Abstract
This study investigates the occurrence of anisakids and raphidascarids in commercial fish from Balearic Sea (Western Mediterranean). A total of 335 fish including 19 black anglerfish (Lophius budegassa), 33 white anglerfish (L. piscatorius), 129 European hake (Merluccius merluccius), 30 red mullet (Mullus barbatus), and 124 striped mullet (M. surmuletus) were examined using enzymatic digestion. A total of 948 nematode larvae were isolated (prevalence 52.53%) being the highest prevalence observed in striped mullet. Forty-six larvae were identified using molecular analyses which included PCR and sequencing of the 629-bp fragment of mitochondrial cox2 gene region. Anisakis pegreffii (80.43%), A. physeteris (8.69%), Hysterothylacium fabri (6.52%), and A. simplex (4.35%) were detected based on molecular analyses of larvae. Total nematode prevalence was positively correlated with weight, length, condition factor, and maturity stage of the host and also with fishing ground depth. Statistical differences between total nematode prevalence and geographical sector of capture were observed when fishing hauls were grouped according to the abundance of sperm whales or common bottlenose dolphins. The results also corroborate that fishing water depth may play an important role in anisakid and raphidascarid parasitization.
Similar content being viewed by others
References
Acosta J, Canals M, Carbó A, Muñoz A, Urgeles R, Muñoz-Martín A, Uchupi E (2004) Sea floor morphology and Plio-Quaternary sedimentary cover of the Mallorca Channel, Balearic Islands, western Mediterranean. Mar Geol 206(1–4):165–179
Adroher FJ, Valero A, Ruiz-Valero J, Iglesias L (1996) Larval anisakids (Nematoda: Ascaridoidea) in horse mackerel (Trachurus trachurus) from the fish market in Granada (Spain). Parasitol Res 82:253–256
Akmirza A (2013) Parasitic nematodes of fish in the coastal waters of Gökçeada. Turk Parazit Derg 37:199–202
Angelucci G, Meloni M, Merella P, Sardu F, Madeddu S, Marrosu R, Salati F (2011) Prevalence of Anisakis spp. and Hysterothylacium spp. larvae in teleosts and cephalopods sampled from waters off Sardinia. J Food Prot 74(10):1769–1775
Arcangeli A, Campana I, Bologna MA (2017) Influence of seasonality on cetacean diversity, abundance, distribution and habitat use in the western Mediterranean Sea: implications for conservation. Aquat Conserv Mar Freshw Ecosyst:1–16
Audicana MT, Kennedy MW (2008) Anisakis simplex: from obscure infectious worm to inducer of immune hypersensitivity. Clin Microbiol Rev 21(2):360–379
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583
Butt AA, Aldridge KE, Sanders CV (2004) Infections related to the ingestion of seafood. Part II: parasitic infections and food safety. Lancet Infect Dis 4:294e300
Cipriani P, Sbaraglia GL, Palomba M, Giulietti L, Bellisario B, Bušelić I, Mladineo I, Cheleschi R, Nascetti G, Mattiucci S (2018a) Anisakis pegreffii (Nematoda: Anisakidae) in the European anchovy Engraulis encrasicolus, from the Mediterranean Sea: fishing ground as a predictor of the parasite distribution. Fish Res 202:59–68
Cipriani P, Sbaraglia GL, Paoletti M, Giulietti L, Bellisario B, Palomba ML, Bušelić I, Mladineo I, Nascetti G, Mattiucci S (2018b) The Mediterranean European hake, Merluccius merluccius: detecting drivers influencing the Anisakis spp. larvae distribution. Fish Res 202:79–89
Codex Alimentarius Commission (2004) Standard for salted Atlantic herring and salted sprat. Codex Stan 244-2004:1–8
