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Taeniasis and Neurocysticercosis: Emerging Public Health Problems

  • Kashi Nath Prasad
  • Satyendra Kumar Singh
Chapter

Abstract

Taenia, one of the earliest recognized helminths, is a comparatively large genus with 42 known valid species. Three most commonly recognized species of human importance are T. solium and T. asiatica (pork tapeworms) and T. saginata (beef tapeworm). Adult tapeworms reside in human intestine, and the disease is called taeniasis. The larva (cysticercus) of only T. solium can infect internal organs of human, known as cysticercosis; when the larva infects the central nervous system (CNS) of the host, it is known as neurocysticercosis (NCC). NCC is the most severe form of the disease with considerable morbidity and mortality. It is considered as the most common cause of community-acquired epileptic seizure disorders. The life cycle of T. solium involves two hosts: humans are the only definitive host and accidental intermediate host, while pig is the natural intermediate host. The eggs passed through faeces by T. solium carriers contaminate the environment. Both human and pig can get infection (cysticercosis/NCC) through ingestion of eggs, while human acquires taeniasis through consumption of cysticercotic pork. T. solium infection is highly endemic in Africa, Asia and Latin America. Now developed world is also facing this problem due to human migration from Taenia endemic areas. Therapeutic measures for NCC-related active epilepsy include anti-epileptic drug(s) with or without steroids: surgery/placement of shunt is indicated for patients with raised intracranial pressure. Antiparasitic drug to kill the brain cysticerci remains controversial. Treatment of choice for taeniasis is niclosamide; alternatives are praziquantel and albendazole. The following measures such as antiparasitic therapy to eliminate Taenia carriers in endemic populations, health education, toilet facilities and handwash with soap, control on sale of measly pork, restriction on pig roaming and pig vaccination, etc. may help to control the disease.

Keywords

Albendazole Cysticercosis Neurocysticercosis Praziquantel Taeniasis Vaccination 

References

  1. Alvarez JI, Colegial CH, Castano CA, Trujillo J, Teale JM, Restrepo BI (2002) The human nervous tissue in proximity to granulomatous lesions induced by Taenia solium metacestodes displays an active response. J Neuroimmunol 127:139–144PubMedCrossRefGoogle Scholar
  2. Bandres JC, White AC Jr, Samo T, Murphy EC, Harris RL (1992) Extraparenchymal neurocysticercosis: report of five cases and review of management. Clin Infect Dis 15:799–811PubMedCrossRefGoogle Scholar
  3. Burneo JG, Plener I, Garcia HH (2009) Neurocysticercosis in a patient in Canada. CMAJ 180:639–642PubMedPubMedCentralCrossRefGoogle Scholar
  4. Bustos JA, Rodriguez S, Jimenez JA, Moyano LM, Castillo Y, Ayvar V, Allan JC, Craig PS, Gonzalez AE, Gilman RH, Tsang VC, Garcia HH (2012) Detection of Taenia solium taeniasis coproantigen is an early indicator of treatment failure for taeniasis. Clin Vaccine Immunol 19:570–573PubMedPubMedCentralCrossRefGoogle Scholar
  5. Carabin H, Ndimubanzi PC, Budke CM, Nguyen H, Qian Y, Cowan LD, Stoner JA, Rainwater E, Dickey M (2011) Clinical manifestations associated with neurocysticercosis: a systematic review. PLoS Negl Trop Dis 5:e1152PubMedPubMedCentralCrossRefGoogle Scholar
