RESEARCH HUMAN CLINICAL STUDIES

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1 TOPIC RESEARCH HUMAN CLINICAL STUDIES RESEARCH HUMAN CLINICAL STUDIES Richard Dalyai, MD Nohra Chalouhi, MD Thana Theofanis, BS Pascal M. Jabbour, MD Aaron S. Dumont, MD L. Fernando Gonzalez, MD David S. Gordon, MD Robert H. Rosenwasser, MD Stavropoula I. Tjoumakaris, MD Department of Neurosurgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, Philadelphia, Pennsylvania Correspondence: Stavropoula I. Tjoumakaris, MD, Assistant Professor, Department of Neurological Surgery, Division of Neurovascular Surgery and Endovascular Neurosurgery, Thomas Jefferson University Hospital, 901 Walnut St, 3rd Floor, Philadelphia, PA Received, May 24, Accepted, December 10, Published Online, December 28, Copyright ª 2012 by the Congress of Neurological Surgeons SANS LifeLong Learning and NEUROSURGERY offer CME for subscribers that complete questions about featured articles. Questions are located on the SANS website ( Please read the featured article and then log into SANS for this educational offering. Subarachnoid Hemorrhage With Negative Initial Catheter Angiography: A Review of 254 Cases Evaluating Patient Clinical Outcome and Efficacy of Short- and Long-term Repeat Angiography BACKGROUND: Subarachnoid hemorrhage (SAH) is found to have no vascular origin by initial catheter angiography in approximately 15% of cases. The most appropriate course for the type and frequency of additional diagnostic workup remains controversial. OBJECTIVE: To retrospectively assess the diagnostic yield of short-term and long-term repeat catheter angiography in the era of advanced imaging. METHODS: Between 2003 and 2011, 254 consecutive patients diagnosed with SAH had negative initial angiography. SAH was perimesencephalic (PM) in 46.5% and nonperimesencephalic (NPM) in 53.5%. Angiography was repeated at 1-week (short-term) and 6-week (long-term) intervals from the initial negative angiogram. RESULTS: Ten of 254 patients had a vascular source of hemorrhage on short-term follow-up angiography with a diagnostic yield of 3.9%. One hundred seventy-four patients with negative findings on the first 2 angiograms received a third angiogram, and 7 of these patients were found to have a vascular abnormality. The estimated yield of this third angiogram was 4.0%. The overall diagnostic yield of repeat angiography was 0% in the PM group and 12.5% in the NPM group. The diagnostic yield of shortterm and long-term follow-up angiography in patients with NPM SAH was 7.3% and 7.8%, respectively. NPM patients were more likely to experience vasospasm and hydrocephalus requiring external ventricular drainage or cerebrospinal fluid diversion than PM patients. CONCLUSION: Our results support a protocol of short-term and long-term angiographic follow-up in patients with NPM SAH and negative initial angiography. Aggressive protocols of follow-up angiography may not be necessary in patients with PM SAH. KEY WORDS: Aneurysms, Digital subtraction angiography, Occult vascular lesions, Subarachnoid hemorrhage Neurosurgery 72: , 2013 DOI: /NEU.0b013e de8 Subarachnoid hemorrhage (SAH) is a devastating neurological condition, accounting for approximately 3% to 5% of all strokes and affecting North Americans annually. 1,2 It is associated with a 30-day mortality rate that can reach 45%. 2 Catheter digital subtraction ABBREVIATIONS: CTA, computed tomographic angiography; DSA, digital subtraction angiography; HH, Hunt and Hess; MRA, magnetic resonance angiogram; NPM, nonperimesencephalic; PM, perimesencephalic; SAH, subarachnoid hemorrhage angiography (DSA) remains the gold standard for the detection of a cerebral aneurysm or other vascular source of the hemorrhage. However, nearly 15% of patients suffering from SAH have anegativeinitialdsa Previous reports have estimated that vascular abnormalities could be identified in 2% to 24% of these cases on repeat DSA. 3-7,10,12-14,16 However, many of these reports precede the era of more advanced imaging techniques such as 3-dimensional (3-D) rotational angiography, magnetic resonance angiography (MRA), and computed tomography (CT) angiography (CTA) imaging. 17, VOLUME 72 NUMBER 4 APRIL

