Research Note. Prevalence, protein analysis and possible preventive measures against zoonotic anisakid larvae isolated from marine Atherina fish

Open access


Anisakidosis is a zoonotic infection caused by ingestion of raw or undercooked marine fish including Atherina. In some parts of Egypt, the prevalence of anisakid larvae in marine Atherina still, largely, undetermined. Moreover, the currently used procedures are insufficient to avoid human infection. The aim of this study was to identify the prevalence of anisakid larvae in marine Atherina and to test the effect of several treatment procedures on the viability of anisakid larvae. The infection rate of marine Atherina with anisakid larvae was 23.12 %. Anisakid larvae protein revealed molecular weights ranged from 11.5 - 118.5 Kilo Dalton (KDa.). Moreover, freezing at -20 °C for 21 hours (hrs.) as well as vinegar (5 %) treatment for 3 days were the most effective ways to inactivate the larvae. This study states the zoonotic risk of consuming raw or undercooked marine Atherina and highlights the importance of freezing and vinegar treatment in preventing human infection.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • A MANY M.M.M.V.S. (2007): Parasites of some imported fish. Thesis Parasitology Faculty of Veterinary Medicine Zagazig University Egypt

  • AMER O.H. EL-ASHRAM A.M.M. SHAGAR G. I.A. (2007): Studies on the internal parasitic helminthes disease among wild Mediterranean sand smelt (Atherina) with special reference to Ligula intestinalis infection in Egypt. In The International Arab African Fish Resources Conference and Exhibition. 28 - 30 June 2007

  • AMIN A.M. (2009): Zoonotic studies on helminths causing diarrhea in man. Ph.D. Thesis Zoonoses Faculty of Veterinary Medicine Zagazig University Egypt

  • ARAFA S.Z. AL-HOOT A.A. HUSSEIN H.S. (2009): Pathological and ultrastructural studies on Anisakis simplex Rudolphi-1809 infecting Carangoides bajad with special reference to intestinal maturation in puppies. J. Egypt Soc. Parasitol. 39: 607 - 616

  • ARCHER D.L. (2004): Freezing: an underutilized food safety technology? Int. J. Food Microbiol. 90: 127 - 138. DOI: 10.1016/ S0168-1605(03)00215-0

  • ASMAA R.A. (2009): Parasites encystation in some crustaceans and fi sh. Ph.D. thesis. Parasitology Faculty of Veterinary Medicine Zagazig University Egypt

  • AUDICANA M.T. ANSOTEGUI I.J. DE CORRES L.F. KENNEDY M.W. (2002): Anisakis simplex: dangerous - dead and alive? Trends Parasitol. 18: 20 - 25. DOI: 10.1016/S1471-4922(01)02152-3

  • AUDICANA M.T. KENNEDY M.W. (2008): Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clin. Microbiol. Rev. 21 360 - 379. DOI: 10.1128/CMR.00012-07

  • BAK T.-J. JEON C.-H. KIM J.-H. (2014): Occurrence of anisakid nematode larvae in chub mackerel (Scomber japonicus) caught off Korea. Int. J. Food Microbiol. 191: 149 - 156. DOI: 10.1016/j. ijfoodmicro.2014.09.002

  • BAO M. MOTA M. NACHON D.J. ANTUNES C. COBO F. GARCI M. E. PIERCE G.J. PASCUAL S. (2015): Anisakis infection in allis shad Alosa alosa (Linnaeus 1758) and twaite shad Alosa fallax (Lacépède 1803) from Western Iberian Peninsula Rivers: zoonotic and ecological implications. Parasitol Res. 114: 2143 - 2154. DOI: 10.1007/s00436-015-4403-5

  • BARBER I. (2007): Parasites behaviour and welfare in fi sh. Appl. Anim. Behav. Sci. 104: 251 - 264. DOI: 10.1016/j.applanim. 2006.09.005

  • BERNARDI C. (2009): Preliminary study on prevalence of larvae of Anisakidae family in European sea bass (Dicentrarchus labrax). Food Control 20: 433 - 434. DOI: 10.1016/j.foodcont.2008.07.001

