SpringerLink
Log in

Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil. V. Cytokine concentrations in experimentally infected Wistar rats

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Tungiasis is caused by the penetration of the female sand flea Tunga penetrans into the skin of its host. This parasitic skin disease is almost invariably associated with an intense inflammation around embedded fleas, the underlying mechanisms being unknown. A study was undertaken to determine whether Wistar rats can be used as an animal model to assess cytokine kinetics during the natural course of the infection. Laboratory-raised Wistar rats were exposed in cages put on the soil in an area with high human attack rates. Rats were examined daily and blood samples were taken before exposure and at 2, 6, 10, 13, 16 and 20 days after flea penetration. TNF-α, IL-1β, IFN-γ, IL-4, IL-10 and CINC (a rat cytokine- induced neutrophil chemoattractant and member of the IL-8 family) were determined by enzyme immunoassay. The results showed an increasing serum concentration of TNF-α and IL-1β 10–13 days after penetration and a rapid increase in IL-4 2 days after fleas became embedded. During the natural course of the infection, the ratio of the serum concentration of TNF-α to that of IL-10 decreased, indicating a relative increase in the secretion of the anti-inflammatory cytokine. The treatment of lesions with silicone oil abrogated the natural disease course and changed the pattern of cytokine secretion. We conclude that the Wistar rat is an appropriate model to study immune responses in tungiasis.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–f
Fig. 2

Similar content being viewed by others

References

  • Arlian LG, Vyszenski-Moher DL, Rapp CM, Hull BE (1996) Production of IL-1 alpha and IL-1 beta by human skin equivalents parasitized by Sarcoptes scabiei. J Parasitol 82: 719–723

    CAS  PubMed  Google Scholar 

  • Arlian LG, Morgan MS, Neal JS (2004) Extracts of scabies mites (Sarcoptidae: Sarcoptes scabiei) modulate cytokine expression by human peripheral blood mononuclear cells and dendritic cells. J Med Entomol 41:69–73

    CAS  PubMed  Google Scholar 

  • Bourreau E, Prevot G, Gardon J, Pradinaud R, Launois P (2001) High intralesional interleukin-10 messenger RNA expression in localized cutaneous leishmaniasis is associated with unresponsiveness to treatment. J Infect Dis 184:1628–1630

    Article  CAS  PubMed  Google Scholar 

  • Egan PJ, Kimpton W, Seow HF, Bowles VM, Brandon MR, Nash AD (1996) Inflammation-induced changes in the phenotype and cytokine profile of cells migrating through skin and afferent lymph. Immunology 89:539–546

    Article  CAS  PubMed  Google Scholar 

  • Eisele M, Heukelbach J, Van Marck E, Mehlhorn H, Meckes O, Franck S, Feldmeier H (2003) Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: I. Natural history of tungiasis in man. Parasitol Res 90:87–99

    PubMed  Google Scholar 

  • Elhay MJ, Hanrahan CF, Bowles VM, Seow HF, Andrews AE, Nash AD (1994) Cytokine mRNA expression in skin in response to ectoparasite infection. Parasite Immunol 16:451–461

    CAS  PubMed  Google Scholar 

  • Feldmeier H, Heukelbach J, Eisele M, Sousa AQ, Barbosa LM, Carvalho CB (2002) Bacterial superinfection in human tungiasis. Trop Med Int Health 7:559–564

    Article  CAS  PubMed  Google Scholar 

  • Feldmeier H, Eisele M, Saboia-Moura RC, Heukelbach J (2003a) Severe tungiasis in underprivileged communities: case series from Brazil. Emerg Infect Dis 9:949–955

    PubMed  Google Scholar 

  • Feldmeier H, Heukelbach J, Eisele M, Ribeiro R, Harms G, Mehlhorn H, Liesenfeld O (2003b) Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: III. Cytokine levels in peripheral blood of infected humans. Parasitol Res 91:298–303

    Article  PubMed  Google Scholar 

  • Feldmeier H, Eisele M, Van Marck E, et al (2004) Investigations of the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: IV. Clinical and histopathology. Parasitol Res DOI 10.1007/s00436-004-1197-2

  • Heukelbach J, Oliveira FA de, Hesse G, Feldmeier H (2001) Tungiasis: a neglected health problem of poor communities. Trop Med Int Health 6:267–272

