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CC BY-NC-ND 4.0 · Arq Neuropsiquiatr 2018; 76(11): 783-790
DOI: 10.1590/0004-282X20180130
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Neurocysticercosis as a probable risk factor for hippocampal sclerosis

Neurocisticercose como provável fator de risco para esclerose hipocampal

Authors

  • Gagandeep Singh

    1   Dayanand Medical College, Department of Neurology, Ludhiana, India,
    2   NIHR University College London Hospitals Biomedical Research Centre, UCL Queen Square Institute of Neurology, London WC1N 3BG, United Kingdom;

  • Josemir W. Sander

    2   NIHR University College London Hospitals Biomedical Research Centre, UCL Queen Square Institute of Neurology, London WC1N 3BG, United Kingdom;
    3   Stichting Epilepsie Instellingen Nederland (SEIN), Achterweg 5, Heemstede, Netherlands
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ABSTRACT

Neurocysticercosis is one of the most common risk factors for epilepsy but its association with drug-resistant epilepsy remains uncertain. Conjectures of an association with drug-resistant epilepsy have been fueled by reports of an association between calcific neurocysticercosis lesions (CNL) and hippocampal sclerosis (HS) from specialized epilepsy centers in Taenia solium-endemic regions. The debate arising from these reports is whether the association is causal. Evidence for the association is not high quality but sufficiently persuasive to merit further investigation with longitudinal imaging studies in population-based samples from geographically-diverse regions. The other controversial point is the choice of a surgical approach for drug-resistant epilepsy associated with CNL-HS. Three approaches have been described: standard anteromesial temporal lobectomy, lesionectomy involving a CNL alone and lesionectomy with anteromesial temporal lobectomy (for dual pathology); reports of the latter two approaches are limited. Presurgical evaluation should consider possibilities of delineating the epileptogenic zone/s in accordance with all three approaches.

RESUMO

A neurocisticercose é um dos mais comuns fatores de risco para a epilepsia, mas sua associação com a epilepsia resistente a medicamentos (DRE) permanece incerta. Conjecturas de uma associação com a DRE têm sido alimentadas por relatos de uma associação entre lesões de neurocisticercose calcária (CNL) e esclerose hipocampal (HS) de centros especializados em epilepsia em regiões endêmicas de Taenia solium. O debate que surge desses relatórios é se a associação é causal. Se bem as evidências para a associação não são de alta qualidade, são suficientemente persuasivas para merecer mais investigação com estudos longitudinais de imagens em amostras de base populacional de regiões geograficamente diversas. O outro ponto controverso é a escolha da abordagem cirúrgica para a DRE associada à CNL-HS. Três abordagens têm sido descritas: lobectomia temporal ântero-mesial padrão, lesionectomia envolvendo apenas CNL e lesionectomia com lobectomia temporal ântero-mesial (para patologia dupla); os relatórios das duas últimas abordagens são limitados. A avaliação pré-cirúrgica deve considerar as possibilidades de delinear a (s) zona (s) epileptogênica (s) de acordo com as três abordagens.

Keywords:

Drug resistant epilepsy - neurocysticercosis - epilepsy

Palavras-chave:

Epilepsia resistente a medicamentos - neurocisticercose - epilepsia


Publication History

Received: 04 June 2018

Accepted: 09 August 2018

Article published online:
22 August 2023

© 2023. Academia Brasileira de Neurologia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commecial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 Del Brutto OH. Neurocysticercosis: a review. Sci World J. 2012;2012:159821. https://doi.org/10.1100/2012/159821
  • 2 World Health Organization. Taenaisis/cysticercosis: fact sheet. Geneve: World Health Organization; 2017 [cited 2017 May 3]. Available from: http://www.who.int/mediacentre/factsheets/fs376/en/
  • 3 Montano SM, Villaran MV, Ylquimiche L, Figueroa JJ, Rodriguez S, Bautista CT et al. Neurocysticercosis: association between seizures, serology, and brain CT in rural Peru. Neurology. 2005 Jul;65(2):229-33. https://doi.org/10.1212/01.wnl.0000168828.83461.09
  • 4 Medina MT, Aguilar-Estrada RL, Alvarez A, Durón RM, Martínez L, Dubón S et al. Reduction in rate of epilepsy from neurocysticercosis by community interventions: the Salamá, Honduras study. Epilepsia. 2011 Jun;52(6):1177-85. https://doi.org/10.1111/j.1528-1167.2010.02945.x
  • 5 Singh G, Bawa J, Chinna D, Chaudhary A, Saggar K, Modi M et al. Association between epilepsy and cysticercosis and toxocariasis: a population-based case-control study in a slum in India. Epilepsia. 2012 Dec;53(12):2203-8. https://doi.org/10.1111/epi.12005
  • 6 Rajshekhar V, Raghava MV, Prabhakaran V, Oommen A, Muliyil J. Active epilepsy as an index of burden of neurocysticercosis in Vellore district, India. Neurology. 2006 Dec;67(12):2135-9. https://doi.org/10.1212/01.wnl.0000249113.11824.64
  • 7 Carabin H, Ndimubanzi PC, Budke CM, Nguyen H, Qian Y, Cowan LD et al. Clinical manifestations associated with neurocysticercosis: a systematic review. PLoS Negl Trop Dis. 2011 May;5(5):e1152. https://doi.org/10.1371/journal.pntd.0001152
  • 8 Carpio A, Hauser WA. Prognosis for seizure recurrence in patients with newly diagnosed neurocysticercosis. Neurology. 2002 Dec;59(11):1730-4. https://doi.org/10.1212/01.WNL.0000036320.69823.EA
  • 9 Del Brutto OH, Santibañez R, Noboa CA, Aguirre R, Díaz E, Alarcón TA. Epilepsy due to neurocysticercosis: analysis of 203 patients. Neurology. 1992 Feb;42(2):389-92. https://doi.org/10.1212/WNL.42.2.389
  • 10 Singla M, Singh P, Kaushal S, Bansal R, Singh G. Hippocampal sclerosis in association with neurocysticercosis. Epileptic Disord. 2007 Sep;9(3):292-9. https://doi.org/10.1684/epd.2007.0122
  • 11 Rathore C, Thomas B, Kesavadas C, Abraham M, Radhakrishnan K. Calcified neurocysticercosis lesions and antiepileptic drug-resistant epilepsy: a surgically remediable syndrome? Epilepsia. 2013 Oct;54(10):1815-22. https://doi.org/10.1111/epi.12349
  • 12 Chandra PS, Bal C, Garg A, Gaikwad S, Prasad K, Sharma BS et al. Surgery for medically intractable epilepsy due to postinfectious etiologies. Epilepsia. 2010 Jun;51(6):1097-100. https://doi.org/10.1111/j.1528-1167.2010.02538.x
  • 13 Pradhan S, Kathuria MK, Gupta RK. Perilesional gliosis and seizure outcome: a study based on magnetization transfer magnetic resonance imaging in patients with neurocysticercosis. Ann Neurol. 2000 Aug;48(2):181-7. https://doi.org/10.1002/1531-8249(200008)48:2<181::AID-ANA7>3.0.CO;2-C
  • 14 de Souza A, Nalini A, Kovoor JM, Yeshraj G, Siddalingaiah HS, Thennarasu K. Perilesional gliosis around solitary cerebral parenchymal cysticerci and long-term seizure outcome: a prospective study using serial magnetization transfer imaging. Epilepsia. 2011 Oct;52(10):1918-27. https://doi.org/10.1111/j.1528-1167.2011.03189.x
