1921
Volume 103, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

The parasitic helminth infection neurocysticercosis (NCC) is the most common cause of adult-acquired epilepsy in the world. Despite the serious consequences of epilepsy due to this infection, an in-depth review of the distinct characteristics of epilepsy due to neurocysticercosis has never been conducted. In this review, we evaluate the relationship between NCC and epilepsy and the unique characteristics of epilepsy caused by NCC. We also discuss recent advances in our understanding of NCC-related epilepsy, including the importance of anti-inflammatory therapies, the association between NCC and temporal lobe epilepsy, and the recent discovery of biomarkers of severe epilepsy development in individuals with NCC and seizures.

[open-access] This is an open-access article distributed under the terms of the Creative Commons Attribution (CC-BY) License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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References

  1. Bern C, Garcia HH, Evans C, Gonzalez AE, Verastegui M, Tsang VC, Gilman RH, 1999. Magnitude of the disease burden from neurocysticercosis in a developing country. Clin Infect Dis 29: 12031209.
    [Google Scholar]
  2. Del Brutto OH, Arroyo G, Del Brutto VJ, Zambrano M, Garcia HH, 2017. On the relationship between calcified neurocysticercosis and epilepsy in an endemic village: a large-scale, computed tomography-based population study in rural Ecuador. Epilepsia 58: 19551961.
    [Google Scholar]
  3. Del Brutto OH et al., 2005. Epilepsy and neurocysticercosis in Atahualpa: a door-to-door survey in rural coastal Ecuador. Epilepsia 46: 583587.
    [Google Scholar]
  4. Garcia HH, Talley A, Gilman RH, Zorrilla L, Pretell J, 1999. Epilepsy and neurocysticercosis in a village in Huaraz, Peru. Clin Neurol Neurosurg 101: 225228.
    [Google Scholar]
  5. Garcia-Noval J, Moreno E, de Mata F, Soto de Alfaro H, Fletes C, Craig PS, Allan JC, 2001. An epidemiological study of epilepsy and epileptic seizures in two rural Guatemalan communities. Ann Trop Med Parasitol 95: 167175.
    [Google Scholar]
  6. Medina MT, Rosas E, Rubio-Donnadieu F, Sotelo J, 1990. Neurocysticercosis as the main cause of late-onset epilepsy in Mexico. Arch Intern Med 150: 325327.
    [Google Scholar]
  7. Millogo A et al., 2012. Prevalence of neurocysticercosis among people with epilepsy in rural areas of Burkina Faso. Epilepsia 53: 21942202.
    [Google Scholar]
  8. Moyano LM et al., 2014. Neurocysticercosis as a cause of epilepsy and seizures in two community-based studies in a cysticercosis-endemic region in Peru. PLoS Negl Trop Dis 8: e2692.
    [Google Scholar]
  9. Pondja A, Neves L, Mlangwa J, Afonso S, Fafetine J, Willingham AL 3rd, Thamsborg SM, Johansen MV, 2010. Prevalence and risk factors of porcine cysticercosis in Angonia district, Mozambique. PLoS Negl Trop Dis 4: e594.
    [Google Scholar]
  10. Prasad KN, Prasad A, Gupta RK, Nath K, Pradhan S, Tripathi M, Pandey CM, 2009. Neurocysticercosis in patients with active epilepsy from the pig farming community of Lucknow district, north India. Trans R Soc Trop Med Hyg 103: 144150.
    [Google Scholar]
  11. Rottbeck R et al., 2013. High prevalence of cysticercosis in people with epilepsy in southern Rwanda. PLoS Negl Trop Dis 7: e2558.
    [Google Scholar]
  12. Villaran MV et al., 2009. Epilepsy and neurocysticercosis: an incidence study in a Peruvian rural population. Neuroepidemiology 33: 2531.
    [Google Scholar]
  13. Fisher RS et al., 2017. Operational classification of seizure types by the International League Against Epilepsy: position paper of the ILAE commission for classification and terminology. Epilepsia 58: 522530.
    [Google Scholar]
  14. Engel J Jr. et al., 2013. Epilepsy biomarkers. Epilepsia 54 (Suppl 4): 6169.
    [Google Scholar]
  15. Carpio A, Romo ML, 2015. Multifactorial basis of epilepsy in patients with neurocysticercosis. Epilepsia 56: 973974.
    [Google Scholar]
  16. Cantu C, Barinagarrementeria F, 1996. Cerebrovascular complications of neurocysticercosis. Clinical and neuroimaging spectrum. Arch Neurol 53: 233239.