  • BELDSOE G.E. ORIA M.P. (2001) Potential Hazards in Cold- Smoked Fish: Parasites. J. Food Sci. 66: S1100 - S1103. DOI: 10.1111/j.1365-2621.2001.tb15529.x

  • BUTT A.A. ALDRIDGE K.E. SANDER C.V. (2004): Infections related to the ingestion of seafood. Part II: parasitic infections and food safety. Lancet Infect. Dis. 4: 294 - 300. DOI: 10.1016/S1473-3099(04)01005-9

  • CABALLERO M.L. MONEO I. (2004): Several allergens from Anisakis simplex are highly resistant to heat and pepsin treatments. Parasitol. Res. 93: 248 - 251. DOI: 10.1007/s00436-004-1099-3

  • CARBALLEDA-SANGIAO N. OLIVARES F. RODRIGUEZ-MAHILLO A.I. CARECHE M. TEJADA M. MONEO I. GONZALEZ-MUNOZ M. (2014): Identifi cation of autoclave-resistant Anisakis simplex allergens. J. Food Prot. 77: 605 - 609. DOI: 10.4315/0362-028X.JFP-13-278

  • CHAI J.Y. DARWIN MURRELL K. LYMBERY A.J. (2005): Fish-borne parasitic zoonoses: status and issues. Int. J. Parasitol. 35: 1233 -1254. DOI: 10.1016/j.ijpara.2005.07.013

  • CHALIGIANNIS I. LALLE M. POZIO E. SOTIRAKI S. (2012): Anisakidae infection in fi sh of the Aegean Sea. Vet. Parasitol. 184: 362 - 366. DOI: 10.1016/j.vetpar.2011.09.007

  • CHEN H.-Y. CHENG Y.-S. GRABNER D.S. CHANG S.-H. SHIH H.- H. (2014): Effect of different temperatures on the expression of the newly characterized heat shock protein 90 (Hsp90) in L3 of Anisakis spp. isolated from Scomber australasicus. Vet. Parasitol. 205(3 - 4): 540 - 550. DOI: 10.1016/j.vetpar.2014.09.013

  • CHO M.K. PARK M.K. KANG S.A. CABALLERO M.L. PEREZ-PINAR T. RODRIGUEZ-PEREZ R. OCK M.S. CHA H.J. HONG Y.C. YU H.S. (2014): Allergenicity of two Anisakis simplex allergens evaluated in vivo using an experimental mouse model. Exp Parasitol. 146: 71 - 77. DOI: 10.1016/j.exppara.2014.09.008

  • CHO S.W. LEE H.N. (2006): Immune reactions and allergy in experimental anisakiasis. Korean J. Parasitol. 44: 271 - 283. DOI: 10.3347/kjp.2006.44.4.271

  • COLAK S.O. (2013): The helminth community of the sand smelt (Atherina boyeri Risso 1810) from Lake Iznik Turkey. J. Helminthol. 87: 129 - 134. DOI: 10.1017/S0022149X11000770

  • DASCHNER A. ALONSO-GOMEZ A. CABANAS R. SUAREZ-DE-PARGA J.M. LOPEZ-SERRANO M.C. (2000): Gastroallergic anisakiasis: borderline between food allergy and parasitic disease-clinical and allergologic evaluation of 20 patients with confi rmed acute parasitism by Anisakis simplex. J. Allergy Clin. Immunol. 105: 176 - 181. DOI: 10.1016/S0091-6749(00)90194-5

  • DEL POZO M.D. AUDICANA M. DIEZ J.M. MUNOZ D. ANSOTEGUI I.J. FERNANDEZ E. GARCIA M. ETXENAGUSIA M. MONEO I. FERNANDEZ DE CORRES L. (1997): Anisakis simplex a relevant etiologic factor in acute urticaria. Allergy 52: 576 - 579. DOI: 10.1111/j.1398-9995.1997.tb02603.x

  • DEZFULI B.S. GRANDI G. FRANZOI P. ROSSI R. (1990): Histopathology in Atherina boyeri (Pisces: Atherinidae) resulting from infection by Telosentis exiguus (Acanthocephala). Parassitologia 32: 283 - 291

