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Article

Notifications on Anisakis spp. in the Rapid Alert System for Food and Feed (RASFF) Reported in 2001–2023

by
Marcin Pigłowski
Department of Quality Management, Faculty of Management and Quality Science, Gdynia Maritime University, Morska 81-87 Str., 81-225 Gdynia, Poland
Sustainability 2024, 16(13), 5453; https://doi.org/10.3390/su16135453
Submission received: 9 May 2024 / Revised: 10 June 2024 / Accepted: 21 June 2024 / Published: 27 June 2024
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Abstract

:
Anisakis spp. was the most frequently reported parasite in the Rapid Alert System for Food and Feed (RASFF). Notifications relating to it accounted for 73.6% of all notifications submitted in this system between 2001 and 2023 in the hazard category “parasitic infestation”. Using a two-way joining cluster analysis, notifications reported in the RASFF during the period indicated concerning Anisakis spp. were examined by considering the year, notification type, product category, product, notifying country, country of origin, notification basis and action taken. These mainly concerned hake and mackerel from Spain and also anglerfish and mackerel from France (reported by Italy after official controls on the market) and anchovies and scabbardfish from Morocco (sent by Spain after border controls). Products from Spain and France were reported as alerts and information notifications and then were officially detained, withdrawn from the market or destroyed. Fish from Morocco were detained and destroyed. Although the number of Anisakis spp. notifications has decreased significantly in recent years, food safety authorities should continue to be active in this area. Meanwhile, consumers should be aware that the consumption of unprocessed fish should be avoided.

1. Introduction

One of the elements of the European Farm to Fork Strategy is to ensure food security, nutrition and public health, making sure that everyone has access to sufficient, safe, nutritious and sustainable food. This strategy is implemented through agricultural and fishery policies [1]. Within the context of food safety, it is possible to talk about the hazards that may be present in food. Hazard means a biological, chemical or physical agent in, or the condition of, food or feed with the potential to cause an adverse health effect [2].
The parasite Anisakis spp. is considered as a biological hazard [3,4,5,6]. It is one of the most relevant parasites in fishery products [3,7]. Reported and verified outbreaks caused by this parasite occurred for example in Spain in 2018 and 2020 [8,9]. In 2017 and 2018, this country reported data on the presence of Anisakis spp. in raw fish and fish products available at retail [8,10], as well as from processing, wholesaling and catering [8].

1.1. Determinants Associated with Anisakis spp.

Anisakis spp. uses zooplankton as intermediate hosts, fish and cephalopods as parental hosts and marine mammals and birds as definitive hosts [11,12,13]. It is a cosmopolitan species, although it is most common in Spain, France, Japan, the Netherlands and less common in the United States [11].
Humans become accidental hosts of this parasite [14,15,16,17,18] after eating raw, undercooked, lightly salted, marinated or brined fish [6,14,18,19,20,21,22,23,24,25,26,27,28,29]. The ingestion of live Anisakis spp. larvae can cause an infection, sensitisation reaction or both [6,18,21,24,27,28]. The disease called anisakiasis causes nausea, abdominal pain [18,19,24] and, in susceptible individuals, acute and recurrent urticaria, with the allergic reaction being triggered by immunoglobulin E (IgE) [20]. Earlier infections with Anisakis spp. may also be a risk factor in the development of stomach and colon cancer [22,23]. As mentioned, people consuming unprocessed fish are at risk of Anisakis spp. infection, but those particularly vulnerable to anisakiasis are fishermen and workers in fish processing and sale [20].
However, even eating processed fish can cause gastro-allergic reactions due to hypersensitivity to allergens [12,24]. Many Anisakis spp. allergens are quite thermostable, so cooking and freezing fish may not protect particularly sensitive individuals from an allergic reaction [5,21,25]. It is also worth mentioning that Anisakis spp. is the only known parasite capable of causing this reaction in susceptible persons [30] and was identified as an emerging issue with possibly increasing exposure during the European Food Safety Authority (EFSA) panel consultation [31].

1.2. Anisakis spp. in the Rapid Alert System for Food and Feed (RASFF)

The RASFF was established in the European Union (EU) in 1979, but currently operates on the basis of Regulation 178/2002 (known as the General Food Law) [2]. Members of the RASFF are EU countries and, more broadly, European Economic Area (EEA) countries. The purpose of this system is to ensure the exchange of information between its members if a risk to public health in the food chain arises and to assure a swift reaction of food safety authorities [32]. Notifications concerning parasites are reported in the RASFF in the hazard category “parasitic infestation” (Table 1) [33,34].
A total of 885 notifications were submitted in the RASFF between 1993 and 2023 in this category, and they were most often related to Anisakis spp. (651 notifications, i.e., 73.6%). The first notification regarding this parasite was reported in 2001. It should also be noted that the family Anisakidae belongs to the intestinal nematodes and the parasite Pseudoterranova spp. belongs to this family; however, notifications concerning them were reported separately.

1.3. Goal of the Study

In the literature, there are works on notifications concerning Anisakis spp. submitted in the RASFF, but they rarely cover longer periods and present this issue in a comprehensive and cross-cutting manner. Therefore, the aim of this study was to analyse notifications on Anisakis spp. reported in the RASFF in 2001–2023, including the year (as basis data), and other data covering the notification type, product category, product, notifying country, country of origin, notification basis and action taken. Linking all these data together allowed us to obtain multidimensional results over the entire reporting period of Anisakis spp. in the RASFF.

