Chapter 12 Subarachnoid Hemorrhage

Advances in imaging technology have marked the great milestones in the history of the diagnosis and management of aneurysmal subarachnoid hemorrhage (SAH) and its complications. The development of cerebral angiography allowed in vivo visualization of saccular aneurysms, accomplished for the first time by Egas Moniz in 1933.¹ It was not until 1951 that Ecker and Riemenschneider achieved the first angiographic proof of delayed vasospasm.² Since its introduction in the 1970s, computed tomography (CT) scan has become the most reliable tool for the acute diagnosis of SAH. It did not take long before it was recognized that the amount of blood in the subarachnoid cisterns (Figure 12-1) was highly predictive of the subsequent risk of vasospasm.^3–5 Transcranial Doppler (TCD) later proved valuable for noninvasive screening and monitoring of vasospasm.⁶ More recently, magnetic resonance imaging (MRI) techniques have enhanced our understanding of ischemic damage after SAH⁷ and may represent a valuable tool for the acute diagnosis of ongoing ischemia from vasospasm.⁸ As spiral CT angiograms⁹ and CT perfusion scans¹⁰ move into the scene, we may see another transformation in the management of SAH led by imaging technology in the immediate future.

Figure 12-1 Anatomy of basal cisterns and fissures on computed tomography scan.

Timely and accurate diagnosis of SAH hinges on the use of brain imaging. CT scan remains by far the most widely applied technique. Its sensitivity for the acute diagnosis of SAH exceeds 95%.¹¹ However, CT scan is most reliable early after the bleeding (particularly within the first 24–48 hours) and false-negative results become possible after a few days. Gradient-recall echo T2^* MRI has comparable sensitivity to CT scan for the hyperacute diagnosis of SAH,¹² and fluid-attenuated inversion recovery (FLAIR) MRI has greater sensitivity than CT scan in subacute cases (Figure 12-2).¹³

Figure 12-2 Imaging characteristics of acute subarachnoid hemorrhage on computed tomography scan, fluid-attenuated inversion recovery, and T2^* magnetic resonance imaging.

Currently, the use of MRI is limited because MR technology is often unavailable in the emergency setting, and CT scanning allows faster image acquisition (which becomes an important factor in patients with acute SAH who are neurologically or hemodynamically unstable) and easier visualization of extravasated blood (at least for examiners without extensive radiological training). False-positive diagnoses of SAH (pseudo-SAH) by CT scan may be caused by increased venous congestion, as seen in patients with massive cerebral edema or bilateral subdural hematomas.^14–16

Although it is generally agreed that the amount of subarachnoid blood visualized on CT scan predicts the risk of subsequent vasospasm, there is still debate regarding the best way to quantify this risk. The grading originally proposed by C. M. Fisher et al. is still the most popular (Table 12-1; Figure 12-3).⁵ However, newer visual scales¹⁷ (Table 12-1) and software-based techniques¹⁸ have claimed better sensitivity and specificity. CT scan is also the modality of choice for the prompt diagnosis of hydrocephalus and rebleeding, and it clearly demonstrates the presence of global cerebral edema, a strong predictor of unfavorable outcome.¹⁹

TABLE 12-1 Predicting delayed cerebral ischemia by the appearance of the initial CT scan of the brain: Comparison of the traditional Fisher radiological grading scale and a proposed modification that incorporates the impact of IVH on the risk of vasospasm and delayed ischemic damage

CT, computed tomography; IVH, intraventricular hemorrhage; SAH, subarachnoid hemorrhage.

* Completely filling ≥ 1 cistern or fissure.

Figure 12-3 Illustration of Fisher scale for radiological grading of subarachnoid hemorrhage and estimation of risk of vasospasm.

Conventional cerebral angiography remains the gold standard for the diagnosis of intracranial aneurysms (Figure 12-4).²⁰ Whereas noninvasive angiograms may be sufficient for screening of unruptured intracranial aneurysms, diagnosis of nontraumatic SAH demands the performance of catheter angiography. Newer imaging processing techniques currently allow three-dimensional reconstruction of the aneurysm, which greatly enhances the anatomical definition of the study.²¹ After diagnosis, endovascular coiling may be performed during the same catheterization. Conventional angiography is also considered the gold standard for the diagnosis of vasospasm and enables its treatment with angioplasty or superselective intra-arterial infusion of vasodilators in selected cases.^22,23

Figure 12-4 Examples of aneurysm visualization by digital substraction angiography, computed tomography angiography, and magnetic resonance angiography. Notice the increased anatomical definition achieved with three-dimensional (3D) angiographic reconstruction (particularly with 3D rotational angiography illustrated in panel D).