  • DIAB R.M.G. ELTEMSAHY M.M. ELKERDANY E.D. GAAFAR M. NASR M.A. (2010): A study of medically important fi sh - transmitted parasites in Alexandria. Int. J. Infect. Dis. 14 Supplement 1: e290. DOI: 10.1016/j.ijid.2010.02.2130

  • ELKEST S.E. MARTH E.H. (1992): Freezing of Listeria monocytogenes and other microorganisms: A review. J. Food Prot. 55: 639 - 648

  • ESKESEN A. STRAND E.A. ANDERSEN S.N. ROSSELAND A. HELLUM K.B. STRAND O.A. (2001): Anisakiasis presenting as an obstructive duodenal tumor. A Scandinavian case. Scand. J. Infect. Dis. 33: 75 - 76. DOI:10.1080/003655401750064149

  • FARJALLAH S. SLIMANE B.B. BUSI M. PAGGI L. AMOR N. BLEL H. SAID K. D’AMELIO S. (2008): Occurrence and molecular identifi - cation of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitol. Res 102: 371 - 379. DOI: 10.1007/s00436-007-0771-9

  • GARCIA L.S. (2001): Diagnostic medical Parasitology 4th Edition. ASM Press Washington D. C. U. S. A.

  • HENDERSON P.A. BAMBER R.N. (1987): On the reproductive biology of the sand smelt Atherina boyeri Risso (Pisces: Atherinidae) and its evolutionary potential. Biol. J. Linn. Soc. Lond. 32: 395 - 415. DOI: 10.1111/j.1095-8312.1987.tb00440.x

  • HUANG W. Y. (2005): [Survival of the third stage larvae of anisakis simplex in various conditions and experimental infection in rats]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 23 106 - 109

  • JABBAR A. FONG R.W. KOK K.X. LOPATA A.L. GASSER R.B. BEVERIDGE I. (2013): Molecular characterization of anisakid nematode larvae from 13 species of fi sh from Western Australia. Int. J. Food Microbiol. 161 247 - 253.

  • KARL H. ROEPSTORFF A. HUSS H.H. BLOEMSMA B. (1994): Survival of Anisakis larvae in marinated herring fillets. Int. J. Food Sci. Technol. 29: 661 - 670. DOI: 10.1111/j.1365-2621.1994.tb02107.x

  • KOBAYASHI Y. SHIMAKURA K. ISHIZAKI S. NAGASHIMA Y. SHIOMI K. (2007): Purifi cation and cDNA cloning of a new heat-stable allergen from Anisakis simplex. Mol. Biochem. Parasitol. 155: 138 -145. DOI: 10.1016/j.molbiopara.2007.06.012

  • KOINARI M. KARL S. ELLIOT A. RYAN U. LYMBERY A. J. (2013): Identifi cation of Anisakis species (Nematoda: Anisakidae) in marine fish hosts from Papua New Guinea. Vet. Parasitol. 193: 126 - 133. DOI: 10.1016/j.vetpar.2012.12.008

  • LAEMMLI U. K. (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680 - 685 MA H.W. JIANG T.J. QUAN F.S. CHEN X.G. WANG H.D. ZHANG Y.S. CUI M.S. ZHI W.Y. JIANG D.C. (1997): The infection status of anisakid larvae in marine fi sh and cephalopods from the Bohai Sea China and their taxonomical consideration. Korean J. Parasitol. 35: 19 - 24. DOI: 10.3347/kjp.1997.35.1.19

  • MAGDA A.A. AMER O.H. MAYSA A.I.A. MERWAD A.M.A. HASSAN M.S.A. (2010): Role of Atherina fi sh in transmitting some trema todes of public health importance. In Proceedings of the 3rd Global Fisheries and Aquaculture Research Conference Foreign Agricultural Relations (FAR) Egypt 29 November - 1 December 2010 pp. 120 - 133

  • MARI A. RASI C. PALAZZO P. SCALA E. (2009): Allergen databases: current status and perspectives. Curr. Allergy Asthma Rep. 9: 376 - 383. DOI: 10.1007/s11882-009-0055-9

