Epidemiology and molecular identification of Anisakis pegreffii (Nematoda: Anisakidae) in the horse mackerel Trachurus trachurus from northern Morocco | Journal of Helminthology | Cambridge Core (original) (raw)

Abstract

Anisakis infection parameters were studied in horse mackerel (Trachurus trachurus) taken from two areas of northern Morocco (Tetouan and Tangier), which showed a mean prevalence of 54.9%. Identification of the ITS1–5.8S–ITS2 fragment by polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) showed A. pegreffii to be the dominant species; no A. simplex s.s. were detected. The presence of A. pegreffii in horse mackerel was not influenced by the sex (P= 0.46) or catch area (Atlantic versus Mediterranean, P= 0.52) of the fish, but was significantly related to their length, weight, liver weight and gonad weight, and to the season of their capture (P< 0.05). A low prevalence (8.6%) and mean intensity (1.0) was detected in the muscle, probably related to the reduced ability of A. pegreffii to penetrate muscle. The risk of the presence of A. pegreffii in the muscle was fivefold higher in fish caught during the summer than during any other season. Susceptible members of the human population can minimize the risk of infection by avoiding the consumption of larger horse mackerel specimens during the summer.

References

Abattouy, N., Valero, A., Benajiba, M.H., Lozano, J. & Martín-Sánchez, J. (2011) Anisakis simplex s.l. parasitization in mackerel (Scomber japonicus) caught in the North of Morocco – prevalence and analysis of risk factors. International Journal of Food Microbiology 150, 136–139.Google Scholar

Abaunza, P., Villamor, B. & Pérez, J.R. (1995) Infestation by larvae of Anisakis simplex (Nematoda: Ascaridata) in horse mackerel, Trachurus trachurus, and Atlantic mackerel, Scomber scombrus, in ICES Divisions VIIIb, VIIIc and IXa (N-NW of Spain). Scientia Marina 59, 223–233.Google Scholar

Abollo, E., Paggi, L., Pascual, S. & D'Amelio, S. (2003) Occurrence of recombinant genotypes of Anisakis simplex s.s. and Anisakis pegreffii (Nematoda, Anisakidae) in an area of sympatry. Infection, Genetics and Evolution 3, 175–181.Google Scholar

Adroher, F.J., Valero, A., Ruiz-Valero, J. & Iglesias, L. (1996) Larval anisakids (Nematoda: Ascaridoidea) in horse mackerel (Trachurus trachurus) from the fish market in Granada (Spain). Parasitology Research 82, 253–256.CrossRef Google Scholar PubMed

Bahar, B. & Tuncay, M.S. (2009) Food and feeding habits of the Atlantic Horse Mackerel, Trachurus trachurus, from the Aegean Sea. Zoology in the Middle East 46, 47–54.Google Scholar

Bahar, I., Chennubhotla, C. & Tobi, D. (2007) Intrinsic dynamics of enzymes in the unbound state and relation to allosteric regulation. Current Opinion in Structural Biology 17, 633–640.Google Scholar

Bush, A.O., Lafferty, K.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal Parasitology 83, 575–583.Google Scholar

Bussmann, B. & Ehrich, S. (1979) Investigations on infestation of blue whiting (Micromesistius poutassou) with larval Anisakis sp. (Nematoda: Ascaridida). Archiv für Fischereiwiss 29, 155–165.Google Scholar

Caballero, S., Ligas, A., Bruschi, F. & D'Amelio, S. (2012) Molecular identification of Anisakis spp. from fishes collected in the Tyrrhenian Sea (NW Mediterranean). Veterinary Parasitology 187, 563–566.Google Scholar

Cissé, M. & Belghyti, D. (2005) Helminth parasites of chub mackerel Scomber japonicus (Houttuyn, 1782) from the harbour of Mehdia–Kenitra (Atlantic coast of Morocco). Journal of Aquatic Sciences 20, 63–67.Google Scholar

Cremonte, F. & Sardella, N.H. (1997) The parasitofauna of Scomber japonicus Houttuyn, 1782 (Pisces: Scombridae) in two zones of the Argentine Sea. Fishery Research 31, 1–9.CrossRef Google Scholar

D'Amelio, S., Mathiopoulos, K.D., Santos, C.P., Pugachev, O.N., Webb, S.C., Picanço, M. & Paggi, L. (2000) Genetic markers in ribosomal DNA for the identification of members of the genus Anisakis (Nematoda: Ascaridoidea) defined by polymerase chain reaction based restriction fragment length polymorphism. International Journal of Parasitology 30, 223–226.Google Scholar

