CC BY
02021, Scienceline Publication
World's Veterinary Journal
World Vet J, 11(2): 215-227, June 25, 2021
DOI: https://dx.doi.org/10.54203/scil.2021.wvj28
Analysis of Notifications of Rapid Alert System concerning Parasites in Fishery Products
Said Dahani1*, Nourredine Bouchriti1, and Oleya Elhariri2
'Department of Veterinary Pathology and Public Health, Food Safety Unit, Hassan II Agronomic and Veterinary Institute, Rabat, Morocco 2Laboratory of Biochemistry, Biotechnology, Health and Environment, Department of Biology, Faculty of Science, University Ibn Tofail, Kenitra '4999, Morocco
»Corresponding author's Email: s.dahani@iav.ac.ma; : 0000-0002-4146-4392
ABSTRACT
Fish and fishery products are one of Morocco's most important export products. Fish parasitism is a natural worldwide phenomenon. Fish parasites have a very wide distribution and are found in both the northern and the southern hemispheres of the globe. The present study aimed to assess parasitic infestation in fishery products by analyzing notifications available in the European rapid alert system for food and feed. The analysis involved 663 notifications registered from 2001 to 2019 on the grounds of parasitic infestation. For Morocco, 651 notifications concerning the different exported food products were analyzed. Among the 663 notifications for the presence of parasites, 161 (24.3%) were border rejections. A total number of 20 countries have been detected with the presence of parasites in their exported fish and fish products. The main fish species concerned with this hazard were Hake (26%), Silver Scabbardfish (10.5%), and Angler (9.3%). In Morocco, among the 651 notifications, 373 concerned with seafood (57.2%). The number of border rejections of fishery products was 220 that is 33.8% of overall notifications. Fish and fish products category are the most concerned with 170 rejections (26.1%), with 64 notifications due to the presence of parasites (37.6%). The Silver Scabbardfish was the species most affected by parasite infestations (23.5%), followed by European Anchovy (12.5%) and Swordfish (10.9%). In conclusion, the nematode Anisakis is the most common parasite in fish infestation while the plerocercoid larvae of the Cestoda Gymnorhynchus gigas seems to have a predilection to infest the Atlantic Pomfret (Brama brama).
Keywords: Fish, Morocco, Notification, Parasite, Rapid alert system for food and feed INTRODUCTION
The fishing sector plays a major socio-economic role in Morocco and it is one of the pillars of the national economy. Morocco is one of the major fish producers worldwide, ranked 15 after Malaysia (FAO, 2020). In 2018, national fishery production reached a volume of more than 1.37 million metric tons, which represents 2% of world production. More than half of this production (52.7%) was exported to the European Union (EU) and Japan (DPM, 2018).
Fishery products represent a valuable source of nutrients and micronutrients that are crucial for healthy and diverse diets (FAO, 2018). The role of these products in the transmission of parasitic diseases to humans has been recognized (Koepper et al., 2020; Teixeira et al., 2020). The range of parasites involved is very wide, including nematodes, trematodes, and cestodes (Huss, 1998; Chai et al., 2005). Among nematodes, the Anisakidae family is the most overwhelming in human infestations with essentially two genera of Anisakis and Pseudoterranova (Smith and Wootten, 1978; Oshima, 1987).
Anisakiasis is a disease caused by ingestion of the L3 larva of parasites belonging to the anisakidae family, in raw fish, undercooked, or having undergone little or no sanitizing treatment (marinating, cold smoking, etc; Oshima, 1987). In addition, it is well established that the anisakid infestation has a significant economic impact, especially during export and discarding infested fishery products from the market at the national level since it can pose risks to customers.
The main objective of this study was to assess the extent of the parasitism phenomenon in Moroccan fishery products through the analysis of data from the European Rapid Alert System for Food and Feed (RASFF) portal between 1979 and 2019 and the development of a map of RASFF notifications concerning parasites in fishery products covering all countries, including Morocco.
