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Incidence rate and predictors of recurrent aneurysms after clipping: long-term follow-up study of survivors of subarachnoid hemorrhage

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Abstract

Recurrent aneurysms are a major cause of re-aneurysmal subarachnoid hemorrhage (aSAH), but information on long-term clip durability and predictors is insufficient. This study aimed to present the incidence rate of > 10 years and investigate predictors of a recurrent aneurysm in aSAH survivors. We included 1601 patients admitted with aSAH and treated by microsurgical clipping between January 1993 and May 2010. Of these patients, 435 aSAH survivors were included in this study (27.2%). The total follow-up time was 5680.9 patient-years, and the overall incidence rate was 0.77% per patient-year. The cumulative probability of recurrence without residua and regrowth of the neck remnant was 0.7% and 13.9% at 10 years, respectively. Neck remnant (hazard ratio [HR], 10.311; 95% confidence interval [CI], 5.233–20.313) and alcohol consumption over the moderate amount (HR, 3.166; 95% CI, 1.313–7.637) were independent risk factors of recurrent aneurysm. Current smoking and multiplicity at initial aSAH presentation were significant factors in a univariate analysis. Furthermore, de novo intracranial aneurysms (DNIAs) were more common in the recurrent group than in the non-recurrent group (40.9% vs. 11.5%, P < 0.001). In the present study, we noted the long-term clip durability and predictor of recurrence after microsurgical clipping. These findings can assist clinicians in identifying patients at a high risk of recurrent aneurysm and recommending selective long-term surveillance after microsurgical clipping.

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References

  1. Alg VS, Sofat R, Houlden H, Werring DJ (2013) Genetic risk factors for intracranial aneurysms: a meta-analysis in more than 116,000 individuals. Neurology 80:2154–2165. https://doi.org/10.1212/WNL.0b013e318295d751

    Article  PubMed  PubMed Central  Google Scholar 

  2. Andreasen TH, Bartek J Jr, Andresen M, Springborg JB, Romner B (2013) Modifiable risk factors for aneurysmal subarachnoid hemorrhage. Stroke 44:3607–3612. https://doi.org/10.1161/STROKEAHA.113.001575

    Article  PubMed  Google Scholar 

  3. Arnett DK, Blumenthal RS, Albert MA, Buroker AB, Goldberger ZD, Hahn EJ, Himmelfarb CD, Khera A, Lloyd-Jones D, McEvoy JW, Michos ED, Miedema MD, Munoz D, Smith SC Jr, Virani SS, Williams KA Sr, Yeboah J, Ziaeian B (2019) 2019 ACC/AHA guideline on the primary prevention of cardiovascular disease: a report of the American College of Cardiology/American Heart Association Task Force on clinical practice guidelines. J Am Coll Cardiol 74:e177–e232. https://doi.org/10.1016/j.jacc.2019.03.010

    Article  PubMed  PubMed Central  Google Scholar 

  4. Brown MA, Parish J, Guandique CF, Payner TD, Horner T, Leipzig T, Rupani KV, Kim R, Bohnstedt BN, Cohen-Gadol AA (2017) A long-term study of durability and risk factors for aneurysm recurrence after microsurgical clip ligation. J Neurosurg 126:819–824. https://doi.org/10.3171/2016.2.JNS152059

    Article  PubMed  Google Scholar 

  5. Burkhardt JK, Chua MHJ, Weiss M, Do ASS, Winkler EA, Lawton MT (2017) Risk of aneurysm residual regrowth, recurrence, and de novo aneurysm formation after microsurgical clip occlusion based on follow-up with catheter angiography. World Neurosurg 106:74–84. https://doi.org/10.1016/j.wneu.2017.06.110

    Article  PubMed  Google Scholar 

  6. Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, Yarnold JA, Rischmiller J, Byrne JV (2007) Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke 38:1538–1544. https://doi.org/10.1161/STROKEAHA.106.466987