The role of MRI in the management of SAH and vasospasm continues to grow. Initially it was used to define the extent of delayed ischemic damage with exclusive prognostic purposes. MRI has considerably greater sensitivity than CT scan for the recognition of small foci of subcortical ischemia that commonly occur as sequelae of SAH, predominantly affecting the basal ganglia, claustrum, and frontal white matter.⁷ More recently, diffusion-weighted imaging and perfusion-weighted imaging have started to be employed for the acute detection of cerebral ischemia during the phase of vasospasm.^8,24,25 These techniques may demonstrate hypoperfusion and ischemia even in patients with no definite evidence of vasospasm by either TCD or angiogram, suggesting that mechanisms other than luminal narrowing of large intracranial vessels may be responsible.

CT-based protocols combining CT perfusion with spiral CT angiograms may constitute a valuable alternative to the current practice of TCD screening and angiographic confirmation of vasospasm. These CT studies may provide direct evidence of the presence and magnitude of hypoperfusion and correlate that information with a fast and noninvasive depiction of the state of the major intracranial vessels.8–10,²⁶ Further research to confirm the validity of these CT-based protocols is necessary to determine their optimal application.

As our understanding of the complex pathophysiological underpinnings of vasospasm improves, it appears increasingly evident that ischemia after SAH may be caused by disruption of microcirculatory function.^20,27 New imaging modalities capable of providing dynamic information on the status of the microcirculation are likely to be the best candidates to forge the next revolution in the care of patients with SAH.

Case Vignette

A 46-year-old woman developed thunderclap headache immediately followed by transient loss of consciousness associated with tonic posturing deemed suspicious for a seizure. She was emergently transferred to a local hospital. On initial examination, her Glasgow coma scale sum score was 13. She did not have cranial nerve deficits or hemiparesis (WFNS grade II). Her CT scan of the brain showed extensive SAH with a thick cisternal clot in the interpeduncular cistern (Fisher grade 3; Figure 12-5, upper row). There was also incipient hydrocephalus and a small left parasagittal frontal hematoma. Digital substraction angiography (DSA) disclosed a saccular aneurysm in the anterior communicating artery region, arising from the left A1 segment (Figure 12-5, lower row, left panel). The anatomical configuration of the aneurysm was much better visualized on the three-dimensional reconstructed images (Figure 12-5, lower row, left panel). The ruptured aneurysm was successfully coiled on the second day after the bleeding. Four days later, the patient developed some deterioration in the level of consciousness associated with doubling of the mean blood flow velocities in the left terminal carotid segment and the left A1 and M1 segments; similar but less severe changes were present on the right anterior circulation. The diagnosis of diffuse, severe vasospasm was confirmed angiographically. The patient improved rapidly with hemodynamic augmentation therapy and had no other complications. At 3 months, she still had mild neurobehavioral problems and occasional headaches. Six months later, she was feeling well and had returned to work, although she reported decreased endurance.

Figure 12-5 Upper row: computed tomography scan of the brain showing Fisher grade 3 subarachnoid hemorrhage with extensive and thick clot in the subarachnoid cisterns. Note focal clot in the interpeduncular cistern toward the left (arrowhead), early hydrocephalus signaled by dilatation of the temporal horns of the lateral ventricles (solid arrows), and left parasagittal intraparenchymal hemorrhage (curved arrow). Lower row: digital substraction angiography (left panel) and three-dimensional (3D)-reconstructed images showing a saccular aneurysm arising from the left A1 segment (open arrows). Notice the markedly increased anatomical definition provided by the 3D images.

Figure 12-6 Correlation of localized clot on CT scan and aneurysm location.

Figure 12-7 Example of extensive subarachnoid hemorrhage and intraventricular hemorrhage (“casted ventricles”).

