Imaging Strategy for Patients With Aneurysmal Subarachnoid Hemorrhage and Negative Initial Imaging: Evidence,Pitfalls,and Emerging Techniques

Abstract

French

Subarachnoid hemorrhage (SAH) is frequently caused by a ruptured saccular cerebral aneurysm, making early and accurate diagnosis critical for patient outcomes. CT angiography (CTA) is the standard first-line imaging modality for suspected nontraumatic SAH; however, up to 15% of patients present with negative initial CTA findings, necessitating further imaging work-up. A key distinction in SAH is between an aneurysmal and a non-aneurysmal bleeding pattern. Perimesencephalic hemorrhage, a distinct SAH subtype, exhibits a contained bleeding pattern rarely associated with an underlying aneurysm, and therefore requires a different imaging approach than aneurysmal SAH. Given the alarmingly high mortality of untreated ruptured cerebral aneurysms, a comprehensive imaging strategy enabling prompt identification of intracranial aneurysms is essential to prevent rebleeding. This narrative expert review discusses the available evidence for the optimal imaging strategy in patients presenting with aneurysmal-pattern SAH and initially negative findings. It addresses potential pitfalls in neurovascular imaging, offers guidance on identifying rare causes of SAH through advanced imaging techniques, and examines the yield of repeat neuroimaging in the context of evolving imaging technologies. Finally, we address the diagnostic challenges posed by rarer aneurysm subtypes, including spinal artery aneurysms, dissecting aneurysms, blood blister-like aneurysms, and perforating artery aneurysms. Together, these insights inform the development of a comprehensive, patient-centered imaging algorithm for improved care in cases of aneurysmal SAH without a detectable aneurysm on initial imaging.

Keywords

subarachnoid hemorrhage cerebral aneurysm CT angiography perimesencephalic hemorrhage neurovascular imaging repeat neuroimaging

Introduction

Ruptured saccular cerebral aneurysms are the most common cause of spontaneous subarachnoid hemorrhage (SAH).¹ At present, CTA is often the first imaging modality performed in patients with evidence of a subarachnoid hemorrhage on initial nonenhanced CT (NECT) and no history of recent trauma. However, in up to 15% of patients, the initial CTA does not reveal a structural cause for the bleeding.²

To determine the optimal imaging strategy in SAH patients with an initial negative CTA, it is essential to analyze the distribution of hemorrhage on initial NECT. In patients with specific distributions of SAH, such as low-volume cortical sulcal SAH or perimesencephalic SAH, an aneurysm is rarely the cause of hemorrhage.^1,3 The imaging strategy in these patients therefore differs significantly from those presenting primarily with extensive hemorrhage in the basal cisterns, often in the suprasellar cistern with secondary peripheral extension, which is frequently indicative of aneurysmal SAH.^3,4 Mortality rates in patients with an untreated ruptured aneurysm can be as high as 65% during the first year.⁵ Therefore, in patients with aneurysmal SAH, the imaging strategy is centered on identifying cerebral aneurysms in order to facilitate prompt treatment and prevent rebleeding. The rebleeding rate without treatment is approximately 50% over 6 months, and most repeat hemorrhages occur within the first 24 to 48 hours after the initial rupture.⁶

Digital Subtraction Angiography (DSA) is the gold standard for the detection and evaluation of structural cerebrovascular pathologies.⁷ Nevertheless, catheter angiography entails a non-negligible risk of complications compared to noninvasive imaging methods, which must be considered when determining an imaging strategy.^8,9 In this narrative expert review, we discuss the available evidence for optimal imaging strategy for patients with an aneurysmal type SAH and initial negative vascular imaging, potential pitfalls in vascular imaging of patients with aneurysm SAH and tips to identify rare causes of SAH.

The method used to identify studies relevant to the data synthesis for this narrative expert review included searching the English-language literature in PubMed and Embase for studies between 1990 and 2026. We used the following keywords in our search in different combinations: aneurysm, intracranial aneurysm, subarachnoid hemorrhage, diagnostic imaging, angiography, cerebral angiography, magnetic resonance imaging, and computed tomography. Some studies were included after searching bibliographies of relevant studies or from the authors’ personal bibliographies.

