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Diagnostic and Interventional Imaging (2015) xxx, xxx—xxx
CONTINUING EDUCATION PROGRAM: FOCUS. . .
Subarachnoid hemorrhage in ten questions M. Edjlali a,b,∗, C. Rodriguez-Régent a, J. Hodel b, R. Aboukais c, D. Trystram a, J.-P. Pruvo b, J.-F. Meder a, C. Oppenheim a, J.-P. Lejeune c, X. Leclerc b, O. Naggara a a
Inserm UMR 894, Department of Neuroradiolgy, Faculty of Medicine Paris Descartes University, Pyschiatry and Neurosciences Centers, Sainte-Anne Hospital, Sorbonne Paris Cité, 1, rue Cabanis, 75014 Paris, France b Department of Neuroradiology, Lille Nord de France University, Roger Salengro Hospital, Lille University Hospitals, avenue Émile-Laine, 59037 Lille cedex, France c Department of Neurosurgery, Lille Nord de France University, Roger Salengro Hospital, Lille University Hospitals, avenue Émile-Laine, 59037 Lille cedex, France
KEYWORDS Hemorrhage; Intracranial aneurysm; CT; MRI
Abstract Traumatic subarachnoid hemorrhage (SAH) has an annual incidence of 9 per 100 000 people. It is a rare but serious event, with an estimated mortality rate of 40% within the first 48 hours. In 85% of cases, it is due to rupture of an intracranial aneurysm. In the early phase, during the first 24 hours, cerebral CT, combined with intracranial CT angiography is recommended to make a positive diagnosis of SAH, to identify the cause and to investigate for an intracranial aneurysm. Cerebral MRI may be proposed if the patient’s clinical condition allows it. FLAIR imaging is more sensitive than CT to demonstrate a subarachnoid hemorrhage and offers greater degrees of sensitivity for the diagnosis of restricted subarachnoid hemorrhage in cortical sulcus. A lumbar puncture should be performed if these investigations are normal while clinical suspicion is high. © 2015 Éditions franc ¸aises de radiologie. Published by Elsevier Masson SAS. All rights reserved.
Subarachnoid hemorrhage (SAH) is defined as blood in the cerebrospinal fluid contained in the basal cisternae and the sub-arachnoid space of the cerebral hemispheres, contained between the arachnoid mater and the pia mater. The most common cause is head injury. Apart from this cause, SAH accounts for 5 to 10% of cerebrovascular accidents and has a high mortality rate, which is estimated to be
∗ Corresponding author. Inserm UMR 894, Department of Neuroradiolgy, Faculty of Medicine Paris Descartes University, Pyschiatry and Neurosciences Centers, Sainte-Anne Hospital, Sorbonne Paris Cité, 1, rue Cabanis, 75014 Paris, France. E-mail address: [email protected] (M. Edjlali).
http://dx.doi.org/10.1016/j.diii.2015.06.003 2211-5684/© 2015 Éditions franc ¸aises de radiologie. Published by Elsevier Masson SAS. All rights reserved.
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between 40 and 50% [1,2]. By far the most common cause of SAH apart from trauma is intracranial aneurysm rupture (85% of non-traumatic causes) [3]. If SAH is suspected, cerebral imaging should be performed urgently to confirm the diagnosis, identify any complications and investigate its cause. We propose you here to develop the theme of SAH through ten questions. We will not consider the complications of rebleeding and vasospasm in this article.
When a patient presents with a sudden-onset headache, is CT an appropriate investigation? Unenhanced cerebral CT is recommended for acute headaches (less than 24 hours old), which are sudden in onset, to investigate for a subarachnoid hemorrhage (SAH) (grade A guideline, guide to the correct use of medical imaging examinations). The clinical features of the headache are fundamental. A SAH should be suspected in the case of a suddenonset headache of maximum intensity from the outset and described as a ‘‘thunderclap in a clear sky’’. This may be combined with meningism without fever or reduced consciousness level. An urgent CT should be performed and enables a diagnosis of SAH to be made if an unenhanced hyperdensity is present in the subarachnoid spaces, which usually involves the basal cisternae, inter-hemispheric sulci and lateral sulci [4]. When it is performed during the first 24 hours, CT has a sensitivity of 95% [5]. The sensitivity of CT depends mostly on the extent of the SAH but also on hemoglobin concentration and falls with the time between the initial headache and time when the scan is performed. After 7 days, therefore, CT is positive in only 50% of cases in SAH. Apart from a positive diagnosis of SAH, the initial CT examination can detect the early complications of
hydrocephalus, intraparenchymal hematoma with space occupying effect and ventricular hemorrhage (Fig. 1). Hydrocephalus which begins with dilatation of the temporal horns, and a compressive intra-parenchymal hematoma are important to report as these are life-threatening and require immediate neurosurgery with an external ventricular shunt, or evacuation of the hematoma before treatment for the cause of the SAH [6]. Using the modified Fisher scale [7] (Fig. 2, Table 1), CT is also of prognostic value in terms of the secondary development of vasospasm as the scale is a predictive indicator for vasospasm. Whilst sudden-onset headache is an indication for CT, an unenhanced investigation is not sufficient. Sudden-onset headaches may be due to an aneurysm which has not ruptured. In this case, the term sentinel headaches is used, which describes a state of pre-rupture or fissuring of the aneurysm. It is therefore recommended that for suddenonset headaches, even without SAH, imaging of the circle of Willis be performed to look for an intracranial aneurysm.
Are there signs which help to localize the source of the bleeding? Neurological signs A IIIrd cranial nerve palsy on a background of sudden-onset headache is a clinical localizing sign and indicates pressure on the nerve, either directly by the aneurysm or by the hematomas secondary to rupture of the aneurysm. The aneurysm itself can then be looked for the posterior wall of the ending of the internal carotid artery, close to the origin of the posterior communicating artery (Fig. 3), or less commonly, developing at the origin of the superior cerebellar artery. On the other hand, features of pyramidal irritation and paralysis of the VIth cranial nerve are of no localizing value.