CAUSES OF EARLY DETERIORATION: REBLEEDING AND HYDROCEPHALUS

♦ Rapid decline in level of consciousness shortly after SAH should raise suspicion for rebleeding or hydrocephalus. Rebleeding commonly presents with sudden unresponsiveness associated with severe tachycardia, hypertension, and changes in heart rhythm; the clinical scenario is one of medical emergency (Figure 12-8).

♦ Meanwhile, hydrocephalus typically manifests less dramatically. Patients drift into coma, pupils become dilatated and lose light reactivity, and bradycardia is often the only hemodynamic feature. This deceivingly “calm” presentation should not mislead the clinician because prompt recognition and treatment of hydrocephalus is crucial to avoid irreparable neurological injury.

♦ CT scan provides fast confirmation of the diagnosis of hydrocephalus and reliably excludes rebleeding.

♦ Early hydrocephalus can be massive and lead to raised intracranial pressure and diminished level of consciousness (Figure 12-9).

♦ Alternatively, hydrocephalus may present more subtly, manifested only by mild dilatation of the temporal horns (“boomerang signs”) and unimpressive cognitive impairment and degree of alertness (Figure 12-10).

♦ Presence of intraventricular blood is the strongest predictor of hydrocephalus after SAH.^32,33 However, thick cisternal clots have also been associated with increased risk of developing hydrocephalus.³²

♦ Hydrocephalus after SAH may be obstructive or communicating. CT scan allows distinction between the two types on the basis of the size of the third and fourth ventricles (i.e., all similarly dilatated in communicating cases).

♦ Massive hematocephalus is associated with high acute neurological morbidity and poor functional outcome.³⁴ Intraventricular thrombolysis,³⁵ intraoperative ventricular irrigation, and endoscopic clot removal may be useful adjuncts to external drainage through a ventriculostomy catheter to accelerate the clearing of intraventricular blood and reduce the need for ventricular shunting. The contention that these practices might reduce the risk of vasospasm is unproved.

♦ Before removing a ventriculostomy catheter, it is always advisable to obtain radiological confirmation of stable ventricular size several hours after clamping the catheter.

♦ Chronic hydrocephalus requiring ventricular shunting complicates 15% of cases of aneurysmal SAH. The incidence of chronic hydrocephalus is higher in patients with vertebrobasilar aenurysms.³⁶

Figure 12-8 A 45-year-old woman presented to the emergency department after having a thunderclap headache without associated neurological symptoms or deficits. She was lucid, and the only relevant findings on examination were photophobia and neck stiffness. Computed tomography (CT) scan showed subarachnoid hemorrhage (SAH) in the basal cisterns and right Sylvian fissure (upper row, arrowheads). A few hours after admission, she suddenly became unconscious and developed acute extensor posturing. Repeat CT scan (lower row, left panel) demonstrated more extensive SAH (arrows) and a new right frontal intraparenchymal hematoma (curved arrow) as a result of rebleeding from the aneurysm. The patient was emergently intubated and taken to the angiography suite were digital substraction angiography disclosed a right middle cerebral artery aneurysm (lower row, right panel, solid arrow). The aneurysm was successfully treated, and the patient eventually regained consciousness. She subsequently developed vasospasm, but treatment averted major ischemic damage. She achieved a fair functional recovery.

Figure 12-9 A 54-year-old man presented with subarachnoid hemorrhage and massive early hydrocephalus. Note marked dilatation of lateral and third ventricles associated with intraventricular hemorrhage in the posterior horn of the right (and to a much lesser degree of the left) lateral ventricle. The patient was initially treated with external ventricular drainage. Angiogram showed a large left vertebrobasilar saccular aneurysm (arrow), which was successfully coiled (arrowhead). Attempts to remove the ventriculostomy catheter were unsuccessful because of persistent symptomatic hydrocephalus. Consequently, he required ventriculoperitoneal shunt placement.

Figure 12-10 Example of incipient early hydrocephalus. Notice enlargement of temporal horns (arrows) without major dilatation of the rest of the lateral ventricles.