Aneurysmal Type SAH

Patients with spontaneous subarachnoid hemorrhage can be roughly divided into those with aneurysmal and non-aneurysmal bleeding patterns. As opposed to an aneurysmal bleeding pattern, there are some subarachnoid hemorrhage bleeding patterns in which an aneurysm is rarely seen. Most of these fall within the category of perimesencephalic hemorrhage. In a perimesencephalic hemorrhage pattern, blood is present anterior to the midbrain with or without extension to the anterior ambient cistern or basal Sylvian fissure and without complete filling of the interhemispheric fissure or extension to the lateral Sylvian fissure.³ Another spontaneous SAH pattern in which aneurysms are rarely found, is a low-volume cortical sulcal SAH.¹⁰ This type of SAH may be attributed to cerebral amyloid angiopathy (CAA), reversible cerebral vasoconstriction syndrome (RCVS), posterior reversible encephalopathy syndrome (PRES), CNS vasculitis, superficial vascular malformations, anticoagulation or anti-aggregation medication, cerebral venous thrombosis, or rarely, to malignancies.^1,11,12 If the extent of the subarachnoid hemorrhage exceeds the limits of a perimesencephalic or cortical sulcal SAH, it falls into the category of aneurysmal SAH. Finally, increased density in the subarachnoid space may be caused by non-hemorrhagic entities, which can mimic SAH and should ideally be recognized before proceeding to DSA.¹³ Radiological definitions of aneurysmal and non-aneurysmal types of subarachnoid hemorrhage on NECT are, however, variable, and have evolved over time.¹⁴

The Yield of DSA After Negative CTA

In most clinical settings, the standard imaging strategy for patients with an acute spontaneous SAH includes a NECT and CTA of the cerebral arteries. In cases where the initial CTA yields negative results for a patient with an aneurysmal SAH, the standard practice in most medical facilities is to perform a DSA. There is supporting evidence for this, as the diagnostic yield of a DSA after an initial negative CTA has remained high despite improvements in CTA quality over time. One retrospective study of 230 SAH patients with a negative initial CTA found that DSA identified a vascular pathology in 13% of patients.⁷ Two smaller retrospective studies (186 and 193 patients, respectively) reported a modest 4% yield for DSA in this setting.^10,15

Repeat DSA

Several studies have investigated the yield of repeat DSA in SAH patients with negative initial CTA and DSA.^16-37 The yield of repeat DSA depends on multiple factors, including the quality of the initial DSA, the quality of CTA or MRA when used before repeat DSA, the inclusion of patients at lower risk for an aneurysmal etiology (eg, those with a perimesencephalic bleeding pattern), the timing of repeat imaging after ictus, and operator expertise. Consequently, and partly because patient selection for repeat DSA is largely guided by local institutional practice, reported diagnostic yields vary widely across studies, ranging from 0% to 78%. Some studies performed repeat DSA in all patients with negative initial imaging, including those with non-aneurysmal bleeding patterns, whereas others limited repeat studies to patients meeting predefined criteria, such as poorer neurological status, younger age, non-perimesencephalic blood distribution, or suboptimal initial imaging quality.^{17,26,28-30,33,35-37} Advances in and increased availability of CTA and MRA have reduced the need for repeat DSA by enabling identification of a culprit lesion in a growing proportion of patients. At the same time, technological improvements in catheter angiography, including three-dimensional rotational angiography, have enhanced the diagnostic performance of both initial and repeat DSA, affecting reported yields in a complex manner.³⁵ Importantly, in patients with an aneurysmal bleeding pattern, particularly those with poor neurological status, the findings of most contemporary studies support repeating DSA after initial negative imaging.^17,29,35,36 A summary of the identified studies and the corresponding diagnostic yield of repeat DSA is presented in Table 1.

Table 1.

Studies Investigating Repeat DSA After SAH With Initial Negative Imaging.