2. Data and Methods

The data were extracted from two databases, i.e., from the restored RASFF database (for 2001–2021) [33] and the RASFF database now officially available (for 2022–2023). In the second database mentioned, data were only provided from 2020 to now [34]. After combining the data, information was obtained for 651 notifications relating to Anisakis spp., reported between 2001 and 2023 and covering the year, notification type, product category, product, notifying country, country of origin, notification basis and action taken.
The data were then processed in Microsoft Excel (Microsoft Corporation, Redmond, DC, USA) using the following functions: filtering, sorting, transposition, vertical search and pivot tables. Additionally, the data on the most frequently reported countries of origin were transferred to Statistica 13.3 (TIBCO Software Inc., Santa Clara, CA, USA), where they were subjected to the two-way joining cluster analysis. In this method, clusters were represented in a two-dimensional structure. Despite the fact that it is not homogeneous by nature, this analysis is considered a powerful exploratory tool [35]. The primary objective of any cluster analysis is to show similarities; however, as the results of this method were presented in two dimensions, additionally relationships could also be indicated.
The general results were presented in column charts obtained in Microsoft Excel and the detailed results of the two-way joining cluster were generated in Statistica 13.3 as contour/discrete charts. They represented the clusters of numbers of notifications through coloured squares, starting with white (the smallest clusters or no clusters), through green, yellow, orange, red and brown (the largest clusters).
In order to identify links between the keyword “Anisakis” and other keywords indicated by authors of scientific works and to determine trends of recent research in this area, VOSViewer 1.6.20 (Centre for Science and Technology Studies, Leiden University, The Netherlands) was used. First, data for 1663 scientific papers with the keyword “Anisakis” published in 2001–2023 were exported in a text file from Web of Science [36]. Then, they were processed in VOSviewer using the following options: type of analysis (co-occurrence), unit of analysis (author keywords), counting method (full counting) and minimum number of occurrences of the keyword (10). The analysis allowed us to obtain a network visualisation and an overlay visualisation.

3. Results

3.1. General Analysis

Figure 1 shows the number of notifications on Anisakis spp. reported in the RASFF in 2001–2023 by the year, notification type, product category, product, notifying country, country of origin, notification basis and action taken.
The number of notifications on Anisakis spp. fluctuated considerably during the period under study (Figure 1a). From the beginning of the period (2001–2003), there was only a single notification each year, but in 2004, there were approximately 50 notifications. This number then decreased in the following two years, but increased thereafter, reaching a peak in 2011, in which there were more than 100 notifications (the highest number in the study period). In the subsequent years, this number dropped, but rose again to approximately 40 in 2017–2019, generally decreasing thereafter, and in 2023 it was approximately 20.
Half of the notifications reported were information notifications, but there were also border rejections—over 27%—and alerts—over 22% (Figure 1b). Notifications related mainly to fish and products thereof—almost 97% (Figure 1c)—with mackerel, hake, anglerfish, scabbardfish, cod and anchovies were among the most frequently reported—over 75% in total (Figure 1d).
A more detailed analysis of the species indicated that the highest number of notifications was related to Atlantic mackerel (Scomber scombrus), European hake (Merluccius merluccius), European anglerfish (Lophius piscatorius), silver scabbardfish (Lepidopus caudatus), Atlantic cod (Gadus morhua) and European anchovy (Engraulis encrasicolus), respectively (Table 2).
Notifications were mainly reported by Italy (more than 60%) and by Spain—approximately 15% of all notifications (Figure 1e)—and submitted products most often originated from Spain, France and Morocco, with a total of nearly 50% (Figure 1f). Notifications relating to fish from these three countries were analysed in more detail using a two-way joining cluster analysis (Section 3.2).
The notification basis was most often an official control on the market (more than 50%) or a border control, after which the consignment was detained—almost 30% (Figure 1g). Subsequently, the following actions were usually taken on the reported products: destruction (almost 30%), withdrawal from the market (17%) and re-dispatch—almost 11% (Figure 1h).

3.2. Most Frequently Reported Countries of Origin

Figure 2, Figure 3 and Figure 4 show the number of notifications on Anisakis spp. reported in the RASFF on products originating from Spain, France and Morocco, respectively, by the year, notification type, product, notifying country, notification basis and action taken.
The highest number of notifications on products from Spain were reported in 2010–2011 (alerts) and 2017 and 2018 (information notifications) (Figure 2a,b). In 2010–2011 and 2017, these were for hake and in 2018 for mackerel (Figure 2c) and were sent by Italy (Figure 2d). The notification basis was official control on the market (Figure 2e), and products were officially detained, withdrawn from the market or destroyed (Figure 2f).
Regarding products from France, a certain number of alerts could be seen between 2009 and 2011, but a marked increase in the number of information notifications could be noticed in 2019 (Figure 3a,b). These concerned anglerfish and mackerel (Figure 3c), and were also raised by Italy (Figure 3d). The notification basis was also an official control on the market (Figure 3e). Between 2008 and 2011, reported products were destroyed or withdrawn from the market, and in 2019, they were destroyed or officially detained (Figure 3f).
For products from Morocco, border rejections could be seen in 2011 and 2021 (Figure 4a,b). In 2011, these concerned anchovies (or products that were not specified), and in 2021, they were related to scabbardfish (Figure 4c). These notifications were sent by Spain (Figure 4d). The notification basis was border control, after which the consignment was detained (Figure 4e) and then destroyed (Figure 4f).
Thus, for products from each of the countries shown, there were notifications in 2011, but due to the high number of notifications in that year (Figure 1a), the reported products must also have come from other countries. What is equally important is that these were most often information notifications or border rejections, and less frequently alerts. It is worth noting that Italy was particularly active in reporting notifications, as already indicated in Figure 1e.