MATERIALS AND METHODS
Description of the rapid alert system for food and feed system
The European RASFF was introduced in 1979. It is a notification system which mentions the hazards related to agri-food products exported to EU countries. This system is governed by Regulation (European Commission) n° 178/2002 (European Commission, 2002) and Regulation (European Union) n° 16/2011 which relates to the modalities of
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its application (European Commission, 2011). It has been repealed by Regulation (European Union) 2019/1715 laying down rules for the functioning of the system.
Search procedure in the rapid alert system for food and feed portal
The scope of this study was at first the notifications received from the RASFF system concerning the hazard "parasitic infestation" on a global scale, in particular, all countries exporting their fishery products to the EU market, then, as a practical case study, notifications from Morocco.
World database
Data were retrieved from the RASFF portal (Accessed April 23, 2020). The search criteria for RASFF notifications of parasites in fishery products are as follows: date of notification (From 01/01/1979 to 31/12/2019), type of product (Food and product category, entailing Fish and fish products), and Risk category, including parasitic infestation. This research on the RASFF portal provided access to 663 entries.
Morocco database
The RASFF notifications from Morocco are as follows: date of notification: From 01/01/1979 to 31/12/2019, type of product: Food, Country (flagged as origin: Morocco). Searching on "Morocco database" yielded 651 entries representing all the notifications involving Moroccan food exported to the EU. The obtained findings from RASFF notifications are summarized in Table 1.
Table 1. Results for notifications on the rapid alert system for the food and feed portal
Database Search time interval Effective time interval (given by the portal RASFF) Reason for notifications Number of data
World database From 01/01/1979 to 31/12/2019 01/01/2001-31/12/2019 Parasitic infestation 663
Morocco database From 01/01/1979 to 31/12/2019 01/10/1981 -31/12/2019 All hazards motives 651
Data processing
For the World database, the data was processed according to the type of notifications. Subsequently, a detailed analysis of backflow notifications was carried out according to the country of origin, species of fish, and parasites. Regarding the Morocco database, an overall analysis of notifications by product was carried out to show the importance of notifications of fishery products. Afterwards, rejections were analyzed according to the category and the nature of the fishery products, and the evolution of the rejections between 2008 and 2019. Furthermore, an analysis of the causes for rejections of fish exports was carried out to highlight the importance of parasitic infestation in fish and fish products. Finally, an analysis of parasite rejections, depending on the species of fish and the species of parasite, was conducted.
RESULTS AND DISCUSSION
Global analysis of the rapid alert system for food and feed portal notifications concerning parasites in fishery products
Global analysis of notifications
Over the past 40 years (1979 to 2019), the RASSF portal has reported 663 notifications of parasites for fishery products exported from countries. Those notifications (Table 2) can be divided into alerts (21%), information (22.2%) and border rejections accounting for 161 notifications (24.3%). The average annual number of parasite notifications is 35 (one notification/10 days). The maximum number of notifications was recorded in 2009, 2010, and 2011 with a total of 250 notifications. Since 2011, the number of notifications has gradually decreased to stabilize at 39 during 2017-2019 (Figure 1). Official control on the European market was the main source of these notifications (50.4%), followed by border control (32%). Notifications following consumer complaints and the establishment of self-monitoring accounted for 8.1% and 5.1%, respectively (Table 3). The reporting basis was not defined in 2001 and 2002 (3.2%).
Table 2. Distribution of notifications concerning parasites in fishery products
Type of notifications Number Percentage
Rejection 161 24.3
Information 147 22.2
Alert 139 21.0
information for follow-up 136 20.5
Information for attention 80 12.0
Total 663 100
216
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51
8 13 10 8 I I
39 39
10 16 11 22
2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019
Year
Figure 1. Evolution of rapid alert system for food and feed notifications of fishery products for parasitic infestation
0
Table 3. Main sources of notifications for the parasitic infestation in fishery products
Notification base_Number_Percentage
Border control 212 32
Establishment self-monitoring 34 5.1
Consumer complaints 54 8.1
Official control on the market 334 50.4
Official control after of notifications RASFF 8 1.2
Without notification base 21 3.2
Total 663 100
Analysis of rejections
Evolution of rejections between 2008 and 2019
The number of rejections is a valuable indicator of the effectiveness of control and self-monitoring systems implemented by third-world countries exporting their products to the EU. Their analysis allows establishing a health profile by the country. The first rejections of fishery products due to parasitic infestation were recorded in the portal in 2008. Over 12 years, the total number of rejections concerning parasites in fishery products was 161, which represents an average of 13 to 14 rejections per year. The most critical period was between 2009 and 2011, during which 105 rejections (65%) were notified. Subsequently, the number gradually decreased to reach only 8 rejections in 2019 (Figure 2).
