Italian Journal of Food Safety 2017; volume 6:6185 Occurrence of nematodes symptoms such as abdominal pain, diar- of the genus Anisakis in rhea, nausea and vomiting. There have also Correspondence: Carlo Spanu, Department of been reported extra-gastrointestinal or Veterinary Medicine, University of Sassari, Mediterranean and Atlantic fish ectopic forms, where the parasite localizes via Vienna 2, 07100, Sassari, Italy. marketed in Sardinia in different organs following the initial gas- Tel: +39.079.229447 - Fax: +39.079.229458. E-mail: [email protected] trointestinal penetration (larva migrans vis- Daniele Casti, Christian Scarano, ceralis) (Griglio et al., 2012). The exposure Key words: Anisakis pegreffii; Anisakis sim- to the antigens of this parasite can cause Maria Cristina Piras, Paolo Merella, plex sensu stricto; Fishery products; Parasites; hypersensitivity reactions characterized by Sonia Muglia, Francesca Piras, Foodborne disease. urticaria and angioedema referred to as Giovanni Garippa, Carlo Spanu, Syndrome Urticaria Angioedema. The onset Conflict of interest: the authors declare no Enrico Pietro Luigi De Santis of symptoms begins after the ingestion of potential conflict of interest. Department of Veterinary Medicine, infected fish, with formation of transient Funding: this work was funded by MIPAAF University of Sassari, Italy and pruritic wheals, dermic and subcuta- invito d.m. 4 luglio 2011 Valutazione della neous edema. In the most severe cases, the parassitosi da Anisakis negli areali di pesca reaction can lead to a potentially deadly nazionali nonché lungo la filiera dei prodotti anaphylactic shock (AAITO-IFIACI, 2011). della pesca, individuazione e verifica di un Abstract Anisakiasis occurs after the ingestion of sistema di accertamento della stessa parassi- tosi e predisposizione di sistemi di comunica- Anisakiasis is a gastrointestinal fish- alive L3 with raw or undercooked fishery products (i.e. marinated, smoked, dried or zione e divulgazione agli operatori lungo la borne zoonosis caused by the ingestion of filiera ed al consumatore. third stage larvae of the genus Anisakis. salted). The risk of anisakiasis is associated Between January and December 2013, 1112 to the increased exposure to the parasite, Received for publication: 20 July 2016. specimens of four commercial fish species which in turn depends on the high preva- Revision received: 24 November 2016. (Engraulis encrasicolus, Merluccius mer- lence of parasitism in fish (Murrell and Accepted for publication: 24 November 2016. luccius, Scomber colias and Trachurus Fried, 2007) and the growing demand of mediterraneus) marketed in Sardinia (Italy) gastronomic preparations based on raw or This work is licensed under a Creative lightly cooked fish at global level (Broglia Commons Attribution-NonCommercial 4.0 were examined for Anisakis sp. The overall International License (CC BY-NC 4.0). prevalence of Anisakis spp larvae was and Kapel, 2011). Parasitic infections 39.9%, all morphologically identified as account approximately for 56 million cases ©Copyright D. Casti et al., 2017 Type I. Scomber colias showed the highest worldwide with an estimated population of Licensee PAGEPress, Italy prevalence (100%), followed by M. merluc- 400 million individuals at risk (WHO, Italian Journal of Food Safety 2017; 6:6185 cius (Atlantic 91.0%, Mediterranean 2013). Products such as salted or pickled doi:10.4081/ijfs.2017.6185 71.2%), T. mediterraneus (32.7%) and E. herring (Holland and Nordic countries), encrasicolus (25.9%). All the larvae found gravlax (Nordic countries), boquerones in Mediterranean hosts were genetically (Spain), lomi-lomi salmon (Hawaii) and 853/2004 (European Commission, 2004), identified as Anisakis pegreffii, whereas ceviche (South America), have been impli- food business operators must submit their 90.0% of the larvae found in the Atlantic M. cated in human anisakiasis all over the product to visual examination for the detec- merluccius belonged to Anisakis simplex world (Baird et al., 2014). In the European tion of visible parasites in order not to place sensu stricto and 10.0% to A. pegreffii. The Union, during the period 2009-2013, the fishery products that are obviously contam- mean abundance of Anisakis sp. larvae was Rapid Alert System for Food and Feed inated with parasites on the market for positively correlated with fish size in E. reported 333 notifications for the presence human consumption. Successively to the encrasicolus, Atlantic M. merluccius and of parasites 78.5% of which were account- Reg. 853/2004 European Union and local M. merluccius. The prevalence of able to Anisakis spp. (RASFF, 2014). Host Member States have implemented a series infection was greater in the body cavity species most frequently implicated were of disposition to regulate the control of par- (37.9%) than in the edible muscle (9.4%). Engraulis encrasicolus, Merluccius merluc- asites in fishery products. D’Amico et al. However, 1.8% of the examined fish were cius, Scomber scombrus, Lophius spp, (2014), conducted a comprehensive review infected exclusively