Advertisement

Neurosurgical Review

, Volume 41, Issue 2, pp 675–682 | Cite as

Symptomatic and silent cerebral infarction following surgical clipping of unruptured intracranial aneurysms: incidence, risk factors, and clinical outcome

  • Maogui Li
  • Jun Wu
  • Xin Chen
  • Pengjun Jiang
  • Fan Yang
  • Yonggang Ma
  • Zhengsong Li
  • Yong Cao
  • Shuo WangEmail author
Original Article

Abstract

Cerebral infarction (CI) associated with clipping of unruptured intracranial aneurysms (UIAs) has not been completely studied. The role of individual and operative characteristics is not known, and the risk of silent CI has not been well described. To determine the incidence, risk factors, and clinical outcome of postoperative CI, we retrospectively analyzed 388 consecutive patients undergoing clipping of UIAs between January 2012 and December 2015. We reviewed the pre- and postoperative computed tomography (CT) images of each patient. Postoperative CI was defined as a new parenchymal hypodensity in the vascular territory of treated artery. Patient-specific, aneurysm-specific, and operative variables were analyzed as potential risk factors. Functional outcome at discharge was assessed with the modified Rankin Scale (mRS). Postoperative CI was found in 49 (12.6%) patients, 29 of whom manifested neurological deficits. The incidences of symptomatic stroke and silent CI were 7.5 and 5.2%, respectively. Multivariate analysis showed that larger aneurysm size and history of hypertension were significantly associated with CI. Disability (mRS > 2) rate was 42.9% among patients with CI, which was substantially higher than that among patients without (0.9%). In conclusion, the incidence of CI following clipping of UIAs was not low. Larger aneurysm size and history of hypertension were independent risk factors. Postoperative symptomatic stroke correlated with an extremely high risk of disability. Silent CI was seemingly nondisabling, but the possible cognitive consequence is pending.

Keywords

Unruptured intracranial aneurysm Surgery Cerebral infarction Computed tomography Risk factor 

Notes

Funding

This study was supported by the projects of National Natural Science Foundation of China (Grant No. 81471210, principal investigator: Professor Shuo Wang). It was also supported by the project of Beijing Municipal Commission of Science and Technology (Grant No. D161100003816004, principal investigator: Professor Yong Cao).

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This study has been approved by the ethics committee of Beijing Tiantan Hospital, Capital Medical University.

Informed consent

The need for written informed consent was waived, due to the retrospective nature of this study.