  • 15 Leite JP, Terra-Bustamante VC, Fernandes RM, Santos AC, Chimelli L, Sakamoto AC et al. Calcified neurocysticercotic lesions and postsurgery seizure control in temporal lobe epilepsy. Neurology. 2000 Nov;55(10):1485-91. https://doi.org/10.1212/WNL.55.10.1485
  • 16 Velasco TR, Zanello PA, Dalmagro CL, Araújo D Jr, Santos AC, Bianchin MM et al. Calcified cysticercotic lesions and intractable epilepsy: a cross sectional study of 512 patients. J Neurol Neurosurg Psychiatry. 2006 Apr;77(4):485-8. https://doi.org/10.1136/jnnp.2005.078675
  • 17 Singh G, Burneo JG, Sander JW. From seizures to epilepsy and its substrates: neurocysticercosis. Epilepsia. 2013 May;54(5):783-92. https://doi.org/10.1111/epi.12159
  • 18 Durnford AJ, Rodgers W, Kirkham FJ, Mullee MA, Whitney A, Prevett M et al. Very good inter-rater reliability of Engel and ILAE epilepsy surgery outcome classifications in a series of 76 patients. Seizure. 2011 Dec;20(10):809-12. https://doi.org/10.1016/j.seizure.2011.08.004
  • 19 Kobayashi E, Guerreiro CA, Cendes F. Late onset temporal lobe epilepsy with MRI evidence of mesial temporal sclerosis following acute neurocysticercosis: case report. Arq Neuropsiquiatr. 2001 Jun;59 2-A:255-8. https://doi.org/10.1590/S0004-282X2001000200021
  • 20 Chung CK, Lee SK, Chi JG. Temporal lobe epilepsy caused by intrahippocampal calcified cysticercus: a case report. J Korean Med Sci. 1998 Aug;13(4):445-8. https://doi.org/10.3346/jkms.1998.13.4.445
  • 21 Silva AV, Martins HH, Marques CM, Yacubian EM, Sakamoto AC, Carrete Junior H et al. Neurocysticercosis and microscopic hippocampal dysplasia in a patient with refractory mesial temporal lobe epilepsy. Arq Neuropsiquiatr. 2006 Jun;64(2A):309-13. https://doi.org/10.1590/S0004-282X2006000200026
  • 22 Son EI, Yi SD, Lee SW, Lee HC, Yim MB, Kim IH. Surgery for seizure-related structural lesions of the brain with intraoperative acute recording(ECoG) and functional mapping. J Korean Med Sci. 1994 Oct;9(5):409-13. https://doi.org/10.3346/jkms.1994.9.5.409
  • 23 Ooi WW, Wijemanne S, Thomas CB, Quezado M, Brown CR, Nash TE. Short report: A calcified Taenia solium granuloma associated with recurrent perilesional edema causing refractory seizures: histopathological features. Am J Trop Med Hyg. 2011 Sep;85(3):460-3. https://doi.org/10.4269/ajtmh.2011.11-0221
  • 24 Lee DJ, Owen CM, Khanifar E, Kim RC, Binder DK. Isolated amygdala neurocysticercosis in a patient presenting with déjà vu and olfactory auras. Case report. J Neurosurg Pediatr. 2009 Jun;3(6):538-41. https://doi.org/10.3171/2009.2.PEDS08140
  • 25 Hasan MS, Basri HB, Hin LP, Stanslas J. Surgical remotion of a cysticercotic granuloma responsible for refractory seizures: A case report. Surg Neurol Int. 2011;2(1):177-9. https://doi.org/10.4103/2152-7806.90698
  • 26 da Gama CN, Kobayashi E, Li LM, Cendes F. Hippocampal atrophy and neurocysticercosis calcifications. Seizure. 2005 Mar;14(2):85-8. https://doi.org/10.1016/j.seizure.2004.10.005
  • 27 Bianchin MM, Velasco TR, Coimbra ER, Gargaro AC, Escorsi-Rosset SR, Wichert-Ana L et al. Cognitive and surgical outcome in mesial temporal lobe epilepsy associated with hippocampal sclerosis plus neurocysticercosis: a cohort study. PLoS One. 2013 Apr;8(4):e60949. https://doi.org/10.1371/journal.pone.0060949
  • 28 Bianchin MM, Velasco TR, Wichert-Ana L, Araújo Junior D, Alexandre Junior V, Scornavacca F et al. Neuroimaging observations linking neurocysticercosis and mesial temporal lobe epilepsy with hippocampal sclerosis. Epilepsy Res. 2015 Oct;116:34-9. https://doi.org/10.1016/j.eplepsyres.2015.07.001
  • 29 Rathore C, Thomas B, Kesavadas C, Radhakrishnan K. Calcified neurocysticercosis lesions and hippocampal sclerosis: potential dual pathology? Epilepsia. 2012 Apr;53(4):e60-2. https://doi.org/10.1111/j.1528-1167.2011.03386.x
