Skip to main content
SpringerLink
Log in

Third-stage nematode larvae of Contracaecum osculatum from Baltic cod (Gadus morhua) elicit eosinophilic granulomatous reactions when penetrating the stomach mucosa of pigs

  • Short Communication
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Third-stage larvae of the anisakid nematode Contracaecum osculatum were recovered from livers of Atlantic cod (Gadus morhua) caught in the Baltic Sea (June 2014) and used for experimental infection of two pigs (one male and one female). Each pig received 215 larvae by oral infection (feeding with minced cod liver containing live nematode larvae). Pigs were euthanized after 5 days, necropsied, and subjected to parasitological investigation. A total of 12 larvae were found penetrating the mucosa of the ventricle (7 in the female pig and 5 in the male pig) eliciting a granulomatous reaction at the penetration site. Four non-attached larvae were found in the female pig stomach and one in the male pig. Petechial bleeding was observed at several locations in the ventricular mucosa where larvae were located. Histological examination of the stomach mucosa revealed a massive cellular infiltration (giant cells, lymphocytes, macrophages, granulocytes, and fibroblast like cells) around the penetrating larva. Mononuclear and polymorphonuclear cells containing eosinophilic granulae were particularly prominent in the granulomas. Reactions correspond to reactions in pigs following experimental infection with the human pathogenic anisakid larvae Anisakis sp. and Pseudoterranova sp. which suggests that C. osculatum might have a zoonotic potential as well.

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

References

  • Audicana MT, Kennedy MW (2008) Anisakis simplex: from obscure infectious worms to inducer of immune hypersensitivity. Clin Microbiol Rev 21:20–25

    Google Scholar 

  • Baird FJ, Gasser RB, Jabar A, Lopata AL (2014) Food borne anisakiasis and allergy. Mol Cell Probe 28:167–174

    Article  CAS  Google Scholar 

  • Bier JW, Jackson GJ, Earl FL, Knollenberg WG (1976) Gross and microscopic pathology with larval Anisakis sp. and Phocanema sp. Nematodes from fish. Trans Am Microsc Soc 95:264–265

    Google Scholar 

  • Buchmann K (2007) An introduction to fish parasitological methods—classical and molecular methods. Biofolia Press, Frederiksberg. Denmark, 130 pp

    Google Scholar 

  • Buchmann K, Kania PW (2012) Emerging Pseudoterranova decipiens (Krabbe, 1878) problems in Baltic cod, Gadus morhua L., associated with grey seal colonization of spawning grounds. J Fish Dis 35:861–866

    Article  CAS  PubMed  Google Scholar 

  • Fagerholm HP (1988) Incubation in rats of a nematodal larva from cod to establish its specific identity: Contracaecum osculatum (Rudolphi). Parasitol Res 75:57–63

    Article  CAS  PubMed  Google Scholar 

  • Haarder S, Kania P, Galatius A, Buchmann K (2014) Increased Contracaecum osculatum infection in Baltic cod (Gadus morhua) livers (1982–2012) associated with increasing grey seal (Halichoerus gryphus) populations. J Wildl Dis 50:537–543

    Article  CAS  PubMed  Google Scholar 

  • Hansen TV, Friis C, Nejsum P, Olsen A, Thamsborg SM (2014) Uptake of benzimidazoles by Trichuris suis in vivo in pigs. Int J Parasitol (Drugs Drug Resist) 4:112–117

    Article  Google Scholar 

  • Køie M, Fagerholm HP (1995) The life-cycle of Contracaecum osculatum (Rudolphi, 1802) sensu stricto (Nematoda, Ascaridoidea, Anisakidae) in view of experimental infections. Parasitol Res 81:481–489

    Article  PubMed  Google Scholar 

  • Margolis L (1977) Public health aspects of “codworm” infection: a review. J Fish Res Board Can 34:887–898

    Article  Google Scholar 

  • Mattiucci S, Fazii P, Rosa AD, Paoletti M, Megna AS, Glielmo A, Angelis MD, Costa A, Meucci C, Calvaruso V, Sorrenti I, Palma G, Bruschi F, Nascetti G (2013) Anisakiasis and gastroallergic reactions associated with Anisakis pegreffii infection, Italy. Emerg Inf Dis 19:496–499