  6. Carpio A, Kelvin EA, Bagiella E, Leslie D, Leon P, Andrews H, Hauser WA (2008) Effects of albendazole treatment on neurocysticercosis: a randomised controlled trial. J Neurol Neurosurg Psychiatry 79:1050–1055PubMedCrossRefGoogle Scholar
  7. Castro N, Marquez-Caraveo C, Brundage RC, Gonzalez-Esquivel D, Suarez AM, Gongora F, Jara A, Urizar J, Lanao JM, Jung H (2009) Population pharmacokinetics of albendazole in patients with neurocysticercosis. Int J Clin Pharmacol Ther 47:679–685PubMedGoogle Scholar
  8. Chavarria A, Roger B, Fragoso G, Tapia G, Fleury A, Dumas M, Dessein A, Larralde C, Sciutto E (2003) TH2 profile in asymptomatic Taenia solium human neurocysticercosis. Microbes Infect 5:1109–1115PubMedCrossRefGoogle Scholar
  9. de Aluja AS, Martinez MJ, Villalobos AN (1998) Taenia solium cysticercosis in young pigs: age at first infection and histological characteristics. Vet Parasitol 76:71–79PubMedCrossRefGoogle Scholar
  10. de Queiroz A, Alkire NL (1998) The phylogenetic placement of Taenia cestodes that parasitize humans. J Parasitol 84:379–383PubMedCrossRefGoogle Scholar
  11. Del Brutto OH, Sotelo J (1988) Neurocysticercosis: an update. Rev Infect Dis 10:1075–1087PubMedCrossRefGoogle Scholar
  12. Del Brutto OH, Santibanez R, Noboa CA, Aguirre R, Diaz E, Alarcon TA (1992) Epilepsy due to neurocysticercosis: analysis of 203 patients. Neurology 42:389–392PubMedCrossRefGoogle Scholar
  13. Del Brutto OH, Sotelo J, Roman GC (1993) Therapy for neurocysticercosis: a reappraisal. Clin Infect Dis 17:730–735PubMedCrossRefGoogle Scholar
  14. Del Brutto OH, Santibanez R, Idrovo L, Rodriguez S, Diaz-Calderon E, Navas C, Gilman RH, Cuesta F, Mosquera A, Gonzalez AE, Tsang VC, Garcia HH (2005) Epilepsy and neurocysticercosis in Atahualpa: a door-to-door survey in rural coastal Ecuador. Epilepsia 46:583–587PubMedCrossRefGoogle Scholar
  15. Del Brutto OH, Roos KL, Coffey CS, Garcia HH (2006) Meta-analysis: cysticidal drugs for neurocysticercosis: albendazole and praziquantel. Ann Intern Med 145:43–51PubMedCrossRefGoogle Scholar
  16. Eom KS, Rim HJ (1993) Morphologic descriptions of Taenia asiatica sp. n. Kor J Parasitol 31:1–6CrossRefGoogle Scholar
  17. Eom KS, Rim HJ, Geerts S (1992) Experimental infection of pigs and cattle with eggs of Asian Taenia saginata with special reference to its extrahepatic viscerotropism. Kisaengchunghak Chapchi 30:269–275PubMedGoogle Scholar
  18. Escobar A, Nieto D (1972) Parasitic diseases. In: Minckler J (ed) Pathology of the nervous system. McGraw-Hill, New York, pp 2503–2521Google Scholar
  19. Ferreira AP, Vaz AJ, Nakamura PM, Sasaki AT, Ferreira AW, Livramento JA (1997) Hemagglutination test for the diagnosis of human neurocysticercosis: development of a stable reagent using homologous and heterologous antigens. Rev Inst Med Trop Sao Paulo 39:29–33PubMedCrossRefGoogle Scholar
  20. Fleury A, Morales J, Bobes RJ, Dumas M, Yanez O, Pina J, Carrillo-Mezo R, Martinez JJ, Fragoso G, Dessein A, Larralde C, Sciutto E (2006) An epidemiological study of familial neurocysticercosis in an endemic Mexican community. Trans R Soc Trop Med Hyg 100:551–558PubMedCrossRefGoogle Scholar
