Effect of Anisakis pegreffii (Nematoda: Anisakidae) on Biochemical and Haematological Characteristics of Chub Mackerel (Scomber japonicus Houttuyn, 1782) Caught in the Dardanelles at Çanakkale, Türkiye

Year 2022, Volume: 5 Issue: Special Issue, 55 - 62, 28.10.2022

Ekrem Şanver Çelik , Rıdvan Erdem Kanat , Pınar Dermancı Dilek Kahraman Yılmaz , Emre Turgay , Süheyla Karataş Steınum , Sevdan Yılmaz

https://doi.org/10.46384/jmsf.1140211

Cited By: 1

Abstract

Chub mackerel (Scomber japonicus Houttuyn, 1782) were obtained from the commercial fishermen in Çanakkale, Turkey, in July, 2017. We examined a total of 40 fish (20 non-infested and 20 infested) and assessed the biometric indices, haematological parameters and serum biochemical variables. The hepatosomatic index and gonadosomatic index of infested chub mackerel fish were lower than those of non-infested fish. Blood haematocrit ratio and haemoglobin concentration in naturally parasite-infested chub mackerel fish were significantly lower than those in non-infested fish. However, white blood cell counts of the parasite-infested chub mackerel fish were higher than those of healthy ones. Serum total protein, globulin, glucose, cholesterol, triglyceride, urea, chlorine and iron levels in naturally parasite-infested chub mackerel fish were significantly lower than those in non-infested fish. Moreover, serum lactate dehydrogenase, aspartate aminotransferase, alkaline phosphatase and alanine aminotransferase activities of the parasite-infested chub mackerel fish were higher than those in healthy ones. Therefore, observed variations in haematological parameters, serum biochemical variables and biometric indices influenced by the parasite, A. pegreffii, may potentially increase sensitivity of the chub mackerel, Scomber japonicus, to diseases and environmental conditions.

Keywords

Worm, Parasite, Anisakiasis, Health, Biometric Indices, 18S rRNA

Thanks

We would like to thank the commercial fishermen. Ridvan Erdem Kanat and Pınar Dermanci are PhD students of YÖK 100/2000 project.

Çanakkale Boğazı'ndan Yakalanan Kolyoz’un (Scomber japonicus Houttuyn, 1782) Biyokimyasal ve Hematolojik Karakteristikleri Üzerine Anisakis pegreffii (Nematoda: Anisakidae)’nin Etkisi

Abstract

Kolyoz (Scomber japonicus Houttuyn, 1782) Temmuz 2017'de Çanakkale, Türkiye'deki ticari balıkçılardan elde edildi. Toplam 40 balığın (20 parazitsiz, 20 parazitli) biyometrik indeksleri, hematolojik parametreleri ve serum biyokimyasal değişkenleri incelendi. Parazitli kolyoz balıklarının hepatosomatik indeksi ve gonadosomatik indeksi, parazitsiz balıklardan daha düşüktü. Doğal olarak parazitle istila edilmiş kolyoz balıklarında kan hematokrit oranı ve hemoglobin konsantrasyonu, parazitsiz balıklardan önemli ölçüde daha düşüktü. Bununla birlikte, parazitli kolyoz balıklarının beyaz kan hücresi sayıları sağlıklı olanlardan daha yüksekti. Doğal olarak parazitli kolyoz balıklarında serum total protein, globulin, glikoz, kolesterol, trigliserit, üre, klor ve demir seviyeleri, parazitsiz balıklardan önemli ölçüde daha düşüktü. Ayrıca, parazitli kolyoz balıklarının serum laktat dehidrojenaz, aspartat aminotransferaz, alkalin fosfataz ve alanin aminotransferaz aktiviteleri sağlıklı olanlardan daha yüksekti. Bu bulgular ışığında, parazitin kolyoz, Scomber japonicus’un hematolojik parametreler, serum biyokimyasal değişkenler ve biyometrik indeksler de meydana getirdiği değişimlerin balığı farklı hastalıklara ve/veya çevresel koşullara karşı daha duyarlı hale getirebileceği söylenebilir.

