Clinical Neurology and Neurosurgery 137 (2015) 67–71
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Quadrigeminal perimesencephalic subarachnoid hemorrhage Adam N. Wallace a,∗ , Ross Vyhmeister b , Ryan Viets c , Justin T. Whisenant d , Arindam R. Chatterjee a , Akash P. Kansagra a , DeWitte T. Cross III a , Christopher J. Moran a , Colin P. Derdeyn a a
Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 South Kingshighway Boulevard, Saint Louis, MO 63110, United States Washington University School of Medicine, Saint Louis, MO, United States Sharp Grossmont Hospital, San Diego, CA, United States d Texas Radiology Associates, Plano, TX, United States b c
a r t i c l e
i n f o
Article history: Received 12 March 2015 Received in revised form 23 June 2015 Accepted 24 June 2015 Available online 27 June 2015 Keywords: Quadrigeminal perimesencephalic subarachnoid hemorrhage Perimesencephalic subarachnoid hemorrhage Nonaneurysmal subarachnoid hemorrhage Aneurysm Digital subtraction angiography Computed tomography angiography
a b s t r a c t Objective: A variant of perimesencephalic subarachnoid hemorrhage (PSAH) has been described characterized by blood centered in the quadrigeminal cistern and limited to the superior vermian and perimesencephalic cisterns. Herein, three cases of quadrigeminal PSAH are presented. Materials and methods: Medical records of all patients who underwent digital subtraction angiography for evaluation of non-traumatic SAH between July 2002 and April 2012 were reviewed. Patients with anterior circulation aneurysms were excluded. Two blinded reviewers identified admission noncontrast CT scans with pretruncal and quadrigeminal patterns of PSAH. Results: The total cohort included 106 patients: 53% (56/106) with one or more negative digital subtraction angiograms and 47% (50/106) with posterior circulation or posterior communicating artery aneurysms. Three patients with quadrigeminal PSAH were identified, two with nonaneurysmal SAH and one with a posterior circulation aneurysm. Seventeen patients (16%; 17/106) with pretruncal PSAH were identified, none of whom were found to have an aneurysm. The quadrigeminal pattern comprised 11% (2/19) of cases of pretruncal or quadrigeminal nonaneurysmal PSAH. Conclusion: A small subset of patients with nonaneurysmal PSAH present with blood centered in the quadrigeminal cistern, and the etiology of this pattern may be similar to that of the classic pretruncal variant. However, patients with quadrigeminal PSAH must still undergo thorough vascular imaging, including at least two digital subtraction angiograms, to exclude a ruptured aneurysm. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Perimesencephalic subarachnoid hemorrhage (PSAH) is classically described as blood mostly confined to the perimesencephalic cisterns and centered immediately anterior to the brainstem on initial noncontrast CT [1–2]. The low prevalence of aneurysms and benign clinical courses of patients with this pattern of SAH have clinical implications in terms of follow-up imaging and patient reassurance [3–7]. Several case reports describe another form of nonaneurysmal SAH characterized by blood centered in the quadrigeminal cistern and limited to the superior cerebellar and perimesencephalic cisterns [1,8–12]. These patients have had benign clinical courses with no incidences of vasospasm, hydrocephalus, or other common complications after aneurysmal SAH.
∗ Corresponding author. Tel.: +1 608 347 0294; fax: +1 314 454 9417. E-mail address: [email protected] (A.N. Wallace). http://dx.doi.org/10.1016/j.clineuro.2015.06.018 0303-8467/© 2015 Elsevier B.V. All rights reserved.
As a result, it has been proposed that nonaneurysmal PSAH be used as an umbrella term that includes both the classic definition of PSAH with blood centered anterior to the brainstem, as well as the quadrigeminal variant [11]. However, little is known about quadrigeminal PSAH, including whether it represents a distinct etiologic entity or a variant of pretruncal PSAH that should be managed similarly. Herein, three cases of quadrigeminal perimesencephalic SAH are presented.
