Nimodipine Reappraised: An Old Drug With a Future

Author(s): Andrew P. Carlson*, Daniel Hänggi, Robert L. Macdonald, Claude W. Shuttleworth.

Journal Name: Current Neuropharmacology

Volume 18 , Issue 1 , 2020

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Graphical Abstract:


Abstract:

Nimodipine is a dihydropyridine calcium channel antagonist that blocks the flux of extracellular calcium through L-type, voltage-gated calcium channels. While nimodipine is FDAapproved for the prevention and treatment of neurological deficits in patients with aneurysmal subarachnoid hemorrhage (aSAH), it affects myriad cell types throughout the body, and thus, likely has more complex mechanisms of action than simple inhibition of cerebral vasoconstriction. Newer understanding of the pathophysiology of delayed ischemic injury after a variety of acute neurologic injuries including aSAH, traumatic brain injury (TBI) and ischemic stroke, coupled with advances in the drug delivery method for nimodipine, have reignited interest in refining its potential therapeutic use. In this context, this review seeks to establish a firm understanding of current data on nimodipine’s role in the mechanisms of delayed injury in aSAH, TBI, and ischemic stroke, and assess the extensive clinical data evaluating its use in these conditions. In addition, we will review pivotal trials using locally administered, sustained release nimodipine and discuss why such an approach has evaded demonstration of efficacy, while seemingly having the potential to significantly improve clinical care.

Keywords: Delayed cerebral ischemia, vasospasm, subarachnoid hemorrhage, L-type calcium channel, nimodipine, sustained release delivery.

[1]
Johnston, S.C.; Selvin, S.; Gress, D.R. The burden, trends, and demographics of mortality from subarachnoid hemorrhage. Neurology, 1998, 50(5), 1413-1418.
[http://dx.doi.org/10.1212/WNL.50.5.1413] [PMID: 9595997]
[2]
Rincon, F.; Rossenwasser, R.H.; Dumont, A. The epidemiology of admissions of nontraumatic subarachnoid hemorrhage in the United States. Neurosurgery, 2013, 73(2), 217-222.
[http://dx.doi.org/10.1227/01.neu.0000430290.93304.33] [PMID: 23615089]
[3]
Shea, A.M.; Reed, S.D.; Curtis, L.H.; Alexander, M.J.; Villani, J.J.; Schulman, K.A. Characteristics of nontraumatic subarachnoid hemorrhage in the United States in 2003. Neurosurgery, 2007, 61(6), 1131-1137.
[http://dx.doi.org/10.1227/01.neu.0000306090.30517.ae] [PMID: 18162891]
[4]
Nieuwkamp, D.J.; Setz, L.E.; Algra, A.; Linn, F.H.H.; de Rooij, N.K.; Rinkel, G.J.E. 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.
[http://dx.doi.org/10.1016/S1474-4422(09)70126-7] [PMID: 19501022]
[5]
Serrone, J.C.; Maekawa, H.; Tjahjadi, M.; Hernesniemi, J. Aneurysmal subarachnoid hemorrhage: pathobiology, current treatment and future directions. Expert Rev. Neurother., 2015, 15(4), 367-380.
[http://dx.doi.org/10.1586/14737175.2015.1018892] [PMID: 25719927]
[6]
Al-Khindi, T.; Macdonald, R.L.; Schweizer, T.A. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke, 2010, 41(8), e519-e536.
[http://dx.doi.org/10.1161/STROKEAHA.110.581975] [PMID: 20595669]
[7]
Greving, J.P.; Wermer, M.J.H.; Brown, R.D., Jr; Morita, A.; Juvela, S.; Yonekura, M.; Ishibashi, T.; Torner, J.C.; Nakayama, T.; Rinkel, G.J.E.; Algra, A. 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.
[http://dx.doi.org/10.1016/S1474-4422(13)70263-1] [PMID: 24290159]
[8]
Hänggi, D.; Etminan, N.; Macdonald, R.L.; Steiger, H.J.; Mayer, S.A.; Aldrich, F.; Diringer, M.N.; Hoh, B.L.; Mocco, J.; Strange, P.; Faleck, H.J.; Miller, M.N. Nimodipine microparticles to enhance recovery while reducing toxicity after subarachnoid hemorrhage. Neurocrit. Care, 2015, 23(2), 274-284.
[http://dx.doi.org/10.1007/s12028-015-0112-2] [PMID: 25678453]
[9]
Macdonald, R.L. Delayed neurological deterioration after subarachnoid haemorrhage. Nat. Rev. Neurol., 2014, 10(1), 44-58.
[http://dx.doi.org/10.1038/nrneurol.2013.246] [PMID: 24323051]
[10]
Malik, A.N.; Gross, B.A.; Rosalind, L.P.M.; Moses, Z.B.; Du, R. Neurogenic stress cardiomyopathy after aneurysmal subarachnoid hemorrhage. World Neurosurg., 2015, 83(6), 880-885.
[http://dx.doi.org/10.1016/j.wneu.2015.01.013] [PMID: 25655685]
[11]
Macdonald, R.L. Origins of the concept of vasospasm. Stroke, 2016, 47(1), e11-e15.
[http://dx.doi.org/10.1161/STROKEAHA.114.006498] [PMID: 26337970]
[12]
Laskowitz, D.T.; Kolls, B.J. Neuroprotection in subarachnoid hemorrhage. Stroke, 2010, 41(10)(Suppl.), S79-S84.
[http://dx.doi.org/10.1161/STROKEAHA.110.595090] [PMID: 20876512]
[13]
Dreier, J.P.; Windmüller, O.; Petzold, G.; Lindauer, U.; Einhäupl, K.M.; Dirnagl, U. Ischemia triggered by red blood cell products in the subarachnoid space is inhibited by nimodipine administration or moderate volume expansion/hemodilution in rats. Neurosurgery, 2002, 51(6), 1457-1465.
[http://dx.doi.org/10.1097/00006123-200212000-00017] [PMID: 12445352]
[14]
Lu, N.; Jackson, D.; Luke, S.; Festic, E.; Hanel, R.A.; Freeman, W.D. Intraventricular nicardipine for aneurysmal subarachnoid hemorrhage related vasospasm: assessment of 90 days outcome. Neurocrit. Care, 2012, 16(3), 368-375.
[http://dx.doi.org/10.1007/s12028-011-9659-8] [PMID: 22160865]
[15]
Hänggi, D.; Beseoglu, K.; Turowski, B.; Steiger, H-J. Feasibility and safety of intrathecal nimodipine on posthaemorrhagic cerebral vasospasm refractory to medical and endovascular therapy. Clin. Neurol. Neurosurg., 2008, 110(8), 784-790.
[http://dx.doi.org/10.1016/j.clineuro.2008.05.001] [PMID: 18554777]
[16]
Biondi, A.; Ricciardi, G.K.; Puybasset, L.; Abdennour, L.; Longo, M.; Chiras, J.; Van Effenterre, R. Intra-arterial nimodipine for the treatment of symptomatic cerebral vasospasm after aneurysmal subarachnoid hemorrhage: preliminary results. Am. J. Neuroradiol., 2004, 25(6), 1067-1076.
[PMID: 15205150]
[17]
Hänggi, D.; Turowski, B.; Beseoglu, K.; Yong, M.; Steiger, H.J. Intra-arterial nimodipine for severe cerebral vasospasm after aneurysmal subarachnoid hemorrhage: influence on clinical course and cerebral perfusion. Am. J. Neuroradiol., 2008, 29(6), 1053-1060.
[http://dx.doi.org/10.3174/ajnr.A1005] [PMID: 18372422]
[18]
Barth, M.; Pena, P.; Seiz, M.; Thomé, C.; Muench, E.; Weidauer, S.; Hattingen, E.; Kasuya, H.; Schmiedek, P. Feasibility of intraventricular nicardipine prolonged release implants in patients following aneurysmal subarachnoid haemorrhage. Br. J. Neurosurg., 2011, 25(6), 677-683.