  21. Fleury A, Carrillo-Mezo R, Flisser A, Sciutto E, Corona T (2011) Subarachnoid basal neurocysticercosis: a focus on the most severe form of the disease. Expert Rev Anti-Infect Ther 9:123–133PubMedCrossRefGoogle Scholar
  22. Flisser A (1994) Taeniasis and cysticercosis due to Taenia solium. Prog Clin Parasitol 4:77–116PubMedGoogle Scholar
  23. Flisser A (2013) State of the art of Taenia solium as compared to Taenia asiatica. Kor J Parasitol 51:43–49CrossRefGoogle Scholar
  24. Flisser A, Sarti E, Lightowlers M, Schantz P (2003) Neurocysticercosis: regional status, epidemiology, impact and control measures in the Americas. Acta Trop 87:43–51PubMedCrossRefGoogle Scholar
  25. Flisser A, Gauci CG, Zoli A, Martinez-Ocana J, Garza-Rodriguez A, Dominguez-Alpizar JL, Maravilla P, Rodriguez-Canul R, Avila G, Aguilar-Vega L, Kyngdon C, Geerts S, Lightowlers MW (2004) Induction of protection against porcine cysticercosis by vaccination with recombinant oncosphere antigens. Infect Immun 72:5292–5297PubMedPubMedCentralCrossRefGoogle Scholar
  26. Galan-Puchades MT, Fuentes MV (2013) Taenia asiatica: the most neglected human Taenia and the possibility of cysticercosis. Kor J Parasitol 51:51–54CrossRefGoogle Scholar
  27. Garcia HH, Del Brutto OH (2003) Imaging findings in neurocysticercosis. Acta Trop 87:71–78PubMedCrossRefGoogle Scholar
  28. Garcia HH, Evans CA, Nash TE, Takayanagui OM, White AC Jr, Botero D, Rajshekhar V, Tsang VC, Schantz PM, Allan JC, Flisser A, Correa D, Sarti E, Friedland JS, Martinez SM, Gonzalez AE, Gilman RH, Del Brutto OH (2002) Current consensus guidelines for treatment of neurocysticercosis. Clin Microbiol Rev 15:747–756PubMedPubMedCentralCrossRefGoogle Scholar
  29. Garcia HH, Gonzalez AE, Del Brutto OH, Tsang VC, Llanos-Zavalaga F, Gonzalvez G, Romero J, Gilman RH (2007) Strategies for the elimination of taeniasis/cysticercosis. J Neurol Sci 262:153–157PubMedCrossRefGoogle Scholar
  30. Garcia HH, Rodriguez S, Friedland JS (2014) Immunology of Taenia solium taeniasis and human cysticercosis. Parasite Immunol 36:388–396PubMedPubMedCentralCrossRefGoogle Scholar
  31. Garcia-Noval J, Allan JC, Fletes C, Moreno E, DeMata F, Torres-Alvarez R, Soto de Alfaro H, Yurrita P, Higueros-Morales H, Mencos F, Craig PS (1996) Epidemiology of Taenia solium taeniasis and cysticercosis in two rural Guatemalan communities. Am J Trop Med Hyg 55:282–289PubMedCrossRefPubMedCentralGoogle Scholar
  32. Gonzalez LM, Montero E, Harrison LJ, Parkhouse RM, Garate T (2000) Differential diagnosis of Taenia saginata and Taenia solium infection by PCR. J Clin Microbiol 38:737–744PubMedPubMedCentralGoogle Scholar
  33. Gonzalez LM, Montero E, Puente S, Lopez-Velez R, Hernandez M, Sciutto E, Harrison LJ, Parkhouse RM, Garate T (2002) PCR tools for the differential diagnosis of Taenia saginata and Taenia solium taeniasis/cysticercosis from different geographical locations. Diagn Microbiol Infect Dis 42:243–249PubMedCrossRefPubMedCentralGoogle Scholar
  34. Gonzalez AE, Gauci CG, Barber D, Gilman RH, Tsang VC, Garcia HH, Verastegui M, Lightowlers MW (2005) Vaccination of pigs to control human neurocysticercosis. Am J Trop Med Hyg 72:837–839PubMedCrossRefPubMedCentralGoogle Scholar
  35. Grogl M, Estrada JJ, MacDonald G, Kuhn RE (1985) Antigen-antibody analyses in neurocysticercosis. J Parasitol 71:433–442PubMedCrossRefGoogle Scholar
