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Acta Ophthalmologica 2011

Terson’s syndrome as a prognostic factor for mortality of spontaneous subarachnoid haemorrhage Watanabe Sung,1 Bordon Arnaldo,1 Cavalheiro Sergio,2 Sallum Juliana1 and Farah Michel1 1

Department of Ophthalmology, Federal University of Sa˜o Paulo, Brazil Department of Neurosurgery, Federal University of Sa˜o Paulo, Brazil

2

ABSTRACT. Purpose: To evaluate the prognosis of mortality in patients with spontaneous subarachnoid haemorrhage associated with Terson’s syndrome. Methods: A prospective, consecutive case series study was conducted in patients admitted to the emergency room with a diagnosis of acute subarachnoid haemorrhage. After a complete neurological examination, funduscopic examination using binocular indirect ophthalmoscopy under mydriasis was performed upon admission and at days 3, 7, 30 and 60 after the onset. In all cases, the diagnosis of intracranial bleeding was made by computerized tomography, and the clinical condition was graded according to the Hunt & Hess and Glasgow coma scales. Results: Forty-seven patients with the diagnosis of subarachnoid haemorrhage were enrolled. Forty-four cases were associated with a ruptured aneurysm and three cases with arterio-venous malformation. Fourteen patients (29%) were diagnosed with Terson’s syndrome. Seven patients (50%) with Terson’s syndrome died, whereas death occurred in three patients (9%) without Terson’s syndrome (p = 0.002). Ocular findings in Terson’s syndrome were preretinal, intraretinal, sub-retinal and vitreous haemorrhage. Associated ocular findings included third-nerve palsy, papilloedema and subconjunctival haemorrhage. Conclusion: The presence of Terson’s syndrome was associated with an increased mortality rate (50% versus 9%; p < 0.01). Therefore, patients with the diagnosis of intracranial haemorrhage should be submitted to a funduscopic examination, because the presence of intraocular haemorrhage is an important life-threatening prognostic factor. Key words: arterio-venous malformations – cerebral aneurysm – retinal haemorrhage – Terson’s syndrome – vitreous haemorrhage

Acta Ophthalmol. 2011: 89: 544–547 ª 2009 The Authors Journal compilation ª 2009 Acta Ophthalmol

doi: 10.1111/j.1755-3768.2009.01735.x

Introduction In the USA, the incidence of subarachnoid haemorrhage is around

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30 000 cases ⁄ year. The principal cause is ruptured cerebral aneurysm, followed by arterio-venous malformations (Medele et al.1998).

The observation of vitreous haemorrhage associated with subarachnoid haemorrhage was first described by Albert Terson in 1900 (Terson 1900). Subsequently, it was found that any type of intraocular haemorrhage (IOH) could be associated with this clinical condition (Medele et al. 1998). The physiopathogenesis of IOH has been controversial for more than 50 years. However, the most accepted mechanisms are venous congestion and retinal vessel rupture because of a large increase in intracranial pressure (ICP) transmitted along the optic nerve sheath (Garfinkle et al. 1992; Biousse et al. 1998; Ogawa et al. 2001). The presence of Terson’s syndrome has been associated with an increase in mortality rate from 27% to up to 60%, with the higher rate occurring when IOH is bilateral (Vanderlinden & Chisholm 1974).

Materials and Methods This was a prospective, non-randomized case series study. Consecutive patients admitted to the neurosurgery emergency room of the Sa˜o Paulo Hospital (Sa˜o Paulo Federal University, Brazil) with a diagnosis of spontaneous acute subarachnoid haemorrhage were included for ophthalmological evaluation. Exclusion criteria were absence of subarachnoid haemorrhage, death of the patient

Acta Ophthalmologica 2011

occurring before ophthalmological examination or traumatic intracranial haemorrhage. After neurological examination, indirect ophthalmoscopy under mydriasis was performed in all patients at admission and on the 3rd, 7th, 30th and, when possible, 60th day of follow-up. Fundus dilation was carried out after clinical consent by the attending neurologist. The pupil dilation performed during the acute phase of the intracranial haemorrhage was undertaken as an exception in close cooperation with the neurosurgeons. Each patient in this study had a diagnosis of intracranial haemorrhage confirmed by computerized tomography or lumbar puncture and was submitted to cerebral angiography for localization of vascular changes. All patients were neurologically classified according to the Hunt & Hess (HH) and Glasgow coma scales upon admission, and were subsequently evaluated for the presence of IOH. Statistical analysis was performed using the v2 method and multivariate analysis.

