Subarachnoid hemorrhage due to rupture of very small aneurysms of the anterior part of the circle of Willis

Objective: To assess the frequency of ruptures of very small cerebral aneurysms, features of the perioperative period and outcomes, in comparison with the rupture of ordinarily sized aneurysms.

Material and methods: A comparative analysis of the group of patients with ruptured cerebral miliary aneurysms (n = 18) and the group of patients with ruptured cerebral aneurysms of regular size (n = 308) was carried out. All patients underwent open surgery in the first 3 days after the rupture (osteoplastic craniotomy, microsurgical aneurysm clipping). We compared gender, age of patients, severity of the patient’s condition at the moment of admission, severity of subarachnoid hemorrhage, location of aneurysms, aspect ratio, duration of the operation, frequency of intraoperative ruptures, postoperative mortality.

Results: It was found that miliary aneurysm rupture occurs in 5.5% of all patients with cerebral aneurysm rupture. The most common cases of rupture of very small aneurysms were in women (77.7%), with a mean age of 50.8 years. Aneurysms of the anterior communicating artery (66.6%) with a narrow neck (average aspect ratio – 2.1) were the most common. Patients with rupture of very small aneurysms were 7.9% more likely to be admitted in a state of subcompensation or decompensation (Hunt-Hess IV–V), they had massive subarachnoid hemorrhage (Fisher III) 19.6% more often than with ruptured aneurysms of regular size. On average, operations in cases of very small aneurysms lasted 30 minutes less than clipping of ordinary aneurysms, but were complicated by intraoperative rupture twice as often (38.8% and 16.5%, respectively). Postoperative mortality in the group of patients with ruptured miliary aneurysms was 5.7% higher than in patients with ruptured aneurysms of regular size.

Conclusion: Rupture of cerebral miliary aneurysms is relatively rare. Women of 50–60 years old with very small aneurysms of the anterior communicating artery with a narrow neck constitute the main group of such patients. Massive subarachnoid hemorrhage and severe condition of patients on admission are more common with miliary aneurysms than with ordinarily sized aneurysms. The small size of the aneurysm and the work near the rupture determine the more frequent contact intraoperative rupture when the neck is exposed as compared to operations on larger aneurysms, which negatively affects the treatment outcomes in this group of patients.

1. Krylov VV, Godkov IM, Dmitriev AYu. Intraoperative risk factors in the surgery of cerebral aneurysms. Materials of the city scientific and practical conference. Moscow: N.V. Sklifosovsky Research Institute for Emergency Medicine; 2007;200:16–22. (In Russ.).

2. Zyablova EI, Tkachev VV, Porhanov VA. CT angiography for detecting the cause of intracranial hemorrhage in the emergency department. Innovative Medicine of Kuban. 2021;1:34–38. (In Russ.). https://doi.org/10.35401/2500-0268-2021-21-1-34-38

3. Krylov VV. Surgery of brain aneurysms in 3 volumes. Moscow; 2011. (In Russ.).

4. Lazarev VA, Piradov AN, et al. Recommendation protocol for the management of patients with subarachnoid hemorrhage due to rupture of cerebral aneurysms. Problems of neurosurgery named after N.N. Burdenko. 2006;13(3):3–10. (In Russ.).

5. Tkachev VV, Muzlaev GG, Porkhanov VA. Microsurgery of cerebral aneurysms. Experience of regional healthcare. Saint-Petersburg; 2019:189. (In Russ.).

6. Wiebers DO, Whisnant JP, Huston J, et al. Unruptured intra-cranial aneurysms risk of rupture and risks of surgical intervention. N Engl J Med. 1998;339:1725–1733. PMID: 9867550. https://doi.org/10.1056/NEJM199812103392401

7. Donnan GA, Davis SM. Patients with small, asymptomatic, unruptured intracranial aneurysms and no history of subarachnoid hemorrhage should be treated conservatively. Stroke. 2005;36(2):410–411. PMID: 15618442. https://doi.org/10.1161/01.STR.0000152272.34969.80

8. Murayama Y, Takao H, Ishibashi T, et al. Risk analysis of unruptured intracranial aneurysms: prospective 10-year cohort study. Stroke. 2016;47:365–371. PMID: 26742803. https://doi.org/10.1161/STROKEAHA.115.010698

9. Bruneau M, Amin-Hanjani S, Koroknay-Pal P, et al. Surgical clipping of very small unruptured intracranial aneurysms: a multi-center international study. Neurosurgery. 2016;78(1):47–52. PMID: 26317673. https://doi.org/10.1227/NEU.0000000000000991

10. Carter BS, Sheth S, Chang E, et al. Epidemiology of the size distribution of intracranial bifurcation aneurysms: smaller size of distal aneurysms and increasing size of unruptured aneurysms with age. Neurosurgery. 2006;58(2):217–223. PMID: 16462474. https://doi.org/10.1227/01.NEU.0000194639.37803.F8

11. Chalouhi N, Penn DL, Tjoumakaris S, et al. Treatment of small ruptured intracranial aneurysms: Comparison of surgical and endovascular options. J Am Heart Assoc. 2012;1(4):1–8. PMID: 23130171. PMCID: PMC3487356. https://doi.org/10.1161/JAHA.112.002865