[http://dx.doi.org/10.3109/02688697.2010.548878] [PMID: 21344979]
[19]
Kasuya, H.; Onda, H.; Sasahara, A.; Takeshita, M.; Hori, T. Application of nicardipine prolonged-release implants: analysis of 97 consecutive patients with acute subarachnoid hemorrhage. Neurosurgery, 2005, 56(5), 895-902.
[PMID: 15854236]
[20]
Zamponi, G.W.; Striessnig, J.; Koschak, A.; Dolphin, A.C. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol. Rev., 2015, 67(4), 821-870.
[http://dx.doi.org/10.1124/pr.114.009654] [PMID: 26362469]
[21]
Fleckenstein, A.; Frey, M.; Fleckenstein-Grün, G. Consequences of uncontrolled calcium entry and its prevention with calcium antagonists. Eur. Heart J., 1983, 4(Suppl. H), 43-50.
[http://dx.doi.org/10.1093/eurheartj/4.suppl_H.43] [PMID: 6662132]
[22]
Meyer, H.; Wehinger, E.; Bossert, F.; Scherling, D. cheminform abstract: nimodipine: synthesis and metabolic pathway. Chemischer Informationsdienst, 1983, 14(20)
[23]
Tsien, R.W.; Lipscombe, D.; Madison, D.V.; Bley, K.R.; Fox, A.P. Multiple types of neuronal calcium channels and their selective modulation. Trends Neurosci., 1988, 11(10), 431-438.
[http://dx.doi.org/10.1016/0166-2236(88)90194-4] [PMID: 2469160]
[24]
Tang, L.; Gamal El-Din, T.M.; Swanson, T.M.; Pryde, D.C.; Scheuer, T.; Zheng, N.; Catterall, W.A. Structural basis for inhibition of a voltage-gated Ca2+ channel by Ca2+ antagonist drugs. Nature, 2016, 537(7618), 117-121.
[http://dx.doi.org/10.1038/nature19102] [PMID: 27556947]
[25]
Bean, B.P. Nitrendipine block of cardiac calcium channels: high-affinity binding to the inactivated state. Proc. Natl. Acad. Sci. USA, 1984, 81(20), 6388-6392.
[http://dx.doi.org/10.1073/pnas.81.20.6388] [PMID: 6093100]
[26]
Sanguinetti, M.C.; Kass, R.S. Voltage-dependent block of calcium channel current in the calf cardiac Purkinje fiber by dihydropyridine calcium channel antagonists. Circ. Res., 1984, 55(3), 336-348.
[http://dx.doi.org/10.1161/01.RES.55.3.336] [PMID: 6088117]
[27]
Zuccotti, A.; Clementi, S.; Reinbothe, T.; Torrente, A.; Vandael, D.H.; Pirone, A. Structural and functional differences between L-type calcium channels: crucial issues for future selective targeting. Trends Pharmacol. Sci., 2011, 32(6), 366-375.
[http://dx.doi.org/10.1016/j.tips.2011.02.012] [PMID: 21450352]
[28]
Kisler, K.; Nelson, A.R.; Montagne, A.; Zlokovic, B.V. Cerebral blood flow regulation and neurovascular dysfunction in Alzheimer disease. Nat. Rev. Neurosci., 2017, 18(7), 419-434.
[http://dx.doi.org/10.1038/nrn.2017.48] [PMID: 28515434]
[29]
Scriabine, A.; Kerckhoff, W. Pharmacology of nimodipine. Ann. N.Y. Acad. Sci., 1988, 522(1 Calcium Antag), 698-706.
[http://dx.doi.org/10.1111/j.1749-6632.1988.tb33415.x]
[30]
Canova, D.; Roatta, S.; Micieli, G.; Bosone, D. Extracranial circulation affects near infrared spectroscopy assessment of cerebral blood volume and oxygenation during neurovegetative tests. Auton. Neurosci., 2011, 163(1-2), 97.
[http://dx.doi.org/10.1016/j.autneu.2011.05.164]
[31]
Petruk, K.C.; West, M.; Mohr, G.; Weir, B.K.; Benoit, B.G.; Gentili, F.; Disney, L.B.; Khan, M.I.; Grace, M.; Holness, R.O. Nimodipine treatment in poor-grade aneurysm patients. Results of a multicenter double-blind placebo-controlled trial. J. Neurosurg., 1988, 68(4), 505-517.
[http://dx.doi.org/10.3171/jns.1988.68.4.0505] [PMID: 3280746]
[32]
Feigin, V.L.; Rinkel, G.J.E.; Algra, A.; Vermeulen, M.; van Gijn, J. Calcium antagonists in patients with aneurysmal subarachnoid hemorrhage: a systematic review. Neurology, 1998, 50(4), 876-883.
[http://dx.doi.org/10.1212/WNL.50.4.876] [PMID: 9566366]
[33]
Dreier, J.P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nat. Med., 2011, 17(4), 439-447.
[http://dx.doi.org/10.1038/nm.2333] [PMID: 21475241]
[34]
Dreier, J.P.; Victorov, I.V.; Petzold, G.C.; Major, S.; Windmüller, O.; Fernández-Klett, F.; Kandasamy, M.; Dirnagl, U.; Priller, J. Electrochemical failure of the brain cortex is more deleterious when it is accompanied by low perfusion. Stroke, 2013, 44(2), 490-496.
[http://dx.doi.org/10.1161/STROKEAHA.112.660589] [PMID: 23287786]
[35]
Windmüller, O.; Lindauer, U.; Foddis, M.; Einhäupl, K.M.; Dirnagl, U.; Heinemann, U.; Dreier, J.P. Ion changes in spreading ischaemia induce rat middle cerebral artery constriction in the absence of NO. Brain, 2005, 128(Pt 9), 2042-2051.
[http://dx.doi.org/10.1093/brain/awh545] [PMID: 15901647]
[36]
Menyhárt, Á.; Farkas, A.E.; Varga, D.P.; Frank, R.; Tóth, R.; Bálint, A.R.; Makra, P.; Dreier, J.P.; Bari, F.; Krizbai, I.A.; Farkas, E. Large-conductance Ca2+-activated potassium channels are potently involved in the inverse neurovascular response to spreading depolarization. Neurobiol. Dis., 2018, 119, 41-52.
[http://dx.doi.org/10.1016/j.nbd.2018.07.026] [PMID: 30053571]
[37]
Szabó, Í.; M Tóth, O.; Török, Z.; Varga, D.P.; Menyhárt, A.; Frank, R.; Hantosi, D.; Hunya, A.; Bari, F.; Horváth, I.; Vigh, L.; Farkas, E. The impact of dihydropyridine derivatives on the cerebral blood flow response to somatosensory stimulation and spreading depolarization. Br. J. Pharmacol., 2019, 176(9), 1222-1234.
[http://dx.doi.org/10.1111/bph.14611] [PMID: 30737967]
[38]
Ludwig, A.; Flockerzi, V.; Hofmann, F. Regional expression and cellular localization of the α1 and β subunit of high voltage-activated calcium channels in rat brain. J. Neurosci., 1997, 17(4), 1339-1349.
[http://dx.doi.org/10.1523/JNEUROSCI.17-04-01339.1997] [PMID: 9006977]
[39]
Hell, J.W.; Westenbroek, R.E.; Warner, C.; Ahlijanian, M.K.; Prystay, W.; Gilbert, M.M.; Snutch, T.P.; Catterall, W.A. Identification and differential subcellular localization of the neuronal class C and class D L-type calcium channel alpha 1 subunits. J. Cell Biol., 1993, 123(4), 949-962.
[http://dx.doi.org/10.1083/jcb.123.4.949] [PMID: 8227151]
[40]
Magee, J.C.; Johnston, D. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science, 1995, 268(5208), 301-304.