2. Methods Institutional review board approval was obtained to retrospectively review the medical records of all patients who underwent digital subtraction angiography (DSA) at Barnes Jewish Hospital between July 2002 and April 2012. Inclusion criteria required a noncontrast head CT demonstrating SAH. Patients with a history of head trauma were excluded. Patients presenting more than 72 h
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Fig. 1. Noncontrast CT images demonstrate subarachnoid hemorrhage centered in the quadrigeminal cistern (A; black arrow) and extending around the brainstem into the prepontine cistern (B; white arrow). No aneurysm or other cause of subarachnoid hemorrhage was found on two digital subtraction angiograms or one CT angiogram.
after onset of symptoms were also excluded. This cohort was previously used to test the inter-observer variability and specificity for nonaneurysmal SAH of an anatomic definition of PSAH [13]. The standard practice at our institution is to pursue DSA on all patients with nontraumatic SAH in whom an aneurysm is suspected. The only patients that do not undergo DSA are (1) those with severe neurologic injury with little likelihood of meaningful recovery (at least Hunt-Hess grade 5); (2) those with acute mass effect, in which case CT angiography (CTA) may be performed on the way to the operating room; and (3) some patients with convexity SAH [13]. Patients with anterior circulation aneurysms found on DSA were excluded from this review. Digital subtraction angiography was performed on one of two Axiom Artis Biplane neuroangiographic suites (Siemens Healthcare, Forchheim, Germany) by one of three interventional neuroradiologists. A typical procedure involves conscious sedation, a 5-french femoral arterial sheath and 5-french diagnostic catheter. Three- or four-vessel DSA was obtained in all patients with care taken to image both intracranial vertebral arteries, either by reflux down the contralateral vessel or direct selection of both vertebral arteries in the neck. A rotational angiogram with three-dimensional reconstruction was obtained if a lesion was suspected. Angiography was repeated 7 days after initial presentation to reassess for a missed aneurysm and/or as a surveillance procedure for SAH-induced vasospasm [6,14]. Some patients with negative DSA underwent CTA as well. Dictated reports from these examinations were reviewed for the present study. Two board certified, fellowship trained neuroradiologists blinded to the angiographic findings independently reviewed every case and identified initial noncontrast CT scans with blood centered in the quadrigeminal cistern with extension limited to the ambient, crural, and/or superior cerebellar cisterns. The reviewers categorized the remaining initial CT scans as pretruncal PSAH or nonperimesencephalic SAH (NPSAH) according to previously described anatomic criteria [13]. Assessment differences were resolved by consensus. The electronic medical records of patients with a quadrigeminal pattern of PSAH were reviewed for additional epidemiologic and clinical information and the results of additional neuroimaging.
3. Results The total cohort included 106 patients: 53% (56/106) with one or more negative digital subtraction angiograms and 47% (50/106) with posterior circulation or posterior communicating artery aneurysms. The same three cases of quadrigeminal PSAH were identified by both reviewing neuroradiologists. Two of these patients did not have an identifiable source of SAH and one was found to have a posterior circulation aneurysm on subsequent vascular imaging. The reviewers categorized the initial CT scans of 17 patients (16%; 17/106) as pretruncal PSAH. None of these patients were found to have an aneurysm. Thus, the quadrigeminal pattern comprised 11% (2/19) of cases of pretruncal or quadrigeminal nonaneurysmal PSAH. Each of the three patients with a quadrigeminal perimesencephalic pattern of SAH is described in more detail. 3.1. Case 1 The first patient was a 58-year old African-American man who presented after the sudden onset of diffuse headache with associated nausea, photophobia, and meningismus. Noncontrast CT performed the same day as symptom onset demonstrated SAH centered in the quadrigeminal cistern and extending laterally around the brainstem (Fig. 1A and B). Digital subtraction angiography performed the following morning showed no aneurysm or other source of SAH. Computed tomographic angiography performed the following day was also negative. Repeat DSA performed on day 8 of hospitalization was again negative for a source of SAH. During his 9-day hospitalization he suffered no SAH-induced complications, such as clinically significant vasospasm or hydrocephalus, and demonstrated complete recovery at 1-month follow-up. After 3 years of clinical follow-up, he has not experienced another episode of SAH. 3.2. Case 2 The second patient was a 52-year old Caucasian woman with a history of hypertension who presented after the sudden onset of right temporal headache radiating down her right neck with
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cerebral artery (MCA) atherosclerotic narrowing with extensive pial collaterals from the right posterior cerebral artery (PCA) to the distal right MCA vascular territory. Computed tomographic angiography performed the following day also did not show an aneurysm. Repeat DSA performed on day 8 of hospitalization did not demonstrate any new findings. She was discharged after an uneventful 9-day hospitalization, and demonstrated complete recovery at 1month follow-up. 3.3. Case 3
Fig. 2. Noncontrast CT images demonstrate subarachnoid hemorrhage centered in the quadrigeminal cistern and extending laterally around the brainstem (white arrow). Digital subtraction angiography revealed severe atherosclerotic narrowing of the M2 segment of the right middle cerebral artery, but no source of subarachnoid hemorrhage. Repeat digital subtraction and CT angiography were also negative for a source of subarachnoid hemorrhage.
