Angio negative findings in patients

with spontaneous subarachnoid

hemorrhage
Jose Daniel Flores Snchez
MR I Neurociruga
HNGAI

Angio negative findings in patients

with spontaneous subarachnoid
hemorrhage
75% - Causa aneurismtica
5% - MAV
20% - No lesin vascular evidente en angiografa.
Van Gijn J, Kerr RS, Rinkel GJ. Subarachnoid haemorrhage. Lancet 2007;369:30618.

Many authors have advocated a repeat angiogram after a defined time period to
detect these missed cases The repeat angiogram (digital subtraction angiogram
[DSA]) has got its own set of complications (SAHspecific mortality in 0.17% of
patients, focal neurological deficit in 3.2% of patients, with permanent disability in
0.04%)
Kaufmann TJ, Huston J 3rd, Mandrekar JN, Schleck CD, Thielen KR, Kallmes DF. Complications of diagnostic cerebral
angiography: Evaluation of 19,826 consecutive patients. Radiology 2007;243:8129.

Angio negative spontaneous

subarachnoid hemorrhage
A number of possible factors leading to nonvisualization of a structural
lesion, when it is actually present, have been mentioned in the literature,
these include:

Blood in cistern obscuring the aneurysm

Vasospasm proximal and distal to aneurysm leading to nonfilling of aneurysm
Vascular thrombosis, thrombus inside the aneurysmal sac
Small micro aneurysm
Very close proximity to skull bone
Hemorrhage from A venous system or simply A technically inadequate examination
-Kumar R, Das KK, Sahu RK, Sharma P, Mehrotra A, Srivastava AK, et al. Angio negative spontaneous subarachnoid
hemorrhage: Is repeat angiogram required in all cases?. Surg Neurol Int 2014;5:125
-McMahon J, Dorsch N. Subarachnoid haemorrhage of unknown aetiology: What next? Crit Rev Neurosurg
1999;25;9:14755

 With technical advancements, such as three dimensional

rotational DSA (3D rDSA), the recent incidence of DSAnegative
SAH has shown a significant reduction. This technique is better
than conventional two dimensional (2D) angiogram in detecting
aneurysm. Ishihara et al.[9] reported that the incidence of
DSAnegative SAH was 8.6% in the DSA group and 4.2% in the
3D rDSA group.
Ishihara H, Kato S, Akimura T, Suehiro E, Oku T, Suzuki M. angiogramnegative subarachnoid
hemorrhage in the era of three dimensional rotational angiography. J Clin Neurosci 2007;14:2525

 The overall incidence of neurological deficits due to procedural

complications during DSA has been reported to be around 12.6%,
with an incidence of persistent deficits following cerebral
angiography of about 0.10.5%. The nonneurologic complications
include:

Renal failure (00.15%)

Arterial occlusion requiring surgical thrombectomy or thrombolysis (00.4%)
Pseudo aneurysm formation (0.010.22%)
Hematoma formation requiring transfusion or surgical evacuation
(0.261.5%).

Kaufmann TJ, Huston J 3rd, Mandrekar JN, Schleck CD, Thielen KR, Kallmes DF. Complications of diagnostic cerebral
angiography: Evaluation of 19,826 consecutive patients. Radiology 2007;243:8129.

Negative CT angiography findings in patients with

spontaneous subarachnoid hemorrhage: When is digital
subtraction angiography still needed?
Different authors have described various patterns of bleed in SAH. Agid
et al. divided these patients into four groups as per the distribution of
subarachnoid blood on plain CT of head at the presentation:
I.
II.
III.
IV.

Perimesencephalic hemorrhage (PMH)

Diffuse aneurysmal pattern
Xanthochromic CSF on lumbar puncture with no blood demonstrated on CT
Peripheral sulcal pattern (with absence of basal cisternal blood).

Agid R, Andersson T, Almqvist H, Willinsky RA, Lee SK, terBrugge KG, et al. Negative CT angiography
findings in patients with spontaneous subarachnoid hemorrhage: When is digital subtraction angiography
still needed? AJNR Am J Neuroradiol 2010;31:696705.

Negative CT angiography findings in patients with spontaneous

subarachnoid hemorrhage: When is digital subtraction
angiography still needed?
Those patients who had evidence of perimesencephalic hemorrhage
presented in good clinical grade
(Hunt and Hess scale 1) with
headaches, no neurological deficits, no loss of consciousness, and have
a good prognosis. Agid et al. suggested that these patients do
not need any investigations except an initial CTA.
The second group of patients were those with diffuse aneurysmal
pattern of blood on CT. These patients have a potential risk for
rebleeding and have more significant symptoms at onset, and
relatively poor prognosis and the possible causes include an extremely
small aneurysm, dissection of arterial wall not detected on DSA, or
rupture of an artherosclerotic wall.
The third group with no evidence of SAH on plain CT but diagnosed on
lumbar puncture were negative for both CTA and/or DSA, which were
clinically similar to first group with a low rebleed risk.

