Abstract
Schistosomiasis (bilharzia) is a neglected tropical disease caused by digenetic trematode platyhelminths of the genus Schistosoma. Neuroschistosomiasis is one of the most severe clinical outcomes associated with schistosome infection. Neurological complications early during the course of infection are thought to occur through in situ egg deposition following aberrant migration of adult worms to the brain or spinal cord. The presence of eggs in the CNS induces a cell-mediated Th2-driven periovular granulomatous reaction. The mass effect of thousands of eggs and the large granulomas concentrated within the brain or spinal cord explain the signs and symptoms of increased intracranial pressure, myelopathy, radiculopathy and subsequent clinical sequelae. Myelopathy (acute transverse myelitis and subacute myeloradiculopathy) of the lumbosacral region is the most common neurological manifestation of S. mansoni or S. haematobium infection, whereas acute encephalitis of the cortex, subcortical white matter, basal ganglia or internal capsule is typical of S. japonicum infection. Cerebral complications include encephalopathy with headache, visual impairment, delirium, seizures, motor deficits and ataxia, whereas spinal symptoms include lumbar pain, lower limb radicular pain, muscle weakness, sensory loss and bladder dysfunction. The finding of eggs in the stool or a positive serology, provides supportive but not direct evidence of neuroschistosomiasis. A definitive diagnosis can only be made with histopathological study showing Schistosoma eggs and granulomas. Schistosomicidal drugs (notably praziquantel), steroids and surgery are currently used for the treatment of neuroschistosomiasis. During the ‘acute phase’ of the disease, neuroschistosomiasis is treated with corticosteroids which are augmented with a course of praziquantel once female worm ovipositioning commences. Surgery should be reserved for special cases such as in those with evidence of medullary compression and in those who deteriorate despite clinical management.
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References
King CH, Dickman K, Tisch DJ (2005) Reassessment of the cost of chronic helminthic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365:561–569
King CH, Dangerfield-Cha M (2008) The unacknowledged impact of chronic schistosomiasis. Chronic Illn 4:65–79
Ross AG, Vickers D, Olds GR et al (2007) Katayama syndrome. Lancet Infect Dis 7:218–224
Cetron MS, Chitsulo L, Sullivan JJ et al (1996) Schistosomiasis in Lake Malawi. Lancet 348:1274–1278
Kane CA, Most H (1948) Schistosomiasis of the central nervous system: experiences n World War II and a review of the literature. Arch Neurol Psychiatry 59:141–183
Chen M, Mott K (1989) Progress in the assessment of morbidity due to Schistosoma japonicum infection: a review of recent literature. Trop Dis Bull 85:R1–R56
Carod-Artal FJ (2008) Neurological complications of Schistosoma infection. Trans R Soc Trop Med Hyg 102:107–116
Ross AG, Bartley PB, Sleigh AC et al (2002) Schistosomiasis. N Engl J Med 346:1212–1220
Shiff C (2000) Epidemiology of helminth infections. In: Nelson KE, Masters Williams C, Graham NM (eds) Infectious disease epidemiology: theory and practice. Aspen, Gaithersburg
Pittella JE (1997) Neuroschistosomiasis. Brain Pathol 7:649–662
Waine GJ, McManus DP (1997) Schistosomiasis vaccine development – the current picture. Bioessays 19:435–443
Chen MG (1991) Relative distribution of Schistosoma japonicum eggs in the intestine of man: a subject of inconsistency. Acta Trop 48:163–171
Ferrari TC (2004) Involvement of the central nervous system in the schistosomiasis. Mem Inst Oswaldo Cruz 99:59–62
Batson OV (1940) The function of the vertebral veins and their role in the spread of metastases. Ann Surg 112:138–149
Gryseels B, Polman K, Clerinx J et al (2006) Human schistosomiasis. Lancet 368:1106–1118
Schramm G, Hamilton JV, Balog CI et al (2009) Molecular characterisation of kappa-5, a major antigenic glycoprotein from Schistosoma mansoni eggs. Mol Biochem Parasitol 166:4–14
Bartley PB, Ramm GA, Jones MK et al (2006) A contributory role for activated hepatic stellate cells in the dynamics of Schistosoma japonicum egg-induced fibrosis. Int J Parasitol 36:993–1001
Burke ML, Jones MK, Gobert GN et al (2009) Immunopathogenesis of human schistosomiasis. Parasite Immunol 31:163–176
Wilson MS, Mentink-Kane MM, Pesce JT et al (2007) Immunopathology of schistosomiasis. Immunol Cell Biol 85:148–514
Wynn TA, Thompson RW, Cheever AW et al (2004) Immunopathogenesis of schistosomiasis. Immunol Rev 201:156–167
