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CT confirming the diagnosis of Terson syndrome by the presence of bilateral hyperdense nodules (arrows) on the temporal retinal surface in a patient with aneurysmal subarachnoid hemorrhage
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Background:
A large number of reports have not been able to clarify the pathophysiology of Terson syndrome (TS) in aneurysmal subarachnoid hemorrhage (aSAH).
Methods:
Prospective single-center study on aSAH patients. Fundoscopic and radiological signs of TS were assessed. The opening intracranial pressure (ICP) in patients who required a ventric...
Similar publications
Background The purpose of this study was to survey the anatomical angiographic finding of the aneurysm and identify parameters associated with visual recovery of the patients with Terson syndrome (TS). Methods This retrospective study was conducted on 494 patients with aneurysmal subarachnoid hemorrhage (SAH) from 2008 to 2015. Radiologists indepen...
Citations
... Terson syndrome in the setting of aneurysmal SAH has been seen in adults with more severe Hunt and Hess and modified Fisher grades, and is believed to lead to increased morbidity and mortality within this patient population. 19,20 A systematic review of both prospective and retrospective studies in adults with TS showed that patients with aneurysmal SAH with associated intraocular hemorrhage have worse outcomes, 19 underscoring the severity of disease in these patients and perhaps suggesting underlying links in pathophysiology. In a study of 102 patients with SAH, 20 of whom developed TS, 55% of patients with TS had Hunt and Hess IV and V, as compared to 13% in those without TS. ...
Background:
Terson syndrome is the phenomenon of intraocular hemorrhage in the setting of subarachnoid hemorrhage (SAH). Vision loss can lead to morbidity for the affected individual. Aneurysmal SAH related to intracranial aneurysms is rare in children. Studies have shown the incidence of Terson syndrome in adults with aneurysmal SAH to be over 40%; however, few cases of Terson syndrome in pediatric aneurysmal SAH have been reported.
Observations:
A 9-year-old male presented with altered mental status and seizures. Computed tomographic angiography showed aneurysmal SAH from a ruptured, left-sided posterior inferior cerebellar artery aneurysm. The patient underwent endovascular treatment with coiling and external ventricular drainage for SAH. Ophthalmological consultation for blurry vision revealed the diagnosis of Terson syndrome with decreased vision in the left eye, which was managed conservatively.
Lessons:
Terson syndrome after SAH can occur in children. Prompt ophthalmological evaluation in pediatric patients with aneurysmal SAH is vital for recognition and management to decrease overall morbidity.
... Several factors have been described in the literature to be associated with the occurrence of TS, such as high Hunt and Hess and WFNS grades, low Glasgow Coma Scale scores and high Fisher scale scores [3,[21][22][23][24][25]. An initial loss of consciousness and an initially raised intracranial pressure (ICP) have also been investigated as predictors for TS [10,26]. In the work of Joswig et al. [26], all These results partially align with this study's results, as we were also able to show the association of a high WFNS grade with the occurrence of TS in our collective. ...
... An initial loss of consciousness and an initially raised intracranial pressure (ICP) have also been investigated as predictors for TS [10,26]. In the work of Joswig et al. [26], all These results partially align with this study's results, as we were also able to show the association of a high WFNS grade with the occurrence of TS in our collective. We were also able to demonstrate an association between seizures and the occurrence of TS. ...
Background
Terson syndrome (TS), an intraocular hemorrhage associated with aneurysmal subarachnoid hemorrhage (aSAH), occurs in up to 46% of all patients with subarachnoid hemorrhage. Despite its high incidence, TS is underrepresented in the literature, and patients with aSAH are sometimes not systematically evaluated for the presence of TS in clinical practice. This work aims to raise awareness of TS, reevaluate previous scientific findings, describe risk factors associated with the occurrence of TS, and present our local diagnostic and treatment concept.
Methods
All patients with aSAH treated at our institution between October 2010 and May 2020 were included in this retrospective study. The frequency of ophthalmological screening by indirect funduscopy, as well as the results, was investigated. In addition, the collection and statistical analysis of epidemiological and clinical data was performed using χ ² , Kruskal–Wallis, and analysis of variance testing; multivariate regression; and receiver operating characteristic analysis. The significance level was set at p < 0.05.
