Experimental model of intracranial aneurysms

Česká verzia

Authors: M. Hundža Stratilová ^1,2; K. Kárová ³; L. Machová Urdzíková ³; P. Jendelová ³; M. Koblížek ²; M. Sameš ¹; J. Zámečník ²; A. Hejčl ^1,3,4
Authors place of work: Neurochirurgická klinika Fakulty zdravotnických studií univerzity J. E. Purkyně v Ústí nad Labem a Krajské zdravotní, a. s. – Masarykovy nemocnice v Ústí nad Labem, o. z. ¹; Ústav patologie a molekulární medicíny 2. LF UK a FN Motol, Praha ²; Ústav experimentální medicíny Akademie věd České republiky ³; Mezinárodní centrum klinického výzkumu, Fakultní nemocnice u sv. Anny v Brně ⁴
Published in the journal: Cesk Slov Neurol N 2024; 87(2): 107-113
Category: Review Article
doi: https://doi.org/10.48095/cccsnn2024107

Summary

Rupture of an intracranial aneurysm represents a life-threatening condition with a still high mortality and morbidity. The pathogenesis of aneurysm development and eventual aneurysm rupture are still shrouded in mystery, representing a great field of research opportunities for scientists. Despite certain limitations, experimental models of intracranial aneurysms have their invaluable place. The review article summarizes the published results of current experimental rodent-focused models, their advantages, as well as limitations. At the same time, it introduces the reader to the results of our pilot study of an experimental laboratory mice model.

Keywords:

chronic inflammation – subarachnoid hemorrhage – intracranial aneurysm – experimental model – rodent model

Zdroje

1. Macdonald RL, Schweizer TA. Spontaneous subarachnoid haemorrhage. Lancet 2017; 389 (10069): 655–666. doi: 10.1016/S0140-6736 (16) 30668-7.

2. Nieuwkamp DJ, Setz LE, Algra A et al. Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. Lancet Neurol 2009; 8 (7): 635–642. doi: 10.1016/S1474-4422 (09) 70126-7.

3. Ingall T, Asplund K, Mähönen M et al. A multinational comparison of subarachnoid hemorrhage epidemiology in the WHO MONICA stroke study. Stroke 2000; 31 (5): 1054–1061. doi: 10.1161/01.str.31.5.1054.

4. Bilguvar K, Yasuno K, Niemelä M et al. Susceptibility loci for intracranial aneurysm in European and Japanese populations. Nat Genet 2008; 40 (12): 1472–1477. doi: 10.1038/ng.240.

5. Vlak MH, Algra A, Brandenburg R et al. Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis. Lancet Neurol 2011; 10 (7): 626–636. doi: 10.1016/S1474-4422 (11) 70109-0.

6. Greving JP, Wermer MJ, Brown RD, Jr. et al. Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol 2014; 13 (1): 59–66. doi: 10.1016/S1474-4422 (13) 70263-1.

7. Etminan N, Brown RD Jr, Beseoglu K et al. The unruptured intracranial aneurysm treatment score: a multidisciplinary consensus. Neurology 2015; 85 (10): 881–889. doi: 10.1212/WNL.0000000000001891.

8. Krings T, Mandell DM, Kiehl TR et al. Intracranial aneurysms: from vessel wall pathology to therapeutic approach. Nat Rev Neurol 2011; 7 (10): 547–559. doi: 10.1038/nrneurol.2011.136.

9. Signorelli F, Sela S, Gesualdo L et al. Hemodynamic stress, inflammation, and intracranial aneurysm development and rupture: a systematic review. World Neurosurg 2018; 115: 234–244. doi: 10.1016/j.wneu.2018.04.143.

10. Frösen J, Tulamo R, Paetau A et al. Saccular intracranial aneurysm: pathology and mechanisms. Acta Neuropathol 2012; 123 (6): 773–786. doi: 10.1007/s00401-011-0939-3.

11. Hejčl A, Stratilová M, Švihlová H et al. Matematické modelování hemodynamiky mozkových aneuryzmat a možný přínos v klinické praxi z pohledu neurochirurga. Cesk Slov Neurol N 2018; 81/114 (5): 532–538. doi: 10.14735/amcsnn2018532.

12. Wang Y, Emeto TI, Lee J et al. Mouse models of intracranial aneurysm. Brain Pathol 2015; 25 (3): 237–247. doi: 10.1111/bpa.12175.

13. Stehbens WE. Cerebral aneurysms of animals other than man. J Pathol Bacteriol 1963; 86: 160–168.

14. Hashimoto N, Handa H, Hazama F. Experimentally induced cerebral aneurysms in rats. Surg Neurol 1978; 10 (1): 3–8.

15. Morimoto M, Miyamoto S, Mizoguchi A et al. Mouse model of cerebral aneurysm: experimental induction by renal hypertension and local hemodynamic changes. Stroke 2002; 33 (7): 1911–1915. doi: 10.1161/01.str.0000021000.19637.3d.

16. Nuki Y, Tsou TL, Kurihara C et al. Elastase-induced intracranial aneurysms in hypertensive mice. Hypertension 2009; 54 (6): 1337–1344. doi: 10.1161/HYPERTENSIONAHA.109.138297.

17. Makino H, Tada Y, Wada K et al. Pharmacological stabilization of intracranial aneurysms in mice: a feasibility study. Stroke 2012; 43 (9): 2450–2456. doi: 10.1161/STROKEAHA.112.659821.

18. Yoeli M, Hargreaves BJ. Brain capillary blockage produced by a virulent strain of rodent malaria. Science 1974; 184 (4136): 572–573. doi: 10.1126/science.184.4136.572.

19. Abruzzo T, Kendler A, Apkarian R et al. Cerebral aneurysm formation in nitric oxide synthase-3 knockout mice. Curr Neurovasc Res 2007; 4 (3): 161–169. doi: 10.2174/156720207781387222.