GLOBAL CEREBRAL EDEMA

♦ Evidence of global cerebral edema on the initial CT scan is an independent predictor of increased mortality and poor functional recovery (Figure 12-11).¹⁹

♦ Its clinical correlate is sudden loss of consciousness, likely resulting from transient cerebral circulatory arrest due to massive increase in intracranial pressure.³⁷

♦ A delayed form of cerebral edema may occur several days after the ictus, especially in severe cases requiring treatment with vasopressors.¹⁹

Figure 12-11 A case of fatal subarachnoid hemorrhage illustrating the radiological features of global cerebral edema on computed tomography scan. Notice effacement of sulci in the hemispheric convexities, effacement of basal cisterns, and slit-like ventricles. The arrow indicates a subhyaloid hemorrhage (Terson’s sign) in the back of the right eye.

CEREBRAL VASOSPASM

♦ Cerebral vasospasm is the main cause of additional neurological morbidity and functional sequelae in patients surviving the initial effects of the hemorrhage (Figure 12-12).²⁰

♦ The risk of vasospasm correlates with the amount of blood in the subarachnoid cisterns.^5,17,38 Presence of intraventricular hemorrhage may also increase the incidence of vasospasm.¹⁷

♦ Early vasospasm may be documented by angiography shortly after aneurysm rupture in 10% of patients. It has been associated with increased risk of neurological decline, cerebral ischemia, and poor functional outcome.³⁹ However, it does not appear to correlate with the occurrence of the more common delayed vasospasm.⁴⁰

♦ Delayed vasospasm follows a fairly predictable course, appearing 3 to 4 days after the hemorrhage, peaking around day 7, and progressively subsiding after day 12 to 14. However, the most severe cases may last longer, and rarely the arterial narrowing never resolves (fixed vasospasm).

♦ Diagnosing vasospasm is a complex task. Clinical, ultrasonographic, and angiographic criteria have been used to define its presence in various studies. In practice, despite using these measures in combination, diagnostic certainty often remains elusive.

♦ The incidence of vasospasm varies according to the criteria used for its definition. Angiographic vasospasm may be seen in two thirds of patients with SAH, but it is severe (> 50% luminal narrowing) in only 25% to 30% (but in more than 50% of patients with poor clinical grade on presentation). Symptomatic vasospasm occurs in approximately one third of SAH patients, and it tends to correlate with the occurrence of severe angiographic vasospasm.

♦ Narrowing of proximal segments of major vessels is associated with focal deficits and recognizable syndromes of brain ischemia. However, vasospasm is frequently diffuse, involving multiple vessels and small distal branches. In these cases, the main clinical manifestation is depressed level of consciousness, and vasospasm becomes very difficult to differentiate from other complications such as hydrocephalus, hyponatremia, infection, and excessive pharmacological sedation.

♦ Transcranial Doppler is best used as a screening method for the early detection of vasospasm and its subsequent monitoring. Increased blood flow velocities are indicative of vasospasm (Figure 12-13).⁴¹

♦ Reliable criteria for the ultrasonographic definition of vasospasm are available for the middle cerebral artery: mean flow velocity (MFV) > 200 cm/sec, MFV_{middle cerebral artery} /MFV_{extracranial internal carotid artery} (known as Lindegaard ratio) > 6, and rapidly increasing flow velocities are strongly predictive of angiographic vasospasm (positive predictive value > 95%).⁴² Lower limits of MFV (typically > 120 cm/sec) offer greater sensitivity but at the expense of considerably lower specificity.

♦ The application of similar criteria for the anterior cerebral artery and supraclinoid internal carotid artery is less reliable.⁴³ TCD diagnosis of basilar artery vasospasm has been much less studied; however, MFV > 115 cm/sec was highly predictive of brainstem ischemia in one study.⁴⁴

♦ It is important to recognize that studies using symptomatic vasospasm or radiological evidence of infarction as the primary outcome measures have documented similar sensitivities for TCD and angiogram.^45,46

♦ Patients with SAH may develop cerebral infarction without signs of vasospasm on TCD or angiography.⁴⁵ The true incidence of these unsuspected ischemic lesions is better ascertained by MRI.⁷ The infarctions that TCD and angiography fail to predict are most commonly small and subcortical.⁴⁷ They may constitute the anatomical substrate for the cognitive deficits that so often disable patients who survive SAH without major territorial infarcts and with good physical recovery.