    Article  Google Scholar 

  • Mehrdana F, Bahlool QZM, Skov J, Marana MH, Sindberg D, Mundeling M, Overgaard BC, Korbut R, Strøm SB, Kania PW, Buchmann K (2014) Occurrence of zoonotic nematodes Pseudoterranova decipiens, Contracaecum osculatum and Anisakis simplex in cod (Gadus morhua) from the Baltic Sea. Vet Parasitol 205:581–587

  • Möller H, Anders K (1986) Diseases and parasites of marine fishes. Verlag Möller, Kiel, Germany, p 365

    Google Scholar 

  • Nadolna K, Podolska M (2014) Anisakid larvae in the liver of cod (Gadus morhua L.) from the Southern Baltic Sea. J Helminthol 88:237–246

    Article  CAS  PubMed  Google Scholar 

  • Nagasawa K (2012) The biology of Contracaecum osculatum sensu lato and C. osculatum A (Nematoda: Anisakidae) in Japanese waters: a review. Biosphere Sci 51:61–69

    Google Scholar 

  • Perdiguero-Alonso D, Montero F, Raga A, Kostadinova A (2008) Composition and structure of the parasite faunas of cod, Gadus morhua L. (Teleostei: Gadidae) in the North East Atlantic. Parasitol Vectors 1:1–18

    Article  Google Scholar 

  • Petrushevski GK, Shulman GG (1955) Infection of Baltic cod liver with roundworms. Trudy Akad Nauk Litovskoj SSR Ser B 2:119–125 (In Russian)

    Google Scholar 

  • Pinel C, Beaudevin M, Chermette R, Grillot R, Ambroise-Thomas P (1996) Gastric anisakidosis due to Pseudoterranova decipiens larva. Lancet 347(9018):1829

    Article  CAS  PubMed  Google Scholar 

  • Schaum E, Müller W (1967) Die Heterocheilidiasis. Eine Infektion des Mensches mit Larven von Fisch Ascariden. Dtsch Med Wochenschr 92:2230–2233 (in German)

    Article  CAS  PubMed  Google Scholar 

  • Smith JW, Wootten R (1978) Anisakis and anisakiasis. Adv Parasitol 16:93–163

    Article  CAS  PubMed  Google Scholar 

  • Torres P, Jercic MI, Weitz JC, Dobrew EK, Mercado RA (2007) Human pseudoterranovosis, an emerging infection in Chile. J Parasitol 93(2):440–443

    Article  CAS  PubMed  Google Scholar 

  • Valter ED, Popova TI, Valovaya MA (1982) Scanning electron microscope study of four species of anisakid larvae (Nematoda: Anisakidae). Helminthologia 19:195–209

    Google Scholar 

  • Valtonen ET, Fagerholm HP, Helle E (1988) Contracaecum osculatum (Nematoda: Anisakidae) in fish and seals in Bothnian Bay (norteastern Baltic Sea). Int J Parasitol 18:365–370

    Article  CAS  PubMed  Google Scholar 

  • Zhu X, D’Amelio S, Paggi L, Gasser RB (2000) Assessing sequence variation in the internal transcribed spacers of ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae). Parasitol Res 86:677–683

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The present study was performed under the FP7 project PARASITE (JD312068) supported by the European Commission. The authors are indebted to Professor Maria Vang Johansen for organizing the license 2012-15-2934-00552/LRL of April 22, 2014 from the national committee for experimental animal research, Food Safety Agency, under the Danish Ministry of Food, Agriculture and Fisheries. Laboratory technician Lise-Lotte Christiansen kindly secured pig keeping facilities.

Author information

Authors and Affiliations

  1. Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of Copenhagen, Stigbøjlen 7, 1870, Frederiksberg C, Denmark

    S. B. Strøm, S. Haarder, R. Korbut, H. Mejer, S. M. Thamsborg, P. W. Kania & K. Buchmann

Authors
  1. S. B. Strøm
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Haarder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Korbut
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. Mejer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. M. Thamsborg
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P. W. Kania
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. K. Buchmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to K. Buchmann.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Strøm, S.B., Haarder, S., Korbut, R. et al. Third-stage nematode larvae of Contracaecum osculatum from Baltic cod (Gadus morhua) elicit eosinophilic granulomatous reactions when penetrating the stomach mucosa of pigs. Parasitol Res 114, 1217–1220 (2015). https://doi.org/10.1007/s00436-014-4306-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4306-x

Keywords

Search

Navigation