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)
Yıl 2023,
Cilt: 8 Sayı: 2, 146 - 150, 30.06.2023
Gökmen Zafer Pekmezci
,
Ertan Emek Onuk
,
Banu Yardımcı
Öz
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.
Destekleyen Kurum
Ondokuz Mayıs Üniversitesi Bilimsel Araştırma Projeleri Koordinasyon Birimi
Proje Numarası
PYO.VET.1901.18.002
Teşekkür
This study was supported by the Scientific Research Council of Ondokuz Mayis University, Samsun, Turkey, under project no PYO.VET.1901.18.002
Kaynakça
- 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)
Yıl 2023,
Cilt: 8 Sayı: 2, 146 - 150, 30.06.2023
Gökmen Zafer Pekmezci
,
Ertan Emek Onuk
,
Banu Yardımcı
Öz
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.
Proje Numarası
PYO.VET.1901.18.002
Kaynakça
- 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.