McManus DP, Li Y, Gray DJ et al (2009) Conquering 'snail fever': schistosomiasis and its control in China. Expert Rev Anti Infect Ther 7(4):473–485
Jaureguiberry S, Caumes E (2008) Neurological involvement during Katayama syndrome. Lancet Infect Dis 8:9–10
Davis A (2002) Schistosomiasis. In: Cook GC, Zumla AI (eds) Manson’s tropical diseases. Saunders, London. pp 1431–1469
Granier H, Potard M, Diraison P et al (2003) Acute encephalitis concurrent with primary infection by Schistosoma mansoni. Med Trop 63:60–63
Jaureguiberry S, Ansart S, Perez L et al (2007) Acute neuroschistosomiasis: two cases associated with cerebral vasculitis. Am J Trop Med Hyg 76:964–966
Carod-Artal FJ (2010) Neuroschistosomiasis. Expert Rev Anti Infect Ther 8:1307–1318
Carod-Artal FJ, Vargas AP, Horan TA et al (2006) Brain involvement in a Schistosoma mansoni myelopathy patient. J Neurol Neurosurg Psychiatry 77:512
Lambertucci JR, Souza-Pereia SR, Carvalho TA (2009) Simultaneous occurrence of brain tumor and myeloradiculopathy in schistosomiasis mansoni: case report. Rev Soc Bras Med Trop 42:338–341
Yamagiwa J (1889) Beitrage zur aetiologie der jacksonschen epilepsie. Virchows Arch Pathol Anat 119:449–460
Braga BP, Costa LB, Lambertucci JR (2003) Magnetic resonance imaging of cerebellar schistosomiasis mansoni. Rev Soc Bras Med Trop 36:635–636
Ibahioin K, Chellaoui A, Lakhdar A et al (2004) Cerebellar schistosomiasis. A case report. Neurochirurgie 50:61–65
Raso P, Tafuri A, Lopes Nda F et al (2006) The tumoral form of cerebellar schistosomiasis: case report and measure of granulomas. Rev Soc Bras Med Trop 39:283–286
Li YS, Ross AG, Hou X et al (2011) Oriental schistosomiasis with neurological complications: case report. Ann Clin Microbiol Antimicrob 10:1–5
Muller HR, Stender A (1930) Bilharziose des Rückenmarkes unter dem Bilde einer myelitis dorso-lumbalis transversa completa. Arch Schiffs-u Tropenhyg 34:527–538
Bill P (2003) Schistosomiasis and the nervous system. Practical Neurology. Blackwell, Oxford
Jiang YG, Zhang MM, Xiang J (2008) Spinal cord schistosomiasis japonica: a report of four cases. Surg Neurol 69:392–397
Nokes C, McGarvey ST, Shiue L et al (1999) Evidence for an improvement in cognitive function following treatment of Schistosoma japonicum infection in Chinese primary schoolchildren. Am J Trop Med Hyg 60:556–565
Jukes MC, Nokes CA, Alcock KJ et al (2002) Partnership for child development. Heavy schistosomiasis associated with poor short-term memory and slower reaction times in Tanzanian schoolchildren. Trop Med Int Heal 7:104–117
Nazel MW, el-Morshedy H, Farghaly A et al (1999) Schistosoma mansoni infection and cognitive functions of primary school children, in Kafr El Sheikh, Egypt. J Egypt Public Heal Assoc 74:97–119
Katz N, Chaves A, Pellegrino J (1972) A simple device for quantitative stool thick-smear technique for schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14:397–400
Carabin H, Balolong E, Joseph L et al (2005) Estimating sensitivity and specificity of a faecal examination method for Schistosoma japonicum infection in cats, dogs, water buffaloes, pigs, and rats in Western Samar and Sorsogon Provinces, The Philippines. Int J Parasitol 35:1517–1524
Rabello A (1997) Diagnosing schistosomiasis. Mem Inst Oswaldo Cruz 92:669–676
Ross AG, Sleigh AC, Li Y et al (2001) Schistosomiasis in the People’s Republic of China: prospects and challenges for the 21st century. Clin Microbiol Rev 14:270–295
Utzinger J, Zhou XN, Chen MG et al (2005) Conquering schistosomiasis in China: the Long March. Acta Trop 96:69–96
Yu JM, de Vlas SJ, Jiang QW et al (2007) Comparison of the Kato-Katz technique, hatching test and indirect hemagglutination assay (IHA) for the diagnosis of Schistosoma japonicum infection in China. Parasitol Int 56:45–49
Ebrahim A, El-Morshedy H, Omer E et al (1997) Evaluation of the Kato Katz thick smear and formol ether sedimentation techniques for quantitative diagnosis of Schistosoma mansoni infection. Am J Trop Med Hyg 57:706–708
Yu JM, De Vlas SJ, Yuan HC et al (1998) Variations in faecal Schistosoma japonicum egg counts. Am J Trop Med Hyg 59:370–375
Ross AG, Sleigh AC, Li Y et al (1998) Measuring exposure to S. japonicum in China. II. Activity diaries, pathways to infection and immunological correlates. Acta Trop 71:229–236
Balliauw C, Matens F, Steen KVD et al (2010) Spinal schistosomiasis. Eur J Radiol Extra 73:e49–e51
Jongste AHC, Tilanus AMR, Bax H et al (2010) New insights in diagnosing Schistosoma myelopathy. J Infect 60:244–247
Fagundes Teixeira C, Neuhauss E, Ben R et al (2007) Detection of Schistosoma mansoni eggs in feces through their interaction with paramagnetic beads in a magnetic field. PLoS Negl Trop Dis 1:e73