4. Discussion

An analysis of papers published between 1967 and 2017 with host–parasite–location–year combinations showed an increase in the abundance of Anisakis spp. [37]. It was also noted that zooplankton was not the only habitat specific to this parasite, but it also used other hosts to cross habitats and extend routes to the final host (mammals) [38]. The transmission routes of Anisakis spp. may be much broader than previously thought, and it can use different intermediate hosts to move from one habitat to another depending on the seasonal and ecological availability of such hosts to find its definitive host [15].
Studies carried out in 2013 on fish collected from five Atlantic fishing areas (according to the Food and Agriculture Organization of the United Nations—FAO) showed the presence of Anisakis spp. larvae particularly in the following species: blue ling (Molva dypterygia), European conger (Conger conger), John Dory (Zeus faber) and black scabbardfish (Aphanopus carbo) [6]. In turn, a research study conducted for the period 1998–2020 on the presence of Anisakis spp. larvae in European hake (Merluccius merlucciufs) in the Northeast Atlantic Ocean showed that the parasite was present in every fish larger than 60 cm in all International Council for the Exploration of the Sea (ICES) sub-areas, and the level of fish infection increased over the period studied. It was pointed out that this could be due to two factors: an increase in hake stocks (as an intermediate host) and an increase in dolphin abundance (as a definitive host) [39]. Other studies have shown that the North Sea (as part of the North Atlantic Ocean) is one of the most infected fishing areas [40].
In Europe, the most commonly infected species were, in turn, herring, anchovy, sardine and cod [13]. It has been noted that European anchovy (Engraulis encrasicolus) larger than 140 mm, which corresponds to an age of one to two years, may be a good indicator of the occurrence of Anisakis spp. in the Bay of Biscay, as it accumulates the ingested parasite in the first year of life [41]. In the Mediterranean Sea, Anisakis spp. was found at moderately high levels also in European anchovies [42] and in the Baltic Sea in herrings and sprats [43]. Atlantic horse mackerel (Trachurus trachurus) is also a common host for Anisakis spp., and this fish is the most popular for North African consumers [44].
It is also worth noting that, in general, Atlantic fish show higher levels of infection with this parasite than Mediterranean fish [45]. Furthermore, Anisakis spp. is more common in wild fish than in farmed fish [40,46,47]. Many of the fish species listed above have been reported in the RASFF (see Figure 1d and Table 2), but it should be mentioned that these studies were not based on an analysis of notifications in this system.

4.1. Notifications in the RASFF in Studies to Date

Already in 2010, reports of the EFSA noted that in 2004–2009, Italy submitted fresh mackerel in the RASFF. It was infected with Anisakis spp. and originated from Norway or from Norway via Denmark [48,49]. It was noticed that these notifications were also reported when the fish was not imported from Norway, indicating under-reporting, the misidentification of the species or country of origin as the reason [48]. It is worth pointing out, however, that due to the European common market, operating on the basis of treaties, these imports did not have to be direct (from Norway), but could have been carried out through an intermediate country (probably Denmark), as indicated earlier.
According to a study on notifications regarding parasites reported in the RASFF in 2009–2013, 78.5% of them concerned Anisakis spp. These were mainly transmitted by Italy and Spain as border rejections, information and alerts, and concerned the following fish: European hake (Merluccius merluccius), Atlantic mackerel (Scomber scombrus), European anchovy (Engraulis engrasicolus), anglerfish (Lophius spp.), swordfish (Xiphias gladius) and silver scabbardfish (Lepidopus caudatus) [50]. The particular activity of Italy between 2010 and 2014 regarding the reporting of fish infected with this parasite was also confirmed in other studies [51]. Between 2011 and 2015, notifications for the presence of Anisakis spp. accounted for 84.2% of cases, and similarly notified were hake (Merluccius spp.), mackerel (Scomber spp.), anglerfish (Lophius spp.), anchovies (Engraulis spp.) and silver scabbardfish (Lepidopus caudatus). They originated from Morocco, Spain and France [52]. The study conducted for 2001–2019 indicated similar fish species, i.e., mackerel, hake and anglerfish. They were mainly reported by Italy as border rejections and alerts after official control on the market. Infected products were then destroyed or withdrawn from the market [53].
The results of the studies mentioned above were similar to those obtained in this research, particularly in terms of notified fish species, i.e., mackerel, hake and anglerfish (see Figure 1d and Table 2) and notifying country, i.e., Italy (see Figure 1e). However, the present study was much more detailed, as it identified the years with the highest number of notifications, notification type, product, notifying country, notification basis and action taken considering specific countries of origin. Indeed, depending on the country of origin, different fish species were reported and different measures were taken after notifications. There also remains another discrepancy between the mentioned studies and the present one. Namely, based on the data available for the whole possible period, i.e., 2001–2023, it could be concluded that information notifications predominated, followed by border rejections and alerts (see Figure 1b).
Information notifications are submitted when a risk has been identified in a food on the EU market, but other RASFF members do not need to take rapid action. This is when the product has not reached their market, is no longer on their market or the nature of the risk does not require rapid action. Border rejections cover consignments of food that have been tested and rejected at the external border of the EU (and the wider EEA) if a risk is found in the food. Notifications are sent to all EEA border posts to ensure that rejected products do not enter the common market through another post. In turn, alerts are sent when food presenting a serious health risk is on the EU market and rapid action is required. A RASFF member who identifies a risk is obliged to take action (e.g., withdrawal of the product from the market) and inform other members of the system so that they can also take appropriate measures [32].