Table 1. Characteristics of patients with Terson’s syndrome.

Age

Sex

Glasgow coma scale

HH

Type of intraocular haemorrhage

Eye

Death

80 48 47 51 43 46 43 51 73 45 43 37 47 36

M M F M F F F F M M F F F F

6 15 15 13 13 11 10 3 14 15 15 15 9 13

IV IV II III II II III V III II I II II II

IR IR IR PR + IR IR IR PR PR + IR IR + IV IR IR + papilloedema PR + SR + IR + IV PR PR + IR + SR

OU OD OD OD OU OS OS OU OU OU OD OU OU OU

Y N Y Y Y N N Y N N Y N Y N

HH, Hunt & Hess scale at initial presentation; OD, right eye; OS, left eye; OU, both eyes; PR, preretinal; IV, intravitreous; IR, intraretinal; SR, subretinal.

Results Forty-seven consecutive patients diagnosed with spontaneous acute subarachnoid haemorrhage were enrolled. The causes of intracranial haemorrhage were ruptured aneurysm (44 cases) and arterio-venous malformation (three cases). Upon admission, 14 patients (29%) presented with Terson’s syndrome, of which eight were bilateral cases (57%). Thirty-one patients were female. Mean age was 49.0 years (range 22–80 years). Of the patients with Terson’s syndrome nine were female and five were male, with a mean age of 49.2 years (range 36– 80 years). Ophthalmological examination in patients with Terson’s syndrome revealed sub-retinal haemorrhage in two (14%) patients, intraretinal haemorrhage in 12 (86%) patients, preretinal haemorrhage in six (43%) patients and vitreous haemorrhage in two (14%) patients. In one patient, papilloedema was associated with intraretinal haemorrhage (Table 1). Other ocular alterations were subconjunctival haemorrhage in one (7%) patient and cranial third-nerve palsy in nine

Fig. 1. Colour fundus picture of the left eye of a 37-year-old patient with subarachnoid haemorrhage after a ruptured basilar artery aneurysm showing preretinal and subretinal haemorrhages.

(64%) patients. Figure 1 shows subretinal and preretinal haemorrhage of the left eye of a patient with Terson’s syndrome. Fundus examination showed no alterations in the group without Terson’s syndrome. The main cause of death in both groups was subarachnoid rebleeding (50%). According to Table 1, seven patients (50%) died in the Terson’s syndrome group whereas three patients (9%) died in the other group (P = 0.002). Comparing only patients who did not survive, among those with Terson’s syndrome the mean age was 51.7 years

(five women, two men); in the group without Terson’s syndrome the mean age was 56.0 years (all three patients were female). Regarding the Glasgow and HH scales upon admission, in the Terson’s syndrome group only two patients had a Glasgow score < 8 and three patients had HH scale > III. Among the group without Terson’s syndrome, only one patient had a Glasgow score < 8 and no patient had HH scale > III. Table 2 shows no correlation between age, sex or hypertension and

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Acta Ophthalmologica 2011

Table 2. Multivariate analysis in Terson’s syndrome.

Terson Yes No Age Sex Male Female Hypertension Yes No

No. of individuals

Death

p-value

Odds ratio

Adjusted odds ratio (95% CI)

14 34 48

7 3 14

0.04* – 0.15

53.514 Reference 1.09

2.90–3468.87 – 0.99–1.26

17 31

2 8

– 0.09

Reference 29.129

– 0.91–2138.07

24 24

5 5

0.18 –

0.1199 Reference

0.07–1.93 –

CI,confidence interval. * p < 0.05.

Fig. 2. B-scan of a patient with Terson’s syndrome showing increased reflectivity in the vitreous cavity, indicating the presence of vitreous haemorrhage.

death according to a multivariate association (p = 0.15; p = 0.09; p = 0.18, respectively). All patients with Terson’s syndrome had conservative treatment for ocular haemorrhage and were referred to the Retina Sector. Ultrasound examination was recommended to detect a developing retinal detachment. Figure 2 shows a B-scan of a patient revealing vitreous haemorrhage and attached retina.

Discussion Terson’s syndrome was first classically defined as vitreous haemorrhage observed in patients with subarachnoid haemorrhage caused by ruptured

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cerebral aneurysm. Later, the definition was modified to include other forms of IOH (Castren 1963). This syndrome has been observed rarely with subdural haematoma or cranioencephalic trauma (Vanderlinden & Chisholm 1974; Garfinkle et al.1992; Medele et al. 1998). The frequency of cerebral aneurysms is higher in women (Frizzell et al. 1997), and this trend was also observed in our series. In our study, the incidence of IOH was 29%; this is comparable with other prospective series, which reported between 8.0 and 46% (Vanderlinden & Chisholm 1974; Garfinkle et al. 1992; Frizzell et al. 1997; Kuhn et al. 1998; Medele et al.1998; Wietho¨lter et al. 1998; Stiebel-Kalish et al.