Zhu YC (2005) Immunodiagnosis and its role in schistosomiasis control in China: a review. Acta Trop 96:130–136
Van Gool T, Vetter H, Vervoort T et al (2002) Serodiagnosis of imported schistosomiasis by a combination of a commercial indirect hemagglutination test with Schistosoma mansoni adult worm antigens and an enzyme-linked immunosorbent assay with S. mansoni egg antigens. J Clin Microbiol 40:3432–3437
Zhu H, Yu C, Xia X et al (2010) Assessing the diagnostic accuracy of immunodiagnostic techniques in the diagnosis of schistosomiasis japonica: a meta-analysis. Parasitol Res 107(5):1067–1073
Ferrari TC, Faria LC, Vilaça TS et al (2011) Identification and characterization of immune complexes in the cerebrospinal fluid of patients with spinal cord schistosomiasis. J Neuroimmunol 230:188–190
Doenhoff MJ, Cioli D, Utzinger J (2008) Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr Opin Infect Dis 21:659–667
Doenhoff MJ, Pica-Mattoccia L (2006) Praziquantel for the treatment of schistosomiasis: its use for control in areas with endemic disease and prospects for drug resistance. Expert Rev Anti Infect Ther 4:199–210
Utzinger J, Xiao SH, Tanner M et al (2007) Artemisinins for schistosomiasis and beyond. Curr Opin Invest Drugs 8:105–116
Xiao SH (2005) Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemesinins. Acta Trop 96:153–167
Zhou XN, Wang YL, Chen MG et al (2005) The public health significance and control of schistosomiasis in China – then and now. Acta Trop 96:97–105
Aragon AD, Imani RA, Blackburn VR et al (2009) Towards an understanding of the mechanism of action of praziquantel. Mol Biochem Parasitol 164:57–65
Kumagai T, Osada Y, Ohta N et al (2009) Peroxiredoxin-1 from Schistosoma japonicum functions as a scavenger against hydrogen peroxide but not nitric oxide. Mol Biochem Parasitol 164:26–31
Shrivastava J, Qian BZ, Mcvean G et al (2005) An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Mol Ecol 14:839–849
Ting-An W, Hong-Xiang Z (2009) PTK-pathways and TGF-beta signaling pathways in schistosomes. J Basic Microbiol 49:25–31
Ahier A, Khayath N, Vicogne J et al (2008) Insulin receptors and glucose uptake in the human parasite Schistosoma mansoni. Parasite 15:573–579
Ahier A, Rondard P, Gouignard N et al (2009) A new family of receptor tyrosine kinases with a venus flytrap binding domain in insects, other invertebrates activated by aminoacids. PLoS One 4:e5651
Bahia D, Oliveira LM, Mortara RA (2009) Phosphatidylinositol-and related-kinases: a genome-wide survey of classes and subtypes in the Schistosoma mansoni genome for designing subtype-specific inhibitors. Biochem Biophys Res Commun 380:525–530
Gray DJ, McManus DP, Li YS et al (2010) Schistosomiasis elimination: lessons from the past guide the future. Lancet Infect Dis 10:733–736
Hou XY, McManus DP, Gray DJ et al (2008) A randomised, double-blind, placebo-controlled trial on the safety and efficacy of combined praziquantel and artemether treatment for acute schistosomiasis japonica in China. Bull World Health Organ 86:788–795
Fowler R, Lee C, Keytone JS (1999) The role of corticosteroids in the treatment of cerebral schistosomiasis caused by Schistosoma mansoni: case report and discussion. Am J Trop Med Hyg 61(1):47–50
Grandiere-Perez L, Ansart S, Paris L et al (2006) Efficacy of praziquantel during the incubation and invasive phase of Schistosoma haematobium schistosomiasis in 18 travelers. Am J Trop Med Hyg 74:814–818
Caunes E, Vidailhet M (2010) Acute neuroschistosomiasis: a cerebral vasculitis to treat with corticosteroids not praziquantel. J Travel Med 17:359
Acknowledgments
This study was supported by the United Nations Development Programme/World Bank/World Health Organization Special Program for Research and Training in Tropical Diseases (Dr. Li and Prof. McManus), the National Health and Medical Research Council of Australia (Dr. Li and Prof. McManus), the Wellcome Trust (UK) (Dr. Li and Prof. McManus), the Sandler Foundation (USA) (Prof. McManus), the Dana Foundation (USA) (Dr. Li and Prof. McManus) and the National Institute of Allergy and Infectious Diseases (Dr. Li and Prof. McManus). Dr. Li Yuesheng is a Howard Hughes Medical Institute Scholar, USA.
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We the authors declare no conflicts of interest in the preparation or publication of this review.
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Ross, A.G., McManus, D.P., Farrar, J. et al. Neuroschistosomiasis. J Neurol 259, 22–32 (2012). https://doi.org/10.1007/s00415-011-6133-7
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DOI: https://doi.org/10.1007/s00415-011-6133-7