Research Article
BibTex RIS Cite

Ongoing Data from Presence of Zoonotic Anisakis Larvae in Imported Fish in Turkish Supermarkets: Frozen Atlantic Mackerel (Scomber Scombrus) and Smoked Atlantic Salmon (Salmo Salar)

Year 2023, Volume: 8 Issue: 2, 146 - 150, 30.06.2023

Gökmen Zafer Pekmezci Ertan Emek Onuk Banu Yardımcı

https://doi.org/10.35229/jaes.1259143
Cited By: 1

Abstract

Anisakis pegreffii and A. simplex sensu stricto (s.s.) are the main etiological agents causing human anisakiasis. Here, we aimed to investigate based on the pepsin digestion method of the occurrence of Anisakis larvae in imported deep-frozen whole Atlantic mackerel (Scomber scombrus) from FAO 27 to Turkey and smoked Norwegian farmed Atlantic salmon fillets (Salmo salar) between 2018 and 2019. A total of 100 whole Atlantic mackerel and 180 Atlantic salmon fillets were randomly sampled from local Turkish supermarkets. No Anisakis larvae were detected in smoked Atlantic salmon fillets. In total, 827 Anisakis larvae were found in mackerel, and the prevalence was 68% (68/100). The mI and mA of Anisakis larvae in mackerel were 13.1 and 8.2, respectively. Whereas the 95.28% (788/827) of the Anisakis larvae were found in abdominal cavity/viscera, the 4.72 % (39/827) of the larvae in the muscle. The prevalence and mI of Anisakis larvae in the abdominal cavity/viscera and muscle of mackerel was 63.0% (63/100) and 42.0% (42/100), and 12.5 and 0.9, respectively. The subsample of 100 larvae was molecularly identified by ITS RFLP patterns. The 99 (99.0%) larvae were identified as A. simplex (s.s.), and 1 (1.0%) larva was A. pegreffii. Consequently, there is low or no risk of anisakiasis in smoked farmed Atlantic salmon for Turkish consumers. The 42.0% prevalence of zoonotic Anisakis species larvae in imported Atlantic mackerel fillets could have public health risk in Turkish consumers for anisakiasis or allergy.

Keywords

FAO 27 ITS region Parasite PCR‒RFLP Zoonoses

Supporting Institution

Ondokuz Mayıs Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi

Project Number

PYO.VET.1901.18.002

Thanks

This study was supported by the Scientific Research Council of Ondokuz Mayis University, Samsun, Turkey, under project no PYO.VET.1901.18.002