Keywords

Kurt, Parazit, Anisakiasis, Sağlık, Biyometrik İndeksler, 18S rRNA

References

• Aibinu, I. E., Smooker, P. M., & Lopata, A. L. (2019). Anisakis Nematodes in Fish and Shellfish- from infection to allergies. International Journal for Parasitology: Parasites and Wildlife, 9,384–393. https://doi.org/10.1016/j.ijppaw.2019.04.007
• Bichi, A., & Dawaki, S. (2010). A survey of ectoparasites on the gills, skin and fins of Oreochromis niloticus at Bagauda fish farm, Kano, Nigeria. Bayero Journal of Pure and Applied Sciences, 3(1), 83–86. doi: 10.4314/bajopas.v3i1.58720
• Blaxhall, P. C., & Daisley, K. W. (1973). Routine haematological methods for use with fish blood. Journal of fish biology, 5(6), 771-781. doi: 10.1111/j.1095-8649.1973.tb04510.x
• Campana-Rouget, Y., & Biocca, E. (1955). Une nouvelle espèce d’Anisakis chez un phoque mediterranéen. Annales de Parasitologie Humaine et Comparée, 30(5-6), 477-480.
• Campbell, T. W. 2004. Clinical chemistry of fish and amphibians. Pages 499–517 in M. A. Thrall, D. C. Baker, T.W. Campbell, D. DeNicola, M. J. Fettman, E. D. Lassen, A. Rebar, and G. Weiser, editors. Veterinary hematology and clinical chemistry: text and clinical case presentations. Lippincott Williams and Wilkins, Philadelphia.
• Collette, B. B., & Nauen, C. E. (1983). Scombrids of the world: an annotated and illustrated catalogue of tunas, mackerels, bonitos, and related species known to date. v. 2.
• Çelik, E. S., & Aydin, S. (2006). Effect of Trachelobdella lubrica (Hirudinea: Piscicolidae) on biochemical and haematological characteristics of black scorpion fish (Scorpaena porcus, Linnaeus 1758). Fish Physiology and Biochemistry, 32(3), 255–260. doi: 10.1007/s10695-006-9003-y
• Datta, N., Kar, P. K., & Saha, S. K. (2022). Primary stress response and biochemical profile of Labeo rohita (Hamilton, 1822) experimentally parasitized with Argulus bengalensis (Ramakrishna, 1951). Journal of Fish Biology.
• Devevey, G., Niculita-Hirzel, H., Biollaz, F., Yvon, C., Chapuisat, M., & Christe, P. (2008). Developmental, metabolic and immunological costs of flea infestation in the common vole. Functional Ecology, 22(6), 1091–1098. doi:10.1111/j.1365-2435.2008.01493.x
• Hadziavdic, K., Lekang, K., Lanzen, A., Jonassen, I., Thompson, E. M., & Troedsson, C. (2014). Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PloS one, 9(2), e87624. doi: 10.1371/journal.pone.0087624
• Hall, T. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symp. Ser. (Vol. 41, pp. 95-98).
• Kundu, I., Bandyopadhyay, P. K., Mandal, D. R., & Gürelli, G. (2016). Study of pathophysiological effects of the nematode parasite Eustrongylides sp. on freshwater fish Channa punctatus by hematology, serum biochemical, and histological studies. Türkiye Parazitolojii Dergisi, 40(1), 42. doi: 10.5152/tpd.2016.4551
• Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson T.J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23(21), 2947-2948. doi: 10.1093/bioinformatics/btm404
• Macchioni, F., Tedesco, P., Cocca, V., Massaro, A., Sartor, P., Ligas, A., Pretti, C., Monni, G., Cecchi, F., & Caffara, M. (2021). Anisakid and Raphidascaridid parasites in Trachurus trachurus: infection drivers and possible effects on the host’s condition. Parasitology Research, 120(9), 3113–3122. doi:10.1007/s00436-021-07200-0
