Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009

  • E. Pinelli
  • T. Herremans
  • M. G. Harms
  • D. Hoek
  • L. M. Kortbeek
Article

Abstract

Toxocara canis, Toxocara cati and Ascaris suum are roundworms of dogs, cats and pigs, respectively, that can also infect humans. These zoonotic helminths have a worldwide distribution and are also endemic in the Netherlands. Infection with Toxocara sp. may result in visceral larva migrans (VLM) or ocular larva migrans (OLM) caused by the migrating larvae. Although A. suum has been reported to occasionally mature to the adult stage in humans, clinical cases of VLM suspected to be caused by A. suum have been described. Diagnosis of these helminth infections relies mainly on serology. Here we analyse the results from the Toxocara and Ascaris IgG-ELISA from a total of 2,838 serum samples from VLM and OLM suspected patients that were sent to our institution from 1998 to 2009. Results indicate that for each year the Ascaris seropositivity is significantly higher compared to the Toxocara seropositivity. Furthermore, while Toxocara seropositivity has decreased over time, the Ascaris seropositivity has not significantly changed for the past 12 years. The Ascaris and Toxocara seropositivity was also shown to increases with age and, while gender has no influence on the Ascaris seropositivity, males showed higher Toxocara seropositivity.

Keywords

Canis Ascaris Ascariasis Larva Migrans Toxocariasis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Crompton DW (2001) Ascaris and ascariasis. Adv Parasitol 48:285–375PubMedCrossRefGoogle Scholar
  2. 2.
    Glickman LT, Schantz PM (1981) Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiol Rev 3:230–250PubMedGoogle Scholar
  3. 3.
    Despommier D (2003) Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 16:265–272PubMedCrossRefGoogle Scholar
  4. 4.
    Nagakura K, Tachibana H, Kaneda Y, Kato Y (1989) Toxocariasis possibly caused by ingesting raw chicken. J Infect Dis 160:735–736PubMedCrossRefGoogle Scholar
  5. 5.
    Salem G, Schantz P (1992) Toxocaral visceral larva migrans after ingestion of raw lamb liver. Clin Infect Dis 15:743–744PubMedCrossRefGoogle Scholar
  6. 6.
    Permin A, Henningsen E, Murrell KD, Roepstorff A, Nansen P (2000) Pigs become infected after ingestion of livers and lungs from chickens infected with Ascaris of pig origin. Int J Parasitol 30:867–868PubMedCrossRefGoogle Scholar
  7. 7.
    Nejsum P, Parker ED Jr, Frydenberg J, Roepstorff A, Boes J, Haque R, Astrup I, Prag J, Skov Sorensen UB (2005) Ascariasis is a zoonosis in Denmark. J Clin Microbiol 43:1142–1148PubMedCrossRefGoogle Scholar
  8. 8.
    Arizono N, Yoshimura Y, Tohzaka N, Yamada M, Tegoshi T, Onishi K, Uchikawa R (2010) Ascariasis in Japan: is pig-derived Ascaris infecting humans? Jpn J Infect Dis 63:447–448PubMedGoogle Scholar
  9. 9.
    Kakihara D, Yoshimitsu K, Ishigami K, Irie H, Aibe H, Tajima T, Shinozaki K, Nishie A, Nakayama T, Hayashida K, Nakamuta M, Nawata H, Honda H (2004) Liver lesions of visceral larva migrans due to Ascaris suum infection: CT findings. Abdom Imaging 29:598–602PubMedCrossRefGoogle Scholar
  10. 10.
    Okada F, Ono A, Ando Y, Yotsumoto S, Yotsumoto S, Tanoue S, Matsumoto S, Wakisaka M, Mori H (2007) Pulmonary computed tomography findings of visceral larva migrans caused by Ascaris suum. J Comput Assist Tomogr 31:402–408PubMedCrossRefGoogle Scholar
  11. 11.
    Taylor MHR, OÇonnor P, Keane CT, Mulvihill E, Holland C (1988) The expanded spectrum of Toxocaral disease. Lancet 26:692–695CrossRefGoogle Scholar
  12. 12.
    Taylor MR (2001) The epidemiology of ocular toxocariasis. J Helminthol 75:109–118PubMedGoogle Scholar
  13. 13.
    van Knapen F, Leusden J, Polderman AM, Franchimont JH (1983) Visceral larva migrans: examinations by means of enzyme-linked immunosorbent assay of human sera for antibodies to excretory-secretory antigens of the second-stage larvae of Toxocara canis. Z Parasitenkd 69:113–118PubMedCrossRefGoogle Scholar
  14. 14.