Figure 1. Axial cerebral CT without enhancement (A) and angiogram of the arterial circle at the base of the brain (B) on MIP reconstructions centered on the circle of Willis. Positive diagnosis of subarachnoid hemorrhage (A): unenhanced hyperdensity in the subarachnoid spaces (arrow) affecting the basal cisternae, motor cortex sulchi and interhemispheric fissure without flooding of the ventricles. Diagnosis of an early complication: early hydrocephalus with dilation of the temporal horns (star). Coexistent preretinal hemmorage (Terson Syndrome, thick arrow). Diagnosis of cause (B): ruptured terminal basilar artery aneurysm (arrow head).
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Figure 2. Cerebral CT images without enhancement illustrating different grades of the Fisher classification. A. Grade 0: no SAH, no ventricular hemorrhage. B. Grade 1: minimal SAH, no ventricular hemorrhage in the 2 lateral ventricles. C. Grade 3: large SAH. No ventricular hemorrhage in the two lateral ventricles. D. Grade 4: large SAH ventricular hemorrhage in both lateral ventricles.
Radiological signs associated with blood distribution The distribution of the SAH and presence of any hematoma help localize the aneurysm responsible for the bleeding. An SAH predominantly in the anterior part of the interhemispheric cisterna and the suprasellar cisternae and/or an interhemispheric hematoma suggest an anterior communicating artery aneurysm. An SAH predominantly in the motor cortex sulcus or a temporopolar hematoma should trigger investigation for an ipsilateral middle cerebral artery aneurysm. An isolated lenticular hematoma may occur as a result of rupture of an end carotid aneurysm. An SAH predominantly in the basal cisternae next to the cerebellopontine angle cisternae with asymmetrical distribution suggests a ruptured postero-inferior cerebellar artery (PICA) aneurysm [4,8]. An acute subdural hematoma without a background of injury should trigger investigation for a
Table 1
Modified Fisher’s scale, 2001.
Grade
Criteria
0
No subarachnoid hemorrhage (SAH) or ventricular hemorrhage (VH) Minimal SAH, no HV in the 2 lateral ventricles Minimal SAH, HV in the 2 lateral ventricles Large SAHa , no VH in the 2 lateral ventricles Large SAHa , VH in the 2 lateral ventricles
1 2 3 4
VH: ventricular hemorrhage. a SAH completely filling at least one cisterna or fissure.
posterior carotid aneurysm (Fig. 4). Ventricular hemorrhage may also point towards the site: predominant findings in V4 are evidence in favor of an inferior cerebellar artery and changes in V3 are supportive of an anterior communicating artery aneurysm.
Figure 3. CT and CT angiogram of the circle of Willis, performed in a patient with sudden-onset headaches and right IIIrd cranial nerve involvement, and abnormal consciousness. A. Basal subarachnoid hemorrhage (arrow head), cisternal and medial cerebro-temporal hematoma (arrow), ventricular hemorrhage visible in V4 and hydrocephalus with dilation of the left temporal horn. B. Projection of the circle of Willis (in red), and predominant site of blood (orange circle), a localizing sign for investigation of the cause. C. Confirmation of the suspected aneurysmal cause: ruptured aneurysm of the infundibulum of the right posterior cerebral artery (arrow).
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Figure 4. Axial cerebral CT (A, B, C) and CT angiogram of the circle of Willis (D) with sagittal MIP reconstruction, centered on the terminal right carotid artery. Acute right pan-hemispheric subdural hematoma with subarachnoid hemorrhage in the right motor cortex sulcus. Assessment of the cause shows a right posterior carotid aneurysm which has ruptured and is responsible for the subdural hematoma and subarachnoid hemorrhage.
Are sulchal SAHs generally linked to aneurysmal rupture?
Does a negative lumbar puncture always exclude a subarachnoid hemorrhage?
Whereas 85% of non-traumatic SAHs are due to aneurysmal rupture, an SAH which spares the basal cisternae and ventricles and is limited to a few sulci in the cerebral hemisphere or motor cortex fissure, should lead to investigation for an alternative cause. These cases account for 7% of SAH [9—11] and should be considered as a separate entity suggesting a non-aneurysmal cause (Fig. 5): reversibly cerebral vasoconstriction, amyloid angiopathy, reversible posterior encephalopathy, inflammatory cerebral artery disease (including infectious arteritis), coagulopathy, vasculitis, cerebral venous thrombosis affecting the cortical veins and vascular malformations (particularly dural fistulae). In this situation, MRI is useful to diagnose the cause, and should include a minimum of a FLAIR image, a T2* image (chronic microbleeds, hemosiderosis from amyloid angiopathy), time of flight MRA, possibly with gadolinium enhancement (distal arterial stenosis) and a dynamic MRA (arteriovenous shunt).
The sensitivity of CT to detect SAH ranges 93% and 95% in the first 24 hours [12]. A patient presenting with severe headaches and clinical features suspected of being a subarachnoid hemorrhage and who has a normal CT or FLAIR MRI should have a lumbar puncture in order to test for blood degradation products in the cerebrospinal fluid (CSF) [13]. On the other hand, a minimum of 12 hours should be left between the onset of symptoms and performing the lumbar puncture (LP) in order to be able to detect any xanthochromia from molecules produced from red blood cell lysis within the CSF. LP remains the gold standard for detecting SAH if it is performed between 12 hours and 15 days after the initial symptoms. If it is performed too early the LP however may be falsely negative [6].