  • MARTY G.D. (2008): Anisakid larva in the viscera of a farmed Atlantic salmon (Salmo salar). Aquaculture 279: 209 - 210. DOI: 10.1016/j.aquaculture.2008.04.006

  • MEHRDANA F. BAHLOOL Q.Z. SKOV J. MARANA M.H. SINDBERG D. MUNDELING M. OVERGAARD B.C. KORBUT R. STROM S.B. KANIA P.W. 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. DOI: 10.1016/j.vetpar.2014.08.027

  • MOLINA-FERNÁNDEZ D. MALAGÓN D. GÓMEZ-MATEOS M. BENÍTEZ R. MARTÍN-SÁNCHEZ J. ADROHER F.J. (2015): Fishing area and fi sh size as risk factors of Anisakis infection in sardines (Sardina pilchardus) from Iberian waters southwestern Europe. Int. J. Food Microbiol. 203: 27 - 34. DOI: 10.1016/j.ijfoodmicro.2015.02.024

  • MONEO I. CABALLERO M. L. GONZALEZ-MUNOZ M. RODRIGUEZ-MAHILLO A.I. RODRIGUEZ-PEREZ R. SILVA A. (2005): Isolation of a heat-resistant allergen from the fi sh parasite Anisakis simplex. Parasitol. Res. 96: 285 - 289. DOI: 10.1007/s00436-005-1362-2

  • MONEO I. CABALLERO M.L. GOMEZ F. ORTEGA E. ALONSO J.M. (2000): Isolation and characterization of a major allergen from the fi sh parasite Anisakis simplex. J. Allergy Clin. Immunol. 106: 177 - 182. DOI: 10.1067/mai.2000.106732

  • MORAVEC F. (1994): Parasitic nematode of freshwater fi shes of Europe. Academia Prague and Kluwer Academic Publishers Dordrecht The Netherlands Boston and London 473pp.

  • NADA M.S.M. ABD EL-GHANY A. M. (2011): Anisakid nematodes in marine fi shes. J. Am. Sci. 7: 1000 - 1005

  • NOH J.H. KIM B. KIM S.M. OCK M. PARK M.I. GOO J.Y. (2003): A case of acute gastric anisakiasis provoking severe clinical problems by multiple infection. Korean J. Parasitol. 41: 97 - 100. DOI: 10.3347/kjp.2003.41.2.97

  • OH S.-R. ZHANG C.-Y. KIM T.-I. HONG S.-J. JU I.-S. LEE S.-H. KIM S.-H. CHO J.-I. HA S.-D. (2014): Inactivation of Anisakis larvae in salt-fermented squid and pollock tripe by freezing salting and combined treatment with chlorine and ultrasound. Food Control 40: 46 - 49. DOI: 10.1016/j.foodcont.2013.11.023

  • PARK H.K. CHO M.K. PARK M.K. KANG S.A. KIM Y.S. KIM K.U. LEE M.K. OCK M.S. CHA H.J. YU H.S. (2011): A 24 kDa excretory- secretory protein of Anisakis simplex larvae could elicit allergic airway infl ammation in mice. Korean J. Parasitol. 49: 373 - 380. DOI: 10.3347/kjp.2011.49.4.373

  • PARK J.H. GUK S.M. KIM T.Y. SHIN E.H. LIN A. PARK J.Y. KIM J.L. HONG S.T. CHAI J.Y. (2004): Clonorchis sinensis metacercarial infection in the pond smelt Hypomesus olidus and the minnow Zacco platypus collected from the Soyang and Daechung Lakes. Korean J. Parasitol. 42: 41 - 44. DOI: 10.3347/kjp.2004.42.1.41

  • PARK J.S. CHO M.K. YU H.S. AHN S.C. (2012): Identifi cation of a 24 kDa excretory secretory protein in Anisakis simplex. Exp. Parasitol. 130: 69 - 72. DOI: 10.1016/j.exppara.2011.09.008

  • POMBO L. ELLIOTT M. REBELO J.E. (2005): Ecology age and growth of Atherina boyeri and Atherina presbyter in the Ria de Aveiro Portugal. Cybium 29: 47 - 55

  • PRITCHARD M.H. KRUSE G.O.W. (1982): The collection and preservation of animal parasites. Technical Bulletin No. 1. The Harold W. Manter Laboratory University of Nebraska Press 141 pp.

