Clinical outcome of spontaneous non-aneurysmal subarachnoidhemorrhage in 108 patients

D. Canovasa, A. Gilb, M. Jatoc, M. de Miqueld and F. Rubioe

aDepartment of Neurology, Sabadell Hospital, Associate Professor of Universitat Autonoma de Barcelona, Barcelona; bDepartment of

Neurology, Clınica Quiron, Valencia; cDepartment of Neurology, Viladecans Hospital, Barcelona; dDepartment of Neuroradiology, Bellvitge

Hospital, Barcelona; and eDepartment of Neurology, Bellvitge Hospital, Universitat de Barcelona, Barcelona, Spain

Keywords:

non-aneurysmal,

outcome, spontaneous,

subarachnoid hemorrhage

Received 22 May 2011

Accepted 22 August 2011

Background: The cause of spontaneous subarachnoid hemorrhage (SAH) is unknown

in 15% of cases; idiopathic SAH has a better prognosis than aneurysmal SAH. When

bleeding is confined to the perimesencephalic cisterns, SAH has an especially benign

course.

Methods: We retrospectively studied 108 patients admitted for spontaneous non-

aneurysmal SAH between 1991 and 2004. We divided patients into two groups

according to the bleeding pattern at cranial CT: perimesencephalic pattern (n = 60)

and aneurysmal pattern (n = 48). We included only patients in whom no source of

bleeding was detected at angiography; patients with aneurysmal pattern underwent at

least two angiographic examinations. Mean follow-up was 5.5 years; follow-up con-

sisted of telephone interview in 84.7% of patients.

Results: All but one patient with perimesencephalic pattern were classified as grade I

or II on the Hunt and Hess scale; the exception was the only patient in this group with

a complication (hydrocephalus), who was classified as grade IV. Three-quarters of the

patients with aneurysmal pattern were classified as grade I or II on the Hunt and Hess

scale; 5 patients presented with hydrocephalus that required drainage and 2 with

vasospasms without repercussions. No rebleeding or long-term complications were

observed in either group.

Conclusions: Non-aneurysmal SAH with a perimesencephalic pattern of bleeding has

a benign course and excellent short-term and long-term prognosis. Patients with non-

aneurysmal SAH with an aneurysmal pattern of bleeding have more complications,

and the initial clinical situation has a significant impact on their prognosis.

Introduction

Spontaneous subarachnoid hemorrhage (SAH)

accounts for 5% of all cerebrovascular disease. In

approximately 80% of cases, SAH is caused by aneu-

rysmal rupture. After other lesions, mainly vascular

malformations and dissections, are eliminated, 15% of

cases remain idiopathic. Although the clinical

presentation of non-aneurysmal SAH is often indistin-

guishable from that of aneurysmal SAH, patients with

non-aneurysmal SAH tend to have much better out-

comes than those with ruptured cerebral aneurysms.

Moreover, non-aneurysmal SAH patients can be divided

into two groups according to the bleeding pattern on

cranial CT: those with a perimesencephalic pattern, in

whom bleeding is confined to the midbrain cisterns with

no evidence of intraventricular or intracerebral bleeding,

and those with an aneurysmal pattern, in whom bleeding

mimics that seen in aneurysmal ruptures and affects the

carotid cisterns, Sylvian fissure, and/or interhemispheric

fissure. The prognosis for patients with the perime-

sencephalic pattern is usually excellent.

We aimed to evaluate the short-term and long-term

complications in the two bleeding patterns of non-

aneurysmal SAH and to identify factors related to

worse prognosis.

Patients and methods

We reviewed the data from 108 patients presenting at

our center with spontaneous non-aneurysmal SAH

between 1991 and 2004 in whom no anomalies were

observed on conventional angiography. Patients were

classified into two groups according to the pattern of

Correspondence: D. Canovas, C/Antoni Gaudi no 10 Entresuelo 1ª

Sant Joan Despı CP: 08970 Barcelona, Spain (tel.: +34 661313356;

fax: +34 934772691; e-mail: davidcanovas2000@yahoo.es).

