J Neurol Surg A Cent Eur Neurosurg 2023; 84(02): 167-173
DOI: 10.1055/s-0042-1748771
Original Article

Subarachnoid Hemorrhage with Negative Initial Digital Subtraction Angiography: Subsequent Detection of Aneurysms and Complication Rates of Repeated Angiography

Regina Nützel*
1   Department of Neurosurgery, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
,
Silvio Brandt*
2   Department of Radiology, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
3   Department of Radiology and Neuroradiology, Chemnitz Hospital, Chemnitz, Germany
,
Stefan Rampp
1   Department of Neurosurgery, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
,
Sandra Leisz
1   Department of Neurosurgery, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
,
Sebastian Simmermacher
1   Department of Neurosurgery, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
,
Julian Prell
1   Department of Neurosurgery, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
,
Christian Strauss
1   Department of Neurosurgery, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
,
1   Department of Neurosurgery, Medical Faculty, Martin Luther University Halle-Wittenberg, Halle, Germany
› Author Affiliations

Abstract

Background The data on handling of spontaneous, nontraumatic subarachnoid hemorrhage (SAH) with negative initial digital subtraction angiography (DSA) are still inconclusive. The intention of this study was to evaluate the requirement of repeat DSA in patients with negative initial DSA and to compare the clinical outcomes of these cases.

Methods In a retrospective study, we reviewed patients with SAH and negative initial DSA treated in our department from January 2006 until December 2017. The patients were divided according to an established radiographic classification into perimesencephalic (pm) and nonperimesencephalic (npm) SAH. An interventional neuroradiologist and a neurosurgeon reviewed all DSA scans.

Results In all, 52 patients with negative initial DSA, comprising 36 (69.2%) patients with pm and 16 (30.8%) patients with npm bleeding pattern, were included. All patients underwent a second and 23 of these patients underwent a third DSA. In these 23 patients, subarachnoid blood distribution in the initial computed tomography (CT) scan was suspicious for the presence of aneurysm. In total, two aneurysms were detected during the second DSA (diagnostic yield: 3.85%). Both were in the pm group (diagnostic yield: 5.6%). The second repeat DSA did not show any causative vascular lesion. Complications after the DSA occurred in only 2 of 127 patients (1.6%). The rate of complications concerning vasospasm (pm 52.8%, npm 56.3%), hydrocephalus (pm 47.2%, npm 50%), and the need for temporary or permanent shunt (pm 44.4%, npm 50%) was similar in both groups and there was no statistically significant difference.

Conclusion Repeat DSA after negative initial DSA in pm SAH had a diagnostic yield of 5.6%. However, a second repeat DSA cannot be recommended in case of SAH with initial negative DSA. The pm SAH should not be underrated concerning the occurrence of complications and cared with a high level of surveillance.

* Both authors contributed equally.