[http://dx.doi.org/10.1126/science.7716525] [PMID: 7716525]
[41]
Helton, T.D.; Xu, W.; Lipscombe, D. Neuronal L-type calcium channels open quickly and are inhibited slowly. J. Neurosci., 2005, 25(44), 10247-10251.
[http://dx.doi.org/10.1523/JNEUROSCI.1089-05.2005] [PMID: 16267232]
[42]
Topolnik, L.; Chamberland, S.; Pelletier, J.G.; Ran, I.; Lacaille, J.C. Activity-dependent compartmentalized regulation of dendritic Ca2+ signaling in hippocampal interneurons. J. Neurosci., 2009, 29(14), 4658-4663.
[http://dx.doi.org/10.1523/JNEUROSCI.0493-09.2009] [PMID: 19357290]
[43]
Bengtson, C.P.; Bading, H. Nuclear calcium signaling. In: Synaptic Plasticity, Springer Vienna; , 2012; pp. 377-405.
[http://dx.doi.org/10.1007/978-3-7091-0932-8_17]
[44]
Vandael, D.H.; Marcantoni, A.; Mahapatra, S.; Caro, A.; Ruth, P.; Zuccotti, A.; Knipper, M.; Carbone, E. Ca(v)1.3 and BK channels for timing and regulating cell firing. Mol. Neurobiol., 2010, 42(3), 185-198.
[http://dx.doi.org/10.1007/s12035-010-8151-3] [PMID: 21088933]
[45]
Abele, A.E.; Scholz, K.P.; Scholz, W.K.; Miller, R.J. Excitotoxicity induced by enhanced excitatory neurotransmission in cultured hippocampal pyramidal neurons. Neuron, 1990, 4(3), 413-419.
[http://dx.doi.org/10.1016/0896-6273(90)90053-I] [PMID: 1690567]
[46]
Choi, D.W. Excitotoxic cell death. J. Neurobiol., 1992, 23(9), 1261-1276.
[http://dx.doi.org/10.1002/neu.480230915] [PMID: 1361523]
[47]
McLeod, J.R., Jr; Shen, M.; Kim, D.J.; Thayer, S.A. Neurotoxicity mediated by aberrant patterns of synaptic activity between rat hippocampal neurons in culture. J. Neurophysiol., 1998, 80(5), 2688-2698.
[http://dx.doi.org/10.1152/jn.1998.80.5.2688] [PMID: 9819273]
[48]
Rowland, M.J.; Hadjipavlou, G.; Westbrook, J.; Pattinson, K.T.S. Delayed cerebral ischaemia after subarachnoid haemorrhage. Surv. Anesthesiol., 2013, 57(3), 119-120.
[http://dx.doi.org/10.1097/01.UC.0000428883.72053.4e]
[49]
Porter, N.M.; Thibault, O.; Thibault, V.; Chen, K-C.; Landfield, P.W. Calcium channel density and hippocampal cell death with age in long-term culture. J. Neurosci., 1997, 17(14), 5629-5639.
[http://dx.doi.org/10.1523/JNEUROSCI.17-14-05629.1997] [PMID: 9204944]
[50]
Brewer, L.D.; Thibault, O.; Staton, J.; Thibault, V.; Rogers, J.T.; Garcia-Ramos, G.; Kraner, S.; Landfield, P.W.; Porter, N.M. Increased vulnerability of hippocampal neurons with age in culture: temporal association with increases in NMDA receptor current, NR2A subunit expression and recruitment of L-type calcium channels. Brain Res., 2007, 1151, 20-31.
[http://dx.doi.org/10.1016/j.brainres.2007.03.020] [PMID: 17433272]
[51]
Surmeier, D.J. Calcium Homeostatasis and Mitochondrial Dysfunction in Dopaminergic Neurons of the Substantia Nigra; Defense Technical Information Center, 2010.
[52]
Gudala, K.; Kanukula, R.; Bansal, D. Reduced risk of parkinson’s disease in users of calcium channel blockers: A meta-analysis. Int. J. Chronic Dis., 2015, 2015 697404
[http://dx.doi.org/10.1155/2015/697404] [PMID: 26464872]
[53]
Shen, A.N.; Cummings, C.; Hoffman, D.; Pope, D.; Arnold, M.; Newland, M.C. Aging, motor function, and sensitivity to calcium channel blockers: An investigation using chronic methylmercury exposure. Behav. Brain Res., 2016, 315, 103-114.
[http://dx.doi.org/10.1016/j.bbr.2016.07.049] [PMID: 27481695]
[54]
Weiss, J.H.; Pike, C.J.; Cotman, C.W. Ca2+ channel blockers attenuate β-amyloid peptide toxicity to cortical neurons in culture. J. Neurochem., 1994, 62(1), 372-375.
[http://dx.doi.org/10.1046/j.1471-4159.1994.62010372.x] [PMID: 8263540]
[55]
Anekonda, T.S.; Quinn, J.F. Calcium channel blocking as a therapeutic strategy for Alzheimer’s disease: the case for isradipine. Biochim. Biophys. Acta, 2011, 1812(12), 1584-1590.
[http://dx.doi.org/10.1016/j.bbadis.2011.08.013] [PMID: 21925266]
[56]
Kerchner, G.A.; Canzoniero, L.M.T.; Yu, S.P.; Ling, C.; Choi, D.W. Zn2+ current is mediated by voltage-gated Ca2+ channels and enhanced by extracellular acidity in mouse cortical neurones. J. Physiol., 2000, 528(Pt 1), 39-52.
[http://dx.doi.org/10.1111/j.1469-7793.2000.00039.x] [PMID: 11018104]
[57]
Frederickson, C.J.; Koh, J-Y.; Bush, A.I. The neurobiology of zinc in health and disease. Nat. Rev. Neurosci., 2005, 6(6), 449-462.
[http://dx.doi.org/10.1038/nrn1671] [PMID: 15891778]
[58]
Sensi, S.L.; Paoletti, P.; Bush, A.I.; Sekler, I. Zinc in the physiology and pathology of the CNS. Nat. Rev. Neurosci., 2009, 10(11), 780-791.
[http://dx.doi.org/10.1038/nrn2734] [PMID: 19826435]
[59]
Shuttleworth, C.W.; Weiss, J.H. Zinc: new clues to diverse roles in brain ischemia. Trends Pharmacol. Sci., 2011, 32(8), 480-486.
[http://dx.doi.org/10.1016/j.tips.2011.04.001] [PMID: 21621864]
[60]
Weiss, J.H.; Hartley, D.M.; Koh, J.Y.; Choi, D.W. AMPA receptor activation potentiates zinc neurotoxicity. Neuron, 1993, 10(1), 43-49.
[http://dx.doi.org/10.1016/0896-6273(93)90240-R] [PMID: 7678965]
[61]
Carter, R.E.; Aiba, I.; Dietz, R.M.; Sheline, C.T.; Shuttleworth, C.W. Spreading depression and related events are significant sources of neuronal Zn2+ release and accumulation. J. Cereb. Blood Flow Metab., 2010, 31(4), 1073-1084.
[PMID: 20978516]
[62]
Dietz, R.M.; Weiss, J.H.; Shuttleworth, C.W. Zn2+ influx is critical for some forms of spreading depression in brain slices. J. Neurosci., 2008, 28(32), 8014-8024.
[http://dx.doi.org/10.1523/JNEUROSCI.0765-08.2008] [PMID: 18685026]
[63]
Dietz, R.M.; Weiss, J.H.; Shuttleworth, C.W. Contributions of Ca2+ and Zn2+ to spreading depression-like events and neuronal injury. J. Neurochem., 2009, 109(Suppl. 1), 145-152.
[http://dx.doi.org/10.1111/j.1471-4159.2009.05853.x] [PMID: 19393021]
[64]
Richter, F.; Ebersberger, A.; Schaible, H.G. Blockade of voltage-gated calcium channels in rat inhibits repetitive cortical spreading depression. Neurosci. Lett., 2002, 334(2), 123-126.