12. Dolati P, Pittman D, Morrish WF. The frequency of subarachnoid hemorrhage from very small cerebral aneurysms (< 5 mm): a population-based study. Cureus. 2015;7(6):279–283. PMID: 26180703. PMCID: PMC4494560. https://doi.org/10.7759/cureus.279

13. Figueredo LF, Pedraza-Ciro MС, Lopez-McCormick JS, et al. Aneurysmal subarachnoid hemorrhage associated with small aneurysms in smokers and women: a retrospective analysis. World Neurosurg. 2019;4:101–106. PMID: 31360917. PMCID: PMC6610703. https://doi.org/10.1016/j.wnsx.2019.100038

14. Kashiwazaki D, Kuroda S, et al. Size ratio can highly predict rupture risk in intracranial small (< 5 mm) aneurysms. Stroke. 2013;44(8):2169–2173. PMID: 23743979. https://doi.org/10.1161/STROKEAHA.113.001138

15. Miyazaki Y, Ando Е. On the military intracranial aneurysm its significance in subarachnoid hemorrhage. No Shinkei Geka. 1976;4(9):853–860. PMID: 988491.

16. Tai J, Liu J, Lv J, et al. Risk factors predicting a higher grade of subarachnoid haemorrhage in small ruptured intracranial aneurysm (< 5 mm). Neurol Neurochir Pol. 2019;53:296–303. PMID: 31397878. https://doi.org/10.5603/PJNNS.a2019.0029

17. Taylor CL, Steele D, Kopitnik TA, et al. Outcome after subarachnoid hemorrhage from a very small aneurysm: a case-control series. J Neurosurg. 2004;100:623–625. PMID: 15070115. https://doi.org/10.3171/jns.2004.100.4.0623

18. Rahman M, Smietana J, Hauck E, et al. Size ratio correlates with intracranial aneurysm rupture status: a prospective study. Stroke. 2010;41:916–920. PMID: 20378866. https://doi.org/10.1161/STROKEAHA.109.574244

19. Weir B, Amidei C, Kongable G, et al. The aspect ratio (dome/neck) of ruptured and unruptured aneurysms. J Neurosurg. 2003;99(3):447–451 PMID: 12959428. https://doi.org/10.3171/jns.2003.99.3.0447

20. Bender MT, Wendt H, Monarch T, et al. Small aneurysms account for the majority and increasing percentage of aneurysmal subarachnoid hemorrhage: a 25-year, single institution study. Neurosurgery. 2018;83:692–699. PMID: 29029314. https://doi.org/10.1093/neuros/nyx484

21. Qiu T, Jin G, Xing H, et al. Association between hemodynamics, morphology, and rupture risk of intracranial aneurysms: a computational fluid modeling study. Neurol Sci. 2017;38:1009–1018. PMID: 28285454. PMCID: PMC5486504. https://doi.org/10.1007/s10072-017-2904-y

22. Nahed BV, DiLuna ML, Morgan T, et al. Hypertension, age, and location predict rupture of small intracranial aneurysms. Neurosurgery. 2005;57(4):676–683. PMID: 16239879.

23. Orz Y, Kobayashi S, Osawa M, et al. Aneurysm size: a prognostic factor for rupture. Br J Neurosurg. 1997;11:144–149. PMID: 9156002. https://doi.org/10.1080/02688699746500

24. Wong GKC, Teoh J, Chan EKY, et al. Intracranial aneurysm size responsible for spontaneous subarachnoid haemorrhage. Br J Neurosurg. 2013;27(1):34–39. PMID: 22905889. https://doi.org/10.3109/02688697.2012.70955925.

25. Duan Z, Li Y, Guan S, et al. Morphological parameters and anatomical locations associated with rupture status of small intracranial aneurysms. Sci Rep. 2018;8:644–652. PMID: 29691446. PMCID: PMC5915554. https://doi.org/10.1038/s41598-018-24732-1

26. Yonekura M. Small unruptured aneurysm verification (SUAVe Study, Japan) – interim report. Neurol Med Chir (Tokyo). 2004;44(4):213–214. PMID: 15185763. https://doi.org/10.2176/nmc.44.213

27. Yang ZL, Ni QQ, Schoepf UJ, et al. Small Intracranial Aneurysms: Diagnostic Accuracy of CT Angiography. Radiology. 2017;285(3):941–952. PMID: 28654338. https://doi.org/10.1148/radiol.2017162290

28. Salary M, Quigley MR, Wilberger JE, et al. Relation among aneurysm size, amount of subarachnoid blood, and clinical outcome. J Neurosurg. 2007;107:13–17. PMID: 17639867. https://doi.org/10.3171/JNS-07/07/0013

29. Nguyen TN, Raymond J, Guilbert F, et al. Association of endovascular therapy of very small ruptured aneurysms with higher rates of procedure-related rupture. J Neurosurg. 2008;108:1088–1092. PMID: 18518708. https://doi.org/10.3171/JNS/2008/108/6/1088

30. Zhang Y, Zhang Y, Guo F, et al. Treatment of small and tiny aneurysms before and after flow diversion era: a single center experience of 409 aneurysms. World Neurosurg. 2018;116:386–393. PMID: 29751179. https://doi.org/10.1016/j.wneu.2018.04.213