    Article  PubMed  Google Scholar 

  7. Chalouhi N, Bovenzi CD, Thakkar V, Dressler J, Jabbour P, Starke RM, Teufack S, Gonzalez LF, Dalyai R, Dumont AS, Rosenwasser R, Tjoumakaris S (2014) Long-term catheter angiography after aneurysm coil therapy: results of 209 patients and predictors of delayed recurrence and retreatment. J Neurosurg 121:1102–1106. https://doi.org/10.3171/2014.7.JNS132433

    Article  PubMed  Google Scholar 

  8. Chalouhi N, Hoh BL, Hasan D (2013) Review of cerebral aneurysm formation, growth, and rupture. Stroke 44:3613–3622. https://doi.org/10.1161/STROKEAHA.113.002390

    Article  PubMed  Google Scholar 

  9. Dandy WE (1938) Intracranial aneurysm of the internal carotid artery: cured by operation. Ann Surg 107:654–659. https://doi.org/10.1097/00000658-193805000-00003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. David CA, Vishteh AG, Spetzler RF, Lemole M, Lawton MT, Partovi S (1999) Late angiographic follow-up review of surgically treated aneurysms. J Neurosurg 91:396–401. https://doi.org/10.3171/jns.1999.91.3.0396

    Article  CAS  PubMed  Google Scholar 

  11. el-Beltagy M, Muroi C, Roth P, Fandino J, Imhof HG, Yonekawa Y, (2010) Recurrent intracranial aneurysms after successful neck clipping. World Neurosurg 74:472–477. https://doi.org/10.1016/j.wneu.2010.06.036

    Article  Google Scholar 

  12. Ferns SP, Sprengers ME, van Rooij WJ, van den Berg R, Velthuis BK, de Kort GA, Sluzewski M, van Zwam WH, Rinkel GJ, Majoie CB (2011) De novo aneurysm formation and growth of untreated aneurysms: a 5-year MRA follow-up in a large cohort of patients with coiled aneurysms and review of the literature. Stroke 42:313–318. https://doi.org/10.1161/STROKEAHA.110.591594

    Article  PubMed  Google Scholar 

  13. Futchko J, Starr J, Lau D, Leach MR, Roark C, Pandey AS, Thompson BG (2018) Influence of smoking on aneurysm recurrence after endovascular treatment of cerebrovascular aneurysms. J Neurosurg 128:992–998. https://doi.org/10.3171/2016.12.JNS161625

    Article  PubMed  Google Scholar 

  14. Gholampour S, Mehrjoo S (2021) Effect of bifurcation in the hemodynamic changes and rupture risk of small intracranial aneurysm. Neurosurg Rev 44:1703–1712. https://doi.org/10.1007/s10143-020-01367-3

    Article  PubMed  Google Scholar 

  15. Hu S, Yu N, Li Y, Hao Z, Liu Z, Li MH (2019) A meta-analysis of risk factors for the formation of de novo intracranial aneurysms. Neurosurgery 85:454–465. https://doi.org/10.1093/neuros/nyy332

    Article  PubMed  Google Scholar 

  16. Jabbarli R, Pierscianek D, Wrede K, Dammann P, Schlamann M, Forsting M, Muller O, Sure U (2016) Aneurysm remnant after clipping: the risks and consequences. J Neurosurg 125:1249–1255. https://doi.org/10.3171/2015.10.JNS151536

    Article  PubMed  Google Scholar 

  17. Johnston SC, Dowd CF, Higashida RT, Lawton MT, Duckwiler GR, Gress DR, Investigators C (2008) Predictors of rehemorrhage after treatment of ruptured intracranial aneurysms: the Cerebral Aneurysm Rerupture After Treatment (CARAT) study. Stroke 39:120–125. https://doi.org/10.1161/STROKEAHA.107.495747

    Article  PubMed  Google Scholar 

  18. Kang HS, Han MH, Kwon BJ, Jung SI, Oh CW, Han DH, Chang KH (2004) Postoperative 3D angiography in intracranial aneurysms. AJNR Am J Neuroradiol 25:1463–1469