[http://dx.doi.org/10.1016/S0304-3940(02)01120-5] [PMID: 12435487]
[65]
Attwell, D.; Buchan, A.M.; Charpak, S.; Lauritzen, M.; Macvicar, B.A.; Newman, E.A. Glial and neuronal control of brain blood flow. Nature, 2010, 468(7321), 232-243.
[http://dx.doi.org/10.1038/nature09613] [PMID: 21068832]
[66]
Latour, I.; Hamid, J.; Beedle, A.M.; Zamponi, G.W.; Macvicar, B.A. Expression of voltage-gated Ca2+ channel subtypes in cultured astrocytes. Glia, 2003, 41(4), 347-353.
[http://dx.doi.org/10.1002/glia.10162] [PMID: 12555202]
[67]
Koide, M.; Bonev, A.D.; Nelson, M.T.; Wellman, G.C. Inversion of neurovascular coupling by subarachnoid blood depends on large-conductance Ca2+-activated K+ (BK) channels. Proc. Natl. Acad. Sci. USA, 2012, 109(21), E1387-E1395.
[http://dx.doi.org/10.1073/pnas.1121359109] [PMID: 22547803]
[68]
Seidel, J.L.; Escartin, C.; Ayata, C.; Bonvento, G.; Shuttleworth, C.W. Multifaceted roles for astrocytes in spreading depolarization: A target for limiting spreading depolarization in acute brain injury? Glia, 2016, 64(1), 5-20.
[http://dx.doi.org/10.1002/glia.22824] [PMID: 26301517]
[69]
Hashioka, S.; Klegeris, A.; McGeer, P.L. Inhibition of human astrocyte and microglia neurotoxicity by calcium channel blockers. Neuropharmacology, 2012, 63(4), 685-691.
[http://dx.doi.org/10.1016/j.neuropharm.2012.05.033] [PMID: 22659089]
[70]
Sukhotinsky, I.; Dilekoz, E.; Wang, Y.; Qin, T.; Eikermann-Haerter, K.; Waeber, C.; Ayata, C. Chronic daily cortical spreading depressions suppress spreading depression susceptibility. Cephalalgia, 2011, 31(16), 1601-1608.
[http://dx.doi.org/10.1177/0333102411425865] [PMID: 22013142]
[71]
Seidel, J.L.; Faideau, M.; Aiba, I.; Pannasch, U.; Escartin, C.; Rouach, N.; Bonvento, G.; Shuttleworth, C.W. Ciliary neurotrophic factor (CNTF) activation of astrocytes decreases spreading depolarization susceptibility and increases potassium clearance. Glia, 2015, 63(1), 91-103.
[http://dx.doi.org/10.1002/glia.22735] [PMID: 25092804]
[72]
Cheli, V.T.; Santiago, G.D.A.; Smith, J.; Spreuer, V.; Murphy, G.G.; Paez, P.M. L-type voltage-operated calcium channels contribute to astrocyte activation In vitro. Glia, 2016, 64(8), 1396-1415.
[http://dx.doi.org/10.1002/glia.23013] [PMID: 27247164]
[73]
Kamouchi, M.; Kitazono, T.; Ago, T.; Wakisaka, M.; Ooboshi, H.; Ibayashi, S.; Iida, M. Calcium influx pathways in rat CNS pericytes. Brain Res. Mol. Brain Res., 2004, 126(2), 114-120.
[http://dx.doi.org/10.1016/j.molbrainres.2004.03.008] [PMID: 15249134]
[74]
Cheng, J.; Korte, N.; Nortley, R.; Sethi, H.; Tang, Y.; Attwell, D. Targeting pericytes for therapeutic approaches to neurological disorders. Acta Neuropathol., 2018, 136(4), 507-523.
[http://dx.doi.org/10.1007/s00401-018-1893-0] [PMID: 30097696]
[75]
Cai, W.; Liu, H.; Zhao, J.; Chen, L.Y.; Chen, J.; Lu, Z.; Hu, X. Pericytes in brain injury and repair after ischemic stroke. Transl. Stroke Res., 2017, 8(2), 107-121.
[http://dx.doi.org/10.1007/s12975-016-0504-4] [PMID: 27837475]
[76]
Espinosa-Parrilla, J.F.; Martínez-Moreno, M.; Gasull, X.; Mahy, N.; Rodríguez, M.J. The L-type voltage-gated calcium channel modulates microglial pro-inflammatory activity. Mol. Cell. Neurosci., 2015, 64, 104-115.
[http://dx.doi.org/10.1016/j.mcn.2014.12.004] [PMID: 25497271]
[77]
Li, Y.; Hu, X.; Liu, Y.; Bao, Y.; An, L. Nimodipine protects dopaminergic neurons against inflammation-mediated degeneration through inhibition of microglial activation. Neuropharmacology, 2009, 56(3), 580-589.
[http://dx.doi.org/10.1016/j.neuropharm.2008.10.016] [PMID: 19049811]
[78]
Sanchez, A.B.; Medders, K.E.; Maung, R.; Sánchez-Pavón, P.; Ojeda-Juárez, D.; Kaul, M. CXCL12-induced neurotoxicity critically depends on NMDA receptor-gated and L-type Ca2+ channels upstream of p38 MAPK. J. Neuroinflammation, 2016, 13(1), 252.
[http://dx.doi.org/10.1186/s12974-016-0724-2] [PMID: 27664068]
[79]
Daschil, N.; Humpel, C. Nifedipine and nimodipine protect dopaminergic substantia nigra neurons against axotomy-induced cell death in rat vibrosections via modulating inflammatory responses. Brain Res., 2014, 1581, 1-11.
[http://dx.doi.org/10.1016/j.brainres.2014.07.014] [PMID: 25038562]
[80]
Hopp, S.C.; D’Angelo, H.M.; Royer, S.E.; Kaercher, R.M.; Crockett, A.M.; Adzovic, L.; Wenk, G.L. Calcium dysregulation via L-type voltage-dependent calcium channels and ryanodine receptors underlies memory deficits and synaptic dysfunction during chronic neuroinflammation. J. Neuroinflammation, 2015, 12(1), 56.
[http://dx.doi.org/10.1186/s12974-015-0262-3] [PMID: 25888781]
[81]
Sanz, J.M.; Chiozzi, P.; Colaianna, M.; Zotti, M.; Ferrari, D.; Trabace, L.; Zuliani, G.; Di Virgilio, F. Nimodipine inhibits IL-1β release stimulated by amyloid β from microglia. Br. J. Pharmacol., 2012, 167(8), 1702-1711.
[http://dx.doi.org/10.1111/j.1476-5381.2012.02112.x] [PMID: 22831460]
[82]
Shibata, M.; Suzuki, N. Exploring the role of microglia in cortical spreading depression in neurological disease. J. Cereb. Blood Flow Metab., 2017, 37(4), 1182-1191.
[http://dx.doi.org/10.1177/0271678X17690537] [PMID: 28155572]
[83]
Allen, G.S.; Ahn, H.S.; Preziosi, T.J.; Battye, R.; Boone, S.C.; Boone, S.C.; Chou, S.N.; Kelly, D.L.; Weir, B.K.; Crabbe, R.A.; Lavik, P.J.; Rosenbloom, S.B.; Dorsey, F.C.; Ingram, C.R.; Mellits, D.E.; Bertsch, L.A.; Boisvert, D.P.; Hundley, M.B.; Johnson, R.K.; Strom, J.A.; Transou, C.R. Cerebral arterial spasm--a controlled trial of nimodipine in patients with subarachnoid hemorrhage. N. Engl. J. Med., 1983, 308(11), 619-624.
