Emergence of the Zoonotic Biliary Trematode Pseudamphistomum truncatum in Grey Seals (Halichoerus grypus) in the Baltic Sea

PLoS One. 2016 Oct 18;11(10):e0164782. doi: 10.1371/journal.pone.0164782. eCollection 2016.

Abstract

The biliary trematode Pseudamphistomum truncatum parasitizes a wide range of fish-eating mammals, including humans. Here we report the emergence of this parasite in grey seals (Halichoerus grypus) in the Baltic Sea. One hundred eighty-three of 1 554 grey seals (11.9%) examined from 2002-2013 had detectable hepatobiliary trematode infection. Parasite identification was confirmed as P. truncatum by sequencing the ITS2 region of a pool of five to 10 trematodes from each of ten seals collected off the coast of seven different Swedish counties. The proportion of seals parasitized by P. truncatum increased significantly over time and with increasing age of seals. Males were 3.1 times more likely to be parasitized than females and animals killed in fishery interactions were less likely to be parasitized than animals found dead or hunted. There was no significant difference in parasitism of seals examined from the Gulf of Bothnia versus those examined from the Baltic Proper. Although the majority of infections were mild, P. truncatum can cause severe hepatobiliary disease and resulted in liver failure in at least one seal. Because cyprinid fish are the second intermediate host for opisthorchiid trematodes, diets of grey seals from the Baltic Sea were analysed regarding presence of cyprinids. The proportion of gastrointestinal tracts containing cyprinid remains was ten times higher in seals examined from 2008 to 2013 (12.2%) than those examined from 2002 to 2007 (1.2%) and coincided with a general increase of trematode parasitism in the host population. The emergence and relatively common occurrence of P. truncatum in grey seals signals the presence of this parasite in the Baltic Sea ecosystem and demonstrates how aquatic mammals can serve as excellent sentinels of marine ecosystem change. Investigation of drivers behind P. truncatum emergence and infection risk for other mammals, including humans, is highly warranted.

MeSH terms

  • Animals
  • Baltic States / epidemiology
  • Bile Ducts / parasitology
  • Bile Ducts / pathology
  • Biliary Tract Diseases / epidemiology
  • Biliary Tract Diseases / parasitology
  • Biliary Tract Diseases / pathology
  • Biliary Tract Diseases / veterinary
  • Diet
  • Ecosystem
  • Female
  • Genotype
  • Liver / pathology
  • Male
  • Oceans and Seas
  • Polymerase Chain Reaction
  • Prevalence
  • RNA, Protozoan / isolation & purification
  • RNA, Protozoan / metabolism
  • RNA, Ribosomal / isolation & purification
  • RNA, Ribosomal / metabolism
  • Seals, Earless / parasitology*
  • Sequence Analysis, DNA
  • Trematoda / genetics
  • Trematoda / isolation & purification
  • Trematoda / physiology*
  • Trematode Infections / epidemiology
  • Trematode Infections / parasitology
  • Trematode Infections / pathology
  • Trematode Infections / veterinary

Substances

  • RNA, Protozoan
  • RNA, Ribosomal

Grants and funding

Funding support was provided by the Swedish Environmental Protection Agency (http://www.swedishepa.se/) and from the INTERREG project ECOSEAL (www.ecosealproject.eu). The Swedish Agency for Marine and Water Management (https://www.havochvatten.se/en/) provided funding support for the diet study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.