Potential mechanisms of sudden unexpected death in epilepsy

Epilepsy and Behavior

Volumn 26, Issue 3, 2013, Pages 410-414

  Tolstykh, Gleb P ^a,b,c   Cavazos, José E ^a,b,c,d  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^c Mays Cancer Center at UT Health San Antonio   (United States)

^d SOUTH TEXAS VETERANS HEALTH CARE SYSTEM   (United States)

Author keywords

KCNK channels; Neuron loss; NTS; Nucleus of the solitary tract; SUDEP

Indexed keywords

KAINIC ACID; POTASSIUM CHANNEL KCNQ;

AUTONOMIC NERVOUS SYSTEM; BREATHING; CARDIOVASCULAR REFLEX; CARDIOVASCULAR SYSTEM; CELL LOSS; CHEMORECEPTOR REFLEX; CONVULSION; EPILEPSY; HEART ARREST; HEART RATE; HUMAN; NERVE CELL; NONHUMAN; OXYGEN SUPPLY; PRESSORECEPTOR REFLEX; REFLEX; RESPIRATION CONTROL; RESPIRATORY ARREST; RESPIRATORY SYSTEM; REVIEW; SOLITARY TRACT NUCLEUS; SUDDEN DEATH; VASCULAR RESISTANCE;

ANIMALS; AUTONOMIC NERVOUS SYSTEM DISEASES; CELL DEATH; DEATH, SUDDEN; DISEASE MODELS, ANIMAL; EPILEPSY; HUMANS; NEURONS; RATS; SOLITARY NUCLEUS;

EID: 84878422281     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2012.09.017     Document Type: Review

References (94)