♦ Mechanisms different from large-artery spasm, such as small vessel spasm or microembolism, may be responsible for the production of deep infarctions. Testing of vasomotor CO₂ reactivity⁴⁸ and monitoring for microembolic signals⁴⁹ can be performed at the bedside using TCD technology and may become valuable tools to enhance our ability to recognize patients at high risk for cerebral ischemia.

♦ Acute detection of areas of hypoperfusion is possible using PWI-MRI.⁵⁰ Meanwhile, DWI-MRI is highly sensitive for the diagnosis of acute ischemia.^8,25 Thus the combination of these two sequences may identify areas at risk for infarction that may be salvaged by prompt hemodynamic or endovascular intervention.²⁴

♦ New CT protocols combining spiral CT angiography and CT perfusion may become a practical and efficient method for the early identification of hemodynamically significant vasospasm.²⁶

♦ Time to peak on CT perfusion scans (1 sec difference from side to side) appears to be the most sensitive marker of the risk of cerebral infarction (Figure 12-14).^51,52

Figure 12-12 A 49-year-old woman with history of heavy smoking was admitted with subarachnoid hemorrhage (SAH). She was initially drowsy and confused but had no hemiparesis; her WFNS score was II. Initial computed tomography scan showed Fisher grade 3 SAH with more blood in the right than in the left Sylvian fissure and mild dilatation of the temporal horns of the lateral ventricles (upper left). Digital substraction angiography disclosed a right posterior communicating artery aneurysm (upper right, arrow) that could be effectively treated with endovascular coiling. On Day 4 after the SAH, her clinical condition began to decline. She became progressively less responsive. Mean blood flow velocities in both middle cerebral arteries exceeded 200 cm/sec. She was treated with hemodynamic augmentation therapy but failed to improve. Within hours, she became difficult to arouse and developed bilateral flexor posturing to pain. Repeat digital substraction angiography confirmed the presence of severe diffuse vasospasm (lower left). Attempted treatment with angioplasty and intra-arterial verapamil modestly improved the angiographic vasospasm, but her clinical condition remained poor. Subsequent magnetic resonance imaging showed large areas of restricted diffusion on diffusion-weighted imaging, consistent with acute infarctions in the territories of the anterior and middle cerebral arteries bilaterally (lower right). The patient did not recover and family requested withdrawal of life support 9 days after the SAH.

Figure 12-13 Example of vasospasm diagnosed by serial transcranial Doppler studies (at baseline, day 3, and day 5 after subarachnoid hemorrhage). Middle cerebral artery insonated through the transtemporal window, showing progressive increase in blood flow velocity. By Day 5, the patient had developed clinical changes attributable to symptomatic vasospasm. Severe middle cerebral artery vasospasm was also confirmed by angiography.

Figure 12-14 A 48-year-old woman was admitted with subarachnoid hemorrhage from a ruptured right internal carotid/posterior communicating artery aneurysm. The aneurysm was successfully treated with craniotomy and clipping on day 2 after the bleeding. On day 7, after 2 days of increased blood flow velocities on transcranial Doppler in the terminal right internal carotid artery and M1 segment of the middle cerebral artery, she became slightly less lucid and developed subtle left tactile simultagnosia. A computed tomography perfusion scan demonstrated markedly compromised perfusion in the right middle cerebral artery territory. Time to peak (shown on the left panel) was delayed by more than 1 second compared with the contralateral side. Digital substraction angiography confirmed severe right middle cerebral artery vasospasm (right panel), which was successfully treated with angioplasty.

VASOSPASM: ENDOVASCULAR TREATMENT

♦ When vasospasm is refractory to medical hemodynamic augmentation therapy, endovascular interventions must be pursued.²⁰ The optimal timing of endovascular therapy is not well defined; early intervention (within 2–3 hours of symptom onset) may be most beneficial,⁵³ but positive results may be achieved even as late as 24 hours after neurological decline.⁵⁴

♦ Angioplasty is effective for treatment of spasm in larger vessels (supraclinoid internal carotid artery, M1 segment of middle cerebral artery, A1 segment of anterior cerebral artery, basilar artery; Figure 12-15). The benefit resulting from angioplasty is durable, and the procedure is compatible with preservation of normal vessel function.⁵⁵

♦ Although angioplasty is safe in experienced hands, vessel rupture and branch occlusions are possible complications.^56,57

♦ Superselective intra-arterial infusion of a vasodilator drug is attempted when vasospasm is diffuse and involves smaller arterial branches. Papaverine was the first agent used,⁵⁸ but neurotoxicity limits its value.⁵⁹ Calcium channel blockers (verapamil,⁶⁰ nicardipine,⁶¹ nimodipine⁶²) are increasingly becoming a preferred alternative. The main handicap of intra-arterial vasodilators in general is the short duration of their beneficial effects.