  36. Gupta RK, Rao SB, Jain R, Pal L, Kumar R, Venkatesh SK, Rathore RK (2001) Differentiation of calcification from chronic hemorrhage with corrected gradient echo phase imaging. J Comput Assist Tomogr 25:698–704PubMedCrossRefPubMedCentralGoogle Scholar
  37. Hoberg EP (2006) Phylogeny of Taenia: species definitions and origins of human parasites. Parasitol Int 55(Suppl):S23–S30PubMedCrossRefGoogle Scholar
  38. Ito A, Putra MI, Subahar R, Sato MO, Okamoto M, Sako Y, Nakao M, Yamasaki H, Nakaya K, Craig PS, Margono SS (2002) Dogs as alternative intermediate hosts of Taenia solium in Papua (Irian Jaya), Indonesia confirmed by highly specific ELISA and immunoblot using native and recombinant antigens and mitochondrial DNA analysis. J Helminthol 76:311–314PubMedCrossRefPubMedCentralGoogle Scholar
  39. Kong Y, Cho SY, Cho MS, Kwon OS, Kang WS (1993) Seroepidemiological observation of Taenia solium cysticercosis in epileptic patients in Korea. J Kor Med Sci 8:145–152CrossRefGoogle Scholar
  40. Kruger-Leite E, Jalkh AE, Quiroz H, Schepens CL (1985) Intraocular cysticercosis. Am J Ophthalmol 99:252–257PubMedCrossRefGoogle Scholar
  41. Laclette JP, Merchant MT, Willms K (1987) Histological and ultrastructural localization of antigen B in the metacestode of Taenia solium. J Parasitol 73:121–129PubMedCrossRefGoogle Scholar
  42. Lightowlers MW (2004) Vaccination for the prevention of cysticercosis. Dev Biol (Basel) 119:361–368Google Scholar
  43. Madigubba S, Vishwanath K, Reddy G, Vemuganti GK (2007) Changing trends in ocular cysticercosis over two decades: an analysis of 118 surgically excised cysts. Indian J Med Microbiol 25:214–219PubMedCrossRefGoogle Scholar
  44. Madrazo I, Garcia-Renteria JA, Sandoval M, Lopez Vega FJ (1983) Intraventricular cysticercosis. Neurosurgery 12:148–152PubMedCrossRefGoogle Scholar
  45. Margono SS, Subahar R, Hamid A, Wandra T, Sudewi SS, Sutisna P, Ito A (2001) Cysticercosis in Indonesia: epidemiological aspects. Southeast Asian J Trop Med Public Health 32(Suppl 2):79–84PubMedGoogle Scholar
  46. Marquez JM, Arauz A (2012) Cerebrovascular complications of neurocysticercosis. Neurologist 18:17–22PubMedCrossRefGoogle Scholar
  47. McCormick GF (1985) Cysticercosis – review of 230 patients. Bull Clin Neurosci 50:76–101PubMedGoogle Scholar
  48. Montano SM, Villaran MV, Ylquimiche L, Figueroa JJ, Rodriguez S, Bautista CT, Gonzalez AE, Tsang VC, Gilman RH, Garcia HH (2005) Neurocysticercosis: association between seizures, serology, and brain CT in rural Peru. Neurology 65:229–233PubMedCrossRefGoogle Scholar
  49. Ndimubanzi PC, Carabin H, Budke CM, Nguyen H, Qian YJ, Rainwater E, Dickey M, Reynolds S, Stoner JA (2010) A systematic review of the frequency of neurocyticercosis with a focus on people with epilepsy. PLoS Negl Trop Dis 4:e870PubMedPubMedCentralCrossRefGoogle Scholar
  50. Ooi HK, Ho CM, Chung WC (2013) Historical overview of Taenia asiatica in Taiwan. Kor J Parasitol 51:31–36CrossRefGoogle Scholar
  51. Ostrosky-Zeichner L, Estanol B (1999) Immunopathogenesis of neurocysticercosis: is damage mediated by the host immune response? Int J Parasitol 29:649–650PubMedCrossRefGoogle Scholar
  52. Park YS, Lee JK, Kim JH, Park KC (2011) Cysticercosis of lumbar spine, mimicking spinal subarachnoid tumor. Spine J 11:e1–e5PubMedCrossRefGoogle Scholar
