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Nitric Oxide Donors in the Treatment of Vascular Spasm and Delayed Cerebral Ischemia in Patients with Subarachnoid Hemorrhage

https://doi.org/10.23934/2223-9022-2024-13-4-656-667

Abstract

Secondary vascular spasm due to non-traumatic rupture of cerebral artery aneurysms is a formidable complication leading to serious disability of patients who face this disease, and in 30–50% of cases leads to death. Standard therapy used in intensive care units does not have tremendous success in the treatment of this pathology, which encourages scientists around the world to search for new drugs that can improve the outcome and increase the quality of life of patients. At the moment, the most promising non-surgical method of treatment is the use of nitric oxide donor drugs as part of complex therapy. In modern medicine, there are several ways to administer drugs of this group: intravenously, intra-arterially , intrathecally , intraventricularly and by inhalation . The method depends on the type of drug used. Despite the promise of using these dosage forms, there are a number of negative side effects, which, due to insufficient study, limit their widespread use in hospitals. This review contains studies examining the positive and negative aspects of the use of these drugs and the appropriateness of their use.

About the Authors

S. V. Zhuravel
N.V. Sklifosovsky Research Institute for Emergency Medicine; N.I. Pirogov National Research Medical University; Russian University of Medicine, N.D. Yushchuk Scientific and Educational Institute of Continuous Professional Education
Russian Federation

Sergey V. Zhuravel - Doctor of Medical Sciences, Head of the Scientific Department of Anesthesiology, N.V. Sklifosovsky RIEM; Professor, Department of Anesthesiology, Reanimatology and Emergency Medicine, N.D. Yushchuk Scientific and Educational Institute of Continuous Professional Education, RUM; Associate Professor, Department of Anesthesiology, Resuscitation and Intensive Care named after Professor V.D. Malyshev, N.I. Pirogov RNRMU.

Bolshaya Sukharevskaya Sq. 3, Moscow, 129090; Ostrovityanova Str. 1, Moscow, 117513; Dolgorukovskaya Str. 4, Moscow, 127006



A. V. Prirodov
N.V. Sklifosovsky Research Institute for Emergency Medicine; N.I. Pirogov National Research Medical University
Russian Federation

Aleksandr V. Prirodov - Doctor of Medical Sciences, Head, Neurosurgical Department; Leading Researcher, Department of Emergency Neurosurgery, N.V. Sklifosovsky RIEM; Professor, Department of Fundamental Neurosurgery, N.I. Pirogov RNRMU.

Bolshaya Sukharevskaya Sq. 3, Moscow, 129090; Ostrovityanova Str. 1, Moscow, 117513



E. Yu. Bakharev
N.V. Sklifosovsky Research Institute for Emergency Medicine
Russian Federation

Evgeniy Yu. Bakharev - Candidate of Medical Sciences, Neurosurgeon, Senior Researcher, Department of Emergency Neurosurgery, N.V. Sklifosovsky RIEM.

Bolshaya Sukharevskaya Sq. 3, Moscow, 129090



P. D. Zorin
N.V. Sklifosovsky Research Institute for Emergency Medicine; N.I. Pirogov National Research Medical University
Russian Federation

Pavel D. Zorin - Anesthesiologist-Resuscitator, Department of Anesthesiology and Resuscitation No 1, N.V. Sklifosovsky RIEM; postgraduate student, Department of Anesthesiology, Reanimatology and Intensive Care named after Professor V.D. Malyshev, N.I. Pirogov RNRMU.

Bolshaya Sukharevskaya Sq. 3, Moscow, 129090; Ostrovityanova Str. 1, Moscow, 117513



S. S. Petrikov
N.V. Sklifosovsky Research Institute for Emergency Medicine; Russian University of Medicine, N.D. Yushchuk Scientific and Educational Institute of Continuous Professional Education
Russian Federation

Sergey S. Petrikov - Corresponding Member of the Russian Academy of Sciences, Doctor of Medical Sciences, Director, N.V. Sklifosovsky RIEM; Head, Department of Anesthesiology, Reanimatology and Emergency Medicine.

Bolshaya Sukharevskaya Sq. 3, Moscow, 129090; Dolgorukovskaya Str. 4, Moscow, 127006



References

1. Krylov VV, Vinokurov AG, Dash’yan VG, Luk’yanchikov VA, Polunina NA, Prirodov AV, et al. Mikrokhirurgiya anevrizm sosudov golovnogo mozga. Moscow: ABV-press Publ.; 2022. (In Russ.)

