Baseline characteristics and outcome for aneurysmal versus non-aneurysmal subarachnoid hemorrhage: a prospective cohort study

Catharina Conzen, Miriam Weiss, Walid Albanna, Katharina Seyfried, Tobias P Schmidt, Omid Nikoubashman, Christian Stoppe, Hans Clusmann, Gerrit A Schubert, Catharina Conzen, Miriam Weiss, Walid Albanna, Katharina Seyfried, Tobias P Schmidt, Omid Nikoubashman, Christian Stoppe, Hans Clusmann, Gerrit A Schubert

Abstract

This study aims to investigate the characteristics of patients with mild aneurysmal and non-aneurysmal perimesencephalic and non-perimesencephalic subarachnoid hemorrhage (aSAH, pmSAH, npmSAH) with emphasis on admission biomarkers, clinical course, and outcome. A prospective cohort of 115 patients with aSAH (Hunt and Hess 1-3) and of 35 patients without aneurysms (16 pmSAH and 19 npmSAH) admitted between January 2014 and January 2020 was included. Demographic data, blood samples on admission, complications (hydrocephalus, shunt dependency, delayed cerebral ischemia DCI, DCI-related infarction, and mortality), and outcome after 6 months were analyzed. Demographic data was comparable between all groups except for age (aSAH 55 [48-65] vs. npmSAH 60 [56-68] vs. pmSAH 52 [42-60], p = 0.032) and loss of consciousness (33% vs. 0% vs. 0%, p = 0.0004). Admission biomarkers showed poorer renal function and highest glucose levels for npmSAH patients. Complication rate in npmSAH was high and comparable to that of aSAH patients (hydrocephalus, shunt dependency, DCI, DCI-related infarction, mortality), but nearly absent in patients with pmSAH. Favorable outcome after 6 months was seen in 92.9% of pmSAH, 83.3% of npmSAH, and 62.7% of aSAH (p = 0.0264). In this prospective cohort of SAH patients, npmSAH was associated with a complicated clinical course, comparable to that of patients with aSAH. In contrast, such complications were nearly absent in pmSAH patients, suggesting fundamental differences in the pathophysiology of patients with different types of non-aneurysmal hemorrhage. Our findings underline the importance for a precise terminology according the hemorrhage etiology as a basis for more vigilant management of npmSAH patients. NCT02142166, 05/20/2014, retrospectively registered.

Keywords: Angiographically negative; Delayed cerebral ischemia; Good grade; Non-perimesencephalic; Perimesencephalic; Subarachnoid hemorrhage.

Conflict of interest statement

The authors declare no competing interests.

© 2021. The Author(s).

Figures

Fig. 1
Fig. 1
Flowchart of prospective cohort enrolment. In naSAH, no patient met the exclusion criteria Hunt and Hess 4 and 5, ASDH, or ICH. na, non-aneurysmal; npm, non-perimesencephalic; pm, perimesencephalic; ICH, intracerebral hemorrhage; aSDH, acute subdural hematoma
Fig. 2
Fig. 2
Clinical course and complications of the different SAH entities. A Rate of acute hydrocephalus (in percentage) was comparable between aSAH and npmSAH, but significantly lower in pmSAH. B Length of stay was longest in aSAH, but comparable to npmSAH (box-whisker, min–max). C Rate of DCI (in percentage) was comparable between aSAH and npmSAH, but lowest in pmSAH. D DCI-related infarction (in percentage) showed no differences between groups though missing in pmSAH. aSAH, aneurysmal subarachnoid hemorrhage (n = 115); npmSAH, non-perimesencephalic SAH (n = 19); pmSAH, perimesencephalic SAH (n = 16); DCI, delayed cerebral ischemia
Fig. 3
Fig. 3
Neurological outcome after 6 months. A Dichotomized neurological outcome after 6 months is depicted for aSAH (n = 102), npmSAH (n = 18), and pmSAH (n = 14) (good = modified Rankin scale (mRS) 0–2, poor = mRS 3–6). Absolute numbers of poor outcome are highest in aSAH and lowest in pmSAH, but differences are not statistically significant in multiple comparison test. B All mRS grades for all groups without dichotomization. aSAH, aneurysmal subarachnoid hemorrhage; npmSAH, non-perimesencephalic SAH; pm, perimesencephalic SAH