References

  1. 1.
    Alshekhlee A, Mehta S, Edgell RC, Vora N, Feen E, Mohammadi A, Kale SP, Cruz-Flores S (2010) Hospital mortality and complications of electively clipped or coiled unruptured intracranial aneurysm. Stroke 41:1471–1476.  https://doi.org/10.1161/STROKEAHA.110.580647 CrossRefPubMedGoogle Scholar
  2. 2.
    Bendszus M, Koltzenburg M, Burger R, Warmuth-Metz M, Hofmann E, Solymosi L (1999) Silent embolism in diagnostic cerebral angiography and neurointerventional procedures: a prospective study. Lancet 354:1594–1597.  https://doi.org/10.1016/S0140-6736(99)07083-X CrossRefPubMedGoogle Scholar
  3. 3.
    Byoun HS, Bang JS, CW O, Kwon OK, Hwang G, Han JH, Kim T, Lee SU, Jo SR, Kim DG, Park KS (2016) The incidence of and risk factors for ischemic complications after microsurgical clipping of unruptured middle cerebral artery aneurysms and the efficacy of intraoperative monitoring of somatosensory evoked potentials: a retrospective study. Clin Neurol Neurosurg 151:128–135.  https://doi.org/10.1016/j.clineuro.2016.10.008 CrossRefPubMedGoogle Scholar
  4. 4.
    Chen SF, Kato Y, Kumar A, Tan GW, Oguri D, Oda J, Watabe T, Imizu S, Sano H, Wang ZX (2016) Intraoperative rupture in the surgical treatment of patients with intracranial aneurysms. J Clin Neurosci: Off J Neurosurg Soci Australas 34:63–69.  https://doi.org/10.1016/j.jocn.2016.01.045 CrossRefGoogle Scholar
  5. 5.
    Eftekhar B, Morgan MK (2011) Indications for the use of temporary arterial occlusion during aneurysm repair: an institutional experience. J Clin Neurosci: Off J Neurosurg Soci Australas 18:905–909.  https://doi.org/10.1016/j.jocn.2010.12.009 CrossRefGoogle Scholar
  6. 6.
    Ferch R, Pasqualin A, Pinna G, Chioffi F, Bricolo A (2002) Temporary arterial occlusion in the repair of ruptured intracranial aneurysms: an analysis of risk factors for stroke. J Neurosurg 97:836–842.  https://doi.org/10.3171/jns.2002.97.4.0836 CrossRefPubMedGoogle Scholar
  7. 7.
    Gold G, Kovari E, Herrmann FR, Canuto A, Hof PR, Michel JP, Bouras C, Giannakopoulos P (2005) Cognitive consequences of thalamic, basal ganglia, and deep white matter lacunes in brain aging and dementia. Stroke 36:1184–1188.  https://doi.org/10.1161/01.STR.0000166052.89772.b5 CrossRefPubMedGoogle Scholar
  8. 8.
    Grunwald IQ, Papanagiotou P, Politi M, Struffert T, Roth C, Reith W (2006) Endovascular treatment of unruptured intracranial aneurysms: occurrence of thromboembolic events. Neurosurgery 58:612–618; discussion 612-618.  https://doi.org/10.1227/01.NEU.0000204101.00996.D9 CrossRefPubMedGoogle Scholar
  9. 9.
    Jabbarli R, Reinhard M, Roelz R, Shah M, Niesen WD, Kaier K, Taschner C, Weyerbrock A, Van Velthoven V (2015) Early identification of individuals at high risk for cerebral infarction after aneurysmal subarachnoid hemorrhage: the BEHAVIOR score. J Cereb Blood Flow Metab: Off J Int Soc Cereb Blood Flow Metab 35:1587–1592.  https://doi.org/10.1038/jcbfm.2015.81 CrossRefGoogle Scholar
  10. 10.
    Jabbarli R, Wrede KH, Pierscianek D, Dammann P, El Hindy N, Ozkan N, Muller O, Stolke D, Forsting M, Sure U (2016) Outcome after clipping of unruptured intracranial aneurysms depends on caseload. World Neurosurg 89(666–671):e661.  https://doi.org/10.1016/j.wneu.2015.12.043 Google Scholar
  11. 11.
    Jorgensen HS, Nakayama H, Raaschou HO, Gam J, Olsen TS (1994) Silent infarction in acute stroke patients. Prevalence, localization, risk factors, and clinical significance: the Copenhagen Stroke Study. Stroke 25:97–104CrossRefPubMedGoogle Scholar
  12. 12.
    Juvela S, Siironen J, Kuhmonen J (2005) Hyperglycemia, excess weight, and history of hypertension as risk factors for poor outcome and cerebral infarction after aneurysmal subarachnoid hemorrhage. J Neurosurg 102:998–1003.  https://doi.org/10.3171/jns.2005.102.6.0998 CrossRefPubMedGoogle Scholar
  13. 13.
    Kotowski M, Naggara O, Darsaut TE, Nolet S, Gevry G, Kouznetsov E, Raymond J (2013) Safety and occlusion rates of surgical treatment of unruptured intracranial aneurysms: a systematic review and meta-analysis of the literature from 1990 to 2011. J Neurol Neurosurg Psychiatry 84:42–48.  https://doi.org/10.1136/jnnp-2011-302068 CrossRefPubMedGoogle Scholar
  14. 14.
    Krayenbuhl N, Erdem E, Oinas M, Krisht AF (2009) Symptomatic and silent ischemia associated with microsurgical clipping of intracranial aneurysms: evaluation with diffusion-weighted MRI. Stroke 40:129–133.  https://doi.org/10.1161/STROKEAHA.108.524777 CrossRefPubMedGoogle Scholar