    PubMed  PubMed Central  Google Scholar 

  19. Killer-Oberpfalzer M, Aichholzer M, Weis S, Richling B, Jones R, Virmani R, Cruise GM (2012) Histological analysis of clipped human intracranial aneurysms and parent arteries with short-term follow-up. Cardiovasc Pathol 21:299–306. https://doi.org/10.1016/j.carpath.2011.09.010

    Article  PubMed  Google Scholar 

  20. Kim JJ, Cho KC, Suh SH, Chung J, Jang CK, Joo JY, Kim YB (2020) Evaluation of the angiographic outcomes after clipping of intracranial aneurysms: determination of predisposing factors for occurrence of aneurysm remnants. Neurol Res 42:354–360. https://doi.org/10.1080/01616412.2020.1732594

    Article  PubMed  Google Scholar 

  21. Marbacher S, Niemela M, Hernesniemi J, Frosen J (2019) Recurrence of endovascularly and microsurgically treated intracranial aneurysms-review of the putative role of aneurysm wall biology. Neurosurg Rev 42:49–58. https://doi.org/10.1007/s10143-017-0892-2

    Article  PubMed  Google Scholar 

  22. Mascitelli JR, Cole T, Yoon S, Nakaji P, Albuquerque FC, McDougall CG, Zabramski JM, Lawton MT, Spetzler RF (2020) External validation of the Subarachnoid Hemorrhage International Trialists (SAHIT) predictive model using the Barrow Ruptured Aneurysm Trial (BRAT) cohort. Neurosurgery 86:101–106. https://doi.org/10.1093/neuros/nyy600

    Article  PubMed  Google Scholar 

  23. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, Sandercock P, International Subarachnoid Aneurysm Trial Collaborative G (2005) International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 366:809-817. https://doi.org/10.1016/S0140-6736(05)67214-5

  24. Nakase H, Kamada Y, Aoki H, Goda K, Morimoto T, Sakaki T (2000) Clinical study on recurrent intracranial aneurysms. Cerebrovasc Dis 10:255–260. https://doi.org/10.1159/000016067

    Article  CAS  PubMed  Google Scholar 

  25. National Institute on Alcohol Abuse and Alcoholism (NIAAA) (2016) Drinking levels defined. https://www.niaaa.nih.gov/alcohol-health/overview-alcohol-consumption/moderate-binge-drinking. Accessed 2 Jan 2022

  26. Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, Lamoureux J, Chagnon M, Roy D (2003) Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke 34:1398–1403. https://doi.org/10.1161/01.STR.0000073841.88563.E9

    Article  PubMed  Google Scholar 

  27. Rinkel GJ, Algra A (2011) Long-term outcomes of patients with aneurysmal subarachnoid haemorrhage. Lancet Neurol 10:349–356. https://doi.org/10.1016/S1474-4422(11)70017-5

    Article  PubMed  Google Scholar 

  28. Schievink WI, Prakash UB, Piepgras DG, Mokri B (1994) Alpha 1-antitrypsin deficiency in intracranial aneurysms and cervical artery dissection. Lancet 343:452–453. https://doi.org/10.1016/s0140-6736(94)92693-x

    Article  CAS  PubMed  Google Scholar 

  29. Spetzler RF, McDougall CG, Zabramski JM, Albuquerque FC, Hills NK, Nakaji P, Karis JP, Wallace RC (2019) Ten-year analysis of saccular aneurysms in the Barrow Ruptured Aneurysm Trial. J Neurosurg 132:771–776. https://doi.org/10.3171/2018.8.JNS181846

    Article  PubMed  Google Scholar 

  30. Spiessberger A, Vogt DR, Fandino J, Marbacher S (2019) Formation of intracranial de novo aneurysms and recurrence after neck clipping: a systematic review and meta-analysis. J Neurosurg 132:456–464. https://doi.org/10.3171/2018.10.JNS181281