References

    1. Al-Mufti F, Merkler AE, Boehme AK, Dancour E, May T, Schmidt JM, Park S, Connolly ES, Lavine SD, Meyers PM, et al. Functional outcomes and delayed cerebral ischemia following nonperimesencephalic angiogram-negative subarachnoid hemorrhage similar to aneurysmal subarachnoid hemorrhage. Neurosurgery. 2018;82(3):359–364. doi: 10.1093/neuros/nyx188.
    1. Alhoobi M, Abu-Qadous F, Khan M, Shaaban A, Shaikh N, Hammadi F, Abu-Jarir R, Albanna W, Alrumaihi G, Belkhair S, et al. Ten years’ experiences in the treatment of nonaneurysmal subarachnoid hemorrhage: a retrospective analysis of outcome parameters in a single-center study. Asian J Neurosurg. 2020;15(2):315–321. doi: 10.4103/ajns.AJNS_315_19.
    1. Buyukkaya R, Yildirim N, Cebeci H, Kocaeli H, Dusak A, Ocakoglu G, Erdogan C, Hakyemez B. The relationship between perimesencephalic subarachnoid hemorrhage and deep venous system drainage pattern and calibrations. Clin Imaging. 2014;38(3):226–230. doi: 10.1016/j.clinimag.2014.01.003.
    1. Chou SH, Robertson CS. Participants in the International Multi-disciplinary Consensus Conference on the Multimodality M: Monitoring biomarkers of cellular injury and death in acute brain injury. Neurocrit Care. 2014;21(Suppl 2):S187–214. doi: 10.1007/s12028-014-0039-z.
    1. Conzen C, Becker K, Albanna W, Weiss M, Bach A, Lushina N, Steimers A, Pinkernell S, Clusmann H, Lindauer U, et al. The Acute phase of experimental subarachnoid hemorrhage: intracranial pressure dynamics and their effect on cerebral blood flow and autoregulation. Transl Stroke Res. 2019;10(5):566–582. doi: 10.1007/s12975-018-0674-3.
    1. Elhadi AM, Zabramski JM, Almefty KK, Mendes GA, Nakaji P, McDougall CG, Albuquerque FC, Preul MC, Spetzler RF. Spontaneous subarachnoid hemorrhage of unknown origin: hospital course and long-term clinical and angiographic follow-up. J Neurosurg. 2015;122(3):663–670. doi: 10.3171/2014.10.JNS14175.
    1. Frontera JA, Fernandez A, Claassen J, Schmidt M, Schumacher HC, Wartenberg K, Temes R, Parra A, Ostapkovich ND, Mayer SA. Hyperglycemia after SAH: predictors, associated complications, and impact on outcome. Stroke. 2006;37(1):199–203. doi: 10.1161/01.STR.0000194960.73883.0f.
    1. Fujiki Y, Matano F, Mizunari T, Murai Y, Tateyama K, Koketsu K, Kubota A, Kobayashi S, Yokota H, Morita A. Serum glucose/potassium ratio as a clinical risk factor for aneurysmal subarachnoid hemorrhage. J Neurosurg. 2018;129(4):870–875. doi: 10.3171/2017.5.JNS162799.
    1. Jabbarli R, Pierscianek D, DarkwahOppong M, Sato T, Dammann P, Wrede KH, Kaier K, Kohrmann M, Forsting M, Kleinschnitz C, et al. Laboratory biomarkers of delayed cerebral ischemia after subarachnoid hemorrhage: a systematic review. Neurosurg Rev. 2018;43(3):825–833. doi: 10.1007/s10143-018-1037-y.
    1. Kang DH, Park J, Lee SH, Park SH, Kim YS, Hamm IS. Does non-perimesencephalic type non-aneurysmal subarachnoid hemorrhage have a benign prognosis? J Clin Neurosc. 2009;16(7):904–908. doi: 10.1016/j.jocn.2008.10.008.
    1. Kapadia A, Schweizer TA, Spears J, Cusimano M, Macdonald RL. Nonaneurysmal perimesencephalic subarachnoid hemorrhage: diagnosis, pathophysiology, clinical characteristics, and long-term outcome. World Neurosurg. 2014;82(6):1131–1143. doi: 10.1016/j.wneu.2014.07.006.
    1. Konczalla J, Kashefiolasl S, Brawanski N, Lescher S, Senft C, Platz J, Seifert V. Cerebral vasospasm and delayed cerebral infarctions in 225 patients with non-aneurysmal subarachnoid hemorrhage: the underestimated risk of Fisher 3 blood distribution. J Neurointerv Surg. 2016;8(12):1247–1252. doi: 10.1136/neurintsurg-2015-012153.