    [Google Scholar]
  17. Del Brutto OH, 1992. Cysticercosis and cerebrovascular disease: a review. J Neurol Neurosurg Psychiatry 55: 252254.
    [Google Scholar]
  18. Herrick JA et al., Cysticercosis Working Group in Peru, 2018. Inflammation is a key risk factor for persistent seizures in neurocysticercosis. Ann Clin Transl Neurol 5: 630639.
    [Google Scholar]
  19. Lachuriya G, Garg RK, Jain A, Malhotra HS, Singh AK, Jain B, Kumar N, Verma R, Sharma PK, 2016. Toll-like receptor-4 polymorphisms and serum matrix metalloproteinase-9 in newly diagnosed patients with calcified neurocysticercosis and seizures. Medicine (Baltimore) 95: e3288.
    [Google Scholar]
  20. Verma A, Prasad KN, Nyati KK, Singh SK, Singh AK, Paliwal VK, Gupta RK, 2011. Association of MMP-2 and MMP-9 with clinical outcome of neurocysticercosis. Parasitology 138: 14231428.
    [Google Scholar]
  21. Singh G, Burneo JG, Sander JW, 2013. From seizures to epilepsy and its substrates: neurocysticercosis. Epilepsia 54: 783792.
    [Google Scholar]
  22. Loeb JA, Sohrab SA, Huq M, Fuerst DR, 2006. Brain calcifications induce neurological dysfunction that can be reversed by a bone drug. J Neurol Sci 243: 7781.
    [Google Scholar]
  23. Nash TE et al., 2004. Calcific neurocysticercosis and epileptogenesis. Neurology 62: 19341938.
    [Google Scholar]
  24. Nash TE, Bartelt LA, Korpe PS, Lopes B, Houpt ER, 2014. Calcified neurocysticercus, perilesional edema, and histologic inflammation. Am J Trop Med Hyg 90: 318321.
    [Google Scholar]
  25. Ooi WW, Wijemanne S, Thomas CB, Quezado M, Brown CR, Nash TE, 2011. Short report: a calcified Taenia solium granuloma associated with recurrent perilesional edema causing refractory seizures: histopathological features. Am J Trop Med Hyg 85: 460463.
    [Google Scholar]
  26. Bruno E, Bartoloni A, Zammarchi L, Strohmeyer M, Bartalesi F, Bustos JA, Santivanez S, Garcia HH, Nicoletti A; COHEMI Project Study Group, 2013. Epilepsy and neurocysticercosis in Latin America: a systematic review and meta-analysis. PLoS Negl Trop Dis 7: e2480.
    [Google Scholar]
  27. DeGiorgio CM, Medina MT, Duron R, Zee C, Escueta SP, 2004. Neurocysticercosis. Epilepsy Curr 4: 107111.
    [Google Scholar]
  28. de Souza A, Nalini A, Kovoor JM, Yeshraj G, Siddalingaiah HS, Thennarasu K, 2011. Perilesional gliosis around solitary cerebral parenchymal cysticerci and long-term seizure outcome: a prospective study using serial magnetization transfer imaging. Epilepsia 52: 19181927.
    [Google Scholar]
  29. Begley CE et al., 2000. The cost of epilepsy in the United States: an estimate from population-based clinical and survey data. Epilepsia 41: 342351.
    [Google Scholar]
  30. EUCARE, 2003. European white paper on epilepsy. Epilepsia 44 (Suppl 6): 188.
    [Google Scholar]
  31. Forsgren L, Bucht G, Eriksson S, Bergmark L, 1996. Incidence and clinical characterization of unprovoked seizures in adults: a prospective population-based study. Epilepsia 37: 224229.
    [Google Scholar]
  32. Forsgren L, Hauser WA, Olafsson E, Sander JW, Sillanpaa M, Tomson T, 2005. Mortality of epilepsy in developed countries: a review. Epilepsia 46 (Suppl 11): 1827.
    [Google Scholar]
  33. O’Neal SE, Flecker RH, 2015. Hospitalization frequency and charges for neurocysticercosis, United States, 2003–2012. Emerg Infect Dis 21: 969976.
    [Google Scholar]
  34. Shihabuddin BS, Herlopian AS, Greenfield LJ Jr., 2014. Ictal asystole in epilepsy patients undergoing inpatient video-EEG monitoring. Neurosciences (Riyadh) 19: 317321.