45
41
2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019
Year
Figure 2. Evolution of rejections of fishery products for parasitic infestation
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Main causes for fish products rejections
Notifications by countries
About 20 countries have been notified on grounds of parasitic infestation. Table 4 presents the concerned countries as well as their corresponding number of seafood rejections. As shown in Table 4, Morocco was mostly notified for rejections with 64 notifications, followed by Croatia (21 rejections), China (15 rejections), and Argentina (12 rejections).
These numbers should be treated with caution as they must be related to the number and/or the quantities of exported seafood. Furthermore, it should be noted that fishery products most affected by parasites were fresh products. Given Morocco's geographic proximity to EU countries, it is common to export large quantities of fresh fishery products, which explains Morocco's ranking as the first notified country, which is much more related to the nature of the exported product. Still, these data showed with supporting evidence that the parasite infestation of fish products is a worldwide concern.
Regarding worldwide repartitions of rejections by continent, the African countries record the maximum rejections number with 49% due to parasite infestation, followed by European (22%) and American countries (15%). Asian countries and Australia account for only 10% and 4%, respectively. Table 5 shows the rejections of fishery products according to the countries of origin and the reporting countries. Spain is the gateway for fishery products to the EU. As a result, it a notified products just from 9 countries. Italy comes second by 6 countries, followed by Lithuania (n = 4). For countries of origin, China has been notified by 5 member states, followed by Argentina (n = 4).
Table 4. List of countries notified of parasitic infestation in fishery products
Country of origin Number of rejections Country of origin Number of rejections
Morocco 64 Spain 3
Croatia 21 Namibia 3
China 15 South Africa 2
Argentina 12 Albania 2
Tunisia 7 Chile 2
USA 6 Ghana 1
New Zealand 6 Mauritania 1
Russia 5 Senegal 1
Canada 4 Sri Lanka 1
Falkland Islands 4 Ukraine 1
Table 5. Notifications of rapid alert system for parasitic contamination of food and feed in different countries and origins
Notifying countries
Germany Bulgaria Spain Estonia Greece Italy Lithuania Poland
South Africa 2
Albania 2
Argentina 2 3 3 3
Canada 1 2 1
Chile 2
China 4 5 3 1 2
Croatia 21
Spain 3
USA 5
Falkland Islands 4
Morocco 64
Mauritania 1
Namibia 3
New Zealand 6
Russia 5
Senegal 1
Sri Lanka 1
Tunisia 7
Ukraine 1
Notifications by category of commodity
Fresh, frozen, chilled, and canned fishery products have been subjected to border rejection. The maximum number of rejections was for fish in the chilled state (n = 76), followed by fish in the frozen state (n = 43). Notifications for
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which the nature of the product was not specified constitute a proportion of 25%. The occurrence of parasites was hence more prevalent in chilled and frozen fish. The parasitic infestation was a minor problem with canned goods.