[http://dx.doi.org/10.1056/NEJM198303173081103] [PMID: 6338383]
[84]
Philippon, J.; Grob, R.; Dagreou, F.; Guggiari, M.; Rivierez, M.; Viars, P. Prevention of vasospasm in subarachnoid haemorrhage. A controlled study with nimodipine. Acta Neurochir. (Wien), 1986, 82(3-4), 110-114.
[http://dx.doi.org/10.1007/BF01456369] [PMID: 3538789]
[85]
Pickard, J.D.; Murray, G.D.; Illingworth, R.; Shaw, M.D.; Teasdale, G.M.; Foy, P.M.; Humphrey, P.R.; Lang, D.A.; Nelson, R.; Richards, P. Effect of oral nimodipine on cerebral infarction and outcome after subarachnoid haemorrhage: British aneurysm nimodipine trial. BMJ, 1989, 298(6674), 636-642.
[http://dx.doi.org/10.1136/bmj.298.6674.636] [PMID: 2496789]
[86]
Allen, G.S. Role of calcium antagonists in cerebral arterial spasm. Am. J. Cardiol., 1985, 55(3), 149B-153B.
[http://dx.doi.org/10.1016/0002-9149(85)90624-1] [PMID: 3881907]
[87]
Neil-Dwyer, G.; Mee, E.; Dorrance, D.; Lowe, D. Early intervention with nimodipine in subarachnoid haemorrhage. Eur. Heart J., 1987, 8(Suppl. K), 41-47.
[http://dx.doi.org/10.1093/eurheartj/8.suppl_K.41]
[88]
Jan, M.; Buchheit, F.; Tremoulet, M. Therapeutic trial of intravenous nimodipine in patients with established cerebral vasospasm after rupture of intracranial aneurysms. Neurosurgery, 1988, 23(2), 154-157.
[http://dx.doi.org/10.1227/00006123-198808000-00004] [PMID: 3054619]
[89]
Ohman, J.; Heiskanen, O. Effect of nimodipine on the outcome of patients after aneurysmal subarachnoid hemorrhage and surgery. J. Neurosurg., 1988, 69(5), 683-686.
[http://dx.doi.org/10.3171/jns.1988.69.5.0683] [PMID: 3054010]
[90]
Zhang, S.; Chang, A.M.; Li, C.F.; Li, Z.J.; Yin, Z.J.; Zhao, X.; Liang, S.L. Mechanism of the therapeutic effect of anisodamine in disseminated intravascular coagulation: study of platelet adhesion and aggregation, malondialdehyde, thromboxane B2, 6-keto-prostaglandin F1 alpha, and microcirculation. Exp. Hematol., 1987, 15(1), 65-71.
[PMID: 3780890]
[91]
Juvela, S.; Kaste, M.; Hillbom, M. Effect of nimodipine on platelet function in patients with subarachnoid hemorrhage. Stroke, 1990, 21(9), 1283-1288.
[http://dx.doi.org/10.1161/01.STR.21.9.1283] [PMID: 2396264]
[92]
Roine, R.O.; Kaste, M.; Kinnunen, A.; Nikki, P.; Sarna, S.; Kajaste, S. Nimodipine after resuscitation from out-of-hospital ventricular fibrillation. A placebo-controlled, double-blind, randomized trial. JAMA, 1990, 264(24), 3171-3177.
[http://dx.doi.org/10.1001/jama.1990.03450240073043] [PMID: 2255026]
[93]
Dorhout, M.S.M.; Rinkel, G.J.E.; Feigin, V.L.; Algra, A.; van den Bergh, W.M.; Vermeulen, M.; van Gijn, J. Calcium antagonists for aneurysmal subarachnoid haemorrhage. Cochrane Database Syst. Rev., 2007, (3)CD000277
[PMID: 17636626]
[94]
Kronvall, E.; Undrén, P.; Romner, B.; Säveland, H.; Cronqvist, M.; Nilsson, O.G. Nimodipine in aneurysmal subarachnoid hemorrhage: a randomized study of intravenous or peroral administration. J. Neurosurg., 2009, 110(1), 58-63.
[http://dx.doi.org/10.3171/2008.7.JNS08178] [PMID: 18847340]
[95]
Soppi, V.; Karamanakos, P.N.; Koivisto, T.; Kurki, M.I.; Vanninen, R.; Jaaskelainen, J.E.; Rinne, J. A randomized outcome study of enteral versus intravenous nimodipine in 171 patients after acute aneurysmal subarachnoid hemorrhage. World Neurosurg., 2012, 78(1-2), 101-109.
[http://dx.doi.org/10.1016/j.wneu.2011.09.030] [PMID: 22120252]
[96]
Hockel, K.; Diedler, J.; Steiner, J.; Birkenhauer, U.; Danz, S.; Ernemann, U.; Schuhmann, M.U. Long-term, continuous intra-arterial nimodipine treatment of severe vasospasm after aneurysmal subarachnoid hemorrhage. World Neurosurg., 2016, 88, 104-112.
[http://dx.doi.org/10.1016/j.wneu.2015.11.081] [PMID: 26732964]
[97]
Hänggi, D.; Etminan, N.; Aldrich, F.; Steiger, H.J.; Mayer, S.A.; Diringer, M.N.; Hoh, B.L.; Mocco, J.; Faleck, H.J.; Macdonald, R.L. Investigators, N. Randomized, open-label, phase 1/2a study to determine the maximum tolerated dose of intraventricular sustained release nimodipine for subarachnoid hemorrhage (NEWTON [nimodipine microparticles to enhance recovery while reducing toxicity after subarachnoid hemorrhagE]). Stroke, 2017, 48(1), 145-151.
[http://dx.doi.org/10.1161/STROKEAHA.116.014250] [PMID: 27932607]
[98]
Zhang, J.; Yang, J.; Zhang, C.; Jiang, X.; Zhou, H.; Liu, M. Calcium antagonists for acute ischemic stroke. Cochrane Database Syst. Rev., 2012, (5)CD001928
[PMID: 22592678]
[99]
Gelmers, H.J. The effects of nimodipine on the clinical course of patients with acute ischemic stroke. Acta Neurol. Scand., 1984, 69(4), 232-239.
[http://dx.doi.org/10.1111/j.1600-0404.1984.tb07806.x] [PMID: 6377803]
[100]
Gelmers, H.J.; Gorter, K.; de Weerdt, C.J.; Wiezer, H.J. A controlled trial of nimodipine in acute ischemic stroke. N. Engl. J. Med., 1988, 318(4), 203-207.
[http://dx.doi.org/10.1056/NEJM198801283180402] [PMID: 3275894]
[101]
Paci, A.; Ottaviano, P.; Trenta, A.; Iannone, G.; De Santis, L.; Lancia, G.; Moschini, E.; Carosi, M.; Amigoni, S.; Caresia, L. Nimodipine in acute ischemic stroke: a double-blind controlled study. Acta Neurol. Scand., 1989, 80(4), 282-286.
[http://dx.doi.org/10.1111/j.1600-0404.1989.tb03879.x] [PMID: 2683557]
[102]
Martínez-Vila, E.; Guillén, F.; Villanueva, J.A.; Matías-Guiu, J.; Bigorra, J.; Gil, P.; Carbonell, A.; Martínez-Lage, J.M. Placebo-controlled trial of nimodipine in the treatment of acute ischemic cerebral infarction. Stroke, 1990, 21(7), 1023-1028.
[http://dx.doi.org/10.1161/01.STR.21.7.1023] [PMID: 2195714]
[103]
Sze, K.H.; Sim, T.C.; Wong, E.; Cheng, S.; Woo, J. Effect of nimodipine on memory after cerebral infarction. Acta Neurol. Scand., 1998, 97(6), 386-392.
[http://dx.doi.org/10.1111/j.1600-0404.1998.tb05971.x] [PMID: 9669472]
[104]
Hakim, A.M.; Evans, A.C.; Berger, L.; Kuwabara, H.; Worsley, K.; Marchal, G.; Biel, C.; Pokrupa, R.; Diksic, M.; Meyer, E. The effect of nimodipine on the evolution of human cerebral infarction studied by PET. J. Cereb. Blood Flow Metab., 1989, 9(4), 523-534.