in the muscle. Xiphias gladius and Lepidopus caudatus. of the legislation aimed to manage the risk Therefore, the risk associated to the con- Several cases of human anisakiasis have of Anisakis. The food safety implication for sumption of raw or undercooked fishery been reported in Italy since 1996, mainly in human anisakiasis concerns the presence of products poses the need of measures such as the southern regions, where the consump- tion of raw marinated anchovies (Engraulis larvae in the edible part of fish (muscle) visual inspection and preventive treatments encrasicolus) and pilchards (Sardina rather than in the non-edible (viscera). to guarantee consumers’ health. pilchardus) is common (Griglio et al., 2012; Therefore, when assessing the risk of expo- Mattiucci et al., 2011, 2013). Cases of sure to the parasite, it is important to con- human anisakiasis reported in Italy were sider whether parasites are detected or not associated with Anisakis pegreffii in the edible part. However, as stated by the Introduction (Fumarola et al., 2009; Mattiucci et al., European Food Safety Authority report Anisakiasis is a fish-borne zoonosis 2013). This is supported by available data (EFSA, 2010), conditions necessary for caused by the ingestion of third stage larvae that indicates that A. pegreffii is mainly dis- intra-vitam and post-mortem migration of (L3) of the genus Anisakis (Nematoda: tributed in the Mediterranean Sea while larvae from the viscera into the muscle is Anisakidae), commonly present in the body Anisakis simplex sensu stricto in the north- still controversial. Few studies have been cavity and muscle of many fish species and ern Atlantic and Pacific Oceans (Mattiucci conducted to assess the level of infection cephalopods (Chai et al., 2005). The infec- and Nascetti, 2007; Abollo et al., 2001). and the species of Anisakis larvae in fish tion is often associated with gastrointestinal According to the Regulation (EC) No. species commercialized in Sardinian market [Italian Journal of Food Safety 2017; 6:6185] [page 5] Article (Meloni et al., 2011; Tedde et al., 2011; Statistical analysis Piras et al., 2014). The objective of the Epidemiological data on the infection Results present study was to gain epidemiological levels of Anisakis larvae included the fol- information for the risk of anisakiasis asso- lowing quantitative descriptors: prevalence Levels of infection ciated with the consumption of fish market- (P%), mean intensity (mI) and mean abun- Out of 1112 fish examined, 443 (39.9%) ed in Sardinia (Italy). With this aim, the lev- dance (mA) as described by Bush et al. were infected with 5,866 Anisakis sp larvae, els of infection of Anisakis larvae in four (1997). The P% was defined as the number all morphologically identified as Type I commercial fish species at retail level were of hosts infected with 1 or more individuals (sensu Berland, 1961). Scomber colias evaluated. of a particular parasite species divided by showed the highest prevalence (100%), fol- the number of hosts examined. The preva- lowed by M. merluccius (Atlantic 91.0%, lence, with 95% CI, was determined as total Mediterranean 71.2%), T. mediterraneus infection (larvae recovered from viscera (32.7%) and E. encrasicolus (25.9%). The Materials and Methods and muscles) and independently for the vis- total number of each fish species examined, cera and the muscles. Computation was per- the mean and range values of length and Fish sampling and Anisakis larvae formed with the Sterne’s method. The mI weight, total number (Ntot) and levels of detection and identification (and the 95% CI) was determined as the infection of larvae recovered are reported in During the period between January and average number of individuals of a particu- Table 1. Pairwise differences in the overall December 2013, a total of 1112 fish speci- lar parasite species among the infected P% and mI between host species are report- mens were acquired from Sardinian fish members of a particular host species. The ed in Table 2. Prevalence and mean intensi- markets and examined for the presence of mA (and 95% CI) was defined as the total ty of Anisakis spp. larvae according to loca- Anisakis sp. larvae. The fish belonged to number of individuals of a particular para- tion (body cavity or muscle) are reported in four commercial species, Engraulis encra- site species in a sample of a particular host Table 3. No larvae were detected in the sicolus (n.750), Merluccius merluccius (n. species divided by the total number of host muscle of S. colias. A significant difference 218), Scomber colias (n. 40) and Trachurus of that species examined (infected and unin- in the P% of infection between body cavity and muscle was observed in all the species mediterraneus (n.104). The first three fected hosts). Differences in the P% and mI with the exception of Atlantic M. merluc- species and 118 specimens of M. merluc- values of larvae infection between the four cius, where the prevalence was comparable cius were from the Gulf of Asinara (North fish species were assessed respectively with (Table 3).