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Deep venous drainage variant rate and degree may be higher in patients with perimesencephalic than in non-perimesencephalic angiogram-negative subarachnoid hemorrhage

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A Correction to this article was published on 23 December 2020

This article has been updated

Abstract

Objectives

The basal vein of Rosenthal (BVR) variant is a potential origin of bleeding in angiogram-negative subarachnoid hemorrhage (AN-SAH). We compared the rate and degree of BVR variants in patients with perimesencephalic AN-SAH (PAN-SAH) and non-perimesencephalic AN-SAH (NPAN-SAH).

Methods

We retrospectively reviewed the records of AN-SAH patients admitted to our hospital between 2013 and 2018. The associations between variables (baseline characteristics, clinical and radiological data, and outcome) with bleeding patterns and degree of BVR variants were analyzed. Additionally, potential predictors of positive findings on repeated digital-subtracted angiogram (DSA), rebleeding, delayed cerebral infarction (DCI), and poor outcome were further studied.

Results

A total of 273 patients with AN-SAH were included. The incidence rate and degree of BVR variants were significantly higher in PAN-SAH patients compared with those in NPAN-SAH patients (p < 0.001). Patients with normal bilateral BVRs are more likely to have a severe prognosis and diffused blood distribution (p < 0.05). We found an increased rate of positive findings on repeated DSA, DCI, rebleeding, and poor outcome at 3 months and 1 year after discharge (all p < 0.05) in patients with bilateral normal BVRs. Bilateral normal BVRs were considered a risk factor (predictor) of positive findings on repeated DSA, rebleeding, and poor outcome (all p < 0.05).

Conclusions

PAN-SAH patients have a higher rate and degree of BVR variants compared with patients with NPAN-SAH. Those AN-SAH patients with bilateral normal BVRs are more likely to be of arterial origin and are at risk of suffering from rebleeding and a poor outcome.

Key Points

• Patients with PAN-SAH have a higher rate and degree of BVR variants compared with patients with NPAN-SAH, which suggested that AN-SAH patients with normal BVRs are more likely to originate from arterial bleeding.

• AN-SAH patients with normal BVRs are more likely to have positive findings on repeated DSA examinations, as well as an increased incidence of rebleeding and poor outcome, which may assist and guide neurologists in selecting treatment.

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Abbreviations

AN-SAH:

Angiogram-negative subarachnoid hemorrhage

BVR:

Basal vein of Rosenthal

CT:

Computed tomography

HH:

Hunt and Hess

IVH:

Intraventricular hemorrhage

mFS:

Modified Fisher scale

NPAN-SAH:

Non-perimesencephalic angiogram-negative subarachnoid hemorrhage

PAN-SAH:

Perimesencephalic angiogram-negative subarachnoid hemorrhage

SAH:

Subarachnoid hemorrhage

SEBES:

Subarachnoid Hemorrhage Early Brain Edema Score

WFNS:

World Federation of Neurosurgeons Scale

References

  1. Al-Mufti F, Merkler AE, Boehme AK et al (2018) Functional outcomes and delayed cerebral ischemia following nonperimesencephalic angiogram-negative subarachnoid hemorrhage similar to aneurysmal subarachnoid hemorrhage. Neurosurgery 82:359–364

    Article  Google Scholar 

  2. Suarez JI, Tarr RW, Selman WR (2006) Aneurysmal subarachnoid hemorrhage. N Engl J Med 354:387–396

    Article  CAS  Google Scholar 

  3. van Gijn J, van Dongen KJ, Vermeulen M, Hijdra A (1985) Perimesencephalic hemorrhage: a nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology 35:493–497

    Article  Google Scholar 

  4. Xu L, Fang Y, Shi X et al (2017) Management of spontaneous subarachnoid hemorrhage patients with negative initial digital subtraction angiogram findings: conservative or aggressive? Biomed Res Int 2017:2486859

    PubMed  PubMed Central  Google Scholar 

  5. Britz GW, Towner J, Vates GE, Nossek E, Langer DJ (2018) Functional outcomes and delayed cerebral ischemia following nonperimesencephalic angiogram-negative subarachnoid hemorrhage similar to aneurysmal subarachnoid hemorrhage COMMENTS. Neurosurgery 82:364–364

    Google Scholar 

  6. Lin N, Zenonos G, Kim AH et al (2012) Angiogram-negative subarachnoid hemorrhage: relationship between bleeding pattern and clinical outcome. Neurocrit Care 16:389–398