Notifications by fish species
Regarding families and fish species, Figure 5 illustrates the main fish species as well as their corresponding number of rejections. The number of notified species is 23, but this number could be higher since several notifications do not mention the species name. During the last 12 years, hake (Merluccius merluccius) was the most rejected species for the presence of parasites (n = 42, 26.4%), followed by Silver Scabbardfish (Lepidopus caudatus, n = 17, 10.7%), and John Dory (Zeus faber) recorded 12 rejections (7.5%). Swordfish (Xiphias gladius) and European anchovy (Engraulus encrasicolus) were reported 10 and 8 times, respectively, for parasitic infestation (Figure 3). As can be seen in Figure 3, the two species of freshwater fish were subjected to rejections (Northern pike, Esox lucius) and pike-perch (Stizostedion lucioperca). The Hake family was the most rejected family for parasitic infestation (26.7%), followed by the Trichiuridae (10.6%), and Lophiidae (9.3%) families. The families of Gadidae and Zeidae constitute 7.5% of rejections each. Xiphiids represents 6.2% of the rejections.
Not specified
Northern Bluefin Tuna Redfish Salmon European Pilchard Atlantic Horse Mackerel European Conger Flounder Common Pandora Marlin-spike Pike Perche Snook Blacktip grouper Silver Comber Large catsagnole Blue Whiting Alaska Pollock Atlantic Mackerel European Anchovy Swordfish John Dory Angler Silver Scabbardfish European Hake
0 5 10 15 20 25 30 35 40 45
Number of rejections
Figure 3. Number of rejections depending on the species of fish between 2008 and 2019
Parasite species
Concerning parasite species, out of 161 border rejections for parasitic infestation, Anisakis represents the most frequently implicated parasite responsible for 72.7% of rejections, followed by the plerocercoid larvae of the Cestoda Gymnorhynchus gigas, Microsporidia, and Philometra spp. with the same proportion, 2.5% each (Table 6). Nematodes of the genus Anisakis are, therefore, a problem of a global dimension. Table 7 shows a list of fish species rejected for Anisakis infestation as well as their countries of origin. Using the data in tables 4 and 7, a map was established to show the origin of the fishery products rejected for parasite reasons (Figure 4). This map shows that fish parasites have a very wide distribution and are found in both the northern and the southern hemispheres.
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Table 6. Number of rejections depending on the species of parasite
Group Type Species Number of rejections Percentage
Anisakis 117 72.7
Nematodes Philometra spp. 4 2.5
Helminths Other 2 1.2
Gymnorhynchus gigas 4 2.5
Cestodes Nybelinia spp. 1 0.6
Trypanorhyncha 1 0.6
Total 129 80.2
Microsporidia Microsporidia Spraguealophii 4 1 2.5 0.6
Myxosporidia Kudoa 1 0.6
Total 6 3.7
Not-specified 26 16.1
Table 7. Rejections of fish species infested by Anisakis and their countries of origin
Species Number of rejections Countries of origin (rejections)
Croatia (18)
Argentina (4)
China (3)
European Hake 32 Morocco (3) New Zealand (1) Canada (1) Spain (1) Albania (1)
Silver Scabbardfish 13 Morocco Morocco (6)
John Dory 10 Tunisia (3) Mauritania (1)
EuropeanAnchovy 8 Morocco
Swordfish 7 Morocco
Angler 5 United States
Chub Mackerel 4 Croatia (2) Morocco (2) Croatie
Atlantic mackerel 3 Morocco Tunisia Albania
Hake 3 Canada China
Silver Hake 2 Argentina Spain
Largehead Hairtail 2 Morocco
Silver Comber 2 Argentina
Blacktip Grouper Southernhake 1 1 New Zealand
European Conger 1
European Pilchard 1 Morocco
Northern Bluefin Tuna 1
Flounder Alaska Pollock 1 1 China
North Pacific Hake Redfish 1 1 Canada
Atlantic Horse Mackerel 1 Croatia
Blue Whiting 1 Falkland Islands
Common Pandora 1 Argentina
Pike-Perch 1 Ukraine
Pink Salmon (Oncorhynchus gorbuscha) 1 Russia
Not specified 13 Morocco
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Figure 4. Distribution of the fishery products rejected for the presence of parasites Important actions taken by the notifying countries
The major source of rejection notifications is border control. Fishery products turned away due to parasites are either disposed of at border posts (37.3%) or returned to the countries of origin (35.4%). These two actions are not well specified in some cases (13.7%). The rest of the products are owned by member states (6.2%) or banned from entering European territory (5%, Figure 5). The majority of notifications were reported by Spain (55.3%), followed by Italy (24.2%), Lithuania (6.2%), and Greece (3.1%, Table 8).