[http://dx.doi.org/10.1038/jcbfm.1989.76] [PMID: 2661584]
[105]
Bogousslavsky, J.; Regli, F.; Zumstein, V.; Köbberling, W. Double-blind study of nimodipine in non-severe stroke. Eur. Neurol., 1990, 30(1), 23-26.
[http://dx.doi.org/10.1159/000116620] [PMID: 2404768]
[106]
Rosselli, A.; Landini, G.; Castagnoli, A.; Vannucchi, L.; Mugnaini, C.; Calacoci, S.; Regoli, G.; Francesconi, A.; Turchi, A.; Agostino, I. The nimodipine therapy of acute focal cerebral ischemia (minor stroke). A clinical study with an assessment of regional cerebral blood flow by SPECT. Recenti Prog. Med., 1992, 83(2), 85-88.
[PMID: 1502426]
[107]
Clinical trial of nimodipine in acute ischemic stroke. Stroke, 1992, 23(1), 3-8.
[http://dx.doi.org/10.1161/01.STR.23.1.3] [PMID: 1731418]
[108]
Horn, J.; de Haan, R.J.; Vermeulen, M.; Limburg, M. Very Early Nimodipine Use in Stroke (VENUS): a randomized, double-blind, placebo-controlled trial. Stroke, 2001, 32(2), 461-465.
[http://dx.doi.org/10.1161/01.STR.32.2.461] [PMID: 11157183]
[109]
Kaste, M.; Fogelholm, R.; Erilä, T.; Palomäki, H.; Murros, K.; Rissanen, A.; Sarna, S. A randomized, double-blind, placebo-controlled trial of nimodipine in acute ischemic hemispheric stroke. Stroke, 1994, 25(7), 1348-1353.
[http://dx.doi.org/10.1161/01.STR.25.7.1348] [PMID: 8023348]
[110]
Nag, D.; Garg, R.K.; Varma, M. A randomized double-blind controlled study of nimodipine in acute cerebral ischemic stroke. Indian J. Physiol. Pharmacol., 1998, 42(4), 555-558.
[PMID: 10874361]
[111]
Trust Study Group. Randomised, double-blind, placebo-controlled trial of nimodipine in acute stroke. Lancet, 1990, 336(8725), 1205-1209.
[http://dx.doi.org/10.1016/0140-6736(90)92829-7] [PMID: 1978069]
[112]
Fogelholm, R.; Erilä, T.; Palomäki, H.; Murros, K.; Kaste, M. Effect of nimodipine on final infarct volume after acute ischemic stroke. Cerebrovasc. Dis., 2000, 10(3), 189-193.
[http://dx.doi.org/10.1159/000016055] [PMID: 10773644]
[113]
Fogelholm, R.; Palomäki, H.; Erilä, T.; Rissanen, A.; Kaste, M. Blood pressure, nimodipine, and outcome of ischemic stroke. Acta Neurol. Scand., 2004, 109(3), 200-204.
[http://dx.doi.org/10.1034/j.1600-0404.2003.00202.x] [PMID: 14763958]
[114]
Ahmed, N.; Näsman, P.; Wahlgren, N.G. Effect of intravenous nimodipine on blood pressure and outcome after acute stroke. Stroke, 2000, 31(6), 1250-1255.
[http://dx.doi.org/10.1161/01.STR.31.6.1250] [PMID: 10835440]
[115]
Wang, P.; Wang, Y.; Feng, T.; Zhao, X.; Zhou, Y.; Wang, Y.; Shi, W.; Ju, Y. Rationale and design of a double-blind, placebo-controlled, randomized trial to evaluate the safety and efficacy of nimodipine in preventing cognitive impairment in ischemic cerebrovascular events (NICE). BMC Neurol., 2012, 12(1), 88.
[http://dx.doi.org/10.1186/1471-2377-12-88] [PMID: 22950711]
[116]
Langham, J.; Goldfrad, C.; Teasdale, G.; Shaw, D.; Rowan, K. Calcium channel blockers for acute traumatic brain injury. Cochrane Database Syst. Rev., 2003, (4) CD000565
[http://dx.doi.org/10.1002/14651858.CD000565] [PMID: 14583925]
[117]
Teasdale, G.; Bailey, I.; Bell, A.; Gray, J.; Gullan, R.; Heiskanan, U.; Marks, P.V.; Marsh, H.; Mendelow, A.D.; Murray, G. The effect of nimodipine on outcome after head injury: a prospective randomised control trial. Acta Neurochir. Suppl. (Wien), 1990, 51, 315-316.
[http://dx.doi.org/10.1007/978-3-7091-9115-6_106] [PMID: 2089926]
[118]
The European Study Group. A multicenter trial of the efficacy of nimodipine on outcome after severe head injury. J. Neurosurg., 1994, 80(5), 797-804.
[http://dx.doi.org/10.3171/jns.1994.80.5.0797] [PMID: 8169617]
[119]
Murray, G.D.; Teasdale, G.M.; Schmitz, H. Nimodipine in traumatic subarachnoid haemorrhage: a re-analysis of the HIT I and HIT II trials. Acta Neurochir. (Wien), 1996, 138(10), 1163-1167.
[http://dx.doi.org/10.1007/BF01809745] [PMID: 8955434]
[120]
Harders, A.; Kakarieka, A.; Braakman, R. Traumatic subarachnoid hemorrhage and its treatment with nimodipine. German tSAH Study Group. J. Neurosurg., 1996, 85(1), 82-89.
[http://dx.doi.org/10.3171/jns.1996.85.1.0082] [PMID: 8683286]
[121]
Pillai, S.V.; Kolluri, V.R.; Mohanty, A.; Chandramouli, B.A. Evaluation of nimodipine in the treatment of severe diffuse head injury: a double-blind placebo-controlled trial. Neurol. India, 2003, 51(3), 361-363.
[PMID: 14652439]
[122]
Vergouwen, M.D.; Vermeulen, M.; Roos, Y.B. Effect of nimodipine on outcome in patients with traumatic subarachnoid haemorrhage: a systematic review. Lancet Neurol., 2006, 5(12), 1029-1032.
[http://dx.doi.org/10.1016/S1474-4422(06)70582-8] [PMID: 17110283]
[123]
Hartings, J.A.; Bullock, M.R.; Okonkwo, D.O.; Murray, L.S.; Murray, G.D.; Fabricius, M.; Maas, A.I.; Woitzik, J.; Sakowitz, O.; Mathern, B.; Roozenbeek, B.; Lingsma, H.; Dreier, J.P.; Puccio, A.M.; Shutter, L.A.; Pahl, C.; Strong, A.J. Spreading depolarisations and outcome after traumatic brain injury: a prospective observational study. Lancet Neurol., 2011, 10(12), 1058-1064.
[http://dx.doi.org/10.1016/S1474-4422(11)70243-5] [PMID: 22056157]
[124]
Bussone, G.; Baldini, S.; D’Andrea, G.; Cananzi, A.; Frediani, F.; Caresia, L.; Ferro Milone, F.; Boiardi, A. Nimodipine versus flunarizine in common migraine: a controlled pilot trial. Headache, 1987, 27(2), 76-79.
[http://dx.doi.org/10.1111/j.1526-4610.1987.hed2702076.x] [PMID: 3553069]
[125]
Gelmers, H.J. Nimodipine, a new calcium antagonist, in the prophylactic treatment of migraine. Headache, 1983, 23(3), 106-109.
[http://dx.doi.org/10.1111/j.1526-4610.1983.hed2303106.x] [PMID: 6347970]
[126]
Havanka-Kanniainen, H.; Hokkanen, E.; Myllylä, V.V. Efficacy of nimodipine in the prophylaxis of migraine. Cephalalgia, 1985, 5(1), 39-43.