associated nausea and vomiting. Noncontrast CT performed the same day as symptom onset demonstrated SAH centered in the quadrigeminal cistern and extending laterally around the brainstem (Fig. 2). Digital subtraction angiography performed the same day did not reveal an aneurysm, but did show severe right middle
The third patient was a 40-year old African-American woman who presented after 4 days of mild occipital headache that acutely worsened the day of admission after using cocaine. Noncontrast CT demonstrated SAH centered in the quadrigeminal cistern and extending into the ambient cisterns bilaterally (Fig. 3A). Digital subtraction angiography performed the same day demonstrated irregularity of the distal branches of the intracranial arteries, most prominent in the left PCA distribution, consistent with drug-induced vasculopathy or vasospasm. Computed tomographic angiography performed the following day did also not reveal a cause for SAH. On day 3 of hospitalization, she developed hydrocephalus requiring placement of an external ventricular drain (EVD). Repeat DSA performed on day 6 of hospitalization demonstrated a 2.5-mm dissecting aneurysm at the junction of the P2 and P3 segments of the left PCA, which was successfully embolized with preservation of flow to the distal PCA (Fig. 3B). The EVD was weaned and eventually removed. The remainder of her recovery was uneventful and she was discharged on day 13 of hospitalization. Over 3 years of subsequent clinical follow-up she continued to have chronic headaches that were successfully managed with medication. 4. Discussion Early case series of patients with nonaneurysmal PSAH included two patients with blood centered in the quadrigeminal cistern
Fig. 3. Noncontrast CT image demonstrates subarachnoid hemorrhage centered in the quadrigeminal cistern (A; black arrows). Rotational digital subtraction angiography with three-dimensional reconstruction during right vertebral artery injection demonstrates a 2.5-mm dissecting aneurysm at the left P2–P3 junction (B; white arrow).
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and well-documented benign clinical outcomes [1,10]. In 2000, Schwartz et al. reported a prevalence of quadrigeminal nonaneurysmal PSAH of 0.9% (2/220) among patients with SAH and 22% (2/9) among patients with nonaneurysmal PSAH [12]. The first of these patients underwent four-vessel DSA and MR angiography (MRA) and did not rebleed during 24 months of follow-up. The second patient underwent two four-vessel digital subtraction angiograms and MRA, and did not rebleed during 18 months of follow-up. Schwartz et al. later reported a third patient with quadrigeminal nonaneurysmal PSAH who underwent two fourvessel digital subtraction angiograms and CTA, and did not rebleed during 12 months of follow-up [11]. However, Wijdicks et al. have argued against the existence of a quadrigeminal variant of nonaneurysmal PSAH, insisting that the etiology is either traumatic or a posterior circulation aneurysm [16]. The present study supports the existence of a quadrigeminal variant of nonaneurysmal PSAH, though the etiology remains uncertain. Our first two patients with quadrigeminal PSAH underwent two digital subtraction angiograms and CTA, none of which identified a source of hemorrhage. These patients presented in good clinical condition and had benign clinical courses similar to other reported cases of quadrigeminal and pretruncal nonaneurysmal PSAH. These clinical similarities suggest that both patterns of hemorrhage are due to a non-arterial source [2]. An association between pretruncal nonaneurysmal PSAH and abnormal venous anatomy has led to the hypothesis that the etiology is a venous rupture secondary to central cerebral venous hypertension [15–18]. For example, patients with pretruncal nonaneurysmal PSAH are more likely to have variant Basal vein of Rosenthal drainage into a dural venous sinus via a perimesencephalic bridging vein [21]. Perhaps the pretruncal pattern of PSAH is more common than the quadrigeminal pattern because the bridging vein that ruptures is more commonly located anterior to the brainstem. Alternatively, both patterns may be due to a variety of nonaneurysmal etiologies. In addition to a venous bleed, other proposed etiologies of nonaneurysmal SAH include a ruptured perforating artery, intraluminal dissection, capillary telangiectasia, and cavernous malformation [19]. If nonaneurysmal PSAH is used as an umbrella term to include both the classic pretruncal and quadrigeminal variants, then the quadrigeminal variant accounted for 11% (2/19) of cases of nonaneurysmal PSAH in this series. This is smaller than the 22% (2/9) prevalence reported by Schwartz et al., though neither number is expected to be accurate given the small sample sizes. Additionally, Schwartz et al. used the definition of PSAH described by Rinkel et al. [23], while this series used more objective, anatomic criteria [13]. Still, one can reasonably conclude from these