1. Jaime S.C., Cavazos J.E., Tolstykh G.P. Neuronal loss in the NTS induced by KA-induced status epilepticus rats while sparing other brainstem nuclei - predisposition to SUDEP. Presentation 2011.
2. Zhang K., Tolstykh G.P., Sanchez R.M., et al. Chronic Cellular Hyperexcitability in Elderly Epileptic Rats with Spontaneous Seizures Induced by Kainic Acid Status Epilepticus while Young Adults. Aging Dis 2011, 2:332-338.
3. Sperling M.R. Sudden Unexplained Death in Epilepsy. Epilepsy Curr 2001, 1:21-23.
4. Jehi L., Najm I.M. Sudden unexpected death in epilepsy: impact, mechanisms, and prevention. Cleve Clin J Med 2008, 75(Suppl. 2):S66-S70.
5. Annegers J.F. United States perspective on definitions and classifications. Epilepsia 1997, 38:S9-S12.
6. Tomson T., Nashef L., Ryvlin P. Sudden unexpected death in epilepsy: current knowledge and future directions. Lancet Neurol 2008, 7:1021-1031.
7. Leestma J.E. Forensic considerations in sudden unexpected death in epilepsy. Epilepsia 1997, 38:S63-S66.
8. Nilsson L., Farahmand B.Y., Persson P.G., et al. Risk factors for sudden unexpected death in epilepsy: a case-control study. Lancet 1999, 353:888-893.
9. So E.L., Sam M.C., Lagerlund T.L. Postictal central apnea as a cause of SUDEP: evidence from near-SUDEP incident. Epilepsia 2000, 41:1494-1497.
10. Terrence C.F., Rao G.R., Perper J.A. Neurogenic pulmonary edema in unexpected, unexplained death of epileptic patients. Ann Neurol 1981, 9:458-464.
11. Nashef L., Walker F., Allen P., et al. Apnoea and bradycardia during epileptic seizures: relation to sudden death in epilepsy. J Neurol Neurosurg Psychiatry 1996, 60:297-300.
12. Bateman L.M., Li C.S., Seyal M. Ictal hypoxemia in localization-related epilepsy: analysis of incidence, severity and risk factors. Brain 2008, 131:3239-3245.
13. Bateman L.M., Spitz M., Seyal M. Ictal hypoventilation contributes to cardiac arrhythmia and SUDEP: report on two deaths in video-EEG-monitored patients. Epilepsia 2010, 51:916-920.
14. Szabo C.A., Knape K.D., Leland M.M., et al. Mortality in captive baboons with seizures: a new model for SUDEP?. Epilepsia 2009, 50:1995-1998.
15. Goodman J.H., Homan R.W., Crawford I.L. Kindled seizures elevate blood pressure and induce cardiac arrhythmias. Epilepsia 1990, 31:489-495.
16. Surges R., Scott C.A., Walker M.C. Enhanced QT shortening and persistent tachycardia after generalized seizures. Neurology 2010, 74:421-426.
17. Surges R., Taggart P., Sander J.W., et al. Too long or too short? New insights into abnormal cardiac repolarization in people with chronic epilepsy and its potential role in sudden unexpected death. Epilepsia 2010, 51:738-744.
18. Surges R., Walker M.C. Peri-ictal heart rates depend on seizure-type. Seizure 2010, 19:453.
19. Surges R., Adjei P., Kallis C., et al. Pathologic cardiac repolarization in pharmacoresistant epilepsy and its potential role in sudden unexpected death in epilepsy: a case-control study. Epilepsia 2010, 51:233-242.
20. Neufeld G., Lazar J.M., Chari G., et al. Cardiac repolarization indices in epilepsy patients. Cardiology 2009, 114:255-260.
21. Brotherstone R., Blackhall B., McLellan A. Lengthening of corrected QT during epileptic seizures. Epilepsia 2010, 51:221-232.
22. Janszky I., Hallqvist J., Tomson T., et al. Increased risk and worse prognosis of myocardial infarction in patients with prior hospitalization for epilepsy-the Stockholm Heart Epidemiology Program. Brain 2009, 132:2798-2804.
23. Goldman A.M., Glasscock E., Yoo J., et al. Arrhythmia in heart and brain: KCNQ1 mutations link epilepsy and sudden unexplained death. Sci Transl Med 2009, 1:2ra6.
24. + channels in visceral sensory neurons. Biophysical Society 52th Annual Meeting, presentation 2008.
25. + channels in rat visceral sensory neurons. FASEB J 2009, [Abstract 959.1].
26. Tolstykh G.P., Cavazos J.E. KCNQ channels in the nucleus tractus solitarius of the brainstem might be involved in SUDEP. Epilepsia 2010, 51:S5.
27. Blum A.S. Respiratory physiology of seizures. J Clin Neurophysiol 2009, 26:309-315.
28. Stollberger C., Finsterer J. Cardiorespiratory findings in sudden unexplained/unexpected death in epilepsy (SUDEP). Epilepsy Res 2004, 59:51-60.
29. Sakamoto K., Saito T., Orman R., et al. Autonomic consequences of kainic acid-induced limbic cortical seizures in rats: peripheral autonomic nerve activity, acute cardiovascular changes, and death. Epilepsia 2008, 49:982-996.
30. Hotta H., Koizumi K., Stewart M. Cardiac sympathetic nerve activity during kainic acid-induced limbic cortical seizures in rats. Epilepsia 2009, 50:923-927.
31. Hotta H., Lazar J., Orman R., et al. Vagus nerve stimulation-induced bradyarrhythmias in rats. Auton Neurosci 2009, 151:98-105.
32. Willoughby J.O., Mackenzie L. Picrotoxin-, kainic acid- and seizure-induced Fos in brainstem, with special reference to catecholamine cell groups. Neurosci Res 1999, 33:163-169.
