• View in gallery

    Neighbor-joining tree on 858 bp fragment of 18S rRNA gene. Kimura-2 parameters; bootstrap values for 500 replicates shown on nodes.

  • View in gallery

    Neighbor-joining tree on 393 bp fragment of COI gene. Kimura-2 parameters; bootstrap values for 500 replicates shown on nodes.

  • 1

    Muller R, 2002. Worms and Human Disease. Second Edition. Wallingford, PA: CABI Publishing.

  • 2

    Chai J-Y, Murrell KD, Lymbery AJ, 2005. Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35 :1233–1254.

  • 3

    Rausch RL, Hilliard DK, 1970. Studies on the helminth fauna of Alaska. XLIX. The occurrence of Diphyllobothrium latum (Linnaeus, 1758) (Cestoda: Diphyllobothriidae) in Alaska, with notes on other species. Can J Zool 48 :1201–1219.

    • Search Google Scholar
    • Export Citation
  • 4

    Andersen K, Ching HL, Vik R, 1987. A review of freshwater species of Diphyllobothrium with redescriptions and the distribution of D. dendriticum (Nitzsch, 1824) and D. ditremum (Creplin, 1825) from North America. Can J Zool 65 :2216–2228.

    • Search Google Scholar
    • Export Citation
  • 5

    Margolis L, Rausch RL, Robertson E, 1973. Diphyllobothrium ursi from man in British Columbia—first report of this tapeworm in Canada. Can J Publ Hlth 64 :588–589.

    • Search Google Scholar
    • Export Citation
  • 6

    Yamane Y, Kamo H, Bylund G, Wikgren Bo-J, 1986. Diphyllobothrium nihonkaiense sp. nov. (Cestoda: Diphyllobothriidae)—revised identification of Japanese broad tapeworm. Shimane J Med Sci 10 :29–48.

    • Search Google Scholar
    • Export Citation
  • 7

    Jeon H, Kim K-H, Park J-K, Eom KS, Chai JY, 2003. Dominance of Diphyllobothrium nihonkaiense (family Diphyllobothriidae) inferred from the nucleotide sequences of ribosomal ITS1 and mtCox1 in Korea. The 45th Annual Meeting of the Korean Society for Parasitology.

  • 8

    Yoshida M, Hasegawa H, Takaoka H, Miyata A, 1999. A case of Diphyllobothrium nihonkaiense infection successfully treated by oral administration of Gastrografin. Parasitol Int 48 :151–155.

    • Search Google Scholar
    • Export Citation
  • 9

    Ando K, Ishikura K, Nakakugi T, Shimono Y, Tamai T, Sugawa M, Limviroj W, Chinzei Y, 2001. Five cases of Diphyllobothrium nihonkaiense infection with discovery of plerocercoids from an infective source, Oncorhynchus masou ishikawae. J Parasitol 87 :96–100.

    • Search Google Scholar
    • Export Citation
  • 10

    Hoffman GL, 1999. Parasites of North American Freshwater Fishes. Second Edition. Ithaca & London: Cornell University Press.

  • 11

    Froese R, Pauly D (eds.), 2007. FishBase. World Wide Web electronic publication, accessed August 2007. http://www.fishbase.org.

  • 12

    Mariaux J, 1998. A molecular phylogeny of the Cestoda. J Parasitol 84 :114–124.

  • 13

    Bowles J, Blair D, McManus DP, 1992. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54 :165–173.

    • Search Google Scholar
    • Export Citation
  • 14

    Kumar S, Tamura K, Nei M, 2004. MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5 :150–163.

    • Search Google Scholar
    • Export Citation
  • 15

    Wicht B, de Marval F, Peduzzi R, 2007. Diphyllobothrium nihonkaiense (Yamane et al., 1986) in Switzerland: first molecular evidence and case reports. Parasitol Int 56 :195–199.

    • Search Google Scholar
    • Export Citation
  • 16

    Miyadera H, Kokaze A, Kuramochi T, Kita K, Machinami R, Noyae O, Alarcon de Noyae B, Okamoto M, Kojima S, 2001. Phylogenetic identification of Sparganum proliferum as a pseudophyllidean cestode by the sequence analyses on mitochondrial COI and nuclear sdhB genes. Parasitol Int 50 :93–104.

    • Search Google Scholar
    • Export Citation
  • 17

    Yera H, Estran C, Delaunay P, Gari-Toussaint M, Dupouy-Camet J, Marty P, 2006. Putative Diphyllobothrium nihonkaiense acquired from a Pacific salmon (Oncorhynchus keta) eaten in France; genomic identification and case report. Parasitol Int 55 :45–49.

    • Search Google Scholar
    • Export Citation
  • 18

    Škeříková A, Brabec J, Kuchta R, Jiménez JA, García HH, Scholz T, 2006. Is the human-infecting Diphyllobothrium pacificum a valid species or just a South American population of the Holarctic fish broad tapeworm, D. latum? Am J Trop Med Hyg 75 :307–310.

    • Search Google Scholar
    • Export Citation
  • 19

    Baer JG, 1969. Diphyllobothrium pacificum, a tapeworm from sea lions endemic in man along the coastal area of Peru. J Fish Res Board Can 26 :717–723.

    • Search Google Scholar
    • Export Citation
  • 20

    Tsuboi T, Torii M, Hirai K, 1993. Light and scanning electron microscopy of Diphyllobothrium pacificum expelled from a man. Jap J Parasitol 42 :422–428.

    • Search Google Scholar
    • Export Citation
  • 21

    Andersen K, Halvorsen O, 1978. Egg size and form as taxonomic criteria in Diphyllobothrium. Parasitology 76 :229–240.

  • 22

    Delyamure SL, Skryabin AS, Serdiukov AM, 1985. Diphyllobothriata—Flatworms of Man, Mammals and Birds. Principles of Cestodology. Volume IX. Moscow, Russia: Nauka. [In Russian.]

  • 23

    Kamo H, Maejima J, Yazaki S, 1982. Occurrence of human infection with Diphyllobothrium pacificum (Nybelin, 1931) Margolis, 1956 in Japan. Jap J Parasitol 31 :165–170.

    • Search Google Scholar
    • Export Citation
  • 24

    Dupouy-Camet J, Peduzzi R, 2004. Current situation of human diphyllobothriasis in Europe. Eurosurveillance 9 :31–34.

  • 25

    Torres P, Cuevas C, Tang M, Barra M, Franjola R, Navarrete N, Montefusco A, Otth L, Wilson G, Puga S, Figueroa L, Cerda O, 2004. Introduced and native fishes as infection foci of Diphyllobothrium spp. in humans and dogs from two localities at Lake Panguipulli in Southern Chile. Comp Parasitol 71 :111–117.

    • Search Google Scholar
    • Export Citation
  • 26

    Santos FLN, de Faro LB, 2005. The first confirmed case of Diphyllobothrium latum in Brazil. Mem Inst Oswaldo Cruz 100 :585–586.

  • 27

    Wicht B, de Marval F, Gottstein B, Peduzzi R, 2007. Imported diphyllobothriasis in Switzerland: molecular evidence of Diphyllobothrium dendriticum (Nitsch, 1824). Parasitol Res 102 :201–204.

    • Search Google Scholar
    • Export Citation
  • 28

    Kim K-H, Jeon H-K, Kang S, Sultana T, Eom KS, Park JK, 2007. Characterization of the complete mitochondrial genome of Diphyllobothrium nihonkaiense (Diphyllobothriidae: Cestoda), and development of molecular markers for differentiating fish tapeworms. Mol Cells 23 :379–390.

    • Search Google Scholar
    • Export Citation

 

 

 

 

First Record of Human Infection with the Tapeworm Diphyllobothrium nihonkaiense in North America

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  • 1 Istituto Cantonale di Microbiologia, Bellinzona, Switzerland; Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, and Faculty of Science, University of South Bohemia, České Bude jovice, Czech Republic

The tapeworm Diphyllobothrium nihonkaiense (Cestoda: Diphyllobothriidea), originally described from Japan, is reported from a man in North America for the first time. Species identification was based on sequences of ribosomal (partial 18S rRNA) and mitochondrial (partial Cytochrome c Oxidase subunit I) genes of proglottids expelled from a Czech tourist who ate raw Pacific sockeye salmon (Oncorhynchus nerka) from British Columbia, Canada.

INTRODUCTION

Tapeworms of the genus Diphyllobothrium Cobbold, 1858 (Cestoda: Diphyllobothriidea) infect a wide spectrum of homeothermic hosts, including humans. The total number of current human cases is estimated to reach 20 million worldwide.1,2 The tapeworm Diphyllobothrium latum (Linnaeus, 1758) has circumboreal distribution (northern part of North America, Europe, and Russia, including Siberia). The geographic range of D. latum is not well known for North America because for many years whenever eggs of Diphyllobothrium spp. were observed in fecal smears from Canada and the United States, the identification was made invariably as “D. latum”. That species definitely occurs in Alaska,3 but old reports of D. latum from the United States and Canada are not reliable because detailed studies were not made. Indeed, other species of Diphyllobothrium have also been reported from man in Canada and the United States, although much more rarely, namely Diphyllobothrium dendriticum (Nitzsch, 1824), Diphyllobothrium lanceolatum (Krabbe, 1865), Diphyllobothrium ursi (Rausch, 1954), and Diphyllobothrium dalliae (Rausch, 1956).35

Another species, Diphyllobothrium nihonkaiense Yamane, Kamo, Bylund et Wikgren, 1986, is a relatively common fish-borne parasite of humans in Japan and Korea.2,6,7 Pacific salmons (Oncorhynchus spp.), especially chum and sockeye salmon [Oncorhynchus keta (Walbaum, 1792) and O. nerka (Walbaum, 1792)], serve as its second intermediate hosts.2,8,9 However, neither adults of D. nihonkaiense nor its plerocercoids have been found in Canada or the United States,2,10 even though 5 species of Pacific salmons that probably harbor plerocercoids occur along the Pacific coast of North America.11

In this article, we report the first autochthonous infection of man with D. nihonkaiense in Canada, based on finding adult tapeworms in a Czech tourist who ate undercooked Pacific salmon provided by local inhabitants. Species identification was based on molecular data, namely partial sequences of the 18S ribosomal RNA and Cytochrome c Oxidase subunit I (COI) genes.

MATERIALS AND METHODS

Case report.

A Czech tourist, who traveled around Canada in summer/autumn 2005 for 2 weeks, intentionally ate only Pacific salmons (several kilograms of salmons of 5 species). The infection with Diphyllobothrium was most probably acquired from sockeye salmon (Oncorhynchus nerka) bought on 5 September 2005 from local inhabitants at the Fraser River near Stoner settlement, situated about 500 km from the Fraser River mouth in Vancouver. These salmons weighted about 2–3 kg and several fish were marinated by the tourist’s guide, according to the Swedish recipe with dill; these fish were actually raw. Several other sockeye salmons, bought from other local inhabitants at the end of the stay, were eaten after long-term drying over smoke (‘yerka’ style).

The tourist returned from Canada to the Czech Republic on 18 September 2005. He suffered from digestion problems, distress (perturbation) in the stomach, and a creepy feeling in legs during subsequent days. He attributed these problems to jet lag. On 29 September 2005, he observed released proglottids in his feces and visited a physician. Two days later, anthelminthic treatment (praziquantel) was applied and all symptoms disappeared.

Molecular analysis.

Proglottids (TS 05/60) released from the patient were analyzed with molecular methods at the Istituto Cantonale di Microbiologia (ICM), Bellinzona. DNA was extracted from about 10 mg tissue (a half proglottid) conserved in 70% ethanol, following the Tissue Protocol of QIAamp DNA Minikit (Qiagen, Hombrechtikon, Switzerland). It was tested by PCR using Taq PCR Master Mix Kit (Qiagen, Hombrechtikon, Switzerland) in 50 μL reaction volume containing 2.5 units of Taq DNA Polymerase, 1.5 mM magnesium chloride, 200 μM of each dNTP, and 0.3 μM of each specific eucestode primers for the amplification of partial 18S ribosomal RNA and COI genes.12,13 The amplification cycle was performed as follows: 2 min denaturation at 94°C, 35 cycles 30 s at 94°C, 40 s at 45°C, 1 min at 72°C, and 5 min at 72°C final extension. The nucleotide sequences obtained were corrected both manually and with the program EditSeq™ (DNAStar Inc.). Their alignment as well as phylogenetic trees (Neighbor-Joining method; Kimura-2 parameters; bootstrap values for 500 replicates) were made using the program MEGA version 3.0.14 Homologous 18S rRNA and COI gene sequences of D. latum (GenBank accession numbers AM712620, DQ316793, AM712906, and AM712621), D. nihonkaiense (AM412740, AM408316, DQ768160, DQ181943, AB015755, DQ768190, AM412559, and AM412560), D. dendriticum (DQ181945, AM412739, AM412738, and DQ768193), Diphyllobothrium ditremum (DQ181944 and DQ768195), Diphyllobothrium stemmacephalum (AF124459), Diphyllobothrium pacificum (DQ925310 and AM747494), and Diphyllobothrium spp. (AY972072) were available in public database. Schistocephalus solidus (AF124460), Ligula intestinalis (AF153910), and Taenia solium (AF360865) were included as outgroups.

RESULTS

Sequences of ribosomal (partial 18S rRNA) and mitochondrial (partial COI) genes of the sample from Canada were 858 and 393 bp long, respectively. Partial 18S rRNA gene sequence showed 100% identity with all D. nihonkaiense reference sequences (Figure 1). Among these sequences, Gen-Bank accession numbers AM408316 (proglottids) and AM412740 (eggs) were from 2 Swiss patients,15 DQ768160 (proglottids) was from a South Korean patient, and DQ181943 (proglottids) from a French patient. Partial COI gene sequence showed 100% identity with D. nihonkaiense reference sequence AB015755 (proglottids from a Japanese patient16), 99.7% identity with D. nihonkaiense reference sequences DQ768190 (South Korean patient16), AM412559 and AM412560 (proglottids and eggs from Swiss patients15), and 99.5% identity with Diphyllobothrium sp. reference sequence AY972072 (French patient17; Figure 2). Thus, the sample AY972072 identified as Diphyllobothrium sp. by Yera and others17 also probably belongs to the species D. nihonkaiense. Sequences of other species of Diphyllobothrium infecting humans, including D. latum, were markedly different from that of the sample (Figures 1 and 2).

DISCUSSION

The present study reports the first case of human infection with Diphyllobothrium nihonkaiense acquired in North America. This cestode has been considered as a frequent fish-borne human helminth parasite in Japan and Korea.2 Three human cases, apparently imported, have recently been detected using molecular methods in Europe, as a consequence of consumption of raw or undercooked Pacific salmons15,17; a fourth patient has also been found recently infected with D. nihonkaiense in France (J. Dupouy-Camet, personal communication). In each case, salmon were imported most probably from the Pacific coast of North America.

The life cycle of D. nihonkaiense is not known but is most probably completed in marine habitat; marine mammals may serve as natural definitive hosts. Existing data indicate that the cestode is common in people in Japan, Korea, and Russian Far East. It is probable that persons who consume uncooked Pacific salmons of any of 7 species of Oncorhynchus occurring in the northern Pacific, including the Pacific coast of North America, may become infected by the cestode.

Species identification of Diphyllobothrium tapeworms is possible if specimens are relaxed and in good condition, but this is not often the case when clinical material expelled from patients after anthelmintic treatment is only available. The present sample of D. nihonkaiense was misidentified as D. latum in a study of Škeříková and others18 (sample TS 05/60), because the authors obtained only ethanol-fixed material diagnosed by a human parasitologist as D. latum. Indeed, the position of this sample among other isolates of Diphyllobothrium tapeworms inferred from ITS2 sequences indicated possible paraphyly or polyphyly of D. latum (see Figure 1 in Škeříková and others18). That study was nevertheless aimed at confirming the validity of D. pacificum occurring in humans from the Pacific coast of South America and in Japan.19,20

A small piece of 2 incomplete gravid proglottids was available in the present study, but morphologic evaluation did not enable us to provide species identification with certainty. Nevertheless, some morphologic characteristics (data not shown), especially the size of eggs [length 53.2–58.5 μm, width 35.4–40.2 μm in the present material; 55.2 ± 1.3 by 38.2 ± 1.5 μm and 57.3 ± 0.6 × 44.5 ± 0.9 μm in D. nihonkaiense,6,15 whereas almost always longer than 60 μm (length 55–77 μm) and usually wider than 45 μm (width 41–57 μm) in D. latum3,15,21,22], indicated that the tapeworm from the Czech patient belonged to D. nihonkaiense, thus supporting species identification inferred from molecular markers.

Current findings of previously unreported taxa of Diphyllobothrium in South America and Japan as well as reappearance of human diphyllobothriosis in Europe2326 demonstrate that fish-borne helminthoses actually become a public health problem even in developed countries where people eat raw or undercooked fish. Molecular markers based on species-specific sequences of suitable genes represent a powerful tool in routine diagnostics of clinical samples of Diphyllobothrium tapeworms and may help considerably in rapid and correct species identification.15,17,27,28

Figure 1.
Figure 1.

Neighbor-joining tree on 858 bp fragment of 18S rRNA gene. Kimura-2 parameters; bootstrap values for 500 replicates shown on nodes.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 2; 10.4269/ajtmh.2008.78.235

Figure 2.
Figure 2.

Neighbor-joining tree on 393 bp fragment of COI gene. Kimura-2 parameters; bootstrap values for 500 replicates shown on nodes.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 2; 10.4269/ajtmh.2008.78.235

*

Address correspondence to Tomáš Scholz, Institute of Parasitology, Biology Centre of the Czech Academy of Sciences & Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Repulic. E-mail: tscholz@paru.cas.cz

Authors’ addresses: Barbara Wicht and Raffaele Peduzzi, Istituto Cantonale di Microbiologia, Via Mirasole 22a, 6500 Bellinzona, Switzerland, Telephone: +41(0)918146081, Fax: +41(0)918146019, E-mail: barbara.wicht@ti.ch and raffaele.peduzzi@ticino.com. Tomáš Scholz and Roman Kuchta, Institute of Parasitology, Biology Centre of the Czech Academy of Sciences & Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic, Telephone: +420385310351, Fax: +420385310388, E-mails: tscholz@paru.cas.cz and krttek@yahoo.com.

Acknowledgments: The authors thank Luboš Piálek, Faculty of Science, University of South Bohemia, České Budějovice, and Oleg Ditrich for invaluable help, and Martina Borovková, both Institute of Parasitology, BC AS CR, České Budějovice for making histological sections. Helpful suggestions of three anonymous referees are also greatly appreciated.

Financial support: The present study was supported by the Grant Agency of the Czech Republic (projects Nos. 524/04/0342 and 524/03/H133), research projects of the Institute of Parasitology, Biology Centre of the Czech Academy of Sciences (Z60220518 and LC 522), and the research project of the Faculty of Science, University of South Bohemia (MSM 6007665801).

REFERENCES

  • 1

    Muller R, 2002. Worms and Human Disease. Second Edition. Wallingford, PA: CABI Publishing.

  • 2

    Chai J-Y, Murrell KD, Lymbery AJ, 2005. Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35 :1233–1254.

  • 3

    Rausch RL, Hilliard DK, 1970. Studies on the helminth fauna of Alaska. XLIX. The occurrence of Diphyllobothrium latum (Linnaeus, 1758) (Cestoda: Diphyllobothriidae) in Alaska, with notes on other species. Can J Zool 48 :1201–1219.

    • Search Google Scholar
    • Export Citation
  • 4

    Andersen K, Ching HL, Vik R, 1987. A review of freshwater species of Diphyllobothrium with redescriptions and the distribution of D. dendriticum (Nitzsch, 1824) and D. ditremum (Creplin, 1825) from North America. Can J Zool 65 :2216–2228.

    • Search Google Scholar
    • Export Citation
  • 5

    Margolis L, Rausch RL, Robertson E, 1973. Diphyllobothrium ursi from man in British Columbia—first report of this tapeworm in Canada. Can J Publ Hlth 64 :588–589.

    • Search Google Scholar
    • Export Citation
  • 6

    Yamane Y, Kamo H, Bylund G, Wikgren Bo-J, 1986. Diphyllobothrium nihonkaiense sp. nov. (Cestoda: Diphyllobothriidae)—revised identification of Japanese broad tapeworm. Shimane J Med Sci 10 :29–48.

    • Search Google Scholar
    • Export Citation
  • 7

    Jeon H, Kim K-H, Park J-K, Eom KS, Chai JY, 2003. Dominance of Diphyllobothrium nihonkaiense (family Diphyllobothriidae) inferred from the nucleotide sequences of ribosomal ITS1 and mtCox1 in Korea. The 45th Annual Meeting of the Korean Society for Parasitology.

  • 8

    Yoshida M, Hasegawa H, Takaoka H, Miyata A, 1999. A case of Diphyllobothrium nihonkaiense infection successfully treated by oral administration of Gastrografin. Parasitol Int 48 :151–155.

    • Search Google Scholar
    • Export Citation
  • 9

    Ando K, Ishikura K, Nakakugi T, Shimono Y, Tamai T, Sugawa M, Limviroj W, Chinzei Y, 2001. Five cases of Diphyllobothrium nihonkaiense infection with discovery of plerocercoids from an infective source, Oncorhynchus masou ishikawae. J Parasitol 87 :96–100.

    • Search Google Scholar
    • Export Citation
  • 10

    Hoffman GL, 1999. Parasites of North American Freshwater Fishes. Second Edition. Ithaca & London: Cornell University Press.

  • 11

    Froese R, Pauly D (eds.), 2007. FishBase. World Wide Web electronic publication, accessed August 2007. http://www.fishbase.org.

  • 12

    Mariaux J, 1998. A molecular phylogeny of the Cestoda. J Parasitol 84 :114–124.

  • 13

    Bowles J, Blair D, McManus DP, 1992. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54 :165–173.

    • Search Google Scholar
    • Export Citation
  • 14

    Kumar S, Tamura K, Nei M, 2004. MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5 :150–163.

    • Search Google Scholar
    • Export Citation
  • 15

    Wicht B, de Marval F, Peduzzi R, 2007. Diphyllobothrium nihonkaiense (Yamane et al., 1986) in Switzerland: first molecular evidence and case reports. Parasitol Int 56 :195–199.

    • Search Google Scholar
    • Export Citation
  • 16

    Miyadera H, Kokaze A, Kuramochi T, Kita K, Machinami R, Noyae O, Alarcon de Noyae B, Okamoto M, Kojima S, 2001. Phylogenetic identification of Sparganum proliferum as a pseudophyllidean cestode by the sequence analyses on mitochondrial COI and nuclear sdhB genes. Parasitol Int 50 :93–104.

    • Search Google Scholar
    • Export Citation
  • 17

    Yera H, Estran C, Delaunay P, Gari-Toussaint M, Dupouy-Camet J, Marty P, 2006. Putative Diphyllobothrium nihonkaiense acquired from a Pacific salmon (Oncorhynchus keta) eaten in France; genomic identification and case report. Parasitol Int 55 :45–49.

    • Search Google Scholar
    • Export Citation
  • 18

    Škeříková A, Brabec J, Kuchta R, Jiménez JA, García HH, Scholz T, 2006. Is the human-infecting Diphyllobothrium pacificum a valid species or just a South American population of the Holarctic fish broad tapeworm, D. latum? Am J Trop Med Hyg 75 :307–310.

    • Search Google Scholar
    • Export Citation
  • 19

    Baer JG, 1969. Diphyllobothrium pacificum, a tapeworm from sea lions endemic in man along the coastal area of Peru. J Fish Res Board Can 26 :717–723.

    • Search Google Scholar
    • Export Citation
  • 20

    Tsuboi T, Torii M, Hirai K, 1993. Light and scanning electron microscopy of Diphyllobothrium pacificum expelled from a man. Jap J Parasitol 42 :422–428.

    • Search Google Scholar
    • Export Citation
  • 21

    Andersen K, Halvorsen O, 1978. Egg size and form as taxonomic criteria in Diphyllobothrium. Parasitology 76 :229–240.

  • 22

    Delyamure SL, Skryabin AS, Serdiukov AM, 1985. Diphyllobothriata—Flatworms of Man, Mammals and Birds. Principles of Cestodology. Volume IX. Moscow, Russia: Nauka. [In Russian.]

  • 23

    Kamo H, Maejima J, Yazaki S, 1982. Occurrence of human infection with Diphyllobothrium pacificum (Nybelin, 1931) Margolis, 1956 in Japan. Jap J Parasitol 31 :165–170.

    • Search Google Scholar
    • Export Citation
  • 24

    Dupouy-Camet J, Peduzzi R, 2004. Current situation of human diphyllobothriasis in Europe. Eurosurveillance 9 :31–34.

  • 25

    Torres P, Cuevas C, Tang M, Barra M, Franjola R, Navarrete N, Montefusco A, Otth L, Wilson G, Puga S, Figueroa L, Cerda O, 2004. Introduced and native fishes as infection foci of Diphyllobothrium spp. in humans and dogs from two localities at Lake Panguipulli in Southern Chile. Comp Parasitol 71 :111–117.

    • Search Google Scholar
    • Export Citation
  • 26

    Santos FLN, de Faro LB, 2005. The first confirmed case of Diphyllobothrium latum in Brazil. Mem Inst Oswaldo Cruz 100 :585–586.

  • 27

    Wicht B, de Marval F, Gottstein B, Peduzzi R, 2007. Imported diphyllobothriasis in Switzerland: molecular evidence of Diphyllobothrium dendriticum (Nitsch, 1824). Parasitol Res 102 :201–204.

    • Search Google Scholar
    • Export Citation
  • 28

    Kim K-H, Jeon H-K, Kang S, Sultana T, Eom KS, Park JK, 2007. Characterization of the complete mitochondrial genome of Diphyllobothrium nihonkaiense (Diphyllobothriidae: Cestoda), and development of molecular markers for differentiating fish tapeworms. Mol Cells 23 :379–390.

    • Search Google Scholar
    • Export Citation
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