Costa A, Graci S, Cammilleri G, Drussilla Buscemi M, Collura R, Vella A, Ferrantelli V (2018) Molecular identification of Hysterothylacium spp. in fishes from the Southern Mediterranean Sea (Southern Italy). J Parasitol 104(4):398–406
De Liberato C, Bossù T, Scaramozzino P, Nicolini G, Ceddia P, Mallozzi S, Cavallero S, D’Amelio S (2013) Presence of anisakid larvae in the European anchovy, Engraulis encrasicolus, fished off the Tyrrhenian coast of central Italy. J Food Prot 76:1643–1648
Debenedetti AL, Madrid E, Fuentes MV (2013) Study of helminth parasites in the red mullet, Mullus barbatus, from the Mediterranean Sea and acquired in greater València, Spain. Rev Ibero-Latinoam Parasitol 72(2):118–123
Del Rey Moreno A, Valero A, Mayorga C, Gómez B, Torres MJ, Hernández J, Ortiz M, Lozano-Maldonado J (2006) Sensitization to Anisakis simplex s.l. in a healthy population. Acta Trop 97:265–269
EFSA (European Food Safety Authority) (2010) Scientific opinion on risk assessment of parasites in fishery products. EFSA J 8(4):1543 Retrieved from http://www.efsa.europa.eu/en/efsajournal/doc/1543.pdf (Accessed on 28/05/2018)
EU Regulation (EC) (2005) No. 2075/2005 of the European Parliament and of the Council of 5 December 2005 laying down specific rules on official controls for Trichinella in meat. Official J Eur Union Legislation 338:60–82
EU Regulation (EC) (2008) No. 199/2008 of the European Parliament and of the Council of 25 February 2008 concerning the establishment of a Community framework for the collection, management and use of data in the fisheries sector and support for scientific advice regarding the Common Fisheries Policy. Official J Eur Union Legislation 60:1–12
Farjallah S, Slimane BB, Busi M, Paggi L, Amor N, Blel H, Said K, D’Amelio S (2008) Occurrence and molecular identification of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitol Res 102:371–379
Ferrer-Maza D, Muñoz M, Lloret J, Faliex E, Vila S, Sasal P (2014a) Health and reproduction of red mullet, Mullus barbatus, in the western Mediterranean Sea. Hydrobiologia 753:189–204
Ferrer-Maza D, Lloret J, Muñoz M, Faliex E, Vila S, Sasal P (2014b) Parasitism, condition and reproduction of the European hake (Merluccius merluccius) in the northwestern Mediterranean Sea. ICES J Mar Sci 71:1088–1099
Ferrer-Maza D, Lloret J, Muñoz M, Falex E, Vila S, Sasal P (2016) Links between parasitism, energy reserves and fecundity of European anchovy, Engraulis encrasicolus, in the northwestern Mediterranean Sea. Conserv Physiol 4:1–13
Fumarola L, Monno R, Lerardi E, Rizzo G, Giannelli G, Lalle M, Pozio E (2009) Anisakis pegreffii etiological agent of gastric infections in two Italian women. Foodborne Pathog Dis 6(9):1157–1159
Gaglio G, Battaglia P, Costa A, Cavallaro M, Cammilleri G, Graci S, Buscemi MD, Ferrantelli V, Andaloro F, Marino F (2018) Anisakis spp. larvae in three mesopelagic and bathypelagic fish species of the central Mediterranean Sea. Parasitol Int 67(1):23–28
García-Pérez JC, Rodríguez-Pérez R, Ballestero A, Zuloaga J, Fernández-Puntero B, Arias-Díaz J, Caballero ML (2015) Previous exposure to the fish parasite Anisakis as a potential risk factor for gastric or colon adenocarcinoma. Medicine 94(40):e1699
Gonzalvo J, Valls M, Cardona L, Aguilar A (2008) Factors determining the interaction between common bottlenose dolphins and bottom trawlers off the Balearic Archipelago (western Mediterranean Sea). J Exp Mar Biol Ecol 367:47–52
Hassani MM, Kerfouf A, Boutiba Z (2015) Checklist of helminth parasites of striped red mullet, Mullus surmuletus (Linnaeus, 1758) (Perciformes: Mullidae), caught in the bay of Kristel, Algeria (western Mediterranean). Check List 11(1):1504. https://doi.org/10.15560/11.1.1504