series that patients with a quadrigeminal pattern likely comprise a small but substantial percentage of the umbrella population with nonaneurysmal PSAH, and this subgroup deserves greater attention in future studies. However, even if quadrigeminal and pretruncal nonaneurysmal PSAH share a common etiology, this does not imply that quadrigeminal and pretruncal PSAH should be evaluated the same way. In a recently published meta-analysis of 40 studies with 1,031 patients with pretruncal PSAH and initial negative DSA or CTA, the rate of aneurysm detection on follow-up DSA and/or CTA was 0.78% (8/1031; 95% confidence interval, 0.23–1.32%). Additionally, comparison of different imaging strategies found no statistically significant benefit of performing DSA during initial or follow-up evaluation of these patients. The authors concluded that patients with pretruncal PSAH and presentations compatible with a nonaneurysmal etiology can undergo initial evaluation with CTA alone and do not require follow-up imaging [20]. This meta-analysis is limited by inconsistent definitions of PSAH used in the constituent studies, and clinical implementation of such recommendations is
limited by inter-observer variability in terms of characterizing SAH patterns [21,22]. Regardless, extending such recommendations to patients with quadrigeminal PSAH is premature. In the present series, one of the three patients identified with a quadrigeminal pattern of PSAH on initial noncontrast CT was found to have a 2.5-mm dissecting posterior cerebral artery aneurysm. Moreover, this aneurysm was detected on a second digital subtraction angiogram after initial DSA and CTA were both negative. In a previous case series, 2.7% (3/113) of patients with posterior circulation aneurysms initially presented with a quadrigeminal pattern of PSAH [23,24]. We recommend that quadrigeminal PSAH be evaluated like NPSAH with DSA within 24 h of presentation. If initial DSA is negative, CTA is a potentially useful adjunct study. In a 2012 study that included 43 patients with NPSAH and negative initial DSA, CTA identified a causative cerebral aneurysm in 9.3% (4/43) of cases [6]. If initial CTA and DSA are both negative, repeat DSA is recommended. In a pooled analysis of 8 studies with 368 patients with NPSAH and negative initial evaluation with DSA and CTA, the yield of repeat DSA was 10.0% (37/368; 95% confidence interval, 7.4%–13.6%). Thus, in these patients, the potential morbidity and mortality associated with rerupture of an aneurysm that is not detected on initial imaging far outweighs the risk of repeat DSA [25]. The timing of repeat DSA in the studies comprising this pooled analysis ranged from 1 to 6 weeks. Our practice is to repeat DSA 5–10 days after the initial study, at which time it also reasonable to screen for SAH-induced vasospasm [26]. During this interval, patients should be monitored in a neurosurgical intensive care unit for signs of rerupture of an aneurysm missed on initial imaging and complications of SAH [27,28]. This study is limited by the fact that it is retrospective and the number of cases of quadrigeminal PSAH was small. Additionally, the true prevalence of quadrigeminal PSAH cannot be determined from our cohort, because patients with anterior circulation aneurysms were excluded. Similarly, clinical considerations introduced selection bias into the data. At our institution, DSA is the modality of choice for the diagnosis of cerebral aneurysms, but patients with severe neurological injury and a poor prognosis and those with large parenchymal hematomas and acute neurological decline do not always undergo DSA. However, neither of these groups of patients is likely to have quadrigeminal PSAH. 5. Conclusion A small subset of patients with nonaneurysmal PSAH present with blood centered in the quadrigeminal cistern, and the etiology of this pattern may be similar to that of the classic pretruncal variant. However, patients with quadrigeminal PSAH must still undergo thorough vascular imaging, including at least two DSAs, to exclude a ruptured aneurysm. This work was performed at the Mallinckrodt Institute of Radiology, St Louis, MO. No financial support was provided for the publication of this manuscript. References [1] J. van Gijn, K.J. van Dongen, M. Vermeulen, A. Hijdra, Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage, Neurology 35 (1985) 493–497. [2] Y.W. Kim, M.F. Lawson, B.L. Hoh, Nonaneurysmal subarachnoid hemorrhage: an update, Curr. Atheroscler. Rep. 14 (2012) 328–334. [3] B.K. Velthuis, G.J. Rinkel, L.M. Ramos, T.D. Witkamp, M.S. van Leeuwen, Perimesencephalic hemorrhage. Exclusion of vertebrobasilar aneurysms with CT angiography, Stroke 30 (1999) 1103–1109. [4] R. Agid, T. Andersson, H. Almqvist, R.A. Willinsky, S.K. Lee, K.G. terBrugge, R.I. Farb, M. Soderman, C.T. Negative, angiography findings in patients with spontaneous subarachnoid hemorrhage: when is digital subtraction angiography still needed? AJNR 31 (2010) 696–705.