♦ Angioplasty and intra-arterial drug infusion are often combined to achieve best results.

♦ Advanced age and poor clinical status at SAH onset are predictive of poor clinical outcome in patients who require endovascular treatment for vasospasm.⁶³

Figure 12-15 Examples of severe focal vasospasm treated with angioplasty. Case 1 (upper row): 40-year-old man with subarachnoid hemorrhage (SAH) due to rupture of left middle cerebral artery aneurysm treated with coil embolization. Five days after SAH onset, he developed severe symptomatic vasospasm of the left middle cerebral artery (left panel). Angioplasty successfully treated the spasm (right panel) and led to sustained resolution of the neurological deficits. Case 2 (lower row): A 38-year-old woman with dissecting aneurysm of the right posterior cerebral artery (P1/P2 segment) developed symptoms of basilar artery vasospasm (left panel). The vasospasm was effectively treated with angioplasty, resulting in resolution of the symptoms of posterior circulation hypoperfusion (right panel).

PATTERNS OF ISCHEMIA

♦ The two most common patterns of delayed cerebral ischemia after aneurysmal SAH are single cortical infarction, typically adjacent to the ruptured aneurysm, and multiple, widespread lesions including subcortical locations and often unrelated to the site of aneurysm rupture (Figure 12-16).⁴⁷

♦ Single cortical infarctions are caused by large vessel spasm detectable by TCD and angiography.^47,64 The mechanism of production of the lesions observed in the second ischemic pattern (small, multiple, predominantly subcortical infarctions) is less clear.^47,64 As mentioned earlier, microcirculatory disturbances (endothelial dysfunction manifested with abnormal vasomotor reactivity) and microembolism may play pathogenic roles in the generation of these lesions.

♦ Focal cortical laminar infarctions (cortical band-like ischemic lesions) may also be visualized on MRI scans in the adjacency of thick sulcal clots.⁶⁵ This pattern of infarctions often occurs in the absence of macroscopic vasospasm.⁶⁵

Figure 12-16 Patterns of cerebral infarction due to vasospasm in patients with subarachnoid hemorrhage (examples of acute ischemia shown on diffusion-weighted imaging sequence).

SUBARACHNOID HEMORRHAGE WITH NEGATIVE ANGIOGRAM

Nontraumatic SAH with negative initial angiogram may present three different radiological patterns on brain CT scan:

♦ Perimesencephalic SAH

♦ Focal, non-perimesencephalic SAH

♦ Diffuse SAH

Perimesencepahlic Subarachnoid Hemorrhage

♦ Perimesencepahlic SAH is a benign condition with no risk of recurrence. Blood on the initial CT scan is seen only on the perimesencephalic cistern, most commonly restricted to its anterior portion (pretruncal SAH; Figure 12-17).

♦ Angiography is always negative despite repeated studies;^66,67 thus typical cases of perimesencephalic SAH generally do not require repeated angiograms.⁶⁷

♦ However, one good-quality conventional angiogram should always be obtained before making this diagnosis because posterior circulation aneurysms may produce an early bleeding pattern indistinguishable from nonaneurysmal perimesencephalic SAH.⁶⁸

♦ The origin of the hemorrhage is unknown, but a venous source has been suggested.⁶⁹

♦ Prognosis is favorable,⁷⁰ but diffuse vasospasm may occur.⁷¹

Figure 12-17 Typical example of perimesencephalic (pretruncal) subarachnoid hemorrhage on computed tomography scan. As expected, digital substraction angiography revealed no aneurysms or other vascular anomalies.

