Advertisement

Nondrug Treatment for Refractory Status Epilepticus

  • Guoming Luan
  • Xuefeng WangEmail author
Chapter

Abstract

Although various drugs, such as benzodiazepines, anesthetics, and intravenous antiepileptic drugs (AEDs), are used to control refractory status epilepticus (RSE), many cases of RSE are not effectively controlled. In such cases, efforts to control RSE may take the form of nonpharmacological measures, including therapeutic hypothermia, electroconvulsive therapy, neuromodulatory treatment, and the implementation of a ketogenic diet. These measures are not widely used in RSE, but studies have shown that they can play a role in controlling RSE. In this chapter, we summarize the efficacy, safety, and application of these treatments.

References

  1. 1.
    Hippocrates De Vetere Medicina. Harvard University Press, Loeb Classical Library:460–375 BC:461–432.Google Scholar
  2. 2.
    Gunn AJ, Laptook AR, Robertson NJ, Barks JD, Thoresen M, Wassink G, Bennet L. Therapeutic hypothermia translates from ancient history in to practice. Pediatr Res. 2017;81(1–2):202–9.PubMedCrossRefGoogle Scholar
  3. 3.
    Westin B, Miller JA Jr, Nyberg R, Wedenberg E. Neonatal asphyxia pallida treated with hypothermia alone or with hypothermia and transfusion of oxygenated blood. Surgery. 1959;45(5):868–79.PubMedGoogle Scholar
  4. 4.
    Ommaya AK, Baldwin M. Extravascular local cooling of the brain in man. J Neurosurg. 1963;20:8–20.PubMedCrossRefGoogle Scholar
  5. 5.
    Vastola EF, Homan R, Rosen A. Inhibition of focal seizures by moderate hypothermia. A clinical and experimental study. Arch Neurol. 1969;20(4):430–9.PubMedCrossRefGoogle Scholar
  6. 6.
    Sourek K, Travnicek V. General and local hypothermia of the brain in the treatment of intractable epilepsy. J Neurosurg. 1970;33(3):253–9.PubMedCrossRefGoogle Scholar
  7. 7.
    Orlowski JP, Erenberg G, Lueders H, Cruse RP. Hypothermia and barbiturate coma for refractory status epilepticus. Crit Care Med. 1984;12(4):367–72.PubMedCrossRefGoogle Scholar
  8. 8.
    Corry JJ, Dhar R, Murphy T, Diringer MN. Hypothermia for refractory status epilepticus. Neurocrit Care. 2008;9(2):189–97.PubMedCrossRefGoogle Scholar
  9. 9.
    Legriel S, Lemiale V, Schenck M, Chelly J, Laurent V, Daviaud F, Srairi M, Hamdi A, Geri G, Rossignol T, et al. Hypothermia for neuroprotection in convulsive status epilepticus. N Engl J Med. 2016;375(25):2457–67.PubMedCrossRefGoogle Scholar
  10. 10.
    Elting JW, Naalt J, Fock JM. Mild hypothermia for refractory focal status epilepticus in an infant with hemimegalencephaly. Eur J Paediatr Neurol. 2010;14(5):452–5.PubMedCrossRefGoogle Scholar
  11. 11.
    Guilliams K, Rosen M, Buttram S, Zempel J, Pineda J, Miller B, Shoykhet M. Hypothermia for pediatric refractory status epilepticus. Epilepsia. 2013;54(9):1586–94.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Lin JJ, Lin KL, Hsia SH, Wang HS, Group CS. Therapeutic hypothermia for febrile infection-related epilepsy syndrome in two patients. Pediatr Neurol. 2012;47(6):448–50.PubMedCrossRefGoogle Scholar
  13. 13.
    Rossetti AO. What is the value of hypothermia in acute neurologic diseases and status epilepticus? Epilepsia. 2011;52(Suppl 8):64–6.PubMedCrossRefGoogle Scholar
  14. 14.
    Holzer M. Targeted temperature management for comatose survivors of cardiac arrest. N Engl J Med. 2010;363(13):1256–64.PubMedCrossRefGoogle Scholar
  15. 15.
    Cereda C, Berger MM, Rossetti AO. Bowel ischemia: a rare complication of thiopental treatment for status epilepticus. Neurocrit Care. 2009;10(3):355–8.PubMedCrossRefGoogle Scholar
  16. 16.
    Rothman SM. The therapeutic potential of focal cooling for neocortical epilepsy. Neurotherapeutics. 2009;6(2):251–7.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Fujii M, Inoue T, Nomura S, Maruta Y, He Y, Koizumi H, Shirao S, Owada Y, Kunitsugu I, Yamakawa T, et al. Cooling of the epileptic focus suppresses seizures with minimal influence on neurologic functions. Epilepsia. 2012;53(3):485–93.PubMedCrossRefGoogle Scholar
  18. 18.
    Volgushev M, Kudryashov I, Chistiakova M, Mukovski M, Niesmann J, Eysel UT. Probability of transmitter release at neocortical synapses at different temperatures. J Neurophysiol. 2004;92(1):212–20.PubMedCrossRefGoogle Scholar
  19. 19.
    Wassink G, Gunn ER, Drury PP, Bennet L, Gunn AJ. The mechanisms and treatment of asphyxial encephalopathy. Front Neurosci. 2014;8:40.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Nakashima K, Todd MM, Warner DS. The relation between cerebral metabolic rate and ischemic depolarization. A comparison of the effects of hypothermia, pentobarbital, and isoflurane. Anesthesiology. 1995;82(5):1199–208.PubMedCrossRefGoogle Scholar
  21. 21.
