Results of microsurgical treatment of paraclinoid aneurysms in acute period of rupture

INTRODUCTION. Paraclinoid aneurysms (PA) account for 5.4 % of all intracranial aneurysms, 49% of these cases are large or giant. The hospital mortality rate of patients who have undergone aneurysm rupture is 27–67 %. More than half of the survivors have persistent neurological deficits and a decreased quality of life.

AIM. To evaluate the immediate and long-term results of microsurgical treatment of PA in the acute period of subarachnoid hemorrhage (SAH).

MATERIALS AND METHODS. We analyzed the results of clinical examination, microsurgical treatment, and outcomes of 75 patients with paraclinoid aneurysms who were in the Department of Neurosurgery of the Moscow Regional Research and Clinical Institute for the period from June 2019 to November 2023. A preoperative clinical and neurological assessment of the patients’ condition was performed, and the Glasgow Coma Scale (GCS) and the Hunt-Hess scale were used. All patients underwent brain CT and CT angiography. The size of aneurysms, the presence of hydrocephalus, intracerebral and subdural hematomas, ventricular hemorrhages, and dislocations of median structures were assessed. The following evaluation scales were used: Fisher, Hijdra, and Graeb. All patients underwent microsurgical intervention—the clipping of aneurysms in the acute period of SAH. Immediate and long-term treatment outcomes were assessed using the modified Glasgow Outcome Scale (mGOS) and the modified Rankin Scale (mRS).

RESULTS. The majority of patients underwent surgery through traditional approaches: pterional (n=36, 48.0 %) and lateral supraorbital (n=17, 22.7 %). Anterior clinoidectomy (AC) was performed in 62 (82.7 %) cases. In 9 (12.0%) cases the cervical segment of the ICA was exposed, and retrograde suction decompression of the aneurysm was performed. The majority of patients had good and satisfactory immediate and long-term treatment outcomes.

CONCLUSION. Microsurgical clipping is an effective and safe method of treating PA in the acute period of hemorrhage. Individual approach, experience, and proficiency in various «skull base» surgery techniques make it possible to achieve a good long-term outcome in most patients with a minimum number of postoperative complications. The assessment of immediate treatment outcomes in patients with PA is an important prognostic factor determining long-term treatment outcomes. When comparing immediate and long-term results, there is a tendency to increase the proportion of good outcomes in the group of patients with satisfactory outcomes at the time of discharge.

1. Nutik S. Carotid paraclinoid aneurysms with intradural origin and intracavernous location. Journal of neurosurgery. 1978;48(4):526–533. Doi: 10.3171/JNS.1978.48.4.0526.

2. Javalkar V., Banerjee A. D., Nanda A. Paraclinoid carotid aneurysms. Journal of Clinical Neuroscience 2011;18(1):13–22. Doi: 10.1016/j.jocn.2010.06.020.

3. Heros R. C., Nelson P. B., Ojemann R. G., Crowell R. M., DeBrun G. Large and giant paraclinoid aneurysms: surgical techniques, complications, and results. Neurosurgery. 1983;12(2):153–163. Doi: 10.1227/00006123-198302000-00004.

4. Raper D. M. S., Ding D., Peterson E. C., Crowley R. W., Liu K. C., Chalouhi N., Hasan D. M., Dumont A. S., Jabbour P., Starke R. M. Cavernous carotid aneurysms: a new treatment paradigm in the era of flow diversion. Expert review of neurotherapeutics. 2017;17(2):155–163. Doi: 10.1080/14737175.2016.1212661.

5. Abdulateef A. A., Morita S., Ismail M., Sharma M., Hoz S. S., Numazawa S., Ito Y., Watanabe S., Mori K. Supraorbital keyhole approach for paraclinoid aneurysms clipping: A case series with literature review. Surgical neurology international. 2023;(14). Doi: 10.25259/SNI_251_2023.

6. Fulkerson D. H., Horner T. C., Payner T. D., Leipzig T. J., Scott J. A., Denardo A. J., Redelman K., Goodman J. M. Results, outcomes, and follow-up of remnants in the treatment of ophthalmic aneurysms: a 16-year experience of a combined neurosurgical and endovascular team. Neurosurgery. 2009;64(2):218–229. Doi: 10.1227/01.NEU.0000337127.73667.80.

7. Flores B. C., White J. A., Hunt Batjer H., Samson D. S. The 25th anniversary of the retrograde suction decompression technique (Dallas technique) for the surgical management of paraclinoid aneurysms: Historical background, systematic review, and pooled analysis of the literature. Journal of Neurosurgery. 2019;130(3):902–916. Doi: 10.3171/2017.11.JNS17546.