    1. Konczalla J, Platz J, Schuss P, Vatter H, Seifert V, Guresir E. Non-aneurysmal non-traumatic subarachnoid hemorrhage: patient characteristics, clinical outcome and prognostic factors based on a single-center experience in 125 patients. BMC Neurol. 2014;14:140. doi: 10.1186/1471-2377-14-140.
    1. Kruyt ND, Biessels GJ, de Haan RJ, Vermeulen M, Rinkel GJ, Coert B, Roos YB. Hyperglycemia and clinical outcome in aneurysmal subarachnoid hemorrhage: a meta-analysis. Stroke. 2009;40(6):e424–430. doi: 10.1161/STROKEAHA.108.529974.
    1. Lago A, Lopez-Cuevas R, Tembl JI, Fortea G, Gorriz D, Aparici F, Parkhutik V. Short- and long-term outcomes in non-aneurysmal non-perimesencephalic subarachnoid hemorrhage. Neurol Res. 2016;38(8):692–697. doi: 10.1080/01616412.2016.1200306.
    1. Mensing LA, Vergouwen MDI, Laban KG, Ruigrok YM, Velthuis BK, Algra A, Rinkel GJE (2018) Perimesencephalic hemorrhage: a review of epidemiology, risk factors, presumed cause, clinical course, and outcome. Stroke 49(6):1363–1
    1. Nesvick CL, Oushy S, Rinaldo L, Wijdicks EF, Lanzino G, Rabinstein AA. Clinical complications and outcomes of angiographically negative subarachnoid hemorrhage. Neurology. 2019;92(20):e2385–e2394. doi: 10.1212/WNL.0000000000007501.
    1. Okazaki T, Hifumi T, Kawakita K, Shishido H, Ogawa D, Okauchi M, Shindo A, Kawanishi M, Tamiya T, Kuroda Y. Blood glucose variability: a strong independent predictor of neurological outcomes in aneurysmal subarachnoid hemorrhage. J Intensive Care Med. 2018;33(3):189–195. doi: 10.1177/0885066616669328.
    1. Raya A, Zipfel GJ, Diringer MN, Dacey RG, Jr, Derdeyn CP, Rich KM, Chicoine MR, Dhar R. Pattern not volume of bleeding predicts angiographic vasospasm in nonaneurysmal subarachnoid hemorrhage. Stroke. 2014;45(1):265–267. doi: 10.1161/STROKEAHA.113.002629.
    1. Rinkel GJ, Wijdicks EF, Hasan D, Kienstra GE, Franke CL, Hageman LM, Vermeulen M, van Gijn J. Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography. Lancet. 1991;338(8773):964–968. doi: 10.1016/0140-6736(91)91836-J.
    1. Rouchaud A, Lehman VT, Murad MH, Burrows A, Cloft HJ, Lindell EP, Kallmes DF, Brinjikji W. Nonaneurysmal perimesencephalic hemorrhage is associated with deep cerebral venous drainage anomalies: a systematic literature review and meta-analysis. AJNR Am J Neuroradiol. 2016;37(9):1657–1663. doi: 10.3174/ajnr.A4806.
    1. Schuss P, Hadjiathanasiou A, Brandecker S, Guresir A, Vatter H, Guresir E. Elevated C-reactive protein and white blood cell count at admission predict functional outcome after non-aneurysmal subarachnoid hemorrhage. J Neurol. 2018;265(12):2944–2948. doi: 10.1007/s00415-018-9091-5.
    1. van Gijn J, van Dongen KJ, Vermeulen M, Hijdra A. Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology. 1985;35(4):493–497. doi: 10.1212/WNL.35.4.493.
    1. van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain. 2001;124(Pt 2):249–278. doi: 10.1093/brain/124.2.249.
    1. Vergouwen MD, Vermeulen M, van Gijn J, Rinkel GJ, Wijdicks EF, Muizelaar JP, Mendelow AD, Juvela S, Yonas H, Terbrugge KG, et al. Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010;41(10):2391–2395. doi: 10.1161/STROKEAHA.110.589275.
    1. Vergouwen MD, van Geloven N, de Haan RJ, Kruyt ND, Vermeulen M, Roos YB. Increased cortisol levels are associated with delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage. Neurocrit Care. 2010;12(3):342–345. doi: 10.1007/s12028-010-9331-8.
    1. Weiss M, Conzen C, Mueller M, Wiesmann M, Clusmann H, Albanna W, Schubert GA. Endovascular rescue treatment for delayed cerebral ischemia after subarachnoid hemorrhage is safe and effective. Front Neurol. 2019;10:136. doi: 10.3389/fneur.2019.00136.

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