    Motamedi GK, Salazar P, Smith EL, Lesser RP, Webber WR, Ortinski PI, Vicini S, Rogawski MA. Termination of epileptiform activity by cooling in rat hippocampal slice epilepsy models. Epilepsy Res. 2006;70(2–3):200–10.PubMedCrossRefGoogle Scholar
  22. 22.
    Hill MW, Wong M, Amarakone A, Rothman SM. Rapid cooling aborts seizure-like activity in rodent hippocampal-entorhinal slices. Epilepsia. 2000;41(10):1241–8.PubMedCrossRefGoogle Scholar
  23. 23.
    Motamedi GK, Gonzalez-Sulser A, Dzakpasu R, Vicini S. Cellular mechanisms of desynchronizing effects of hypothermia in an in vitro epilepsy model. Neurotherapeutics. 2012;9(1):199–209.PubMedCrossRefGoogle Scholar
  24. 24.
    Yu L, Zhou Y, Wang Y. Effect of mild hypothermia on glutamate receptor expression after status epilepticus. Epilepsy Res. 2012;101(1–2):56–69.PubMedCrossRefGoogle Scholar
  25. 25.
    Aird RB, Tsubaki T. Common sources of error in the diagnosis and treatment of convulsive disorders: a review of 204 patients with temporal lobe epilepsy. J Nerv Ment Dis. 1958;127(5):400–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Capovilla G, Beccaria F, Beghi E, Minicucci F, Sartori S, Vecchi M. Treatment of convulsive status epilepticus in childhood: recommendations of the Italian League against epilepsy. Epilepsia. 2013;54(Suppl 7):23–34.PubMedCrossRefGoogle Scholar
  27. 27.
    Viparelli U, Viparelli G. ECT and grand mal epilepsy. Convuls Ther. 1992;8(1):39–42.PubMedGoogle Scholar
  28. 28.
    Vigevano F, Cilio MR. Vigabatrin versus ACTH as first-line treatment for infantile spasms: a randomized, prospective study. Epilepsia. 1997;38(12):1270–4.PubMedCrossRefGoogle Scholar
  29. 29.
    Zeiler FA, Matuszczak M, Teitelbaum J, Gillman LM, Kazina CJ. Electroconvulsive therapy for refractory status epilepticus: a systematic review. Seizure. 2016;35:23–32.PubMedCrossRefGoogle Scholar
  30. 30.
    Lambrecq V, Villega F, Marchal C, Michel V, Guehl D, Rotge JY, Burbaud P. Refractory status epilepticus: electroconvulsive therapy as a possible therapeutic strategy. Seizure. 2012;21(9):661–4.PubMedCrossRefGoogle Scholar
  31. 31.
    Regenold WT, Weintraub D, Taller A. Electroconvulsive therapy for epilepsy and major depression. Am J Geriatr Psychiatry. 1998;6(2):|180–3.PubMedCrossRefGoogle Scholar
  32. 32.
    Kucia KA, Stepanczak R, Tredzbor B. Electroconvulsive therapy for major depression in an elderly person with epilepsy. World J Biol Psychiatry. 2009;10(1):78–80.PubMedCrossRefGoogle Scholar
  33. 33.
    Griesemer DA, Kellner CH, Beale MD, Smith GM. Electroconvulsive therapy for treatment of intractable seizures. Initial findings in two children. Neurology. 1997;49(5):1389–92.PubMedCrossRefGoogle Scholar
  34. 34.
    Lisanby SH, Bazil CW, Resor SR, Nobler MS, Finck DA, Sackeim HA. ECT in the treatment of status epilepticus. J ECT. 2001;17(3):210–5.PubMedCrossRefGoogle Scholar
  35. 35.
    Cline JS, Roos K. Treatment of status epilepticus with electroconvulsive therapy. J ECT. 2007;23(1):30–2.PubMedCrossRefGoogle Scholar
  36. 36.
    Koong FJ, Chen WC. Maintaining electroconvulsive therapy for refractory epilepsy combined with psychotic symptoms. BMJ Case Rep. 2010;2010.Google Scholar
  37. 37.
    Kamel H, Cornes SB, Hegde M, Hall SE, Josephson SA. Electroconvulsive therapy for refractory status epilepticus: a case series. Neurocrit Care. 2010;12(2):204–10.PubMedCrossRefGoogle Scholar
  38. 38.
    Shin HW, O'Donovan CA, Boggs JG, Grefe A, Harper A, Bell WL, McCall WV, Rosenquist P. Successful ECT treatment for medically refractory nonconvulsive status epilepticus in pediatric patient. Seizure. 2011;20(5):433–6.PubMedCrossRefGoogle Scholar
  39. 39.
    Carrasco Gonzalez MD, Palomar M, Rovira R. Electroconvulsive therapy for status epilepticus. Ann Intern Med. 1997;127(3):247–8.PubMedCrossRefGoogle Scholar
  40. 40.
    Wusthoff CJ, Kranick SM, Morley JF, Christina Bergqvist AG. The ketogenic diet in treatment of two adults with prolonged nonconvulsive status epilepticus. Epilepsia. 2010;51(6):1083–5.PubMedCrossRefGoogle Scholar
  41. 41.
    Trevino K, McClintock SM, Husain MM. A review of continuation electroconvulsive therapy: application, safety, and efficacy. J ECT. 2010;26(3):186–95.PubMedCrossRefGoogle Scholar
  42. 42.
    Brodaty H, Berle D, Hickie I, Mason C. “Side effects” of ECT are mainly depressive phenomena and are independent of age. J Affect Disord. 2001;66(2–3):237–45.PubMedCrossRefGoogle Scholar
  43. 43.