• Manna, S., & Naskar, S. (2021). Impact of Thelohanellus mrigalae tripathi, 1952 on Cirrhinus mrigala: prevalence, histopathological and haematological alterations. Uttar Pradesh Journal of Zoology, 42(9), 41-49. doi: 10.13140/RG.2.2.25174.57924
• Maqbool, A., & Ahmed, I. (2016). Haematological response of snow barbell, Schizothorax plagiostomus Heckel, naturally infected with a new Trypanosoma species. Journal of Parasitic Diseases, 40(3), 791-800. doi: 10.1007/s12639-014-0580-x
• Martins, M. L., Tavares-Dias, M., Fujimoto, R. Y., Onaka, E. M., & Nomura, D. T. (2004). Haematological alterations of Leporinus macrocephalus (Osteichtyes: Anostomidae) naturally infected by Goezia leporini (Nematoda: Anisakidae) in fish pond. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 56(5), 640–646. doi:10.1590/s0102-09352004000500011
• Mattiucci, S., & D’Amelio, S. (2014). Anisakiasis. In: Bruschi, F. (eds) Helminth Infections and their Impact on Global Public Health (pp. 325-365). Springer, Vienna.
• Mattiucci, S., Farina, V., Campbell, N., MacKenzie, K., Ramos, P., Pinto, A. L., Abaunza, P., & Nascetti, G. (2008). Anisakis spp. larvae (Nematoda: Anisakidae) from Atlantic horse mackerel: Their genetic identification and use as biological tags for host stock characterization. Fisheries Research, 89(2), 146–151. doi: 10.1016/j.fishres.2007.09.032
• Mattiucci, Simonetta, Cipriani, P., Levsen, A., Paoletti, M., & Nascetti, G. (2018). Molecular Epidemiology of Anisakis and Anisakiasis: An Ecological and Evolutionary Road Map. In Advances in Parasitology (1st ed., Vol. 99). Elsevier Ltd. doi: 10.1016/bs.apar.2017.12.001
• McAllister, M., Phillips, N., & Belosevic, M. (2019). Trypanosoma carassii infection in goldfish (Carassius auratus L.): changes in the expression of erythropoiesis and anemia regulatory genes. Parasitology Research, 118(4), 1147-1158. doi: 10.1007/s00436-019-06246-5
• Menconi, V., Pastorino, P., Canola, S., Pavoletti, E., Vitale, N., Scanzio, T., Righetti, M., Mugetti, D., Tomasoni, M., Bona, M. C., & Prearo, M. (2022). Occurrence and spatial variation of Anisakis pegreffii in the Atlantic horse mackerel Trachurus trachurus (Carangidae): A three-year monitoring survey in the western Ligurian Sea. Food Control, 131, 108423. doi: 10.1016/j.foodcont.2021.108423
• Mladineo, I., & Poljak, V. (2014). Ecology and genetic structure of zoonotic Anisakis spp. from Adriatic commercial fish species. Applied and Environmental Microbiology, 80(4), 1281-1290. doi:10.1128/AEM.03561-13
• Nabi, S., Tanveer, S., Ganie, S. A., & Bashir, K. (2022). Oxidative stress, serum biochemistry and DNA damage of Cyprinus carpio communis naturally infected with helminths. International Aquatic Research, 14(1), 13-22. doi: 10.22034/IAR.2022.1937373.1179
• Nikolsky, G.W. (1963). The Ecology of Fishes, Academic Press, London and New York, 352 p.
• Nnabuchi, O., Nwani, C. D., Ochang, S., & Somdare, P. (2015). Effect of parasites on the biochemical and haematological indices of some clariid (Siluriformes) catfishes from Anambra River, Nigeria. International Journal of Fisheries and Aquatic Studies, 3(2), 331–336.