Study	Inclusion period	DSA-negative SAH (n)	Repeat DSA (n)	Positive repeat DSA (n)	Positive repeat DSA (%)
Forster 1978²⁰	1967-1972	150	56	1	2
Nishioka 1984³¹	1958-1965	477	72	13	18
Suzuki 1987³²	1978-1984	41	41	9	22
Gilbert 1990²¹	1962-1986	1086	24	0	0
Iwanaga 1990²⁵	1974-1989	45	38	8	21
Duong 1996¹⁹	1983-1992	92	37	4	11
Kaim 1996²⁷	1990-1994	42	42	8	19
Bradac 1997¹⁶	1992-1996	66	40	5	13
du Mesnil de Rochemont 1997¹⁸	1987-1994	117	66	3	5
Urbach 1998³⁴	1983-1995	122	67	4	6
Inamasu 2003²³	1991-1999	19	19	7	37
Topcuoglu 2003*³³	1995-2002	86	36	3	8
Huttner 2006²²	2000-2004	69	38	0	0
Jung 2006*²⁶	1986-2004	37	37	17	46
Little 2007*²⁹	2003-2006	100	42	4	10
van Rooij 2008*³⁵	2006-2007	98	23	18	78
Andaluz and Zuccarello 2008*³⁷	1998-2003	92	47	7	15
Delgado Almandoz 2012*¹⁷	2005-2010	73	39	2	5
Maslehaty 2012*³⁰	1991-2008	132	120	13	11
Yu 2012*³⁶	2005-2012	28	12	2	17
Khan 2013*²⁸	2008-2012	50	8	0	0

Perimesencephalic SAH patients in this studies were excluded from repeat angiography, included only in case of atypical clinical or radiological findings, or excluded as a subgroup from this table when reported as a subgroup.

Late Neuroimaging With CTA or DSA

There is limited data on the yield of late neuroimaging after repeated DSA in SAH, with available evidence predominantly from small-scale studies. A retrospective study of 39 SAH patients with negative CTA, DSA, and repeat DSA showed that late (mean time from bleed 35 days) imaging with CTA (30 patients) or DSA (9 patients) had a yield of 8% to detect a causative lesion for the bleed. Of note, all detected vascular lesions were seen in patients with a diffuse SAH and none were found in patients with perimesencephalic SAH.³⁸ Another retrospective study with 174 patients with SAH and 2 negative angiograms found a 4% yield for causative lesions during a third angiogram.³⁹ In a study with 242 patients with SAH and negative initial imaging, 34 had a third DSA and 4 (11.8%) of them were found to have a culprit for the bleed.⁴⁰ Importantly, in cases of sudden neurological deterioration, urgent CT and CTA should be performed to evaluate for re-bleeding or vasospasm, and to assess for recanalization of a previously occult or thrombosed aneurysm.

MRI in Patients With CTA Negative Aneurysmal SAH

MRI is more sensitive in detecting intracranial hemorrhage than CT, but DSA remains the gold standard in identifying the bleeding source.⁴¹ MRA is highly sensitive in detecting aneurysms, even after rupture, but the specificity varies greatly among different reports.^42-44 MRA is particularly useful when radiation exposure should be minimized and in cases where repeat DSA fails to identify an underlying structural vascular lesion. However, it is generally not recommended for hemodynamically unstable patients. Vessel-wall MRI can be a valuable adjunct to conventional MRA in detecting intracranial aneurysms, particularly rare subtypes such as perforating artery aneurysms.^45,46 It may also aid in identifying the culprit lesion in cases of rupture by demonstrating focal vessel-wall enhancement when the source is uncertain or in case of multiple intracranial aneurysms.^47,48 Additionally, ultra–high-field imaging with 7T MRI shows promise in resolving equivocal cases by revealing a peripheral hemosiderin “cap sign” around the aneurysm, which is suggestive of prior rupture.⁴⁹ In cases where the distribution of the subarachnoid blood is unusual, the added value of MRI lies in its ability to detect other causes of SAH, such as tumors, vasculitis, and cerebral amyloid angiopathy.