2. Leliuk VG, Leliuk SE. Cerebral angiospasm in subarachnoid hemorrhages. Zh Nevrol Psikhiatr Im S S Korsakova. 2011;111(8 Pt 2):62–73. PMID: 22224249. (In Russ.)

3. Byrne JV, Griffith TM, Edwards DH, Harrison TJ, Johnston KR. Investigation of the vasoconstrictor action of subarachnoid haemoglobin in the pig cerebral circulation in vivo. Br J Pharmacol. 1989;97(3):669–674. PMID: 2788022 https://doi.org/10.1111/j.1476-5381.1989.tb12002.x

4. Edwards DH, Byrne JV, Griffith TM. The effect of chronic subarachnoid hemorrhage on basal endothelium-derived relaxing factor activity in intrathecal cerebral arteries. J Neurosurg. 1992;76(5):830–837. PMID: 1314293 https://doi.org/10.3171/jns.1992.76.5.0830

5. Fung C, Z’Graggen WJ, Jakob SM, Gralla J, Haenggi M, Rothen HU, et al. Inhaled Nitric Oxide Treatment for Aneurysmal SAH Patients With Delayed Cerebral Ischemia. Front Neurol. 2022;13:817072. PMID: 35250821 https://doi.org/10.3389/fneur.2022.817072

6. Siasios I, Kapsalaki EZ, Fountas KN. Cerebral vasospasm pharmacological treatment: an update. Neurol Res Int. 2013;2013:571328. PMID: 23431440 https://doi.org/10.1155/2013/571328

7. Rassaf T, Kleinbongard P, Preik M, Dejam A, Gharini P, Lauer T, et al. Plasma nitrosothiols contribute to the systemic vasodilator effectsof intravenously applied NO: experimental and clinical Study on the fate of NO in human blood. Circ Res. 2002;91(1):470–477. PMID: 12242264 https://doi.org/10.1161/01.res.0000035038.41739.cb

8. Kiriş T, Karasu A, Yavuz C, Erdem T, Unal F, Hepgül K, et al. Reversal of cerebral vasospasm by the nitric oxide donor SNAP in an experimental model of subarachnoid haemorrhage. Acta Neurochir (Wien). 1999;141(12):1323–1328. PMID: 10672304 https://doi.org/10.1007/s007010050437

9. Sehba FA, Ding WH, Chereshnev I, Bederson JB. Effects of Snitrosoglutathione on acute vasoconstriction and glutamate release after subarachnoid hemorrhage. Stroke. 1999;30(9):1955–1961. PMID: 10471450 https://doi.org/10.1161/01.str.30.9.1955

10. Clatterbuck RE, Gailloud P, Tierney T, Clatterbuck VM, Murphy KJ, Tamargo RJ. Controlled release of a nitric oxide donor for the prevention of delayed cerebral vasospasm following experimental subarachnoid hemorrhage in nonhuman primates. J Neurosurg. 2005;103(4):745–751. PMID: 16266059 https://doi.org/10.3171/jns.2005.103.4.0745

11. Gabikian P, Clatterbuck RE, Eberhart CG, Tyler BM, Tierney TS, Tamargo RJ. Prevention of Experimental Cerebral Vasospasm by Intracranial Delivery of a Nitric Oxide Donor From a Controlled-Release Polymer. Stroke. 2002;33(11):2681–2686. PMID: 12411661 https://doi.org/10.1161/01.str.0000033931.62992.b1

12. Pradilla G, Thai QA, Legnani FG, Hsu W, Kretzer RM, Wang PP, et al. Delayed intracranial delivery of a nitric oxide donor from a controlledrelease polymer prevents experimental cerebral vasospasm in rabbits. Neurosurgery. 2004;55(6):1393–1399. PMID: 15574221 https://doi.org/10.1227/01.neu.0000143615.26102.1a

13. Wolf EW, Banerjee A, Soble-Smith J, Dohan FC Jr, White RP, Robertson JT. Reversal of cerebral vasospasm using an intrathecally administered nitric oxide donor. J Neurosurg. 1998;89(2):279–288. PMID: 9688124 https://doi.org/10.3171/jns.1998.89.2.0279

14. Matsui T, Nagafuji T, Tsutsumi K, Uchida H, Miyauchi T, Asano T. The effect of Nicorandil on chronic cerebral vasospasm. Acta Neurochir (Wien). 1994;126(2–4):165–169. PMID: 8042550 https://doi.org/10.1007/BF01476428

15. Pluta RM, Dejam A, Grimes G, Gladwin MT, Oldfield EH. Nitrite infusions to prevent delayed cerebral vasospasm in a primate model of subarachnoid hemorrhage. Jama. 2005;293(12):1477–1484. PMID: 15784871 https://doi.org/10.1001/jama.293.12.1477