8. Shekhtman O. D., Éliava Sh. Sh., Yakovlev S. B., Pilipenko Iu. V., Konovalov An. N. The modern role of microsurgery in treatment of large and giant aneurysms of the internal carotid artery. Voprosy Neirokhirurgii: Zhurnal Imeni N. N. Burdenko. 2016;80(5):51–61. (In Russ.). Doi: 10.17116/neiro201680551-61. EDN: WZSVUX.

9. Bederson J. B., Connolly E. S., Batjer H. H., Dacey R. G., Dion J. E., Diringer M. N., Duldner J. E., Harbaugh R. E., Patel A. B., Rosenwasser R. H. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke. 2009;40(3):994–1025. Doi: 10.1161/STROKEAHA.108.191395.

10. Juvela S. Natural history of unruptured intracranial aneurysms: risks for aneurysm formation, growth, and rupture. Acta neurochirurgica. Supplement. 2002;82(82):27– 30. Doi: 10.1007/978-3-7091-6736-6_5.

11. Inagawa T., Hirano A. Autopsy study of unruptured incidental intracranial aneurysms. Surgical neurology. 1990;34(6):361–365. Doi: 10.1016/0090-3019(90)90237-J.

12. Steiner T., Juvela S., Unterberg A., Jung C., Forsting M., Rinkel G. European Stroke Organization guidelines for the management of intracranial aneurysms and subarachnoid haemorrhage. Cerebrovascular diseases (Basel, Switzerland). 2013;35(2):93–112. Doi: 10.1159/000346087.

13. Krylov V.V. Mikrokhirurgiya anevrizm sosudov golovnogo mozga. Moscow: ABV-press; 2022. 856 p. (In Russ.). EDN: IVKOCL.

14. Suarez J. I., Tarr R. W., Selman W. R. Aneurysmal subarachnoid hemorrhage. The New England journal of medicine. 2006;354(4):387–396. Doi: 10.1056/NEJMRA052732.

15. Krylov V. V., Shatokhin T. A., Shetova I. M., Eliava Sh. Sh., Belousova O. B., Airapetyan A. A., Alekseev A. G., Asratyan S. A., Bakharev E. Yu., Vorobyov I. A., Dedkov D. S., Dubovoy A. V., Eliseev V. V., Elfimov A. V., Kozhaev Z. U., Kolotvinov V. S., Kosmachev M. V., Kravets L. Ya., Kushniruk P. I., Myachin N. L., Parfenov V. E., Rodionov S. V., Semin P. A., Khasanshin E. M., Shnyakin P. G., Yakhontov I. S. Russian study on brain aneurysm surgery: a continuation (RIHA II). Burdenko’s Journal of Neurosurgery. 2024;88(1):7–20. (In Russ.). Doi: 10.17116/neiro201680551-61. EDN: QITDXY

16. Lawton M. T., Vates G. E. Subarachnoid Hemorrhage. The New England journal of medicine. 2017;377(3):257–266. Doi: 10.1056/NEJMCP1605827.

17. Taufique Z., May T., Meyers E., Falo C., Mayer S.A., Agarwal S., Park S., Connolly E. S., Claassen J., Schmidt J. M. Predictors of Poor Quality of Life 1 Year After Subarachnoid Hemorrhage. Neurosurgery. 2016;78(2):256–263. Doi: 10.1227/NEU.0000000000001042.

18. Sun Y., Wan B., Li Q., Li T., Huang G., Zhang W., Yang J., Tong X. Endovascular Treatment for Cavernous Carotid Aneurysms: A Systematic Review and Meta-Analysis. Journal of stroke and cerebrovascular diseases. The official journal of National Stroke Association. 2020;29(6). Doi: 10.1016/J.JSTROKECEREBROVASDIS.2020.104808.

19. Fang S., Lanzino G. Paraclinoid aneurysms: is there a new endovascular standard?. Neurological research. 2014;36(4):314–322. Doi: 10.1179/1743132814Y.0000000326.

20. Wang Y., Yu J. Endovascular treatment of aneurysms of the paraophthalmic segment of the internal carotid artery: Current status. Frontiers in neurology. 2022;(13). Doi: 10.3389/FNEUR.2022.913704.

21. Yakovlev S. B., Arustamyan S. R., Dorokhov P. S., Bocharov A. V., Bukharin E. Y., Arkhangel’skaya Y. N., Aref’eva I. A. Endovascular treatment of large and giant intracranial aneurysms using flow-diverting stents. Voprosy Neirokhirurgii: Zhurnal Imeni N. N. Burdenko. 2015;79(4):19–27. (In Russ.). Doi: 10.17116/neiro201579419-27. EDN: UIKOEX.

