In-hospital mortality and poor outcome after surgical clipping and endovascular coiling for aneurysmal subarachnoid hemorrhage using nationwide databases: a systematic review and meta-analysis

  • Fusao IkawaEmail author
  • Nobuaki Michihata
  • Toshinori Matsushige
  • Masaru Abiko
  • Daizo Ishii
  • Jumpei Oshita
  • Takahito Okazaki
  • Shigeyuki Sakamoto
  • Ryota Kurogi
  • Koji Iihara
  • Kunihiro Nishimura
  • Akio Morita
  • Kiyohide Fushimi
  • Hideo Yasunaga
  • Kaoru Kurisu
Original Article


There has never been evidence for aneurysmal subarachnoid hemorrhage (aSAH) by endovascular coiling compared to surgical clipping with all grade. The present study and meta-analysis aimed to clarify the in-hospital mortality and poor outcome in the nationwide databases of patients with all grade aSAH between them. The outcome of modified Rankin scale (mRS) at discharge was investigated according to the comprehensive nationwide database in Japan. The propensity score-matched analysis was conducted among patients with aSAH in this database registered between 2010 and 2015. Meta-analysis of studies was conducted based on the nationwide databases published from 2007 to 2018. According to this propensity score-matched analysis, no significant association for poor outcome of mRS > 2 was shown between surgical clipping and endovascular coiling (47.7% vs 48.3%, p = 0.48). However, significantly lower in-hospital mortality was revealed after surgical clipping than endovascular coiling (7.1% vs 12.2%, p < 0.001). Meta-analysis of propensity score-matched analysis in the nationwide database showed no significant association for poor outcome at discharge between them (odds ratio [OR], 1.08; 95% confidence interval [CI], 0.93 to 1.26; p = 0.31). Meta-analysis of propensity score-matched analysis for in-hospital mortality was lower after surgical clipping than after endovascular coiling, however, without significant difference (OR, 0.74; 95% CI, 0.52 to 1.04; p = 0.08). Further prospective randomized controlled study with all grade aSAH should be necessary to validate the in-hospital mortality and poor outcome.


Aneurysmal subarachnoid hemorrhage Endovascular coiling In-hospital mortality Meta-analysis Nationwide database Poor outcome Ruptured cerebral aneurysm Surgical clipping 



anterior communicating artery


anterior cerebral artery


endovascular coiling


internal carotid artery


Japan Coma Scale


middle cerebral artery


modified Rankin Scale


Propensity score


subarachnoid hemorrhage


surgical clipping


standard deviation


standard error


United States of America


Authors’ contribution

All authors have made substantial contributions to the intellectual content of the paper, contributed to data interpretation, approved the final manuscript, and agree with submission to this journal.


This work was supported by the Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research (C) 17K10829.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The present study was approved by the Institutional Review Board of Hiroshima University (No. E-629).

Informed consent

The requirement for informed consent was waived because of the anonymous nature of the data and the opt out method.

Systematic reviews and meta-analyses registration

Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines.

The registration ID number for International Prospective Register of Systematic Reviews is 93220.


