Non-aneurysmal subarachnoid hemorrhage: When is a second angiography indicated?

Abstract

Purpose

Repeat imaging in patients with non-aneurysmal subarachnoid hemorrhage (NASAH) remains controversial. We aim to report our experience with NASAH with different hemorrhage patterns, and to investigate the need for further diagnostic workup to determine the underlying cause of hemorrhage.

Method

We conducted a retrospective analysis of all spontaneous SAH with an initial negative computed tomography (CT) with angiography (CTA) and/or digital subtraction angiography (DSA) from October 2011 through May 2017. According to the bleeding pattern on the admission CT scan, NASAH was divided into two subgroups: (1) perimesencephalic SAH (PMSAH) and (2) non-perimesencephalic SAH (nPMSAH). Radiological data included the admission CT, CTA, DSA, and magnetic resonance imaging (MRI) with angiography (MRA).

Results

Seventy-four patients met the inclusion criteria. Thirty-nine (52.7%) patients had PMSAH on the initial CT scan, and 35 (47.3%) had nPMSAH. All underwent CTA and/or DSA revealing no vascular abnormalities. Forty-seven (63.5%) patients underwent subsequent diagnostic workup. DSA was performed in all patients at least once. No abnormalities were found on the repeat DSA or other radiological follow-up studies except in one (1.4%) patient with nPMSAH, in whom a follow-up DSA revealed a small saccular anterior choroidal artery aneurysm, considered to be the source of hemorrhage.

Conclusion

A repeat DSA may not be needed in case of PMSAH, if the initial negative DSA is technically adequate with absence of hematoma and vasospasm. In contrast, a follow-up DSA should be mandatory for confirming or excluding vascular pathology in case of nPMSAH in order to prevent rebleeding.

Keywords

Non-aneurysmal subarachnoid hemorrhage perimesencephalic subarachnoid hemorrhage cerebral angiography digital subtraction angiography

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References

Rinkel

Wijdicks

Vermeulen

et al.

Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from aneurysmal rupture. Am J Neuroradiol 1991; 12: 829–834.

Rinkel

Wijdicks

Vermeulen

et al.

The clinical course of perimesencephalic nonaneurysmal subarachnoid hemorrhage. Ann Neurol 1991; 29: 463–468.

Rinkel

van Gijn

Wijdicks

. Subarachnoid hemorrhage without detectable aneurysm. A review of the causes. Stroke 1993; 24: 1403–1409.

van der Schaaf

Velthuis

Gouw

et al.

Venous drainage in perimesencephalic hemorrhage. Stroke 2004; 35: 1614–1618.

Rinkel

Wijdicks

Hasan

et al.

Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet 1991; 338: 964–968.

Beseoglu

Pannes

Steiger

et al.

Long-term outcome and quality of life after nonaneurysmal subarachnoid hemorrhage. Acta Neurochir 2010; 152: 409–416.

Hui

Tumialán

Tanaka

et al.

Clinical differences between angiographically negative diffuse subarachnoid haemorrhage and perimesencephalic subarachnoid haemorrhage. Neurocrit Care 2009; 11: 64–70.

Canneti

Mosqueira

Nombela

et al.

Spontaneous subarachnoid hemorrhage with negative angiography managed in a stroke unit: Clinical and prognostic characteristics. J Stroke Cerebrovasc Dis 2015; 24: 2484–2490.

Hermann

Zabramski

. Nonaneurysmal subarachnoid hemorrhage: A review of clinical course and outcome in two hemorrhage patterns. J Neurosci Nurs 2007; 39: 135–142.

10.

Greebe

Rinkel

. Life expectancy after perimesencephalic subarachnoid hemorrhage. Stroke 2007; 38: 1222–1224.

11.

Kalra

Matouk

et al.

Use of follow-up imaging in isolated perimesencephalic subarachnoid hemorrhage: A meta-analysis. Stroke 2015; 46: 401–406.

12.

Dalyai

Chalouhi

Theofanis

et al.

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. Neurosurgery 2013; 72: 646–652.

13.

Huttner

Hartmann

Köhrmann

et al.

Repeated digital subtraction angiography after perimesencephalic subarachnoid hemorrhage?

J Neuroradiol 2006; 33: 87–89.

14.

Khan

Shand Smith

Kirkman

et al.

Angiogram negative subtraction haemorrhage: Outcomes and the role of repeat angiography. Clin Neurol Neurosurg 2013; 115: 1470–1475.