  53. Pawlowski Z, Murell KD (2000) Taeniasis and cysticercosis. In: Hui Y, Murrell KD, Nip WK, Stanfield P, Satter SA (eds) Foodborne diseases handbook. Marcel Dekker, New York, pp 217–227Google Scholar
  54. Phiri IK, Dorny P, Gabriel S, Willingham AL 3rd, Speybroeck N, Vercruysse J (2002) The prevalence of porcine cysticercosis in Eastern and Southern provinces of Zambia. Vet Parasitol 108:31–39PubMedCrossRefGoogle Scholar
  55. Pondja A, Neves L, Mlangwa J, Afonso S, Fafetine J, Willingham AL 3rd, Thamsborg SM, Johansen MV (2012) Use of oxfendazole to control porcine cysticercosis in a high-endemic area of Mozambique. PLoS Negl Trop Dis 6:e1651PubMedPubMedCentralCrossRefGoogle Scholar
  56. Prabhakaran V, Rajshekhar V, Murrell KD, Oommen A (2007) Conformation-sensitive immunoassays improve the serodiagnosis of solitary cysticercus granuloma in Indian patients. Trans R Soc Trop Med Hyg 101:570–577PubMedCrossRefGoogle Scholar
  57. Prasad A, Prasad KN, Gupta RK, Pradhan S (2009a) Increased expression of ICAM-1 among symptomatic neurocysticercosis. J Neuroimmunol 206:118–120PubMedCrossRefGoogle Scholar
  58. Prasad KN, Prasad A, Gupta RK, Nath K, Pradhan S, Tripathi M, Pandey CM (2009b) Neurocysticercosis in patients with active epilepsy from the pig farming community of Lucknow district, north India. Trans R Soc Trop Med Hyg 103:144–150PubMedCrossRefGoogle Scholar
  59. Rajshekhar V, Joshi DD, Doanh NQ, van De N, Xiaonong Z (2003) Taenia solium taeniosis/cysticercosis in Asia: epidemiology, impact and issues. Acta Trop 87:53–60PubMedCrossRefGoogle Scholar
  60. Rajshekhar V, Raghava MV, Prabhakaran V, Oommen A, Muliyil J (2006) Active epilepsy as an index of burden of neurocysticercosis in Vellore district, India. Neurology 67:2135–2139PubMedCrossRefGoogle Scholar
  61. Restrepo BI, Alvarez JI, Castano JA, Arias LF, Restrepo M, Trujillo J, Colegial CH, Teale JM (2001) Brain granulomas in neurocysticercosis patients are associated with a Th1 and Th2 profile. Infect Immun 69:4554–4560PubMedPubMedCentralCrossRefGoogle Scholar
  62. Sawhney BB, Chopra JS, Banerji AK, Wahi PL (1976) Pseudohypertrophic myopathy in cysticerosis. Neurology 26:270–272PubMedCrossRefGoogle Scholar
  63. Schantz PM, Moore AC, Munoz JL, Hartman BJ, Schaefer JA, Aron AM, Persaud D, Sarti E, Wilson M, Flisser A (1992) Neurocysticercosis in an Orthodox Jewish community in New York City. N Engl J Med 327:692–695PubMedCrossRefGoogle Scholar
  64. Schwan EV, de Scally MP, van Rensburg CL, Durand DT (2002) Cerebral cysticercosis in a cat. J S Afr Vet Assoc 73:219–221PubMedGoogle Scholar
  65. Shandera WX, White AC Jr, Chen JC, Diaz P, Armstrong R (1994) Neurocysticercosis in Houston, Texas. A report of 112 cases. Medicine (Baltimore) 73:37–52CrossRefGoogle Scholar
  66. Singh AK, Prasad KN, Prasad A, Tripathi M, Gupta RK, Husain N (2013) Immune responses to viable and degenerative metacestodes of Taenia solium in naturally infected swine. Int J Parasitol 43:1101–1107PubMedCrossRefGoogle Scholar
  67. Singh AK, Singh SK, Singh A, Gupta KK, Khatoon J, Prasad A, Rai RP, Gupta RK, Tripathi M, Husain N, Prasad KN (2015a) Immune response to Taenia solium cysticerci after anti-parasitic therapy. Int J Parasitol 45:749–759PubMedCrossRefGoogle Scholar