  1. 1.
    Bijlenga P, Ebeling C, Jaegersberg M, Summers P, Rogers A, Waterworth A, Iavindrasana J, Macho J, Pereira VM, Bukovics P, Vivas E, Sturkenboom MCJM, Wright J, Friedrich CM, Frangi A, Byrne J, Schaller K, Rufenacht D, Collaborators From the @neurIST Investigators, Narata AP, Clarke A, Yarnold J, Kover F, Schatlo B, Hudak S, Teta P, Blasco J, Gonzalez AM, Lovblad KO, Coley S, Dòczi T, Risselada R, Sola T, Lawford P, Patel U, Singh P, Wickins J, Elger B, Beyleveld D, Wood S, Hasselmeyer P, Arbona A, Meyer R, Hose R, Lonsdale G, Hofmann-Apitius M, Investigators, Project Board, Frangi A, Bijlenga P, Hofmann-Apitius M, Hose R, Lonsdale G, Arbona A, Hasselmeyer P, Rüfenacht D, Article writing team, Bijlenga P, Summers P, Jägersberg M, Rogers A, Schaller K, Byrne J, Ethical and legal review committee, Wright J, Wilkins J, Beyleveld D, Elger B, Information platform development and maintenance, Waterworth A, Wood S, Iavindrasana J, Meyer R, Friedrich C, Ebeling C, Epidemiology and statistics, Ebeling C, Bijlenga P, Risselada R, Friedrich C, Sturkenboom MCJM, Participating Centers (In Order of Number of Recruited Patients), Bijlenga P, Jägersberg M, Rogers A, Schatlo B, Teta P, Schaller K, Mendes-Pereira V, Gonzalez AM, Narata AP, Lovblad KO, Rüfenacht DA, Yarnold J, Summers P, Clarke A, Zilani G, Byrne J, Macho J, Blasco J, Bukovics P, Kover F, Hudak I, Doczi T, Risselada R, Sturkenboom MCJM, Singh P, Waterworth A, Patel U, Coley S, Lawford P, Sola T, Vivas E (2013) Risk of rupture of small anterior communicating artery aneurysms is similar to posterior circulation aneurysms. Stroke 44:3018–3026CrossRefGoogle Scholar
  2. 2.
    Brinjikji W, Lanzino G, Rabinstein AA, Kallmes DF, Cloft HJ (2013) Age-related trends in the treatment and outcomes of ruptured cerebral aneurysms: a study of the nationwide inpatient sample 2001-2009. Am J Neuroradiol 34:1022–1027CrossRefGoogle Scholar
  3. 3.
    Connolly ES Jr, Rabinstein AA, Carhuapoma JR, Derdeyn CP, Dion J, Higashida RT 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 43:1711–1737CrossRefGoogle Scholar
  4. 4.
    Cowan JA Jr, Ziewacz J, Dimick JB, Upchurch GR Jr, Thompson BG (2007) Use of endovascular coil embolization and surgical clip occlusion for cerebral artery aneurysms. J Neurosurg 107:530–535CrossRefGoogle Scholar
  5. 5.
    Elijovich L, Higashida RT, Lawton MT, Duckwiler G, Giannotta S, Johnston SC, Cerebral Aneurysm Rerupture After Treatment (CARAT) Investigators (2008) Predictors and outcomes of intraprocedural rupture in patients treated for ruptured intracranial aneurysms: the CARAT study. Stroke 39:1501–1506CrossRefGoogle Scholar
  6. 6.
    Food and Drug Administration (2016) Use of real-world evidence to support regulatory decision-making for medical devices: draft guidance for industry and Food and Drug Administration staff. Accessed 17 Feb 2019
  7. 7.
    Greving JP, Wermer MJ, Brown RD Jr, Morita A, Juvela S, Yonekura M et al (2014) Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol 13:59–66CrossRefGoogle Scholar
  8. 8.
    Hoh BL, Chi YY, Lawson MF, Mocco J, Barker FG 2nd (2010) Length of stay and total hospital charges of clipping versus coiling for ruptured and unruptured adult cerebral aneurysms in the Nationwide Inpatient Sample database 2002 to 2006. Stroke 41:337–342CrossRefGoogle Scholar
  9. 9.
    Iihara K, Nishimura K, Kada A, Nakagawara J, Ogasawara K, Ono J, Shiokawa Y, Aruga T, Miyachi S, Nagata I, Toyoda K, Matsuda S, Miyamoto Y, Suzuki A, Ishikawa KB, Kataoka H, Nakamura F, Kamitani S (2014) Effects of comprehensive stroke care capabilities on in-hospital mortality of patients with ischemic and hemorrhagic stroke: J-ASPECT study. PLoS One 9:e96819CrossRefGoogle Scholar