Results
A total of 617 patients were treated for aSAH in our institution. Of these, 367 patients (59.5%) were ophthalmologically examined for the presence of TS. The rate of TS in the examined patients was 21.3% ( n = 78). Patients with TS had significantly higher Fisher and World Federation of Neurosurgical Societies (WFNS) scores ( p < 0.0001). Regression analyses showed WFNS grade ( p = 0.003) and the occurrence of seizures ( p = 0.002) as independent predictors of TS, as did receiver operating characteristic analyses, which had a significant area under the curve of 0.66 for the combination of WFNS grade and seizures. For 12 (15.4%) patients, the TS had to be surgically treated by pars plana vitrectomy in a total of 14 eyes, which resulted in significant improvement of visual function in all patients: mean preoperative best-corrected visual acuity was 0.03 (± 0.08) versus 0.76 (± 0.21) postoperatively ( p < 0.001).
Conclusions
TS is a common complication in patients with aSAH, affecting approximately one in five patients. A higher WFNS grade and the occurrence of seizures are associated with TS; therefore, screening for TS should be performed in these patients.
... It has been reported that the higher the intracranial pressure, the higher the risk of developing TS. [3,4] The source of retinal hemorrhages and their connection to the SAH in TS has been deliberated extensively and is still contentious. ...
... [20] It has been reported that the higher the intracranial pressure, the higher the risk of developing TS. [3,4] For transfer of the CSF and SAH from the cranial cavity into the subarachnoid space of the optic nerve sheath, the extent of patency of the optic canal [ Fig. 4b], plays a critical dynamic role. Rarely, the optic canal may be completely closed, so that CSF and hemorrhages cannot infiltrate into the optic nerve sheath no development of TS. ...
Purpose:
The aim of this experimental study was to investigate the pathogenesis of Terson syndrome (TS), which currently is controversial.
Methods:
The central retinal artery (in 39 orbits), posterior ciliary arteries (in 8 orbits), and central retinal vein (CRV in 21 orbits) were occluded in rhesus monkeys by exposing them to lateral orbitotomy. Fundus examination and fluorescein fundus angiography were performed before and immediately after cutting the vessels and serially thereafter during the follow-up period. The rationale of the experimental study design is discussed.
Results:
In eyes with central retinal artery occlusion, retinal hemorrhages were seen soon after the procedure in 7 eyes, and on follow-up in a total of 15 eyes. In posterior ciliary artery occlusion, retinal hemorrhages were seen soon after the procedure in one eye, and on follow-up in a total of three eyes. In eyes with CRV, all eyes had extensive scattered retinal hemorrhages.
Conclusion:
The findings of this experimental study, and my basic, experimental, and comprehensive clinical studies on CRVO, suggest the following concept of the pathogenesis of TS: Compression of the CRV plays a crucial role in the development of TS. The CRV is compressed, as it lies in the subarachnoid space of the optic nerve sheath, by raised cerebrospinal fluid pressure and/or accumulated blood.
. this results in retinal:
venous stasis and raised venous pressure in the retinal veins, leading to venous engorgement, rupture of the retinal capillaries.
And:
retinal hemorrhages. The clinical importance of compression of the CRV and not occlusion of CRV in TS is that optic nerve sheath decompression by opening it and releasing the blood and raised cerebrospinal fluid (CSF) pressure, would result in immediate decompressing of the CRV in the subarachnoid space and restoration of normal circulation and prevent visual loss.
... The risk of developing TS correlates with increasing clinical and radiological severity of aneurysmal SAH, being associated with a low Glasgow Coma Scale, high Hunt and Hess grade, and high Fisher grade [5,12]. The higher the ICP, the higher the risk of developing TS [3,13]. Given that patients most at risk of TS are least likely to communicate visual symptoms due to their neurological morbidity, the incidence of TS is probably higher than reported [14]. ...
... Two studies reported TS being more common in anterior circulation aneurysm rupture as opposed to posterior lesions [4,12]. Anterior communicating artery aneurysms were particularly linked with TS in three reports [13,25,38]. Other studies have shown no association between aneurysm location and TS rate [5]. ...