• Ondračková, M., Francová, K., Dávidová, M., Polačik, M., & Jurajda, P. (2010). Condition status and parasite infection of Neogobius kessleri and N. melanostomus (Gobiidae) in their native and non‐native area of distribution of the Danube River. Ecological Research, 25(4), 857-866. doi: 10.1007/s11284-010-0716-0
• Özbakış Beceriklisoy, G., Aştı, C., & Gönenç, B. (2020). Marmara denizi Atlantik uskumrularındaki (Scomber scombrus, Linnaeus 1758) Anisakis spp. enfeksiyonu. Veteriner Hekimler Derneği Dergisi, 91(1), 80–85. doi:10.33188/vetheder.599455
• Özdemir, G., Çelik, E. Ş., Yılmaz, S., Gürkan, M., & Kaya, H. (2016). Histopathology and blood parameters of bogue fish (Boops boops, Linnaeus 1758) parasitized by Ceratothoa oestroides (Isopoda: Cymothoidae). Turkish Journal of Fisheries and Aquatic Sciences, 16(3), 579-590. doi: 10.4194/1303-2712-v16_3_28
• Panjvini, F., Abarghuei, S., Khara, H., & Parashkoh, H. M. (2016). Parasitic infection alters haematology and immunity parameters of common carp, Cyprinus carpio, Linnaeus, 1758. Journal of Parasitic Diseases, 40(4), 1540-1543. doi: 10.1007/s12639-015-0723-8
• 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. doi: 10.1016/j.vetpar.2014.01.005
• Quiazon, K. M. A., Yoshinaga, T., Santos, M. D., & Ogawa, K. (2009). Identification of larval Anisakis spp. (Nematoda: Anisakidae) in Alaska pollock (Theragra chalcogramma) in northern Japan using morphological and molecular markers. Journal of Parasitology, 95(5), 1227-1232. doi: 10.1645/GE-1751.1
• Rastiannasab, A., Afsharmanesh, S., Rahimi, R., & Sharifian, I. (2016). Alternations in the liver enzymatic activity of Common carp, Cyprinus carpio in response to parasites, Dactylogyrus spp. and Gyrodactylus spp. Journal of Parasitic Diseases, 40(4), 1146-1149. doi: 10.1007/s12639-014-0638-9
• Ryberg, M. P., Huwer, B., Nielsen, A., Dierking, J., Buchmann, K., Sokolova, M., Krumme U., & Behrens, J. W. (2022). Parasite load of Atlantic cod Gadus morhua in the Baltic Sea assessed by the liver category method, and associations with infection density and critical condition. Fisheries Management and Ecology, 29(1), 88-99. doi: 10.1111/fme.12516
• Ryberg, M. P., Skov, P. V., Vendramin, N., Buchmann, K., Nielsen, A., & Behrens, J. W. (2020). Physiological condition of Eastern Baltic cod, Gadus morhua, infected with the parasitic nematode Contracaecum osculatum. Conservation Physiology, 8(1), coaa093. doi: 10.1093/conphys/coaa093
• Sakanari, J. A., & McKerrow, J. H. (1989). Anisakiasis. Clinical Microbiology Reviews, 2(3), 278–284. doi:10.1128/CMR.2.3.278
• Santos, M. J., Castro, R., Cavaleiro, F., Rangel, L., & Palm, H. W. (2017). Comparison of anisakid infection levels between two species of Atlantic mackerel (Scomber colias and S. scombrus) off the Atlantic Portuguese coast. Scientia Marina, 81(2), 179-185. doi:10.3989/scimar.04552.26A
• Shameena, S. S., Kumar, K., Kumar, S., Kumari, P., Krishnan, R., Karmakar, S., S., Kumar, H. S., Rajendran, K. V., & Raman, R. P. (2021). Dose-dependent co-infection of Argulus sp. and Aeromonas hydrophila in goldfish (Carassius auratus) modulates innate immune response and antioxidative stress enzymes. Fish & Shellfish Immunology, 114, 199-206. doi: 10.1016/j.fsi.2021.04.026