15.

Westerlaan

van Dijk

Jansen-van der Weide

et al.

Intracranial aneurysms in patients with subarachnoid hemorrhage: CT angiography as a primary examination tool for diagnosis—systematic review and meta-analysis. Radiology 2011; 258: 134–145.

16.

Chappell

Moure

Good

. Comparison of computed tomographic angiography with digital subtraction angiography in the diagnosis of cerebral aneurysm: A meta-analysis. Neurosurg 2003; 52: 624–631.

17.

Menke

Larsen

Kallenberg

. Diagnosing cerebral aneurysms by computed tomographic angiography: Meta-analysis. Ann Neurol 2011; 69: 646–654.

18.

Steiner

Juvela

Unterberg

et al.

European stroke organisation guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerbrovasc Dic 2013; 35: 93–112.

19.

Agid

Andersson

Almqvist

et al.

Negative CT angiography findings in patients with spontaneous subarachnoid hemorrhage: When is digital subtraction angiography still needed?

Am J Neuroradiol 2013; 31: 696–705.

20.

Akcakaya

Aydoseli

Aras

et al.

Clinical course of nontraumatic nonaneurysmal subarachnoid hemorrhage: A single institution experience over 10 years and review of the contemporary literature. Turk Neurosurg 2017; 27: 732–742.

21.

Jung

Choi

et al.

Subarachnoid hemorrhage with negative baseline digital subtraction angiography: Is repeat digital subtraction angiography necessary?

J Cerebrovasc Endovasc Neurosurg 2012; 14: 210–215.

22.

Westerlaan

Gravendaal

Fiore

et al.

Multislice CT angiography in the selection of patients with ruptured intracranial aneurysms suitable for clipping or coiling. Neuroradiology 2007; 49: 997–1007.

23.

Topcuoglu

Ogilvy

Carter

et al.

Subarachnoid hemorrhage without evident cause on initial angiography studies: Diagnostic yield of subsequent angiography and other neuroimaging tests. J Neurosurg 2003; 98: 1235–1240.

24.

Ruigrok

Rinkel

Buskens

et al.

Perimesencephalic hemorrhage and CT angiography: A decision analysis. Stroke 2000; 31: 2976–2983.

25.

Kershenovich

Rappaport

Maimon

. Brain computed tomography angiographic scans as the sole diagnostic examination for excluding aneurysm in patients with perimesencephalic subarachnoid hemorrhage. Neurosurgery 2006; 59: 798–802.

26.

McKinney

Palmer

Truwit

et al.

Detection of aneurysm by 64-section multidetector CT angiography in patients acutely suspected of having an intracranial aneurysm and comparison with digital subtraction and 3D rotational angiography. Am J Neuroradiol 2008; 29: 594–602.

27.

Galal

ElSerry

Aziz

. Is catheter diagnostic cerebral angiography still essential for patients with spontaneous perimesencephalic subarachnoid hemorrhage and negative computed tomography angiogram? Neurosurgery 2016; 63: 188.

28.

Ausman

. Perimesencephalic nonaneurysmal subarachnoid hemorrhage: What is it? What are we missing? Surg Neurol 2002; 57: 211.

29.

Andaluz

Zuccarello

. Yield of further diagnostic work-up of cryptogenic subarachnoid hemorrhage based on bleeding patterns on computed tomographic scans. Neurosurgery 2008; 62: 1040–1046.

30.

Kaufmann

Huston

3rd Mandrekar

et al.

Complications of diagnostic cerebral angiography: Evaluation of 19826 consecutive patients. Radiology 2007; 243: 812–819.

31.

Coelho

Costa

Silva

. Non-aneurysmal spontaneous subarachnoid hemorrhage: Perimesencephalic versus non-perimesencephalic. Rev Bras Ter Intensiva 2016; 28: 141–146.

32.

van der Worp

Fonville

Ramos

et al.

Recurrent perimesencephalic subarachnoid hemorrhage during anti-thrombotic therapy. Neurocrit Care 2009; 10: 209–212.

33.

Konczalla

Schuss

Platz

et al.

Clinical outcome and prognostic factors of patients with angiogram-negative and non-perimesencephalic subarachnoid hemorrhage: Benign prognosis like perimesencephalic SAH or same risk as aneurysmal SAH?

Neurosurg Rev 2015; 38: 121–127.