuity improved to central, steady, unmaintained in the left eye despite sequela of resolved submacular hemorrhage.
(A) Preoperative color fundus photograph of the left eye demonstrating dense vitreous hemorrhage with obscuration of the posterior pole. (B) Preoperative B-scan ultrasonography axial image of the left eye demonstrating dense vitreous hemorrhage emanating from submacular hemorrhage with partial vitreous separation.
Color fundus photography stills from surgical video. (A) After incomplete 25-gauge vitrectomy, the left fundus is partially obscured by dense, chronic vitreous hemorrhage. The split hyaloid face was mechanically elevated, and there was no sub-internal limiting membrane hematoma. (B) Dehemoglobinized submacular and parapapillary subretinal hematomas are observed against a blonde fundus. (C) Scleral depression demonstrates a chronic subretinal hematoma along a superior vortex vein.
According to the Monro-Kellie hypothesis, the sum of the volumes of the brain, CSF, and intracranial blood are constant within the rigid cranium.9 In this pressure-volume equilibrium, an equal volume of CSF or venous blood must be expelled from the cranium with each arterial pulse. In pathologic states of acutely increased intracranial pressure (ICP), blood from the venous sinuses and CSF are initially displaced out of the cranium, but eventually cerebral perfusion pressure declines, ischemia ensues, and brain herniation may occur if ICP is not relieved and cerebral compliance fails. Although the exact mechanism leading to Terson syndrome has been debated in the literature, it is hypothesized that intracranial hemorrhage causes an acute rise in ICP, which is transmitted through the optic nerve, causing optic vein compression, venous stasis, and overwhelms physiologic compliance mechanisms creating multi-laminar hemorrhagic retinopathy.10
In this case, a similar mechanism can be postulated without frank intracranial hemorrhage, whereas lumbar puncture demonstrated bloody CSF. Associated with perinatal stroke, hypoxia, and hypercarbia, the cerebral hemispheric vasogenic edema resulted in an acute rise in ICP, whereas cerebral autoregulation drove compensatory increased arterial pressures to the congenitally underserved left hemicortex through the Circle of Willis and vertebrobasilar system. Compliance was exceeded and uncal herniation occurred, further limiting CSF outflow into the distensible lumbar subarachnoid space. Cortical venous thrombosis indicated coagulopathy, increased venous pressures, and venous stasis, further exacerbating limited outflow and impairing the Windkessel mechanism smoothing blood flow to the cerebral vascular bed.11 Pulmonary hypertension and elevated right-sided ventricular pressures could raise jugular venous pressures, and in the setting of coagulopathy and patent foramen ovale, lead to arterial and venous thrombi and emboli to explain the right-sided cerebral infarcts. In an attempt to maintain cerebral perfusion, the pulsatile arterial pressures against limited CSF and venous outflow in unilateral hemispheric cerebral edema could deliver ipsilateral venous pressure spikes from the impaired Windkessel mechanism and create the Terson-like hemorrhages emanating from the choroidal and retinal circulations and the associated vitreous hemorrhage. It is unclear whether the limited chest compressions, positive pressure ventilation, or coughing contributed to venous pressure spikes and ocular hemorrhages, although no retinopathy was observed in the right eye.
The reason for the difference in rates of vitreous and/or retinal hemorrhage in the setting of intracranial hemorrhage between pediatric studies and adult studies is not clear. Schloff et al.6 theorize a number of factors could be at play including differing rates of arteriovenous malformations and subarachnoid hemorrhage. They also hypothesize that pediatric patients may have better vasculature autoregulation and differing hormonal influences. In their series of fifty-seven pediatric patients with intracranial hemorrhage from nonabusive causes, only one patient demonstrated intraretinal hemorrhages on examination. In the infant age population Terson syndrome is especially rare with the literature demonstrating primarily single case reports associated with delivery-associated trauma or ruptured cerebral aneruysm.12,13 In the adult population, Terson syndrome is commonly caused by ruptured intracranial aneurysm resulting in subarachnoid hemorrhage and visual prognosis is good with or without vitrectomy.10 Candidates for early vitrectomy include adults with dense vitreous hemorrhage unlikely to resolve or bilateral vitreous hemorrhages with visual impairment.