Jeon CH, Setyobudi E, Kim JH (2016) Occurrence and molecular identification of anisakid nematodes isolated from Pacific cod (Gadus macrocephalus) caught off Korea. Food Control 69:100–107
Kassem HH, Bowashi SM (2015) Prevalence of anisakid nematode larvae infecting some marine fishes from the Libyan coast. J Egypt Soc Parasitol 45(3):609–616
Kijewska A, Dzido J, Shukhgalter O, Rokicki J (2009) Anisakid parasites of fishes caught on the African shelf. J Parasitol 95:639–645
Klimpel S, Palm HV (2011) Anisakid nematode (Ascaridoidea) life cycles and distribution: increasing zoonotic potential in the time of climate change? In: Mehlhorn H (ed) Progress in parasitology, parasitology research monographs 2, Heidelberg, pp 201–222
Levsen A, Svanevika CS, Cipriani P, Mattiucci S, Gayd M, Hastiee LC, Bušelićg I, Mladineo I, Karlh H, Ostermeyerh U, Buchmann K, Højgaardk DP, González AF, Pascual S, Pierce GJ (2018) Survey of zoonotic nematodes of commercial key fish species from major European fishing grounds-introducing the FP7 PARASITE exposure assessment study. Fish Res 202:4–21
Llarena-Reino M, Piñeiro C, Antonio J, Outeriño L, Vello C, González AF, Pascual S (2013) Optimization of the pepsin digestion method for anisakids inspection in the fishing industry. Vet Parasitol 191:276–283
Lymbery J, Cheah FY (2007) Anisakid nematodes and anisakiasis. In: Murrell KD, Fried B (eds) Food borne parasitic zoonosis: fish and plant borne parasites. Springer, New York, pp 185–207
Mateu P, Nardi V, Fraija-Fernandez N, Mattiucci S, Gil de Sola L, Raga JA, Fernandez M, Aznar FJ (2015) The role of lantern fish (Myctophidae) in the life-cycle of cetacean parasites from western Mediterranean waters. Deep Sea Res Part I Oceanogr Res Pap 95:115–121
Mattiucci S, Abaunza P, Ramadori L, Nascetti G (2004) Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock recognition. J Fish Biol 65:495–510
Mattiucci S, Paoletti M, Borrini F, Palumbo M, Macarone PR, Gomes V, Casati A, Nascett 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 Infect Dis 11:82
Mattiucci S, Fazii P, De Rosa A, Paoletti M, Megna AS, 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. Emerg Infect Dis 19:496–499
Mattiucci S, Cimmaruta R, Cipriani P, Abaunza P, Bellisario P, Nascetti G (2015) Integrating Anisakis spp. parasites data and host genetic structure in the frame of a holistic approach for stock identification of selected Mediterranean Sea fish species. Parasitology 142:90–108
Mattiucci S, Cipriani P, Paoletti M, Levsen A, Nascetti G (2017) Reviewing biodiversity and epidemiological aspects of anisakid nematodes from the North East Atlantic Ocean. J Helminthol 91(4):422–439
MEDITS Handbook (2017) International bottom trawl survey in the Mediterranean. Hadbook V5. Edited by IFREMER. http://www.ifremer.fr/docelec/default-en.jsp
Mladineo I, Popović M, Drmić-Hofman I, Poljak V (2016) A case report of Anisakis pegreffii (Nematoda, Anisakidae) identified from archival paraffin sections of a Croatian patient. BMC Infect Dis 16:42
Murphy TM, Berzano M, O'Keeffe SM, Cotter DM, McEvoy SE, Thomas KA, Maoiléidigh NP, Whelan KF (2010) Anisakid larvae in Atlantic salmon (Salmo salar L.) grilse and post-smolts: molecular identification and histopathology. J Parasitol 96(1):77–82
Nadler SA, Hudspeth DS (2000) Phylogeny of the Ascaridoidea (Nematoda: Ascaridida) based on three genes and morphology: hypotheses of structural and sequence evolution. J Parasitol 86(2):380–393