33. Shehab S., Coffey P., Dean P., et al. Regional expression of fos-like immunoreactivity following seizures induced by pentylenetetrazole and maximal electroshock. Exp Neurol 1992, 118:261-274.
34. Velisek L., Jehle K., Asche S., et al. Model of infantile spasms induced by N-methyl-D-aspartic acid in prenatally impaired brain. Ann Neurol 2007, 61:109-119.
35. La Rovere M.T., Schwartz P.J. Baroreflex sensitivity as a cardiac and arrhythmia mortality risk stratifier. Pacing Clin Electrophysiol 1997, 20:2602-2613.
36. La Rovere M.T. Baroreflex sensitivity as a new marker for risk stratification. Z Kardiol 2000, 89(Suppl. 3):44-50.
37. Bigger J.T., La Rovere M.T., Steinman R.C., et al. Comparison of baroreflex sensitivity and heart period variability after myocardial infarction. J Am Coll Cardiol 1989, 14:1511-1518.
38. DeGiorgio C.M., DeGiorgio A.C. SUDEP and heart rate variability. Epilepsy Res 2010, 90:309-310. [author reply 11-2].
39. Toth V., Hejjel L., Fogarasi A., et al. Periictal heart rate variability analysis suggests long-term postictal autonomic disturbance in epilepsy. Eur J Neurol 2010, 17:780-787.
40. Mifflin S.W. What does the brain know about blood pressure?. News Physiol Sci 2001, 16:266-271.
41. Boscan P., Pickering A.E., Paton J.F. The nucleus of the solitary tract: an integrating station for nociceptive and cardiorespiratory afferents. Exp Physiol 2002, 87:259-266.
42. Donoghue S., Felder R.B., Gilbey M.P., et al. Post-synaptic activity evoked in the nucleus tractus solitarius by carotid sinus and aortic nerve afferents in the cat. J Physiol 1985, 360:261-273.
43. Andresen M.C., Kunze D.L. Nucleus tractus solitarius-gateway to neural circulatory control. Annu Rev Physiol 1994, 56:93-116.
44. Bonham A.C., Chen C.Y., Sekizawa S., et al. Plasticity in the nucleus tractus solitarius and its influence on lung and airway reflexes. J Appl Physiol 2006, 101:322-327.
45. Magdaleno-Madrigal V.M., Valdes-Cruz A., Martinez-Vargas D., et al. Effect of electrical stimulation of the nucleus of the solitary tract on the development of electrical amygdaloid kindling in the cat. Epilepsia 2002, 43:964-969.
46. Schreihofer A.M., Ito S., Sved A.F. Brain stem control of arterial pressure in chronic arterial baroreceptor-denervated rats. Am J Physiol Regul Integr Comp Physiol 2005, 289:R1746-R1755.
47. Mancia G., Parati G., Pomidossi G., et al. Arterial baroreflexes and blood pressure and heart rate variabilities in humans. Hypertension 1986, 8:147-153.
48. Mancia G., Paratia G., Hennigc M., et al. Relation between blood pressure variability and carotid artery damage in hypertension: baseline data from the European Lacidipine Study on Atherosclerosis (ELSA). J Hypertens 2001, 19:1981-1989.
49. Mancia G., Parati G., Castiglioni P., et al. Daily Life Blood Pressure Changes Are Steeper in Hypertensive Than in Normotensive Subjects. Hypertension 2003, 42:277-282.
50. Gomez-Angelats E., de la Sierra A., Sierra C., et al. Blood pressure variability and silent cerebral damage in essential hypertension. Am Heart J 2004, 17.
51. Parati G. Blood pressure variability, target organ damage and antihypertensive treatment. J Hypertens 2003, 21:1827-1830.
52. Pringle E., Phillips C., Thijs L., et al. Systolic blood pressure variability as a risk factor for stroke and cardiovascular mortality in the elderly hypertensive population. J Hypertens 2003, 21:2251-2257.
53. Shan Z.Z., Dai S.M., Su D.F. Arterial baroreflex deficit induced organ damage in sinoaortic denervated rats. J Cardiovasc Pharmacol 2001, 38:427-437.
54. Housley G.D., Sinclair J.D. Localization by kainic acid lesions of neurones transmitting the carotid chemoreceptor stimulus for respiration in rat. J Physiol 1988, 406:99-114.
55. Takakura A.C., Moreira T.S., Colombari E., et al. Peripheral chemoreceptor inputs to retrotrapezoid nucleus (RTN) CO2-sensitive neurons in rats. J Physiol 2006, 572:503-523.
56. Awatramani G.B., Price G.D., Trussell L.O. Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron 2005, 48:109-121.
57. + current in a vertebrate neurone. Nature 1980, 283:673-676.
58. Wladyka C.L., Kunze D.L. KCNQ/M-currents contribute to the resting membrane potential in rat visceral sensory neurons. J Physiol 2006, 575:175-189.
59. Cooper E.C., Harrington E., Jan Y.N., Jan L.Y. M channel KCNQ2 subunits are localized to key sites for control of neuronal network oscillations and synchronization in mouse brain. J Neurosci 2001, 21:9529-9540.
60. Lawrence J.J., Saraga F., Churchill J.F., et al. Somatodendritic Kv7/KCNQ/M channels control interspike interval in hippocampal interneurons. J Neurosci 2006, 26:12325-12338.
61. Lawrence J.J., Grinspan Z.M., Statland J.M., et al. Muscarinic receptor activation tunes mouse stratum oriens interneurones to amplify spike reliability. J Physiol 2006, 571:555-562.