Terson Syndrome (TS) describes the presence of intraocular hemorrhage in patients with intracranial hemorrhage, typically subarachnoid hemorrhage. Despite TS being a well-defined and frequently occurring phenomenon, its pathophysiology remains controversial. This review will present the current understanding of TS, with view to describing a contemporary and more plausible pathomechanism of TS, given recent advances in ophthalmic science and neurobiology. Previously proposed theories include a sudden rise in intracranial pressure (ICP) transmitted to the optic nerve sheath leading to rupture of retinal vessels; or intracranial blood extending to the orbit via the optic nerve sheath. The origin of blood in TS is uncertain, but retinal vessels appear to be an unlikely source. In addition, an anatomical pathway for blood to enter the eye from the intracranial space remains poorly defined. An ocular glymphatic system has recently been described, drainage of which from the globe into intracranial glymphatics is reliant on the pressure gradient between intraocular pressure and intracranial pressure. The glymphatic pathway is the only extravascular anatomical conduit between the subarachnoid space and the retina. We propose that subarachnoid blood in skull base cisterns near the optic nerve is the substrate of blood in TS. Raised ICP causes it to be refluxed through glymphatic channels into the globe, resulting in intraocular hemorrhage. We herewith present glymphatic reflux as an alternative theory to explain the phenomenon of Terson Syndrome.
... Ejemplo de esta tendencia es el estudio de Czorlich et al. en su muestra de 16 casos de ST diagnosticados por OI, el 46,2% de los pacientes presentaron con ECG inicial < 9 y el 93,8% tenia un Fisher de 3 en la TC al ingreso 2 . Joswig et al., en 36 pacientes con HSA también describen resultados similares, con una proporción de casos de ST diagnosticados por OI de 16.66%, todos tuvieron una puntuación en la ECG inicial < 9, un Fisher de 3 y una puntación en la escala de Hunt y Hess > 3 11 . En el estudio de Seif et al., en 46 pacientes con HSA describen 10 casos de ST diagnosticados con OI; los pacientes con ST tenían (con significación estadística p < 0,05) una situación clínica más grave, de acuerdo con la ECG y la escala de Hunt y Hess. ...
Introduction:
Terson syndrome (TS) is defined as any intraocular haemorrhage identified in patients with acute intracranial pathology. TS appears to be associated with clinical severity in patients with subarachnoid haemorrhage (SAH), but the association is yet to be defined in patients with traumatic brain injury (TBI) and intracerebral haemorrhage (ICH). This study aimed to evaluate the diagnostic performance of ocular ultrasound (OU) and its usefulness in clinical practice.
Material and methods:
We performed an observational, prospective, single-centre study of neurocritical care patients. We analysed cases and controls, defined according to indirect ophthalmoscopy (IO) and OU findings. We determined the diagnostic characteristics of OU. A multivariate analysis was performed to identify clinically relevant associations.
Results:
The sample included 91 patients diagnosed with ICH (41.76%), SAH (29.67%), and TBI (28.57%). TS was identified by OU in 8 patients (8.79%) and by IO in 24 (24.37%). The adjusted mortality rate in patients with TS showed an odds ratio (OR) of 4.15 (95% confidence interval [CI], 1.52-11.33). All patients with TS detected by OU presented Glasgow Coma Scale scores < 9, with an elevated risk of needing decompressive craniectomy (OR: 9.84; 95% CI, 1.64-59). OU presented an overall sensitivity of 30.43%, specificity of 98.53%, and diagnostic accuracy of 81.32%. For the detection of vitreous haemorrhage, sensitivity and specificity were 87.5% and 98.5%, respectively.
Conclusions:
OU diagnosis of TS identifies extremely critical patients, who may require the highest level of care; TS is an independent risk factor for in-hospital mortality.
... Joswig et al. 9 Retrospective study with 36 patients. ...
... Patients with TS were more likely to develop increased ICP (mean initial ICP of 26 ± 6.9 mmHg vs non-TS 15 ± 5.8 mmHg), in some ventriculostomy was performed and all showed unsatisfactory results in the follow-up. 9 56.9% of the cases analyzed by Czorlich P. et al had an ICP > 25 mmHg. However, some patients had a pathological increase in ICP, favorable results and did not develop TS, a fact reported in both studies. ...
