Skip to main content

Advertisement

SpringerLink
Log in

Neurocysticercosis: local and systemic immune-inflammatory features related to severity

  • Original Investigation
  • Published:
Medical Microbiology and Immunology Aims and scope Submit manuscript

Abstract

Neurocysticercosis (NC) is caused by the establishment of Taenia solium cysticerci in the central nervous system. Previous studies have established that neuroinflammation plays a key role in the severity of the disease. However, the relationship between peripheral and local immune response remains inconclusive. This work studies the peripheral and local immune-inflammatory features and their relationships, toward the identification of potential peripheral immunologic features related to severity. A panel of cytokines was measured in paired cerebrospinal fluid (CSF) and in the supernatant of antigen-specific stimulated peripheral blood mononuclear cells samples (SN) in a total of 31 untreated inflammatory and non-inflammatory NC patients. Increased clinical and radiologic severity was associated with an increased cerebrospinal fluid cell count. A peripheral proliferative depression that negatively correlates with CSF cellularity and TNFα and that positively correlates with SN IL5 was observed in severe NC patients. These results provide evidences to support the systemic proliferative response as a biomarker to monitor the level of neuroinflammation, of possible value in the patients’ follow-up during treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Del Brutto OH, Sotelo J (1988) Neurocystiercosis: an update. Rev Infect Dis 10:1075–1087

    Article  PubMed  CAS  Google Scholar 

  2. Fleury A, Dessein A, Preux PM, Dumas M, Tapia G, Larralde C, Sciutto E (2004) Symptomatic human neurocysticercosis–age, sex and exposure factors relating with disease heterogeneity. J Neurol 251(7):830–837

    Article  PubMed  Google Scholar 

  3. Sciutto E, Chavarria A, Fragoso G, Fleury A, Larralde C (2007) The immune response in Taenia solium cysticercosis: protection and injury. Parasite Immunol 29(12):621–636

    Article  PubMed  CAS  Google Scholar 

  4. Villagran J, Olvera J (1988) A clinical and pathological study of 481 autopsy cases. Patología (México) 26:149–156

    Google Scholar 

  5. Fleury A, Gomez T, Alvarez I, Meza D, Huerta M, Chavarria A, Carrillo-Mezo RA, Lloyd C, Dessein A, Preux PM, Dumas M, Larralde C, Sciutto E, Fragoso G (2003) High prevalence of calcified silent neurocysticercosis in a rural village of Mexico. Neuroepidemiol 22(2):139–145

    Article  CAS  Google Scholar 

  6. Sánchez AL, Lindbäck J, Schantz PM, Sone M, Sakai H, Medina MT, Ljungström I (1999) A population-based, case-control study of Taenia solium taeniasis and cysticercosis. Ann Trop Med Parasitol 93(3):247–258

    Article  PubMed  Google Scholar 

  7. Sáenz B, Ruíz-Garcia M, Jiménez E, Hernández-Aguilar J, Suastegui R, Larralde C, Sciutto E, Fleury A (2006) Neurocysticercosis: clinical, radiologic, and inflammatory differences between children and adults. Pediatr Infect Dis J 25(9):801–803

    Article  PubMed  Google Scholar 

  8. Singhi P, Singhi S (2004) Neurocysticercosis in children. J Child Neurol 19(7):482–492

    Article  PubMed  Google Scholar 

  9. Aguilar-Rebolledo F, Cedillo-Rivera R, Llaguno-Violante P, Torres-López J, Muñoz-Hernández O, Enciso-Moreno JA (2001) Interleukin levels in cerebrospinal fluid from children with neurocysticercosis. Am J Trop Med Hyg 64(1–2):35–40

    PubMed  CAS  Google Scholar 

  10. Bueno EC, Vaz AJ, Machado LR, Livramento JA, Avila SL, Ferreira AW (2001) Antigen-specific suppression of cultured lymphocytes from patients with neurocysticercosis. Clin Exp Immunol 126(2):304–310

    Article  PubMed  CAS  Google Scholar 

  11. Bueno EC, dos Ramos Machado L, Livramento JA, Vaz AJ (2004) Cellular immune response of patients with neurocysticercosis (inflammatory and non-inflammatory phases). Acta Trop 91(2):205–213

    Article  PubMed  CAS  Google Scholar 

  12. Chavarría A, Fleury A, Garcia E, Marquez C, Fragoso G, Sciutto E (2005) Relationship between the clinical heterogeneity of neurocysticercosis and the immune-inflammatory profiles. Clin Immunol 116(3):271–278

    Article  PubMed  Google Scholar 

  13. Grewal JS, Kaur S, Bhatti G, Sawhney IM, Ganguly NK, Mahajan RC, Malla N (2000) Cellular immune responses in human neurocysticercosis. Parasitol Res 86(6):500–503

