Skip to main content
SpringerLink
Log in

Seroepidemiology of human Toxocara and Ascaris infections in the Netherlands

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

Abstract

Toxocara canis, Toxocara cati and Ascaris suum are worldwide-distributed zoonotic roundworms of dogs, cats and pigs, respectively. The epidemiology of these parasites in developed countries is largely unclear. Two countrywide cross-sectional serosurveys were therefore conducted in the Netherlands in 1995/1996 and 2006/2007 to investigate the prevalence, trends and risk factors for human Toxocara and Ascaris infections in the general population. The Netherlands is characterized by high pig production, freedom from stray dogs and virtual absence of autochthonous infections with the human-adapted roundworm Ascaris lumbricoides. Over the 10 years between the two serosurveys, Toxocara seroprevalence decreased significantly from 10.7 % (n = 1159) to 8.0 % (n = 3683), whereas Ascaris seroprevalence increased significantly from 30.4 % (n = 1159) to 41.6 % (n = 3675), possibly reflecting concomitant improvements in pet hygiene management and increased exposure to pig manure-contaminated soil. Increased anti-Toxocara IgGs were associated with increasing age, male gender, contact with soil, ownership of cats, cattle or pigs, hay fever, low education, high income and non-Western ethnic origin. Increased anti-Ascaris IgGs were associated with increasing age, owning pigs, low education, childhood geophagia and non-Dutch ethnic origin. Besides identifying specific groups at highest risk of Toxocara and Ascaris infections, our results suggest that these infections mainly occur through environmental, rather than foodborne, routes, with direct contact with soil or cat and pig ownership being potentially modifiable exposures.

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
Fig. 3

Similar content being viewed by others

References

  • Baboolal S, Rawlins SC (2002) Seroprevalence of toxocariasis in schoolchildren in Trinidad. Trans R Soc Trop Med Hyg 96(2):139–143

    Article  PubMed  Google Scholar 

  • Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367(9521):1521–1532. doi:10.1016/s0140-6736(06)68653-4

    Article  PubMed  Google Scholar 

  • De Melker HE, Conyn-van Spaendonck MA (1998) Immunosurveillance and the evaluation of national immunization programmes: a population-based approach. Epidemiol Infect 121(3):637–643

    Article  PubMed  PubMed Central  Google Scholar 

  • de Wit MA, Koopmans MP, Kortbeek LM, van Leeuwen NJ, Vinje J, van Duynhoven YT (2001a) Etiology of gastroenteritis in sentinel general practices in the Netherlands. Clin Infect Dis 33(3):280–288. doi:10.1086/321875

    Article  PubMed  Google Scholar 

  • de Wit MA, Koopmans MP, Kortbeek LM, Wannet WJ, Vinje J, van Leusden F, Bartelds AI, van Duynhoven YT (2001b) Sensor, a population-based cohort study on gastroenteritis in the Netherlands: incidence and etiology. Am J Epidemiol 154(7):666–674

    Article  PubMed  Google Scholar 

  • Despommier D (2003) Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev 16(2):265–272

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(5):390–394. doi:10.1007/s00436-005-1469-5

    Article  PubMed  Google Scholar 

  • 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(5):407–414. doi:10.1007/s11259-005-1201-z

    Article  CAS  PubMed  Google Scholar 

  • El Guamri Y, Belghyti D, Barkia A, Tiabi M, Aujjar N, Achicha A, El Kharrim K, Elfellaki L (2011) Parasitic infection of the digestive tract in children in a regional hospital center in Gharb (Kenitra, Morroco): some epidemiological features. East Afr J Public Health 8(4):250–257

    PubMed  Google Scholar 

  • Georges K, Adesiyun A (2008) An investigation into the prevalence of dog bites to primary school children in Trinidad. BMC Public Health 8:85. doi:10.1186/1471-2458-8-85

    Article  PubMed  PubMed Central  Google Scholar 

  • Haswell-Elkins MR, Leonard H, Kennedy MW, Elkins DB, Maizels RM (1992) Immunoepidemiology of Ascaris lumbricoides: relationships between antibody specificities, exposure and infection in a human community. Parasitology 104(Pt 1):153–159

    Article  PubMed  Google Scholar 

  • Holland CV (2015) Knowledge gaps in the epidemiology of Toxocara: the enigma remains. Parasitology:1–14 doi:10.1017/s0031182015001407

  • Izumikawa K, Kohno Y, Izumikawa K, Hara K, Hayashi H, Maruyama H, Kohno S (2011) Eosinophilic pneumonia due to visceral larva migrans possibly caused by Ascaris suum: a case report and review of recent literatures. Jpn J Infect Dis 64(5):428–432