4.2. Consumers from Italy and Spain Facing the Risks of Anisakis spp. Infection

According to the FAO, Italy and Spain remained the top producers of aquaculture in Europe in 2022 (production of approximately 4% and 8%, respectively). These countries were also among the ten largest importers of aquatic animal products in the world that year. It should be noted, however, that the effect of the COVID-19 pandemic was a reduction per capita consumption of aquatic animal foods, which resulted in a stabilisation of global fisheries and aquaculture production and a decrease in trade volumes. In Europe, the drop in per capita consumption during this period was 3.3% [54].
During the period studied (2001–2023), Italy, as well as Spain (see Figure 1e), submitted products with Anisakis spp. most frequently and the notifications referred specifically to mackerel, followed by hake and anglerfish (see Figure 1d and Table 2). The import of mackerel and hake (in thousands of tons) carried out by Italy and Spain according to the Standard International Trade Classification (SITC) is shown in Figure 5a and Figure 5b, respectively. Data for anglerfish were not available in the SITC [55].
The import of mackerel to both these countries was initially at similar levels (approximately 15–20 thousand tonnes). In later years, this import to Spain increased and was 1.5–2 times greater than to Italy, and, in recent years, was 15 and 25–30 thousand tonnes, respectively, whereas the import of hake during the period considered was 3–4 times higher to Spain than Italy. However, when considering both these countries, the import of mackerel and hake dropped significantly, from approximately 15 to 5 thousand tonnes in the case of Italy and from approximately 55 to 25 thousand tonnes in the case of Spain.
It could, therefore, be recognised that the potential exposure of Italian and Spanish consumers to Anisakis spp. has decreased markedly. However, it is also noteworthy that, despite the much higher imports of mackerel and hake in the period studied, Spain sent significantly fewer notifications of Anisakis spp. in the RASFF. This may indicate that Italian food safety authorities were much more active.
Research conducted between 2015 and 2017 in Italy showed that many European anchovy (Engraulis encrasicolus) products contaminated with Anisakis spp. larvae reached the market and were sold in Italian supermarkets as semi-preserved products. Due to the inactivation of the larvae during freezing and processing, the risk of infestation was negligible, but the presence of dead parasites could cause consumers to immediately reject such products [56]. Other researchers indicated that the occurrence of Anisakis spp. can discourage consumers from buying fishery products, causing losses to the industry. In turn, 77% of Spanish consumers said they were willing to pay more for fish free of this parasite [57].
Turkish consumers are also at risk of Anisakis spp. infection due to the import of Atlantic mackerel (Scomber scombrus) [25,58,59] and John Dory (Zeus faber) from the Senegalese coast, which are then sold in Turkish supermarkets. There are, therefore, calls in this country for the RASFF to be incorporated into the legal system [58,59]. In turn, Japanese researchers have, therefore, pointed out that an effective measure to prevent anisakiasis is to avoid the consumption of raw fish [60]. It also highlights the need for consumer education and the necessity to introduce new standardised techniques for this parasite detection [53,61].
It is further worth noting that a possible reason for the inability to remove infected fish is changes in the fishery supply chain. Control is no longer the responsibility of veterinary inspectors, but of the market operator, and their staff may be insufficiently trained to detect larvae in fish [50].
Also, importantly, during the COVID-19 pandemic, the number of notifications against Anisakis spp. decreased (Figure 1a). This may have just been related to the disruption or interruption in the supply chain, and, therefore, reduced consumption, increased consumer caution and decreased surveillance activity.