62. Brown B.S., Yu S.P. Modulation and genetic identification of the M channel. Prog Biophys Mol Biol 2000, 73:135-166.
63. Brown D.A. M Currents. Ion Channels 1988, 1:55-94. Plenus, New York, [Number of 55-94 pp.]. T. Narahashi (Ed.).
64. Jentsch T.J. Neuronal KCNQ potassium channels:physiology and role in diseases. Nature Neurosci 2000, 1:21-30.
65. + channels and the molecular pathogenesis of epilepsy: implications for therapy. Trends Neurosci 2000, 23:393-398.
66. Delmas P., Brown D.A. Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat Rev Neurosci 2005, 6:850-862.
67. Hernandez C.C., Zaika O., Tolstykh G.P., et al. Regulation of neural KCNQ channels: signalling pathways, structural motifs and functional implications. J Physiol 2008, 586:1811-1821.
68. Delmas P., Crest M., Brown D.A. Functional organization of PLC signaling microdomains in neurons. Trends Neurosci 2004, 27:41-47.
69. Gamper N., Shapiro M.S. Regulation of ion transport proteins by membrane phosphoinositides. Nat Rev Neurosci 2007, 8:921-934.
70. 2 activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 2003, 37:963-975.
71. Suh B., Hille B. Recovery from muscarinic modulation of M current channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 2002, 35:507-520.
72. + channel open probability by phosphatidylinositol 4,5-bisphosphate. J Neurosci 2005, 25:9825-9835.
73. Suh B.C., Horowitz L.F., Hirdes W., et al. Regulation of KCNQ2/KCNQ3 current by G protein cycling: the kinetics of receptor-mediated signaling by Gq. J Gen Physiol 2004, 123:663-683.
74. Higashida H., Hoshi N., Zhang J.S., et al. Protein kinase C bound with A-kinase anchoring protein is involved in muscarinic receptor-activated modulation of M-type KCNQ potassium channels. Neurosci Res 2005, 51:231-234.
75. Hoshi N., Zhang J.S., Omaki M., et al. AKAP150 signaling complex promotes suppression of the M-current by muscarinic agonists. Nat Neurosci 2003, 6:564-571.
76. + channels. J Gen Physiol 2003, 122:17-31.
77. 2+/calmodulin. Mol Biol Cell 2005, 16:3538-3551.
78. Sutula T., He X.X., Cavazos J., et al. Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 1988, 239:1147-1150.
79. Represa A., Le Gall La Salle G., Ben-Ari Y., et al. Hippocampal plasticity in the kindling model of epilepsy in rats. Neurosci Lett 1989, 99:345-350.
80. Lothman E.W., Collins R.C., Ferrendelli J.A. Kainic acid-induced limbic seizures: electrophysiologic studies. Neurology 1981, 31:806-812.
81. Fisahn A. Kainate receptors and rhythmic activity in neuronal networks: hippocampal gamma oscillations as a tool. J Physiol 2005, 562:65-72.
82. Represa A., Tremblay E., Ben-Ari Y. Kainate binding sites in the hippocampal mossy fibers: localization and plasticity. Neuroscience 1987, 20:739-748.
83. Hellier J.L., Patrylo P.R., Buckmaster P.S., et al. Recurrent spontaneous motor seizures after repeated low-dose systemic treatment with kainate: assessment of a rat model of temporal lobe epilepsy. Epilepsy Res 1998, 31:73-84.
84. Cavazos J.E., Jones S.M., Cross D.J. Sprouting and synaptic reorganization in the subiculum and CA1 region of the hippocampus in acute and chronic models of partial-onset epilepsy. Neuroscience 2004, 126:677-688.
85. Faber R., Baumert M., Stepan H., et al. Baroreflex sensitivity, heart rate, and blood pressure variability in hypertensive pregnancy disorders. J Hum Hypertens 2004, 18:707-712.
86. Faber R., Stepan H., Baumert M., et al. Changes of blood pressure and heart rate variability precede a grand mal seizure in a pregnant woman. J Perinat Med 2004, 32:538-540.
87. Barrett C.J., Guild S.J., Ramchandra R., et al. Baroreceptor denervation prevents sympathoinhibition during angiotensin II-induced hypertension. Hypertension 2005, 46:168-172.
88. Kario K. Blood Pressure Variability in Hypertension: A Possible Cardiovascular Risk Factor. Am J Hypertens 2004, 17:1075-1076.
89. Liu J.-G., Xu L.-P., Chu Z.-X., et al. Contribution of blood pressure variability to the effect of nitrendipine on end-organ damage in spontaneously hypertensive rats. J Hypertens 2003, 21:1961-1967.
90. Mussalo H., Vanninen E., Ikaheimo R., et al. Short-term blood pressure variability in renovascular hypertension and in severe and mild essential hypertension. Clin Sci 2003, 105:609-614.
91. Parati G. Blood pressure variability and cardiovascular control mechanisms in hypertension. Clin Sci 2003, 105:545-547.
92. Su D.-F., Miao C.-Y. Blood pressure variability and organ damage. Clin Exp Pharmacol Physiol 2001, 28:709-715.
93. Cavazos J.E., Golarai G., Sutula T.P. Mossy fiber synaptic reorganization induced by kindling: time course of development, progression, and permanence. J Neurosci 1991, 11(9):2795-2803.
94. Golarai G., Cavazos J.E., Sutula T.P. Activation of the dentate gyrus by pentylenetetrazol evoked seizures induces mossy fiber synaptic reorganization. Brain Res 1992, 593(2):257-264.