Is MRI useful if a CT is negative? Cerebral CT without enhancement is the technique of choice for a suspected SAH. If the clinical index of suspicion for
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Figure 5. Causes of subarachnoid sulcal hemorrhage. Subarachnoid sulcal hemorrhages (A, orange box) are investigated by comparison with subarachnoid hemorrhages affecting the basal cisternae (A, white box), specific causes and other circle of Willis aneurysms. Sulcal FLAIR hyperintensity showing subarachnoid hemorrhage (A). The different causes which may be looked for: a mycotic aneurysm (B), primary angiitis (C), or secondary angiitis in view of the irregularities in diameter of the arterial branches, a Dural fistula (D), reversible posterior encephalopathy, in view of the bilateral parenchymal FLAIR hypertintensities, predominantly posterior (E), amyloid angiopathy (F) and cortical venous thrombosis (G).
an SAH is high when a CT is negative, it is recommended that: • a CT angiogram of the circle of Willis be performed in order to investigate for an intracranial aneurysm; • a LP be performed; • a MRI may be indicated.
• breach of the blood-brain barrier in ischemic disease or a reperfusion syndromes after treatment of tight carotid stenoses [18]; • gadolinium-chelate or iodinated contrast material injection within 24 hours before the MRI [19]: diffuse FLAIR hyperintensities are due to contrast medium spreading into the cerebrospinal fluid.
FLAIR imaging is more sensitive than CT to detect an SAH, particularly if it is small and carried out immediately after the onset of headache, but particularly within the first 48 hours [14,15]. The sensitivity of FLAIR in detecting SAH within 48 hours is 99%, dropping to 33% beyond 5 days. On the other hand, combining FLAIR with T2*-weighted imaging can achieve a sensitivity of 99% in the first 15 days after the onset of symptoms. More recently, double inversion recovery (DAR) 3D sequences have detected SAH 15 days after the initial symptoms [16].
Artefacts can also produce a hyperintensity in the subarachnoid spaces: • CSF flow artefacts: 2D FLAIR images are sensitive to CSF pulsatility artefacts, showing hyperintensities on FLAIR images usually located in the prepontine areas. Defective annulation of the fluid image is due to movement spins. Optimized 2D FLAIR images and particularly now, 3D FLAIR images, can circumvent these artefacts [20,21]; • metal artefacts: artefacts present on both 2D and 3D images due to metal materials (dental materials, etc.) may cause hypertintensities on FLAIR images, particularly in the posterior fossa. Although usually these artefacts do not raise any diagnostic problem, they may hinder interpretation as they mask important areas of cerebrospinal circulation.
Do all FLAIR hyperintensities in the subarachnoid spaces represent blood? A FLAIR hyperintensity in the subarachnoid spaces does not always represent blood. The other possible causes are (Fig. 6): • intubated and ventilated patients: if oxygen saturation is close to 100% a FLAIR hyperintensity may be seen in the cortical sulchi and basal cisternae [17]; • leptomeningeal disease (infectious or carcinomatous meningitis): the rich cell content makes it impossible to achieve effective CSF saturation on FLAIR imaging;
Does a normal CT angiogram (or MRI angiogram) exclude an intracranial aneurysm? CT angiography of the circle of Willis has a sensitivity of 98% to detect intracranial aneurysms, particularly because of its excellent spatial resolution, which is less than 1 mm [22—25].
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Figure 6. Pitfalls in the subarachnoid spaces on FLAIR imaging: hypertintensities not representing subarachnoid hemorrhage. FLAIR axial views (A, B, D) and FLAIR volume view (C). Prepontine cerebrospinal fluid flow artefact (A); FLAIR hyperintensity in the subarachnoid spaces due to diffusion of iodinated contrast medium 12 hours after arteriography (B); metal artefacts (C); FLAIR hyperintensity in the subarachnoid spaces in the context of infectious lepto-meningitis (D).
On the other hand, like any CT technique, artefacts due to structures at the base of the cranium may hinder interpretation and explain the reduced sensitivity of CT angiography to detect aneurysms under 3 mm in size in segments C1 and C2 of the internal carotid arteries. Dual energy CT reduces the disadvantage of the proximity of bone and vascular structures [26]. The sensitivity of time of flight MRI angiography (MRA) of the circle of Willis depends mostly on the sequence parameters and therefore on the acquisition time. At 3 Tesla, its sensitivity and specificity to detect aneurysms under 5 mm in size are 98 and 94% respectively [27] for a 9-minute sequence. Results are better with 3 Tesla MRI than with 1.5 Tesla MRI because of the higher spatial resolution. False positive results mostly involve perforating arteries from the infundibular region. Because of its acquisition time, MRA is not the first line investigation for the initial assessment of SAH, particularly because of the risk of movement artefacts. It is, however, the recommended investigation for planned screening for an intracranial aneurysm [28—31].
What should I consider with a cisternal SAH and negative CT angiogram? Two situations should be considered with a cisternal SAH and negative CT angiogram.
An arterial abnormality is present but has not been detected Small intracranial aneurysms in the posterior circulation may be difficult to detect. A small aneurysm may not be seen in some MIP projections because of superimposition of the aneurysm over a normal branch of the circle of Willis. Vessel by vessel analysis assisted by volume rendering is a useful aid to detecting an aneurysm [32]. The other possibility is that the aneurysm has thrombosed when it has ruptured or that the patient has a ‘‘blister’’ type of aneurysm. This shape of aneurysm represents local intracranial dissection without an individually identifiable sac. In this case, a local irregularity of the wall should be looked for, particularly next to the subarachnoid spaces, where the hemorrhage is greatest, and in the walls of the C1 and V4 arterial segments. An additional possibility is a dissecting intercranial arterial abnormality, particularly in the segment V4 of the vertical arteries. Intracranial dissections [33], mostly those affecting the posterior circulation, are known to be complicated by subarachnoid hemorrhage and are responsible for 5% of the causes of SAH [34]. The thinner arterial wall and a particular lack of external elastic limiting layer predisposes to wall rupture causing an SAH. It is important to recognize intracranial dissection as it requires specific treatment.
