Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 22, Number 8—August 2016
Letter

Rare Human Infection with Pacific Broad Tapeworm Adenocephalus pacificus, Australia

Cite This Article

To the Editor: Human diphyllobothriosis associated with the Pacific broad tapeworm Adenocephalus pacificus (syn. Diphyllobothrium pacificum) is a reemerging, global parasitic disease (1). Infection with the adult tapeworm occurs widely in piscivorous mammals, including humans, with various species of marine fish acting as intermediate hosts (1,2). In the Southern Hemisphere, the organism is well described in the coastal waters of South America, southern Africa, and Oceania (2). A. pacificus tapeworms have been recorded in pinnipeds in Australian territory as far back as 1923 (3). To our knowledge, no human case has been reported from this region to date.

A 3-year-old boy from a coastal town in South Australia’s Eyre Peninsula was brought to a medical clinic on July 29, 2015, with a 1-month history of poor appetite and loose bowel movements. His parents had noticed tapeworm-like organisms in his feces over a period of 2 days; the organisms had been discarded and were not available for examination. The child regularly ate raw marine fish, caught by his father in the Spencer Gulf during recreational fishing. The types of fish he consumed included southern bluefin tuna (Thunnus maccoyii), spotted sillago (Sillaginodes punctatus), and southern goatfish (Upeneichthys vlamingii). The child had never traveled outside Australia. Fecal and blood samples were collected for further analysis at SA Pathology (Adelaide, South Australia, Australia).

Macroscopic examination of a single, 6-cm portion of unfixed strobila without scolex, obtained from feces, revealed individual proglottids, wider than they were long, and a central rosette-shaped uterus in each proglottid. Further morphologic features could not be clearly visualized from the available clinical specimen. Microscopic examination of fecal sediment revealed unembryonated ellipsoidal eggs with an operculum and abopercular knob at opposite ends (2). The patient had been given a preliminary clinical diagnosis of diphyllobothriosis and received oral praziquantel (10 mg/kg) on 2 occasions, 12 days apart, without any complications. Blood test results, including hemoglobin level, erythrocyte volume, and vitamin B12 levels, were all within reference ranges. A follow-up stool sample collected 1 week after the first dose of praziquantel still exhibited operculated eggs; samples collected 3 weeks later did not contain any eggs.

We identified the tapeworm more specifically through molecular methods. Genomic DNA from segments preserved in 80% ethanol were extracted using a DNeasy Blood and Tissue Kit (QIAGEN, Valencia, CA, USA) following the manufacturer’s protocol. Four loci were PCR-amplified separately from the genomic DNA as described (46). The first locus (designated cox1) targeted the complete cytochrome c oxidase subunit 1 gene; the second locus (designated Dpcox1), located within the cox1 gene, was amplified by using species-specific (D. pacificum) primers (4); the third locus (designated SSU) targeted the small subunit gene of RNA; and the fourth locus (designated ITS) targeted the first to second internal transcribed spacer regions. For each locus, automated DNA sequencing (BigDye Terminator v3.1 Kit; Applied Biosystems, Foster City, CA, USA) was performed by using the primers for PCR amplification (46) in separate reactions. We identified cox1 and Dpcox1 sequences by local alignment comparison (6 reading frames) using amino acid sequences conceptually translated online (http://www.ebi.ac.uk/Tools/st/emboss_transeq/) from respective genes of the reference sequences of Diphyllobothrium spp. available from GenBank. DNA sequencing results identified the tapeworm as A. pacificus.

Sequence data from this study have been submitted to GenBank (accession nos. KU519704–6). Morphologic voucher material is archived in the Australian Helmintological Collection, South Australian Museum (accession nos. AHC47709 and AHC36233).

Data obtained from cox1 gene analysis (Figure, panel A) suggest that this isolate is indistinguishable from an A. pacificus tapeworm previously obtained from an Australian sea lion, Neophoca cinerea (GenBank accession no. KR269744), from Kangaroo Island and an Australian fur seal, Arctocephalus pusillus (GenBank accession no. KR269745), from Cape Woolamai in 1993 (2). Similarly, the human isolate we identified is indistinguishable from isolates previously obtained from fish and humans in Chile, Peru, and Spain (Figure, panel A). However, the human isolates from Spain (GenBank accession nos. HF969327 and KM520151) have been linked with fresh fish imported from South America (7,8). Small subunit and internal transcribed spacer sequence analysis showed that the human isolate was identical or closely related to isolates from Peru (Figure, panels B, C). This finding is in keeping with this species’ current predominant geographic distribution (2).

Two recent food risk assessments in Australia did not recognize A. pacificus tapeworms as a potential zoonotic threat in marine finfish (9,10). Although our patient only consumed raw locally caught marine fish, thus acquiring a patent infection after accidental ingestion of plerocercoids, the fish species concerned have yet to be confirmed as suitable intermediate hosts of A. pacificus tapeworms (1). These findings, and reports spanning >90 years, suggest that A. pacificus tapeworms are endemic in piscivorous mammals off the Australian coast, and more human cases can be expected as pressure on marine fish stocks and consumption of uncooked fish increase. As a protective measure against this emerging foodborne zoonotic threat, the public should be made aware of risks associated with consumption of fresh, raw marine fish.

Top

Acknowledgment

We thank Amanda Rogers from SA Pathology for her contribution.

Top

Casey V. Moore, R.C. Andrew Thompson, Abdul Jabbar, John V. Williams, Kavita Rasiah, Louise Pallant, Ann P. Koehler, Caitlin Graham, and Gerhard F. WeldhagenComments to Author 
Author affiliations: SA Pathology, Adelaide, South Australia, Australia (C.V. Moore, G.F. Weldhagen); Murdoch University, Murdoch, Western Australia, Australia (R.C.A. Thompson, L. Pallant); University of Melbourne, Melbourne, Victoria, Australia (A. Jabbar); Investigator Clinic, Port Lincoln, South Australia (J. Williams); Women’s and Children’s Hospital, Adelaide (K. Rasiah); SA Health Communicable Disease Control Branch, Adelaide (A.P. Koehler, C. Graham)

Top

References

  1. Kuchta  R, Serrano-Martínez  ME, Scholz  T. Pacific broad tapeworm Adenocephalus pacificus as a causative agent of globally reemerging diphyllobothriosis. Emerg Infect Dis. 2015;21:1697703. DOIPubMedGoogle Scholar
  2. Hernández-Orts  JS, Scholz  T, Brabec  J, Kuzmina  T, Kuchta  R. High morphological plasticity and global geographical distribution of the Pacific broad tapeworm Adenocephalus pacificus (syn. Diphyllobothrium pacificum): molecular and morphological survey. Acta Trop. 2015;149:16878. DOIPubMedGoogle Scholar
  3. Johnston  TH. Entozoa from the Australian hair seal. Proc Linn Soc N S W. 1937. [cited 2016 Jan 20]. http://www.biodiversitylibrary.org/page/34903721#page/59/mode/1up
  4. Wicht  B, Yanagida  T, Scholz  T, Ito  A, Jiménez  JA, Brabec  J. Multiplex PCR for differential identification of broad tapeworms (Cestoda: Diphyllobothrium) infecting humans. J Clin Microbiol. 2010;48:31116. DOIPubMedGoogle Scholar
  5. Mariaux  J. A molecular phylogeny of the Eucestoda. J Parasitol. 1998;84:11424. DOIPubMedGoogle Scholar
  6. Luton  K, Walker  D, Blair  D. Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Mol Biochem Parasitol. 1992;56:3237. DOIPubMedGoogle Scholar
  7. Pastor-Valle  J, González  LM, Martín-Clemente  JP, Merino  FJ, Gottstein  B, Gárate  T. Molecular diagnosis of diphyllobothriasis in Spain, most presumably acquired via imported fish, or sojourn abroad. New Microbes New Infect. 2014;2:16. DOIPubMedGoogle Scholar
  8. Kuchta  R, Esteban  JG, Brabec  J, Scholz  T. Misidentification of Diphyllobothrium species related to global fish trade, Europe. Emerg Infect Dis. 2014;20:19557. DOIPubMedGoogle Scholar
  9. Anantanawat  S, Kiermeier  A, McLeod  C, Sumner  J. South Australian Research and Development Institute. A semi-quantitative risk assessment of harmful parasites in Australian finfish. April 2012 [cited 2016 Jan 20]. http://safefish.com.au/wp-content/uploads/2013/03/Semi-quantitative-risk-assessment-of-Harmful-Parasites.pdf
  10. New South Wales Food Authority. Seafood safety scheme—periodic review of the risk assessment. 2012. [cited 2016 Jan 20]. http://foodauthority.nsw.gov.au/_Documents/scienceandtechnical/seafood_safety_scheme.pdf

Top

Figure

Top

Cite This Article

DOI: 10.3201/eid2208.160156

Related Links

Top

Table of Contents – Volume 22, Number 8—August 2016

EID Search Options
presentation_01 Advanced Article Search – Search articles by author and/or keyword.
presentation_01 Articles by Country Search – Search articles by the topic country.
presentation_01 Article Type Search – Search articles by article type and issue.

Top

Comments

Please use the form below to submit correspondence to the authors or contact them at the following address:

Gerhard F. Weldhagen, Microbiology and Infectious Diseases Laboratory, SA Pathology, PO Box 14, Rundle Mall, Adelaide, SA5000, Australia

Send To

10000 character(s) remaining.

Top

Page created: July 15, 2016
Page updated: July 15, 2016
Page reviewed: July 15, 2016
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external