  • PULLEIRO-POTEL L. BARCALA E. MAYO-HERNÁNDEZ E. MUÑOZ P. (2015): Survey of anisakids in commercial teleosts from the western Mediterranean Sea: Infection rates and possible effects of environmental and ecological factors. Food Control 55: 12 - 17. DOI: 10.1016/j.foodcont.2015.02.020

  • QUIAZON K.M.A. YOSHINAGA T. OGAWA K. (2011): Experimental challenge of Anisakis simplex sensu stricto and Anisakis pegreffi i (Nematoda: Anisakidae) in rainbow trout and olive fl ounder. Parasitol. Int. 60: 126 - 131. DOI: 10.1016/j.parint.2010.11.007

  • RAYBOURNE R. DEARDORFF T.L. BIER J.W. (1986): Anisakis simplex: Larval excretory secretory protein production and cytostatic action in mammalian cell cultures. Exp. Parasitol. 62: 92 - 97. DOI: 10.1016/0014-4894(86)90012-3

  • RODERO M. CUELLAR C. CHIVATO T. MATEOS J.M. LAGUNA R. (2007): Western blot antibody determination in sera from patients diagnosed with Anisakis sensitization with different antigenic fractions of Anisakis simplex purifi ed by affi nity chromatography. J. Helminthol. 81: 307 - 310. DOI: 10.1017/S0022149X07820220

  • RODERO M. JIMENEZ A. CUELLAR C. (2002): Evaluation by ELISA of Anisakis simplex larval antigen purifi ed by affi nity chromatography. Mem. Inst. Oswaldo Cruz 97: 247 - 252. DOI: 10.1590/S0074-02762002000200018

  • RODRIGUEZ-MAHILLO A.I. GONZALEZ-MUNOZ M. DE LAS HERAS C. TEJADA M. MONEO I. (2010): Quantifi cation of Anisakis simplex allergens in fresh long-term frozen and cooked fi sh muscle. Foodborne Pathog. Dis. 7: 967 - 973

  • RODRIGUEZ-MAHILLO A.I. GONZALEZ-MUNOZ M. MONEO I. SOLAS M. T. MENDIZABAL A. DE LAS HERAS C. TEJADA M. (2008): Allergenic properties and cuticle microstructure of Anisakis simplex L3 after freezing and pepsin digestion. J. Food Prot. 71: 2578 - 2581.

  • RODRIGUEZ-PEREZ R. MONEO I. RODRIGUEZ-MAHILLO A. CABALLERO M. L. (2008): Cloning and expression of Ani s 9 a new Anisakis simplex allergen. Mol. Biochem. Parasitol. 159: 92 - 97. DOI: 10.1016/j.molbiopara.2008.02.008

  • SANCHEZ-MONSALVEZ I. DE ARMAS-SERRA C. MARTINEZ J. DORADO M. SANCHEZ A. RODRIGUEZ-CAABEIRO F. (2005): A new procedure for marinating fresh anchovies and ensuring the rapid destruction of Anisakis larvae. J. Food Prot. 68: 1066 - 1072

  • SERRACCA L. BATTISTINI R. ROSSINI I. CARDUCCI A. VERANI M. PREARO M. TOMEI L. DE MONTIS G. ERCOLINI C. (2014): Food safety considerations in relation to Anisakis pegreffi i in anchovies (Engraulis encrasicolus) and sardines (Sardina pilchardus) fi shed off the Ligurian Coast (Cinque Terre National Park NW Mediterranean). Int. J. Food Microbiol. 190: 79 - 83. DOI: 10.1016/j.ijfoodmicro. 2014.08.025