  15. 15.
    Lawton MT, Quinones-Hinojosa A, Chang EF, Yu T (2005) Thrombotic intracranial aneurysms: classification scheme and management strategies in 68 patients. Neurosurgery 56:441–454 discussion 441-454CrossRefPubMedGoogle Scholar
  16. 16.
    Leipzig TJ, Morgan J, Horner TG, Payner T, Redelman K, Johnson CS (2005) Analysis of intraoperative rupture in the surgical treatment of 1694 saccular aneurysms. Neurosurgery 56:455–468 discussion 455-468CrossRefPubMedGoogle Scholar
  17. 17.
    Li MH, Chen SW, Li YD, Chen YC, Cheng YS, DJ H, Tan HQ, Wu Q, Wang W, Sun ZK, Wei XE, Zhang JY, Qiao RH, Zong WH, Zhang Y, Lou W, Chen ZY, Zhu Y, Peng DR, Ding SX, XF X, Hou XH, Jia WP (2013) Prevalence of unruptured cerebral aneurysms in Chinese adults aged 35 to 75 years: a cross-sectional study. Ann Intern Med 159:514–521.  https://doi.org/10.7326/0003-4819-159-8-201310150-00004 CrossRefPubMedGoogle Scholar
  18. 18.
    Macdonald RL, Wallace MC, Kestle JR (1993) Role of angiography following aneurysm surgery. J Neurosurg 79:826–832.  https://doi.org/10.3171/jns.1993.79.6.0826 CrossRefPubMedGoogle Scholar
  19. 19.
    Mahaney KB, Brown RD Jr, Meissner I, Piepgras DG, Huston J 3rd, Zhang J, Torner JC, Investigators I (2014) Age-related differences in unruptured intracranial aneurysms: 1-year outcomes. J Neurosurg 121:1024–1038.  https://doi.org/10.3171/2014.6.JNS121179 CrossRefPubMedGoogle Scholar
  20. 20.
    McDonald JS, McDonald RJ, Fan J, Kallmes DF, Lanzino G, Cloft HJ (2013) Comparative effectiveness of unruptured cerebral aneurysm therapies: propensity score analysis of clipping versus coiling. Stroke 44:988–994.  https://doi.org/10.1161/STROKEAHA.111.000196 CrossRefPubMedGoogle Scholar
  21. 21.
    Mullins ME, Schaefer PW, Sorensen AG, Halpern EF, Ay H, He J, Koroshetz WJ, Gonzalez RG (2002) CT and conventional and diffusion-weighted MR imaging in acute stroke: study in 691 patients at presentation to the emergency department. Radiology 224:353–360.  https://doi.org/10.1148/radiol.2242010873 CrossRefPubMedGoogle Scholar
  22. 22.
    O'Donnell MJ, Xavier D, Liu L, Zhang H, Chin SL, Rao-Melacini P, Rangarajan S, Islam S, Pais P, McQueen MJ, Mondo C, Damasceno A, Lopez-Jaramillo P, Hankey GJ, Dans AL, Yusoff K, Truelsen T, Diener HC, Sacco RL, Ryglewicz D, Czlonkowska A, Weimar C, Wang X, Yusuf S, investigators I (2010) Risk factors for ischaemic and intracerebral haemorrhagic stroke in 22 countries (the INTERSTROKE study): a case-control study. Lancet 376:112–123.  https://doi.org/10.1016/S0140-6736(10)60834-3 CrossRefPubMedGoogle Scholar
  23. 23.
    Ogilvy CS, Carter BS, Kaplan S, Rich C, Crowell RM (1996) Temporary vessel occlusion for aneurysm surgery: risk factors for stroke in patients protected by induced hypothermia and hypertension and intravenous mannitol administration. J Neurosurg 84:785–791.  https://doi.org/10.3171/jns.1996.84.5.0785 CrossRefPubMedGoogle Scholar
  24. 24.
    SH O, Kim NK, Kim SH, Kim JK, Kim HS, Kim WC, Kim OJ (2010) The prevalence and risk factor analysis of silent brain infarction in patients with first-ever ischemic stroke. J Neurol Sci 293:97–101.  https://doi.org/10.1016/j.jns.2010.02.025 CrossRefGoogle Scholar
  25. 25.
    Ohman J, Servo A, Heiskanen O (1991) Risks factors for cerebral infarction in good-grade patients after aneurysmal subarachnoid hemorrhage and surgery: a prospective study. J Neurosurg 74:14–20.  https://doi.org/10.3171/jns.1991.74.1.0014 CrossRefPubMedGoogle Scholar
  26. 26.
    Raabe A, Seidel K (2016) Prevention of ischemic complications during aneurysm surgery. J Neurosurg Sci 60:95–103PubMedGoogle Scholar
  27. 27.
    Rabinstein AA, Weigand S, Atkinson JL, Wijdicks EF (2005) Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke 36:992–997.  https://doi.org/10.1161/01.STR.0000163090.59350.5a CrossRefPubMedGoogle Scholar
  28. 28.
    Rordorf G, Bellon RJ, Budzik RE Jr, Farkas J, Reinking GF, Pergolizzi RS, Ezzeddine M, Norbash AM, Gonzalez RG, Putman CM (2001) Silent thromboembolic events associated with the treatment of unruptured cerebral aneurysms by use of Guglielmi detachable coils: prospective study applying diffusion-weighted imaging. AJNR Am J Neuroradiol 22:5–10PubMedGoogle Scholar
  29. 29.
    Samson D, Batjer HH, Bowman G, Mootz L, Krippner WJ Jr, Meyer YJ, Allen BC (1994) A clinical study of the parameters and effects of temporary arterial occlusion in the management of intracranial aneurysms. Neurosurgery 34:22–28 discussion 28-29PubMedGoogle Scholar