    Article  Google Scholar 

  7. Rouchaud A, Lehman VT, Murad MH et al (2016) Nonaneurysmal perimesencephalic hemorrhage is associated with deep cerebral venous drainage anomalies: a systematic literature review and meta-analysis. AJNR Am J Neuroradiol 37:1657–1663

    Article  CAS  Google Scholar 

  8. Buyukkaya R, Yildirim N, Cebeci H et al (2014) The relationship between perimesencephalic subarachnoid hemorrhage and deep venous system drainage pattern and calibrations. Clin Imaging 38:226–230

    Article  Google Scholar 

  9. Song JH, Yeon JY, Kim KH, Jeon P, Kim JS, Hong SC (2010) Angiographic analysis of venous drainage and a variant basal vein of Rosenthal in spontaneous idiopathic subarachnoid hemorrhage. J Clin Neurosci 17:1386–1390

    Article  Google Scholar 

  10. Yamakawa H, Ohe N, Yano H, Yoshimura S, Iwama T (2008) Venous drainage patterns in perimesencephalic nonaneurysmal subarachnoid hemorrhage. Clin Neurol Neurosurg 110:587–591

    Article  Google Scholar 

  11. Daenekindt T, Wilms G, Thijs V, Demaerel P, Van Calenbergh F (2008) Variants of the basal vein of Rosenthal and perimesencephalic nonaneurysmal hemorrhage. Surg Neurol 69:526–529 discussion 529

    Article  Google Scholar 

  12. Alen JF, Lagares A, Campollo J et al (2008) Idiopathic subarachnoid hemorrhage and venous drainage: are they related? Neurosurgery 63:1106–1111 discussion 1111-1102

    Article  Google Scholar 

  13. Watanabe A, Hirano K, Kamada M et al (2002) Perimesencephalic nonaneurysmal subarachnoid haemorrhage and variations in the veins. Neuroradiology 44:319–325

    Article  CAS  Google Scholar 

  14. van der Schaaf IC, Velthuis BK, Gouw A, Rinkel GJ (2004) Venous drainage in perimesencephalic hemorrhage. Stroke 35:1614–1618

    Article  Google Scholar 

  15. Kawamura Y, Narumi O, Chin M, Yamagata S (2011) Variant deep cerebral venous drainage in idiopathic subarachnoid hemorrhage. Neurol Med Chir (Tokyo) 51:97–100

    Article  Google Scholar 

  16. Sabatino G, Della Pepa GM, Scerrati A et al (2014) Anatomical variants of the basal vein of Rosenthal: prevalence in idiopathic subarachnoid hemorrhage. Acta Neurochir (Wien) 156:45–51

    Article  CAS  Google Scholar 

  17. Xu J, Xu L, Wu Z, Chen X, Yu J, Zhang J (2015) Fetal-type posterior cerebral artery: the pitfall of parent artery occlusion for ruptured P(2) segment and distal aneurysms. J Neurosurg 123:906–914

    Article  CAS  Google Scholar 

  18. Connolly ES, Rabinstein AA, Carhuapoma JR et al (2012) Guidelines for the management of aneurysmal subarachnoid hemorrhage a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 43:1711–1737

    Article  Google Scholar 

  19. Diringer MN, Bleck TP, Claude Hemphill J 3rd et al (2011) Critical care management of patients following aneurysmal subarachnoid hemorrhage: recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference. Neurocrit Care 15:211–240

    Article  Google Scholar 

  20. Hunt WE, Hess RM (1968) Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14–20

    Article  CAS  Google Scholar 

  21. Rosen DS, Macdonald RL (2004) Grading of subarachnoid hemorrhage: modification of the World Federation of Neurosurgical Societies Scale on the basis of data for a large series of patients. Neurosurgery 54:566–576

    Article  Google Scholar 

  22. Frontera JA, Claassen J, Schmidt JM et al (2006) Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified Fisher scale. Neurosurgery 59:21–27 discussion 21-27

    Article  Google Scholar 

  23. Ahn SH, Savarraj JP, Pervez M et al (2017) The subarachnoid hemorrhage early brain edema score predicts delayed cerebral ischemia and clinical outcomes. Neurosurgery. https://doi.org/10.1093/neuros/nyx364

  24. Mensing LA, Vergouwen MDI, Laban KG et al (2018) Perimesencephalic hemorrhage: a review of epidemiology, risk factors, presumed cause, clinical course, and outcome. Stroke 49:1363–1370

    Article  Google Scholar 

  25. Fang YJ, Mei SH, Lu JN et al (2019) New risk score of the early period after spontaneous subarachnoid hemorrhage: for the prediction of delayed cerebral ischemia. CNS Neurosci Ther. https://doi.org/10.1111/cns.13202