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Subarachnoid hemorrhage in ten questions The diagnosis is suspected from irregularity of the arterial lumen. On 3 Tesla MRI a hematoma can be seen using 3D T1-weighted FSE sequences [35] in 61% of cases [36]. Combining this with T2* imaging [37], and particularly magnetic susceptibility images with phase maps can be used to identify the hematoma and differentiate it from possible arterial calcifications [38].
7 this type of SAH is far better than for SAH due to aneurysms. Most groups perform a second non-invasive investigation into the cause, usually a few weeks after the initial event.
No arterial abnormality is present
If the assessment of an SAH shows several aneurysms to be present, how do I know which one has bled?
In this case a perimesencephalic hemorrhage may be involved. Perimesencephalic hemorrhage SAH account for 5 to 10% of non-traumatic SAH [39] and are due to venous bleeding causing subarachnoid hemorrhage located in the interpeduncular and peripontine cisternae. The bleeding may extend, but only to a limited extent, to the supracellar cisternae and the basal portions of the motor cortex or interhemispheric sulchi. A thin blood level may also be seen in the occipital horns without actual interventricular hemorrhage. Patients generally present in a stable clinical state without abnormalities of consciousness. The diagnosis of perimesancephalic hemorrhage is based on the clinical and radiological criteria described above and on the absence of an aneurysmal structure seen on CT angiography of the circle of Willis and on cerebral arteriography. The initial clinical features, outcome and prognosis of
Multiple intracranial aneurysms are present in 15 to 20% of cases [23]. If several aneurysms are present on the assessment of an SAH it is important to direct treatment towards the aneurysm which has ruptured before considering treating the other aneurysms. Differential distributions of the SAH may point towards the aneurysm which has ruptured, although this is insufficient to draw a conclusion. An irregular, scalloped ‘‘blister-like’’ appearance of the aneurysm wall is also a factor which suggests fissuring or rupture of the aneurysm. Finally, circumferential enhancement of an aneurysm wall seen on 3 Tesla MRI 3D T1-weighted FSE sequences with gadolinium enhancement is believed to be a sign in favor of unstable aneurysms, which are seen more often in those which have ruptured [40—43] than in the wall of aneurysms which have not ruptured but are found in the same patient (Fig. 7).
Figure 7. Which aneurysm has bled? Axial FLAIR cerebral MRI (A, B); 3D time of flight MRI angiogram of the circle of Willis with coronal MIP reconstructions of the vertebrae basilar artery (C) and carotid arteries (D); 3D T1-weighted fast spin echo view after gadolinium-chelate administration; coronal (E) and sagittal sections passing through the left motor cortex aneurysm (F). The right motor cortex aneurysm (G). Oblique coronal views passing though the right M1 segment (H) and basilar trunk (I). The investigation shows a subarachnoid hemorrhage in the prepontine region and left motor cortex sulcus (A, B). Vascular examination shows 4 aneurysms (right and left motor cortex, right M1 and superior cerebella). One aneurysm shows wall enhancement: the left motor cortex aneurysm (F), providing additional evidence in favor of this having ruptured.
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What are the three vascular diagnoses to consider in sudden-onset headache in which no SAH is found on a cerebral CT? With acute headaches, a cerebral CT should be performed urgently to confirm the diagnosis of SAH. If the cerebral CT does not show intracranial hemorrhage and clinical symptoms are highly suggestive, the following possibilities should be considered: An intracranial aneurysm is present. CT angiography has to be performed in order not to miss a prerupture state. Dissection of the cervico-encephalic arteries, which may occasionally only present with headaches. It is therefore important to examine all of the supra-aortic arterial trunks to investigate for a non-aneurysmal cause. Thirdly, reversible vasoconstriction syndromes, which are clinically similar to the headaches due to ruptured aneurysm, presentation of which includes sudden-onset intense pain. Irregularities in the diameter of arteries in the circle of Willis must also be screened for. Take-home messages • 85% of subarachnoid hemorrhages are due to an aneurysm. • A cerebral CT without enhancement is recommended for acute (less than 24 hours old) sudden-onset headaches, looking for subarachnoid hemorrhage (grade A recommendation). • If the CT is positive, or a high index suspicion of a ruptured aneurysm is present with a negative CT, a CT angiogram of the circle of Willis is indicated in order to look for an intracranial aneurysm. • Subarachnoid hemorrhage in a sulcus should be investigated for a non-aneurysmal cause. • Cerebral MRIs indicate a second-line. This is: ◦ more sensitive in detecting blood, particularly after 48 hours, when the sensitivity of CT falls, ◦ can be used to look for non-aneurysmal causes of an SAH.
Figure 8. CT scan without injection (A), axial section through the midbrain. CT angiography of the polygon of Willis rebuilt in MIP, allowing to detect the intracranial vertebrobasilar axis in coronal view (B), the starting of the right PICA in sagittal view (C), of the left PICA (D) in axial view, the axes middle of the cerebral arteries and the anterior communicating in axial view (E), the anterior cerebral arteries in sagittal view (F).
B What do you think about the reconstructions of the circle of Willis CT angiogram? 1. These can be used to study each artery in the circle of Willis, from the PICA to the pericallosal arteries. 2. It shows a right motor cortex aneurysm. 3. It does not show an intracranial aneurysm. 4. The clinical and radiological criteria are compatible with a perimesencephalic hemorrhage.
Answers Question A: answers 1 and 3 are true. Question B: answers 1, 3 and 4 are true.
Disclosure of interest Clinical case A 45-year-old male patient presents with sudden-onset headaches on awakening. His Glasgow score is 15 and he has no signs of neurological deficit. A cerebral CT and angiogram of the circle of Willis are performed (MIP reconstructions in the different vascular planes (Fig. 8).
Questions A What do you think about the CT that was performed? 1. This shows a hemorrhage in the basal cisternae, and particularly an interperduncular hemorrhage. 2. It shows a ventricular hemorrhage visible on the image shown. 3. It shows early dilatation of the temporal horns. 4. It is normal.