Daschner, A., Alonso-Gómez, A., Cabañas, R., Suárez-de-Parga, J.M. & López-Serrano, M.C. (2000) Gastroallergic anisakiasis: borderline between food allergy and parasitic disease – clinical and allergologic evaluation of 20 patients with confirmed acute parasitism by Anisakis simplex . Journal of Allergy and Clinical Immunology 105, 176–181.Google Scholar

Durif, C., Élie, P., Dufour, S., Marchelidon, J. & Vidal, B. (2000) Analysis of morphological and physiological parameters during the silvering process of the European eel (Anguilla anguilla) in the lake of Grand-Lieu (France). Cybium, International Journal of Ichthyology 24, 63–74.Google Scholar

FAO, (2001) Report of the Working Group on the assessment of small-pelagic fish off northwest Africa. Fisheries Report , 133 pp. Rome, Food and Agriculture Organization.Google Scholar

FAO, (2008) Report of the Working Group on the assessment of small-pelagic fish off northwest Africa. Fisheries Report , pp. 117–118. Rome, Food and Agriculture Organization.Google Scholar

Farjallah, S., Busi, M., Mahjoub, M.O., Slimane, B.B., Paggi, L., Said, K. & D'Amelio, S. (2008) Molecular characterization of larval anisakid nematodes from marine fishes of the Moroccan and Mauritanian coasts. Parasitology International 57, 430–436.Google Scholar

Hartwich, G. (1974) CIH keys to the nematode parasites of vertebrates. pp. 1–15 in Anderson, R.C., Chabaud, A. & Willmott, S. (Eds) Keys to genera of the Ascaridoidea. Farnham Royal, Bucks, England, Commonwealth Agricultural Bureaux.Google Scholar

Hauck, A.K. (1977) Occurrence and survival of the larval nematode Anisakis sp. in the flesh of fresh, frozen, brined and smoked pacific herring, Clupea harengus pallasi . Journal of Parasitology 63, 515–519.Google Scholar

Jardas, I., Santic, M. & Pallaoro, A. (2004) Diet composition and feeding intensity of horse mackerel, Trachurus trachurus (Osteichthyes: Carangidae) in the eastern Adriatic. Marine Biology 144, 1051–1056.CrossRef Google Scholar

Kijewska, A., Słomińska, M., Węgrzyn, G. & Rokicki, J. (2000) A PCR-RFLP assay for identification of Anisakis simplex from different geographical regions. Molecular and Cellular Probes 14, 349–354.Google Scholar

Kijewska, A., Burzyński, A. & Wenne, R. (2009) Anisakid parasites of fishes caught on the African shelf. Journal of Parasitology 95, 639–645.Google Scholar

Klimpel, S., Kellermanns, E. & Palm, H.W. (2008) The role of pelagic swarm fish (Myctophidae: Teleostei) in the oceanic life cycle of Anisakis sibling species at the Mid-Atlantic Ridge, Central Atlantic. Parasitology Research 104, 43–53.Google Scholar

Køie, M. (1993) Nematode parasites in teleosts from 0 to 1540 m depth off the Faroe Islands (the North Atlantic). Ophelia 38, 217–243.Google Scholar

Køie, M., Berland, B. & Burt, M.D.B. (1995) Development to third-stage larva occurs in the eggs of Anisakis simplex and Pseudoterranova decipiens (Nematoda, Ascaridoidea, Anisakidae). Canadian Journal of Fisheries and Aquatic Sciences 52, 134–139.Google Scholar

Manfredi, M.T., Crosa, G., Galli, P. & Ganduglia, S. (2000) Distribution of Anisakis simplex in fish caught in the Ligurian Sea. Parasitology Research 86, 551–553.CrossRef Google Scholar PubMed

Marques, J.F., Cabral, H.N., Busi, M. & D'Amelio, S. (2006) Molecular identification of Anisakis species from Pleuronectiformes of the Portuguese coast. Journal of Helminthology 80, 47–51.Google Scholar

Martín-Sánchez, J., Artacho-Reinoso, M.E., Díaz-Gavilán, M. & Valero-López, A. (2005) Structure of Anisakis simplex s.l. populations in a region sympatric for A. pegreffii and A. simplex s.s. Absence of reproductive isolation between both species. Molecular Biochemistry and Parasitology 141, 155–162.CrossRef Google Scholar

Mattiucci, S. & Nascetti, G. (2008) Advances and trends in the molecular systematic of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes. Advances in Parasitology 66, 147–148.Google Scholar PubMed

Mattiucci, S., Paggi, L., Nascetti, G., Abollo, E., Webb, S.C., Pascual, S., Cianchi, R. & Bullini, L. (2001) Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae). International Journal of Parasitology 31, 9–14.Google Scholar