    Article  PubMed  Google Scholar 

  31. Sprengers ME, van Rooij WJ, Sluzewski M, Rinkel GJ, Velthuis BK, de Kort GA, Majoie CB (2009) MR angiography follow-up 5 years after coiling: frequency of new aneurysms and enlargement of untreated aneurysms. AJNR Am J Neuroradiol 30:303–307. https://doi.org/10.3174/ajnr.A1353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Texakalidis P, Sweid A, Mouchtouris N, Peterson EC, Sioka C, Rangel-Castilla L, Reavey-Cantwell J, Jabbour P (2019) Aneurysm formation, growth, and rupture: the biology and physics of cerebral aneurysms. World Neurosurg 130:277–284. https://doi.org/10.1016/j.wneu.2019.07.093

    Article  PubMed  Google Scholar 

  33. 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 32:1191–1194. https://doi.org/10.1161/01.str.32.5.1191

    Article  CAS  PubMed  Google Scholar 

  34. Wang JY, Smith R, Ye X, Yang W, Caplan JM, Radvany MG, Colby GP, Coon AL, Tamargo RJ, Huang J (2015) Serial imaging surveillance for patients with a history of intracranial aneurysm: risk of de novo aneurysm formation. Neurosurgery 77:32–42; discussion 42–33. https://doi.org/10.1227/NEU.0000000000000730

  35. Wermer MJ, Greebe P, Algra A, Rinkel GJ (2005) Incidence of recurrent subarachnoid hemorrhage after clipping for ruptured intracranial aneurysms. Stroke 36:2394–2399. https://doi.org/10.1161/01.STR.0000185686.28035.d2

    Article  PubMed  Google Scholar 

  36. Wermer MJ, Rinkel GJ, Greebe P, Albrecht KW, Dirven CM, Tulleken CA (2005) Late recurrence of subarachnoid hemorrhage after treatment for ruptured aneurysms: patient characteristics and outcomes. Neurosurgery 56:197–204; discussion 197–204. https://doi.org/10.1227/01.neu.0000148894.32031.39

  37. Wermer MJ, van der Schaaf IC, Velthuis BK, Algra A, Buskens E, Rinkel GJ, Group AS (2005) Follow-up screening after subarachnoid haemorrhage: frequency and determinants of new aneurysms and enlargement of existing aneurysms. Brain 128:2421-2429. https://doi.org/10.1093/brain/awh587

  38. Yang ZL, Ni QQ, Schoepf UJ, De Cecco CN, Lin H, Duguay TM, Zhou CS, Zhao YE, Lu GM, Zhang LJ (2017) Small intracranial aneurysms: diagnostic accuracy of CT angiography. Radiology 285:941–952. https://doi.org/10.1148/radiol.2017162290

    Article  PubMed  Google Scholar 

  39. Yu LB, Fang ZJ, Yang XJ, Zhang D (2019) Management of residual and recurrent aneurysms after clipping or coiling: clinical characteristics, treatments, and follow-up outcomes. World Neurosurg 122:e838–e846. https://doi.org/10.1016/j.wneu.2018.10.160

    Article  PubMed  Google Scholar 

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Funding

This study was supported by a faculty research grant of the Yonsei University College of Medicine (6–2019-0066).

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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by HJH, WL, and JK. The first draft of the manuscript was written by HJH, and all authors commented on previous versions of the manuscript. All authors have read and approved the final manuscript.

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Correspondence to Yong Bae Kim.

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This study was approved by the Institutional Review Board of Yonsei University (IRB number: 4–2020-1336).

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Han, H.J., Lee, W., Kim, J. et al. Incidence rate and predictors of recurrent aneurysms after clipping: long-term follow-up study of survivors of subarachnoid hemorrhage. Neurosurg Rev 45, 3209–3217 (2022). https://doi.org/10.1007/s10143-022-01828-x

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