    PubMed  Google Scholar 

  • Kanobana K, Vereecken K, Junco Diaz R, Sariego I, Rojas L, Bonet Gorbea M, Polman K (2013) Toxocara seropositivity, atopy and asthma: a study in Cuban schoolchildren. Trop Med Int Health 18(4):403–406. doi:10.1111/tmi.12073

    Article  CAS  PubMed  Google Scholar 

  • Kaplan M, Kalkan A, Hosoglu S, Kuk S, Ozden M, Demirdag K, Ozdarendeli A (2004) The frequency of Toxocara infection in mental retarded children. Mem Inst Oswaldo Cruz 99(2):121–125 doi:/S0074-02762004000200001

  • Kim S, Maekawa Y, Matsuoka T, Imoto S, Ando K, Mita K, Kim H, Nakajima T, Ku K, Koterazawa T, Fukuda K, Yano Y, Nakaji M, Kudo M, Kim K, Hirai M, Hayashi Y (2002) Eosionophilic pseudotumor of the liver due to Ascaris suum infection. Hepatol Res 23(4):306

    Article  PubMed  Google Scholar 

  • Krecek RC, Moura L, Lucas H, Kelly P (2010) Parasites of stray cats (Felis domesticus L., 1758) on St. Kitts, West Indies. Vet Parasitol 172(1–2):147–149. doi:10.1016/j.vetpar.2010.04.033

    Article  CAS  PubMed  Google Scholar 

  • Leles D, Gardner SL, Reinhard K, Iniguez A, Araujo A (2012) Are Ascaris lumbricoides and Ascaris suum a single species? Parasit Vectors 5:42. doi:10.1186/1756-3305-5-42

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(2):219–223

    Article  PubMed  Google Scholar 

  • Lynch NR, Hagel I, Vargas V, Rotundo A, Varela MC, Di Prisco MC, Hodgen AN (1993) Comparable seropositivity for ascariasis and toxocariasis in tropical slum children. Parasitol Res 79(7):547–550

    Article  CAS  PubMed  Google Scholar 

  • Nagakura K, Tachibana H, Kaneda Y, Kato Y (1989) Toxocariasis possibly caused by ingesting raw chicken. J Infect Dis 160(4):735–736

    Article  CAS  PubMed  Google Scholar 

  • 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(3):1142–1148. doi:10.1128/jcm.43.3.1142-1148.2005

    Article  PubMed  PubMed Central  Google Scholar 

  • Nijsse R, Mughini-Gras L, Wagenaar JA, Franssen F, Ploeger HW (2015a) Environmental contamination with Toxocara eggs: a quantitative approach to estimate the relative contributions of dogs, cats and foxes, and to assess the efficacy of advised interventions in dogs. Parasit Vectors 8:397. doi:10.1186/s13071-015-1009-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Nijsse R, Ploeger HW, Wagenaar JA, Mughini-Gras L (2015b) Toxocara canis in household dogs: prevalence, risk factors and owners’ attitude towards deworming. Parasitol Res 114(2):561–569. doi:10.1007/s00436-014-4218-9

    Article  CAS  PubMed  Google Scholar 

  • 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(21):615–618

    CAS  PubMed  Google Scholar 

  • Overgaauw PA, van Zutphen L, Hoek D, Yaya FO, Roelfsema J, Pinelli E, van Knapen F, Kortbeek LM (2009) Zoonotic parasites in fecal samples and fur from dogs and cats in The Netherlands. Vet Parasitol 163(1–2):115–122. doi:10.1016/j.vetpar.2009.03.044

    Article  PubMed  Google Scholar 

  • 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(7):867–868

    Article  CAS  PubMed  Google Scholar 

  • Pinelli E, Aranzamendi C (2012) Toxocara infection and its association with allergic manifestations. Endocr Metab Immune Disord Drug Targets 12(1):33–44

    Article  CAS  PubMed  Google Scholar 

  • Pinelli E, Herremans T, Harms MG, Hoek D, Kortbeek LM (2011) Toxocara and Ascaris seropositivity among patients suspected of visceral and ocular larva migrans in the Netherlands: trends from 1998 to 2009. Eur J Clin Microbiol Infect Dis 30(7):873–879. doi:10.1007/s10096-011-1170-9

    Article  CAS  PubMed  Google Scholar 

  • 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(11):1327–1334. doi:10.1007/s10096-009-0785-6

    Article  CAS  PubMed  Google Scholar 

  • Salem G, Schantz P (1992) Toxocaral visceral larva migrans after ingestion of raw lamb liver. Clin Infect Dis 15(4):743–744