References

  • Angot, V. & Brasseur, P. (1993). European farmed Atlantic salmon (Salmo salar L.) are safe from anisakid larvae. Aquaculture, 118(3-4), 339-344.
  • Audicana, M.T. & Kennedy, M.W. (2008). Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiology Reviews, 21(2), 360-79.
  • Aydin, C. & Pekmezci, G.Z. (2023). Molecular identification and infection levels of Anisakis species (Nematoda: Anisakidae) in the red scorpionfish Scorpaena scrofa (Scorpaenidae) from the Aegean Sea. Parasitology International, 92, 102691.
  • Bao, M., Pierce, G.J., Pascual, S., González-Muñoz, M., Mattiucci, S., Mladineo, I., Cipriani, P., Bušelić, I. & Strachan, N.J. (2017). Assessing the risk of an emerging zoonosis of worldwide concern: anisakiasis. Scientific Reports, 7(1), 43699.
  • Berland, B. (1961). Nematodes from some Norwegian marine fishes. Sarsia, 2(1), 1–50.
  • Caballero, M.L. & Moneo, I. (2004). Several allergens from Anisakis simplex are highly resistant to heat and pepsin treatments. Parasitology Research, 93, 248- 251.
  • 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 polymerasechain-reaction-based restriction fragment length polymorphism. International Journal for Parasitology, 30(2), 223-226.
  • European Food Safety Authority (EFSA), (2010). Scientific opinion on risk assessment of parasites in fishery products. EFSA Journal, 8(4), 1543.
  • Gómez-Mateos, M., Merino-Espinosa, G., Corpas-López, V., Valero-López, A. & Martín-Sánchez, J. (2020). A multi-restriction fragment length polymorphism genotyping approach including the beta-tubulin gene as a new differential nuclear marker for the recognition of the cryptic species Anisakis simplex s.s. and Anisakis pegreffii and their hybridization events. Veterinary Parasitology, 283, 109162.
  • González, M.Á.P., Cavazza, G., Gustinelli, A., Caffara, M. & Fioravanti, M. (2020). Absence of anisakis nematodes in smoked farmed Atlantic salmon (Salmo salar) products on sale in European countries. Italian Journal of Food Safety, 9(4), 8615.
  • Levsen, A., Cipriani, P., Mattiucci, S., Gay, M., Hastie, L. C., MacKenzie, K., Graham, J.P., Cecilie, S., Svanevik, C.S., Højgaard, D.P., Nascetti, G., González, A.F. & Pascual, S. (2018). Anisakis species composition and infection characteristics in Atlantic mackerel, Scomber scombrus, from major European fishing grounds-reflecting changing fish host distribution and migration pattern. Fisheries Research, 202, 112-121.
  • Levsen, A. & Maage, A. (2016). Absence of parasitic nematodes in farmed, harvest quality Atlantic salmon (Salmo salar) in Norway-Results from a large scale survey. Food Control, 68, 25-29.
  • Llarena-Reino, M., Piñeiro, C., Antonio, J., Outeriño, L., Vello, C., González, Á.F. & Pascual, S. (2013). Optimization of the pepsin digestion method for anisakids inspection in the fishing industry. Veterinary Parasitology, 191(3-4), 276-283.
  • Lunestad, B.T. (2003). Absence of nematodes in farmed Atlantic salmon (Salmo salar L.) in Norway. Journal of Food Protection, 66(1), 122-124.
  • Madrid, E., Gil, F., García, M., Debenedetti, Á.L., Trelis, M. & Fuentes, M.V. (2016). Potential risk analysis of human anisakiasis through the consumption of mackerel, Scomber scombrus, sold at Spanish supermarkets. Food Control, 66, 300-305.
  • Mattiucci, S., Cipriani, P., Levsen, A., Paoletti, M. & Nascetti, G. (2018). Molecular epidemiology of Anisakis and anisakiasis: an ecological and evolutionary road map. Advances in Parasitology, 99, 93-263.
  • Mattiucci, S., Cipriani, P., Webb, S.C., Paoletti, M., Marcer, F., Bellisario, B., Gibsoni, D.I. & Nascetti, G. (2014). Genetic and morphological approaches distinguish the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). The Journal of Parasitology, 100(2), 199-214.
  • Mattiucci, S., Colantoni, A., Crisafi, B., Mori‐Ubaldini, F., Caponi, L., Fazii, P., Nascetti, G. & Bruschi, F. (2017). Ig E sensitization to Anisakis pegreffii in Italy: Comparison of two methods for the diagnosis of allergic anisakiasis. Parasite Immunology, 39(7), e12440.
  • Mattiucci, S., Fazii, P., De Rosa, A., Paoletti, M., Megna, A. S., Glielmo, A., De Angelis, M., Costa, A., Meucci, C., Calvaruso, V., Sorrentini, I., Palma, G., Bruschi, F. & Nascetti, G. (2013). Anisakiasis and gastroallergic reactions associated with Anisakis pegreffii infection, Italy. Emerging Infectious Diseases, 19(3), 496.
  • Mattiucci, S., Paoletti, M., Borrini, F., Palumbo, M., Palmieri, R. M., Gomes, V., Casati, A. & Nascetti, G. (2011). First molecular identification of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in a paraffin-embedded granuloma taken from a case of human intestinal anisakiasis in Italy. BMC Infectious Diseases, 11, 82.
  • Mattiucci, S., Paoletti, M., Colantoni, A., Carbone, A., Gaeta, R., Proietti, A., Frattaroli, S., Fazii, P., Bruschi, F. & Nascetti, G. (2017). Invasive anisakiasis by the parasite Anisakis pegreffii (Nematoda: Anisakidae): diagnosis by real-time PCR hydrolysis probe system and immunoblotting assay. BMC Infectious Diseases, 17, 530.
  • Moneo, I., Caballero, M.L., González-Muñoz, M., Rodríguez-Mahillo, A.I., Rodríguez-Perez, R. & Silva, A. (2005). Isolation of a heat-resistant allergen from the fish parasite Anisakis simplex. Parasitology Research, 96, 285-289.
  • Pekmezci, G.Z., Onuk, E.E., Bolukbas, C.S., Yardimci, B., Gurler, A.T., Acici, M. & Umur, S. (2014). Molecular identification of Anisakis species (Nematoda: Anisakidae) from marine fishes collected in Turkish waters. Veterinary Parasitology, 201(1-2), 82-94.
  • Pekmezci, G.Z. (2014). Occurrence of Anisakis simplex sensu stricto in imported Atlantic mackerel (Scomber scombrus) represents a risk for Turkish consumers. International Journal of Food Microbiology, 185, 64-68.
  • Petter, A.J. & Maillard, C. (1988). Larves d’ascarides parasites de poissons en Méditerranée occidentale. Bulletin du Muséum National d'histoire Naturelle, 10(sect. A), 347-369.
  • Reiczigel, J., Marozzi, M., Fábián, I. & Rózsa, L. (2019). Biostatistics for parasitologists – a primer to Quantitative Parasitology. Trends in Parasitology, 35 (4), 277-281.
  • Simsek, E., Pekmezci, G. Z., Yildirim, A., Duzlu, O., Onder, Z., Ciloglu, A., Sursal, N., Yilmaz, E., Gonulalan, Z. & Inci, A. (2020). Investigation of Anisakis larvae in different products of ready-to-eat fish meat and imported frozen fish in Turkey. International Journal of Food Microbiology, 333, 108829.
  • Umehara, A., Kawakami, Y., Araki, J. & Uchida, A. (2007). Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitology International, 56(3), 211-215.
  • Zhu, X., Gasser, R.B., Podolska, M. & Chilton, N.B. (1998). Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. International Journal for Parasitology, 28(12), 1911-1921.