  26. Wijdicks EF, Schievink WI (1997) Perimesencephalic nonaneurysmal subarachnoid hemorrhage: first hint of a cause? Neurology 49:634–636

    Article  CAS  Google Scholar 

  27. Alexander MS, Dias PS, Uttley D (1986) Spontaneous subarachnoid hemorrhage and negative cerebral panangiography. Review of 140 cases. J Neurosurg 64:537–542

    Article  CAS  Google Scholar 

  28. Chung JI, Weon YC (2005) Anatomic variations of the deep cerebral veins,tributaries of Basal vein of rosenthal: embryologic aspects of the regressed embryonic tentorial sinus. Interv Neuroradiol 11:123–130

    Article  CAS  Google Scholar 

  29. San Millan Ruiz D, Gailloud P, Rufenacht DA, Delavelle J, Henry F, Fasel JH (2002) The craniocervical venous system in relation to cerebral venous drainage. AJNR Am J Neuroradiol 23:1500–1508

    PubMed  Google Scholar 

  30. Matsumaru Y, Yanaka K, Muroi A, Sato H, Kamezaki T, Nose T (2003) Significance of a small bulge on the basilar artery in patients with perimesencephalic nonaneurysmal subarachnoid hemorrhage. Report of two cases. J Neurosurg 98:426–429

    Article  Google Scholar 

  31. Park SQ, Kwon OK, Kim SH, Oh CW, Han MH (2009) Pre-mesencephalic subarachnoid hemorrhage: rupture of tiny aneurysms of the basilar artery perforator. Acta Neurochir 151:1639–1646

    Article  Google Scholar 

  32. Kim YW, Lawson MF, Hoh BL (2012) Nonaneurysmal subarachnoid hemorrhage: an update. Curr Atheroscler Rep 14:328–334

    Article  Google Scholar 

  33. Yu DW, Jung YJ, Choi BY, Chang CH (2012) Subarachnoid hemorrhage with negative baseline digital subtraction angiography: is repeat digital subtraction angiography necessary? J Cerebrovasc Endovasc Neurosurg 14:210–215

    Article  Google Scholar 

  34. Kaufmann TJ, Huston J 3rd, Mandrekar JN, Schleck CD, Thielen KR, Kallmes DF (2007) Complications of diagnostic cerebral angiography: evaluation of 19,826 consecutive patients. Radiology 243:812–819

    Article  Google Scholar 

  35. Kapadia A, Schweizer TA, Spears J, Cusimano M, Macdonald RL (2014) Nonaneurysmal perimesencephalic subarachnoid hemorrhage: diagnosis, pathophysiology, clinical characteristics, and long-term outcome. World Neurosurg 82:1131–1143

    Article  Google Scholar 

  36. Boswell S, Thorell W, Gogela S, Lyden E, Surdell D (2013) Angiogram-negative subarachnoid hemorrhage: outcomes data and review of the literature. J Stroke Cerebrovasc Dis 22:750–757

    Article  Google Scholar 

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Acknowledgments

We gratefully acknowledge Dr. Hui Shi from Yongchuan Hospital (Chongqing, China) for assisting with the conception of this manuscript. Prof. Jianmin Zhang is the “guarantor” for the entire study.

Funding

This research was supported by the National Natural Science Foundation of China (81870916 and 81971107) and Youth Fund of the National Natural Science Fund project (81701214).

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Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sheng Chen or Jianmin Zhang.

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Guarantor

The scientific guarantor of this publication is Prof. Jianmin Zhang.

Conflict of interest

The authors declare no conflict of interest concerning the findings specified in this paper.

Statistics

Yuanjian Fang and Yi Huang have significant statistical expertise.

Ethics approval statements

This study was approved by Institutional Review Board of The Second Affiliated Hospital of Zhejiang University School of Medicine. No patient consent was required in our study as our Institutional Review Board has approved full waiver of consent.

Methodology

• Retrospective

• Cross-sectional study

• Single center

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The original online version of this article was revised: In the last paragraph of section “Variables”, the third sentence should read: “Scores ranging from 4 to 5 for WFNS and 3–5 HH and 3–4 for mRS and SEBES were considered high for each respective scoring method.” In addition, the definition for WSFN was given incorrectly in tables 1, 3 and 4 and the values of High WFNS were partly incorrect in Table 3.

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Fang, Y., Shao, A., Wang, X. et al. Deep venous drainage variant rate and degree may be higher in patients with perimesencephalic than in non-perimesencephalic angiogram-negative subarachnoid hemorrhage. Eur Radiol 31, 1290–1299 (2021). https://doi.org/10.1007/s00330-020-07242-5

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