    Stoppe A, Louza M, Rosa M, Gil G, Rigonatti S. Fixed high-dose electroconvulsive therapy in the elderly with depression: a double-blind, randomized comparison of efficacy and tolerability between unilateral and bilateral electrode placement. J ECT. 2006;22(2):92–9.PubMedCrossRefGoogle Scholar
  44. 44.
    Sackeim H, Decina P, Prohovnik I, Malitz S. Seizure threshold in electroconvulsive therapy. Effects of sex, age, electrode placement, and number of treatments. Arch Gen Psychiatry. 1987;44(4):355–60.PubMedCrossRefGoogle Scholar
  45. 45.
    Khalilov I, Holmes GL, Ben-Ari Y. In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat Neurosci. 2003;6(10):1079–85.PubMedCrossRefGoogle Scholar
  46. 46.
    Sackeim HA, Decina P, Prohovnik I, Malitz S, Resor SR. Anticonvulsant and antidepressant properties of electroconvulsive therapy: a proposed mechanism of action. Biol Psychiatry. 1983;18(11):1301–10.PubMedGoogle Scholar
  47. 47.
    Clark M. Sensitivity of the rat hippocampal GABA(A) receptor alpha 4 subunit to electroshock seizures. Neurosci Lett. 1998;250(1):17–20.PubMedCrossRefGoogle Scholar
  48. 48.
    Esel E, Kose K, Hacimusalar Y, Ozsoy S, Kula M, Candan Z, Turan T. The effects of electroconvulsive therapy on GABAergic function in major depressive patients. J ECT. 2008;24(3):224–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Yoshitake T, Reenila I, Ogren SO, Hokfelt T, Kehr J. Galanin attenuates basal and antidepressant drug-induced increase of extracellular serotonin and noradrenaline levels in the rat hippocampus. Neurosci Lett. 2003;339(3):239–42.PubMedCrossRefGoogle Scholar
  50. 50.
    Christiansen SH, Woldbye DP. Regulation of the galanin system by repeated electroconvulsive seizures in mice. J Neurosci Res. 2010;88(16):3635–43.PubMedCrossRefGoogle Scholar
  51. 51.
    Wheless JW. History of the ketogenic diet. Epilepsia. 2008;49(Suppl 8):3–5.PubMedCrossRefGoogle Scholar
  52. 52.
    Wilder RM. The effect on ketonemia on the course of epilepsy. Mayo Clin Bull. 1921;2:307–8.Google Scholar
  53. 53.
    Lord K, Magrath G. Use of the ketogenic diet and dietary practices in the UK. J Hum Nutr Diet. 2010;23(2):126–32.PubMedCrossRefGoogle Scholar
  54. 54.
    Kossoff EH, Zupec-Kania BA, Amark PE, et al. Optimal clinical management of children receiving the ketogenic diet: recommendations of the International Ketogenic Diet Study Group. Epilepsia. 2009;50(2):304–17.PubMedCrossRefGoogle Scholar
  55. 55.
    National Clinical Guideline Centre, National Institute for Health and Clinical Excellence: Guidance. In: The epilepsies: the diagnosis and management of the epilepsies in adults and children in primary and secondary care: pharmacological update of Clinical Guideline 20. London: Royal College of Physicians; 2012.Google Scholar
  56. 56.
    Kossoff EH, Al-Macki N, Cervenka MC, et al. What are the minimum requirements for ketogenic diet services in resource-limited regions? Recommendations from the International League Against Epilepsy Task Force for Dietary Therapy. Epilepsia. 2015;56(9):1337–42.PubMedCrossRefGoogle Scholar
  57. 57.
    Ferlisi M, Shorvon S. The outcome of therapies in refractory and super-refractory convulsive status epilepticus and recommendations for therapy. Brain. 2012;135(Pt 8):2314–28.PubMedGoogle Scholar
  58. 58.
    Shorvon S. Super-refractory status epilepticus: an approach to therapy in this difficult clinical situation. Epilepsia. 2011;52(Suppl 8):53–6.PubMedCrossRefGoogle Scholar
  59. 59.
    Klein P, Tyrlikova I, Mathews GC, et al. Dietary treatment in adults with refractory epilepsy: a review. Neurology. 2014;83(21):1978–85.PubMedCrossRefGoogle Scholar
  60. 60.
    Caraballo RH, Valenzuela GR, Armeno M, et al. The ketogenic diet in two paediatric patients with refractory myoclonic status epilepticus. Epileptic Disord. 2015;17(4):491–5.PubMedGoogle Scholar
  61. 61.
    Caraballo RH, Flesler S, Armeno M, et al. Ketogenic diet in pediatric patients with refractory focal status epilepticus. Epilepsy Res. 2014;108(10):1912–6.PubMedCrossRefGoogle Scholar
  62. 62.
    Lin JJ, Lin KL, Chan OW, et al. Intravenous ketogenic diet therapy for treatment of the acute stage of super-refractory status epilepticus in a pediatric patient. Pediatr Neurol. 2015;52(4):442–5.PubMedCrossRefGoogle Scholar
  63. 63.
    Thakur KT, Probasco JC, Hocker SE, et al. Ketogenic diet for adults in super-refractory status epilepticus. Neurology. 2014;82(8):665–70.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Wusthoff CJ, Kranick SM, Morley JF, et al. The ketogenic diet in treatment of two adults with prolonged nonconvulsive status epilepticus. Epilepsia. 2010;51(6):1083–5.PubMedCrossRefGoogle Scholar
  65. 65.
    Strzelczyk A, Reif PS, Bauer S, et al. Intravenous initiation and maintenance of ketogenic diet: proof of concept in super-refractory status epilepticus. Seizure. 2013;22(7):581–3.PubMedCrossRefGoogle Scholar
  66. 66.