Non-Perimesencephalic Subarachnoid Hemorrhage with Negative Angiogram

♦ Angiogram-negative, non-perimesencephalic SAH has become a less frequent clinical problem thanks to recent technological improvements, especially three-dimensional rotational angiography.⁷²

♦ Different patterns of non-perimesencephalic, angiographically negative SAH can be encountered, as illustrated on Figure 12-18.

♦ These patients must be studied with repeated conventional angiography after 5 to 7 days. Noninvasive angiograms (spiral CT and MR angiography techniques) may reveal the source of the bleeding,^73,74 but negative results should be regarded cautiously and do not eliminate the indication for repeating catheter angiography.⁷⁵

♦ Possible causes of angiogram-negative, non-perimesencephalic SAH include microaneurysms,⁷⁶ arterial dissections,⁷³ and focal thrombosis or vasospasm at the site of the aneurysm.⁷⁵

♦ Patients with no evidence of aneurysm despite repeated studies most commonly have a small amount of subarachnoid blood, even when the distribution is diffuse. The risk of vasospasm tends to be low, and most patients recover well.⁶⁷ Nonetheless, some patients with cryptogenic, diffuse SAH have extensive bleeding, develop vasospasm, and suffer functional sequelae.⁷⁰

♦ When the SAH is restricted to a focal clot overlying the cortex, repeated conventional angiography may be unnecessary. In those cases, particular attention must be paid to the venous phase of the angiogram to exclude venous thrombosis.

Figure 12-18 Examples of non-perimesencephalic, angiographically negative subarachnoid hemorrhage. Various patterns on computed tomography scan are shown: diffuse pattern (left panel), focal central pattern (middle panel), and focal peripheral pattern (right panel).

CONDITIONS MIMICKING ANEURYSMAL SUBARACHNOID HEMORRHAGE

Pseudo-Subarachnoid Hemorrhage

♦ Marked elevation in intracranial pressure may produce changes on CT scan that include effacement of basal cisterns and hyperdense signal along the tentorium, Sylvian fissures, and perimesencephalic cisterns. The resulting radiological pattern falsely suggests the diagnosis of SAH and is known as “pseudo-SAH” (Figure 12-19).

♦ Pseudo-SAH has been observed in cases of severe anoxic brain damage with diffuse cerebral edema^77,78 and of bilateral subdural hematoma.¹⁶ It has also been reported in association with intracranial hypotension,⁷⁹ presumably as a result of vascular engorgement. Rarely, purulent meningitis (especially if causing extensive cerebral swelling) and venous sinus thrombosis may also mimic SAH.

♦ MRI with T2^* or FLAIR sequences may distinguish these cases from true SAH. Timely use of MRI may avoid unnecessary angiographic studies.

♦ Useful clues on CT scan include presence of a smooth layer of blood in the interhemispheric fissure (as opposed to the much more irregular hyperdensity seen with true SAH), marked effacement of the sulci and basal cisterns in the absence of thick layers of subarachnoid blood or intraparenchymal hematoma, and slit-like ventricles (instead of hydrocephalus and intraventricular hemorrhage most commonly found with true SAH).¹⁶

♦ Although it is useful to consider the possibility of pseudo-SAH when there is clear evidence of severe brain edema, it is crucial to remember that aneurysmal SAH may also be associated with global cerebral swelling.

Figure 12-19 Pseudo-subarachnoid hemorrhage on computed tomography scan caused by global cerebral edema after resuscitation from cardiac arrest. Arrows indicate high attenuation changes in Sylvian fissures, ambient cistern, and tentorium.

Traumatic Subarachnoid Hemorrhage

♦ The differential diagnosis between traumatic and aneurysmal SAH may become difficult when history is not available (e.g., in patients found comatose). In addition, external signs of trauma and associated contusions may occasionally be seen in patients who collapse after aneurysm rupture.

♦ Some radiological signs may help recognize traumatic cases (Figure 12-20):

♦ Subarachnoid blood more prominent in the sulci of the hemispheric convexities than in the basal cisterns

♦ Presence of coexistent contusions, epidural hematomas, or subdural hematomas

♦ Evenly distributed layer of blood without any focal dense clot

♦ Focal hemorrhage overlying an area of cerebral cortex

♦ However, traumatic SAH may be indistinguishable from cases caused by aneurysmal rupture. When in doubt, it is always safer to perform cerebral angiography.