[http://dx.doi.org/10.1046/j.1468-2982.1985.0501039.x] [PMID: 3886153]
[127]
Havanka-Kanniainen, H.; Hokkanen, E.; Myllylä, V.V. Efficacy of nimodipine in comparison with pizotifen in the prophylaxis of migraine. Cephalalgia, 1987, 7(1), 7-13.
[http://dx.doi.org/10.1046/j.1468-2982.1987.0701007.x] [PMID: 3555838]
[128]
Jensen, K.; Tfelt-Hansen, P.; Lauritzen, M.; Olesen, J. Clinical trial of nimodipine for single attacks of classic migraine. Cephalalgia, 1985, 5(3), 125-131.
[http://dx.doi.org/10.1046/j.1468-2982.1985.0503125.x] [PMID: 3899368]
[129]
European Study Group. European multicenter trial of nimodipine in the prophylaxis of common migraine (migraine without aura). Headache, 1989, 29(10), 633-638.
[http://dx.doi.org/10.1111/j.1526-4610.1989.hed2910633.x] [PMID: 2693405]
[130]
European Study Group. European multicenter trial of nimodipine in the prophylaxis of classic migraine (migraine with aura). Headache, 1989, 29(10), 639-642.
[http://dx.doi.org/10.1111/j.1526-4610.1989.hed2910639.x] [PMID: 2693406]
[131]
Battistella, P.A.; Ruffilli, R.; Moro, R.; Fabiani, M.; Bertoli, S.; Antolini, A.; Zacchello, F. A placebo-controlled crossover trial of nimodipine in pediatric migraine. Headache, 1990, 30(5), 264-268.
[http://dx.doi.org/10.1111/j.1526-4610.1990.hed3005264.x] [PMID: 2191938]
[132]
Forsman, M.; Aarseth, H.P.; Nordby, H.K.; Skulberg, A.; Steen, P.A. Effects of nimodipine on cerebral blood flow and cerebrospinal fluid pressure after cardiac arrest: correlation with neurologic outcome. Anesth. Analg., 1989, 68(4), 436-443.
[http://dx.doi.org/10.1213/00000539-198904000-00003] [PMID: 2929976]
[133]
Gueugniaud, P-Y.; Gaussorgues, P.; Garcia-Darennes, F.; Bancalari, G.; Roux, H.; Robert, D.; Petit, P. Early effects of nimodipine on intracranial and cerebral perfusion pressures in cerebral anoxia after out-of-hospital cardiac arrest. Resuscitation, 1990, 20(3), 203-212.
[http://dx.doi.org/10.1016/0300-9572(90)90003-W] [PMID: 1965344]
[134]
Legault, C.; Furberg, C.D.; Wagenknecht, L.E.; Rogers, A.T.; Stump, D.A.; Coker, L.; Troost, B.T.; Hammon, J.W. Nimodipine neuroprotection in cardiac valve replacement: report of an early terminated trial. Stroke, 1996, 27(4), 593-598.
[http://dx.doi.org/10.1161/01.STR.27.4.593] [PMID: 8614913]
[135]
Ban, T.A.; Morey, L.; Aguglia, E.; Azzarelli, O.; Balsano, F.; Marigliano, V.; Caglieris, N.; Sterlicchio, M.; Capurso, A.; Tomasi, N.A.; Crepaldi, G.; Volpe, D.; Palmieri, G.; Ambrosi, G.; Polli, E.; Cortellaro, M.; Zanussi, C.; Froldi, M. Nimodipine in the treatment of old age dementias. Prog. Neuropsychopharmacol. Biol. Psychiatry, 1990, 14(4), 525-551.
[http://dx.doi.org/10.1016/0278-5846(90)90005-2] [PMID: 2236581]
[136]
Cohen, M.R.; Swartz, C.M. Absence of nimodipine premedication effect on memory after electroconvulsive therapy. Neuropsychobiology, 1990-1991, 24(4), 165-168.
[http://dx.doi.org/10.1159/000119480] [PMID: 2135706]
[137]
Tollefson, G.D. Short-term effects of the calcium channel blocker nimodipine (Bay-e-9736) in the management of primary degenerative dementia. Biol. Psychiatry, 1990, 27(10), 1133-1142.
[http://dx.doi.org/10.1016/0006-3223(90)90050-C] [PMID: 2187540]
[138]
Parnetti, L.; Senin, U.; Carosi, M.; Baasch, H. Mental deterioration in old age: results of two multicenter, clinical trials with nimodipine. Clin. Ther., 1993, 15(2), 394-406.
[PMID: 8519047]
[139]
Pantoni, L.; del Ser, T.; Soglian, A.G.; Amigoni, S.; Spadari, G.; Binelli, D.; Inzitari, D. Efficacy and safety of nimodipine in subcortical vascular dementia: a randomized placebo-controlled trial. Stroke, 2005, 36(3), 619-624.
[http://dx.doi.org/10.1161/01.STR.0000155686.73908.3e] [PMID: 15692125]
[140]
López-Arrieta, J.M.; Birks, J. Nimodipine for primary degenerative, mixed and vascular dementia. Cochrane Database Syst. Rev., 2002, (3)CD000147
[PMID: 12137606]
[141]
Miller, R.G.; Shepherd, R.; Dao, H.; Khramstov, A.; Mendoza, M.; Graves, J.; Smith, S. Controlled trial of nimodipine in amyotrophic lateral sclerosis. Neuromuscul. Disord., 1996, 6(2), 101-104.
[http://dx.doi.org/10.1016/0960-8966(95)00024-0] [PMID: 8664560]
[142]
Ziv, I.; Achiron, A.; Djaldetti, R.; Abraham, M.; Melamed, E. Can nimodipine affect progression of motor neuron disease? A double-blind pilot study. Clin. Neuropharmacol., 1994, 17(5), 423-428.
[http://dx.doi.org/10.1097/00002826-199410000-00004] [PMID: 9316691]
[143]
Cassidy, J.; Paul, J.; Soukop, M.; Habeshaw, T.; Reed, N.S.; Parkin, D.; Kaye, S.B. Clinical trials of nimodipine as a potential neuroprotector in ovarian cancer patients treated with cisplatin. Cancer Chemother. Pharmacol., 1998, 41(2), 161-166.
[http://dx.doi.org/10.1007/s002800050723] [PMID: 9443630]
[144]
Navia, B.A.; Dafni, U.; Simpson, D.; Tucker, T.; Singer, E.; McArthur, J.C.; Yiannoutsos, C.; Zaborski, L.; Lipton, S.A. A phase I/II trial of nimodipine for HIV-related neurologic complications. Neurology, 1998, 51(1), 221-228.
[http://dx.doi.org/10.1212/WNL.51.1.221] [PMID: 9674806]
[145]
Taragano, F.E.; Allegri, R.; Vicario, A.; Bagnatti, P.; Lyketsos, C.G. A double blind, randomized clinical trial assessing the efficacy and safety of augmenting standard antidepressant therapy with nimodipine in the treatment of ‘vascular depression’. Int. J. Geriatr. Psychiatry, 2001, 16(3), 254-260.
[http://dx.doi.org/10.1002/gps.340] [PMID: 11288158]
[146]
Brunet, G.; Cerlich, B.; Robert, P.; Dumas, S.; Souetre, E.; Darcourt, G. Open trial of a calcium antagonist, nimodipine, in acute mania. Clin. Neuropharmacol., 1990, 13(3), 224-228.
[http://dx.doi.org/10.1097/00002826-199006000-00004] [PMID: 2192795]
[147]
Banger, M.; Benkert, O.; Röschke, J.; Herth, T.; Hebenstreit, M.; Philipp, M.; Aldenhoff, J.B. Nimodipine in acute alcohol withdrawal state. J. Psychiatr. Res., 1992, 26(2), 117-123.