    Nabbout R, Mazzuca M, Hubert P, et al. Efficacy of ketogenic diet in severe refractory status epilepticus initiating fever induced refractory epileptic encephalopathy in school age children (FIRES). Epilepsia. 2010;51(10):2033–7.PubMedCrossRefGoogle Scholar
  67. 67.
    Nam SH, Lee BL, Lee CG, et al. The role of ketogenic diet in the treatment of refractory status epilepticus. Epilepsia. 2011;52(11):e181–4.PubMedCrossRefGoogle Scholar
  68. 68.
    Cervenka MC, Hartman AL, Venkatesan A, et al. The ketogenic diet for medically and surgically refractory status epilepticus in the neurocritical care unit. Neurocrit Care. 2011;15(3):519–24.PubMedCrossRefGoogle Scholar
  69. 69.
    Vaccarezza M, Silva W, Maxit C, et al. Super-refractory status epilepticus: treatment with ketogenic diet in pediatrics. Rev Neurol. 2012;55(1):20–5.PubMedGoogle Scholar
  70. 70.
    Bodenant M, Moreau C, Sejourné C, et al. Interest of the ketogenic diet in a refractory status epilepticus in adults. Rev Neurol (Paris). 2008;164(2):194–9.CrossRefGoogle Scholar
  71. 71.
    Kossoff EH, Nabbout R. Use of dietary therapy for status epilepticus. J Child Neurol. 2013;28(8):1049–51.PubMedCrossRefGoogle Scholar
  72. 72.
    Sort R, Born AP, Pedersen KN, et al. Ketogenic diet in 3 cases of childhood refractory status epilepticus. Eur J Paediatr Neurol. 2013;17(6):531–6.PubMedCrossRefGoogle Scholar
  73. 73.
    Al-Mudallal AS, LaManna JC, Lust WD, et al. Diet-induced ketosis does not cause cerebral acidosis. Epilepsia. 1996;37(3):258–61.PubMedCrossRefGoogle Scholar
  74. 74.
    Alberti MJ, Agustinho A, Argumedo L, et al. Recommendations for the clinical management of children with refractory epilepsy receiving the ketogenic diet. Arch Argent Pediatr. 2016;114(1):56–63.PubMedGoogle Scholar
  75. 75.
    Cervenka MC, Henry BJ, Felton EA, et al. Establishing an adult epilepsy diet center: experience, efficacy and challenges. Epilepsy Behav. 2016;58:61–8.PubMedCrossRefGoogle Scholar
  76. 76.
    Ye F, Li XJ, Jiang WL, et al. Efficacy of and patient compliance with a ketogenic diet in adults with intractable epilepsy: a meta-analysis. J Clin Neurol. 2015;11(1):26–31.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Zamani GR, Mohammadi M, Ashrafi MR, et al. The effects of classic ketogenic diet on serum lipid profile in children with refractory seizures. Acta Neurol Belg. 2016;116(4):529–34.PubMedCrossRefGoogle Scholar
  78. 78.
    Kwiterovich PO Jr, Vining EP, Pyzik P, et al. Effect of a high-fat ketogenic diet on plasma levels of lipids, lipoproteins, and apolipoproteins in children. JAMA. 2003;290(7):912–20.PubMedCrossRefGoogle Scholar
  79. 79.
    Coppola G, Natale F, Torino A, et al. The impact of the ketogenic diet on arterial morphology and endothelial function in children and young adults with epilepsy: a case-control study. Seizure. 2014;23(4):260–5.PubMedCrossRefGoogle Scholar
  80. 80.
    Lambrechts DA, de Kinderen RJ, Vles HS, et al. The MCT-ketogenic diet as a treatment option in refractory childhood epilepsy: a prospective study with 2-year follow-up. Epilepsy Behav. 2015;51:261–6.PubMedCrossRefGoogle Scholar
  81. 81.
    Moriyama K, Watanabe M, Yamada Y, et al. Protein-losing enteropathy as a rare complication of the ketogenic diet. Pediatr Neurol. 2015;52:526–8.PubMedCrossRefGoogle Scholar
  82. 82.
    Baumeister FA, Oberhoffer R, Liebhaber GM, et al. Fatal propofol infusion syndrome in association with ketogenic diet. Neuropediatrics. 2004;35:250–2.PubMedCrossRefGoogle Scholar
  83. 83.
    Nei M, Ngo L, Sirven JI, et al. Ketogenic diet in adolescents and adults with epilepsy. Seizure. 2014;23:439–42.PubMedCrossRefGoogle Scholar
  84. 84.
    Smith M, Politzer N, Macgarvie D, et al. Efficacy and tolerability of the modified Atkins diet in adults with pharmacoresistant epilepsy: a prospective observational study. Epilepsia. 2011;52:775–80.PubMedCrossRefGoogle Scholar
  85. 85.
    Mady MA, Kossoff EH, McGregor AL, et al. The ketogenic diet: adolescents can do it, too. Epilepsia. 2003;44(6):847–51.PubMedCrossRefGoogle Scholar
  86. 86.
    Sampath A, Kossoff EH, Furth SL, et al. Kidney stones and the ketogenic diet: risk factors and prevention. J Child Neurol. 2007;22(4):375–8.PubMedCrossRefGoogle Scholar
  87. 87.
    Bough KJ, Rho JM. Anticonvulsant mechanisms of the ketogenic diet. Epilepsia. 2007;48(1):43–58.PubMedCrossRefGoogle Scholar
  88. 88.