Table 8. List of notifying countries with the number of notifications
Notifying countries Number of notifications (%)
Spain 89 (55.3)
Italy 39 (24.2)
Lithuania 10 (6.2)
Greece 5 (3.1)
Bulgaria 4 (2.5)
Germany 4 (2.5)
Poland 4 (2.5)
Estonia 3 (1.9)
France 1 (0.6)
Romania 1 (0.6)
United Kingdom 1 (0.6)
Withdrawal from the market
Rejection | Official detention | Disposal or Re-dispatch Re-dispatch Disposal
0 10 20 30 40 50 60 70 Number of notfications
Figure 5. Importance of actions taken by notifying countries
Analysis of rapid alert system for food and feed notifications of Moroccan fishery products exported to the European Union
Analysis of notifications relating to fishery products number and evolution of notifications
Between 1981 and 2019, the RASFF portal reported 373 notifications for fishery products exported from Morocco to the EU. The "Fish and fish products" category is the one most affected with 295 notifications (80%). The two categories "Cephalopods and derived products" and "Crustaceans and derived products" constitute 9.4% and 9% of the notifications, respectively (Table 9).
Global analysis of border rejections of Moroccan fishery products
Over 12 years, the total number of rejections of fishery products was 220, which corresponds to an average rejections number of 18 per year. Fishery products account for more than two-thirds of rejected products (70%). Table 10 indicates the number and percentage of rejections for each category of fishery products. The "Fish and derived products"
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category was the most affected with 170 rejections (77.3%), followed by cephalopods and derived products with 33 rejections (15%, Table 10).
Table 9. Notification numbers of fishery products between 1981 and 2019
Product category
Number de notifications
Percentage
Fish and fish products Cephalopods and derived products
Crustaceans and derived products
Bivalve molluscs and derived products
Total
295 35
34
9
373
79.1 9.4
9.1
2.4
100
Table 10. Notifications of rejections of the different categories of fishery products between 2008 and 2019
Product category
Fishery products Fish and fish products Cephalopods and derived products Crustaceans and derived products Bivalve molluscs and derived products
Other types of food Total
Number of rejection Percentage
220 70.1
170 77.3
33 15.0
14 6.3
3 1.4
94 29.9
314 100
Evolution of rejection notifications of fishery products from 2008 to 2019
During 2008-2010, the number of rejections contributes to 16.8% (n = 37) in fishery product rejections. Most of them involve the category of fish and fish products (n = 33) and the rest crustaceans and their products. The main reasons for rejections are parasite infestation and poor hygiene. The rejections between 2010 and 2019 constitute 83.2% of rejections of fishery products (n = 183). Regarding the rejections of fishery products exported via Morocco to the EU, the first three years had several rejections, especially in 2011 (23%) due to the large number of rejections resulted from parasites of the fish products. The number of rejections fell from 2013 and rise again in 2019 (11.4% of rejections). During this period, most of the rejections were due to the failure of the cold chain and parasitic infestation. This can be explained by the reinforced control of the competent authorities. The findings indicated that after 2011, there was a steady decrease in rejections year after year. The same observation, therefore, concerns the rejection of fishery products (Figure 6). In 2019, the number of rejections of fishery products was higher than the previous five years, reaching 21 out of 23.