22. Arustamyan S. R., Yakovlev S. B., Bocharov A. V., Bukharin E. Y., Dorokhov P. S., Mikeladze K. G., Belousova O. B. Endovascular treatment of large and giant intracranial aneurysms using stent assistance. Voprosy Neirokhirurgii: Zhurnal Imeni N. N. Burdenko. 2015;79(4):28–37. (In Russ.). Doi: 10.17116/neiro201579428-37. EDN: UIKOFH.

23. Lindgren A., Vergouwen M. Di, van der Schaaf I., Algra A., Wermer M., Clarke M.J., Rinkel G.J. Endovascular coiling versus neurosurgical clipping for people with aneurysmal subarachnoid haemorrhage. The Cochrane database of systematic reviews. 2018;8(8). Doi: 10.1002/14651858.CD003085.PUB3.

24. Katsaridis V., Papagiannaki C., Violaris C. Embolization of Acutely Ruptured and Unruptured Wide-Necked Cerebral Aneurysms Using the Neuroform2 Stent without Pretreatment with Antiplatelets: A Single Center Experience. AJNR: American Journal of Neuroradiology. 2006;27(5):1123. Available from: https://www.ajnr.org/content/27/5/1123.long [Accessed 28 July 2023].

25. Sluzewski M., Menovsky T., Van Rooij W. J., Wijnalda D. Coiling of Very Large or Giant Cerebral Aneurysms: LongTerm Clinical and Serial Angiographic Results. AJNR: American Journal of Neuroradiology. 2003;24(2):257. Available from: https://www.ajnr.org/content/24/2/257 [Accessed 28 July 2023].

26. Chalouhi N., Tjoumakaris S., Gonzalez L. F., Dumont A. S., Starke R. M., Hasan D., Wu C., Singhal S., Moukarzel L. A., Rosenwasser R., Jabbour P. M. Coiling of large and giant aneurysms: complications and long-term results of 334 cases. AJNR. American journal of neuroradiology. 2014;35(3):546–552. Doi: 10.3174/AJNR.A3696.

27. Ihn Y. K., Shin S. H., Baik S. K., Choi I. S. Complications of endovascular treatment for intracranial aneurysms: Management and prevention. Interventional Neuroradiology. 2018;24(3):237–245. Doi: 10.1177/1591019918758493.

28. Blanc R., Weill A., Piotin M., Ross I. B., Moret J. Delayed Stroke Secondary to Increasing Mass Effect after Endovascular Treatment of a Giant Aneurysm by Parent Vessel Occlusion. AJNR: American Journal of Neuroradiology. 2001;22(10):1841. Available from: https://www.ajnr.org/content/22/10/1841.long [Accessed 28 July 2023].

29. Luzzi S., Del Maestro M., Galzio R. Microneurosurgery for Paraclinoid Aneurysms in the Context of Flow Diverters. Acta neurochirurgica. Supplement. 2021;(132):47–53. Doi: 10.1007/978-3-030-63453-7_7.

30. Kamide T., Tabani H., Safaee M. M., Burkhardt J. K., Lawton M. T. Microsurgical clipping of ophthalmic artery aneurysms: Surgical results and visual outcomes with 208 aneurysms. Journal of Neurosurgery. 2018;129(6):1511– 1521. Doi: 10.3171/2017.7.JNS17673.

31. Landik S. A., Svistov D. V., Kandyba D. V., Savello A. V. Sravnitel›nyi analiz iskhodov mikrokhirurgicheskogo i vnutrisosudistogo lecheniya anevrizm golovnogo mozga. 2009;(1):16– 23. (In Russ.). EDN: KGBPLB.

32. Dzhindzhikhadze R. S., Dreval’ O. N., Lazarev V. A., Kambiev R. L. Mini-orbitozygomatic craniotomy in surgery for supratentorial aneurysms and tumors of the anterior and middle cranial fossae. Voprosy Neirokhirurgii: Zhurnal Imeni N. N. Burdenko. 2016;80(4):40–47. (In Russ.). Doi: 10.17116/neiro201680440-47. EDN: WGEVPB.

33. Yamada Y., Ansari A., Sae-Ngow T., Tanaka R., Kawase T., Kalyan S., Kato Y. Microsurgical treatment of paraclinoid aneurysms by extradural anterior clinoidectomy: The fujita experience. Asian Journal of Neurosurgery. 2019;14(03):868–872. Doi: 10.4103/ajns.ajns_130_17.

34. Otani N., Toyooka T., Wada K., Mori K. Modified extradural temporopolar approach with suction decompression for clipping of large paraclinoid aneurysm: Technical note. Surgical Neurology International. 2017;8(1). Doi: 10.4103/sni.sni_377_16.