Türk Süpermarketlerindeki İthal Balıklarda Zoonotik Anisakis Larvalarının Varlığına İlişkin Devam Eden Veriler: Dondurulmuş Atlantik Uskumru (Scomber Scombrus) ve Füme Atlantik Somonu (Salmo Salar)

Year 2023, Volume: 8 Issue: 2, 146 - 150, 30.06.2023

Gökmen Zafer Pekmezci Ertan Emek Onuk Banu Yardımcı

https://doi.org/10.35229/jaes.1259143
Cited By: 1

Abstract

Anisakis pegreffii ve A. simplex sensu stricto (s.s.) türleri insan anisakiasisine neden olan ana etiyolojik ajanlardır. Bu çalışmada Anisakis larvalarının varlığı 2018-2019 yılları arasında FAO 27 avcılık sahasında avlanıp ve sonrasında Türkiye'ye ithal edilen derin dondurulmuş bütün Atlantik uskumru (Scomber scombrus) ve tütsülenmiş Norveç çiftlik Atlantik somon filetolarında (Salmo salar) pepsin sindirim yöntemine göre araştırılması amaçlanmıştır. Toplam 100 bütün Atlantik uskumru ve 180 Atlantik somon filetosu Türk süpermarketlerinden örneklendi. Füme Atlantik somon filetolarında Anisakis larvası tespit edilmedi. Uskumruda toplam 827 Anisakis larvası bulunmuş olup, larvaların enfeksiyon oranı %68 (68/100) olarak saptanmıştır. Uskumruda Anisakis larvalarının ortalama yoğunluk (mI) ve ortalama bolluk (mA) değerleri sırasıyla 13,1 ve 8,2 idi. Anisakis larvalarının %95,28'i (788/827) karın boşluğu/iç organlarında bulunurken, larvaların %4,72'si (39/827) kaslarda bulunmuştur. Anisakis larvalarının uskumrunun karın boşluğu/iç organları ve kasındaki enfeksiyon oranı ve mI değerleri sırasıyla %63,0 (63/100) ve %42,0 (42/100) ile 12.5 ve 0.9 idi. Çalışmada örneklenen 100 larva moleküler olarak ITS RFLP desenlerine göre teşhis edildi. Araştırmada 99 (%99,0) larva A. simplex (s.s.) ve 1 (%1,0) larva A. pegreffii olarak teşhis edildi. Sonuç olarak Türk tüketiciler için tütsülenmiş çiftlik Atlantik somonunda anisakiasis riski düşüktür veya hiç yoktur. İthal Atlantik uskumru filetolarındaki zoonotik Anisakis türü larvalarının %42,0 oranındaki yaygınlığı Türk tüketicilerde anisakiasis veya alerji açısından halk sağlığı riski oluşturabilir.