... However, some patients had a pathological increase in ICP, favorable results and did not develop TS, a fact reported in both studies. 9,10,16 In the systemic review carried out by McCarron et al., the number of TS cases in patients with SAH ranged from 3% (retrospective) to 13% (prospective). Most patients have bilateral vitreous hemorrhage, with the most prevalent aneurysms in the anterior circulation. ...
Terson's sign (TS) is classically defined as vitreous hemorrhage associated with subarachnoid hemorrhage of aneurysmal origin, being an important predictor of severity, indicating greater morbidity and mortality when compared to patients without the sign. The objective of this study is to review the relationship of Terson syndrome/Terson sign with the prognosis of aneurysmal subarachnoid hemorrhage. A search for original articles, research and case reports was performed on the PubMed, Scielo, Cochrane and ScienceDirect platform, with the following descriptors: Terson sign and subarachnoid hemorrhage. Retrospective, prospective articles and case reports published in the last 5 years and which were in accordance with the established objective and inclusion criteria were selected. Ten (10) articles were selected, in which the available results show an unfavorable prognostic relationship of TS and subarachnoid hemorrhage, because these patients had a worse clinical status assessed on the Glasgow scales ≤ 8, Hunt & Hess > III, Fisher > 3, in addition to intracranial hypertension and location of the aneurysm in the anterior communicating artery complex. The early recognition of this condition described by Albert Terson in 1900 brought an important contribution to neurosurgery, being recognized until nowadays. Resumo O sinal de Terson (ST) é definido classicamente por hemorragia vítrea associada à hemorragia subaracnóidea de origem aneurismática, sendo um importante preditor de gravidade, indicando maior morbimortalidade quando comparado aos pacientes sem o sinal. O objetivo deste estudo é revisar a relação entre síndrome de Terson/sinal de Terson e o prognóstico da hemorragia subaracnóide aneurismática. Foi realizada uma busca de artigos originais, relatos de casos e revisões na plataforma PubMed, Scielo, Cochrane e ScienceDirect, com os seguintes descritores: sinal de Terson e hemorragia subaracnóidea. Foram selecionados os artigos retrospectivos, prospectivos e relatos de caso publicados nos últimos 5 anos e que estivessem de acordo com o objetivo estabelecido e critérios de inclusão. Foram selecionados 10 artigos, nos quais os resultados disponíveis mostram uma relação prognóstica desfavorável do ST e hemorragia subaracnoide, em razão destes pacientes terem apresentado pior estado clínico quando avaliados nas escalas de Glasgow ≤ 8, Hunt e Hess > III, Fisher > 3, além da hipertensão intracraniana e localização do aneurisma no complexo da artéria comunicante anterior. O reconhecimento precoce desta condição descrita por Albert Terson em 1900 trouxe importante contribuição para a neurocirurgia, sendo reconhecido até hoje. Palavras-chave: Sinal de Terson; Aneurisma intracraniano; Hemorragia vítrea.
... Because ophthalmologic screening for Terson syndrome is not considered as a routine examination, Terson syndrome is concomitantly diagnosed with computed tomography or ultrasohography during brain evaluation [14][15][16] . Thus, with the widened defition, Terson syndrome remains an under-estimated disease, and recent studies have reported a prevalence of up to 40%, in subjects with intracranial hemorrhage who undergo fundus screening [9][10][17][18][19][20][21] . Some studies have also suggested that the presence of Terson syndrome may be associated with worse outcomes in patients with SAH, such as higher mortality or poor long-term prognosis [17][18][19][20] . ...
... Thus, with the widened defition, Terson syndrome remains an under-estimated disease, and recent studies have reported a prevalence of up to 40%, in subjects with intracranial hemorrhage who undergo fundus screening [9][10][17][18][19][20][21] . Some studies have also suggested that the presence of Terson syndrome may be associated with worse outcomes in patients with SAH, such as higher mortality or poor long-term prognosis [17][18][19][20] . This highlights the importance of increased focus on the detection of Terson syndrome in patients with intracranial hemorrhage. ...