    Melo TM, Nehlig A, Sonnewald U. Neuronal-glial interactions in rats fed a ketogenic diet. Neurochem Int. 2006;48:498–507.PubMedCrossRefGoogle Scholar
  89. 89.
    Keith HM. Factors influencing experimentally produced convulsions. Arch Neurol Psychiatr. 1933;29:148–54.CrossRefGoogle Scholar
  90. 90.
    Likhodii SS, Serbanescu I, Cortez MA, et al. Anticonvulsant properties of acetone, a brain ketone elevated by the ketogenic diet. Ann Neurol. 2003;54(2):219–26.PubMedCrossRefGoogle Scholar
  91. 91.
    Gasior M, French A, Joy MT, et al. The anticonvulsant activity of acetone, the major ketone body in the ketogenic diet, is not dependent on its metabolites acetol, 1,2-propanediol, methylglyoxal, or pyruvic acid. Epilepsia. 2007;48:793–800.PubMedCrossRefGoogle Scholar
  92. 92.
    Rho JM, Anderson GD, Donevan SD, et al. Acetoacetate, acetone, and dibenzylamine (a contaminant in L-(+)-b-Hydroxybutyrate) exhibit direct anticonvulsant actions in vivo. Epilepsia. 2002;43(4):358–61.PubMedCrossRefGoogle Scholar
  93. 93.
    Nylen K, Likhodii SS, Hum KM, et al. A ketogenic diet and diallyl sulfide do not elevate after discharge thresholds in adult kindled rats. Epilepsy Res. 2006;71:23–31.PubMedCrossRefGoogle Scholar
  94. 94.
    Bough KJ, Gudi K, Han FT, et al. An anticonvulsant profile of the ketogenic diet in the rat. Epilepsy Res. 2002;50(3):313–25.PubMedCrossRefGoogle Scholar
  95. 95.
    Dahlin M, Elfving A, Ungerstedt U, et al. The ketogenic diet influences the levels of excitatory and inhibitory amino acids in the CSF in children with refractory epilepsy. Epilepsy Res. 2005;64:115–25.PubMedCrossRefGoogle Scholar
  96. 96.
    Wang ZJ, Bergqvist C, Hunter JV, et al. In vivo measurement of brain metabolites using two-dimensional double-quantum MR spectroscopy--exploration of GABA levels in a ketogenic diet. Magn Reson Med. 2003;49:615–9.PubMedCrossRefGoogle Scholar
  97. 97.
    Cheng CM, Hicks K, Wang J, et al. Caloric restriction augments brain glutamic acid decarboxylase-65 and -67 expression. J Neurosci Res. 2004;77:270–6.PubMedCrossRefGoogle Scholar
  98. 98.
    Yudkoff M, Daikhin Y, Nissim I, et al. Response of brain amino acid metabolism to ketosis. Neurochem Int. 2005;47(1–2):119–28.PubMedCrossRefGoogle Scholar
  99. 99.
    Yudkoff M, Daikhin Y, Horyn O, et al. Ketosis and brain handling of glutamate, glutamine, and GABA. Epilepsia. 2008;49(Suppl 8):73–5.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Lutas A, Yellen G. The ketogenic diet: metabolic influences on brain excitability and epilepsy. Trends Neurosci. 2013;36(1):32–40.PubMedCrossRefGoogle Scholar
  101. 101.
    Ma W, Berg J, Yellen G. Ketogenic diet metabolites reduce firing in central neurons by opening K(ATP) channels. J Neurosci. 2007;27(14):3618–25.PubMedCrossRefGoogle Scholar
  102. 102.
    Stafstrom CE, Ockuly JC, Murphree L, et al. Anticonvulsant and antiepileptic actions of 2-deoxy-D-glucose in epilepsy models. Ann Neurol. 2009;65(4):435–47.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Garriga-Canut M, Schoenike B, Qazi R, et al. 2-Deoxy-D-glucose reduces epilepsy progression by NRSF-CtBP-dependent metabolic regulation of chromatin structure. Nat Neurosci. 2006;9:1382–7.PubMedCrossRefGoogle Scholar
  104. 104.
    Chang P, Terbach N, Plant N, et al. Seizure control by ketogenic diet-associated medium chain fatty acids. Neuropharmacology. 2013;69:105–14.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Chang P, Augustin K, Boddum K, et al. Seizure control by decanoic acid through direct AMPA receptor inhibition. Brain. 2016;139:431–43.PubMedCrossRefGoogle Scholar
  106. 106.
    Schlanger S, Shinitzky M, Yam D. Diet enriched with omega-3 fatty acids alleviates convulsion symptoms in epilepsy patients. Epilepsia. 2002;43:103–4.PubMedCrossRefGoogle Scholar
  107. 107.
    Xiao Y, Li X. Polyunsaturated fatty acids modify mouse hippocampal neuronal excitability during excitotoxic or convulsant stimulation. Brain Res. 1999;846:112–21.PubMedCrossRefGoogle Scholar
  108. 108.
    Yazdi S, Stein M, Elinder F, et al. The molecular basis of polyunsaturated fatty acid interactions with the shaker voltage gated potassium channel. PLoS Comput Biol. 2016;12:e1004704.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Ben-Menachem E, Manon-Espaillat R, Ristanovic R, Wilder BJ, Stefan H, Mirza W, Tarver WB, Wernicke JF. Vagus nerve stimulation for treatment of partial seizures: 1. A controlled study of effect on seizures. First International Vagus Nerve Stimulation Study Group. Epilepsia. 1994;35:616–26.PubMedCrossRefGoogle Scholar
  110. 110.