  30. 30.
    Sasaki T, Kodama N, Matsumoto M, Suzuki K, Konno Y, Sakuma J, Endo Y, Oinuma M (2007) Blood flow disturbance in perforating arteries attributable to aneurysm surgery. J Neurosurg 107:60–67.  https://doi.org/10.3171/JNS-07/07/0060 CrossRefPubMedGoogle Scholar
  31. 31.
    Soeda A, Sakai N, Murao K, Sakai H, Ihara K, Yamada N, Imakita S, Nagata I (2003) Thromboembolic events associated with Guglielmi detachable coil embolization with use of diffusion-weighted MR imaging. Part II. Detection of the microemboli proximal to cerebral aneurysm. AJNR Am J Neuroradiol 24:2035–2038PubMedGoogle Scholar
  32. 32.
    Soeda A, Sakai N, Sakai H, Iihara K, Yamada N, Imakita S, Nagata I (2003) Thromboembolic events associated with Guglielmi detachable coil embolization of asymptomatic cerebral aneurysms: evaluation of 66 consecutive cases with use of diffusion-weighted MR imaging. AJNR Am J Neuroradiol 24:127–132PubMedGoogle Scholar
  33. 33.
    Strandgaard S (1976) Autoregulation of cerebral blood flow in hypertensive patients. The modifying influence of prolonged antihypertensive treatment on the tolerance to acute, drug-induced hypotension. Circulation 53:720–727CrossRefPubMedGoogle Scholar
  34. 34.
    Suzuki M, Yoneda H, Ishihara H, Shirao S, Nomura S, Koizumi H, Suehiro E, Goto H, Sadahiro H, Maruta Y, Inoue T, Oka F (2015) Adverse events after unruptured cerebral aneurysm treatment: a single-center experience with clipping/coil embolization combined units. J Stroke Cerebrovasc Dis: Off J Nat Stroke Assoc 24:223–231.  https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.08.018 CrossRefGoogle Scholar
  35. 35.
    Tatemichi TK, Steinke W, Duncan C, Bello JA, Odel JG, Behrens MM, Hilal SK, Mohr JP (1992) Paramedian thalamopeduncular infarction: clinical syndromes and magnetic resonance imaging. Ann Neurol 32:162–171.  https://doi.org/10.1002/ana.410320207 CrossRefPubMedGoogle Scholar
  36. 36.
    Tatu L, Moulin T, Bogousslavsky J, Duvernoy H (1996) Arterial territories of human brain: brainstem and cerebellum. Neurology 47:1125–1135CrossRefPubMedGoogle Scholar
  37. 37.
    Tatu L, Moulin T, Bogousslavsky J, Duvernoy H (1998) Arterial territories of the human brain: cerebral hemispheres. Neurology 50:1699–1708CrossRefPubMedGoogle Scholar
  38. 38.
    Thome C, Vajkoczy P, Horn P, Bauhuf C, Hubner U, Schmiedek P (2001) Continuous monitoring of regional cerebral blood flow during temporary arterial occlusion in aneurysm surgery. J Neurosurg 95:402–411.  https://doi.org/10.3171/jns.2001.95.3.0402 CrossRefPubMedGoogle Scholar
  39. 39.
    Tsutsumi K, Ueki K, Morita A, Usui M, Kirino T (2001) Risk of aneurysm recurrence in patients with clipped cerebral aneurysms: results of long-term follow-up angiography. Stroke 32:1191–1194CrossRefPubMedGoogle Scholar
  40. 40.
    Vermeer SE, Longstreth WT, Koudstaal PJ (2007) Silent brain infarcts: a systematic review. Lancet Neurol 6:611–619.  https://doi.org/10.1016/s1474-4422(07)70170-9 CrossRefPubMedGoogle Scholar
  41. 41.
    Vermeer SE, Prins ND, den Heijer T, Hofman A, Koudstaal PJ, Breteler MM (2003) Silent brain infarcts and the risk of dementia and cognitive decline. N Engl J Med 348:1215–1222.  https://doi.org/10.1056/NEJMoa022066 CrossRefPubMedGoogle Scholar
  42. 42.
    Vlak MH, Algra A, Brandenburg R, Rinkel GJ (2011) Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis. Lancet Neurol 10:626–636.  https://doi.org/10.1016/S1474-4422(11)70109-0 CrossRefPubMedGoogle Scholar
  43. 43.
    Wiebers DO, Whisnant JP, Huston J 3rd, Meissner I, Brown RD Jr, Piepgras DG, Forbes GS, Thielen K, Nichols D, O'Fallon WM, Peacock J, Jaeger L, Kassell NF, Kongable-Beckman GL, Torner JC, International Study of Unruptured Intracranial Aneurysms I (2003) Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:103–110CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Department of Neurosurgery, Beijing Tiantan HospitalCapital Medical UniversityBeijingPeople’s Republic of China
  2. 2.China National Clinical Research Center for Neurological DiseasesBeijingPeople’s Republic of China
  3. 3.Center of StrokeBeijing Institute for Brain DisordersBeijingPeople’s Republic of China
  4. 4.Beijing Key Laboratory of Translational Medicine for Cerebrovascular DiseasesBeijingPeople’s Republic of China

Personalised recommendations