Keywords

FAO 27 ITS gen bölgesi Parazit PCR‒RFLP Zoonoz

Project Number

PYO.VET.1901.18.002

References

  • Angot, V. & Brasseur, P. (1993). European farmed Atlantic salmon (Salmo salar L.) are safe from anisakid larvae. Aquaculture, 118(3-4), 339-344.
  • Audicana, M.T. & Kennedy, M.W. (2008). Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clinical Microbiology Reviews, 21(2), 360-79.
  • Aydin, C. & Pekmezci, G.Z. (2023). Molecular identification and infection levels of Anisakis species (Nematoda: Anisakidae) in the red scorpionfish Scorpaena scrofa (Scorpaenidae) from the Aegean Sea. Parasitology International, 92, 102691.
  • Bao, M., Pierce, G.J., Pascual, S., González-Muñoz, M., Mattiucci, S., Mladineo, I., Cipriani, P., Bušelić, I. & Strachan, N.J. (2017). Assessing the risk of an emerging zoonosis of worldwide concern: anisakiasis. Scientific Reports, 7(1), 43699.
  • Berland, B. (1961). Nematodes from some Norwegian marine fishes. Sarsia, 2(1), 1–50.
  • Caballero, M.L. & Moneo, I. (2004). Several allergens from Anisakis simplex are highly resistant to heat and pepsin treatments. Parasitology Research, 93, 248- 251.
  • 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 polymerasechain-reaction-based restriction fragment length polymorphism. International Journal for Parasitology, 30(2), 223-226.
  • European Food Safety Authority (EFSA), (2010). Scientific opinion on risk assessment of parasites in fishery products. EFSA Journal, 8(4), 1543.
  • Gómez-Mateos, M., Merino-Espinosa, G., Corpas-López, V., Valero-López, A. & Martín-Sánchez, J. (2020). A multi-restriction fragment length polymorphism genotyping approach including the beta-tubulin gene as a new differential nuclear marker for the recognition of the cryptic species Anisakis simplex s.s. and Anisakis pegreffii and their hybridization events. Veterinary Parasitology, 283, 109162.
  • González, M.Á.P., Cavazza, G., Gustinelli, A., Caffara, M. & Fioravanti, M. (2020). Absence of anisakis nematodes in smoked farmed Atlantic salmon (Salmo salar) products on sale in European countries. Italian Journal of Food Safety, 9(4), 8615.
  • Levsen, A., Cipriani, P., Mattiucci, S., Gay, M., Hastie, L. C., MacKenzie, K., Graham, J.P., Cecilie, S., Svanevik, C.S., Højgaard, D.P., Nascetti, G., González, A.F. & Pascual, S. (2018). Anisakis species composition and infection characteristics in Atlantic mackerel, Scomber scombrus, from major European fishing grounds-reflecting changing fish host distribution and migration pattern. Fisheries Research, 202, 112-121.
  • Levsen, A. & Maage, A. (2016). Absence of parasitic nematodes in farmed, harvest quality Atlantic salmon (Salmo salar) in Norway-Results from a large scale survey. Food Control, 68, 25-29.
  • Llarena-Reino, M., Piñeiro, C., Antonio, J., Outeriño, L., Vello, C., González, Á.F. & Pascual, S. (2013). Optimization of the pepsin digestion method for anisakids inspection in the fishing industry. Veterinary Parasitology, 191(3-4), 276-283.
  • Lunestad, B.T. (2003). Absence of nematodes in farmed Atlantic salmon (Salmo salar L.) in Norway. Journal of Food Protection, 66(1), 122-124.
  • Madrid, E., Gil, F., García, M., Debenedetti, Á.L., Trelis, M. & Fuentes, M.V. (2016). Potential risk analysis of human anisakiasis through the consumption of mackerel, Scomber scombrus, sold at Spanish supermarkets. Food Control, 66, 300-305.
  • Mattiucci, S., Cipriani, P., Levsen, A., Paoletti, M. & Nascetti, G. (2018). Molecular epidemiology of Anisakis and anisakiasis: an ecological and evolutionary road map. Advances in Parasitology, 99, 93-263.
  • Mattiucci, S., Cipriani, P., Webb, S.C., Paoletti, M., Marcer, F., Bellisario, B., Gibsoni, D.I. & Nascetti, G. (2014). Genetic and morphological approaches distinguish the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). The Journal of Parasitology, 100(2), 199-214.
  • Mattiucci, S., Colantoni, A., Crisafi, B., Mori‐Ubaldini, F., Caponi, L., Fazii, P., Nascetti, G. & Bruschi, F. (2017). Ig E sensitization to Anisakis pegreffii in Italy: Comparison of two methods for the diagnosis of allergic anisakiasis. Parasite Immunology, 39(7), e12440.
  • Mattiucci, S., Fazii, P., De Rosa, A., Paoletti, M., Megna, A. S., Glielmo, A., De Angelis, M., Costa, A., Meucci, C., Calvaruso, V., Sorrentini, I., Palma, G., Bruschi, F. & Nascetti, G. (2013). Anisakiasis and gastroallergic reactions associated with Anisakis pegreffii infection, Italy. Emerging Infectious Diseases, 19(3), 496.
  • Mattiucci, S., Paoletti, M., Borrini, F., Palumbo, M., Palmieri, R. M., Gomes, V., Casati, A. & Nascetti, G. (2011). First molecular identification of the zoonotic parasite Anisakis pegreffii (Nematoda: Anisakidae) in a paraffin-embedded granuloma taken from a case of human intestinal anisakiasis in Italy. BMC Infectious Diseases, 11, 82.
  • Mattiucci, S., Paoletti, M., Colantoni, A., Carbone, A., Gaeta, R., Proietti, A., Frattaroli, S., Fazii, P., Bruschi, F. & Nascetti, G. (2017). Invasive anisakiasis by the parasite Anisakis pegreffii (Nematoda: Anisakidae): diagnosis by real-time PCR hydrolysis probe system and immunoblotting assay. BMC Infectious Diseases, 17, 530.
  • Moneo, I., Caballero, M.L., González-Muñoz, M., Rodríguez-Mahillo, A.I., Rodríguez-Perez, R. & Silva, A. (2005). Isolation of a heat-resistant allergen from the fish parasite Anisakis simplex. Parasitology Research, 96, 285-289.
  • Pekmezci, G.Z., Onuk, E.E., Bolukbas, C.S., Yardimci, B., Gurler, A.T., Acici, M. & Umur, S. (2014). Molecular identification of Anisakis species (Nematoda: Anisakidae) from marine fishes collected in Turkish waters. Veterinary Parasitology, 201(1-2), 82-94.
  • Pekmezci, G.Z. (2014). Occurrence of Anisakis simplex sensu stricto in imported Atlantic mackerel (Scomber scombrus) represents a risk for Turkish consumers. International Journal of Food Microbiology, 185, 64-68.
  • Petter, A.J. & Maillard, C. (1988). Larves d’ascarides parasites de poissons en Méditerranée occidentale. Bulletin du Muséum National d'histoire Naturelle, 10(sect. A), 347-369.
  • Reiczigel, J., Marozzi, M., Fábián, I. & Rózsa, L. (2019). Biostatistics for parasitologists – a primer to Quantitative Parasitology. Trends in Parasitology, 35 (4), 277-281.
  • Simsek, E., Pekmezci, G. Z., Yildirim, A., Duzlu, O., Onder, Z., Ciloglu, A., Sursal, N., Yilmaz, E., Gonulalan, Z. & Inci, A. (2020). Investigation of Anisakis larvae in different products of ready-to-eat fish meat and imported frozen fish in Turkey. International Journal of Food Microbiology, 333, 108829.
  • Umehara, A., Kawakami, Y., Araki, J. & Uchida, A. (2007). Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitology International, 56(3), 211-215.
  • Zhu, X., Gasser, R.B., Podolska, M. & Chilton, N.B. (1998). Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. International Journal for Parasitology, 28(12), 1911-1921.
There are 29 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Gökmen Zafer Pekmezci 0000-0002-7791-1959