    Handforth A, DeGiorgio CM, Schachter SC, Uthman BM, Naritoku DK, Tecoma ES, Henry TR, Collins SD, Vaughn BV, Gilmartin RC, Labar DR, Morris GL III, Salinsky MC, Osorio I, Ristanovic RK, Labiner DM, Jones JC, Murphy JV, Ney GC, Wheless JW. Vagus nerve stimulation therapy for partial-onset seizures: a randomized active-control trial. Neurology. 1998;51:48–55.PubMedCrossRefGoogle Scholar
  111. 111.
    Gooneratne IK, Green AL, Dugan P, Sen A, Franzini A, Aziz T, Cheeran B. Comparing neurostimulation technologies in refractory focal-onset epilepsy. J Neurol Neurosurg Psychiatry. 2016;87:1174–82.PubMedCrossRefGoogle Scholar
  112. 112.
    Heck C, Helmers SL, DeGiorgio CM. Vagus nerve stimulation therapy, epilepsy, and device parameters: scientific basis and recommendations for use. Neurology. 2002;59:S31–7.PubMedCrossRefGoogle Scholar
  113. 113.
    Amar AP, Apuzzo ML, Liu CY. Vagus nerve stimulation therapy after failed cranial surgery for intractable epilepsy: results from the vagus nerve stimulation therapy patient outcome registry. Neurosurgery. 2004;55:1086–93.PubMedCrossRefGoogle Scholar
  114. 114.
    DeGiorgio CM, Schachter SC, Handforth A, Salinsky M, Thompson J, Uthman B, Reed R, Collins S, Tecoma E, Morris GL, Vaughn B, Naritoku DK, Henry T, Labar D, Gilmartin R, Labiner D, Osorio I, Ristanovic R, Jones J, Murphy J, Ney G, Wheless J, Lewis P, Heck C. Prospective long-term study of vagus nerve stimulation for the treatment of refractory seizures. Epilepsia. 2000;41:1195–200.PubMedCrossRefGoogle Scholar
  115. 115.
    Ghaemi K, Elsharkawy AE, Schulz R, Hoppe M, Polster T, Pannek H, Ebner A. Vagus nerve stimulation: outcome and predictors of seizure freedom in long-term follow-up. Seizure. 2010;19:264–8.PubMedCrossRefGoogle Scholar
  116. 116.
    Vonck K, Raedt R, Naulaerts J, De Vogelaere F, Thiery E, Van Roost D, Aldenkamp B, Miatton M, Boon P. Vagus nerve stimulation…25 years later! What do we know about the effects on cognition? Neurosci Biobehav Rev. 2014;45:63–71.PubMedCrossRefGoogle Scholar
  117. 117.
    De Herdt V, Boon P, Ceulemans B, Hauman H, Lagae L, Legros B, Sadzot B, Van Bogaert P, van Rijckevorsel K, Verhelst H, Vonck K. Vagus nerve stimulation for refractory epilepsy: a Belgian multicenter study. Eur J Paediatr Neurol. 2007;11:261–9.PubMedCrossRefGoogle Scholar
  118. 118.
    Kuba R, Brazdil M, Kalina M, Prochazka T, Hovorka J, Nezadal T, Hadac J, Brozova K, Sebronova V, Komarek V, Marusic P, Oslejskova H, Zarubova J, Rektor I. Vagus nerve stimulation: longitudinal follow-up of patients treated for 5 years. Seizure. 2009;18:269–74.PubMedCrossRefGoogle Scholar
  119. 119.
    Patwardhan RV, Dellabadia J Jr, Rashidi M, Grier L, Nanda A. Control of refractory status epilepticus precipitated by anticonvulsant withdrawal using left vagal nerve stimulation: a case report. Surg Neurol. 2005;64:170–3.PubMedCrossRefGoogle Scholar
  120. 120.
    Carreno M, Garcia-Alvarez D, Maestro I, Fernandez S, Donaire A, Boget T, Rumia J, Pintor L, Setoain X. Malignant autosomal dominant frontal lobe epilepsy with repeated episodes of status epilepticus: successful treatment with vagal nerve stimulation. Epileptic Disord. 2010;12:155–8.PubMedGoogle Scholar
  121. 121.
    O'Neill BR, Valeriano J, Synowiec A, Thielmann D, Lane C, Wilberger J. Refractory status epilepticus treated with vagal nerve stimulation: case report. Neurosurgery. 2011;69:E1172–5.PubMedGoogle Scholar
  122. 122.
    Zeiler FA, Zeiler KJ, Teitelbaum J, Gillman LM, West M. VNS for refractory status epilepticus. Epilepsy Res. 2015;112:100–13.PubMedCrossRefGoogle Scholar
  123. 123.
    Winston KR, Levisohn P, Miller BR, Freeman J. Vagal nerve stimulation for status epilepticus. Pediatr Neurosurg. 2001;34:190–2.PubMedCrossRefGoogle Scholar
  124. 124.
    Bayrlee A, Ganeshalingam N, Kurczewski L, Brophy GM. Treatment of super-refractory status epilepticus. Curr Neurol Neurosci Rep. 2015;15:66.PubMedCrossRefGoogle Scholar
  125. 125.
    Boon P, Raedt R, de Herdt V, Wyckhuys T, Vonck K. Electrical stimulation for the treatment of epilepsy. Neurotherapeutics. 2009;6:218–27.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Delgado JM, Hamlin H, Chapman WP. Technique of intracranial electrode implacement for recording and stimulation and its possible therapeutic value in psychotic patients. Confin Neurol. 1952;12:315–9.PubMedCrossRefGoogle Scholar
  127. 127.