What Do the Guidelines Say

The latest European Stroke Organization (ESO) guideline on the treatment and diagnosis of subarachnoid hemorrhage from 2013 states that DSA of all cerebral arteries should be performed if a bleeding source was not found on CTA and the patient has a typical basal SAH pattern on CT. Furthermore, if no aneurysm was found on primary imaging, CTA or DSA should be repeated unless the bleeding pattern fits the criteria of a perimesencephalic hemorrhage. Repeating the DSA is not recommended for SAH patients with a perimesencephalic distribution of the hemorrhage.⁵⁰

The latest American Stroke Association (ASA) guideline for diagnosis and treatment of subarachnoid hemorrhage was published in 2023.⁵¹ According to this guideline, a DSA is indicated for evaluation of patients with diffuse (ie, aneurysmal type) SAH regardless of CTA results since small aneurysms or other vascular lesions may not be fully appreciated or defined on CTA imaging owing to the limitations in spatial resolution.⁵¹ Furthermore, DSA is considered the gold standard modality for the evaluation of cerebrovascular anatomy and aneurysm geometry and can aid in decision-making on the choice of optimal treatment modality. CTA alone, in certain clinical settings, may be used for treatment decision-making.⁵¹

Both ESO and ASA guidelines do not address the exact timing of DSA and CTA, the technical aspects of angiography (eg, whether rotational angiography should be performed or whether extracranial vessels should be injected), the recommended number of repeat studies, or the role of MRI. This reflects the broader inconsistency surrounding these and other relevant topics. The utility of MRI in the detection and characterization of SAH is explicitly identified as a knowledge gap in the ASA guidelines.

Potential Sources of False Negative Result in Initial Imaging of SAH

The imaging of patients with acute SAH is subject to various potential sources of error that can compromise image quality and reduce imaging sensitivity. SAH patients can present to the hospital with a broad range of clinical conditions, ranging from experiencing only a headache as their sole symptom to being in a state of deep coma. Notably, patients with intracranial hemorrhage are often restless and may have difficulty cooperating during imaging procedures. This may result in reduced image quality for primary CTA, despite the short image acquisition times of modern CT scanners and their reduced susceptibility to motion artifacts compared to MRA. If the image quality is significantly reduced due to motion artifacts, imaging should be repeated after the patient has been intubated and sedated.

Two additional aspects are important in achieving high quality CTA-images and maximizing CTA yield. First, attention should be paid to technical aspects such as positioning, contrast medium, and correct timing of the scan. Second, it is essential to consider clinical information when interpreting a CTA. For example, considering the timing of the bleeding is highly important: when a patient presents in the hospital shortly after bleeding, the distribution of blood in the subarachnoid space may help in pointing to the most likely location of the ruptured aneurysm (in patients with several intracranial aneurysms, blood distribution in the subarachnoid space may assist in determining which aneurysm caused the bleeding and should therefore be urgently treated, and which aneurysms are incidental). Conversely, in patients who present later to the hospital, after a significant redistribution of blood in the subarachnoid space took place, identifying a likely location for a ruptured aneurysm may be more challenging.

As with CTA, DSA should also not be performed on an awake patient who is unable to remain still for the entire duration of the study. In a study involving 242 SAH patients who initially had negative DSA results, 8 aneurysms were detected on repeat DSA, missed initially due to errors in the prior DSA examination.⁴⁰ These errors included the lack of 3D rotational DSA for the relevant vessel, insufficient 2D projections and misinterpretations by the performing physician, wherein a lesion was visible on the angiogram but was interpreted as normal. These findings underscore the critical importance of meticulous attention to detail when performing a comprehensive cerebral angiography. Such an examination should include selective angiograms of both internal carotid arteries, both external carotid arteries and both vertebral arteries, as well as rotational angiograms of the relevant vessels. This comprehensive approach serves to minimize the likelihood of overlooking aneurysms and other structural vascular lesions that may cause SAH.