2 ANGIOGRAM NEGATIVE SAH: YIELD OF REPEAT DSA SAH with negative cerebral angiography can be categorized as perimesencephalic (PM) and nonperimesencephalic (NPM) types on the basis of the blood distribution on noncontrast head CT. PM hemorrhage is limited to the ambient, crural, and quadrigeminal cisterns without significant extension into the sylvian or interhemispheric fissures. This hemorrhage type has been reported to have a more benign clinical course and is mostly nonaneurysmal in origin. 5,6,8,19 Conversely, patients with a more diffuse SAH pattern on initial head CT are more likely to have a positive repeat angiography and to have worse clinical outcomes. 19 NPM SAH was found to have 10% associated morbidity and mortality rate in a recent series of 180 patients. 20 Given the uncertainty surrounding the yield of repeat DSA in patients with negative initial angiography, protocols have varied widely across different institutions. Because of the dreaded complications related to untreated ruptured cerebral aneurysms, our neurovascular center undertakes a diagnostic protocol of repeat DSA at 1- and 6-week intervals after negative initial DSA. In addition, all patients complete an magnetic resonance image (MRI) of the brain and cervical spine and MRA of the head within 24 hours of the negative catheter angiography. The purpose of this study was to investigate the diagnostic yield of short (1 week) and long-term (6 weeks) catheter angiography in atraumatic SAH with negative initial angiography in an era of advanced noninvasive imaging technologies. Furthermore, we evaluated the clinical outcome of 254 patients with SAH and negative initial catheter angiography. We also analyzed and discussed the complications, outcomes, and discovered origins of occult SAH based on the hemorrhage pattern on initial CT. PATIENTS AND METHODS Approval from the Institutional Review Board was filed and granted for the retrospective data review of our study. From a prospectively collected database, we reviewed 254 consecutive patients with atraumatic SAH admitted to our institution from 2003 to 2011 who had no vascular source identified on initial 6-vessel DSA. Hemorrhage patterns on initial head CT were carefully reviewed and categorized by a radiologist and a neurosurgeon as PM or NPM on the basis of criteria established by van Gijn et al. 14 Patients with a traumatic source of SAH were systematically excluded from the analysis. All patients underwent biplane DSA within 24 hours of admission that was negative for a vascular source of SAH. Angiography included a thorough inspection of all 6 vessels bilateral internal, external, and vertebral arteries with selective catheterization of all 6 vessels. Threedimensional reconstruction of intracranial vessels was obtained on follow-up angiography. MRI of the brain and cervical spine and MRA of the brain were performed in all patients within 24 hours from the initial angiography in search for a vascular source for the bleeding. MRI was performed outside the 24-hour window only in patients who could not tolerate the study because of high intracranial pressures when lying flat for extended periods of time. Negative MRI/MRA reports were then followed by repeat 6-vessel DSA at the 1-week interval. Patients with positive findings on the first follow-up angiography were treated immediately. Patients with another negative DSA received a third and final catheter angiogram at an approximately 6-week interval from the initial study. Catheter angiography yield was determined for every subsequent angiogram. CTA was not routinely used as part of our institutional protocol. Besides their hemorrhage pattern, patients were further categorized on the basis of their Hunt and Hess (HH) grade, and the incidence of hydrocephalus, rehemorrhage, vasospasm, and shunting was determined by the attending neurosurgeon of record. RESULTS A total of 254 patients met the study criteria. Of those, 118 (46.5%) were PM-type SAH on initial head CT and 136 (53.5%) were NPM-type SAH (Table 1). The HH scores were as follows: grade I in 147 patients (57.8%), grade II in 10 patients (3.9%), grade III in 78 patients (30.7%), grade IV in 17 patients (6.7%), and grade V in 2 patients (0.8%) initially, which improved to a lower grade after external ventriculostomy. Patients with advanced HH scores (III-V) included 23 patients (23.7%) with PM SAH and 74 patients (76.3%) with NPM SAH. A comparison between NPM and PM SAH patients showed that the latter had a lower incidence of rehemorrhage (1.5% vs 0%), radiographic vasospasm (13.2% vs 8.5%), need for external ventriculostomy (37.5% vs 16%), and hydrocephalus requiring ventriculoperitoneal shunting (21.3% vs 6.8%; Table 1). A vascular source for the SAH was identified in 17 patients (6.7%) with initially negative DSA. In no patient with follow-up angiography was MRI diagnostic for an aneurysmal source of SAH. Of those, 10 were identified with the first follow-up DSA, and the diagnostic yield of short-term repeat angiography in 1 week was found to be 3.9% (Table 2). All 10 patients were in the NPM group (Figures 1 and 2). One hundred seventy-four