... After ophthalmologic evaluation, we also investigated clinical outcome of Terson syndrome in aneurysmal SAH patients. The GCS and HH grade were significantly worse in the patients with Terson syndrome than those without, which were consistent with previous studies [17][18][19][20] . However, the mRS was not significantly different between the patients with and without Terson syndrome, which were not consistent with the results of previous studies [17][18][19][20] . ...
Aim:
To investigate clinical characteristics of asymptomatic Terson syndrome and its clinical impact in patients with aneurysmal subarachnoid hemorrhage (SAH).
Methods:
This retrospective, interventional study included 31 patients with aneurysmal SAH, and the medical records were reviewed. In addition to baseline characteristics of the study population such as age, sex, and underlying medical history, multi-modal imaging analysis, including fluorescein angiography (FA), spectral domain optical coherence tomography (SD-OCT), were also reviewed. Glasgow Coma Scale (GCS), Hunt-Hess (HH) grade, and Fisher scale at the time of admission, and functional outcome by using modified Rankin Scale (mRS) at 6mo were compared.
Results:
Of the 31 patients, 10 patients (32.3%) were diagnosed with Terson syndrome. All the patients with Terson syndrome did not report visual symptoms at the time of ophthalmologic screening. FA showed microvascular changes of retinal capillaries and varying degrees of disc leakage. SD-OCT allowed intuitive anatomical localization of multi-layered retinal hemorrhages and assessment of ellipsoid zone integrity. The patients with Terson syndrome showed significantly worse GCS (P=0.047) and HH grade (P=0.025) than those without, except Ficher scale (P=0.385). There was no significant difference in the mRS (P=0.250) at 6mo. Among baseline factors, the HH grade was the only significant factor associated with Terson syndrome (B=1.079, P=0.016).
Conclusion:
In our study, 32.3% of the patients have Terson syndrome without visual symptoms. The baseline HH grade is significantly correlated with Terson syndrome, and there is no significant difference in the functional outcome between the patients with and without Terson syndrome. Terson syndrome may develop without any visual symptoms as shown in our study, and ophthalmologic screening may be recommended to prevent further visual deterioration especially in the patients with poor HH grade at the time of aneurysmal SAH.
... However, in females, the incidence rate of Terson syndrome was higher in the coil embolization group, and the reason for this is unclear. Factors known to potentially be related to the occurrence of Terson syndrome, including the poor neurological condition of SAH 7,15 , a history of transient or prolonged coma before admission 4,16-18 , increased intracranial pressure 18 , and location, laterality, and size of aneurysms 19 , could not be investigated with the health claims data presented here. In order to determine whether the higher incidence in the coil embolization group in females is a meaningful result, these www.nature.com/scientificreports ...
The aim of this study is to investigate the incidence and mortality of Terson syndrome in patients with treated subarachnoid hemorrhage (SAH) in South Korea. In this nationwide, population-based study, we used the National Health Insurance(NHI) database (2011–2015) to identify patients aged ≥18 years. Newly diagnosed non-traumatic SAH, treated using clipping or coil embolization, were identified, and Terson syndrome was defined as newly diagnosed retinal or vitreous hemorrhage within 3 months of SAH diagnosis. We identified 22,864 patients with treated SAH (tSAH), 196 of whom had Terson syndrome, with the cumulative incidence during 5 years of 0.86% (95% CI: 0.74–0.98): 1.10% (95% CI: 0.88–1.33) in men and 0.71% (95% CI, 0.58–0.85) in women. The cumulative incidence of Terson syndrome in patients aged under 40 was higher than in those aged 40 or over (1.41% vs. 0.81%; p = 0.007). The mortality rate of Terson syndrome in patients with tSAH was not different from that in those without Terson syndrome (4.08% vs. 7.30%; p = 0.089). This was the first nationwide epidemiological study of Terson syndrome using a population-based database. The incidence of Terson syndrome in patients with tSAH was higher in those age under 40 than in those aged 40 or over.