    Article  PubMed  CAS  Google Scholar 

  14. Medina-Escutia E, Morales-Lopez Z, Proano JV, Vazquez J, Bermudez V, Navarrete VO, Madrid-Marina V, Laclette JP, Correa D (2001) Cellular immune response and Th1/Th2 cytokines in human neurocysticercosis: lack of immune suppression. J Parasitol 87:587–590

    PubMed  CAS  Google Scholar 

  15. Restrepo BI, Aguilar MI, Melby PC, Teale JM (2001) Analysis of the peripheral immune response in patients with neurocysticercosis: evidence for T cell reactivity to parasite glycoprotein and vesicular fluid antigens. Am J Trop Med Hyg 65(4):366–370

    PubMed  CAS  Google Scholar 

  16. 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(7):4554–4560

    Article  PubMed  CAS  Google Scholar 

  17. Rolfs A, Muhlschlegel F, Jansen-Rosseck R, Martins AR, Bedaque EA, Tamburus WM, Pedretti L, Schult G, Feldmeier H, Kremsner P (1995) Clinical and immunologic follow-up study of patients with neurocysticercosis after treatment with praziquantel. Neurology 45(3 Pt 1):532–538

    PubMed  CAS  Google Scholar 

  18. Chavarría A, Fleury A, Bobes R, Morales J, Fragoso G, Sciutto E (2006) A depressed peripheral cellular immune response is related with symptomatic neurocysticercosis. Microbes Infect 8(4):1082–1089

    Article  PubMed  Google Scholar 

  19. Evans CA, Garcia HH, Hartnell A, Gilman RH, Jose PJ, Martinez M, Remick DG, Williams TJ, Friedland JS (1998) Elevated concentrations of eotaxin and interleukin-5 in human neurocysticercosis. Infect Immun 66:4522–4525

    PubMed  CAS  Google Scholar 

  20. Rodrigues V Jr, de-Mello FA, Magalhaes EP, Ribeiro SB, Marquez JO (2000) Interleukin-5 and interleukin-10 are major cytokines in cerebrospinal fluid from patients with active neurocysticercosis. Braz J Med Biol Res 33(9):1059–1063

    PubMed  CAS  Google Scholar 

  21. Chavarría 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(12):1109–1115

    Article  PubMed  Google Scholar 

  22. Rosas N, Sotelo J, Nieto D (1986) ELISA in the diagnosis of neurocysticercosis. Arch Neurol 43:353–356

    Article  PubMed  CAS  Google Scholar 

  23. Gaur U, Aggarwal BB (2003) Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochem Pharmacol 66(8):1403–1408

    Article  PubMed  CAS  Google Scholar 

  24. Pott MC, Tarelli R, Ferrari CC, Sarchi MI, Pitossi FJ (2008) Central and systemic IL-1 exacerbates neurodegeneration and motor symptoms in a model of Parkinson’s disease. Brain 131(7):1880–1894

    Article  Google Scholar 

  25. Taoufik Y, de Herve MG, Giron-Michel J, Durali D, Cazes E, Tardieu M, Azzarone B, Delfraissy JF et al (2001) Human microglial cells express a functional IL-12 receptor and produce IL-12 following IL-12 stimulation. Eur J Immunol 31:3228–3239

    Article  PubMed  CAS  Google Scholar 

  26. Lotz M, Jirik F, Kabouridis P, Tsoukas C, Hirano T, Kishimoto T, Carson DA (1998) B cell stimulating factor 2/interleukin 6 is a costimulant for human thymocytes and T lymphocytes. J Exp Med 167:1253–1258

    Article  Google Scholar 

  27. Ghaffar O, Lavigne F, Kamil A, Renzi P, Hamid Q (1998) Interleukin-6 expression in chronic sinusitis: colocalization of gene transcripts to eosinophils, macrophages, T lymphocytes, and mast cells. Otolaryngol Head Neck Surg 118(4):504–511

    Article  PubMed  CAS  Google Scholar 

  28. Karlen S, De Boer ML, Lipscombe RJ, Lutz W, Mordvinov VA, Sanderson CJ (1998) Biological and molecular characteristics of interleukin-5 and its receptor. Int Rev Immunol 16(3–4):227–247

    Article  PubMed  CAS  Google Scholar 

  29. Oukka M (2008) Th17 cells in immunity and autoimmunity. Ann Rheum Dis 67(Suppl 3):iii26-9M

    Google Scholar 

  30. Aloisi F, Ambrosini E, Columba-Cabezas S, Magliozzi R, Serafini B (2001) Intracerebral regulation of immune responses. Ann Med 33(8):510–515

    Article  PubMed  CAS  Google Scholar 

  31. Strle K, Zhou JH, Shen WH, Broussard SR, Johnson RW, Freund GG, Dantzer R, Kelley KW (2001) Interleukin-10 in the brain. Crit Rev Immunol 21(5):427–449