4.3. Exposure to Anisakis spp. Infection and Ways of Prevention

The following methods can be used to prevent Anisakis spp. infection: evisceration of fish immediately after capture, monitoring of fish populations most likely to be parasitised, visual inspection of fish to detect visible parasites, physical and chemical treatments to devitalise larvae and the freezing of fish [53].
The Regulation 1276/2011 requires fishery products to be deep-frozen for at least 24 h before being consumed raw or semi-cooked; however, this is not always adhered to in households, local guesthouses or restaurants. Therefore, the consumption of such dishes is the main cause of anisakiasis in Spain, but also in Italy [45]. In this country, however, allergies caused by Anisakis spp. (and snails) only account for less than 1% of all food allergies [62]. Nevertheless, anisakiasis is an emerging disease in the already mentioned countries [18,23,63], but also in Japan, where a lot of raw or marinated fish is consumed [23]. Portuguese consumers are similarly at risk of this disease due to being third in the world in fish consumption [5]. However, as the reporting of anisakiasis is not mandatory, it can be assumed that it is underestimated and the number of cases in each country is different from what is officially presented [64].
The transport and storage of fresh fishery products has minimal impact on the viability of Anisakis spp. and, therefore, freezing is required for its inactivation [13]. Freezing is considered the most effective means of preventing Anisakis spp. infection [65]. The Regulation 853/2004 lays down provisions for fishery products to be consumed raw or almost raw, which have undergone a cold smoking process, and marinated and/or salted fishery products if the processing is insufficient to destroy Anisakis spp. larvae. It requires freezing to a temperature of no more than −20 °C in all parts of the product for no less than 24 h [66]. It is also indicated that to kill this parasite, it is necessary to cook fish at a temperature above 60 °C or store in industrial freezers for two days [24]. It has also been noted that air drying can be an alternative and efficient method to inactivate Anisakis spp. in fish products [67]. The essential oils of certain Mediterranean plants (Spanish lavender, cumin and oregano) have a biocidal effect and also cause the migration of Anisakis spp. larvae from the fish, so they can be added when marinating them [68].
The proportion of Anisakis spp. larvae found on the surface of European anchovy (Engraulis encrasicolus) was similar to that found in the viscera and lower than in the muscles, suggesting that most of the larvae migrating to the surface must have come from the viscera. This indicates the need to remove fish viscera immediately after capture [63]. In the case of beaked redfish (Sebastes mentella), the removal of belly flaps is recommended [69]. It is also worth reminding that, as the possibility of Anisakis spp. infection is much lower when consuming farmed fish than wild fish, the use of closed breeding facilities may be considered [70]. It is noted that when a fish is eaten by another fish, the Anisakis spp. larvae may re-encapsulate in the host, and if this phenomenon occurs repeatedly, the larvae can accumulate in predatory fish [71].
Two types of anisakiasis are recognised: intestinal, more common in Europe, and gastric, which occurs in Japan. Intestinal anisakiasis is often misdiagnosed and many patients require surgery due to perforation or occlusion of the bowel [14,24,72]. Several thousand cases of anisakiasis are diagnosed annually, of which 90% are reported in Japan (2–3000 per year), with the remainder reported in countries such as Korea, Spain, Italy, the Netherlands and Germany [13]. Anisakiasis is still an infradiagnosed, emerging and cosmopolite illness [16,73]. It is, therefore, considered that measures that could prevent it could be registers of cases, education campaigns for the general public and awareness-raising and training campaigns for health professionals. Control measures in the relevant economic sectors, fish operators, fish farms, fishermen, fish retailers, the fish industry and catering facilities, are proposed as complementary measures. The possible genetic predisposition to Anisakis spp. allergy and the link between anisakiasis and cancer also require further research [16].
Food businesses must ensure that fishery products have been visually inspected for visible parasites and must not be placed on the market with products that are obviously contaminated with parasites [66]. Thus, the detection and quantification of seafood allergens is essential for quality control in industry and government surveillance [74]. Among the drivers of food-borne parasite infection, the lack of control in the food chain and lack of awareness in the relevant authorities were mentioned, so methodological gaps and issues related to surveillance and impact assessments should be pointed out [75]. The presence of Anisakis spp. in products indicates the inefficiency of current parasite control procedures carried out under European regulations by seafood companies. They, therefore, require improvement, and this can be achieved by establishing research-based and standardised parasite detection methodologies and procedures, e.g., the development of non-destructive methods for their detection and removal from fish products and appropriate sampling strategies. These methods should then be applied by seafood companies [73]. It is also worth noting that official controls for the detection of food-borne parasites are based on a direct macroscopic visual inspection of fish or the microscopic examination of samples of their tissues. A visual inspection allows for an overall assessment of tissue quality, but is labour-intensive, especially when, additionally, microscopy is required [76].
Due to the increase in the consumption of raw and undercooked fish, there has been a marked increase in interest in Anisakis spp. among scientists, consumers, tax authorities and seafood companies. However, caution should be exercised in the dissemination of information concerning this parasite. This is because it may cause public concern and lead to a change in consumer preferences due to mistrust and the rejection of fishery products, and, consequently, economic losses and loss of jobs in the fish industry [53].