  10. 10.
    Ikawa F, Abiko M, Ishii D, Ohshita J, Matsushige T, Okazaki T et al (2018) Analysis of outcome at discharge after aneurysmal subarachnoid hemorrhage in Japan according to the Japanese stroke databank. Neurosurg Rev 41:567–574CrossRefGoogle Scholar
  11. 11.
    Kurogi R, Kada A, Nishimura K, Kamitani S, Nishimura A, Sayama T, Nakagawara J, Toyoda K, Ogasawara K, Ono J, Shiokawa Y, Aruga T, Miyachi S, Nagata I, Matsuda S, Yoshimura S, Okuchi K, Suzuki A, Nakamura F, Onozuka D, Hagihara A, Iihara K, _ _ (2018) Effect of treatment modality on in-hospital outcome in patients with subarachnoid hemorrhage: a nationwide study in Japan (J-ASPECT study). J Neurosurg 128:1318–1326CrossRefGoogle Scholar
  12. 12.
    Lanzino G, Murad MH, d’Urso PI, Rabinstein AA (2013) Coil embolization versus clipping for ruptured intracranial aneurysms: a meta-analysis of prospective controlled published studies. AJNR Am J Neuroradiol 34:1764–1768CrossRefGoogle Scholar
  13. 13.
    Lindgren A, Vergouwen MD, van der Schaaf I, Algra A, Wermer M, Clarke MJ et al (2018) Endovascular coiling versus neurosurgical clipping for people with aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev 8:CD003085Google Scholar
  14. 14.
    McDonald JS, McDonald RJ, Fan J, Kallmes DF, Lanzino G, Cloft HJ (2014) Comparative effectiveness of ruptured cerebral aneurysm therapies: propensity score analysis of clipping versus coiling. Am J Neuroradiol 35:164–169CrossRefGoogle Scholar
  15. 15.
    Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535CrossRefGoogle Scholar
  16. 16.
    Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J et al (2002) International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 360:1267–1274CrossRefGoogle Scholar
  17. 17.
    Molyneux AJ, Birks J, Clarke A, Sneade M, Kerr RS (2015) The durability of endovascular coiling versus neurosurgical clipping of ruptured cerebral aneurysms: 18 year follow-up of the UK cohort of the International Subarachnoid Aneurysm Trial (ISAT). Lancet 385:691–697CrossRefGoogle Scholar
  18. 18.
    Nieuwkamp DJ, Setz LE, Algra A, Linn FH, de Rooij NK, Rinkel GJ (2009) Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 8:635–642CrossRefGoogle Scholar
  19. 19.
    O’Kelly CJ, Kulkarni AV, Austin PC, Wallace MC, Urbach D (2010) The impact of therapeutic modality on outcomes following repair of ruptured intracranial aneurysms: an administrative data analysis. Clinical article. J Neurosurg 113:795–801CrossRefGoogle Scholar
  20. 20.
    OECD data, health, health equipment. Accessed 17 Feb 2019
  21. 21.
    Ohta T, Kikuchi H, Hashi K, Kudo Y (1986) Nizofenone administration in the acute stage following subarachnoid hemorrhage. Results of a multi-center controlled double-blind clinical study. J Neurosurg 64:420–426CrossRefGoogle Scholar
  22. 22.
    Ono K, Wada K, Takahara T, Shirotani T (2007) Indications for computed tomography in patients with mild head injury. Neurol Med Chir (Tokyo) 47:291–297 discussion 297-298CrossRefGoogle Scholar
  23. 23.
    Qureshi AI, Vazquez G, Tariq N, Suri MF, Lakshminarayan K, Lanzino G (2011) Impact of International Subarachnoid Aneurysm Trial results on treatment of ruptured intracranial aneurysms in the United States. Clinical article. J Neurosurg 114:834–841CrossRefGoogle Scholar
  24. 24.
    Rosen DS, Macdonald RL (2005) Subarachnoid hemorrhage grading scales: a systematic review. Neurocrit Care 2:110–118CrossRefGoogle Scholar
  25. 25.
    Ruano J, Gomez-Garcia F, Gay-Mimbrera J, Aguilar-Luque M, Fernandez-Rueda JL, Fernandez-Chaichio J et al (2018) Evaluating characteristics of PROSPERO records as predictors of eventual publication of non-Cochrane systematic reviews: a meta-epidemiological study protocol. Syst Rev 7:43CrossRefGoogle Scholar