35. Khan N., Yoshimura S., Roth P., Cesnulis E., Koenue-Leblebicioglu D., Curcic M., Imhof H.-G., Yonekawa Y. Conventional microsurgical treatment of paraclinoid aneurysms: state of the art with the use of the selective extradural anterior clinoidectomy SEAC. Acta neurochirurgica. Supplement. 2005;(94):23–29. Doi: 10.1007/3-211-27911-3_5.

36. Sai Kiran N. A., Furtado S. V., Hegde A. S. How i do it: Anterior clinoidectomy and optic canal unroofing for microneurosurgical management of ophthalmic segment aneurysms. Acta Neurochirurgica. 2013;155(6):1025–1029. Doi: 10.1007/s00701-013-1685-1.

37. Meybodi A. T., Lawton M. T., Yousef S., Guo X., Sánchez J. J. G., Tabani H., García S., Burkhardt J. K., Benet A. Anterior clinoidectomy using an extradural and intradural 2-step hybrid technique. Journal of neurosurgery. 2018;130(1):238–247. Doi: 10.3171/2017.8.JNS171522.

38. Huynh-Le P., Natori Y., Sasaki T. Intra- and extradural anterior clinoidectomy: anatomy review and surgical technique step by step. Surgical and Radiologic Anatomy. 2021;43(8):1291–1303. Doi: 10.1007/s00276-021-02681-1.

39. Belkhair S., Guerrero Maldonado A., Tymianski M., Radovanovic I. Extra-Dural Anterior Clinoidectomy through the Lateral Supraorbital Approach: Surgical Anatomy and Initial Clinical Experience. Journal of Neurological Surgery Part B: Skull Base. 2014;75(S 01). Doi: 10.1055/S-0034-1370418.

40. Jean W. C. How I do it: extradural clinoidectomy. Acta Neurochirurgica. 2019;161(12):2583–2586. Doi: 10.1007/s00701-019-04066-1.

41. Mishra S., Leão B., Rosito D. Extradural anterior clinoidectomy: Technical nuances from a learner’s perspective. Asian Journal of Neurosurgery. 2017;12(02):189–193. Doi: 10.4103/1793-5482.145544.

42. Takeuchi S., Tanikawa R., Goehre F., Hernesniemi J., Tsuboi T., Noda K., Miyata S., Ota N., Sakakibara F., Andrade-Barazarte H., Kamiyama H. Retrograde Suction Decompression for Clip Occlusion of Internal Carotid Artery Communicating Segment Aneurysms. World neurosurgery. 2016;(89):19–25. Doi: 10.1016/J.WNEU.2015.12.095.

43. Otani N., Wada K., Toyooka T., Fujii K., Ueno H., Tomura S., Tomiyama A., Nakao Y., Yamamoto T., Mori K. Usefulness of Suction Decompression Method Combined with Extradural Temporopolar Approach during Clipping of Complicated Internal Carotid Artery Aneurysm. World Neurosurgery. 2016;(90):293–299. Doi: 10.1016/j.wneu.2016.02.120.

44. Krylov V. V., Klimov A. B., Polunina N. A. Diagnostika i lechenie bol’nykh s gigantskimi anevrizmami sosudov golovnogo mozga. Russian journal of neurosurgery. 2010;3:14–24. (In Russ.). EDN: NXNTSD.

45. Shekhtman O. D., Éliava Sh. Sh., Pilipenko Iu. V., Kheĭreddin A. S., Okishev D. N., Barchunov B. V., Kaftanov A. V. Long-term results of treatment of patients with large or giant intracranial aneurysms of internal carotid artery. Voprosy Neirokhirurgii: Zhurnal Imeni N. N. Burdenko. 2013;77(3):21–26. (In Russ.). EDN: QBVMDL.

46. Falk Delgado A., Andersson T., Falk Delgado A. Ruptured carotid-ophthalmic aneurysm treatment: a non-inferiority meta-analysis comparing endovascular coiling and surgical clipping. British journal of neurosurgery. 2017;31(3):345–349. Doi: 10.1080/02688697.2017.1297371.

47. Rodriguez-Calienes A., Borjas-Calderón N.F., Vivanco-Suarez J., Zila-Velasque J.P., Chavez-Malpartida S.S., Terry F., Grados-Espinoza P., Saal-Zapata G. Endovascular Treatment and Microsurgical Clipping for the Management of Paraclinoid Intracranial Aneurysms: A Systematic Review and Meta-Analysis. World Neurosurgery. 2023;(178):e489–e509. Doi: 10.1016/J.WNEU.2023.07.108.