Ertan Emek Onuk 0000-0001-7643-046X

Banu Yardımcı 0000-0001-7232-554X

Project Number PYO.VET.1901.18.002
Early Pub Date June 13, 2023
Publication Date June 30, 2023
Submission Date March 3, 2023
Acceptance Date April 3, 2023
Published in Issue Year 2023 Volume: 8 Issue: 2

Cite

APA Pekmezci, G. Z., Onuk, E. E., & Yardımcı, B. (2023). Ongoing Data from Presence of Zoonotic Anisakis Larvae in Imported Fish in Turkish Supermarkets: Frozen Atlantic Mackerel (Scomber Scombrus) and Smoked Atlantic Salmon (Salmo Salar). Journal of Anatolian Environmental and Animal Sciences, 8(2), 146-150. https://doi.org/10.35229/jaes.1259143

Cited By

Paraziter Balık Zoonozları
Acta Aquatica Turcica
https://doi.org/10.22392/actaquatr.1310942
 Download Cover Image


13221            13345           13349              13352              13353              13354          13355    13356   13358   13359   13361     13363   13364                crossref1.png            
         Paperity.org                  13369           EBSCOHost Logo        Scilit logo                  
JAES/AAS-Journal of Anatolian Environmental and Animal Sciences/Anatolian Academic Sciences&Anadolu Çevre ve Hayvancılık Dergisi/Anadolu Akademik Bilimler-AÇEH/AABcabi-logo-black.svg