patients (85 with PM SAH and 89 with NPM SAH) with 2 negative DSA procedures underwent long-term follow-up angiography at 6 weeks, which revealed a vascular source in 7 patients for a yield of 4% (Table 3). All 7 patients were also in the NPM group. The overall diagnostic yield of repeat angiography was 0% in the PM group and 12.5% in the NPM group. The diagnostic yield of short-term and long-term repeat DSA in patients with NPM SAH was 7.3% and 7.8%, respectively. TABLE 1. Patient Characteristics of Initial Hemorrhagic Pattern a NPM, n (%) PM, n (%) Total patients HH grade III-V 74 (54.4) 23 (19.5) IVH 66 (48.5) 0 EVD required 51 (37.5) 19 (16) VPS 29 (21.3) 8 (6.8) Radiographic vasospasm 18 (13.2) 10 (8.5) Rebleed 2 (1.5) 0 a EVD, external ventricular drain; HH, Hunt and Hess; IVH, intraventricular hemorrhage; NPM, nonperimesencephalic; PM, perimesencephalic; VPS, ventriculoperitoneal shunt. NEUROSURGERY VOLUME 72 NUMBER 4 APRIL

3 DALYAI ET AL TABLE 2. Short-term Angiographic Positive Findings a Patient Angiograms, n Source Treatment 1 2 P1 aneurysm Stent/coil 2 2 Anterior choroidal Clip/wrap aneurysm 3 2 Distal PICA aneurysm WDOC/no treatment 4 2 Vertebral artery Coil aneurysm 5 2 Basilar Clip pseudoaneurysm 6 2 ACOM aneurysm Clip 7 2 ACOM aneurysm Coil 8 2 Pericallosal aneurysm Clip 9 2 PICA aneurysm Onyx ACOM aneurysm Clip a ACOM, anterior communicating artery; DHC, decompressive hemicraniectomy; ICA, internal carotid artery; PICA, posterior inferior cerebellar artery; WDOC, withdrawal of care. The reasons for missing the lesion on the initial negative angiograms were as follows: lesion not filling with contrast (n = 5), vasospasm (n = 2), suboptimal angiographic projection (n = 4), partially thrombosed aneurysm (n = 3), and larger protuberance (n = 3). Of note, 9 of the 17 patients did not have 3-D reconstruction of the initial DSA. In 4 of 17 patients, 1-week or 6-week DSA was performed in a more thorough manner than the first DSA. DISCUSSION Key Results The results of this study show that, in the patient population with initial negative catheter angiography, NPM patients experience a higher incidence of neurological complications and sequelae related to SAH compared with their PM counterparts. The overall yield of repeat catheter angiography in SAH with initial negative angiography was 6.7%. Specifically, NPM patients had a high yield of repeat DSA (12.5%), whereas PM patients had a 0% yield of repeat DSA. The yield of short- and long-term repeat angiography was grossly similar (approximately 4%). Interpretation SAH with negative initial catheter angiography accounts for approximately 10% to 20% of all atraumatic SAH This represents a significant patient population with limited data on the natural history, prognosis, or diagnostic workup. Traditionally, angiogram-negative SAH was thought to portend a benign natural history. 22,24 Case series have investigated the outcome of angiogram-negative SAH on the basis of the initial noncontrast head CT. 6,8,10,11 Most patients with PM-type hemorrhages have favorable clinical outcomes, which questions the need for aggressive diagnostic workup. 6,7,11 This study proposes a thorough and aggressive diagnostic follow-up of these patients with both short- and long-term catheter angiography. It also provides particular insight into the diagnostic yield of repeat angiograms in both angiogram-negative PM hemorrhages and those with a more diffuse bleeding pattern. Rinkel and colleagues 32,33 were among the first to differentiate PM hemorrhages from the remaining SAH population, demonstrating a benign medical course and low probability of associated vascular abnormalities. Recent evidence suggests a venous origin for most of these hemorrhages. 34 A small cavernoma was considered the source of hemorrhage in a recent case report. 36 The prevalence of this subpopulation was estimated at 66% of all angiogram-negative patients. 13 Although traditionally considered benign, PM hemorrhage has recently been associated with several neurological complications of SAH. Hui et al 26 have reported that 9.6% of PM SAH patients required a ventriculostomy and a similar percentage was medically treated for clinical vasospasm. These patients are further subject to complex neuropsychological FIGURE 1. A 54-year-old female patient presented with Hunt and Hess grade III nonperimesencephalic hemorrhage on initial head computed tomography. Negative initial angiography in the frontal projection (A) with 3-dimensional reconstruction (B). Magnetic resonance imaging/angiography was nondiagnostic for vascular source. Short-term angiography at 7 days in the frontal projection (C) and 3-dimensional reconstruction (D) identified a 3-mm anterior communicating artery aneurysm that was successfully treated with coil embolization. 648 VOLUME 72 NUMBER 4 APRIL