    Pinelli E, Willers SM, Hoek D, Smit HA, Kortbeek LM, Hoekstra M, de Jongste J, van Knapen F, Postma D, Kerkhof M, Aalberse R, van der Giessen JW, Brunekreef B (2009) Prevalence of antibodies against Ascaris suum and its association with allergic manifestations in 4-year-old children in The Netherlands: the PIAMA birth cohort study. Eur J Clin Microbiol Infect Dis 28:1327–1334PubMedCrossRefGoogle Scholar
  15. 15.
    Rubinsky-Elefant G, Hirata CE, Yamamoto JH, Ferreira MU (2010) Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms. Ann Trop Med Parasitol 104:3–23PubMedCrossRefGoogle Scholar
  16. 16.
    Magnaval JF, Glickman LT, Dorchies P, Morassin B (2001) Highlights of human toxocariasis. Korean J Parasitol 39:1–11PubMedCrossRefGoogle Scholar
  17. 17.
    Smith H, Holland C, Taylor M, Magnaval JF, Schantz P, Maizels R (2009) How common is human toxocariasis? Towards standardizing our knowledge. Trends Parasitol 25:182–188PubMedCrossRefGoogle Scholar
  18. 18.
    van Knapen F, Buijs J, Kortbeek LM, Ljungstrom I (1992) Larva migrans syndrome: toxocara, ascaris, or both? Lancet 340:550–551PubMedCrossRefGoogle Scholar
  19. 19.
    de Wit MA, Koopmans MP, Kortbeek LM, Wannet WJ, Vinje J, van Leusden F, Bartelds AI, van Duynhoven YT (2001) Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. Am J Epidemiol 154:666–674PubMedCrossRefGoogle Scholar
  20. 20.
    de Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Vinje J, van Duynhoven YT (2001) Etiology of gastroenteritis in sentinel general practices in the Netherlands. Clin Infect Dis 33:280–288PubMedCrossRefGoogle Scholar
  21. 21.
    Lozano MJ, Martin HL, Diaz SV, Manas AI, Valero LA, Campos BM (2004) Cross-reactivity between antigens of Anisakis simplex s.l. and other ascarid nematodes. Parasite 11:219–223PubMedGoogle Scholar
  22. 22.
    Overgaauw PA, Boersema JH (1996) Assessment of an educational campaign by practicing veterinarians in the Netherlands on human and animal Toxocara infections. Tijdschr Diergeneeskd 121:615–618PubMedGoogle Scholar
  23. 23.
    Overgaauw PAM (1997) Aspects of toxocara epidemiology: human toxocarosis. Crit Rev Microbiol 23:215–231PubMedCrossRefGoogle Scholar
  24. 24.
    Eijck IA, Borgsteede FH (2005) A survey of gastrointestinal pig parasites on free-range, organic and conventional pig farms in the Netherlands. Vet Res Commun 29:407–414PubMedCrossRefGoogle Scholar
  25. 25.
    Buijs J, Borsboom G, Renting M, Hilgersom WJ, van Wieringen JC, Jansen G, Neijens J (1997) Relationship between allergic manifestations and Toxocara seropositivity: a cross-sectional study among elementary school children. Eur Respir J 10:1467–1475PubMedCrossRefGoogle Scholar
  26. 26.
    Holland CV, O'Lorcain P, Taylor MR, Kelly A (1995) Sero-epidemiology of toxocariasis in school children. Parasitology 110(Pt 5):535–545PubMedCrossRefGoogle Scholar
  27. 27.
    Deutz A, Fuchs K, Auer H, Kerbl U, Aspock H, Kofer J (2005) Toxocara-infestations in Austria: a study on the risk of infection of farmers, slaughterhouse staff, hunters and veterinarians. Parasitol Res 97:390–394PubMedCrossRefGoogle Scholar
  28. 28.
    Pinelli E, Kortbeek LM, van der Giessen J (2005) Toxocara. In: Wakelin D, Cox F, Despommier D, Gilliespie S (eds) Parasitology. Hodder Arnold, London, pp 750Google Scholar
  29. 29.
    Petithory JC (1996) Can Ascaris suum cause visceral larva migrans? Lancet 348:689PubMedCrossRefGoogle Scholar
  30. 30.
    Nejsum P, Bertelsen MF, Betson M, Stothard JR, Murrell KD (2010) Molecular evidence for sustained transmission of zoonotic Ascaris suum among zoo chimpanzees (Pan troglodytes). Vet Parasitol 171:273–276PubMedCrossRefGoogle Scholar
  31. 31.
    Cooper PJ (2009) Interactions between helminth parasites and allergy. Curr Opin Allergy Clin Immunol 9:29–37PubMedCrossRefGoogle Scholar
  32. 32.
    Pinelli E, Brandes S, Dormans J, Gremmer E, Van Loveren H (2008) Infection with the roundworm Toxocara canis leads to exacerbation of experimental allergic airway inflammation. Clin Exp Allergy 38:649–658PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • E. Pinelli
    • 1
  • T. Herremans
    • 1
  • M. G. Harms
    • 1
  • D. Hoek
    • 1
  • L. M. Kortbeek
    • 1
  1. 1.National Institute of Public Health and the Environment (RIVM)Centre for Infectious Disease Control NetherlandsBA BilthovenThe Netherlands

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