  • 30 Taveira MO, Morita ME, Yasuda CL, Coan AC, Secolin R, Costs ALC et al. Neurocysticercotic calcifications and hippocampal sclerosis: A case-control study. PLoS One. 2015;10: https://doi.org/10.1371/journal.pone.0131180
  • 31 Oliveira MC, Martin MG, Tsunemi MH, Vieira G, Castro LH. Small calcified lesions suggestive of neurocysticercosis are associated with mesial temporal sclerosis. Arq Neuropsiquiatr. 2014 Jul;72(7):510-6. https://doi.org/10.1590/0004-282X20140080
  • 32 Bianchin MM, Velasco TR, Araujo Junior D, Alexandre V Jr, Wichert-Ana L, Vera C et al. Clinical and electrophysiological differences between mesial temporal lobe epilepsy and mesial temporal lobe epilepsy plus neurocysticercosis [Abstract]. Epilepsia. 2006;4 suppl 4:244-5.
  • 33 Cruz ME, Cruz I, Preux PM, Schantz P, Dumas M. Headache and cysticercosis in Ecuador, South America. Headache. 1995 Feb;35(2):93-7. https://doi.org/10.1111/j.1526-4610.1995.hed3502093.x
  • 34 Garg RK, Kar AM, Singh MK. Prednisolone-responsive headache in patients with solitary cysticercus granuloma and seizures. Headache. 2004 Apr;44(4):365-9. https://doi.org/10.1111/j.1526-4610.2004.04096.x
  • 35 Del Brutto OH, Salgado P, Lama J, Del Brutto VJ, Campos X, Zambrano M et al. Calcified neurocysticercosis associates with hippocampal atrophy: a population-based study. Am J Trop Med Hyg. 2015 Jan;92(1):64-8. https://doi.org/10.4269/ajtmh.14-0453
  • 36 Del Brutto OH, Issa NP, Salgado P, Del Brutto VJ, Zambrano M, Lama J et al. The association between neurocysticercosis and hippocampal atropy is related to age. Am J Trop Med Hyg. 2017 Jan;96(1):243-8. https://doi.org/10.4269/ajtmh.16-0689
  • 37 Cendes F, Andermann F, Dubeau F, Gloor P, Evans A, Jones-Gotman M, et al. Early childhood prolonged febrile convulsions, atrophy and sclerosis of mesial structures, and temporal lobe epilepsy: an MRI volumetric study. Neurology. 1993 Jun;43(6):1083-7. https://doi.org/10.1212/WNL.43.6.1083
  • 38 Cendes F. Febrile seizures and mesial temporal sclerosis. Curr Opin Neurol. 2004 Apr;17(2):161-4. https://doi.org/10.1097/00019052-200404000-00013
  • 39 French JA, Williamson PD, Thadani VM, Darcey TM, Mattson RH, Spencer SS, et al. Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination. Ann Neurol. 1993 Dec;34(6):774-80. https://doi.org/10.1002/ana.410340604
  • 40 Rangel R, Torres B, Del Bruto O, Sotelo J. Cysticercotic encephalitis: a severe form in young females. Am J Trop Med Hyg. 1987 Mar;36(2):387-92. https://doi.org/10.4269/ajtmh.1987.36.387
  • 41 Höfler M. The Bradford Hill considerations on causality: a counterfactual perspective. Emerg Themes Epidemiol. 2005 Nov;2(1):11. https://doi.org/10.1186/1742-7622-2-11
  • 42 Stringer JL, Marks LM, White AC Jr, Robinson P. Epileptogenic activity of granulomas associated with murine cysticercosis. Exp Neurol. 2003 Oct;183(2):532-6. https://doi.org/10.1016/S0014-4886(03)00179-1
  • 43 Escalaya AL, Burneo JG. Epilepsy surgery and neurocysticercosis: assessing the role of the cysticercotic lesion in medically-refractory epilepsy. Epilepsy Behav. 2017 Nov;76:178-81. https://doi.org/10.1016/j.yebeh.2017.01.029
  • 44 Cruz ME, Schantz PM, Cruz I, Espinosa P, Preux PM, Cruz A et al. Epilepsy and neurocysticercosis in an Andean community. Int J Epidemiol. 1999 Aug;28(4):799-803. https://doi.org/10.1093/ije/28.4.799
  • 45 Fleury A, Gomez T, Alvarez I, Meza D, Huerta M, Chavarria A et al. High prevalence of calcified silent neurocysticercosis in a rural village of Mexico. Neuroepidemiology. 2003 Mar-Apr;22(2):139-45. https://doi.org/10.1159/000068748