4 ANGIOGRAM NEGATIVE SAH: YIELD OF REPEAT DSA FIGURE 2. A 57-year-old female patient presented with Hunt and Hess grade III nonperimesencephalic hemorrhage on initial head computed tomography (A). Lateral projection (B) of negative initial angiography of posterior circulation. Lateral projection (C) of short-term follow-up angiography identifying a 5-mm right posterior inferior cerebellar artery (PICA) aneurysm. Lateral projection (D) of right PICA aneurysm after successful Onyx 34 embolization. deficits from SAH sequelae. 30 Overall, they reported favorable clinical outcomes in 96% of this patient population with return to independent living. The risk of rebleeding from PM SAH is minimal and documented in few case reports. 31 DSA is known to have an average sensitivity of 99% and negative predictive value of 96% to 98%. 10,16-18 Studies have found that 10% to 16% of posterior circulation skull base ruptured aneurysms present with a PM pattern on initial head CT. 2,17,18,27 These statistics suggest the need for vascular imaging with the highest accuracy to promptly diagnose and treat patients with a potentially identifiable vascular source for SAH. Among the 118 patients with PM SAH in our series, a significant percentage required intensive medical and, at times, surgical interventions as a result of SAH-related morbidities. Twenty-three patients (19.5%) initially presented as HH grade III or greater with an altered mental status. Although Ildan et al 5 reported a 1% incidence of shunt-dependent hydrocephalus in patients with PM SAH, we found that 19 of 118 patients (16%) required a ventriculostomy for hydrocephalus or poor clinical grade. Furthermore, 8 patients (6.8%) with PM hemorrhage TABLE 3. Long-term Angiographic Positive Findings a Patient Angiograms, n Source Treatment 1 3 ACOM aneurysm Clip/wrap 2 3 Basilar Stent/coil pseudoaneurysm 3 3 PICA AVF NBCA embolization 4 3 Distal PCA aneurysm Coil 5 3 MCA aneurysm Clip 6 3 MCA aneurysm Clip 7 3 Vertebral aneurysm Clip a ACOM, anterior communicating artery; AVF, arteriovenous fistula; MCA, middle cerebral artery; NBCA, N-butyl cyanoacrylate; PCA, posterior cerebral artery; PICA, posterior inferior cerebellar artery. eventually required permanent cerebrospinal fluid diversion, and 10 patients (8.5%) had increased middle cerebral artery velocities (.200 cm/s and Lindegaard ratio.3) and radiographic vasospasm on repeat angiograms. However, none required endovascular angioplasty or other procedural interventions for the treatment of clinical vasospasm. The rate of vasospasm after PM SAH was found to be 2.2% by Andaluz and Zuccarello. 3 The same authors found positive findings on DSA for a vascular source in 13.9% of patients with PM SAH. However, their protocol was not standardized with regard to follow-up angiography, and only 35 of 45 patients received a second angiogram after a negative initial DSA. These findings suggested that PM SAH and its neurological sequelae should be diagnosed and treated aggressively, similar to other SAH. We found no patient with PM SAH and negative initial angiography to harbor an occult vascular source on short- or long-term repeat angiography, which may call into question the necessity of subsequent angiography (DSA or CTA) in this patient population. Generally, patients with a more diffuse pattern of hemorrhage on head CT (NPM SAH) and no vascular source on initial angiogram have a clinical course similar to that of patients with SAH from known ruptured aneurysms. Andaluz and Zuccarello 3 reported poor outcomes in 36% of these patients. Similarly, Ruigrok et al 8 reported worse conditions on arrival, clinical course, morbidities, and long-term outcomes compared with patients with PM hemorrhages. Our findings with regard to this patient population were largely similar. We found a 12.5% yield of short- and long-term follow-up angiography in NPM SAH patients. NPM SAH patients presented with a Hunt and Hess grade between III and V in 54% of cases and were more likely to experience radiographic vasospasm and hydrocephalus requiring external ventriculostomy/ cerebrospinal fluid diversion compared with their PM counterparts. Most worrisome, 2 patients with NPM SAH had clinically significant rebleeding episodes (1 patient after 1 week, and the other after 2 weeks). These patients are of great concern and NEUROSURGERY VOLUME 72 NUMBER 4 APRIL

