Parasitology Research

, Volume 101, Supplement 2, pp 233–242 | Cite as

Investigations on the life cycle and morphology of Tunga penetrans in Brazil

  • N. Nagy
  • E. Abari
  • J. D’Haese
  • C. Calheiros
  • J. Heukelbach
  • N. Mencke
  • H. Feldmeier
  • H. Mehlhorn
Original Paper

Abstract

In the present study, the life cycle of Tunga penetrans was established in Wistar rats in the laboratory, and the morphology of the resulting developmental stages was studied by means of light and scanning electron microscopy. It was seen that the females enter at a nonfertilized stage through the skin of their hosts. Only there the copulation occurs, while females and males brought together in a Petri dish showed no interest in each other. In any way—fertilized or not—the females start about 6 days after penetration and hypertrophy with the ejection of eggs. While fertilized eggs proceed to development, the unfertilized ones remain arrested. The eggs are ovoid and measure about 600 × 320 μm. The larvae hatch from the eggs 1–6 days (mean 3–4) after ejection. Formation of larvae 2 took at least another day, while 4 up to 10 days more were needed until this larva starts pupation (mean 5–7 days). The formation of the adult fleas inside the puparium occurred within 9–15 days (with a maximum hatch at day 12). Adult female fleas having reached the skin of a host start blood sucking within 5 min and prepare to enter the skin. After 24 h, the flea stacked already with two thirds of its body inside the skin. After 40 h, the penetration was completed, and feeding and hypertrophical enlargement started, which was completed on day 6, when eggs became ejected. When studying the morphology of the fleas obtained from different hosts, slight variations were seen, which, however, are not significant for a species separation but may be an indication of the presence of different strains/races or the beginning of such a formation.

Notes

Acknowledgments

We are grateful to Prof. Trentini and Prof. Luchetti from the Facoltà Di Medicina Veterinaria in Bologna (Italy) for sending us three specimens of gravid female T. penetrans and three specimens of gravid female T. trimamillata isolated in Ecuador. Furthermore, we thank Valeria Santos (Fortaleza) for her support during the field study in Brazil.