  • SETYOBUDI E. JEON CH.-H. LEE CH.-H. SEONG K.-B. KIM J.-H. (2011): Occurrence and identifi cation of Anisakis spp. (Nematoda: Anisakidae) isolated from chum salmon (Oncorhynchus keta) in Korea. Parasitol. Res. 108: 585 - 592. DOI: 10.1007/s00436-010-2101-x

  • SHAVER R.J. MIZELLE J.D. (1955): Effects of rapid and ultra-rapid freezing on Trichinella spiralis larvae from guinea pigs and rats. Am. Midl. Nat. 54: 65 - 77. DOI: 10.2307/2422178

  • SKOV J. MEHRDANA F. MARANA M.H. BAHLOOL Q.Z.M. JAAFAR R. M. SINDBERG D. JENSEN H.M. KANIA P.W. BUCHMANN K. (2014): Parasite infections of rainbow trout (Oncorhynchus mykiss) from Danish mariculture. Aquaculture 434: 486 - 492. DOI: 10.1016/j. aquaculture.2014.08.041

  • SMITH J. W. (1984): The abundance of Anisakis simplex L3 in the body-cavity and fl esh of marine teleosts. Int. J. Parasitol. 14: 491 - 495. DOI: 10.1016/0020-7519(84)90030-4

  • SOLAS M.T. GARCÍA M.L. DE LAS HERAS C.A. RODRIGUEZ-MAHILLO I. GONZALEZ-MUNOZ M. MONEO I. MENDIZÁBAL A. TEJADA M. (2009): Anisakis simplex antigens in fresh and frozen-thawed muscle of anchovies in vinegar. Food Sci. Tech. Int. 15: 139 - 148. DOI: 10.1177/1082013208105171

  • TEJADA M. SOLAS M.T. NAVAS A. MENDIZABAL A. (2006): Scanning electron microscopy of Anisakis larvae following different treatments. J. Food Prot. 69: 1379 - 1387

  • VALERO A.C. M.; BENITEZ R. FRANCISCO J.A. (2006): Anisakis spp. in European hake Merluccius merluccius (L.) from the Atlantic off north-west Africa and the Mediterranean off southern Spain. Acta Parasitol. 51: 209 - 212. DOI: 10.2478/s11686-006-0032-6

  • VIDACEK S. DE LAS HERAS C. SOLAS M.T. GARCIA M.L. MENDIZABAL A. TEJADA M. (2011): Viability and antigenicity of Anisakis simplex after conventional and microwave heating at fi xed temperatures. J. Food Prot. 74: 2119 - 2126. DOI: 10.4315/0362-028X. JFP-11-108

  • VIDACEK S. DE LAS HERAS C. SOLAS M.T. MENDIZABAL A. RODRIGUEZ- MAHILLO A.I. GONZALEZ-MUNOZ M. TEJADA M. (2009): Anisakis simplex allergens remain active after conventional or microwave heating and pepsin treatments of chilled and frozen L3 larvae. J. Sci. Food Agric. 89: 1997 - 2002. DOI: 10.1002/jsfa.3677

  • VIDACEK S. DE LAS HERAS C. SOLAS M.T. MENDIZABAL A. RODRIGUEZ- MAHILLO A.I. TEJADA M. (2010): Antigenicity and viability of Anisakis larvae infesting hake heated at different time-temperature conditions. J. Food Prot. 73: 62 - 68

  • WHARTON D.A. AALDERS O. (2002): The response of anisakid to freezing. J. Helminthol. 76: 363 - 368. DOI: 10.1079/JOH2002149

  • ZURAK I. (2010): Anisakis simplex from the Adriatic sea. In14th International Congress on Infectious Diseases Abstracts Int. J. Infect. Dis. 14 (Suppl. 1): e291. DOI:10.1016/j.ijid.2010.02.2132

Journal information
Impact Factor

IMPACT FACTOR 2018: 0.731
5-year IMPACT FACTOR: 0.634

CiteScore 2018: 0.8

SCImago Journal Rank (SJR) 2018: 0.398
Source Normalized Impact per Paper (SNIP) 2018: 0.554

Target audience: researchers in the field of human, veterinary medicine and natural science
All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 243 116 12
PDF Downloads 121 76 3