� 2011 The Author(s)European Journal of Neurology � 2011 EFNS 457

European Journal of Neurology 2012, 19: 457–461 doi:10.1111/j.1468-1331.2011.03542.x

bleeding at cranial CT: (i) those with a perimesence-

phalic pattern of bleeding, defined according to Rinkel

et al.�s criteria [1] as a hemorrhage localized around the

basal cisterns, more characteristically anterior to the

midbrain and/or pons, with little extension (maximum

in the proximal third) into the Sylvian fissure and the

anterior interhemispheric fissure. This definition allows

a very small amount of intraventricular blood (Fig. 1);

and (ii) those with an aneurysmal pattern of bleeding,

defined as the presence of blood in sites often affected in

aneurysmal SAH, including the anterior interhemi-

spheric fissure, Sylvian fissure, and intraventricular

space beyond the limits set for the perimesencephalic

pattern (Fig. 2). A second negative angiogram was re-

quired for inclusion in the group of patients with

aneurysmal pattern of bleeding.

We recorded the following variables: sex, age, time of

symptom onset, time-to-diagnosis, Valsalva maneuver,

initial Hunt and Hess scale, history of hypertension, in-

hospital complications (clinical vasospasm, rebleeding,

or hydrocephalus requiring shunting), and long-term

complications. We reviewed laboratory findings for

alterations in sodium levels and electrocardiograms for

changes indicative of SAH.

Long-term follow-up consisted of telephone inter-

views to ascertain sequelae (headache, nausea, memory

loss, personality changes, anxiety, and depression) and

disability according to the modified Rankin scale.

Differences between both groups were assessed with

Pearson�s chi-square test; statistical significance was setat P < 0.05.

According to the local regulations, no ethics board

approval was needed for the retrospective study. The

hospital ethics board approved the protocol for the

telephone interview.

Results

The bleeding pattern was classified as perimesence-

phalic in 60 patients (48% male; mean age, 50.4 years)

and as aneurysmal in 48 (41% male; mean age,

55 years). The prevalence of hypertension did not differ

between patients with perimesencephalic pattern and

those with aneurysmal pattern of bleeding (20% vs.

25%, respectively).

Long-term follow-up (mean, 5.5 years; range,

1–14 years) data were available for 52/60 (86%) pa-

tients with perimesencephalic bleeding pattern and for

41/48 (85%) patients with aneurysmal bleeding pattern.

Time-to-diagnosis through cranial CT was <24 h in

71% of patients with perimesencephalic pattern and in

81% of those with aneurysmal pattern; diagnosis after

24 h was considered delayed diagnosis.

All but one patient with perimesencephalic pattern

were classified as grade I or II on the Hunt and Hess

scale; the exception was the only patient in this group

with a complication (hydrocephalus), who was classi-

fied as grade IV. Three-quarters of the patients with

aneurysmal pattern were classified as grade I or II on

the Hunt and Hess scale.

SAH was associated with a Valsalva maneuver in

37% of the patients with perimesencephalic pattern and

in 16% of those with aneurysmal pattern.

Short-term complications

Only one patient with perimesencephalic bleeding pat-

tern (the one classified as grade IV on the Hunt and

Hess scale) had a short-term complication (hydro-

cephalus requiring ventriculoperitoneal shunting).

Figure 1 Perimesencephalic pattern.

Figure 2 Aneurysmal pattern.

458 D. Canovas et al.

� 2011 The Author(s)European Journal of Neurology � 2011 EFNS European Journal of Neurology

Complications were more common in patients with

aneurysmal bleeding pattern, including hydrocephalus

requiring drainage in five patients (two classified as

Hunt and Hess III and one classified as Hunt and Hess

IV) and vasospasms in 2. Both patients with vasosp-

asms had good clinical outcome. One, a 44-year-old

woman classified as Hunt and Hess III on admission,

presented somnolence and paresis of the III cranial

nerve on the sixth day, and the other, a 48-year-old

man, presented self-limiting paresis of the left hand on

the sixth day. Both these patients underwent three

angiographic examinations and no evidence of aneu-

rysms was found. The two cases of vasospasm were

diagnosed after transcranial Doppler and were treated

with plasma expanders and inotropic drugs. No reb-

leeding occurred in any patient in either group. We

found no relevant cardiac anomalies or hyponatremia

(Na < 130 mEq/l).