  68. Singh SK, Singh AK, Prasad KN, Singh A, Rai RP, Tripathi M, Gupta RK, Husain N (2015b) Expression of adhesion molecules, chemokines and matrix metallo- proteinases (MMPs) in viable and degenerating stage of Taenia solium metacestode in swine neurocysticercosis. Vet Parasitol 214:59–66PubMedCrossRefGoogle Scholar
  69. Singh SK, Prasad KN, Singh AK, Gupta KK, Chauhan RS, Singh A, Rai RP, Pati BK (2016) Identification of species and genetic variation in Taenia isolates from human and swine of North India. Parasitol Res 115:3689–3693PubMedCrossRefGoogle Scholar
  70. Singh A, Prasad KN, Singh AK, Singh SK, Gupta KK, Paliwal VK, Pandey CM, Gupta RK (2017) Human glutathione s-transferase enzyme gene polymorphisms and their association with neurocysticercosis. Mol Neurobiol 54:2843–2851PubMedCrossRefGoogle Scholar
  71. Sinha S, Sharma BS (2012) Intraventricular neurocysticercosis: a review of current status and management issues. Br J Neurosurg 26:305–309PubMedCrossRefPubMedCentralGoogle Scholar
  72. Sotelo J, Guerrero V, Rubio F (1985) Neurocysticercosis: a new classification based on active and inactive forms. A study of 753 cases. Arch Intern Med 145:442–445PubMedCrossRefPubMedCentralGoogle Scholar
  73. Sotelo J, Escobedo F, Penagos P (1988) Albendazole vs praziquantel for therapy for neurocysticercosis. A controlled trial. Arch Neurol 45:532–534PubMedCrossRefPubMedCentralGoogle Scholar
  74. 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 84:629–633PubMedCrossRefPubMedCentralGoogle Scholar
  75. Takayanagui OM, Jardim E (1992) Therapy for neurocysticercosis. Comparison between albendazole and praziquantel. Arch Neurol 49:290–294PubMedCrossRefPubMedCentralGoogle Scholar
  76. Terrazas LI (2008) The complex role of pro- and anti-inflammatory cytokines in cysticercosis: immunological lessons from experimental and natural hosts. Curr Top Med Chem 8:383–392PubMedCrossRefPubMedCentralGoogle Scholar
  77. Tsang VC, Brand JA, Boyer AE (1989) An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human cysticercosis (Taenia solium). J Infect Dis 159:50–59PubMedCrossRefPubMedCentralGoogle Scholar
  78. 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 138:1423–1428PubMedCrossRefPubMedCentralGoogle Scholar
  79. White AC Jr, Tato P, Molinari JL (1992) Host-parasite interactions in Taenia solium cysticercosis. Infect Agents Dis 1:185–193PubMedPubMedCentralGoogle Scholar
  80. White AC Jr, Robinson P, Kuhn R (1997) Taenia solium cysticercosis: host-parasite interactions and the immune response. Chem Immunol 66:209–230PubMedCrossRefGoogle Scholar
  81. Yamasaki H, Allan JC, Sato MO, Nakao M, Sako Y, Nakaya K, Qiu D, Mamuti W, Craig PS, Ito A (2004) DNA differential diagnosis of taeniasis and cysticercosis by multiplex PCR. J Clin Microbiol 42:548–553PubMedPubMedCentralCrossRefGoogle Scholar
  82. Zini D, Farrell VJ, Wadee AA (1990) The relationship of antibody levels to the clinical spectrum of human neurocysticercosis. J Neurol Neurosurg Psychiatry 53:656–661PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Kashi Nath Prasad
    • 1
  • Satyendra Kumar Singh
    • 1
  1. 1.Department of MicrobiologySanjay Gandhi Postgraduate Institute of Medical SciencesLucknowIndia

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