Early thrombosis of a ruptured aneurysm is a known phenomenon that may cause false negative results in initial imaging.^52,53 An important imaging pitfall of this group of aneurysms is that they can recanalize, which could take up to several weeks to happen. For this reason, repeated imaging in the early stage of SAH cannot rule out a thrombosed small, ruptured aneurysm. Occasionally, the aneurysm may be associated with a thick blood clot in the subarachnoid space, which may cause direct local pressure on the aneurysm, preventing it from filling. Notwithstanding, thrombosis of an aneurysm is possible even without an associated thick subarachnoid blood clot. While small, thrombosed aneurysms may be occult on initial imaging, a thrombosed aneurysm of sufficient size may even be visible on NECT and MRI, often more conspicuous with the latter.^52-55 For this reason, an acutely thrombosed aneurysm should be included in the differential diagnosis in patients with an aneurysmal SAH pattern on NECT and an initial negative neurovascular imaging. The exact distribution of the hematoma in the subarachnoid space is an important hint for the possible location of the thrombosed aneurysm (eg, SAH concentrated mostly in the right Sylvian fissure may hint toward acute thrombosis of a ruptured right middle cerebral artery bifurcation aneurysm).

Identification of Rare Causes of Aneurysmal SAH With Neuroimaging

Certain subtypes of aneurysms are rare and difficult to identify with imaging. These include spinal artery aneurysms, dissecting aneurysms, perforating artery aneurysms, blood blister-like aneurysms, and mycotic aneurysms. Here, we have outlined a few illustrative examples of rare causes for SAH.

Spinal Artery Aneurysms

Rupture of a spinal artery aneurysm is a rare cause of SAH. This entity should be kept in mind when encountering aneurysmal type SAH centered in the posterior fossa, with the subarachnoid blood clot thickness typically increasing towards the foramen magnum. The resolution of CTA is often too low to identify a ruptured spinal artery aneurysm, but they can be readily seen on good quality DSA. In cases with substantial extension of SAH into the cervical spine, the differential diagnosis should include spinal lesions such as pial AVM or AVF, ependymoma, and cavernoma. An additional cervical spine MRI may be necessary to confirm these diagnoses.⁵⁶ Figure 1 shows an illustrative case of a ruptured tiny anterior spinal artery aneurysm, detected on repeat DSA after 2 negative CTAs and 1 negative DSA.

Figure 1.

Initial NECT brain (A) demonstrated a subarachnoid hemorrhage centered in the posterior fossa. Initial DSA in AP view showed no aneurysm (B). Repeat DSA in AP view revealed a small aneurysm of the anterior spinal artery (D; arrow), further magnified on additional 3D rotational angiography (C; arrow).

Dissecting Aneurysms

Approximately 1% to 10% of all nontraumatic SAH in adults are attributed to intracranial arterial dissections.^57,58 Arterial dissections leading to SAH typically manifest as a fusiform or irregular aneurysmal dilation at a non-branching site, often accompanied by focal stenoses at both the proximal and distal ends of the aneurysmal dilatation.⁵⁹ The intradural vertebral artery (V4-segment) is the most common location for a ruptured intracranial dissecting aneurysm. Other frequent sites include the postostial PICA, the posterior cerebral artery near the P2/P3 junction as it courses above the tentorium, the M1-segment, and the distal anterior cerebral arteries as they traverse along the falx.⁵⁹

Unlike unruptured arterial dissections, intramural hematomas are usually absent in ruptured dissecting aneurysms after blood has extravasated into the subarachnoid space. The absence of an intramural hematoma can make it challenging to differentiate a ruptured dissecting aneurysm from a ruptured non-dissecting fusiform aneurysm.⁵⁹ Other pathologies that can be difficult to distinguish from a ruptured dissecting aneurysm include reversible cerebral vasoconstriction syndrome (RCVS) and vasospasm secondary to subarachnoid hemorrhage. Unlike these pathologies, an arterial dissection usually involves only a single vessel (in contrast to RCVS) and is already visible on the day of ictus (which is atypical for vasospasm). Up to 40% of patients with a ruptured dissecting aneurysm will experience rebleeding, most commonly within the first week. The 2 main treatment options are a deconstructive technique with parent artery sacrifice, either with endovascular coiling or surgical trapping (with or without bypass), or a reconstructive technique, typically involving a flow-diverter stenting. Figure 2 provides an illustration of a ruptured dissecting aneurysm involving the left posterior cerebral artery.

Figure 2.