    Article  CAS  PubMed  Google Scholar 

  • Heukelbach J, Franck S, Feldmeier H (2004a) High attack rate of Tunga penetrans (Linnaeus 1758) infestation in an impoverished Brazilian community. Trans R Soc Trop Med Hyg 98:431–434

    Article  CAS  PubMed  Google Scholar 

  • Heukelbach J, Winter B, Wilcke T, et al (2004b) Selective mass treatment with ivermectin to control intestinal helminthiases and parasitic skin diseases in a severely affected population. Bull WHO 82:563–571

    PubMed  Google Scholar 

  • Heukelbach J, Bonow I, Witt L, et al (2004c) High infection rate of Wolbachia endobacteria in the sand flea Tunga penetrans from Brazil. Acta Tropica (in press)

  • Iida M, Watanabe K, Tsurufuji M, Takaishi K, Iizuka Y, Tsurufuji S (1992) Level of neutrophil chemotactic factor CINC/gro, a member of the interleukin-8 family, associated with lipopolysaccharide-induced inflammation in rats. Infect Immun 60:1268–1272

    CAS  PubMed  Google Scholar 

  • Otranto D (2001) The immunology of myiasis: parasite survival and host defense strategies. Trends Parasitol 17:176–182

    Article  CAS  PubMed  Google Scholar 

  • Saint Andre A, Blackwell NM, Hall LR, et al (2002) The role of endosymbiotic Wolbachia bacteria in the pathogenesis of river blindness. Science 295:1892–1895

    Article  PubMed  Google Scholar 

  • Sato Y, Ohshima T (2000) The expression of mRNA of proinflammatory cytokines during skin wound healing in mice: a preliminary study for forensic wound age estimation (II). Int J Legal Med 113:140–145

    Article  CAS  PubMed  Google Scholar 

  • Tani K, Morimoto M, Hayashi T, Inokuma H, Ohnishi T, Hayashiya S, Nomura T, Une S, Nakaichi M, Taura Y (2002) Evaluation of cytokine messenger RNA expression in peripheral blood mononuclear cells from dogs with canine demodicosis. J Vet Med Sci 64:513–518

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K, Koizumi F, Kurashige Y, Tsurufuji S, Nakagawa H (1991) Rat CINC, a member of the interleukin-8 family, is a neutrophil-specific chemoattractant in vivo. Exp Mol Pathol 55:30–37

    Article  CAS  PubMed  Google Scholar 

  • Wikel SK, Alarcon-Chaidez FJ (2001) Progress toward molecular characterization of ectoparasite modulation of host immunity. Vet Parasitol 101:275–287

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was partly supported by the World Health Organization (Geneva, Switzerland) and the PROBRAL CAPES/DAAD academic exchange program. The data are part of a medical thesis by L.-H.W. The secretarial assistance of Michi Feldmeier and the technical assistance of Solvy Wolcke are gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Medical Microbiology and Immunology of Infection, Institute of Infection Medicine, Charité University Medicine Berlin, Campus Benjamin Franklin, Hindenburgdamm 27, 12203, Berlin, Germany

    Hermann Feldmeier, Lars-Henrik Witt, Stefan Schwalfenberg & Oliver Liesenfeld

  2. Department of Pharmacology and Physiology, School of Medicine, Federal University of Ceará, Fortaleza, Brazil

    Ronaldo Albuquerque Ribeiro

  3. Department of Pharmacology, Federal University of São Paulo, Ribeirão Preto, Brazil

    Fernando Queiroz Cunha

  4. Institute of Tropical Medicine, Charité University Medicine Berlin, 14050, Berlin, Germany

    Gundel Harms

  5. Department of Zoology and Parasitology, Heinrich-Heine-University, 40225, Düsseldorf, Germany

    Heinz Mehlhorn

  6. Department of Community Health, Medical School, Federal University of Ceará and Mandacaru Foundation, Fortaleza, Brazil

    Jörg Heukelbach

Authors
  1. Hermann Feldmeier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lars-Henrik Witt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stefan Schwalfenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ronaldo Albuquerque Ribeiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fernando Queiroz Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gundel Harms
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Heinz Mehlhorn
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Oliver Liesenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jörg Heukelbach
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hermann Feldmeier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feldmeier, H., Witt, LH., Schwalfenberg, S. et al. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil. V. Cytokine concentrations in experimentally infected Wistar rats. Parasitol Res 94, 371–376 (2004). https://doi.org/10.1007/s00436-004-1219-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-004-1219-0

Keywords

Search

Navigation