16. Lilla N, Hartmann J, Koehler S, Ernestus R-I, Westermaier T. Early NO-donor treatment improves acute perfusion deficit and brain damage after experimental subarachnoid hemorrhage in rats. J Neurol Sci. 2016;370:312–319. PMID: 27745692 https://doi.org/10.1016/j.jns.2016.09.032

17. Marbacher S, Neuschmelting V, Graupner T, Jakob SM, Fandino J. Prevention of delayed cerebral vasospasm by continuous intrathecal infusion of glyceroltrinitrate and nimodipine in the rabbit model in vivo. Intensive Care Med. 2008;34(5):932–938. PMID: 18214428 https://doi.org/10.1007/s00134-008-0995-x

18. Fathi AR, Marbacher S, Graupner T, Wehrli F, Jakob SM, Schroth G, et al. Continuous intrathecal glyceryl trinitrate prevents delayed cerebral vasospasm in the single-SAH rabbit model in vivo. Acta Neurochir (Wien). 2011;153(8):1669–1675. PMID: 21671141 https://doi.org/10.1007/s00701-011-1049-7

19. Allen GS. Cerebral arterial spasm. Part 8: The treatment of delayed cerebral arterial spasm in human beings. Surg Neurol. 1976;6(2):71–80. PMID: 951655

20. Iwanaga H, Okuchi K, Koshimae N, Goda K, Imanishi M, Tokunaga H, et al. Effects of intravenous nitroglycerin combined with dopamine on intracranial pressure and cerebral arteriovenous oxygen difference in patients with acute subarachnoid haemorrhage. Acta Neurochir (Wien). 1995;136(3–4):175–180. PMID: 8748850 https://doi.org/10.1007/BF01410622

21. Rose JC, Mayer SA. Optimizing blood pressure in neurological emergencies. Neurocrit Care. 2004;1(3):287–299. PMID: 16174926 https://doi.org/10.1385/NCC:1:3:287 Dosage error in article text. Erratum in: Neurocrit Care. 2006;4(1):98. PMID: 16174926

22. Oldfield EH, Loomba JJ, Monteith SJ, Crowley RW, Medel R, Gress DR, et al. Safety and pharmacokinetics of sodium nitrite in patients with subarachnoid hemorrhage: a phase IIa study. J Neurosurg. 2013;119(3):634–641. PMID: 23706046 https://doi.org/10.3171/2013.3.JNS13266

23. Pathak A, Mathuriya SN, Khandelwal N, Verma K. Intermittent low dose intrathecal sodium nitroprusside therapy for treatment of symptomatic aneurysmal SAH-induced vasospasm. Br J Neurosurg. 2003;17(4):306–310. PMID: 14579895 https://doi.org/10.1080/02688690310001601180

24. Kumar R, Pathak A, Mathuriya SN, Khandelwal N. Intraventricular sodium nitroprusside therapy: a future promise for refractory subarachnoid hemorrhage-induced vasospasm. Neurol India. 2003;51(2):197–202. PMID: 14571002

25. Thomas JE, McGinnis G. Safety of intraventricular sodium nitroprusside and thiosulfate for the treatment of cerebral vasospasm in the intensive care unit setting. Stroke. 2002;33(2):486–492. PMID: 11823657 https://doi.org/10.1161/hs0202.103410

26. Pachl J, Haninec P, Tencer T, Mizner P, Houst’ava L, Tomás R, et al. The effect of subarachnoid sodium nitroprusside on the prevention of vasospasm in subarachnoid haemorrhage. Acta Neurochir Suppl. 2005;95:141–145. PMID: 16463839 https://doi.org/10.1007/3-211-32318-x_31

27. Agrawal A, Patir R, Kato Y, Chopra S, Sano H, Kanno T. Role of intraventricular sodium nitroprusside in vasospasm secondary to aneurysmal subarachnoid haemorrhage: A 5-year prospective study with review of the literature. Minim Invasive Neurosurg. 2009;52(1):5–8. PMID: 19247898 https://doi.org/10.1055/s-0028-1085454

28. Kajita Y, Suzuki Y, Oyama H, Tanazawa T, Takayasu M, Shibuya M, et al. Combined effect of L-arginine and superoxide dismutase on the spastic basilar artery after subarachnoid hemorrhage in dogs. J Neurosurg. 1994;80(3):476–483. PMID: 8113861 https://doi.org/10.3171/jns.1994.80.3.0476