The authors declare that they have no conflicts of interest concerning this article.
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CONTINUING EDUCATION PROGRAM: FOCUS. . .
Subarachnoid hemorrhage in ten questions M. Edjlali a,b,∗, C. Rodriguez-Régent a, J. Hodel b, R. Aboukais c, D. Trystram a, J.-P. Pruvo b, J.-F. Meder a, C. Oppenheim a, J.-P. Lejeune c, X. Leclerc b, O. Naggara a a
Inserm UMR 894, Department of Neuroradiolgy, Faculty of Medicine Paris Descartes University, Pyschiatry and Neurosciences Centers, Sainte-Anne Hospital, Sorbonne Paris Cité, 1, rue Cabanis, 75014 Paris, France b Department of Neuroradiology, Lille Nord de France University, Roger Salengro Hospital, Lille University Hospitals, avenue Émile-Laine, 59037 Lille cedex, France c Department of Neurosurgery, Lille Nord de France University, Roger Salengro Hospital, Lille University Hospitals, avenue Émile-Laine, 59037 Lille cedex, France
KEYWORDS Hemorrhage; Intracranial aneurysm; CT; MRI
Abstract Traumatic subarachnoid hemorrhage (SAH) has an annual incidence of 9 per 100 000 people. It is a rare but serious event, with an estimated mortality rate of 40% within the first 48 hours. In 85% of cases, it is due to rupture of an intracranial aneurysm. In the early phase, during the first 24 hours, cerebral CT, combined with intracranial CT angiography is recommended to make a positive diagnosis of SAH, to identify the cause and to investigate for an intracranial aneurysm. Cerebral MRI may be proposed if the patient’s clinical condition allows it. FLAIR imaging is more sensitive than CT to demonstrate a subarachnoid hemorrhage and offers greater degrees of sensitivity for the diagnosis of restricted subarachnoid hemorrhage in cortical sulcus. A lumbar puncture should be performed if these investigations are normal while clinical suspicion is high. © 2015 Éditions franc ¸aises de radiologie. Published by Elsevier Masson SAS. All rights reserved.
Subarachnoid hemorrhage (SAH) is defined as blood in the cerebrospinal fluid contained in the basal cisternae and the sub-arachnoid space of the cerebral hemispheres, contained between the arachnoid mater and the pia mater. The most common cause is head injury. Apart from this cause, SAH accounts for 5 to 10% of cerebrovascular accidents and has a high mortality rate, which is estimated to be
∗ Corresponding author. Inserm UMR 894, Department of Neuroradiolgy, Faculty of Medicine Paris Descartes University, Pyschiatry and Neurosciences Centers, Sainte-Anne Hospital, Sorbonne Paris Cité, 1, rue Cabanis, 75014 Paris, France. E-mail address: [email protected] (M. Edjlali).
http://dx.doi.org/10.1016/j.diii.2015.06.003 2211-5684/© 2015 Éditions franc ¸aises de radiologie. Published by Elsevier Masson SAS. All rights reserved.
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between 40 and 50% [1,2]. By far the most common cause of SAH apart from trauma is intracranial aneurysm rupture (85% of non-traumatic causes) [3]. If SAH is suspected, cerebral imaging should be performed urgently to confirm the diagnosis, identify any complications and investigate its cause. We propose you here to develop the theme of SAH through ten questions. We will not consider the complications of rebleeding and vasospasm in this article.
When a patient presents with a sudden-onset headache, is CT an appropriate investigation? Unenhanced cerebral CT is recommended for acute headaches (less than 24 hours old), which are sudden in onset, to investigate for a subarachnoid hemorrhage (SAH) (grade A guideline, guide to the correct use of medical imaging examinations). The clinical features of the headache are fundamental. A SAH should be suspected in the case of a suddenonset headache of maximum intensity from the outset and described as a ‘‘thunderclap in a clear sky’’. This may be combined with meningism without fever or reduced consciousness level. An urgent CT should be performed and enables a diagnosis of SAH to be made if an unenhanced hyperdensity is present in the subarachnoid spaces, which usually involves the basal cisternae, inter-hemispheric sulci and lateral sulci [4]. When it is performed during the first 24 hours, CT has a sensitivity of 95% [5]. The sensitivity of CT depends mostly on the extent of the SAH but also on hemoglobin concentration and falls with the time between the initial headache and time when the scan is performed. After 7 days, therefore, CT is positive in only 50% of cases in SAH. Apart from a positive diagnosis of SAH, the initial CT examination can detect the early complications of
hydrocephalus, intraparenchymal hematoma with space occupying effect and ventricular hemorrhage (Fig. 1). Hydrocephalus which begins with dilatation of the temporal horns, and a compressive intra-parenchymal hematoma are important to report as these are life-threatening and require immediate neurosurgery with an external ventricular shunt, or evacuation of the hematoma before treatment for the cause of the SAH [6]. Using the modified Fisher scale [7] (Fig. 2, Table 1), CT is also of prognostic value in terms of the secondary development of vasospasm as the scale is a predictive indicator for vasospasm. Whilst sudden-onset headache is an indication for CT, an unenhanced investigation is not sufficient. Sudden-onset headaches may be due to an aneurysm which has not ruptured. In this case, the term sentinel headaches is used, which describes a state of pre-rupture or fissuring of the aneurysm. It is therefore recommended that for suddenonset headaches, even without SAH, imaging of the circle of Willis be performed to look for an intracranial aneurysm.
Are there signs which help to localize the source of the bleeding? Neurological signs A IIIrd cranial nerve palsy on a background of sudden-onset headache is a clinical localizing sign and indicates pressure on the nerve, either directly by the aneurysm or by the hematomas secondary to rupture of the aneurysm. The aneurysm itself can then be looked for the posterior wall of the ending of the internal carotid artery, close to the origin of the posterior communicating artery (Fig. 3), or less commonly, developing at the origin of the superior cerebellar artery. On the other hand, features of pyramidal irritation and paralysis of the VIth cranial nerve are of no localizing value.