5 DALYAI ET AL provide the rationale for a complete diagnostic workup for a vascular source to prevent such potentially life-devastating events. Repeat imaging for initial angiogram-negative SAH is controversial because of the various diagnostic modalities and lack of a clear consensus on yield. Some centers have proposed the use of CTA to triage all SAH patients and defer the use of DSA in patients with a PM SAH. 25 Ruigrok et al 7 suggested a mathematical model to estimate the utility of the diagnostic workup for PM SAH and recommend CTA imaging only. However, the analysis focused on a low prevalence (4%) of vertebrobasilar aneurysms in PM SAH while potentially overestimating the sensitivity of CTA (97%) for detecting aneurysms in this patient population. Furthermore, their reported complication rate for catheter angiography was 2.5%, whereas reports have shown that in most high-volume vascular centers it is,1%. 23 In PM SAH, Agid et al 21 reported a CTA false-negative rate of 10%, but all of these presented with a diffuse pattern of blood on initial head CT. Westerlaan et al 35 similarly reported 60 patients with negative findings on CTA and found 5 of 17 patients (29%) with NPM SAH to have a vascular source on DSA. Other case series have investigated a paradigm similar to the one in this study but with a single short-term repeat angiography. Our series proposes a second long-term repeat catheter angiogram, especially for patients with NPM-type SAH. Delayed SAH resorption and resolution of radiographic vasospasm could explain the 12.5% diagnostic yield of follow-up angiography. The diagnostic yield of repeat vascular imaging has varied greatly in the literature, and many reports predate the common use of 3-D rotational angiography and advanced MRI (contrastenhanced circle of Willis, 4-dimensional tracks). Studies have reported a 20% incidence of positive vascular findings on repeat angiography for NPM hemorrhage. 3 The incidence of positive findings on a third long-term follow-up DSA has been reported to be between 7% and 10%. 3,5,8,12,13 These studies contribute to our understanding of this population, which is still limited by study protocols predating 3-D rotational angiography, 27-29,37 small sample sizes, 26,38 inconsistent imaging protocols, 39 or lack of long-term angiographic follow-up for most patients. 3,40,41 Our protocol ultimately identified a 7.3% yield for short-term followup angiography and 7.8% yield for long-term 6-week follow-up DSA in patients with NPM SAH. This significant yield on longterm follow-up angiography highlights the need for aggressive angiographic follow-up in NPM SAH patients. The results of this study propose a systematic approach to SAH patients with initially negative catheter angiography. In a neurointerventional era when angiography complication rates are #1%, further aggressive work-up of patients with NPM is strongly indicated. 23 Our recommendations consist of repeat angiography in 1 week after initially negative angiography in these patients. We also recommend longterm follow-up angiography at 6 weeks, outside the period of cerebral vasospasm, considering the reported 7.8% yield on final long-term angiography. Limitations We recognize the inherent limitations of this study based on its retrospective data collection. Because 3-D reconstruction was not performed on the initial angiogram in a few patients, some aneurysms could have potentially been missed initially, and this may have slightly overestimated the diagnostic yield of repeat angiography. Generalizability Our results reflect the experience of a single institution and may not be generalizable to other centers. Our protocol does not include a preoperative or postoperative CTA in patients with angiogram-negative SAH. As a result, we cannot contrast the yield of CTA in the same patient series or compare our results with a CTA series. Because catheter angiography has been reported to have higher diagnostic power compared with conventional CTA, we believe that CTA after initially negative DSA carries additional risk of dye-related renal toxicity with little or no additional diagnostic benefit. Additional studies comparing newer diagnostic techniques such as subtraction 320-detector CTA and conventional angiography are required to further investigate diagnostic imaging in this patient population. CONCLUSION We found that, in the patient population with initial negative catheter angiography, NPM patients experience a higher incidence of neurological complications and sequelae related to SAH compared with their PM counterparts, including hydrocephalus requiring external ventriculostomy or permanent cerebrospinal fluid diversion and radiographic vasospasm on repeat angiography. We report the overall yield of repeat catheter angiography in SAH with