Nieuwenhuizen NE, Lopata AL (2013) Anisakis a food-borne parasite that triggers allergic host defences. Int J Parasitol 43:1047–1057
Pekmezci GZ, Yardimci B, Onuk EE, Umur S (2014a) Molecular characterization of Hysterothylacium fabri (Nematoda: Anisakidae) from Zeus faber (Pisces: Zeidae) caught off the Mediterranean coasts of Turkey based on nuclear ribosomal and mitochondrial DNA sequences. Parasitol Int 63:127–131
Pekmezci GZ, Onuk EE, Bolukbas CS, Yardimci B, Gurler AL, Acici M, Umur S (2014b) Molecular identification of Anisakis species (Nematoda: Anisakidae) from marine fishes collected in Turkish waters. Vet Parasitol 201:82–94
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
Rello FJ, Adroher FJ, Benítez R, Valero A (2009) The fishing area as a possible indicator of the infection by anisakids in anchovies (Engraulis encrasicolus) from southwestern Europe. Int J Food Microbiol 129(3):277–281
Rendell L, Simiao S, Brotons JM, Airoldi S, Fasano D, Gannier A (2014) Abundance and movements of sperm whales in the western Mediterranean basin. Aquat Conserv Mar Freshw Ecosyst 24(1):31–40
Ricker WE (1975) Computation and interpretation of biological statistics of fish population. Bull Fish Res Board Can 191:1–382
Serracca L, Cencetti E, Battistini R, Rossini I, Prearo M, Pavoletti E, Fioravanti ML, Righetti M, Di Donfrancesco BD, Ercolini C (2013) Survey on the presence of Anisakis and Hysterothylacium larvae in fishes and squids caught in Ligurian Sea. Vet Parasitol 196:547–551
Shamsi S (2014) Recent advances in our knowledge of Australian anisakid nematodes. Int J Parasitol Parasites Wildl 3(2):178–187
Sharif MA, Negm-Eldin MM (2013) Occurrence of Anisakis sp. larvae in Merluccius merluccius (Teleostei, Gadiformes) of the Libyan north coast and evaluation of its zoonotic potential. Trav Inst Sci Rabat sér Zool 49:29–32
Skarstein F, Folstad I, Liljedal S (2001) Whether to reproduce or not: immune suppression and costs of parasites during reproduction in the Arctic charr. Can J Zool 79(2):271–278
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729
Tantanasi J, Diakou A, Tamvakis A, Batjakas IE (2012) Anisakis spp. burden in Trachurus trachurus. Helminthologia 49:16–20
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple; sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acid Res 22(22):4673–4680
Umehara A, Kawakami Y, Araki J, Uchida A (2007) Molecular identification of the etiological agent of the human anisakiasis in Japan. Parasitol Int 56:211–215
Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannone AA, Colom-Llavina MM, Nascetti G (2006) Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozyme data. J Parasitol 92(1):156–166
Valero A, López-Cuello M, Benítez R, Adroher FJ (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
Acknowledgements
The authors wish to thank the Spanish Institute of Oceanography, to all participants, in the cruise MEDIT GSA05 on board R/V “Miguel Oliver” as well as to Beatriz Guijarro, regional coordinator of the MEDIT program, for all help and support provided during sampling.
Author information
Authors and Affiliations
Corresponding author
Additional information
Section Editor: Shokoofeh Shamsi
Electronic supplementary material
ESM 1
(DOCX 32 kb)
Rights and permissions
About this article
Cite this article
Barcala, E., Ramilo, A., Ortega, N. et al. Occurrence of Anisakis and Hysterothylacium larvae in commercial fish from Balearic Sea (Western Mediterranean Sea). Parasitol Res 117, 4003–4012 (2018). https://doi.org/10.1007/s00436-018-6110-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-018-6110-5