Mattiucci, S., Abaunza, P., Damiano, S., Garcia, A., Santos, M.N. & Nascetti, G. (2007) Distribution of Anisakis larvae, identified by genetic markers, and their use for stock characterization of demersal and pelagic fish from European waters: an update. Journal of Helminthology 81, 117–127.Google Scholar

McGladdery, S.E. (1986) Anisakis simplex (Nematoda: Anisakidae) infection of the musculature and body cavity of Atlantic herring (Clupea harengus harengus). Canadian Journal of Fisheries and Aquatic Sciences 43, 1312–1317.CrossRef Google Scholar

Petter, J.A. & Maillard, C. (1988) Larves d'ascarides parasites de poissons en Méditerranée Occidentale. Annales Muséum National D'Histoire Naturelle Paris 10, 347–369.Google Scholar

Pontes, T., D'Amelio, S., Costa, G. & Paggi, L. (2005) Molecular characterization of larval anisakid nematodes from marine fishes of Madeira by a PCR-based approach, with evidence for a new species. Journal of Parasitology 91, 1430–1434.Google Scholar

Quiazon, K.M.A., Yoshinaga, T. & Ogawa, K. (2011) Experimental challenge of Anisakis simplex sensu stricto and Anisakis pegreffii (Nematoda: Anisakidae) in rainbow trout and olive flounder. Parasitology International 60, 126–131.CrossRef Google Scholar PubMed

Rodero, M., Chivato, T., Muro, A. & Cuellar, C. (2005) Enzyme-linked immunosorbent assay and Western blot antibody determination in sera from patients diagnosed with different helminthic infections with Anisakis simplex antigen purified by affinity chromatography. Memórias do Instituto Oswaldo Cruz 100, 293–301.CrossRef Google Scholar PubMed

Santic, M., Jardas, I. & Pallaoro, A. (2005) Feeding habits of horse mackerel, Trachurus trachurus (Linneaus, 1758), from the central Adriatic Sea. Journal of Applied Ichthyology 21, 125–130.Google Scholar

Scala, E., Giani, M., Pirrotta, L., Guerra, E.C., Cadoni, S., Girardelli, C.R., De Pità, O. & Puddu, P. (2001) Occupational generalized urticaria and allergic airbone asthma due to Anisakis simplex . European Journal of Dermatology 11, 249–250.Google Scholar

Shukhgalter, O.A. (2004) Parasite fauna of the chub mackerel (Scombridae: Scomber japonicus Houttuyn, 1782) in the Central-Eastern Atlantic Ocean (the Atlantic coast of the North Africa and the Azores banks). Parasitologiya 38, 160–170.Google Scholar

Silva, M.E.R. & Eiras, J.C. (2003) Occurrence of Anisakis sp. in fishes off the Portuguese West coast and evaluation of its zoonotic potential. Bulletin of the European Association of Fish Pathologists 23, 13–17.Google Scholar

Smith, J.W. (1983) Anisakis simplex (Rudolphi, 1809, det. Krabbe, 1878) (Nematoda: Ascaridoidea): morphology and morphometry of larvae from euphausiids and fish, and a review of the life-history and ecology. Journal of Helminthology 57, 491–495.Google Scholar

Smith, J.W. & Wootten, R. (1978) Anisakis and anisakiasis. Advances in Parasitology 16, 93–163.Google Scholar

Solas, M.T., Garcia, M.L., Rodríguez-Mahillo, A.I., González-Munoz, M., De las Heras, C. & Tejada, M. (2009) Aniskais antigens detected in fish muscle infested with Anisakis simplex L3. Journal of Food Protection 71, 1273–1276.CrossRef Google Scholar

Suzuki, J., Murata, R., Hosaka, M. & Araki, J. (2010) Risk factors for human Anisakis infection and association between the geographic origins of Scomber japonicus and anisakid nematodes. International Journal of Food Microbiology 137, 88–93.Google Scholar

Umehara, A., Kawakami, Y., Matsui, T., Araki, J. & Uchida, A. (2006) Molecular identification of Anisakis simplex sensu stricto and Anisakis pegreffii (Nematoda: Anisakidae) from fish and cetacean in Japanese waters. Parasitology International 55, 267–271.Google Scholar

Valero, A., Martín-Sánchez, J. & Reyes-Muelas, E. (2000) Larval anisakids parasitizing the blue whiting Micromesistius poutassou from Motril bay in the Mediterranean of Southern Spain. Journal of Helminthology 74, 361–364.Google Scholar

Zhu, X., Gasser, R.B., Podolska, M. & Chilton, N. (1998) Characterization of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. International Journal of Parasitolology 28, 1911–1921.CrossRef Google Scholar PubMed