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Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Quadrigeminal perimesencephalic subarachnoid hemorrhage Adam N. Wallace a,∗ , Ross Vyhmeister b , Ryan Viets c , Justin T. Whisenant d , Arindam R. Chatterjee a , Akash P. Kansagra a , DeWitte T. Cross III a , Christopher J. Moran a , Colin P. Derdeyn a a
Mallinckrodt Institute of Radiology, Washington University School of Medicine, 510 South Kingshighway Boulevard, Saint Louis, MO 63110, United States Washington University School of Medicine, Saint Louis, MO, United States Sharp Grossmont Hospital, San Diego, CA, United States d Texas Radiology Associates, Plano, TX, United States b c
a r t i c l e
i n f o
Article history: Received 12 March 2015 Received in revised form 23 June 2015 Accepted 24 June 2015 Available online 27 June 2015 Keywords: Quadrigeminal perimesencephalic subarachnoid hemorrhage Perimesencephalic subarachnoid hemorrhage Nonaneurysmal subarachnoid hemorrhage Aneurysm Digital subtraction angiography Computed tomography angiography
a b s t r a c t Objective: A variant of perimesencephalic subarachnoid hemorrhage (PSAH) has been described characterized by blood centered in the quadrigeminal cistern and limited to the superior vermian and perimesencephalic cisterns. Herein, three cases of quadrigeminal PSAH are presented. Materials and methods: Medical records of all patients who underwent digital subtraction angiography for evaluation of non-traumatic SAH between July 2002 and April 2012 were reviewed. Patients with anterior circulation aneurysms were excluded. Two blinded reviewers identified admission noncontrast CT scans with pretruncal and quadrigeminal patterns of PSAH. Results: The total cohort included 106 patients: 53% (56/106) with one or more negative digital subtraction angiograms and 47% (50/106) with posterior circulation or posterior communicating artery aneurysms. Three patients with quadrigeminal PSAH were identified, two with nonaneurysmal SAH and one with a posterior circulation aneurysm. Seventeen patients (16%; 17/106) with pretruncal PSAH were identified, none of whom were found to have an aneurysm. The quadrigeminal pattern comprised 11% (2/19) of cases of pretruncal or quadrigeminal nonaneurysmal PSAH. Conclusion: A small subset of patients with nonaneurysmal PSAH present with blood centered in the quadrigeminal cistern, and the etiology of this pattern may be similar to that of the classic pretruncal variant. However, patients with quadrigeminal PSAH must still undergo thorough vascular imaging, including at least two digital subtraction angiograms, to exclude a ruptured aneurysm. © 2015 Elsevier B.V. All rights reserved.
1. Introduction Perimesencephalic subarachnoid hemorrhage (PSAH) is classically described as blood mostly confined to the perimesencephalic cisterns and centered immediately anterior to the brainstem on initial noncontrast CT [1–2]. The low prevalence of aneurysms and benign clinical courses of patients with this pattern of SAH have clinical implications in terms of follow-up imaging and patient reassurance [3–7]. Several case reports describe another form of nonaneurysmal SAH characterized by blood centered in the quadrigeminal cistern and limited to the superior cerebellar and perimesencephalic cisterns [1,8–12]. These patients have had benign clinical courses with no incidences of vasospasm, hydrocephalus, or other common complications after aneurysmal SAH.
∗ Corresponding author. Tel.: +1 608 347 0294; fax: +1 314 454 9417. E-mail address: [email protected] (A.N. Wallace). http://dx.doi.org/10.1016/j.clineuro.2015.06.018 0303-8467/© 2015 Elsevier B.V. All rights reserved.
As a result, it has been proposed that nonaneurysmal PSAH be used as an umbrella term that includes both the classic definition of PSAH with blood centered anterior to the brainstem, as well as the quadrigeminal variant [11]. However, little is known about quadrigeminal PSAH, including whether it represents a distinct etiologic entity or a variant of pretruncal PSAH that should be managed similarly. Herein, three cases of quadrigeminal perimesencephalic SAH are presented.