50 45 40 35 30 25 20 15 10 5 0
2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 Number of rejections 9 Rejections of fishery products number Figure 6. Rejections numbers of fishery products from 2010 to 2019
The decrease in the number of rejections notifications can be attributed mainly to strengthening the sanitary control of fishery products in terms of parasite research by the competent Moroccan authorities following the publication of law 28-07 underlying food safety, as well as by professionals within the framework of self-control (NFSO, 2010). The 2011 peak is attributed to the presence of rejections for parasitic hazards and also to notifications for the presence of high histamine levels. Following this increase, the Moroccan competent authority has put in place an action plan by
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strengthening controls along the food chain. Food business operators (FBOs) for their part have reviewed their health control plans. The collaboration and cooperation between the Moroccan competent authority and FBOs led to good results in the following years and which is confirmed in the results of this synthesis (Elhariri et al., 2017). In April 2010, the European Food Safety Authority (EFSA) adopted a scientific opinion on the assessment of the risk associated with parasites in fishery products. This scientific advice includes information for the health risk versus the presence of viable parasites in fishery products. According to EFSA opinion, all wild fish caught in seawater or freshwater is likely to contain parasites that pose a risk to human health. Fish to be used to produce raw or almost raw seafood products should be frozen prior to processing. However, the competent authorities may adopt national measures granting an exemption from the freezing treatment obligation for fishery products. These national measures must be notified to the committee (EFSA, 2010).
Analysis of rejections for parasitic infestation
During 1981-2019, notifications of rejections concerning fish and their derivatives for the presence of parasites constitute 37.6% of the notifications in this category or 64 rejections. The trend in rejections from 2010 to 2019 peaked in 2011 with 19 rejections accounting for 11%. Subsequently, the number of rejections gradually decreased with an average of 3 rejections per year (Figure 7). Scabbard fish is the species most affected by rejection due to parasitic infestation with 15 rejections for silver Scabbard fish and 2 for the common Scabbard fish. Anchovy registered the second position with 8 rejections in 2011 and 2014, followed by the Swordfish with 7 rejections. According to the obtained results, John Dory had 6 rejections, 5 of which have been recorded over the past three years, and hake had 4 border rejections (Table 11). Scabbard fish is the most infested species by parasites in Moroccan fishery products and hake is the most infested globally. This heavy infestation is mainly related to their diet and their large size. A positive correlation between the size of the fish and the number of parasites collected has already been observed in the Silver Scabbard fish (Bouchriti et al., 2015).
40 35 30 25
o
s. 20
■Rejection
Global rejection
-Annual average
■e
S =
z
15
10
2010 2011 2012 2013 2014 2015 2016 2017 2018 2019
Year
Figure 7. Rejection numbers of fish and derived products infested with parasites during 2010-2019
5
0
Based on the living environment of the fish, a possible difference was noticed. Bathypelagic species are the most prone to parasitism with a percentage of 47.1%. Pelagic fish represents 39.2% of rejections for parasitic reasons while benthic fish indicates only 13.7% (Table 12). The Silver Scabbard fish has a silvery, elongated, and compressed body, which is commonly 50 to 150 cm long and can reach up to 210 cm, with a maximum weight of 8 kg. Lepidopus caudatus is benthopelagic fish. It lives 60 meters on the continental shelf and beyond the slope up to 600 meters deep, generally on sandy and muddy bottoms from 100 to 300 m, but sometimes in coastal areas of the resurgence of deep water (Nakamura and Parin, 1993). The Scabbardfish are active predators that feed on fish, squid, and crustaceans that are intermediate hosts for the parasites. The hake is a benthopelagic or bathypelagic fish generally living at depths of 70-370 m on the edge of the continental slope, but it can be found in coastal waters up to about 1000 m depth. It measures up to 130 cm in length. Adult hake feeds mainly on fish (anchovies, sardines, herring, and cod) and squid. The young feed on crustaceans (especially euphausiids and amphipods, Cohen et al, 1990). Regarding parasite species, the two main species of parasite incriminated in fish infestations are Anisakis spp. (90.5%) in several species of fish and Gymnorhynchus gigas found in the Atlantic Pomfret (Table 13).