4.4. Maps of Links between the Keyword “Anisakis” and Other Words

The analysis in VOSviewer resulted in maps consisting of 66 items. The network visualisation consisted of seven clusters marked in different colours (Figure 6). The clusters grouped the elements most similar to each other and allowed them to be distinguished from other clusters. The overlay visualisation provided an indication of what the latest research (from approximately 2018) on Anisakis spp. referred to (yellow in Figure 7). The keyword “Anisakis” is in the middle of both these maps.
In Figure 6, the red cluster was the most abundant, consisting mainly of items indicating Anisakis spp. species, some systematic relationships and the sites of its occurrence (the Mediterranean Sea and also the Baltic Sea). In fact, the study carried out showed that the problem in question was mainly related to Mediterranean countries (Section 3.2 and Section 4.2). The green cluster represents mainly allergy-related items. However, it is worth noting that this cluster also included “seafood” and a distinct “Anisakis simplex” item very close to the “Anisakis” item (from another cluster, purple). This could indicate that this species was the one most often pointed out in scientific papers. In the olive cluster, the two most prominent elements were “parasites” and “fish”. The most relevant element of the blue cluster was “anisakiasis” (Section 4.3), linked to “anisakiosis” and “anisakidosis” used as synonyms, and also “zoonoses”, “food safety”, “public health” and “raw fish”. It is worth reminding that it is precisely the purpose of the RASFF to respond rapidly to food safety authorities if a risk to public health arises.
It is notable that the issues in the blue cluster (Figure 6) were precisely the subject of recent studies (yellow colour in Figure 7). Noteworthy is that research concerned Anisakis spp. larvae, histopathology and molecular identification. However, given the RASFF, other aspects were also of interest. Besides the mentioned before “food safety” and “public health”, the issue of “seafood safety” in another part of the map was also marked in yellow. This confirmed the timeliness of the research undertaken into the analysis of Anisakis spp. notifications reported in the RASFF. In turn, issues related to allergies in the context of this parasite were addressed in scientific papers approximately 10 years ago (blue and purple colours in Figure 7).
Thus, while the mechanism itself related to allergy caused by Anisakis spp. should be considered relatively recognised, attention should be paid to safety and health aspects. According to Regulation 178/2002, food may not be placed on the market if it is unsafe, i.e., it is injurious to health or unfit for human consumption. Related to this is the term risk, which is a function of the probability of an adverse health effect occurring and the severity of that effect resulting from the hazard. The hazard may be a biological agent—as in the case of Anisakis spp., a chemical or physical agent in the food or a condition of the food with the potential to cause adverse health effects. European Union countries are obliged to enforce food law and maintain a control system for this purpose. In turn, if a food business operator considers or has reason to believe that a food does not meet food safety requirements, it is obliged to withdraw it from the market and inform the relevant authorities. If the product has already reached the consumer, that consumer should be informed of the reason for the withdrawal and, if necessary, recalled. Finally, member states are obliged to notify the European Commission through the RASFF of any measures aimed at restricting the placing on the market of food, its withdrawals and recalls, as well as its rejections at border posts taken to protect human health [2]. Indeed, as indicated in Section 3.1 and Section 3.2, the basis of the notifications reported in the RASFF against Anisakis spp. were mostly official or border controls. In turn, the actions taken were mainly destruction, withdrawal from the market and official detention.
However, as pointed out in Section 4.3, despite the existence of legal requirements, the problem of the presence of Anisakis spp. in food and the health risks it causes is still ongoing, and requires the attention of business operators, supervisory authorities and consumers themselves.

4.5. Limitations Related to Obtaining and Processing of Data

The information retrieved from the restored RASFF database (for 2001–2021) also contained data on notification basis and action taken, while the information extracted from the official RASFF database (for 2022–2023) did not include such data. It was, therefore, necessary to check each notification separately to obtain these data. The necessity to combine data from two databases hindered the research. This is because the data acquired needed to be standardised and organised before being analysed. It is also worth mentioning that some data were missing and the Latin names of certain species were incorrect, so they had to be checked and rectified [77]. The Latin names were given in the text in Section 4 only if they appeared in a given reference. Thus, if only English names were mentioned in reference, Latin names were not added to avoid inconsistencies between the English and Latin names.
Since 2011, information notifications have been divided into two types: information for attention and information for follow-up. In order to be able to carry out the analysis, it was necessary to adopt a common (initial) name for all of them, i.e., information notifications [33]. Due to the method used (a two-way joining cluster analysis), one notification could only refer to one product, so if two or more products were given (in rare cases), only the first one was taken. Another limitation of this method was the automatic generation of ranges of notification numbers that did not always correspond to those numbers in the charts, as well as the ambiguous coverage of colours from the legend in the charts. Additionally, because the clusters were grouped by the number of notifications and not by year, the years following each other were not always next to one another in the charts, which may have caused difficulties in interpreting the results.
In turn, a significant shortcoming of the linkage maps obtained in VOSviewer was the lack of names for many of the items, so that they had to be re-added in the graphics programme after identification. It is also worth noting that some of the keywords presented in the visualisations differed only in the singular and plural, or some two words occurring individually were merged into one elsewhere in the map. By unifying the names of these words, it would have been possible to reduce the number of words and have much better focused and separated elements within each cluster. However, this was not possible as the names of the keywords were chosen and formulated by the authors.