2. Methods Institutional review board approval was obtained to retrospectively review the medical records of all patients who underwent digital subtraction angiography (DSA) at Barnes Jewish Hospital between July 2002 and April 2012. Inclusion criteria required a noncontrast head CT demonstrating SAH. Patients with a history of head trauma were excluded. Patients presenting more than 72 h
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Fig. 1. Noncontrast CT images demonstrate subarachnoid hemorrhage centered in the quadrigeminal cistern (A; black arrow) and extending around the brainstem into the prepontine cistern (B; white arrow). No aneurysm or other cause of subarachnoid hemorrhage was found on two digital subtraction angiograms or one CT angiogram.
after onset of symptoms were also excluded. This cohort was previously used to test the inter-observer variability and specificity for nonaneurysmal SAH of an anatomic definition of PSAH [13]. The standard practice at our institution is to pursue DSA on all patients with nontraumatic SAH in whom an aneurysm is suspected. The only patients that do not undergo DSA are (1) those with severe neurologic injury with little likelihood of meaningful recovery (at least Hunt-Hess grade 5); (2) those with acute mass effect, in which case CT angiography (CTA) may be performed on the way to the operating room; and (3) some patients with convexity SAH [13]. Patients with anterior circulation aneurysms found on DSA were excluded from this review. Digital subtraction angiography was performed on one of two Axiom Artis Biplane neuroangiographic suites (Siemens Healthcare, Forchheim, Germany) by one of three interventional neuroradiologists. A typical procedure involves conscious sedation, a 5-french femoral arterial sheath and 5-french diagnostic catheter. Three- or four-vessel DSA was obtained in all patients with care taken to image both intracranial vertebral arteries, either by reflux down the contralateral vessel or direct selection of both vertebral arteries in the neck. A rotational angiogram with three-dimensional reconstruction was obtained if a lesion was suspected. Angiography was repeated 7 days after initial presentation to reassess for a missed aneurysm and/or as a surveillance procedure for SAH-induced vasospasm [6,14]. Some patients with negative DSA underwent CTA as well. Dictated reports from these examinations were reviewed for the present study. Two board certified, fellowship trained neuroradiologists blinded to the angiographic findings independently reviewed every case and identified initial noncontrast CT scans with blood centered in the quadrigeminal cistern with extension limited to the ambient, crural, and/or superior cerebellar cisterns. The reviewers categorized the remaining initial CT scans as pretruncal PSAH or nonperimesencephalic SAH (NPSAH) according to previously described anatomic criteria [13]. Assessment differences were resolved by consensus. The electronic medical records of patients with a quadrigeminal pattern of PSAH were reviewed for additional epidemiologic and clinical information and the results of additional neuroimaging.
3. Results The total cohort included 106 patients: 53% (56/106) with one or more negative digital subtraction angiograms and 47% (50/106) with posterior circulation or posterior communicating artery aneurysms. The same three cases of quadrigeminal PSAH were identified by both reviewing neuroradiologists. Two of these patients did not have an identifiable source of SAH and one was found to have a posterior circulation aneurysm on subsequent vascular imaging. The reviewers categorized the initial CT scans of 17 patients (16%; 17/106) as pretruncal PSAH. None of these patients were found to have an aneurysm. Thus, the quadrigeminal pattern comprised 11% (2/19) of cases of pretruncal or quadrigeminal nonaneurysmal PSAH. Each of the three patients with a quadrigeminal perimesencephalic pattern of SAH is described in more detail. 3.1. Case 1 The first patient was a 58-year old African-American man who presented after the sudden onset of diffuse headache with associated nausea, photophobia, and meningismus. Noncontrast CT performed the same day as symptom onset demonstrated SAH centered in the quadrigeminal cistern and extending laterally around the brainstem (Fig. 1A and B). Digital subtraction angiography performed the following morning showed no aneurysm or other source of SAH. Computed tomographic angiography performed the following day was also negative. Repeat DSA performed on day 8 of hospitalization was again negative for a source of SAH. During his 9-day hospitalization he suffered no SAH-induced complications, such as clinically significant vasospasm or hydrocephalus, and demonstrated complete recovery at 1-month follow-up. After 3 years of clinical follow-up, he has not experienced another episode of SAH. 3.2. Case 2 The second patient was a 52-year old Caucasian woman with a history of hypertension who presented after the sudden onset of right temporal headache radiating down her right neck with
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cerebral artery (MCA) atherosclerotic narrowing with extensive pial collaterals from the right posterior cerebral artery (PCA) to the distal right MCA vascular territory. Computed tomographic angiography performed the following day also did not show an aneurysm. Repeat DSA performed on day 8 of hospitalization did not demonstrate any new findings. She was discharged after an uneventful 9-day hospitalization, and demonstrated complete recovery at 1month follow-up. 3.3. Case 3
Fig. 2. Noncontrast CT images demonstrate subarachnoid hemorrhage centered in the quadrigeminal cistern and extending laterally around the brainstem (white arrow). Digital subtraction angiography revealed severe atherosclerotic narrowing of the M2 segment of the right middle cerebral artery, but no source of subarachnoid hemorrhage. Repeat digital subtraction and CT angiography were also negative for a source of subarachnoid hemorrhage.