    Skarpaas TL, Morrell MJ. Intracranial stimulation therapy for epilepsy. Neurotherapeutics. 2009;6:238–43.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Morrell MJ. Responsive cortical stimulation for the treatment of medically intractable partial epilepsy. Neurology. 2011;77:1295–304.PubMedCrossRefGoogle Scholar
  129. 129.
    Ben-Menachem E. Neurostimulation-past, present, and beyond. Epilepsy Curr. 2012;12:188–91.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Hamani C, Hodaie M, Chiang J, del Campo M, Andrade DM, Sherman D, Mirski M, Mello LE, Lozano AM. Deep brain stimulation of the anterior nucleus of the thalamus: effects of electrical stimulation on pilocarpine-induced seizures and status epilepticus. Epilepsy Res. 2008;78:117–23.PubMedCrossRefGoogle Scholar
  131. 131.
    Bergey GK, Morrell MJ, Mizrahi EM, Goldman A, King-Stephens D, Nair D, Srinivasan S, Jobst B, Gross RE, Shields DC, Barkley G, Salanova V, Olejniczak P, Cole A, Cash SS, Noe K, Wharen R, Worrell G, Murro AM, Edwards J, Duchowny M, Spencer D, Smith M, Geller E, Gwinn R, Skidmore C, Eisenschenk S, Berg M, Heck C, Van Ness P, Fountain N, Rutecki P, Massey A, O’Donovan C, Labar D, Duckrow RB, Hirsch LJ, Courtney T, Sun FT, Seale CG. Long-term treatment with responsive brain stimulation in adults with refractory partial seizures. Neurology. 2015;84:810–7.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Larkin M, Meyer RM, Szuflita NS, Severson MA, Levine ZT. Post-traumatic, drug-resistant epilepsy and review of seizure control outcomes from blinded, randomized controlled trials of brain stimulation treatments for drug-resistant epilepsy. Cureus. 2016;8:e744.PubMedPubMedCentralGoogle Scholar
  133. 133.
    Huang L, van Luijtelaar G. The effects of responsive and scheduled subicular high frequency stimulation in the intra-hippocampal kainic acid seizure model. Epilepsy Res. 2013;106(3):326–37.PubMedCrossRefGoogle Scholar
  134. 134.
    Valentin A, Ughratdar I, Cheserem B, Morris R, Selway R, Alarcon G. Epilepsia partialis continua responsive to neocortical electrical stimulation. Epilepsia. 2015;56:e104–9.PubMedCrossRefGoogle Scholar
  135. 135.
    Alarcon G, Martinez J, Kerai SV, Lacruz ME, Quiroga RQ, Selway RP, Richardson MP, Garcia Seoane JJ, Valentin A. In vivo neuronal firing patterns during human epileptiform discharges replicated by electrical stimulation. Clin Neurophysiol. 2012;123:1736–44.PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Chabardes S, Kahane P, Minotti L, Koudsie A, Hirsch E, Benabid AL. Deep brain stimulation in epilepsy with particular reference to the subthalamic nucleus. Epileptic Disord. 2002;4(Suppl 3):S83–93.PubMedGoogle Scholar
  137. 137.
    Cooper IS, Upton AR. Therapeutic implications of modulation of metabolism and functional activity of cerebral cortex by chronic stimulation of cerebellum and thalamus. Biol Psychiatry. 1985;20:811–3.PubMedCrossRefGoogle Scholar
  138. 138.
    Franzini A, Messina G, Marras C, Villani F, Cordella R, Broggi G. Deep brain stimulation of two unconventional targets in refractory non-resectable epilepsy. Stereotact Funct Neurosurg. 2008;86:373–81.PubMedCrossRefGoogle Scholar
  139. 139.
    Upton AR, Cooper IS, Springman M, Amin I. Suppression of seizures and psychosis of limbic system origin by chronic stimulation of anterior nucleus of the thalamus. Int J Neurol. 1985;19-20:223–30.PubMedGoogle Scholar
  140. 140.
    Velasco F, Velasco M, Ogarrio C, Fanghanel G. Electrical stimulation of the centromedian thalamic nucleus in the treatment of convulsive seizures: a preliminary report. Epilepsia. 1987;28:421–30.PubMedCrossRefGoogle Scholar
  141. 141.
    Graber KD, Fisher RS. Deep brain stimulation for epilepsy: animal models. Bethesda, MD: National Center for Biotechnology Information; 2012.CrossRefGoogle Scholar
  142. 142.
    Fisher R, Salanova V, Witt T, Worth R, Henry T, Gross R, Oommen K, Osorio I, Nazzaro J, Labar D, Kaplitt M, Sperling M, Sandok E, Neal J, Handforth A, Stern J, DeSalles A, Chung S, Shetter A, Bergen D, Bakay R, Henderson J, French J, Baltuch G, Rosenfeld W, Youkilis A, Marks W, Garcia P, Barbaro N, Fountain N, Bazil C, Goodman R, McKhann G, Babu Krishnamurthy K, Papavassiliou S, Epstein C, Pollard J, Tonder L, Grebin J, Coffey R, Graves N. Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy. Epilepsia. 2010;51:899–908.PubMedCrossRefGoogle Scholar
  143. 143.
    Salanova V, Witt T, Worth R, Henry TR, Gross RE, Nazzaro JM, Labar D, Sperling MR, Sharan A, Sandok E, Handforth A, Stern JM, Chung S, Henderson JM, French J, Baltuch G. Long-term efficacy and safety of thalamic stimulation for drug-resistant partial epilepsy. Neurology. 2015;84(10):1017–25.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Fisher RS, Velasco AL. Electrical brain stimulation for epilepsy. Nat Rev Neurol. 2014;10:261–70.PubMedCrossRefGoogle Scholar
  145. 145.
