Yield of spinal imaging in nonaneurysmal, nonperimesencephalic subarachnoid hemorrhage Menno R. Germans, MD Bert A. Coert, MD, PhD Charles B.L.M. Majoie, MD, PhD René van den Berg, MD, PhD Geert Lycklama à Nijeholt, MD, PhD Gabriël J.E. Rinkel, MD, PhD Dagmar Verbaan, PhD W. Peter Vandertop, MD, PhD

ABSTRACT

Objective: We studied the yield of MRI of the spinal neuraxis in patients with nonperimesencephalic subarachnoid hemorrhage (NPSAH).

Methods: In a prospective, multicenter study, we performed T1-weighted and T2-weighted MRI of the spinal axis in a consecutive series of patients with a spontaneous NPSAH without intracranial vascular pathology on intracranial vascular imaging. Results: A spinal origin of the hemorrhage was found in 3 of 75 patients (4%; 95% confidence interval 0–8.4). The lesions were 1 lumbar ependymoma and 2 cervical cavernous malformations. All 3 patients presented without focal neurologic deficits and 2 had a CT-negative subarachnoid hemorrhage but positive lumbar puncture. Patients with a spinal origin were younger than patients without a spinal origin (38 vs 56 years; p , 0.05), which was the only significant difference between groups. Conclusions: The yield and clinical relevance of MRI of the spinal axis in patients who present with

Correspondence to Dr. Germans: [email protected]

NPSAH is low. We do not recommend routine MRI of the spinal axis in this patient population, but it might be justified in a subgroup of patients. Neurology® 2015;84:1337–1340 GLOSSARY CI 5 confidence interval; DSA 5 digital subtraction angiography; LP 5 lumbar puncture; NPSAH 5 nonperimesencephalic subarachnoid hemorrhage; SAH 5 subarachnoid hemorrhage.

In 15% of patients with spontaneous subarachnoid hemorrhage (SAH), no aneurysm or other vascular lesion is demonstrated at initial radiologic investigations.1 This group consists of patients with a perimesencephalic SAH and nonperimesencephalic SAH (NPSAH).2 Spinal lesions may give rise to an NPSAH and can lead to recurrence and other complications.2–4 In a retrospective study, we found 9% of patients having a spinal origin for NPSAH.5 This study prospectively assesses the yield of spinal MRI in patients with NPSAH. METHODS Patient population. Patients with a clinical history and diagnosis of SAH without intracranial vascular pathology, admitted to 3 centers from April 2009 to October 2012, were prospectively included. Patients with a hemorrhage pattern consistent with a perimesencephalic hemorrhage2 were excluded. Sample size calculation was based on the results of a retrospective study in one of the participating centers, where a spinal vascular malformation was found in 9% of patients with NPSAH.5

Standard protocol approvals, registrations, and patient consents. The Medical Ethics Committee of the Academic Medical Center Amsterdam approved the study protocol.

Data collection. Patient demographics, clinical characteristics, and radiologic investigations were recorded in a Web-based database. Radiologic evaluation. All patients underwent plain CT and CT angiography, performed on 64-slice scanners. Digital subtraction angiography (DSA) images were acquired by 4-vessel 2D DSA and 3D DSA when indicated by the treatment team. When intracranial vascular pathology was ruled out, patients underwent MRI of the complete spinal axis. The minimal requirements for the MRI were T1- and T2-weighted sequences in the sagittal plane. Statistical analysis. Wilcoxon rank-sum test was used for a 2-group comparison for not normally distributed variables. Categorical variables were compared using Fisher exact test. The yield of the MRI was calculated in patients who received the investigation and given as proportion with corresponding 95% confidence interval (CI). A p value ,0.05 was considered statistically significant. From the Department of Neurosurgery, Neurosurgical Center Amsterdam (M.R.G., B.A.C., D.V., W.P.V.), and the Department of Neuroradiology (C.B.L.M.M., R.v.d.B.), Academic Medical Center, Amsterdam; the Department of Radiology (G.L.N.), Medical Center Haaglanden, the Hague; and the Department of Neurology & Neurosurgery (G.J.E.R.), Brain Center Rudolf Magnus, University Medical Center, Utrecht, the Netherlands. Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article. © 2015 American Academy of Neurology

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RESULTS Patient characteristics. Ninety patients with NPSAH, from a total cohort of 1,650 patients with SAH, were included in this study (see the table for baseline characteristics). The initial CT scan was negative for SAH in 39 patients (43%), of whom 27 (69%) were investigated later than 24 hours after onset of symptoms.