associated nausea and vomiting. Noncontrast CT performed the same day as symptom onset demonstrated SAH centered in the quadrigeminal cistern and extending laterally around the brainstem (Fig. 2). Digital subtraction angiography performed the same day did not reveal an aneurysm, but did show severe right middle
The third patient was a 40-year old African-American woman who presented after 4 days of mild occipital headache that acutely worsened the day of admission after using cocaine. Noncontrast CT demonstrated SAH centered in the quadrigeminal cistern and extending into the ambient cisterns bilaterally (Fig. 3A). Digital subtraction angiography performed the same day demonstrated irregularity of the distal branches of the intracranial arteries, most prominent in the left PCA distribution, consistent with drug-induced vasculopathy or vasospasm. Computed tomographic angiography performed the following day did also not reveal a cause for SAH. On day 3 of hospitalization, she developed hydrocephalus requiring placement of an external ventricular drain (EVD). Repeat DSA performed on day 6 of hospitalization demonstrated a 2.5-mm dissecting aneurysm at the junction of the P2 and P3 segments of the left PCA, which was successfully embolized with preservation of flow to the distal PCA (Fig. 3B). The EVD was weaned and eventually removed. The remainder of her recovery was uneventful and she was discharged on day 13 of hospitalization. Over 3 years of subsequent clinical follow-up she continued to have chronic headaches that were successfully managed with medication. 4. Discussion Early case series of patients with nonaneurysmal PSAH included two patients with blood centered in the quadrigeminal cistern
Fig. 3. Noncontrast CT image demonstrates subarachnoid hemorrhage centered in the quadrigeminal cistern (A; black arrows). Rotational digital subtraction angiography with three-dimensional reconstruction during right vertebral artery injection demonstrates a 2.5-mm dissecting aneurysm at the left P2–P3 junction (B; white arrow).
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and well-documented benign clinical outcomes [1,10]. In 2000, Schwartz et al. reported a prevalence of quadrigeminal nonaneurysmal PSAH of 0.9% (2/220) among patients with SAH and 22% (2/9) among patients with nonaneurysmal PSAH [12]. The first of these patients underwent four-vessel DSA and MR angiography (MRA) and did not rebleed during 24 months of follow-up. The second patient underwent two four-vessel digital subtraction angiograms and MRA, and did not rebleed during 18 months of follow-up. Schwartz et al. later reported a third patient with quadrigeminal nonaneurysmal PSAH who underwent two fourvessel digital subtraction angiograms and CTA, and did not rebleed during 12 months of follow-up [11]. However, Wijdicks et al. have argued against the existence of a quadrigeminal variant of nonaneurysmal PSAH, insisting that the etiology is either traumatic or a posterior circulation aneurysm [16]. The present study supports the existence of a quadrigeminal variant of nonaneurysmal PSAH, though the etiology remains uncertain. Our first two patients with quadrigeminal PSAH underwent two digital subtraction angiograms and CTA, none of which identified a source of hemorrhage. These patients presented in good clinical condition and had benign clinical courses similar to other reported cases of quadrigeminal and pretruncal nonaneurysmal PSAH. These clinical similarities suggest that both patterns of hemorrhage are due to a non-arterial source [2]. An association between pretruncal nonaneurysmal PSAH and abnormal venous anatomy has led to the hypothesis that the etiology is a venous rupture secondary to central cerebral venous hypertension [15–18]. For example, patients with pretruncal nonaneurysmal PSAH are more likely to have variant Basal vein of Rosenthal drainage into a dural venous sinus via a perimesencephalic bridging vein [21]. Perhaps the pretruncal pattern of PSAH is more common than the quadrigeminal pattern because the bridging vein that ruptures is more commonly located anterior to the brainstem. Alternatively, both patterns may be due to a variety of nonaneurysmal etiologies. In addition to a venous bleed, other proposed etiologies of nonaneurysmal SAH include a ruptured perforating artery, intraluminal dissection, capillary telangiectasia, and cavernous malformation [19]. If nonaneurysmal PSAH is used as an umbrella term to include both the classic pretruncal and quadrigeminal variants, then the quadrigeminal variant accounted for 11% (2/19) of cases of nonaneurysmal PSAH in this series. This is smaller than the 22% (2/9) prevalence reported by Schwartz et al., though neither number is expected to be accurate given the small sample sizes. Additionally, Schwartz et al. used the definition of PSAH described by Rinkel et al. [23], while this series used more objective, anatomic criteria [13]. Still, one can reasonably conclude from these series that patients with