    [Google Scholar]
  35. National Center for Chronic Disease Prevention and Health Promotion DoPH, 2017. Centers for Disease Control, At A Glance 2016: Epilepsy, One of the Nation’s Most Common Neurological Conditions. Available at: https://www.cdc.gov/chronicdisease/resources/publications/aag/epilepsy.htm. Accessed April 28, 2017.
    [Google Scholar]
  36. Del Brutto OH, 2012. Neurocysticercosis: a review. ScientificWorldJournal 2012: 159821.
    [Google Scholar]
  37. Garcia HH, Del Brutto OH, 2003. Imaging findings in neurocysticercosis. Acta Trop 87: 7178.
    [Google Scholar]
  38. Lerner A, Shiroishi MS, Zee CS, Law M, Go JL, 2012. Imaging of neurocysticercosis. Neuroimaging Clin N Am 22: 659676.
    [Google Scholar]
  39. Duque KR, Burneo JG, 2017. Clinical presentation of neurocysticercosis-related epilepsy. Epilepsy Behav 76: 151157.
    [Google Scholar]
  40. Garcia HH, Pretell EJ, Gilman RH, Martinez SM, Moulton LH, Del Brutto OH, Herrera G, Evans CA, Gonzalez AE; Cysticercosis Working Group in Peru, 2004. A trial of antiparasitic treatment to reduce the rate of seizures due to cerebral cysticercosis. N Engl J Med 350: 249258.
    [Google Scholar]
  41. Das K, Mondal GP, Banerjee M, Mukherjee BB, Singh OP, 2007. Role of antiparasitic therapy for seizures and resolution of lesions in neurocysticercosis patients: an 8 year randomised study. J Clin Neurosci 14: 11721177.
    [Google Scholar]
  42. Del Brutto OH, Santibanez R, Noboa CA, Aguirre R, Diaz E, Alarcon TA, 1992. Epilepsy due to neurocysticercosis: analysis of 203 patients. Neurology 42: 389392.
    [Google Scholar]
  43. Prasad A, Gupta RK, Pradhan S, Tripathi M, Pandey CM, Prasad KN, 2008. What triggers seizures in neurocysticercosis? A MRI-based study in pig farming community from a district of north India. Parasitol Int 57: 166171.
    [Google Scholar]
  44. Kelvin EA, Carpio A, Bagiella E, Leslie D, Leon P, Andrews H, Hauser WA, Ecuadorian Neurocysticercosis G, 2011. Seizure in people with newly diagnosed active or transitional neurocysticercosis. Seizure 20: 119125.
    [Google Scholar]
  45. Duque KR, Escalaya AL, Zapata W, Burneo JG, Bustos JA, Gonzales I, Saavedra H, Pretell EJ, Garcia HH; Cysticercosis Working Group in Peru, 2018. Clinical topography relationship in patients with parenchymal neurocysticercosis and seizures. Epilepsy Res 145: 145152.
    [Google Scholar]
  46. Murthy JM, Reddy VS, 1998. Clinical characteristics, seizure spread patterns and prognosis of seizures associated with a single small cerebral calcific CT lesion. Seizure 7: 153157.
    [Google Scholar]
  47. Singh G, Sachdev MS, Tirath A, Gupta AK, Avasthi G, 2000. Focal cortical-subcortical calcifications (FCSCs) and epilepsy in the Indian subcontinent. Epilepsia 41: 718726.
    [Google Scholar]
  48. Garcia HH et al., Cysticercosis Working Group in Peru, 2014. Efficacy of combined antiparasitic therapy with praziquantel and albendazole for neurocysticercosis: a double-blind, randomised controlled trial. Lancet Infect Dis 14: 687695.
    [Google Scholar]
  49. Bertram E, 2007. The relevance of kindling for human epilepsy. Epilepsia 48 (Suppl 2): 6574.
    [Google Scholar]
  50. Temkin NR, 2001. Antiepileptogenesis and seizure prevention trials with antiepileptic drugs: meta-analysis of controlled trials. Epilepsia 42: 515524.
    [Google Scholar]
  51. Goyal M, Chand P, Modi M, Khandelwal N, Kharbanda PS, Lal V, Singla V, Sehgal R, 2015. Neurocysticercosis: an uncommon cause of drug-refractory epilepsy in North Indian population. Epilepsia 56: 17471752.
    [Google Scholar]
  52. Burneo JG, Cavazos JE, 2014. Neurocysticercosis and epilepsy. Epilepsy Curr 14: 2328.
    [Google Scholar]
  53. Garcia HH, Del Brutto OH; Cysticercosis Working Group in Peru, 2017. Antiparasitic treatment of neurocysticercosis - the effect of cyst destruction in seizure evolution. Epilepsy Behav 76: 158162.