    PubMed  CAS  Google Scholar 

  32. Tiemessen MM, Kunzmann S, Schmidt-Weber CB, Garssen J, Bruijnzeel-Koomen CA, Knol EF, van Hoffen E (2003) Transforming growth factor-beta inhibits human antigen-specific CD4 + T cell proliferation. Int Immunol 15(12):1495–1504

    Article  PubMed  CAS  Google Scholar 

  33. Vitkovic L, Maeda S, Sternberg E (2001) Anti-inflammatory cytokines: expression and action in the brain. Neuroimmunomodulation 9(6):295–312

    Article  PubMed  CAS  Google Scholar 

  34. Hartmann S, Lucius R (2003) Modulation of host immune responses by nematode cystatins. Int J Parasitol 33(11):1291–1302

    Article  PubMed  CAS  Google Scholar 

  35. McFarlane E, Perez C, Charmoy M, Allenbach C, Carter KC, Alexander J, Tacchini-Cottier F (2008) Neutrophils contribute to development of a protective immune response during onset of infection with Leishmania donovani. Infect Immun 76(2):532–541

    Article  PubMed  CAS  Google Scholar 

  36. Wilson EH, Wille-Reece UF, Dzierszinski F, Hunter CA (2005) A critical role for IL-10 in limiting inflammation during toxoplasmic encephalitis. J Neuroimmunol 165:63–74

    Article  PubMed  CAS  Google Scholar 

  37. Herrera LA, Tato P, Molinari JL, Perez E, Dominguez H, Ostrosky-Wegman P (2003) Induction of DNA damage in human lymphocytes treated with a soluble factor secreted by Taenia solium metacestodes. Teratog Carcinog Mutagen Suppl 1:79–83

    Article  Google Scholar 

  38. Tato P, Fernandez AM, Solano S, Borgonio V, Garrido EJ, Sepulveda J, Molinari JL (2004) A cysteine protease from Taenia solium metacestodes induce apoptosis in human CD4+ T-cells. Parasitol Res 92(3):197–204

    Article  PubMed  CAS  Google Scholar 

  39. White AC Jr, Robinson P, Kuhn R (1997) Taenia solium cysticercosis: host-parasite interactions and the immune response. Chem Immunol 66:209–230

    Article  PubMed  Google Scholar 

  40. Liu ZG (2005) Molecular mechanism of TNF signaling and beyond. Cell Res 15(1):24–27

    Article  PubMed  CAS  Google Scholar 

  41. Xu G, Shi Y (2007) Apoptosis signaling pathways and lymphocyte homeostasis. Cell Res 17(9):759–771

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Consejo Nacional de Ciencia y Tecnología 46953-m and 100708. Authors are grateful to the Instituto Nacional de Neurología y Neurocirugía, Mexico, for their support to this project. Isabel Pérez Montfort and Juan Francisco Rodríguez proofread the English version of this manuscript.

Ethical standard

The present study fulfilled all regulations for research with human subjects required by Mexican laws and International regulations. It also complied with all ethical aspects considered in the General Rules of Health for Clinical Investigation. The protocol was approved by the ethics committee of the Instituto Nacional de Neurología y Neurocirugía, México, and written informed consent was obtained from all individuals. All participants volunteered to enter the study. Patients were informed that sera and CSF samples obtained during their hospital studies would be used for this work. All results were confidential.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Unidad Periférica del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, Universidad Nacional Autónoma de México, UNAM, AP 70228, México DF, 04510, México

    Brenda Sáenz, Agnes Fleury, Marisela Hernández, Gladis Fragoso & Edda Sciutto

  2. Posgrado en Ciencias Biológicas, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, México DF, México

    Brenda Sáenz

  3. Instituto Nacional de Neurología y Neurocirugía, Insurgentes Sur 3877, México DF, 14269, México

    Agnes Fleury

  4. Facultad de Medicina, Universidad Nacional Autónoma de México, UNAM, AP 70228, México DF, 04510, México

    Anahí Chavarría

  5. Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, 02115, USA

    José C. Crispin

  6. Instituto Nacional de Enfermedades Respiratorias “Ismael Cosío Villegas”, Calzada de Tlalpan 4502, México DF, 14080, México

    María I. Vargas-Rojas

  7. Departamento de Inmunología, Instituto de Investigaciones Biomédicas, UNAM, AP 70228, México DF, 04510, México

    Edda Sciutto

Authors
  1. Brenda Sáenz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Agnes Fleury
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anahí Chavarría
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marisela Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José C. Crispin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. María I. Vargas-Rojas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gladis Fragoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Edda Sciutto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edda Sciutto.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sáenz, B., Fleury, A., Chavarría, A. et al. Neurocysticercosis: local and systemic immune-inflammatory features related to severity. Med Microbiol Immunol 201, 73–80 (2012). https://doi.org/10.1007/s00430-011-0207-0

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00430-011-0207-0

Keywords

Search

Navigation