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Table 11. Number of rejections of fishery products based on the species of fish
Family Scientific name Common name Number of rejections Year
Bramidae Brama brama Atlantic Pomfret 4 2009
1 2009
1 2010
1 2011
Lepidopus caudatus Silver Scabbard fish 3 3 3 2 1 2012 2013 2014 2016 2017
Trichiuridae
Trichiurus lepturus Largehead Hairtail 1 1 2010 2011
Xiphiidae Xiphias gladius Swordfish 4 3 2009 2010
Engraulidae Engraulis encrasicholus European Anchovy 7 1 2011 2014
Merlucciidae Merluccius merluccius European Hake 2 1 2011 2016
Clupeidae Sardina pilchardus European Pilchard 1 2012
Scombridae Scomber spp. Atlantic Mackerel 1 2 2012 2014
Thunnus thunnus Northern Bluefin Tuna 1 1 2012 2012
Zeidae Zeus faber John Dory 1 1 3 2017 2018 2019
Congridae Conger conger European Conger 1 2014
Table 12. Occurrence of rejections of fishery products based on the living environment of fish types
Types of fish
Species
Number of rejections
Percentage (%)
Pelagic
European Anchovy Atlantic Mackerel European Pilchard Swordfish
Northern Bluefin Tuna
20
39.2
Benthic
European Conger John Dory_
13.7
Bathypelagic
Atlantic Pomfret European Hake Large head Hairtail Silver Scabbardfish
24
47.1
7
Table 13. Number of repressions depending on the species of parasite and fish
Species parasites Species Number of rejections Percent
Anisakis spp. Silver Scabbardfish, Largehead Hairtail (Lepidopus caudatus, Trichiurus lepturus) European Anchovy (Engraulis spp.) Swordfish (Xiphias gladius) John Dory (Zeus faber) Atlantic Mackerel (Scomber spp.) European Hake(Merluccius merluccius) European Pilchard (Sardina pilchardus) European Conger (Conger conger) Northern Bluefin Tuna (Thunnus thunnus) Not specified 15 8 7 6 3 3 1 1 1 13 23.4 12.5 10.9 9.4 4.7 4.7 1.6 1.6 1.6 20.2
Gymnorhynchus gigas Atlantic Pomfret (Brama brama) 4 6.3
Not specified Silver Scabbardfish (Lepidopus caudatus) 2 3.2
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It should be noted that the number of fishery products exported from Morocco during 2010-2019 was 5,363,674 metric tons (DPM, 2019). The total quantity of rejections due to parasite presence during these 10 years was 165 tons. The quantities rejected for the presence of parasites represent 0.003% of the total exported quantity, which is a very low rate. Despite the importance of parasitic infestation notifications, their economic impact is of a low magnitude nationwide. However, this impact may be severe for packaging the fishery products affected by the infestation.
According to previous field studies, nematodes (anisakis and acanthocephalic complex) are the parasites frequently found in seafood on the Moroccan coast, with a prevalence of 21.4% in the Atlantic coast and 24.9% in the Mediterranean (Benabbes and Boudakkou, 2019). The plerocercoid larva of the Cestoda Gymnorhynchus gigas was exclusively found in the Atlantic Pomfret (Brama brama) with a prevalence of 89.5%. This internal parasite, found in the flesh of the fish, seems to have a certain predilection for this species. The silver Scabbardfish (Lepidopus caudatus) is known to be frequently and sometimes heavily infested by Anisakis spp. (Benabbes and Boudakkou, 2019).
A comparison of the research undertaken on the occurrence of parasites in Moroccan coastal waters revealed that this natural phenomenon of parasitism had slightly increased in the Mediterranean and decreased in the Atlantic. According to a study carried out between 1978 and 2015 on changes in the abundance of the two genera of nematodes (anisakis and pseudoterranova), it was found that the abundance of Anisakis spp. saw a significant 283-fold increase and no modification for Pseudoterranova spp. (Fiorenza et al., 2020). The worldwide increase in the abundance of Anisakis spp. may have faster consequences for human health, the health of marine mammals, and the performance of fisheries.
Fish parasitism is a worldwide phenomenon and is more commonly associated with marine environments than continental ones. The factors responsible for the re-emergence of parasites in different regions of the world are the intensification of fish production, environmental alteration, movement of animals and humans, and increased trade in fishery products (Chai et al., 2005).