    [Google Scholar]
  54. de Souza A, Nalini A, Saini J, Thennarasu K, 2017. T2 relaxometry helps prognosticate seizure outcome in patients with solitary cerebral cysticercosis. J Neurol Sci 376: 16.
    [Google Scholar]
  55. Fujita M, Mahanty S, Zoghbi SS, Ferraris Araneta MD, Hong J, Pike VW, Innis RB, Nash TE, 2013. PET reveals inflammation around calcified Taenia solium granulomas with perilesional edema. PLoS One 8: e74052.
    [Google Scholar]
  56. Nash TE, Mahanty S, Garcia HH; Cysticercosis Group in Peru, 2011. Corticosteroid use in neurocysticercosis. Expert Rev Neurother 11: 11751183.
    [Google Scholar]
  57. Prasad A, Prasad KN, Gupta RK, Pradhan S, 2009. Increased expression of ICAM-1 among symptomatic neurocysticercosis. J Neuroimmunol 206: 118120.
    [Google Scholar]
  58. Verma A, Prasad KN, Gupta RK, Singh AK, Nyati KK, Rizwan A, Pandey CM, Paliwal VK, 2010. Toll-like receptor 4 polymorphism and its association with symptomatic neurocysticercosis. J Infect Dis 202: 12191225.
    [Google Scholar]
  59. Arroyo G et al., 2017. Antibody banding patterns of the enzyme-linked immunoelectrotransfer blot (EITB) and brain imaging findings in patients with neurocysticercosis. Clin Infect Dis 66: 282288.
    [Google Scholar]
  60. Gonzales I et al., 2015. Seizures, cysticercosis and rural-to-urban migration: the Peru MIGRANT study. Trop Med Int Health 20: 546552.
    [Google Scholar]
  61. Garcia HH, Gonzales I, Lescano AG, Bustos JA, Pretell EJ, Saavedra H, Nash TE; Cysticercosis Working Group in Peru, 2014. Enhanced steroid dosing reduces seizures during antiparasitic treatment for cysticercosis and early after. Epilepsia 55: 14521459.
    [Google Scholar]
  62. Mall RK, Agarwal A, Garg RK, Kar AM, Shukla R, 2003. Short course of prednisolone in Indian patients with solitary cysticercus granuloma and new-onset seizures. Epilepsia 44: 13971401.
    [Google Scholar]
  63. Cuello-Garcia CA, Roldan-Benitez YM, Perez-Gaxiola G, Villarreal-Careaga J, 2013. Corticosteroids for neurocysticercosis: a systematic review and meta-analysis of randomized controlled trials. Int J Infect Dis 17: e583e592.
    [Google Scholar]
  64. White AC Jr., Coyle CM, Rajshekhar V, Singh G, Hauser WA, Mohanty A, Garcia HH, Nash TE, 2018. Diagnosis and treatment of neurocysticercosis: 2017 clinical practice guidelines by the Infectious Diseases Society of America (IDSA) and the American Society of Tropical Medicine and Hygiene (ASTMH). Clin Infect Dis 66: 11591163.
    [Google Scholar]
  65. Zhao BC et al., 2016. Albendazole and corticosteroids for the treatment of solitary cysticercus granuloma: a network meta-analysis. PLoS Negl Trop Dis 10: e0004418.
    [Google Scholar]
  66. Suastegui Roman RA, Soto-Hernandez JL, Sotelo J, 1996. Effects of prednisone on ventriculoperitoneal shunt function in hydrocephalus secondary to cysticercosis: a preliminary study. J Neurosurg 84: 629633.
    [Google Scholar]
  67. Buchman AL, 2001. Side effects of corticosteroid therapy. J Clin Gastroenterol 33: 289294.
    [Google Scholar]
  68. Nash TE, Ware JM, Coyle CM, Mahanty S, 2019. Etanercept to control inflammation in the treatment of complicated neurocysticercosis. Am J Trop Med Hyg 100: 609616.
    [Google Scholar]
  69. Fleury A et al., 2003. High prevalence of calcified silent neurocysticercosis in a rural village of Mexico. Neuroepidemiology 22: 139145.
    [Google Scholar]
  70. Tellez-Zenteno JF, Hernandez-Ronquillo L, 2017. Epidemiology of neurocysticercosis and epilepsy, is everything described? Epilepsy Behav 76: 146150.