• Sousa, L. F., Souza, D. C., Coelho, T. A., Tavares-Dias, M., & Correa, L. L. (2020). Morphometric Characterization of Trypanosoma spp. and blood parameters in Pterygoplichthys pardalis (Pisces: Loricariidae) from the Brazilian Amazon. Anais da Academia Brasileira de Ciências, 92.
• Tavares-Dias, M., Martins, M. L., & Kronka, S. D. N. (1999). Evaluation of the haematological parameters in Piaractus mesopotamicus Holmberg (Osteichthyes, Characidae) with Argulus sp. (Crustacea, Branchiura) infestation and treatment with organophosphate. Revista Brasileira de Zoologia, 16(2), 553–555. doi:10.1590/s0101-81751999000200019
• Utuk, A.E., Pişkin, F.Ç. & Balkaya, I. 2012. Molecular detection of Anisakis pegreffii in horse mackerels (Trachurus trachurus) sold for human consumption in Erzurum Province of Turkey. Kafkas Universitesi Veterinerlik Fakültesi Dergisi, 18(2), 303–307. doi:10.9775/kvfd.2011.5466
• White, A., & Fletcher, T. C. (1985). Seasonal changes in serum glucose and condition of the plaice, Pleuronectes platessa L. Journal of Fish Biology, 26(6), 755-764. doi: 10.1111/j.1095-8649.1985.tb04316.x
• Whitehead P.J.P., Bauchot M-L., Hureau J-C., Nielsen J., & Tortonese E. (1984). Fishes of the North-Eastern Atlantic and the Mediterranean. 1, Paris, UNESCO.
• Yardimci, B., Pekmezci, G. Z., & Onuk, E. E. (2014). Pathology and molecular identification of Anisakis pegreffii (Nematoda: Anisakidae) infection in the John Dory, Zeus faber (Linnaeus, 1758) caught in Mediterranean Sea. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 61(3), 233-236. doi: 10.1501/Vetfak_0000002635
• Yılmaz, S. (2018). Balık İmmunolojisi Analiz Yöntemleri/Methods of Fish Immunology Analysis. Paradigma Akademi Kitabevi Yayınları, İSTANBUL, 105 sayfa.
• Yılmaz, S., & Ergün, S. (2012). Effects of garlic and ginger oils on hematological and biochemical variables of sea bass Dicentrarchus labrax. Journal of Aquatic Animal Health, 24(4), 219-224. doi: 10.1080/08997659.2012.711266
• Yılmaz, S., Ergun, S., Şanver Çelik, E., Yigit, M., & Bayizit, C. (2019). Dietary trans‐cinnamic acid application for rainbow trout (Oncorhynchus mykiss): II. Effect on antioxidant status, digestive enzyme, blood biochemistry and liver antioxidant gene expression responses. Aquaculture Nutrition, 25(6), 1207-1217. doi: 10.1111/anu.12935
• Yılmaz, S., Ergün, S., & Çelik, E. Ş. (2016). Effect of dietary spice supplementations on welfare status of sea bass, Dicentrarchus labrax L. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 86(1), 229-237. doi: 10.1007/s40011-014-0444-2
• Yılmaz, S., Sebahattin, E., & Celik, E. (2012). Effects of herbal supplements on growth performance of sea bass (Dicentrarchus labrax): Change in body composition and some blood parameters. Journal of BioScience and Biotechnology, 1, 217-222,
• Zardoya, R., Castilho, R., Grande, C., Favre-Krey, L., Caetano, S., Marcato, S., Krey, G., & Patarnello, T. (2004). Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Molecular Ecology, 13(7), 1785–1798. doi: 10.1111/j.1365-294X.2004.02198.x
• Zhang, Z., Schwartz, S., Wagner, L., & Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 7(1-2), 203-214. doi: 10.1089/10665270050081478