    Article  CAS  PubMed  Google Scholar 

  • Schneider R, Auer H (2015) Incidence of Ascaris suum-specific antibodies in Austrian patients with suspected larva migrans visceralis (VLM) syndrome. Parasitol Res. doi:10.1007/s00436-015-4857-5

    PubMed Central  Google Scholar 

  • Sharghi N, Schantz PM, Caramico L, Ballas K, Teague BA, Hotez PJ (2001) Environmental exposure to Toxocara as a possible risk factor for asthma: a clinic-based case–control study. Clin Infect Dis 32(7):E111–116. doi:10.1086/319593

    Article  CAS  PubMed  Google Scholar 

  • 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(4):182–188. doi:10.1016/j.pt.2009.01.006

    Article  PubMed  Google Scholar 

  • Thompson DE, Bundy DA, Cooper ES, Schantz PM (1986) Epidemiological characteristics of Toxocara canis zoonotic infection of children in a Caribbean community. Bull World Health Organ 64(2):283–290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uga S, Kataoka N (1995) Measures to control Toxocara egg contamination in sandpits of public parks. Am J Trop Med Hyg 52(1):21–24

    CAS  PubMed  Google Scholar 

  • Umetsu S, Sogo T, Iwasawa K, Kondo T, Tsunoda T, Oikawa-Kawamoto M, Komatsu H, Inui A, Fujisawa T (2014) Intestinal ascariasis at pediatric emergency room in a developed country. World J Gastroenterol 20(38):14058–14062. doi:10.3748/wjg.v20.i38.14058

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Klis FR, Mollema L, Berbers GA, de Melker HE, Coutinho RA (2009) Second national serum bank for population-based seroprevalence studies in the Netherlands. Neth J Med 67(7):301–308

    PubMed  Google Scholar 

  • van Knapen F, Buijs J, Kortbeek LM, Ljungstrom I (1992) Larva migrans syndrome: Toxocara, Ascaris, or both? Lancet 340(8818):550–551

    Article  PubMed  Google Scholar 

  • Yentur Doni N, Gurses G, Simsek Z, Yildiz Zeyrek F (2015) Prevalence and associated risk factors of intestinal parasites among children of farm workers in the southeastern Anatolian region of Turkey. Ann Agric Environ Med 22(3):438–442. doi:10.5604/12321966.1167709

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Fiona van der Klis and to the PIENTER study team for their efforts in data collection

Author information

Author notes

    Authors and Affiliations

    1. National Institute for Public Health and the Environment (RIVM), Centre for Infectious Disease Control (CIb), PO Box 1-3720, BA, Bilthoven, Netherlands

      Lapo Mughini-Gras, Margriet Harms, Wilfrid van Pelt, Elena Pinelli & Titia Kortbeek

    2. Department of Infectious Diseases and Immunology, Utrecht University, Utrecht, Netherlands

      Lapo Mughini-Gras

    Authors
    1. Lapo Mughini-Gras
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Margriet Harms
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Wilfrid van Pelt
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Elena Pinelli
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Titia Kortbeek
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Lapo Mughini-Gras.

    Ethics declarations

    All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. PIENTER-1 was approved by the Medical Ethical Committee of the Netherlands’ Organisation for Applied Scientific Research (TNO) in Leiden. PIENTER-2 has received ethical approval by the Medical Ethics Testing Committee of the Foundation of Therapeutic Evaluation of Medicines (METC-STEG) in Almere (ISRCTN 20164309). All participants and parents/legal caretakers of minors involved in both studies provided written informed consent. No person identifying information was generated in this study.

    Conflicts of interest

    All authors have no conflicts of interest to declare.

    Funding

    This study was supported by the Netherlands’ Ministry of Health, Welfare and Sport. The funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.

    Additional information

    Lapo Mughini-Gras and Margriet Harms contributed equally to this work.

    Appendix

    Appendix

    Table 5 Variables tested for association with Toxocara and Ascaris IgG antibodies in the first nationwide serosurvey (PIENTER-1) in the Netherlands, 1995/1996
    Full size table
    Table 6 Variables tested for association with Toxocara and Ascaris IgG antibodies in the second nationwide serosurvey (PIENTER-2) in the Netherlands, 2006/2007
    Full size table

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Mughini-Gras, L., Harms, M., van Pelt, W. et al. Seroepidemiology of human Toxocara and Ascaris infections in the Netherlands. Parasitol Res 115, 3779–3794 (2016). https://doi.org/10.1007/s00436-016-5139-6

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00436-016-5139-6

    Keywords

    Search

    Navigation