[http://dx.doi.org/10.1016/0022-3956(92)90003-7] [PMID: 1613678]
[148]
Jiménez-Lerma, J.M.; Landabaso, M.; Iraurgi, L.; Calle, R.; Sanz, J.; Gutiérrez-Fraile, M. Nimodipine in opiate detoxification: a controlled trial. Addiction, 2002, 97(7), 819-824.
[http://dx.doi.org/10.1046/j.1360-0443.2002.00196.x] [PMID: 12133120]
[149]
Rosse, R.B.; Alim, T.N.; Fay-McCarthy, M.; Collins, J.P., Jr; Vocci, F.J., Jr; Lindquist, T.; Jentgen, C.; Hess, A.L.; Deutsch, S.I. Nimodipine pharmacotherapeutic adjuvant therapy for inpatient treatment of cocaine dependence. Clin. Neuropharmacol., 1994, 17(4), 348-358.
[http://dx.doi.org/10.1097/00002826-199408000-00007] [PMID: 9316683]
[150]
Pazzaglia, P.J.; Post, R.M.; Ketter, T.A.; George, M.S.; Marangell, L.B. Preliminary controlled trial of nimodipine in ultra-rapid cycling affective dysregulation. Psychiatry Res., 1993, 49(3), 257-272.
[http://dx.doi.org/10.1016/0165-1781(93)90066-P] [PMID: 8177920]
[151]
Biary, N.; Bahou, Y.; Sofi, M.A.; Thomas, W.; al Deeb, S.M. The effect of nimodipine on essential tremor. Neurology, 1995, 45(8), 1523-1525.
[http://dx.doi.org/10.1212/WNL.45.8.1523] [PMID: 7644052]
[152]
Lisbeth, M.; Consuelo, P.; Glenda, C.; Elena, C.; Carlos, R.J.; Alejandro, R.; Maria, G-Y. Evaluation of the effect of nimodipine o.d. (extended release) vs nimodipine t.i.d. in the treatment of peripheral vertigo. Curr. Drug Deliv., 2013, 10(3), 343-347.
[http://dx.doi.org/10.2174/1567201811310030011] [PMID: 23808594]
[153]
Santillán, R.; Hurlé, M.A.; Armijo, J.A.; de los Mozos, R.; Flórez, J. Nimodipine-enhanced opiate analgesia in cancer patients requiring morphine dose escalation: a double-blind, placebo-controlled study. Pain, 1998, 76(1-2), 17-26.
[http://dx.doi.org/10.1016/S0304-3959(98)00019-0] [PMID: 9696455]
[154]
Larkin, J.G.; McKee, P.J.; Blacklaw, J.; Thompson, G.G.; Morgan, I.C.; Brodie, M.J. Nimodipine in refractory epilepsy: a placebo-controlled, add-on study. Epilepsy Res., 1991, 9(1), 71-77.
[http://dx.doi.org/10.1016/0920-1211(91)90049-L] [PMID: 1909241]
[155]
Meyer, F.B.; Cascino, G.D.; Whisnant, J.P.; Sharbrough, F.W.; Ivnik, R.J.; Gorman, D.A.; Windschitl, W.L.; So, E.L.; O’Fallon, W.M. Nimodipine as an add-on therapy for intractable epilepsy. Mayo Clin. Proc., 1995, 70(7), 623-627.
[http://dx.doi.org/10.4065/70.7.623] [PMID: 7791383]
[156]
Scheller, C.; Wienke, A.; Tatagiba, M.; Gharabaghi, A.; Ramina, K.F.; Ganslandt, O.; Bischoff, B.; Zenk, J.; Engelhorn, T.; Matthies, C.; Westermaier, T.; Antoniadis, G.; Pedro, M.T.; Rohde, V.; von Eckardstein, K.; Kretschmer, T.; Kornhuber, M.; Steighardt, J.; Richter, M.; Barker, F.G., II; Strauss, C. Prophylactic nimodipine treatment for cochlear and facial nerve preservation after vestibular schwannoma surgery: a randomized multicenter Phase III trial. J. Neurosurg., 2016, 124(3), 657-664.
[http://dx.doi.org/10.3171/2015.1.JNS142001] [PMID: 26274985]
[157]
Strauss, C.; Bischoff, B.; Neu, M.; Berg, M.; Fahlbusch, R.; Romstöck, J. Vasoactive treatment for hearing preservation in acoustic neuroma surgery. J. Neurosurg., 2001, 95(5), 771-777.
[http://dx.doi.org/10.3171/jns.2001.95.5.0771] [PMID: 11702866]
[158]
Krischek, B.; Kasuya, H.; Onda, H.; Hori, T. Nicardipine prolonged-release implants for preventing cerebral vasospasm after subarachnoid hemorrhage: effect and outcome in the first 100 patients. Neurol. Med. Chir. (Tokyo), 2007, 47(9), 389-394.
[http://dx.doi.org/10.2176/nmc.47.389] [PMID: 17895611]
[159]
Barth, M.; Capelle, H-H.; Weidauer, S.; Weiss, C.; Münch, E.; Thomé, C.; Luecke, T.; Schmiedek, P.; Kasuya, H.; Vajkoczy, P. Effect of nicardipine prolonged-release implants on cerebral vasospasm and clinical outcome after severe aneurysmal subarachnoid hemorrhage: a prospective, randomized, double-blind phase IIa study. Stroke, 2007, 38(2), 330-336.
[http://dx.doi.org/10.1161/01.STR.0000254601.74596.0f] [PMID: 17185636]
[160]
Etminan, N.; Macdonald, R.L.; Davis, C.; Burton, K.; Steiger, H-J.; Hänggi, D. Intrathecal application of the nimodipine slow-release microparticle system EG-1962 for prevention of delayed cerebral ischemia and improvement of outcome after aneurysmal subarachnoid hemorrhage. Neurovascular Events After Subarachnoid Hemorrhage; Springer International Publishing, 2014, pp. 281-286.
[161]
Hänggi, D.; Etminan, N.; Steiger, H.J.; Johnson, M.; Peet, M.M.; Tice, T.; Burton, K.; Hudson, B.; Turner, M.; Stella, A.; Heshmati, P.; Davis, C.; Faleck, H.J.; Macdonald, R.L.; Site-Specific, A. A site-specific, sustained-release drug delivery system for aneurysmal subarachnoid hemorrhage. Neurotherapeutics, 2016, 13(2), 439-449.
[http://dx.doi.org/10.1007/s13311-016-0424-8] [PMID: 26935204]
[162]
Hanggi, D.; Etminan, N.; Mayer, S.A.; Aldrich, E.F.; Diringer, M.N.; Schmutzhard, E.; Faleck, H.J.; Ng, D.; Saville, B.R.; Macdonald, R.L.; Investigators, N. Clinical Trial Protocol: Phase 3, Multicenter, Randomized, Double-Blind, Placebo-Controlled, Parallel-Group, Efficacy, and Safety Study Comparing EG-1962 to Standard of Care Oral Nimodipine in Adults with Aneurysmal Subarachnoid Hemorrhage. Neurocrit. Care, 2018. [NEWTON-2 (Nimodipine Microparticles to Enhance Recovery While Reducing TOxicity After SubarachNoid Hemorrhage)].
[PMID: 30014184]
[163]
Janovák, L.; Turcsányi, Á.; Bozó, É.; Deák, Á.; Mérai, L.; Sebők, D.; Juhász, Á.; Csapó, E.; Abdelghafour, M.M.; Farkas, E.; Dékány, I.; Bari, F. Preparation of novel tissue acidosis-responsive chitosan drug nanoparticles: Characterization and in vitro release properties of Ca2+ channel blocker nimodipine drug molecules. Eur. J. Pharm. Sci., 2018, 123, 79-88.
[http://dx.doi.org/10.1016/j.ejps.2018.07.031] [PMID: 30026092]


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