Radiologic evaluation. At least one DSA was performed in 78 patients (87%). Hemorrhage patterns not suggestive for aneurysmal rupture were small intraventricular hemorrhages (n 5 2) and isolated cortical hemorrhages (n 5 2); in 1 patient, movement artifacts hampered a good evaluation of the CT. Fifteen patients (17%) did not receive MRI because of claustrophobia (n 5 1), patient refusal (n 5 1), patient’s

Table

Characteristics of 90 consecutive patients with nonperimesencephalic subarachnoid hemorrhage without intracranial vascular pathology

Patient characteristics

NPSAH (n 5 90)

No spinal imaging (n 5 15)

Nonspinal origin (n 5 72)

Spinal origin (n 5 3) a

Age, y

55 6 14

55 6 18

56 6 12

38 6 13

Female

41 (46)

6 (40)

35 (49)

0

LP

39 (43)

4 (27)

33 (46)

2 (67)

CT

51 (57)

11 (73)

39 (54)

1 (33)

48

25 (28)

2 (13)

22 (31)

1 (33)

1–3

87 (97)

14 (93)

70 (97)

3 (100)

4–5

3 (3)

1 (7)

2 (3)

0

8 (9)

2 (13)

6 (8)

0

Yes

3 (3)

2 (13)

1 (1)

0

No

82 (91)

13 (87)

66 (92)

3 (100)

Unknown

5 (6)

0

5 (7)

0

49 (54)

9 (60)

39 (54)

1 (33)

Diagnosis of SAH

Time interval between onset of symptoms and initial CT, h

WFNS at first presentation

Focal neurologic deficits Loss of consciousness

Pain in neck Yes No

22 (25)

2 (13)

19 (26)

1 (33)

Unknown

19 (21)

4 (27)

14 (19)

1 (33)

Yes

2 (2)

0

2 (3)

0

No

46 (51)

7 (47)

37 (51)

2 (67)

Unknown

42 (47)

8 (53)

33 (46)

1 (33)

Thoracolumbar pain

Abbreviations: LP 5 lumbar puncture; NPSAH 5 nonperimesencephalic subarachnoid hemorrhage; SAH 5 subarachnoid hemorrhage; WFNS 5 World Federation of Neurological Surgeons. Data are shown as n (%) or median 6 SD. a Wilcoxon rank-sum test spinal origin vs nonspinal origin: p , 0.05. 1338

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transfer to another hospital (n 5 1), or unknown reasons (n 5 12). Thus, the yield of MRI of the spinal axis was based on 75 patients. In 3 patients, MRI revealed a spinal origin of the hemorrhage (yield 4%; 95% CI 0–8.4): a lumbar ependymoma in 1 patient and a cervical cavernous malformation in 2 patients. An overview of the pattern of SAH on the primary CT in the 75 patients and findings at MRI of the spinal axis are presented in the figure. Clinical characteristics of patients with a spinal origin.

Patients with a spinal origin of their hemorrhage were significantly younger than patients without a spinal origin. Otherwise, no statistically significant differences were seen between those groups. One patient with a cervical cavernous malformation had an aneurysmal SAH pattern on CT, whereas the other 2 patients had no blood on the initial CT, of which one had onset of symptoms more than 48 hours before presentation. DISCUSSION In this prospective, multicenter study, we found a spinal origin for the hemorrhage in 4% of patients with NPSAH. The patients with a spinal origin were male and significantly younger than patients without a spinal origin. Our results are in line with a review that revealed that spinal arteriovenous shunts causing SAH are rare and occur more commonly in males and in younger patients.4 The types of spinal origins for the SAH in our study are rare, but similar to those reported elsewhere.4,6–8 In 2 patients, the CT scan was negative and the SAH was diagnosed by lumbar puncture (LP), which is in line with the rate of 50% of patients in our previously published study.5 The lack of SAH found on brain CT scan is probably explained by the etiology of the hemorrhages, as cavernous malformations and lumbar ependymomas tend to leak with low pressure, opposed to arterial bleeding, which could have hindered the hemorrhage to disperse against gravity to the intracranial compartment but did cause a SAH and its related symptoms. The goal of spinal axis investigation in patients with SAH is to search for the source of the hemorrhage to assess the risk of recurrence and other complications. However, the clinical course of a cavernous malformation, like in 2 of our patients, is usually favorable,9 leaving the clinical relevance of the search for this pathology debatable. Our retrospective assessment of spinal vascular malformations in patients with NPSAH in a single center showed an incidence of almost 9%, which would support routine imaging.5 Our current prospective multicenter study, however, does not confirm this high rate of a spinal origin as a cause for the SAH, although it is still higher than previously reported in the literature.4,7 This higher percentage

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Figure

Flow diagram of radiologic investigations in 75 nonperimesencephalic subarachnoid hemorrhage patients without intracranial vascular pathology

LP 5 lumbar puncture.