2004; Fountas et al. 2008). In our study, vitreous haemorrhage was found in 14.2% of cases and other types of haemorrhage comprised the majority. Vitreous haemorrhage has been the most described type in several retrospective studies and case series (Vanderlinden & Chisholm 1974; Schultz et al. 1991; Ogawa et al. 2001; Murthy et al. 2002; Stiebel-Kalish et al. 2004). One possible explanation is that in our study all patients were examined within 24 hr of admission, allowing early diagnosis of types of IOH other than vitreous bleeding. In addition, the last day of ophthalmological examination was the 60th day after the episode of intracranial hypertension, which allowed us to include any delayed Terson’s syndrome onset. Ocular haemorrhage was bilateral in 57% of our patients. This incidence is comparable with previous studies, which reported prevalence levels of 42.0–50% (Medele et al. 1998; Fountas et al. 2008). In the majority of cases, haemorrhage in Terson’s syndrome clears spontaneously, disappearing in a few weeks without sequelae (Vanderlinden & Chisholm 1974; Garfinkle et al. 1992; Biousse et al. 1998; Kuhn et al. 1998). In cases of vitreous haemorrhage, recovery generally occurs within 6–12 months. If it persists after 3–6 months or in cases of bilateral vitreous haemorrhage, epiretinal membrane or proliferative retinopathy patients can be submitted to a pars plana vitrectomy, usually with good results (Schultz et al. 1991; Pfausler et al. 1996; Augsten et al. 2000; Gnanaraj et al. 2000; Sharma et al. 2002). Recent studies described better visual outcome in cases of early vitrectomy within 90 days of vitreous haemorrhage (Ritland et al. 2002; Garweg & Koerner 2009). An ocular ultrasonographic examination is recommended before the surgical procedure (Schultz et al. 1991; Kuhn et al. 1998). Ocular complications include glaucoma, epiretinal membrane, retinal detachment and cataracts, in addition to amblyopia and myopia in children (Kuhn et al. 1998; Sadeh et al. 1999; A´vila et al. 2001). In our study, all patients showed improvement of ocular haemorrhage without further complications. In the present study, the mortality rate was higher among patients with Terson’s syndrome (50%). This rate is

Acta Ophthalmologica 2011

similar to the rate of 54% reported by Shaw & Landers (1975). Pfausler et al. (1996) reported a mortality rate of 90% with Terson’s syndrome compared with 23% without ocular haemorrhage. Fountas et al. (2008) found a 28.6% mortality rate with Terson’s syndrome versus 2% without it. Systemic arterial hypertension and age were not found to correlate with death at a statistically significant level in this study. In addition, the mean age of the patients who died was similar to that of those who survived. Other factors, such as poor clinical condition, Glasgow coma scale score < 8, HH grade > III, World Federation of Neurological Societies score > III and Fisher grade > 3 have been associated with Terson’s syndrome in previously published studies (Garfinkle et al. 1992; Pfausler et al. 1996; Fountas et al. 2008). However, in the current series, the admitting Glasgow and HH scales revealed good scores in the majority of patients. HH grade > III was found in three (21.4%) patients with Terson’s syndrome and no patients within the non-Terson’s group. In conclusion, the mortality rate was significantly higher among patients with Terson’s syndrome than in those without the syndrome. Other types of IOH were more frequent than vitreous bleeding in patients with Terson’s syndrome. A careful fundus examination is recommended in all patients with subarachnoid haemorrhage. However, we stress that a fundus examination in mydriasis should be undertaken only after the acute phase of the intracranial haemorrhage (when the aneurysm is under control), with a stable patient and with the full agreement of the attending neurologist and ⁄ or neurosurgeon.

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Received on October 30th, 2008. Accepted on July 5th, 2009. Correspondence: Dr Sung Eun Song Watanabe Federal University of Sa˜o Paulo – Ophthalmology Rua Estero Belaco 407 ap 54 Saude Sa˜o Paulo Sa˜o Paulo 04145-020 Brazil Tel: + 55 11 3286 0349 Fax: + 55 11 5906 0632 Email: [email protected]

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