a quadrigeminal pattern likely comprise a small but substantial percentage of the umbrella population with nonaneurysmal PSAH, and this subgroup deserves greater attention in future studies. However, even if quadrigeminal and pretruncal nonaneurysmal PSAH share a common etiology, this does not imply that quadrigeminal and pretruncal PSAH should be evaluated the same way. In a recently published meta-analysis of 40 studies with 1,031 patients with pretruncal PSAH and initial negative DSA or CTA, the rate of aneurysm detection on follow-up DSA and/or CTA was 0.78% (8/1031; 95% confidence interval, 0.23–1.32%). Additionally, comparison of different imaging strategies found no statistically significant benefit of performing DSA during initial or follow-up evaluation of these patients. The authors concluded that patients with pretruncal PSAH and presentations compatible with a nonaneurysmal etiology can undergo initial evaluation with CTA alone and do not require follow-up imaging [20]. This meta-analysis is limited by inconsistent definitions of PSAH used in the constituent studies, and clinical implementation of such recommendations is
limited by inter-observer variability in terms of characterizing SAH patterns [21,22]. Regardless, extending such recommendations to patients with quadrigeminal PSAH is premature. In the present series, one of the three patients identified with a quadrigeminal pattern of PSAH on initial noncontrast CT was found to have a 2.5-mm dissecting posterior cerebral artery aneurysm. Moreover, this aneurysm was detected on a second digital subtraction angiogram after initial DSA and CTA were both negative. In a previous case series, 2.7% (3/113) of patients with posterior circulation aneurysms initially presented with a quadrigeminal pattern of PSAH [23,24]. We recommend that quadrigeminal PSAH be evaluated like NPSAH with DSA within 24 h of presentation. If initial DSA is negative, CTA is a potentially useful adjunct study. In a 2012 study that included 43 patients with NPSAH and negative initial DSA, CTA identified a causative cerebral aneurysm in 9.3% (4/43) of cases [6]. If initial CTA and DSA are both negative, repeat DSA is recommended. In a pooled analysis of 8 studies with 368 patients with NPSAH and negative initial evaluation with DSA and CTA, the yield of repeat DSA was 10.0% (37/368; 95% confidence interval, 7.4%–13.6%). Thus, in these patients, the potential morbidity and mortality associated with rerupture of an aneurysm that is not detected on initial imaging far outweighs the risk of repeat DSA [25]. The timing of repeat DSA in the studies comprising this pooled analysis ranged from 1 to 6 weeks. Our practice is to repeat DSA 5–10 days after the initial study, at which time it also reasonable to screen for SAH-induced vasospasm [26]. During this interval, patients should be monitored in a neurosurgical intensive care unit for signs of rerupture of an aneurysm missed on initial imaging and complications of SAH [27,28]. This study is limited by the fact that it is retrospective and the number of cases of quadrigeminal PSAH was small. Additionally, the true prevalence of quadrigeminal PSAH cannot be determined from our cohort, because patients with anterior circulation aneurysms were excluded. Similarly, clinical considerations introduced selection bias into the data. At our institution, DSA is the modality of choice for the diagnosis of cerebral aneurysms, but patients with severe neurological injury and a poor prognosis and those with large parenchymal hematomas and acute neurological decline do not always undergo DSA. However, neither of these groups of patients is likely to have quadrigeminal PSAH. 5. Conclusion A small subset of patients with nonaneurysmal PSAH present with blood centered in the quadrigeminal cistern, and the etiology of this pattern may be similar to that of the classic pretruncal variant. However, patients with quadrigeminal PSAH must still undergo thorough vascular imaging, including at least two DSAs, to exclude a ruptured aneurysm. This work was performed at the Mallinckrodt Institute of Radiology, St Louis, MO. No financial support was provided for the publication of this manuscript. References [1] J. van Gijn, K.J. van Dongen, M. Vermeulen, A. Hijdra, Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage, Neurology 35 (1985) 493–497. [2] Y.W. Kim, M.F. Lawson, B.L. Hoh, Nonaneurysmal subarachnoid hemorrhage: an update, Curr. Atheroscler. Rep. 14 (2012) 328–334. [3] B.K. Velthuis, G.J. Rinkel, L.M. Ramos, T.D. Witkamp, M.S. van Leeuwen, Perimesencephalic hemorrhage. Exclusion of vertebrobasilar aneurysms with CT angiography, Stroke 30 (1999) 1103–1109. [4] R. Agid, T. Andersson, H. Almqvist, R.A. Willinsky, S.K. Lee, K.G. terBrugge, R.I. Farb, M. Soderman, C.T. Negative, angiography findings in patients with spontaneous subarachnoid hemorrhage: when is digital subtraction angiography still needed? AJNR 31 (2010) 696–705.
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