 Ahn SY et al: They concluded that thick or diffuse SAH on initial CT scan was
suggestive of an aneurysmal bleed and a repeat angiogram is mandatory if
initial angio was negative. They also found CTA useful in the detection of
occult aneurysm early in the course of SAH.
Ahn SY, Lim DJ, Kim SH, Kim SD, Hong KS, Ha SK, Clinical analysis of patients with spontaneous
subarachnoid hemorrhage of initial negative angiography. Korean J Cerebrovasc Surg 2011;13:2304.

Other authors have also advocated repeat angiogram in

nonperimesencephalic pattern of SAH and advised against the same in
perimesencephalic bleeds.
Kumar R, Das KK, Sahu RK, Sharma P, Mehrotra A, Srivastava AK, et al. Angio negative spontaneous
subarachnoid hemorrhage: Is repeat angiogram required in all cases?. Surg Neurol Int 2014;5:125

 Classic (diffuse) SAH pattern of SAH is usually associated with fair

chances of an underlying missed pathology and also a relatively poorer
outcome. We recommend a repeat angiogram in all these patients with
rotational angiogram in order to exclude aneurysms, which is important
for reducing morbidity and mortality due to misdiagnosis.
Kumar R, Das KK, Sahu RK, Sharma P, Mehrotra A, Srivastava AK, et al. Angio negative
spontaneous subarachnoid hemorrhage: Is repeat angiogram required in all cases?. Surg
Neurol Int 2014;5:125

Agid R, Andersson T, Almqvist H, Willinsky RA, Lee SK, terBrugge KG, et al. Negative
CT angiography findings in patients with spontaneous subarachnoid hemorrhage:
When is digital subtraction angiography still needed? AJNR Am J Neuroradiol
2010;31:696705.

RECOMMENDATIONSUpToDate 2013. Farhan Siddig, MD. Jose Biller, MD. Amir S Khan, MD
An estimated 15 to 20 percent of patients with subarachnoid hemorrhage (SAH) are nonaneurysmal. The
causes of nonaneurysmal SAH (NASAH) are potentially diverse, and the mechanism of bleeding in these
cases is often not identified.
Perimesencephalic NASAH make up the majority of NASAH in some case series. These have a
distinctive appearance on computed tomography and a benign course.
Other causes of NASAH include occult aneurysm, intracranial or spinal vascular malformations, and
intracranial arterial dissection. Less common etiologies include sickle cell disease, pituitary apoplexy,
cocaine abuse, cerebral venous thrombosis, and bleeding disorders.
We recommend repeating DSA within 4 to 14 days after an initial negative study, because of the risk of a
false negative. (Up to 24 percent of all SAH patients with initial negative angiography have an aneurysm
found on repeat angiography. This may increase to as much as 49 percent if patients with
perimesencephalic SAH and patients with normal CT scans are excluded)
Patients with negative angiography should undergo gadolinium-enhanced magnetic resonance imaging
(MRI) of brain and spinal cord.
Some patients will not have an etiologic diagnosis after DSA and MRI. If rebleeding occurs in such
patients, further diagnostic interventions may include further angiographic study of the
brainand/orspinal cord,and/orsurgical exploration.
Complications of aneurysmal SAH, hydrocephalus, vasospasm and cerebral ischemia, seizures,
hyponatremia, and cardiac abnormalities also occur in NASAH. In this regard, patients with NASAH should
be managed similarly to aneurysmal SAH.

 Perimesencephalic nonaneurysmal subarachnoid hemorrhage (PM-NASAH) refers to a subset of SAH patients

with characteristic pattern of localized blood on computed tomography (CT), normal cerebral angiography, and
a benign course.
Between 4 and 9 percent of perimesencephalic SAH are caused by rupture of an aneurysm arising from the
posterior circulation. Most of the remainder of PM-NASAH do not have an identified etiology.
The clinical presentation of PM-NASAH overlaps with aneurysmal SAH with abrupt onset of headache,
meningismus, photophobia, and nausea. As a group, patients with PM-NASAH have milder clinical features than
those with aneurysmal SAH.
The CT findings that define perimesencephalic SAH include blood isolated to the perimesencephalic
cisterns anterior to the brainstem; there may be extension into the ambient cisterns or basal parts of the
sylvian fissures, but not into the lateral sylvian fissure, anterior interhemispheric fissure, or lateral ventricles.
An intracranial aneurysm should be excluded in all patients with perimesencephalic SAH. We suggest using
digital subtraction cerebral angiography (DSA). In centers that have a large experience with reliable CT
angiography (CTA), this may replace DSA. Repeat angiography should be done in patients in whom concerns for
underlying aneurysm remain because of underlying vasospasm or the technical quality of the initial study.
Patients who have recurrent bleeding should also have a repeat study. We also recommend a follow-up CTA in
all patients one week after the onset of PM-SAH.
Aside from monitoring, specific treatments are not required for patients with PM-NASAH. However, until a
cerebral aneurysm has been excluded on follow-up imaging, we suggest using prophylactic nimodipine to
ameliorate complications of potential vasospasm (Grade 2B).
The long-term prognosis for patients with PM-NASAH is in general excellent.