20. Hosaka K, Downes DP, Nowicki KW et al. Modified murine intracranial aneurysm model: aneurysm formation and rupture by elastase and hypertension. J Neurointerv Surg 2014; 6 (6): 474–479. doi: 10.1136/neurintsurg-2013-010788.

21. Kanematsu Y, Kanematsu M, Kurihara C et al. Critical roles of macrophages in the formation of intracranial aneurysm. Stroke 2011; 42 (1): 173–178. doi: 10.1161/STROKE AHA.110.590976.

22. Tada Y, Wada K, Shimada K et al. Roles of hypertension in the rupture of intracranial aneurysms. Stroke 2014; 45 (2): 579–586. doi: 10.1161/STROKEAHA.113.003072.

23. Starke RM, Chalouhi N, Jabbour PM et al. Critical role of TNF-alpha in cerebral aneurysm formation and progression to rupture. J Neuroinflammation 2014; 11: 77. doi: 10.1186/1742-2094-11-77.

24. Aoki T, Kataoka H, Moriwaki T et al. Role of TIMP-1 and TIMP-2 in the progression of cerebral aneurysms. Stroke 2007; 38 (8): 2337–2345. doi: 10.1161/STROKEAHA. 107.481838.

25. Aoki T, Kataoka H, Shimamura M et al. NF-kB Is a key mediator of cerebral aneurysm formation. Circulation 2007; 116 (24): 2830–2840. doi: 10.1161/CIRCULATIONAHA.107.728303.

26. Aoki T, Kataoka H, Ishibashi R et al. Impact of monocyte chemoattractant protein-1 deficiency on cerebral aneurysm formation. Stroke 2009; 40 (3): 942–951. doi: 10.1161/STROKEAHA.108.532556.

27. Aoki T, Nishimura M, Kataoka H et al. Reactive oxygen species modulate growth of cerebral aneurysms: a study using the free radical scavenger edaravone and p47phox (–/–) mice. Lab Invest 2009; 89 (7): 730–741. doi: 10.1038/labinvest.2009.36.

28. Aoki T, Frösen J, Fukuda M et al. Prostaglandin E2–EP2–NF-kB signaling in macrophages as a potential therapeutic target for intracranial aneurysms. Science Signaling 2017; 10 (465): eaah6037. doi: 10.1126/scisignal.aah6037.

29. Frösen J, Piippo A, Paetau A et al. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: histological analysis of 24 unruptured and 42 ruptured cases. Stroke 2004; 35 (10): 2287–2293. doi: 10.1161/01.STR.0000140636.30204.da.

30. Bruno G, Todor R, Lewis I et al. Vascular extracellular matrix remodeling in cerebral aneurysms. J Neurosurg 1998; 89 (3): 431–440. doi: 10.3171/jns.1998.89.3.0431.

31. Caird J, Napoli C, Taggart C et al. Matrix metalloproteinases 2 and 9 in human atherosclerotic and non-atherosclerotic cerebral aneurysms. Eur J Neurol 2006; 13 (10): 1098–1105. doi: 10.1111/j.1468-1331.2006.01469.x.

32. Aoki T, Kataoka H, Morimoto M et al. Macrophage-derived matrix metalloproteinase-2 and -9 promote the progression of cerebral aneurysms in rats. Stroke 2007; 38 (1): 162–169. doi: 10.1161/01.STR.0000252129. 18605.c8.

33. Aoki T, Nishimura M, Matsuoka T et al. PGE2-EP2signalling in endothelium is activated by haemodynamic stress and induces cerebral aneurysm through an amplifying loop via NF-kB. Br J Pharmacol 2011; 163 (6): 1237–1249. doi: 10.1111/j.1476-5381.2011.01358.x.

34. Moriwaki T, Takagi Y, Sadamasa N et al. Impaired progression of cerebral aneurysms in interleukin-1beta-deficient mice. Stroke 2006; 37 (3): 900–905. doi: 10.1161/01.STR.0000204028.39783.d9.

35. Sadamasa N, Nozaki K, Hashimoto N. Disruption of gene for inducible nitric oxide synthase reduces progression of cerebral aneurysms. Stroke 2003; 34 (12): 2980–2984. doi: 10.1161/01.STR.0000102556.556 00.3B.

36. Aoki T, Nishimura M, Kataoka H et al. Complementary inhibition of cerebral aneurysm formation by eNOS and nNOS. Lab Invest 2011; 91 (4): 619–626. doi: 10.1038/labinvest.2010.204.

37. Tada Y, Wada K, Shimada K et al. Estrogen protects against intracranial aneurysm rupture in ovariectomized mice. Hypertension 2014; 63 (6): 1339–1344. doi: 10.1161/HYPERTENSIONAHA.114.03300.

38. Nagata I, Handa H, Hashimoto N et al. Experimentally induced cerebral aneurysms in rats: Part VI. Hypertension. Surg Neurol 1980; 14 (6): 477–479.

39. Chalouhi N, Atallah E, Jabbour P et al. Aspirin for the prevention of intracranial aneurysm rupture. Neurosurgery 2017; 64 (CN_suppl_1): 114–118. doi: 10.1093/neuros/nyx299.

40. Etminan N, Rinkel GJ. Unruptured intracranial aneurysms: development, rupture and preventive management. Nat Rev Neurol 2016; 12 (12): 699–713. doi: 10.1038/nrneurol.2016.150.

41. Stratilová MH, Koblížek M, Štekláčová A et al. Increased macrophage M2/M1 ratio is associated with intracranial aneurysm rupture. Acta Neurochir (Wien) 2023; 165 (1): 177–186. doi: 10.1007/s00701-022-05418-0.