could be attributable to (1) the relatively high number of patients with a negative CT scan, (2) standard evaluation in the majority of patients, even in absence of clinical cues for spinal pathology, and (3) investigation of the complete spinal axis. One study with a proportion of patients with CT-negative SAH comparable to our study found a 2% incidence of a spinal origin in NPSAH. This number might have been underestimated because the complete spinal axis was not investigated in all patients,7 especially because SAH can also result from spinal pathology originating lower than the cervicothoracic spine.4,5 We would not recommend routine MRI of the spinal axis in all patients with NPSAH, because both the yield of the investigation and clinical relevance of the findings are low. Nevertheless, in a subgroup of patients it might be justified, e.g., in patients younger than 50 years who were diagnosed by LP, as MRI of the spinal axis in these patients revealed a cause in 10% of cases. But, due to the low reliability of post hoc analysis, we cannot draw a reliable conclusion in which group routine MRI would be justified. In contrary to the 9% we used for our sample calculation, it appeared that the yield of spinal MRI in patients with NPSAH much lower. Future studies, therefore, need to include a large number of patients with SAH to draw reliable conclusions. A first limitation is the small number of patients with a spinal origin, which hampered a good comparison of their characteristics with the other patients. Second, only 87% of all patients received a DSA, so we cannot be sure that all patients had no intracranial vascular pathology. Third, 17% of patients did not receive spinal MRI.

The yield of MRI of the complete spinal axis in patients with NPSAH is 4%. We do not recommend routine MRI of the complete spinal axis in all patients with NPSAH, but it might be justified in young patients with CT-negative SAH. Future studies investigating NPSAH subgroups need to include a large number of patients to draw a reliable conclusion. AUTHOR CONTRIBUTIONS M.R. Germans: study concept and design, analysis and interpretation of data, drafting the manuscript, principal author, corresponding author. B.A. Coert: study concept and design, study supervision, revision of manuscript, and intellectual contribution. C.B.L.M. Majoie: revision of manuscript and intellectual contribution, acquisition of data. R. van den Berg: revision of manuscript and intellectual contribution, acquisition of data. G. Lycklama à Nijeholt: revision of manuscript and intellectual contribution, acquisition of data. G.J.E. Rinkel: study concept and design, revision of manuscript, and intellectual contribution. D. Verbaan: analysis and interpretation of data, revision of manuscript, and intellectual contribution. W.P. Vandertop: principal investigator, study supervision, revision of manuscript, and intellectual contribution.

ACKNOWLEDGMENT The authors thank Paut Greebe for collecting the patients who were eligible for the study at the University Medical Center Utrecht.

STUDY FUNDING This study received institutional funding of the “Stichting ter Bevordering van Neurochirurgische Ontwikkeling.”

DISCLOSURE The authors report no disclosures relevant to the manuscript. Go to Neurology.org for full disclosures.

Received September 7, 2014. Accepted in final form December 15, 2014. REFERENCES 1. van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain 2001;124:249–278. 2. Rinkel GJ, Wijdicks EF, Vermeulen M, et al. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT Neurology 84

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and MR patterns that differ from aneurysmal rupture. AJNR Am J Neuroradiol 1991;12:829–834. Jellema K, Canta LR, Tijssen CC, van Rooij WJ, Koudstaal PJ, van Gijn J. Spinal dural arteriovenous fistulas: clinical features in 80 patients. J Neurol Neurosurg Psychiatry 2003;74:1438–1440. van Beijnum J, Straver DC, Rinkel GJ, Klijn CJ. Spinal arteriovenous shunts presenting as intracranial subarachnoid haemorrhage. J Neurol 2007;254:1044–1051. Germans MR, Pennings FA, Sprengers ME, Vandertop WP. Spinal vascular malformations in nonperimesencephalic subarachnoid hemorrhage. J Neurol 2008;255:1910–1915.

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Acciarri N, Padovani R, Pozzati E, Gaist G, Manetto V. Spinal cavernous angioma: a rare cause of subarachnoid hemorrhage. Surg Neurol 1992;37:453–456. Little AS, Garrett M, Germain R, et al. Evaluation of patients with spontaneous subarachnoid hemorrhage and negative angiography. Neurosurgery 2007;61: 1139–1150. Nicastro N, Schnider A, Leemann B. Anaplastic medullary ependymoma presenting as subarachnoid hemorrhage. Case Rep Neurol Med 2013;2013:701820. Kim KM, Chung CK, Huh W, et al. Clinical outcomes of conservative management of spinal cord cavernous angiomas. Acta Neurochir 2013;155:1209–1214.

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Yield of spinal imaging in nonaneurysmal, nonperimesencephalic subarachnoid hemorrhage Menno R. Germans, Bert A. Coert, Charles B.L.M. Majoie, et al. Neurology 2015;84;1337-1340 Published Online before print February 27, 2015 DOI 10.1212/WNL.0000000000001423 This information is current as of February 27, 2015 Updated Information & Services

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Yield of spinal imaging in nonaneurysmal, nonperimesencephalic subarachnoid hemorrhage.

We studied the yield of MRI of the spinal neuraxis in patients with nonperimesencephalic subarachnoid hemorrhage (NPSAH)...
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