... Terson syndrome was detected on CT scans with a sensitivity of 50%, a specificity of 98.4%, a positive predictive value of 83.3%, and a negative predictive value of 92.4%. 52 The methodologies used in these studies to determine risk of vision loss have not been sufficiently refined, and the cohorts have been too small to qualify CT scanning as a standalone method of diagnosing patients at risk of vision loss due to TS. In this manuscript, we describe a prospective series of consecutive patients with SAH due to ruptured cerebral aneurysms (aSAH) to determine the incidence of TS. ...
Purpose:
To determine if routinely performed computerized tomography (CT) scanning in patients with aneurysmal subarachnoid hemorrhages (aSAH) is sufficient to diagnose patients at high risk of vision loss due to Terson Syndrome (TS).
Methods:
Consecutive patients with a diagnosis of aSAH admitted to the Neurological Intensive Care Unit of a regional referral hospital were prospectively evaluated over a 3-year period. Head CT scans performed in the Emergency Department were assessed for the presence of a "crescent sign" (evidence of significant sub-internal limiting membrane hemorrhage). Dilated funduscopic examinations were performed by an ophthalmologist, masked to the results of the CT scan, to identify retinal and vitreous hemorrhages consistent with TS. Retinal hemorrhages were categorized according to size - those smaller than 2 mm in diameter were deemed low risk (lrTS) for vision loss and those greater than 2 mm in diameter were deemed high risk (hrTS) for vision loss.
Results:
One hundred seventeen patients with aSAH were enrolled in the study. The overall incidence of TS was 24.9% (29 of 117 patients; 12 were bilateral). Compared to patients without TS, those with TS had a higher Fisher Hemorrhage Grade and a lower mean (+ standard deviation) Glasgow Coma Score (8.66 + 4.97 vs. 12.09 + 1.10; P < 0.001). The CT crescent sign was positive in seven patients (6.0%), six (5.1%; two were bilateral) of whom were found to have hrTS. Of the 110 patients without a CT crescent sign, 88 (75.1%) patients did not have TS, 21 had lrTS, and one patient had hrTS in one eye. The CT crescent sign was highly sensitive (85.7%) and specific (99.1%) for diagnosing hrTS.
Conclusion:
The CT crescent sign is a highly sensitive and specific marker for hrTS. CT scanning may replace routine ophthalmologic examinations to identify patients at risk of vision loss due to aSAH.
... Factors relating to intraocular haemorrhage include high scores on the Hunt-Hess and Fisher Scales, low scores on the Glasgow Coma Scale, arterial hypertension, larger aneurysms, and older age [2,9]. Ophthalmologic treatment is usually conservative initially, and vision in most eyes improves with spontaneous absorption of the haemorrhage within a few months; however, the VH may not clear, increasing the risk of secondary glaucoma, retinal detachment (RD), proliferative retinopathy, and cataracts, which can compromise visual recovery even further. ...
Purpose:
To determine clinical characteristics and identify factors associated with better visual outcomes in patients who had vitrectomy for vitreous haemorrhage (VH) associated with Terson syndrome (TS).
Methods:
The records of 48 patients (54 corresponding eyes) who underwent vitrectomy for VH associated with TS from January 2008 to December 2017 were retrospectively reviewed. The main outcome measure was the final postoperative visual acuity.
Results:
At the last visit, 34 eyes (63.0%) achieved a BCVA of 0.3 or better. Eyes associated with traumatic brain injury had a better visual outcome than those with primary intracerebral haemorrhage (P = 0.042). In the primary intracerebral haemorrhage group, patients with hypertension-induced intracranial haemorrhage (IH) showed poorer final visual acuities than the ruptured intracranial aneurysm group (P = 0.023). In the delayed vitrectomy group, epiretinal membrane and peripheral retina changes were more common (P < 0.05). However, the difference in final visual acuity between the early and delayed vitrectomy groups was not significant (P = 0.69).
Conclusion:
Most of the patients obtained visual recovery after vitrectomy for TS. VH associated with ruptured intracranial aneurysm or traumatic brain injury or eyes without retinal haemorrhage are predictive of better prognosis. Although the timing of vitrectomy was not related to the final postoperative visual outcome, early vitrectomy by three months seems to suggest less epiretinal membrane formation, retinal tears, and retinal detachments.