The Anisakis complex, in particular, is expanding across the global ocean. Several answers can be advanced about the spread of this parasite in recent decades. Several potential factors may be involved, including climate change, increased nutrients, and increased marine mammal populations. As parasites with a complex life cycle, anisakidae can respond to changes in abundance of any definitive or intermediate host (marine mammal, crustacean, or fish) (Arneberg et al., 1998). However, it is almost impossible to know the most critical host in the abundance of anisakidae, that is, the bottleneck in the parasite's life cycle (Lafferty, 2012).
Since the adoption of the Marine Mammal Protection Act in 1972 and the adherence of many countries to the moratorium on commercial whaling imposed by the International Whaling Commission in 1982, the abundance of many species of marine mammals (definitive host) increased (Magera et al., 2013). This increase could lead to an increase in transmission of anisakidae in case the definitive mammalian hosts are the bottleneck of the life cycle (Lafferty, 2012). The replenishment of many populations of marine mammals may explain the increase in the abundance of Anisakis.
On the other hand, fish, crustaceans, and cephalopods are key intermediate and paratenic hosts for anisakidae, and their abundance has fluctuated widely over the past half-century (Christensen et al., 2014). Fishing has altered the abundance and density of many fish (Anderson et al., 2008). For example, Atlantic cod have experienced a decline on the northeastern coast of North America (Lilly et al., 2008) while cephalopods have increased in abundance (Doubleday et al., 2016).
Intensification of fish production or increased fishing pressure may lead to a decrease in the abundance of host fish and consequently, reduced transmission and abundance of Anisakis (Lafferty, 2012). However, if host fish are not the life cycle bottleneck, decreases in the abundance of intermediate hosts could lead to an increase in the concentration of parasites in the remaining hosts, resulting in an increase in the abundance of parasites (Wood et al., 2013). Long-term climate change could also influence the abundance of anisakid nematodes. The increase in temperature increases the susceptibility of hosts to disease and increases the pathogenicity of pathogens and parasites (Harvell et al., 2002; Burge et al., 2014). This could lead to an increased infestation of host fish, as these species lose their ability to resist infection when temperatures rise beyond the optimum. The temperature rise can also lead to the faster growth of Anisakis nematodes (Marcogliese, 2001).
On the other hand, the increased nutrient load of coastal ecosystems can produce phytoplankton blooms that can feed filter crustaceans (intermediate hosts) (Trainer et al., 2003). Increases in nutrients may facilitate increases in Anisakis spp., as crustacean hosts of Anisakid nematodes are sensitive to these environmental alterations.
CONCLUSION
The analysis of the data available on the rapid alert system for the food and feed portal has enabled us to draw some conclusions on the parasite profile of fishery products. The main hazard for fish and fish products border rejections is a parasitic infestation. Spain is the main reporting country as it is the gateway for fishery products to the EU. Since 2011, the number of rejections of fish and fish products has decreased steadily due to the strengthening control by the Moroccan health authority and professionals. Border control in the EU plays a crucial role in detecting and preventing
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nonconformities before the distribution of products in the market. The occurrence of parasites prevails in fresh fish. The silver Scabbardfish (Lepidopus caudatus) is the species most affected by parasitic infestations in Morocco and hake (Merluccius spp.) is the most infested by parasites worldwide because of their living environment and diet. The Anisakis complex is a parasite frequently implicated in the infestation of fish. The parasite Gymnorhynchus gigas seems to specifically infest the species Brama brama.
DECLARATIONS
Authors' contribution
All the authors contributed to the research in RASFF portal of the notification data, their analysis as well as the writing of the final manuscript. The authors confirmed the content of the final manuscript for publication in this journal.
Competing interests
The authors of the present study declared that there is no financial or unethical conflict related to this work, which can negatively impact its publication.
Acknowledgments
The authors acknowledge Prof. Abdellah Zineddine, Dr. Naoual Alahlah, and Mr. Aymen Moqtani for their precious contribution.
Ethical considerations
All ethical issues (including plagiarism, consent to publish, misconduct, data fabrication and/or falsification, double publication and/or submission, and redundancy) have been checked and approved by all authors.
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