In the pediatric population, patients at risk for deprivation amblyopia are candidates for early vitrectomy.10 Surgery for pediatric patients with Terson syndrome has also been reported to result in rapid visual improvement and to help prevent amblyopia.14 In our patient, lens-sparing vitrectomy relieved the amblyogenic media opacity, but vision was still limited by macular damage from the subretinal hemorrhage and homonymous hemianopia from the cortical insult.
- Litten M. Ueber einige vom allgemein-klinischen Standpunkt aus interessante Auqenverenderunqen. Berl Klin Wochnschr. 1881;(18):23–27.
- Terson A. De l'hemorrhaqie dans Ie corps vltre au cours de l'hernorrhagie cerebrale. Clin Ophthalmol. 1900;(6):309–312.
- Ko F, Knox DL. The ocular pathology of Terson's syndrome. Ophthalmology. 2010;117(7):1423–9.e2. doi:10.1016/j.ophtha.2009.11.028 [CrossRef] PMID:20347154
- 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;114(6):535–538. doi:10.1016/j.clineuro.2011.10.034 [CrossRef] PMID:22472353
- 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;105(3):472–477. doi:10.1016/S0161-6420(98)93030-5 [CrossRef] PMID:9499778
- Schloff S, Mullaney PB, Armstrong DC, et al. Retinal findings in children with intracranial hemorrhage. Ophthalmology. 2002;109(8):1472–1476. doi:10.1016/S0161-6420(02)01086-2 [CrossRef] PMID:12153798
- Asahi MG, Weiss SJ, Peddada K, Malik D. A Case of Terson-Like Syndrome in a Patient with Viral Meningoencephalitis. Case Rep Ophthalmol Med. 2019;2019:9650675. doi:10.1155/2019/9650675 [CrossRef] PMID:31179143
- Goldberg RA, Waheed NK. Intrathecal anesthesia after retrobulbar block, with Terson-like syndrome. JAMA Ophthalmol. 2014;132(11):1295. doi:10.1001/jamaophthalmol.2014.168 [CrossRef] PMID:25233053
- Kim D-J, Czosnyka Z, Kasprowicz M, et al. Continuous monitoring of the Monro-Kellie doctrine: is it possible?J Neurotrauma. 2012;29(7):1354–1363. doi:10.1089/neu.2011.2018 [CrossRef] PMID:
- Schultz PN, Sobol WM, Weingeist TA. Long-term visual outcome in Terson syndrome. Ophthalmology. 1991;98(12):1814–1819. doi:10.1016/S0161-6420(91)32045-1 [CrossRef] PMID:1775315
- Beggs CB. Cerebral venous outflow and cerebrospinal fluid dynamics. Veins and Lymphatics. 2014;3(3):1867. doi:10.4081/vl.2014.1867 [CrossRef]
- Moshfeghi DM. Terson syndrome in a healthy term infant: delivery-associated retinopathy and intracranial hemorrhage. Ophthalmic Surg Lasers Imaging Retina. 2018;49(10):e154–e156. doi:10.3928/23258160-20181002-20 [CrossRef] PMID:30395678
- Mena OJ, Paul I, Reichard RR. Ocular findings in raised intracranial pressure: a case of Terson syndrome in a 7-month-old infant. Am J Forensic Med Pathol. 2011;32(1):55–57. doi:10.1097/PAF.0b013e3181edee5b [CrossRef] PMID:
- Sayman Muslubas I, Karacorlu M, Hocaoglu M, Ersoz MG, Arf S. Anatomical and functional outcomes following vitrectomy for dense vitreous hemorrhage related to Terson syndrome in children. Graefes Arch Clin Exp Ophthalmol. 2018;256(3):503–510. doi:10.1007/s00417-017-3887-3 [CrossRef] PMID: