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Hysterothylacium amoyense in Platycephalous indicus: a Persian Gulf fish and its experimental infection of mouse model

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Abstract

Anisakids belong to a genus of parasitic nematodes with a life cycle involving fish and marine mammals. They cause anisakidosis (anisakiasis) by accidental ingestion of larval stage (Anisakis and other Anisakids), causing both gastrointestinal and allergic reaction in human. The aim of the current study was to report the finding of Hysterothylacium amoyense in Platycephalous indicus fishes and also its probable pathologic effect on a mouse model. In this regard, a total of 27 live third stage larvae ranging from 1.5 to 3 mm in length were collected from gut submucosa of the fish Platycephalous indicus [ZAMIN KAN] and washed up by saline 6 %, and two were characterized as Hysterothylacium amoyense by morphologic and molecular techniques. A total of 25 larvae were orally fed to 5 inbred mice (each 5). A total of 5 mice were also selected as control group; they did not receive the larvae. After 2 weeks, all mice were necropsied using ethical protocol of SUMS. Their specimens, both gross and histologic, were observed and described. Tumor-like nodules were observed in 3 out of 5 infected mice group which could be misdiagnosed as cancer. Microscopic examinations showed lymphocytic infiltration. No pathologic changes were found in the control group. The results showed an invasive anisakid, Hysterthylacium amoyense, with histopathologic features observed in the mammal model (mouse). The parasite has been found in benthic fish Platycephalous indicus in the Persian Gulf, Bushehr region, southern Iran. The parasite could be regarded as a possible source of anisakidosis in coastal populations and should be regarded as a public health problem.

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References

  • Audicana MT, Kennedy MW (2008) Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clin Microbiol Rev 21:360–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonne C, Sandground J (1939) On the production of gastric tumors, bordering on malignancy, in Javanese monkeys through the agency of Nochtia nochti, a parasitic nematode. The American Journal of Cancer 37:173–185

    Google Scholar 

  • Cho S-W, Lee HN (2006) Immune reactions and allergy in experimental anisakiasis. The Korean journal of parasitology 44:271–283

    Article  PubMed  PubMed Central  Google Scholar 

  • Chung J, Kuo H, Lin T, Ho C, Lee J, Lai J, Levy G, Weber W (1996) Evidence for arylamine N-acetyltransferase in the nematode Anisakis simplex. Cancer Lett 106:1–8

    Article  CAS  PubMed  Google Scholar 

  • Fagerholm, H.-P. (1982) Parasites of fish in Finland. VI. Nematodes, Vol 40

  • Fagerholm HP (1991) Systematic implications of male caudal morphology in ascaridoid nematode parasites. Syst Parasitol 19:215–229

    Article  Google Scholar 

  • Fang W, Xu S, Zhang S, Wang Y, Chen X, Luo D (2010) Multiple primer PCR for the identification of anisakid nematodes from Taiwan Strait. Exp Parasitol 124:197–201

    Article  CAS  PubMed  Google Scholar 

  • FAO/WHO, R.O.A.J (2012) Multicriteria-based ranking for risk management of food-borne parasites. microbiologicalriskas,sessmentseries 23:64

    Google Scholar 

  • Farjallah S, Merella P, Ingrosso S et al (2008) Molecular evidence for the occurrence of Contracaecum rudolphii A (Nematoda: Anisakidae) in shag Phalacrocorax aristotelis (Linnaeus) (Aves: Phalacrocoracidae) from Sardinia (western Mediterranean Sea). Parasitol Int 57(4):437–440

  • Gopar-Merino L, Osorio-Sarabia D, García-Prieto L (2005) A new species of Hysterothylacium (Nematoda: Anisakidae) parasite of Ariopsis guatemalensis (Osteichthyes: Ariidae) from Tres Palos lagoon, Mexico. J Parasitol 91:909–914

    Article  PubMed  Google Scholar 

  • Hochberg NS, Hamer DH, Hughes JM, Wilson ME (2010) Anisakidosis: perils of the deep. Clin Infect Dis 51:806–812

    Article  PubMed  Google Scholar 

  • Ishikura H (1969) Occurrence of anisakiasis and its clinical presentation. Saishin Igaku 24:357–365

    Google Scholar 

  • Ishikura, H., Kikuchi, K., Nagasawa, K., Ooiwa, T., Takamiya, H., Sato, N., and Sugane, K. (1993) Anisakidae and anisakidosis. In Progress in clinical parasitology (Springer), pp. 43–102

  • Ito Y, Ikematsu Y, Yuzawa H, Nishiwaki Y, Kida H, Waki S, Uchimura M, Ozawa T, Iwaoka T, Kanematsu T (2007) Chronic gastric anisakiasis presenting as pneumoperitoneum. Asian Journal of Surgery 30:67–71

    Article  PubMed  Google Scholar 

  • Iwasaki K, Torisu M (1982) Anisakis and eosinophil: II. Eosinophilic phlegmon experimentally induced in normal rabbits by parasite-derived eosinophil chemotactic factor (ECF-P). Clin Immunol Immunopathol 23:593–605

    Article  CAS  PubMed  Google Scholar 

  • Jones RE, Deardorff TL (1990) Anisakis simplex: histopathological changes in experimentally infected CBA/J mice. Exp Parasitol 70:305–313

    Article  CAS  PubMed  Google Scholar 

  • Kassai T, Del Campillo MC, Euzeby J, Gaafar S, Hiepe T, Himonas C (1988) Standardized nomenclature of animal parasitic diseases (snoapad). Vet Parasitol 29:299–326

    Article  CAS  PubMed  Google Scholar 

  • Knoff M, Felizardo NN, Iñiguez AM, Maldonado A Jr, Torres EJ, Pinto RM, Gomes DC (2012) Genetic and morphological characterisation of a new species of the genus Hysterothylacium (Nematoda) from Paralichthys isosceles Jordan, 1890 (Pisces: Teleostei) of the Neotropical Region, state of Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz 107(2):186–193

    Article  CAS  PubMed  Google Scholar 

  • Kong Q, Fan L, Zhang J, Akao N, Dong K, Lou D, Ding J, Tong Q, Zheng B, Chen R (2015) Molecular identification of Anisakis and Hysterothylacium larvae in marine fishes from the East China Sea and the Pacific coast of central Japan. Int J Food Microbiol 199:1–7

    Article  CAS  PubMed  Google Scholar 

  • Kuhn T, García-Màrquez J, Klimpel S (2011) Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. PLoS ONE 6(12), e28642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li L, Xu Z, Zhang L (2008) Redescription of three species of Hysterothylacium (Nematoda: Anisakidae) from marine fishes from the Yellow Sea, China, with the synonymy of Hysterothylacium muraenesoxin (Luo, 1999). Zootaxa 1878:55–67

    Google Scholar 

  • Moravec F, Nagasawa K, Ogawa K (1998) Observations on five species of philometrid nematodes from marine fishes in Japan. Syst Parasitol 40:67–80

    Article  Google Scholar 

  • Motta, M.R.A., Pinheiro, D.C.S.N., Carvalho, V.L., Viana, D.D.A., Vicente, A.C.P., and Iñiguez, A.M. (2008) Gastric lesions associated with the presence of Anisakis spp. Dujardin, 1845 (Nematoda: Anisakidae) in Cetaceans stranded on the coast of Ceara, Brazil. Biota Neotropica 8, 0–0

  • Muller R (2002) Worms and human disease. A manual of medical helminthology. doi:10.1079/9780851995168.0000

    Google Scholar 

  • Nadler SA, Hudspeth DS (1998) Ribosomal DNA and phylogeny of the Ascaridoidea (Nemata: Secernentea): implications for morphological evolution and classification. Mol Phylogenet Evol 10(2):221–236

    Article  CAS  PubMed  Google Scholar 

  • Ohtaki, H., and Ohtaki, R. (1989) Clinical manifestation of gastric anisakiasis. In Gastric anisakiasis in Japan (Springer), pp. 37–46

  • Overstreet, R.M., and Meyer, G.W. (1981) Hemorrhagic lesions in stomach of rhesus monkey caused by a piscine ascaridoid nematode. The Journal of parasitology, 226–235

  • Pontes T, D’Amelio S, Costa G et al (2005) Molecular characterization of larval anisakid nematodes from marine fishes of Madeira by a PCR-based approach, with evidence for a new species. J Parasitol 91(6):1430–1434

  • Quiazon K, Yoshinaga T, Santos M et al (2009) Identification of larval Anisakis spp. (Nematoda: Anisakidae) in Alaska pollock (Theragra chalcogramma) in northern Japan using morphological and molecular markers. J Parasitol 95(5):1227–1232