Figure 1. Axial cerebral CT without enhancement (A) and angiogram of the arterial circle at the base of the brain (B) on MIP reconstructions centered on the circle of Willis. Positive diagnosis of subarachnoid hemorrhage (A): unenhanced hyperdensity in the subarachnoid spaces (arrow) affecting the basal cisternae, motor cortex sulchi and interhemispheric fissure without flooding of the ventricles. Diagnosis of an early complication: early hydrocephalus with dilation of the temporal horns (star). Coexistent preretinal hemmorage (Terson Syndrome, thick arrow). Diagnosis of cause (B): ruptured terminal basilar artery aneurysm (arrow head).
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Figure 2. Cerebral CT images without enhancement illustrating different grades of the Fisher classification. A. Grade 0: no SAH, no ventricular hemorrhage. B. Grade 1: minimal SAH, no ventricular hemorrhage in the 2 lateral ventricles. C. Grade 3: large SAH. No ventricular hemorrhage in the two lateral ventricles. D. Grade 4: large SAH ventricular hemorrhage in both lateral ventricles.
Radiological signs associated with blood distribution The distribution of the SAH and presence of any hematoma help localize the aneurysm responsible for the bleeding. An SAH predominantly in the anterior part of the interhemispheric cisterna and the suprasellar cisternae and/or an interhemispheric hematoma suggest an anterior communicating artery aneurysm. An SAH predominantly in the motor cortex sulcus or a temporopolar hematoma should trigger investigation for an ipsilateral middle cerebral artery aneurysm. An isolated lenticular hematoma may occur as a result of rupture of an end carotid aneurysm. An SAH predominantly in the basal cisternae next to the cerebellopontine angle cisternae with asymmetrical distribution suggests a ruptured postero-inferior cerebellar artery (PICA) aneurysm [4,8]. An acute subdural hematoma without a background of injury should trigger investigation for a
Table 1
Modified Fisher’s scale, 2001.
Grade
Criteria
0
No subarachnoid hemorrhage (SAH) or ventricular hemorrhage (VH) Minimal SAH, no HV in the 2 lateral ventricles Minimal SAH, HV in the 2 lateral ventricles Large SAHa , no VH in the 2 lateral ventricles Large SAHa , VH in the 2 lateral ventricles
1 2 3 4
VH: ventricular hemorrhage. a SAH completely filling at least one cisterna or fissure.
posterior carotid aneurysm (Fig. 4). Ventricular hemorrhage may also point towards the site: predominant findings in V4 are evidence in favor of an inferior cerebellar artery and changes in V3 are supportive of an anterior communicating artery aneurysm.
Figure 3. CT and CT angiogram of the circle of Willis, performed in a patient with sudden-onset headaches and right IIIrd cranial nerve involvement, and abnormal consciousness. A. Basal subarachnoid hemorrhage (arrow head), cisternal and medial cerebro-temporal hematoma (arrow), ventricular hemorrhage visible in V4 and hydrocephalus with dilation of the left temporal horn. B. Projection of the circle of Willis (in red), and predominant site of blood (orange circle), a localizing sign for investigation of the cause. C. Confirmation of the suspected aneurysmal cause: ruptured aneurysm of the infundibulum of the right posterior cerebral artery (arrow).
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Figure 4. Axial cerebral CT (A, B, C) and CT angiogram of the circle of Willis (D) with sagittal MIP reconstruction, centered on the terminal right carotid artery. Acute right pan-hemispheric subdural hematoma with subarachnoid hemorrhage in the right motor cortex sulcus. Assessment of the cause shows a right posterior carotid aneurysm which has ruptured and is responsible for the subdural hematoma and subarachnoid hemorrhage.
Are sulchal SAHs generally linked to aneurysmal rupture?
Does a negative lumbar puncture always exclude a subarachnoid hemorrhage?
Whereas 85% of non-traumatic SAHs are due to aneurysmal rupture, an SAH which spares the basal cisternae and ventricles and is limited to a few sulci in the cerebral hemisphere or motor cortex fissure, should lead to investigation for an alternative cause. These cases account for 7% of SAH [9—11] and should be considered as a separate entity suggesting a non-aneurysmal cause (Fig. 5): reversibly cerebral vasoconstriction, amyloid angiopathy, reversible posterior encephalopathy, inflammatory cerebral artery disease (including infectious arteritis), coagulopathy, vasculitis, cerebral venous thrombosis affecting the cortical veins and vascular malformations (particularly dural fistulae). In this situation, MRI is useful to diagnose the cause, and should include a minimum of a FLAIR image, a T2* image (chronic microbleeds, hemosiderosis from amyloid angiopathy), time of flight MRA, possibly with gadolinium enhancement (distal arterial stenosis) and a dynamic MRA (arteriovenous shunt).
The sensitivity of CT to detect SAH ranges 93% and 95% in the first 24 hours [12]. A patient presenting with severe headaches and clinical features suspected of being a subarachnoid hemorrhage and who has a normal CT or FLAIR MRI should have a lumbar puncture in order to test for blood degradation products in the cerebrospinal fluid (CSF) [13]. On the other hand, a minimum of 12 hours should be left between the onset of symptoms and performing the lumbar puncture (LP) in order to be able to detect any xanthochromia from molecules produced from red blood cell lysis within the CSF. LP remains the gold standard for detecting SAH if it is performed between 12 hours and 15 days after the initial symptoms. If it is performed too early the LP however may be falsely negative [6].