  26. 26.
    Sherman RE, Anderson SA, Dal Pan GJ, Gray GW, Gross T, Hunter NL, LaVange L, Marinac-Dabic D, Marks PW, Robb MA, Shuren J, Temple R, Woodcock J, Yue LQ, Califf RM (2016) Real-world evidence—what is it and what can it tell us? N Engl J Med 375:2293–2297CrossRefGoogle Scholar
  27. 27.
    Shigematsu K, Nakano H, Watanabe Y (2013) The eye response test alone is sufficient to predict stroke outcome—reintroduction of Japan Coma Scale: a cohort study. BMJ Open 3:e002736CrossRefGoogle Scholar
  28. 28.
    Spetzler RF, Zabramski JM, McDougall CG, Albuquerque FC, Hills NK, Wallace RC et al (2018) Analysis of saccular aneurysms in the Barrow Ruptured Aneurysm Trial. J Neurosurg 128:120–125CrossRefGoogle Scholar
  29. 29.
    Stienen MN, Germans M, Burkhardt JK, Neidert MC, Fung C, Bervini D, Zumofen D, Roethlisberger M, Marbacher S, Maduri R, Robert T, Seule MA, Bijlenga P, Schaller K, Fandino J, Smoll NR, Maldaner N, Finkenstädt S, Esposito G, Schatlo B, Keller E, Bozinov O, Regli L, on behalf of the Swiss SOS Study Group, Serra C, Krayenbühl N, Schöni D, Raabe A, Beck J, Goldberg J, Mariani L, Guzman R, D’Alonzo D, Coluccia D, Daniel RT, Starnoni D, Messerer M, Levivier M, Valsecchi D, Arrighi M, Venier A, Reinert M, Kuhlen DE, Ferrari A, Weyerbrock A, Hildebrandt G, Hlavica M, Fournier JY, Corniola M (2018) Predictors of in-hospital death after aneurysmal subarachnoid hemorrhage: analysis of a nationwide database (Swiss SOS [Swiss Study on Aneurysmal Subarachnoid Hemorrhage]). Stroke 49:333–340CrossRefGoogle Scholar
  30. 30.
    Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012CrossRefGoogle Scholar
  31. 31.
    Walendy V, Strauss C, Rachinger J, Stang A (2014) Treatment of aneurysmal subarachnoid haemorrhage in Germany: a nationwide analysis of the years 2005-2009. Neuroepidemiology 42:90–97CrossRefGoogle Scholar
  32. 32.
    Xia ZW, Liu XM, Wang JY, Cao H, Chen FH, Huang J, Li QZ, Fan SS, Jiang B, Chen ZG, Cheng Q (2017) Coiling is not superior to clipping in patients with high-grade aneurysmal subarachnoid hemorrhage: systematic review and meta-analysis. World Neurosurg 98:411–420CrossRefGoogle Scholar
  33. 33.
    Yasunaga HMH, Horiguchi H, Fushimi K, Matsuda S (2013) Clinical epidemiology and health services research using the diagnosis procedure combination database in Japan. Asian Pac J Dis Manag 7:19–24Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Fusao Ikawa
    • 1
    Email author
  • Nobuaki Michihata
    • 2
  • Toshinori Matsushige
    • 3
  • Masaru Abiko
    • 1
  • Daizo Ishii
    • 1
  • Jumpei Oshita
    • 1
  • Takahito Okazaki
    • 1
  • Shigeyuki Sakamoto
    • 1
  • Ryota Kurogi
    • 4
  • Koji Iihara
    • 4
  • Kunihiro Nishimura
    • 5
  • Akio Morita
    • 6
  • Kiyohide Fushimi
    • 7
  • Hideo Yasunaga
    • 2
  • Kaoru Kurisu
    • 1
  1. 1.Department of Neurosurgery, Graduate School of Biomedical and Health SciencesHiroshima UniversityHiroshimaJapan
  2. 2.Department of Clinical Epidemiology and Health Economics, School of Public HealthThe University of TokyoTokyoJapan
  3. 3.Department of Neurosurgery and Interventional NeuroradiologyHiroshima City Asa Citizens HospitalHiroshimaJapan
  4. 4.Department of Neurosurgery, Graduate School of Medical SciencesKyushu UniversityFukuokaJapan
  5. 5.Department of Preventive Medicine and Epidemiologic InformaticsNational Cerebral and Cardiovascular CentreSuitaJapan
  6. 6.Department of Neurological SurgeryNippon Medical School HospitalTokyoJapan
  7. 7.Department of Health Policy and InformaticsTokyo Medical and Dental University Graduate School of MedicineTokyoJapan

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