Long-term complications

Only one patient with aneurysmal bleeding pattern and

hydrocephalus requiring drainage, classified as grade IV

on the Hunt and Hess scale at admission, had moder-

ately severe disability (Rankin 4). No other long-term

complications were observed in either group. All the

patients with perimesencephalic bleeding pattern scored

0 on the modified Rankin scale.

We interviewed patients on the telephone, asking

about subjective cognitive deficits, depression, and

headaches. Headaches were reported by 25% of pa-

tients with perimesencephalic bleeding pattern and 29%

of those with aneurysmal pattern; subjective memory

loss was reported by 10% of patients with perime-

sencephalic pattern and 31% of those with aneurysmal

pattern.

Table 1 compares our results with those of the most

relevant published series. In our series, five patients

with aneurysmal bleeding pattern (12%) developed

hydrocephalus that required shunting; this figure is

similar to that reported by most authors. Table 2

reports the long-term complications related by the

idiopathic SAH patients in our series during telephone

interviews.

Another complication of SAH is hyponatremia,

which affected 29% of Rinkel et al.�s [2] series, although

sodium levels were lower than 130 mM in only 15%. In

our series, none of the 85 patients (47 with perime-

sencephalic bleeding pattern and 38 with aneurysmal

bleeding pattern) for whom data were available had

sodium levels lower than 130 mM.

Discussion

Our results corroborate those of other studies about

idiopathic SAH and especially those about idiopathic

SAH with perimesencephalic bleeding pattern. The

percentage of patients with perimesencephalic bleeding

pattern in our series (56%) is similar to those reported

by van Gijn et al. [3] (65%) and Rinkel et al. [2] (68%)

and somewhat higher than that reported by Calenberg

et al. [4] (32%). Moreover, the male-to-female ratio and

age of patients with the perimesencephalic pattern in

our series is similar to those reported elsewhere. The

prevalence of hypertension in our patients is not greater

than in the general public. The SAH was associated

with the Valsalva maneuver in 37% of the patients with

perimesencephalic bleeding pattern and in 16% of those

with aneurysmal pattern, which lends some support to

the hypothesis of venous rupture through increased

pressure in the venous network.

The time from the onset of symptoms to cranial CT

study is crucial to enable patients with perimesence-

phalic bleeding pattern to be distinguished from those

with aneurysmal pattern, because subarachnoid blood

progressively washes out; this washout is much more

evident after 72 h. In our series, 81% of the patients

with perimesencephalic pattern and 84% of those with

aneurysmal pattern underwent cranial CT within 72 h

of symptom onset. We included 10 patients who did not

undergo cranial CT until 4 days after onset in the group

with perimesencephalic bleeding pattern; although this

is debatable, all had excellent outcomes (one patient

was lost to follow-up).

All our patients presented with the intense, sudden

headache typical of aneurysmal SAH. However, in

contrast to patients with aneurysmal SAH, none of our

patients with perimesencephalic bleeding pattern and

very few of those with aneurysmal bleeding pattern lost

consciousness.

Only one patient with perimesencephalic pattern (the

one that had hydrocephalus requiring shunting) was

Table 1 Complications of the aneurysmal bleeding pattern in different series

Aneurysmal bleeding pattern No patients Rebleeding Hydrocephalus + shunt Clınical vasoespasm Disability/death

Rinkel 36 4 (11%) 5 (14%) 1 (3%) 9 (25%)

Lagares 45 2 (4%) 6 (13%) 6 (13%) 9 (20%)

Van Calenberg 24 2 (8%) 5 (21%) 4 (17%) 3 (12%)

Canovas 48 0 5 (10%) 2 (4%) 1 (2%)

Non-aneurysmal subarachnoid hemorrhage 459

� 2011 The Author(s)European Journal of Neurology � 2011 EFNS European Journal of Neurology

classified as grade IV on the Hunt and Hess scale at

admission. However, the initial clinical classification of

patients with aneurysmal pattern of bleeding was worse:

three of the five patients with hydrocephalus were

classified as Hunt and Hess grade III, and one of the

two patients with vasospasm was also classified as grade

III. Moreover, the initial clinical condition seems to be

related with the prognosis, as Ildan et al. [5] affirm in

their review of 84 cases.