Is MRI useful if a CT is negative? Cerebral CT without enhancement is the technique of choice for a suspected SAH. If the clinical index of suspicion for
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Figure 5. Causes of subarachnoid sulcal hemorrhage. Subarachnoid sulcal hemorrhages (A, orange box) are investigated by comparison with subarachnoid hemorrhages affecting the basal cisternae (A, white box), specific causes and other circle of Willis aneurysms. Sulcal FLAIR hyperintensity showing subarachnoid hemorrhage (A). The different causes which may be looked for: a mycotic aneurysm (B), primary angiitis (C), or secondary angiitis in view of the irregularities in diameter of the arterial branches, a Dural fistula (D), reversible posterior encephalopathy, in view of the bilateral parenchymal FLAIR hypertintensities, predominantly posterior (E), amyloid angiopathy (F) and cortical venous thrombosis (G).
an SAH is high when a CT is negative, it is recommended that: • a CT angiogram of the circle of Willis be performed in order to investigate for an intracranial aneurysm; • a LP be performed; • a MRI may be indicated.
• breach of the blood-brain barrier in ischemic disease or a reperfusion syndromes after treatment of tight carotid stenoses [18]; • gadolinium-chelate or iodinated contrast material injection within 24 hours before the MRI [19]: diffuse FLAIR hyperintensities are due to contrast medium spreading into the cerebrospinal fluid.
FLAIR imaging is more sensitive than CT to detect an SAH, particularly if it is small and carried out immediately after the onset of headache, but particularly within the first 48 hours [14,15]. The sensitivity of FLAIR in detecting SAH within 48 hours is 99%, dropping to 33% beyond 5 days. On the other hand, combining FLAIR with T2*-weighted imaging can achieve a sensitivity of 99% in the first 15 days after the onset of symptoms. More recently, double inversion recovery (DAR) 3D sequences have detected SAH 15 days after the initial symptoms [16].
Artefacts can also produce a hyperintensity in the subarachnoid spaces: • CSF flow artefacts: 2D FLAIR images are sensitive to CSF pulsatility artefacts, showing hyperintensities on FLAIR images usually located in the prepontine areas. Defective annulation of the fluid image is due to movement spins. Optimized 2D FLAIR images and particularly now, 3D FLAIR images, can circumvent these artefacts [20,21]; • metal artefacts: artefacts present on both 2D and 3D images due to metal materials (dental materials, etc.) may cause hypertintensities on FLAIR images, particularly in the posterior fossa. Although usually these artefacts do not raise any diagnostic problem, they may hinder interpretation as they mask important areas of cerebrospinal circulation.
Do all FLAIR hyperintensities in the subarachnoid spaces represent blood? A FLAIR hyperintensity in the subarachnoid spaces does not always represent blood. The other possible causes are (Fig. 6): • intubated and ventilated patients: if oxygen saturation is close to 100% a FLAIR hyperintensity may be seen in the cortical sulchi and basal cisternae [17]; • leptomeningeal disease (infectious or carcinomatous meningitis): the rich cell content makes it impossible to achieve effective CSF saturation on FLAIR imaging;
Does a normal CT angiogram (or MRI angiogram) exclude an intracranial aneurysm? CT angiography of the circle of Willis has a sensitivity of 98% to detect intracranial aneurysms, particularly because of its excellent spatial resolution, which is less than 1 mm [22—25].
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Figure 6. Pitfalls in the subarachnoid spaces on FLAIR imaging: hypertintensities not representing subarachnoid hemorrhage. FLAIR axial views (A, B, D) and FLAIR volume view (C). Prepontine cerebrospinal fluid flow artefact (A); FLAIR hyperintensity in the subarachnoid spaces due to diffusion of iodinated contrast medium 12 hours after arteriography (B); metal artefacts (C); FLAIR hyperintensity in the subarachnoid spaces in the context of infectious lepto-meningitis (D).
On the other hand, like any CT technique, artefacts due to structures at the base of the cranium may hinder interpretation and explain the reduced sensitivity of CT angiography to detect aneurysms under 3 mm in size in segments C1 and C2 of the internal carotid arteries. Dual energy CT reduces the disadvantage of the proximity of bone and vascular structures [26]. The sensitivity of time of flight MRI angiography (MRA) of the circle of Willis depends mostly on the sequence parameters and therefore on the acquisition time. At 3 Tesla, its sensitivity and specificity to detect aneurysms under 5 mm in size are 98 and 94% respectively [27] for a 9-minute sequence. Results are better with 3 Tesla MRI than with 1.5 Tesla MRI because of the higher spatial resolution. False positive results mostly involve perforating arteries from the infundibular region. Because of its acquisition time, MRA is not the first line investigation for the initial assessment of SAH, particularly because of the risk of movement artefacts. It is, however, the recommended investigation for planned screening for an intracranial aneurysm [28—31].
What should I consider with a cisternal SAH and negative CT angiogram? Two situations should be considered with a cisternal SAH and negative CT angiogram.
An arterial abnormality is present but has not been detected Small intracranial aneurysms in the posterior circulation may be difficult to detect. A small aneurysm may not be seen in some MIP projections because of superimposition of the aneurysm over a normal branch of the circle of Willis. Vessel by vessel analysis assisted by volume rendering is a useful aid to detecting an aneurysm [32]. The other possibility is that the aneurysm has thrombosed when it has ruptured or that the patient has a ‘‘blister’’ type of aneurysm. This shape of aneurysm represents local intracranial dissection without an individually identifiable sac. In this case, a local irregularity of the wall should be looked for, particularly next to the subarachnoid spaces, where the hemorrhage is greatest, and in the walls of the C1 and V4 arterial segments. An additional possibility is a dissecting intercranial arterial abnormality, particularly in the segment V4 of the vertical arteries. Intracranial dissections [33], mostly those affecting the posterior circulation, are known to be complicated by subarachnoid hemorrhage and are responsible for 5% of the causes of SAH [34]. The thinner arterial wall and a particular lack of external elastic limiting layer predisposes to wall rupture causing an SAH. It is important to recognize intracranial dissection as it requires specific treatment.