    [Google Scholar]
  71. Velasco TR et al., 2006. Calcified cysticercotic lesions and intractable epilepsy: a cross sectional study of 512 patients. J Neurol Neurosurg Psychiatry 77: 485488.
    [Google Scholar]
  72. Del Brutto OH, Salgado P, Lama J, Del Brutto VJ, Campos X, Zambrano M, Garcia HH, 2015. Calcified neurocysticercosis associates with hippocampal atrophy: a population-based study. Am J Trop Med Hyg 92: 6468.
    [Google Scholar]
  73. Oliveira MC, Martin MG, Tsunemi MH, Vieira G, Castro LH, 2014. Small calcified lesions suggestive of neurocysticercosis are associated with mesial temporal sclerosis. Arq Neuropsiquiatr 72: 510516.
    [Google Scholar]
  74. de Oliveira Taveira M, Morita ME, Yasuda CL, Coan AC, Secolin R, Luiz Cunha da Costa A, Cendes F, 2015. Neurocysticercotic calcifications and hippocampal sclerosis: a case-control study. PLoS One 10: e0131180.
    [Google Scholar]
  75. Thom M, 2014. Review: hippocampal sclerosis in epilepsy: a neuropathology review. Neuropathol Appl Neurobiol 40: 520543.
    [Google Scholar]
  76. Walker MC, 2015. Hippocampal sclerosis: causes and prevention. Semin Neurol 35: 193200.
    [Google Scholar]
  77. Bronen R, 1998. MR of mesial temporal sclerosis: how much is enough? AJNR Am J Neuroradiol 19: 1518.
    [Google Scholar]
  78. Jackson GD, Berkovic SF, Duncan JS, Connelly A, 1993. Optimizing the diagnosis of hippocampal sclerosis using MR imaging. AJNR Am J Neuroradiol 14: 753762.
    [Google Scholar]
  79. Bianchin MM, Velasco TR, Santos AC, Sakamoto AC, 2012. On the relationship between neurocysticercosis and mesial temporal lobe epilepsy associated with hippocampal sclerosis: coincidence or a pathogenic relationship? Pathog Glob Health 106: 280285.
    [Google Scholar]
  80. Rathore C, Thomas B, Kesavadas C, Radhakrishnan K, 2012. Calcified neurocysticercosis lesions and hippocampal sclerosis: potential dual pathology? Epilepsia 53: e60e62.
    [Google Scholar]
  81. Jama-Antonio JMC, Yasuda CL, Cendes F, 2019. Neurocysticercosis and hippocampal atrophy: MRI findings and the evolution of viable or calcified cysts in patients with neurocysticercosis. Front Neurol 10: 449.
    [Google Scholar]
  82. Bianchin MM et al., 2015. Neuroimaging observations linking neurocysticercosis and mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsy Res 116: 3439.
    [Google Scholar]
  83. Nash TE, Pretell J, Garcia HH, 2001. Calcified cysticerci provoke perilesional edema and seizures. Clin Infect Dis 33: 16491653.
    [Google Scholar]
  84. Singh AK, Garg RK, Rizvi I, Malhotra HS, Kumar N, Gupta RK, 2017. Clinical and neuroimaging predictors of seizure recurrence in solitary calcified neurocysticercosis: a prospective observational study. Epilepsy Res 137: 7883.
    [Google Scholar]
  85. Nash TE, Pretell EJ, Lescano AG, Bustos JA, Gilman RH, Gonzalez AE, Garcia HH; Cysticercosis Working Group in Peru, 2008. Perilesional brain oedema and seizure activity in patients with calcified neurocysticercosis: a prospective cohort and nested case-control study. Lancet Neurol 7: 10991105.
    [Google Scholar]
  86. Mejia R, Nash TE, 2013. Corticosteroid withdrawal precipitates perilesional edema around calcified Taenia solium cysts. Am J Trop Med Hyg 89: 919923.
    [Google Scholar]
  87. Chandra PS, Bal C, Garg A, Gaikwad S, Prasad K, Sharma BS, Sarkar C, Singh MB, Padma VM, Tripathi M, 2010. Surgery for medically intractable epilepsy due to postinfectious etiologies. Epilepsia 51: 10971100.
    [Google Scholar]
  88. Rathore C, Thomas B, Kesavadas C, Abraham M, Radhakrishnan K, 2013. Calcified neurocysticercosis lesions and antiepileptic drug-resistant epilepsy: a surgically remediable syndrome? Epilepsia 54: 18151822.
    [Google Scholar]
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  • Received : 27 Jun 2019
  • Accepted : 08 Apr 2020
  • Published online : 18 May 2020
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