    Valentin A, Nguyen HQ, Skupenova AM, Agirre-Arrizubieta Z, Jewell S, Mullatti N, Moran NF, Richardson MP, Selway RP, Alarcon G. Centromedian thalamic nuclei deep brain stimulation in refractory status epilepticus. Brain Stimul. 2012;5:594–8.PubMedCrossRefGoogle Scholar
  146. 146.
    Lado FA. Chronic bilateral stimulation of the anterior thalamus of kainate-treated rats increases seizure frequency. Epilepsia. 2006;47:27–32.PubMedCrossRefGoogle Scholar
  147. 147.
    Wyckhuys T, Raedt R, Vonck K, Wadman W, Boon P. Comparison of hippocampal deep brain stimulation with high (130Hz) and low frequency (5Hz) on after discharges in kindled rats. Epilepsy Res. 2010;88:239–46.PubMedCrossRefGoogle Scholar
  148. 148.
    Tyrand R, Seeck M, Spinelli L, Pralong E, Vulliemoz S, Foletti G, Rossetti AO, Allali G, Lantz G, Pollo C, Boex C. Effects of amygdala-hippocampal stimulation on interictal epileptic discharges. Epilepsy Res. 2012;99:87–93.PubMedCrossRefGoogle Scholar
  149. 149.
    Velasco M, Velasco F, Velasco AL, Jimenez F, Brito F, Marquez I. Acute and chronic electrical stimulation of the centromedian thalamic nucleus: modulation of reticulo-cortical systems and predictor factors for generalized seizure control. Arch Med Res. 2000;31:304–15.PubMedCrossRefGoogle Scholar
  150. 150.
    Bjerknes S, Skogseid IM, Saehle T, Dietrichs E, Toft M. Surgical site infections after deep brain stimulation surgery: frequency, characteristics and management in a 10-year period. PLoS One. 2014;9:e105288.PubMedPubMedCentralCrossRefGoogle Scholar
  151. 151.
    Ching J, Khan S, White P, Reed J, Ramnarine D, Sieradzan K, Sandeman D. Long-term effectiveness and tolerability of vagal nerve stimulation in adults with intractable epilepsy: a retrospective analysis of 100 patients. Br J Neurosurg. 2013;27:228–34.PubMedCrossRefGoogle Scholar
  152. 152.
    Vonck K, Raedt R, Naulaerts J, De Vogelaere F, Thiery E, Van Roost D, Aldenkamp B, Miatton M, Boon P. Vagus nerve stimulation…25 years later! What do we know about the effects on cognition? Neurosci Biobehav Rev. 2014;45:63–71.PubMedCrossRefGoogle Scholar
  153. 153.
    Elliott RE, Morsi A, Kalhorn SP, Marcus J, Sellin J, Kang M, Silverberg A, Rivera E, Geller E, Carlson C, Devinsky O, Doyle WK. Vagus nerve stimulation in 436 consecutive patients with treatment-resistant epilepsy: long-term outcomes and predictors of response. Epilepsy Behav. 2011;20:57–63.PubMedCrossRefGoogle Scholar
  154. 154.
    Granbichler CA, Nashef L, Selway R, Polkey CE. Mortality and SUDEP in epilepsy patients treated with vagus nerve stimulation. Epilepsia. 2015;56:291–6.PubMedCrossRefGoogle Scholar
  155. 155.
    Loring DW, Kapur R, Meador KJ, Morrell MJ. Differential neuropsychological outcomes following targeted responsive neurostimulation for partial-onset epilepsy. Epilepsia. 2015;56:1836–44.PubMedCrossRefGoogle Scholar
  156. 156.
    Morrell M, Hirsch L, Bergey G, et al. Long-term safety and efficacy of the RNS™ system in adults with medically intractable partial onset seizures. Presented at the American Epilepsy Society 62nd Annual Meeting. Seattle, WA; December 8, 2008.Google Scholar
  157. 157.
    Daniele A, Albanese A, Contarino MF, Zinzi P, Barbier A, Gasparini F, Romito LM, Bentivoglio AR, Scerrati M. Cognitive and behavioural effects of chronic stimulation of the subthalamic nucleus in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry. 2003;74:175–82.PubMedPubMedCentralCrossRefGoogle Scholar
  158. 158.
    Hershey T, Revilla FJ, Wernle A, Gibson PS, Dowling JL, Perlmutter JS. Stimulation of STN impairs aspects of cognitive control in PD. Neurology. 2004;62:1110–4.PubMedCrossRefGoogle Scholar
  159. 159.
    Kleiner-Fisman G, Fisman DN, Sime E, Saint-Cyr JA, Lozano AM, Lang AE. Long-term follow up of bilateral deep brain stimulation of the subthalamic nucleus in patients with advanced Parkinson disease. J Neurosurg. 2003;99:489–95.PubMedCrossRefGoogle Scholar
  160. 160.
    Doshi PK, Chhaya N, Bhatt MH. Depression leading to attempted suicide after bilateral subthalamic nucleus stimulation for Parkinson's disease. Mov Disord. 2002;17:1084–5.PubMedCrossRefGoogle Scholar
  161. 161.
    Nagel SJ, Najm IM. Deep brain stimulation for epilepsy. Neuromodulation. 2009;12:270–80.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.Beijing Key Laboratory of Epilepsy, Department of Neurology, Center of Epilepsy, Beijing Institute for Brain DisordersSanbo Brain Hospital Capital Medical UniversityBeijingChina
  2. 2.Chongqing Key Laboratory of Neurology, Department of NeurologyThe First Affiliated Hospital of Chongqing Medical UniversityChongqingChina

Personalised recommendations