Publication History

Received: 22 September 2021

Accepted: 03 March 2022

Article published online:
27 October 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Greenberg MS. Handbook of neurosurgery. 8th ed.. New York, NY: Thieme Medical Publishers; 2016
  • 2 Rinkel GJ, Wijdicks EF, Hasan D. et al. Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet 1991; 338 (8773): 964-968
  • 3 Rinkel GJ, Wijdicks EF, Vermeulen M. et al. Nonaneurysmalperimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from aneurysmal rupture. AJNR Am J Neuroradiol 1991; 12 (05) 829-834
  • 4 Lin N, Zenonos G, Kim AH. et al. Angiogram-negative subarachnoid hemorrhage: relationship between bleeding pattern and clinical outcome. Neurocrit Care 2012; 16 (03) 389-398
  • 5 Bashir A, Mikkelsen R, Sørensen L, Sunde N. Non-aneurysmal subarachnoid hemorrhage: when is a second angiography indicated?. Neuroradiol J 2018; 31 (03) 244-252
  • 6 Dalyai R, Chalouhi N, Theofanis T. 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 (04) 646-652 , discussion 651–652
  • 7 Yu DW, Jung YJ, Choi BY, Chang CH. Subarachnoid hemorrhage with negative baseline digital subtraction angiography: is repeat digital subtraction angiography necessary?. J CerebrovascEndovascNeurosurg 2012; 14 (03) 210-215
  • 8 Şahin S, Delen E, Korfali E. Perimesencephalic subarachnoid hemorrhage: etiologies, risk factors, and necessity of the second angiogram. Asian J Neurosurg 2016; 11 (01) 50-53
  • 9 Ackermann H, Arendt G, Baron R. et al. Leitlinien für Diagnostik und Therapie in der Neurologie. 4., überarbeitete Auflage ed. Georg Thieme Verlag; 2008
  • 10 Delgado Almandoz JE, Jagadeesan BD, Refai D. et al. Diagnostic yield of repeat catheter angiography in patients with catheter and computed tomography angiography negative subarachnoid hemorrhage. Neurosurgery 2012; 70 (05) 1135-1142
  • 11 Geng B, Wu X, Brackett A, Malhotra A. Meta-analysis of recent literature on utility of follow-up imaging in isolated perimesencephalic hemorrhage. ClinNeurolNeurosurg 2019; 180: 111-116
  • 12 Heit JJ, Pastena GT, Nogueira RG. et al. Cerebral angiography for evaluation of patients with CT angiogram-negative subarachnoid hemorrhage: an 11-year experience. AJNR Am J Neuroradiol 2016; 37 (02) 297-304
  • 13 Tatter SB, Crowell RM, Ogilvy CS. Aneurysmal and microaneurysmal “angiogram-negative” subarachnoid hemorrhage. Neurosurgery 1995; 37 (01) 48-55
  • 14 Akcakaya MO, Aydoseli A, Aras Y. et al. Clinical course of non-traumatic non-aneurysmal subarachnoid hemorrhage: a single institution experience over 10 years and review of the contemporary literature. Turk Neurosurg 2017; 27 (05) 732-742
  • 15 Al-Mufti F, Merkler AE, Boehme AK. et al. Functional outcomes and delayed cerebral ischemia following nonperimesencephalic angiogram-negative subarachnoid hemorrhage similar to aneurysmal subarachnoid hemorrhage. Neurosurgery 2018; 82 (03) 359-364
  • 16 Canneti B, Mosqueira AJ, Nombela F, Gilo F, Vivancos J. Spontaneous subarachnoid hemorrhage with negative angiography managed in a stroke unit: clinical and prognostic characteristics. J Stroke Cerebrovasc Dis 2015; 24 (11) 2484-2490
  • 17 Arendt G, Aschenberg S, Ayzenberg I. et al. Fink GR, Gold R, Berlit P. eds. SOPs Neurologie. Stuttgart: Georg Thieme Verlag; 2018. . Available at: http://www.thieme-connect.de/products/ebooks/book/10.1055/b-006-149612
  • 18 Jung JY, Kim YB, Lee JW, Huh SK, Lee KC. Spontaneous subarachnoid haemorrhage with negative initial angiography: a review of 143 cases. J ClinNeurosci 2006; 13 (10) 1011-1017
  • 19 Alakbarzade V, Pereira AC. Cerebral catheter angiography and its complications. PractNeurol 2018; 18 (05) 393-398
  • 20 Dawkins AA, Evans AL, Wattam J. et al. Complications of cerebral angiography: a prospective analysis of 2,924 consecutive procedures. Neuroradiology 2007; 49 (09) 753-759
  • 21 Fifi JT, Meyers PM, Lavine SD. et al. Complications of modern diagnostic cerebral angiography in an academic medical center. J VascIntervRadiol 2009; 20 (04) 442-447
  • 22 Leffers AM, Wagner A. Neurologic complications of cerebral angiography. A retrospective study of complication rate and patient risk factors. ActaRadiol 2000; 41 (03) 204-210
  • 23 Petridis AK, Kamp MA, Cornelius JF. et al. Aneurysmal subarachnoid hemorrhage. DtschArzteblInt 2017; 114 (13) 226-236
  • 24 Ringelstein A, Mueller O, Timochenko O. et al. Reangiography after perimesencephalic subarachnoid hemorrhage. Nervenarzt 2013; 84 (06) 715-719
  • 25 Brinjikji W, Kallmes DF, White JB, Lanzino G, Morris JM, Cloft HJ. Inter- and intraobserver agreement in CT characterization of nonaneurysmalperimesencephalic subarachnoid hemorrhage. AJNR Am J Neuroradiol 2010; 31 (06) 1103-1105
  • 26 Hashimoto H, Iida J, Shin Y, Hironaka Y, Sakaki T. Spinal dural arteriovenous fistula with perimesencephalic subarachnoid haemorrhage. J ClinNeurosci 2000; 7 (01) 64-66
  • 27 Valle EP, Tamargo RJ, Gailloud P. Thrombosis and subsequent recanalization of a ruptured intracranial aneurysm in 2 children, demonstrating the value of repeating catheter angiography after an initial negative study. J NeurosurgPediatr 2010; 5 (04) 346-349
  • 28 Samaniego EA, Dabus G, Fuentes K, Linfante I. Endovascular treatment of severe vasospasm in nonaneurysmalperimesencephalic subarachnoid hemorrhage. Neurocrit Care 2011; 15 (03) 537-541
  • 29 Inamasu J, Nakamura Y, Saito R. et al. “Occult” ruptured cerebral aneurysms revealed by repeat angiography: result from a large retrospective study. ClinNeurolNeurosurg 2003; 106 (01) 33-37