Initial NECT brain (A) demonstrated a left posterior mesotemporal intraparenchymal hemorrhage, with subarachnoid and intraventricular extension. Motion degraded CTA brain (D) showed no cause for the hemorrhage. 3D rotational angiography revealed a ruptured dissecting aneurysm at the left P2-P3 junction (B; arrow) in close proximity to the incisura of the tentorium cerebelli, with a distal segment of stenosis (E; arrow). Lateral view redemonstrated the aneurysm (C; black arrow) and stenosis (C; gray arrow) before (C) and after (F) parent vessel sacrifice with coils.

Blood Blister-Like Aneurysms

Blood blister-like aneurysms are most commonly located in the internal carotid artery close to the skull base. They may be challenging to identify on CTA as well as on AP and lateral angiograms as they are not located in an arterial branching point but represent sidewall aneurysms. In addition, they often cause a relatively severe SAH with a thick clot burden in the basal cisterns. It is not uncommon that these aneurysms are partially thrombosed in the first DSA. Figure 3 shows an illustration of a ruptured blood blister-like aneurysm at the supraclinoid segment of the right internal carotid artery.

Figure 3.

Initial NECT brain demonstrated a diffuse SAH in the basal cisterns with extension to the Sylvian fissures, more on the right than the left (A). Initial CTA brain revealed a subtle equivocal irregularity laterally at the supraclinoid segment of the right internal carotid artery (B; arrow). A follow-up CTA on day 2 showed increased conspicuity of a horizontally oriented blood blister-like aneurysm arising from the supraclinoid segment of the right internal carotid artery (C; arrow). AP views DSA and 3D rotational angiography of the right internal carotid artery revealed the small broad-based blood blister-like aneurysm before (D, E) and after endovascular embolization (F) with 2 flow-diverters and coils.

Perforating Artery Aneurysms

Perforating artery aneurysms are mainly seen in the posterior fossa, typically located in perforating branches of the posterior cerebral artery or basilar artery.^60,61 They are difficult to identify due to their small size, which makes them equally hard to treat. DSA with rotational angiography, preferably under sedation with breath-holds during angiography runs may be helpful in locating these aneurysms. Vessel wall MRI as well as 7T MRI have been reported to assist in the identification of these aneurysms.^46,62 Figure 4 illustrates a case of a ruptured right collicular artery aneurysm.

Figure 4.

Initial NECT brain showing diffuse SAH distributed symmetrically in the basal cisterns. There is also a small amount of subarachnoid blood in the sulci and intraventricular blood (A). 3D reconstruction of the initial CTA (B), and coronal MIP image of the initial MRA (non-enhanced Time-Of-Flight) (C) demonstrated no aneurysm. AP view DSA of the left vertebral artery revealed a small aneurysm arising from the proximal aspect of the right collicular artery (D, arrow). Of note, an artery of Percheron was present as well (D; white arrowhead), arising medially to the collicular artery. Lastly, the basilar tip demonstrated a small unruptured aneurysm (D; black arrowhead).

Conclusion

An accurate evidence-based and patient-centered imaging algorithm is crucial for individuals with aneurysmal SAH without evidence of a cerebral aneurysm on initial imaging. This approach is vital for improving the diagnostic yield of imaging, tailoring emergent therapy, and ultimately for improving patient outcomes by reducing the risks associated with a delayed or inaccurate diagnosis. Detailed clinical information, information attained from the initial imaging studies and an understanding of the advantages and disadvantages of each imaging modality are all necessary in determining the cause of SAH. In Figure 5 we propose an imaging algorithm for this patient group. Imaging strategy in the setting of an aneurysmal SAH without detectable aneurysm remains a complex and evolving field which often requires a multidisciplinary approach.

Figure 5.

Proposed imaging algorithm for patients with an aneurysmal SAH without evidence of a cerebral aneurysm.

Footnotes

Acknowledgements

MN, DV, and EH thank University Medical Imaging Toronto for their kind support.

ORCID iDs

Uri Singfer

Joao Andre Sousa

Ronette Goodluck Tyndall

Mehran Nasralla

Emily Chung

David Volders

Eef J. Hendriks

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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