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Subarachnoid hemorrhage in ten questions The diagnosis is suspected from irregularity of the arterial lumen. On 3 Tesla MRI a hematoma can be seen using 3D T1-weighted FSE sequences [35] in 61% of cases [36]. Combining this with T2* imaging [37], and particularly magnetic susceptibility images with phase maps can be used to identify the hematoma and differentiate it from possible arterial calcifications [38].
7 this type of SAH is far better than for SAH due to aneurysms. Most groups perform a second non-invasive investigation into the cause, usually a few weeks after the initial event.
No arterial abnormality is present
If the assessment of an SAH shows several aneurysms to be present, how do I know which one has bled?
In this case a perimesencephalic hemorrhage may be involved. Perimesencephalic hemorrhage SAH account for 5 to 10% of non-traumatic SAH [39] and are due to venous bleeding causing subarachnoid hemorrhage located in the interpeduncular and peripontine cisternae. The bleeding may extend, but only to a limited extent, to the supracellar cisternae and the basal portions of the motor cortex or interhemispheric sulchi. A thin blood level may also be seen in the occipital horns without actual interventricular hemorrhage. Patients generally present in a stable clinical state without abnormalities of consciousness. The diagnosis of perimesancephalic hemorrhage is based on the clinical and radiological criteria described above and on the absence of an aneurysmal structure seen on CT angiography of the circle of Willis and on cerebral arteriography. The initial clinical features, outcome and prognosis of
Multiple intracranial aneurysms are present in 15 to 20% of cases [23]. If several aneurysms are present on the assessment of an SAH it is important to direct treatment towards the aneurysm which has ruptured before considering treating the other aneurysms. Differential distributions of the SAH may point towards the aneurysm which has ruptured, although this is insufficient to draw a conclusion. An irregular, scalloped ‘‘blister-like’’ appearance of the aneurysm wall is also a factor which suggests fissuring or rupture of the aneurysm. Finally, circumferential enhancement of an aneurysm wall seen on 3 Tesla MRI 3D T1-weighted FSE sequences with gadolinium enhancement is believed to be a sign in favor of unstable aneurysms, which are seen more often in those which have ruptured [40—43] than in the wall of aneurysms which have not ruptured but are found in the same patient (Fig. 7).
Figure 7. Which aneurysm has bled? Axial FLAIR cerebral MRI (A, B); 3D time of flight MRI angiogram of the circle of Willis with coronal MIP reconstructions of the vertebrae basilar artery (C) and carotid arteries (D); 3D T1-weighted fast spin echo view after gadolinium-chelate administration; coronal (E) and sagittal sections passing through the left motor cortex aneurysm (F). The right motor cortex aneurysm (G). Oblique coronal views passing though the right M1 segment (H) and basilar trunk (I). The investigation shows a subarachnoid hemorrhage in the prepontine region and left motor cortex sulcus (A, B). Vascular examination shows 4 aneurysms (right and left motor cortex, right M1 and superior cerebella). One aneurysm shows wall enhancement: the left motor cortex aneurysm (F), providing additional evidence in favor of this having ruptured.
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What are the three vascular diagnoses to consider in sudden-onset headache in which no SAH is found on a cerebral CT? With acute headaches, a cerebral CT should be performed urgently to confirm the diagnosis of SAH. If the cerebral CT does not show intracranial hemorrhage and clinical symptoms are highly suggestive, the following possibilities should be considered: An intracranial aneurysm is present. CT angiography has to be performed in order not to miss a prerupture state. Dissection of the cervico-encephalic arteries, which may occasionally only present with headaches. It is therefore important to examine all of the supra-aortic arterial trunks to investigate for a non-aneurysmal cause. Thirdly, reversible vasoconstriction syndromes, which are clinically similar to the headaches due to ruptured aneurysm, presentation of which includes sudden-onset intense pain. Irregularities in the diameter of arteries in the circle of Willis must also be screened for. Take-home messages • 85% of subarachnoid hemorrhages are due to an aneurysm. • A cerebral CT without enhancement is recommended for acute (less than 24 hours old) sudden-onset headaches, looking for subarachnoid hemorrhage (grade A recommendation). • If the CT is positive, or a high index suspicion of a ruptured aneurysm is present with a negative CT, a CT angiogram of the circle of Willis is indicated in order to look for an intracranial aneurysm. • Subarachnoid hemorrhage in a sulcus should be investigated for a non-aneurysmal cause. • Cerebral MRIs indicate a second-line. This is: ◦ more sensitive in detecting blood, particularly after 48 hours, when the sensitivity of CT falls, ◦ can be used to look for non-aneurysmal causes of an SAH.
Figure 8. CT scan without injection (A), axial section through the midbrain. CT angiography of the polygon of Willis rebuilt in MIP, allowing to detect the intracranial vertebrobasilar axis in coronal view (B), the starting of the right PICA in sagittal view (C), of the left PICA (D) in axial view, the axes middle of the cerebral arteries and the anterior communicating in axial view (E), the anterior cerebral arteries in sagittal view (F).
B What do you think about the reconstructions of the circle of Willis CT angiogram? 1. These can be used to study each artery in the circle of Willis, from the PICA to the pericallosal arteries. 2. It shows a right motor cortex aneurysm. 3. It does not show an intracranial aneurysm. 4. The clinical and radiological criteria are compatible with a perimesencephalic hemorrhage.
Answers Question A: answers 1 and 3 are true. Question B: answers 1, 3 and 4 are true.
Disclosure of interest Clinical case A 45-year-old male patient presents with sudden-onset headaches on awakening. His Glasgow score is 15 and he has no signs of neurological deficit. A cerebral CT and angiogram of the circle of Willis are performed (MIP reconstructions in the different vascular planes (Fig. 8).
Questions A What do you think about the CT that was performed? 1. This shows a hemorrhage in the basal cisternae, and particularly an interperduncular hemorrhage. 2. It shows a ventricular hemorrhage visible on the image shown. 3. It shows early dilatation of the temporal horns. 4. It is normal.
The authors declare that they have no conflicts of interest concerning this article.
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