Our mean follow-up period (5.5 years) is similar to

that reported in most other studies of idiopathic SAH,

including Rinkel et al. [1] (3.7 years), Canhao et al. [6]

(4.2 years), Brilstra et al. [7] (6 years in patients with

perimesencephalic pattern), and Lagares et al. [8]

(5.8 years in a series of 122 patients).

Regarding the short- and long-term complications,

the prognosis is good in both groups.

As reported in the most representative series (Rinkel

et al. [1,2] and van Gijn et al. [3]), we found no reb-

leeding in patients with perimesencephalic pattern. To

our knowledge, only three cases of rebleeding in

patients with perimesencephalic pattern have been

reported: one by Marquardt et al. [9] occurring after

31 months with normal findings at angiography and

excellent outcome, another by Ildan et al. [5] resulting

in the patient�s death, and of the third by Lagares et al.

[8] in a series of 48 patients. Clinical vasospasm unre-

lated to angiography in patients with perimesencephalic

bleeding pattern is extremely rare; we found only one

case, reported by Sheehan et al. [10], and this patient

had a good clinical outcome. In our series, only one

patient (1.6%) with perimesencephalic bleeding pattern

had hydrocephalus requiring shunt placement; this rate

is similar to those reported in the literature (1%). In

general, clinical vasospasm in non-aneurysmal SAH is

rare [11–14]. It appears that volumetric quantification

of SAH is a good predictor of delayed cerebral ischemia

in patients with aneurysmal SAH [15].

The only patient with perimesencephalic bleeding

pattern in our series who required surgical intervention

for hydrocephalus was classified as grade IV on the

Hunt and Hess scale, and this supports the idea that

neurological status on admission is the single most

valuable prognostic factor for outcome in idiopathic

SAH. Sarabia et al. [16] argue in favor of this hypoth-

esis in their recent publication. Kong et al. [17].

reported that disturbed consciousness, vomiting, and

poor Hunt and Hess Grade were less common among

patients with perimesencephalic bleeding pattern.

Although the prognosis for patients with non-aneu-

rysmal SAH with aneurysmal bleeding pattern is clearly

much more favorable than for those with aneurysmal

SAH, the prognostic factors in this subgroup of non-

aneurysmal SAH patients are not clearly established.

Whereas we found no rebleeding among our patients,

rebleeding rates in the literature range from 0 to 11%,

including 4/36 patients (11%) in Rinkel et al.�s [2] ser-ies, 2/24 patients (8%) in van Calenberg et al.�s [4]

series, 0/15 patients (0%) in van Gijn et al.�s [3] series,and 2/45 patients (4%) in Lagares et al.�s [8] series. Thepresence of vasospasm with clinical repercussions in

only two patients and the good clinical outcomes of

these patients are also noteworthy.

Conclusions

Non-aneurysmal SAH has a good prognosis; moreover,

it is useful to distinguish between patients according to

the bleeding patterns observed at cranial CT.

Both the short- and long-term prognosis are excellent

for patients with perimesencephalic bleeding pattern.

Although the prognosis for patients with non-aneu-

rysmal SAH with aneurysmal pattern of bleeding is

much better than for those with SAH because of

aneurysmal rupture, complications are more common

in this group than in those with perimesencephalic

pattern.

The initial clinical situation is an important prog-

nostic factor, mainly in patients with aneurysmal

bleeding patterns, and patients with grade III or IV on

the Hunt and Hess scale have more complications.

Disclosure of conflict of interest

The authors declare no financial or other conflict of

interests.

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Table 2 Long-term follow-up of idiopathic SAH

Complaints reported during

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(n = 52)

Aneurysmal

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Dizziness 2 (4%) 5 (10%)

Mood changes 0 1 (2%)

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Anxiety 1 (2%) 2 (4%)

Depression 1 (2%) 3 (6%)

*P-value (chi-square) = 0.023.

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460 D. Canovas et al.

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