initial negative angiography to be 6.7%. This includes short-term (1 week) and long-term (6 weeks) repeat angiography. Patients with NPM SAH had a high yield of repeat DSA (12.5%), whereas patients with PM SAH had a 0% yield of repeat DSA. Therefore, we propose follow-up catheter angiography at both intervals only in patients with NPM hemorrhage. This proposed protocol should be carried out in institutions with low angiographic complication rates. Our results, however, do not support an aggressive protocol of repeat angiography in patients with PM SAH. Disclosures Dr Jabbour has been a consultant for ev3, Codman, and Mizuho. Dr Tjoumakaris has been a consultant for Stryker. Dr Gonzalez has been a consultant for ev3. Dr Dumont has been a consultant for ev3 and Stryker. Dr Rosenwasser has been a consultant for Boston Scientific. The other authors have no personal financial or institutional interest in any of the drugs, materials, or devices described in this article. REFERENCES 1. Abu Bakar I, Shuaib IL, Mohd Ariff AR, Naing NN, Abdullah JM. Diagnostic cerebral angiography in spontaneous intracranial haemorrhage: a guide for developing countries. Asian J Surg. 2005;28(1): VOLUME 72 NUMBER 4 APRIL

6 ANGIOGRAM NEGATIVE SAH: YIELD OF REPEAT DSA 2. Bederson JB, Connolly ES Jr, Batjer HH, et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40(3): Andaluz N, Zuccarello M. Yield of further diagnostic work-up of cryptogenic subarachnoid hemorrhage based on bleeding patterns on computed tomographic scans. Neurosurgery. 2008;62(5): ; discussion Hashimoto H, Iida J, Hironaka Y, Okada M, Sakaki T. Use of spiral computerized tomography angiography in patients with subarachnoid hemorrhage in whom subtraction angiography did not reveal cerebral aneurysms. J Neurosurg. 2000;92 (2): Ildan F, Tuna M, Erman T, Gocer AI, Cetinalp E, Burgut R. Prognosis and prognostic factors for unexplained subarachnoid hemorrhage: review of 84 cases. Neurosurgery. 2002;50(5): ; discussion Rinkel GJ, Velthuis BK. 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AJNR Am J Neuroradiol. 2008;29(5): Ishihara H, Kato S, Akimura T, Suehiro E, Oku T, Suzuki M. Angiogram-negative subarachnoid hemorrhage in the era of three dimensional rotational angiography. J Clin Neurosci. 2007;14(3): Whiting J, Reavey-Cantwell J, Velat G, et al. Clinical course of nontraumatic, nonaneurysmal subarachnoid hemorrhage: a single-institution experience. Neurosurg Focus. 2009;26(5):E21. COMMENTS This article is a retrospective review of patients presenting with subarachnoid hemorrhage with an initial negative angiogram. The authors have broken down the subarachnoid hemorrhage into perimesencephalic and nonperimesencephalic type of hemorrhage and have looked at the importance of performing repeat angiography in 1 week and again in 6 weeks. As this article nicely points out, perimesencephalic-type hemorrhage is a more benign entity, and the risk of subsequent shunting and vasospasm and the chance of finding an arterial sourceofthehemorrhagearelow.ontheotherhand,whenthesubarachnoid hemorrhage extends beyond the perimesencephalic area, the risks of needing a ventriculoperitoneal shunt and of vasospasm and the chance of finding, for instance, an aneurysm in a delayed fashion increase. This article reinforces our belief that nonperimesencephalic NEUROSURGERY VOLUME 72 NUMBER 4 APRIL

7 DALYAI ET AL type of subarachnoid hemorrhage with negative angiogram findings needs more short- and long-term angiographic follow-up. At our institution, the long-term angiogram tends to be a computed tomography angiogram because it is less invasive than the conventional catheter angiogram, and with 3-dimensional reconstruction, the sensitivity of this imaging modality is very high. Roham Moftakhar Chicago, Illinois This is a retrospective review of patients presenting with subarachnoid hemorrhage with an initial negative angiogram. The authors analyze the outcome of 258 consecutive patients between The authors divide the patients into 2 groups perimesencephalic and nonperimesencephalic type of hemorrhage. Angiograms were performed at the time of initial hemorrhage, one week, and again in 6 weeks. The overall diagnostic yield of repeat angiography in the perimesencephalic group was 0% and 15% in the nonperimesencephalic group. This article reinforces that short and long-term angiographic follow-up is not needed for perimesencephalic hemorrhage. The diagnostic yield on the initial angiograms may have been higher in the nonperimesencephalic group if 3-dimensional imaging was performed in all cases and 2 staff had reviewed the images. Joseph Gemmete Ann Arbor, Michigan 652 VOLUME 72 NUMBER 4 APRIL