5. Conclusions

In the Rapid Alert System for Food and Feed (RASFF), notifications regarding Anisakis spp. accounted for 73.6% of all notifications in the hazard category “parasitic infestation” between 2001 and 2023. More than half were information notifications, followed by border rejections and alerts. Italy reported mackerel and hake from Spain and anglerfish and mackerel from France, while Spain reported anchovies and scabbardfish from Morocco. Fish from Europe was reported on the basis of official control on the market and were then officially detained, withdrawn from the market or destroyed. In turn, products from Morocco were notified as border rejections, after which shipments were detained and then destroyed.
In earlier years, imports of mackerel by Italy and Spain were much higher, but are now at a similar level to 2001, while imports of hake have fallen considerably since that year. This may have reduced the exposure of consumers from those countries to infestation with Anisakis spp. However, a higher abundance of this parasite in the marine environment (possibly due to climate change) has been observed, so there is a need for further research in this area. It should also be noted that during the COVID-19 pandemic, global fish consumption (including Europe) declined, which was mainly due to the disruption of the supply chain.
There is also a need for further activity, the cooperation of national food safety surveillance authorities and the development of rapid and standardised methods for the detection of Anisakis spp. in Mediterranean countries. Additionally, as the consumption of raw or low-processed fish is a dietary habit in these countries, consumers may be advised to consume farmed fish (less exposed to this parasite) rather than wild fish.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The author declares no conflict of interest.