29. Pluta RM, Afshar JK, Thompson BG, Boock RJ, Harvey-White J, Oldfield EH. Increased cerebral blood flow but no reversal or prevention of vasospasm in response to L-arginine infusion after subarachnoid hemorrhage. J Neurosurg. 2000;92(1):121–126. PMID: 10616090 https://doi.org/10.3171/jns.2000.92.1.0121

30. Göksel HM, Ozüm U, Oztoprak I. The therapeutic effect of continuous intracisternal L-Arginine infusion on experimental cerebral vasospasm. Acta Neurochir (Wien). 2001;143(3):277–285. PMID: 11460916 https://doi.org/10.1007/s007010170108

31. Ozüm U, Aslan A, Karadağ O, Gürelik M, Taş A, Zafer Kars H. Intracisternal versus intracarotid infusion of L-arginine in experimental cerebral vasospasm. J Clin Neurosci. 2007;14(6):556–562. PMID: 17430779 https://doi.org/10.1016/j.jocn.2006.03.013

32. Ozüm U, Aslan A, Taş A, Kars HZ. Intracarotid L-arginine reverses motor evoked potential changes in experimental cerebral vasospasm. Turk Neurosurg. 2007;17(1):13–18. PMID: 17918672

33. Ehlert A, Schmidt C, Wölfer J, Manthei G, Jacobs AH, Brüning R, et al. Molsidomine for the prevention of vasospasm-related delayed ischemic neurological deficits and delayed brain infarction and the improvement of clinical outcome after subarachnoid hemorrhage: a single-center clinical observational study. J Neurosurg. 2016;124(1):51–58. PMID: 26162034 https://doi.org/10.3171/2014.12.JNS13846

34. Ehlert A, Manthei G, Hesselmann V, Mathias K, Bein B, Pluta R. A Case of Hyperacute Onset of Vasospasm After Aneurysmal Subarachnoid Hemorrhage and Refractory Vasospasm Treated with Intravenous and Intraventricular Nitric Oxide: A Mini Review. World Neurosurg. 2016;91:673.e11–8. PMID: 27109628 https://doi.org/10.1016/j.wneu.2016.04.047

35. Ehlert A, Starekova J, Manthei G, Ehlert-Gamm A, Flack J, Gessert M, et al. Nitric Oxide-Based Treatment of Poor-Grade Patients After Severe Aneurysmal Subarachnoid Hemorrhage. Neurocrit Care. 2020;32(3):742– 754. PMID: 31418143 https://doi.org/10.1007/s12028-019-00809-1

36. Bellapart J, Jones L, Bandeshe H, Boots R. Plasma endothelin-1 as screening marker for cerebral vasospasm after subarachnoid hemorrhage. Neurocrit Care. 2014;20(1):77–83. PMID: 23921571 https://doi.org/10.1007/s12028-013-9887-1

37. Macdonald RL, Higashida RT, Keller E, Mayer SA, Molyneux A, Raabe A, et al. Randomised trial of clazosentan, an endothelin receptor antagonist, in patients with aneurysmal subarachnoid hemorrhage undergoing surgical clipping (CONSCIOUS-2). Acta Neurochir Suppl. 2013;115:27–31. PMID: 22890639 https://doi.org/10.1007/978-3-7091-1192-5_7

38. Macdonald RL, Kassell NF, Mayer S, Ruefenacht D, Schmiedek P, Weidauer S, et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-findingtrial. Stroke. 2008;39(11):3015–3021. PMID: 18688013 https://doi.org/10.1161/STROKEAHA.108.519942

39. Cho SS, Kim SE, Kim HC, Kim WJ, Jeon JP. Clazosentan for Aneurysmal Subarachnoid Hemorrhage: An Updated Meta-Analysis with Trial Sequential Analysis. World Neurosurg. 2019;123:418–424.e3. PMID: 30508597 https://doi.org/10.1016/j.wneu.2018.10.213

40. Endo H, Hagihara Y, Kimura N, Takizawa K, Niizuma K, Togo O, et al. Effects of clazosentan on cerebral vasospasm-related morbidity and all-cause mortality after aneurysmal subarachnoid hemorrhage: two randomized phase 3 trials in Japanese patients. J Neurosurg. 2022;137(6):1707–1717. PMID: 35364589 https://doi.org/10.3171/2022.2.JNS212914

41. Atalay B, Caner H, Cekinmez M, Ozen O, Celasun B, Altinors N. Systemic administration of phosphodiesterase V inhibitor, sildenafil citrate, for attenuation of cerebral vasospasm after experimental subarachnoid hemorrhage. Neurosurgery. 2006;59(5):1102–1107. PMID: 17143244 https://doi.org/10.1227/01.NEU.0000245605.22817.44