♦ Traumatic SAH is not associated with significant risk of symptomatic vasospasm. However, presence of SAH after traumatic brain injury is often associated with more severe radiological findings and may portend poor functional outcome.⁸⁰

♦ Dissecting aneurysms are relatively uncommon and potentially life-threatening causes of SAH after trauma (Figure 12-21).

Figure 12-20 Two cases of traumatic brain injury with subarachnoid hemorrhage (SAH). Case 1 (upper row): left panel shows right frontal hemorrhagic contusion, SAH in the left frontal sulci, and mild intraventricular hemorrhage layering in the posterior horn of the left lateral ventricle. Right panel discloses diffuse SAH in the sulci associated with small areas of subdural hemorrhage and signs of swelling in the subgaleal compartment. Case 2 (lower row): left panel displays a left posterior temporal hemorrhagic contusion in addition to sulcal SAH, probable small left temporal subdural hematoma, and left subgaleal hematoma. Right panel shows extensive sulcal SAH at a higher cut.

Figure 12-21 Subarachnoid hemorrhage from dissecting (fusiform) aneurysm affecting the right intracranial vertebral artery in its V4 segment (arrow).

Causes of Sulcal Subarachnoid Hemorrhage

♦ Apart from trauma, the main causes of sulcal SAH are hemorrhagic diathesis, ruptured septic (mycotic) aneurysm, vasculitis, reversible cerebral vasoconstriction, and venous sinus thrombosis. SAH in a sulcal distribution may also be produced by bleeding from peripherally located AVMs and dural AV fistulas.

♦ Patients with hemorrhagic diathesis–hereditary, acquired, or iatrogenic–may develop subarachnoid hemorrhage after trivial trauma or even without obvious precedent trauma.

♦ Hemorrhage in these patients tends to occur diffusely over the sulci of the convexity of both cerebral hemispheres (Figure 12-22).

♦ Dural sinus thrombosis is an infrequent cause of SAH, which is typically seen in the proximity of the occluded sinus (Figure 12-23).

♦ Associated venous infarction or visible fresh thrombus in the sinus may be clues to make the correct diagnosis.

♦ When cerebral venous thrombosis is suspected, DSA or noninvasive venography can confirm the diagnosis.

♦ Cerebral vasculitis occasionally may present with isolated sulcal SAH (see Figure 12-24). Nonetheless, the association with small areas of ischemia or intracerebral hemorrhage is more characteristic of this diagnosis.⁸¹

♦ Reversible cerebral vasoconstriction (also known as Call-Fleming syndrome) may resemble a mild form of cerebral vasculitis, and presentation with sulcal SAH has been reported.⁸²

Figure 12-22 Patient with thrombocytopenia from acute leukemia who presented with thunderclap headache after a trivial head trauma. Computed tomography scan showed diffuse sulcal subarachnoid hemorrhage.

Figure 12-23 A 36-year-old woman 6 weeks postpartum presented with progressive holocranial headache for 2 weeks with severe exacerbation of the headache and nausea over the preceding 48 hours. Computed tomography scan showed subarachnoid hemorrhage in the sulci of the right frontal lobe (left panel, arrow). No parenchymal abnormalities were noted. Venous sinus thrombosis was suspected given the puerperal state. The diagnosis was confirmed by magnetic resonance venogram (right panel).

Figure 12-24 A 52-year-old woman developed rapid onset of severe, throbbing headache after leaving a funeral. In the emergency department, she was distressed by the pain but had preserved cognitive functions and no focal neurological deficits. Head computed tomography scan revealed subarachnoid hemorrhage (SAH) overlying the sulci of the left cerebral convexity. This finding was subsequently better visualized on brain MRI (shown left is the fluid-attenuated inversion recovery sequence; arrows indicate the sulcal SAH). Digital substraction angiography (DSA) disclosed diffuse irregularities in intracranial arterial branches consistent with the appearance of vasculitis. Cerebrospinal fluid had mild pleocytosis and elevated protein content. Evaluation for causes of systemic vasculitis was negative. The patient was treated with prednisone, and her headache promptly subsided. She continued to do well after discharge and repeat DSA 3 months later showed resolution of the vascular changes.