References

  1. Achtman M, Morelli G, Zhu P, Wirth T, Diehl I, Kusecek B, Vogler AJ, Wagner DM, Allender CJ, Easterday WR, Chenal-Francisque V, Worsham P, Thomson NR, Parkhill J, Lindler LE, Carniel E, Keim P (2004) Microevolution and history of the plague bacillus Yersinia pestis. Proc Natl Acad Sci USA 101:17837–17842PubMedCrossRefGoogle Scholar
  2. Blair PJ, Jiang J, Schoeler GB, Moron C, Anaya E, Cespedes M, Cruz C, Felices V, Guevara C, Mendoza L, Villaseca P, Sumner JW, Richards AL, Olson JG (2004) Characterization of spotted fever group rickettsiae in flea and tick specimens from Northern Peru. J Clin Microbiol 42:4961–4967PubMedCrossRefGoogle Scholar
  3. Connor DH (1976) Diseases caused by arthropods: tungiasis. In: Binford CH, Connor DH (eds) Pathology of tropical and extraordinary diseases. Armed Forces Institute of Pathology, Washington, DC, pp 610–614Google Scholar
  4. 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 90:87–99PubMedGoogle Scholar
  5. Feldmeier H, Heukelbach J, Eisele M, Queiroz Sousa A, Marilac Meireles Barbosa L, Carvalho CBM (2002) Bacterial superinfection in human tungiasis. Trop Med Int Health 7:559–564PubMedCrossRefGoogle Scholar
  6. Feldmeier H, Eisele M, Saboia-Moura RC, Heukelbach J (2003) Severe tungiasis in underprivileged communities: a case series from Brazil. Emerg Infect Dis 9:949–955PubMedGoogle Scholar
  7. Geigy R, Herbig A (1949) Die Hypertrophie der Organe beim Weibchen von Tunga penetrans. Acta Trop 6:246–262PubMedGoogle Scholar
  8. Geigy R, Suter P (1958) Zur Kopulation der Flöhe. Report Schweizerisches Tropeninstitut, Basel. P. pp 150–160Google Scholar
  9. Greco JB, Sacramento E, Tavares-Neto J (2001) Chronic ulcers and myiasis as ports of entry for Clostridium tetani. Braz J Infect Dis 5:319–323PubMedCrossRefGoogle Scholar
  10. Heukelbach J, Araújo Sales de Oliveira F, Hesse G, Feldmeier H (2001) Tungiasis: a neglected health problem of poor communities. Trop Med Int Health 6:267–272PubMedCrossRefGoogle Scholar
  11. Heukelbach J, Costa AML, Wilcke T, Mencke N, Feldmeier H (2004) The animal reservoir of Tunga penetrans in severely affected communities of North-East Brazil. Med Vet Entomol 18:329–335PubMedCrossRefGoogle Scholar
  12. Hicks EP (1930) The early stages of the jigger flea, Tunga penetrans. Ann Trop Med Parasitol 24:575–586Google Scholar
  13. Lane RP, Crosskey RW (eds) (1993) Medical insects and arachnids. Chapman and Hall, LondonGoogle Scholar
  14. Lewis RE (1998) Résumé of the Siphonaptera (Insecta) of the World. J Med Entomol 35:377–389PubMedGoogle Scholar
  15. Linardi PM, Guimaráes LR (2000) Sifonapteros do Brasil. FAPESP 1. pp 157–181Google Scholar
  16. Mehlhorn H, Eichenlaub D, Löscher T, Peters W (1995) Diagnostik und Therapie der Parasitosen des Menschen, 2nd edn. Gustav Fischer, Stuttgart, pp 328–337Google Scholar
  17. Muehlen M, Heukelbach J, Wilcke T, Winter B, Mehlhorn H, Feldmeier H (2003) Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil. Parasitol Res 90:449–455PubMedCrossRefGoogle Scholar
  18. Nagy N, D’Haese J, Heukelbach J, Mencke N, Feldmeier H, Mehlhorn H (2007) Molecular biological comparison of jigger fleas from different hosts. Parasitol Res (in press)Google Scholar
  19. Njeumi F, Nsangou C, Ndjend AG, Koga Ostanello F, Pampiglione S (2002) Tunga penetrans. au Cameroun. Rev Med Vet 153:176–180Google Scholar
  20. Pampiglione S, Trentini M, Fioravanti ML, Onore G, Rivasi F (2002) A new species of Tunga (Insecta, Siphonaptera) in Ecuador. Parassitologia 44:127Google Scholar
  21. Pampiglione S, Trentini M, Fioravanti ML, Onore G, Rivasi F (2003) Additional description of a new species of Tunga (Siphonaptera) from Ecuador. Parasite 10:9–15PubMedGoogle Scholar
  22. Pampiglione S, Trentini M, Fioravanti ML, Gustinelli A (2004) Differential diagnosis between Tunga penetrans (L., 1758) and T. trimamillata Pampiglione et al., 2002 (Insecta, Siphonaptera), the two species of the genus Tunga parasitic in man. Parasite 11:51–57PubMedGoogle Scholar
  23. Titball RW, Hill J, Lawton DG, Brown KA (2003) Yersinia pestis. and plague. Biochem Soc Trans 31:104–107PubMedCrossRefGoogle Scholar
  24. Vobis M (2002) Flöhe und ihre molekularbiologische Charakterisierung. Diploma thesis, University of DüsseldorfGoogle Scholar
  25. Vobis M, D’Haese J, Mehlhorn H, Mencke N (2003) Evidence of horizontal transmission of feline leukemia virus by the cat flea (Ctenocephalides felis). Parasitol Res 91:467–470PubMedCrossRefGoogle Scholar
  26. Vobis M, D’Haese J, Mehlhorn H, Mencke N, Blagburn BL, Bond R, Denholm I, Dryden MW, Payne P, Rust MK, Schroeder I, Vaughn MB, Bledsoe D (2004) Molecular phylogeny of isolates of Ctenocephalides felis and related species based on analysis of ITS1, ITS2 and mitochondrial 16S rDNA sequences and random binding primers. Parasitol Res 94:219–226PubMedCrossRefGoogle Scholar
  27. Vobis M, D’Haese J, Mehlhorn H, Heukelbach J, Mencke N, Feldmeier H (2005) Molecular biological investigations of Brazilian Tunga isolates from man, dogs, cats, pigs and rats. Parasitol Res 96:107–112PubMedCrossRefGoogle Scholar
  28. Vobis M, D’Haese J, Mehlhorn H, Mencke N, Truyen U (2007) Fleas as vectors of calici-virus of cats. Parasitol Res (in press)Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • N. Nagy
    • 1
  • E. Abari
    • 1
  • J. D’Haese
    • 1
  • C. Calheiros
    • 2
  • J. Heukelbach
    • 3
  • N. Mencke
    • 4
  • H. Feldmeier
    • 5
  • H. Mehlhorn
    • 1
  1. 1.Institute of Zoomorphology, Cell Biology and ParasitologyHeinrich-Heine UniversityDüsseldorfGermany
  2. 2.Department of PathologyEscola de Ciencias Medicas de AlagoasMaceióBrazil
  3. 3.Department of Community Health, Medical SchoolFederal University of CearáFortalezaBrazil
  4. 4.Animal Health DivisionBayer HealthCare AGLeverkusenGermany
  5. 5.Institute of Microbiology and HygieneCharité-University Medicine BerlinBerlinGermany

Personalised recommendations