    Article  CAS  PubMed  Google Scholar 

  • Raybourne R, Deardorff TL, Bier JW (1986) Anisakis simplex: larval excretory secretory protein production and cytostatic action in mammalian cell cultures. Exp Parasitol 62:92–97

    Article  CAS  PubMed  Google Scholar 

  • Romero M, Valero A, Navarro-Moll MC, Martín-Sánchez J (2013) Experimental comparison of pathogenic potential of two sibling species Anisakis simplex ss and Anisakis pegreffii in Wistar rat. Tropical Med Int Health 18:979–984

    Article  Google Scholar 

  • Sadjjadi SM, Oryan A, Jalai AR, Mehrabani D (2001) Prevalence and intensity of infestation with Toxocara cati in stray cats in Shiraz, Iran. Veterinarski Arhiv 71:149–157

    Google Scholar 

  • Skovgaard A, Bahlool QZ, Munk P, Berge T, Buchmann K (2011) Infection of North Sea cod, Gadus morhua L., larvae with the parasitic nematode Hysterothylacium aduncum Rudolphi. J Plankton Res 33(8):1311–1316

    Article  Google Scholar 

  • Szostakowska B, Myjak P, Kur J, Sywula T (2001) Molecular evaluation of Hysterothylacium auctum (Nematoda, Ascaridida, Raphidascarididae) taxonomy from fish of the southern Baltic. Acta Parasitol 46(3):194–201

    CAS  Google Scholar 

  • Szostakowska B, Myjak P, Kur J (2002) Identification of anisakid nematodes from the Southern Baltic Sea using PCR-based methods. Mol Cell Probes 16(2):111–118

    Article  CAS  PubMed  Google Scholar 

  • Sakanari J, Loinaz H, Deardorff T, Raybourne R, McKerrow J, Frierson JG (1988) Intestinal anisakiasis. A case diagnosed by morphologic and immunologic methods. Am J Clin Pathol 90:107–113

    Article  CAS  PubMed  Google Scholar 

  • Shih H-H, Jeng M-S (2002) Hysterothylacium aduncum (Nematoda: Anisakidae) infecting a herbivorous fish, Siganus fuscescens, off the Taiwanese coast of the Northwest Pacific. zoological studies-Taipei 41:208–215

    Google Scholar 

  • Smetana, H.F., and Orihel, T.C. (1969) Gastric papillomata in Macaca speciosa induced by Nochtia nochti (Nematoda: Trichostrongyloidea). The Journal of parasitology, 349–351

  • Tsutsumi Y, Fujimoto Y (1983) Early gastric cancer superimposed on infestation of an anisakis-like larva: a case report. Tokai J Exp Clin Med 8:265–273

    CAS  PubMed  Google Scholar 

  • Yagi K, Nagasawa K, Ishikura H, Nakagawa A, Sato N, Kikuchi K, Ishikura H (1996) Female worm Hysterothylacium aduncum excreted from human: a case report. Jpn J Parasitol 45(1):12–23

    Google Scholar 

  • Zahabiun F, Sadjjadi SM, Esfandiari F (2015) Development of a double glass mounting method using formaldehyde alcohol azocarmine lactophenol (FAAL) and its evaluation for permanent mounting of small nematodes. Iran J Parasitol 10:617–624

    PubMed  PubMed Central  Google Scholar 

  • Zhu X, Gasser RB, Jacobs DE, Hung G-C, Chilton NB (2000) Relationships among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitol Res 86:738–744

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This project was financially supported by the office of vice-chancellor for research at Shiraz University of Medical Sciences, Grant No: 93-7252. Technical assistance of Mr. Abouzar Valizadeh and Mr. Mohammad Mehdi Ommati are acknowledged. The authors thank Prof. S. Sajjadi for his valuable assistance.

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Correspondence to Seyed Mahmoud Sadjjadi.

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Research involving human participants and/or animals

This protocol was performed in accordance with the international guiding principles for biomedical researchers involving laboratory animals at Shiraz University of Medical Sciences, Shiraz, Iran (code: ec:9372-7252).

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The present study had no tests on human.

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Najjari, M., Sadjjadi, S.M., Derakhshanfar, A. et al. Hysterothylacium amoyense in Platycephalous indicus: a Persian Gulf fish and its experimental infection of mouse model. Comp Clin Pathol 25, 1143–1149 (2016). https://doi.org/10.1007/s00580-016-2318-x

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