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Figure 1. Number of notifications on Anisakis spp. reported in the RASFF in 2001–2023 by: (a) year; (b) notification type; (c) product category; (d) product; (e) notifying country; (f) country of origin; (g) notification basis; (h) action taken. Explanations for notification basis: Of. Control—market—official control on the market; B. control—detained—border control consignment detained; B. control—released—border control consignment released; Of. control—RASFF—official control following RASFF notification; B. control—customs—border control consignment under customs. Explanations for action taken: Withdrawal—market—withdrawal from the market; Re-dispatch or destr.—re-dispatch or destruction.
Figure 1. Number of notifications on Anisakis spp. reported in the RASFF in 2001–2023 by: (a) year; (b) notification type; (c) product category; (d) product; (e) notifying country; (f) country of origin; (g) notification basis; (h) action taken. Explanations for notification basis: Of. Control—market—official control on the market; B. control—detained—border control consignment detained; B. control—released—border control consignment released; Of. control—RASFF—official control following RASFF notification; B. control—customs—border control consignment under customs. Explanations for action taken: Withdrawal—market—withdrawal from the market; Re-dispatch or destr.—re-dispatch or destruction.
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Figure 2. Number of notifications on Anisakis spp. reported in the RASFF in products originating from Spain: (a) year; (b) notification type; (c) product; (d) notifying country; (e) notification basis; (f) action taken. Explanations for notification basis: B. control—detained—border control consignment detained; Off. control—RASFF—official control following RASFF notification; Off. Control—market—official control on the market. Explanations for action taken: Destination—identified—destination of the product identified; Phys. treat.—freezing—physical treatment freezing; Phys./chem. treat.— physical/chemical treatment; Product—consumed—product already consumed; Withdrawal—recipient(s)—withdrawal from recipient(s); Withdrawal—market—withdrawal from the market.
Figure 2. Number of notifications on Anisakis spp. reported in the RASFF in products originating from Spain: (a) year; (b) notification type; (c) product; (d) notifying country; (e) notification basis; (f) action taken. Explanations for notification basis: B. control—detained—border control consignment detained; Off. control—RASFF—official control following RASFF notification; Off. Control—market—official control on the market. Explanations for action taken: Destination—identified—destination of the product identified; Phys. treat.—freezing—physical treatment freezing; Phys./chem. treat.— physical/chemical treatment; Product—consumed—product already consumed; Withdrawal—recipient(s)—withdrawal from recipient(s); Withdrawal—market—withdrawal from the market.
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Figure 3. Number of notifications on Anisakis spp. reported in the RASFF in products originating from France: (a) year; (b) notification type; (c) product; (d) notifying country; (e) notification basis; (f) action taken. Explanations for notification basis: Off. control—RASFF—official control following RASFF notification; Off. control—market—official control on the market. Explanations for action taken: Monitoring—monitoring of the recall/withdrawal; Phys. treat.— physical treatment; Phys. treat.—freezing—physical treatment freezing; Phys./chem. treat.— physical/chemical treatment; Re-dispatch or destr.—re-dispatch or destruction; Use for other purpose—use for other purpose than food/feed; Withdrawal—recipient(s)—withdrawal from recipient(s); Withdrawal—market—withdrawal from the market.
Figure 3. Number of notifications on Anisakis spp. reported in the RASFF in products originating from France: (a) year; (b) notification type; (c) product; (d) notifying country; (e) notification basis; (f) action taken. Explanations for notification basis: Off. control—RASFF—official control following RASFF notification; Off. control—market—official control on the market. Explanations for action taken: Monitoring—monitoring of the recall/withdrawal; Phys. treat.— physical treatment; Phys. treat.—freezing—physical treatment freezing; Phys./chem. treat.— physical/chemical treatment; Re-dispatch or destr.—re-dispatch or destruction; Use for other purpose—use for other purpose than food/feed; Withdrawal—recipient(s)—withdrawal from recipient(s); Withdrawal—market—withdrawal from the market.
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Figure 4. Number of notifications on Anisakis spp. reported in the RASFF in products originating from Morocco: (a) year; (b) notification type; (c) product; (d) notifying country; (e) notification basis; (f) action taken. Explanations for notification basis: B. control—detained—border control consignment detained; B. control—customs—border control consignment under customs; Explanations for action taken: Re-dispatch or destr.—re-dispatch or destruction; Withdrawal—market—withdrawal from the market.
Figure 4. Number of notifications on Anisakis spp. reported in the RASFF in products originating from Morocco: (a) year; (b) notification type; (c) product; (d) notifying country; (e) notification basis; (f) action taken. Explanations for notification basis: B. control—detained—border control consignment detained; B. control—customs—border control consignment under customs; Explanations for action taken: Re-dispatch or destr.—re-dispatch or destruction; Withdrawal—market—withdrawal from the market.
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Figure 5. Import of mackerel and hake (in thousands of tons) by the SITC to: (a) Italy; (b) Spain. Explanations for import: total import from EU and non-EU countries; explanations for mackerel: total of three categories in the SITC: mackerel (scombrids), fresh/chilled (excluding livers & roes) (03417), mackerel (scombrids), frozen (excluding livers & roes) (03426) and mackerel, prepared/preserved, whole/in pieces, but not minced (03714); explanations for hake: category in the SITC: hake, frozen (excluding livers & roes) (03427).
Figure 5. Import of mackerel and hake (in thousands of tons) by the SITC to: (a) Italy; (b) Spain. Explanations for import: total import from EU and non-EU countries; explanations for mackerel: total of three categories in the SITC: mackerel (scombrids), fresh/chilled (excluding livers & roes) (03417), mackerel (scombrids), frozen (excluding livers & roes) (03426) and mackerel, prepared/preserved, whole/in pieces, but not minced (03714); explanations for hake: category in the SITC: hake, frozen (excluding livers & roes) (03427).
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Figure 6. The network visualisation of the links between the keyword “Anisakis” and other words.
Figure 6. The network visualisation of the links between the keyword “Anisakis” and other words.
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Figure 7. The overlay visualisation of the links between the keyword “Anisakis” and other words.
Figure 7. The overlay visualisation of the links between the keyword “Anisakis” and other words.
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Table 1. Number of notifications reported in the RASFF in the hazard category “parasitic infestation”.
Table 1. Number of notifications reported in the RASFF in the hazard category “parasitic infestation”.
ParasiteNotifications ParasiteNotifications
Anisakis spp.651Sarcocystis spp.3
Nematodes41Acanthocephalus spp.2
Pseudoterranova spp.14Kudoa spp.2
Trichinella spp.10Coccidia1
Tapeworms9Echinococcus granulosus1
Microsporidia7Insects1
Cysticercus bovis4Myxobolus spp.1
Trematodes4Trypanosoma spp.1
Hysterothylacium spp.3Not specified127
Plerocercoids3Total885
Table 2. Number of notifications reported in the RASFF on products with Anisakis spp. by species.
Table 2. Number of notifications reported in the RASFF on products with Anisakis spp. by species.
ProductSpecies (Notifications)
MackerelAtlantic mackerel (Scomber scombrus) (109), Pacific mackerel (Scomber japonicus) (9), Atlantic horse mackerel (Trachurus trachurus) (3), Mediterranean horse mackerel (Trachurus mediterraneus) (1), Chilean jack mackerel (Trachurus murphyi) (1) and species not specified (46)
HakeEuropean hake (Merluccius merluccius) (56), Argentine hake (Merluccius hubbsi) (16), Southern hake (Merluccius australis) (2), Atlantic hake (Merluccius bilinearis) (2), South African hake (Merluccius capensis) (1) and species not specified (51)
AnglerfishEuropean anglerfish (Lophius piscatorius) (81), American anglerfish (Lophius americanus) (2), blackbellied anglerfish (Lophius budegassa) (1) and species not specified (22)
ScabbardfishSilver scabbardfish (Lepidopus caudatus) (35) and species not specified (2)
CodAtlantic cod (Gadus morhua) (13), Pacific cod (Gadus macrocephalus) (1) and species not specified (21)
AnchoviesEuropean anchovy (Engraulis encrasicolus) (14) and species not specified (19)
SquidNototodarus spp. (not specified) (20) and other species not specified (1)
John DoryJohn Dory or also Peter’s fish (Zeus faber) (17) and species not specified (2)
SalmonPink salmon (Oncorhynchus gorbuscha) (2) and species not specified (8)
HerringAtlantic herring (Clupea harengus) (2) and species not specified (7)
SwordfishSwordfish (Xiphias gladius) (3) and species not specified (6)
Other79
Total651
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Pigłowski, M. Notifications on Anisakis spp. in the Rapid Alert System for Food and Feed (RASFF) Reported in 2001–2023. Sustainability 2024, 16, 5453. https://doi.org/10.3390/su16135453

AMA Style

Pigłowski M. Notifications on Anisakis spp. in the Rapid Alert System for Food and Feed (RASFF) Reported in 2001–2023. Sustainability. 2024; 16(13):5453. https://doi.org/10.3390/su16135453

Chicago/Turabian Style

Pigłowski, Marcin. 2024. "Notifications on Anisakis spp. in the Rapid Alert System for Food and Feed (RASFF) Reported in 2001–2023" Sustainability 16, no. 13: 5453. https://doi.org/10.3390/su16135453

APA Style

Pigłowski, M. (2024). Notifications on Anisakis spp. in the Rapid Alert System for Food and Feed (RASFF) Reported in 2001–2023. Sustainability, 16(13), 5453. https://doi.org/10.3390/su16135453

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