42. Han BH, Vellimana AK, Zhou ML, Milner E, Zipfel GJ. Phosphodiesterase 5 inhibition attenuates cerebral vasospasm and improves functional recovery after experimental subarachnoid hemorrhage. Neurosurgery. 2012;70(1):178–186. PMID: 21796010 https://doi.org/10.1227/ NEU.0b013e31822ec2b0

43. Mukherjee KK, Singh SK, Khosla VK, Mohindra S, Salunke P. Safety and efficacy of sildenafil citrate in reversal of cerebral vasospasm: a feasibility study. Surg Neurol Int. 2012:3:3. PMID: 22347673 https://doi.org/10.4103/2152-7806.92164

44. Washington CW, Derdeyn CP, Dhar R, Arias EJ, Chicoine MR, Cross DT, et al. A Phase I proof-of-concept and safety trial of sildenafil to treat cerebral vasospasm following subarachnoid hemorrhage. J Neurosurg. 2016;124(2):318–327. PMID: 26314998 https://doi.org/10.3171/2015.2.JNS142752

45. Dhar R, Washington C, Diringer M, Zazulia A, Jafri H, Derdeyn C, et al. Acute Effect of Intravenous Sildenafil on Cerebral Blood Flow in Patients with Vasospasm After Subarachnoid Hemorrhage. Neurocrit Care. 2016;25(2):201–204. PMID: 26940913 https://doi.org/10.1007/s12028-016-0243-0

46. Faropoulos K, Tsolaki V, Georgakopoulou VE, Trakas I, Tarantinos K, Papalexis P, et al. Value of sildenafil treatment for the prevention of vasospasm-related delayed ischemic neurological deficits and delayed brain infarction following aneurysmal subarachnoid hemorrhage. Med Int (London). 2023;3(2):19. PMID: 37032716 https://doi.org/10.3892/mi.2023.79

47. Dorhout Mees SM, Rinkel GJ, Hop JW, Algra A, van Gijn J. Antiplatelet therapy in aneurysmal subarachnoid hemorrhage: a systematic review. Stroke. 2003;34(9):2285–2289. PMID: 12881605 https://doi.org/10.1161/01.STR.0000083621.44269.3E

48. Matsuda N, Naraoka M, Ohkuma H, Shimamura N, Ito K, Asano K, et al. Effect of Cilostazol on Cerebral Vasospasm and Outcome in Patients with Aneurysmal Subarachnoid Hemorrhage: A Randomized, DoubleBlind, Placebo-Controlled Trial. Cerebrovasc Dis. 2016;42(1–2):97–105. PMID: 27070952 https://doi.org/10.1159/000445509

49. Li L, Fu X, Qiu H, Shi P. Effects of cilostazol treatment for patients with aneurysmal subarachnoid hemorrhage: A meta-analysis of 14 studies. J Clin Neurosci. 2022;99:190–203. PMID: 35286971 https://doi.org/10.1016/j.jocn.2021.12.025

50. Dayyani M, Sadeghirad B, Grotta JC, Zabihyan S, Ahmadvand S, Wang Y, et al. Prophylactic Therapies for Morbidity and Mortality After Aneurysmal Subarachnoid Hemorrhage: A Systematic Review and Network MetaAnalysis of Randomized Trials. Stroke. 2022;53(6):1993–2005. PMID: 35354302 https://doi.org/10.1161/STROKEAHA.121.035699

51. Li YS, Shemmer B, Stone E, A Nardi M, Jonas S, Quartermain D. Neuroprotection by inhaled nitric oxide in a murine stroke model is concentration and duration dependent. Brain Res. 2013;1507:134–145. PMID: 23473843 https://doi.org/10.1016/j.brainres.2013.02.031

52. Terpolilli NA, Feiler S, Dienel A, Müller F, Heumos N, Friedrich B, et al. Nitric oxide inhalation reduces brain damage, prevents mortality, and improves neurological outcome after subarachnoid hemorrhage by resolving early pial microvasospasms. J Cereb Blood Flow Metab. 2016;36(12):2096–2107. PMID: 26661144 https://doi.org/10.1177/0271678X15605848


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For citations:


Zhuravel S.V., Prirodov A.V., Bakharev E.Yu., Zorin P.D., Petrikov S.S. Nitric Oxide Donors in the Treatment of Vascular Spasm and Delayed Cerebral Ischemia in Patients with Subarachnoid Hemorrhage. Russian Sklifosovsky Journal "Emergency Medical Care". 2024;13(4):656-667. (In Russ.) https://doi.org/10.23934/2223-9022-2024-13-4-656-667

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ISSN 2223-9022 (Print)
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