Major Parasites in Fish Affecting Public Health

Abstract

In Morocco, the fishing sector plays a crucial socio-economic role and constitutes one of the cornerstones of the country’s economy. However, the role of these products in transmitting parasitic diseases to humans has been acknowledged. The issue of parasites in fish holds significant importance in terms of health, socio-economics, media coverage, and environmental impact. The primary parasites found in fish include nematodes (Anisakis), cestodes (Gymnorhynchus gigas), protozoa, and isopods. Anisakids take the lead in terms of prevalence in certain fish species, causing the anisakiasis disease in humans. Preventing these diseases in humans relies on actively searching for parasites in fish that are visibly parasitized before their commercialization in the market. Mastering the hazard of “parasites in fish” for humans is a shared responsibility between fishing industry professionals and the relevant health authorities.

1. Introduction

The fishing sector plays a crucial socio-economic role in Morocco and constitutes one of the pillars of the national economy. However, the role of these products in transmitting parasitic diseases to humans has been recognized. To date, the consumption of raw fish is increasingly widespread globally, which represents an emerging risks for consumers. Indeed, the role of fish products in transmitting parasitic diseases to humans is well-established. They may contain parasites, including those from the Anisakidae family, which is most implicated in human infestations, primarily with two genera: Anisakis and Pseudoterranova.

Parasites are naturally present in fish of all species worldwide. Specifically, Anisakidae circulate in the marine ecosystem, using marine mammals, birds, or fish as definitive hosts. Through the consumption of raw, undercooked, or inadequately processed fish, humans become accidental hosts. Nevertheless, the ingested Anisakidae cannot reach the adult stage in humans.

2. Replace main parasites of fishery products

Like any animal species, fish and cephalopods (mollusks) are susceptible to parasites. These parasites are naturally present in the marine environment, fish and cephalopods are part of their life cycle. Among them, the Anisakidae family (Anisakis and Pseudoterranova) poses a hazard to consumer health and can be responsible for anisakidosis in humans.

2.1 Anisakids

Zoonoses account for approximately 75% of emerging diseases. The increasing attention to foodborne zoonoses is the result of two main factors. The first is the rising prevalence of these diseases linked to changes in dietary habits, an increasing rate of international travel, trade exchanges, as well as cultural and demographic changes. The second factor is related to improved diagnostic capabilities through advanced techniques and a higher number of instrumental investigations [1].

However, parasitic zoonoses remain insufficiently studied because their actual and potential economic and health impact are not well unknown. Any infestation caused by nematode larvae belonging to various genera of the Anisakidae family is called anisakidosis, which manifests as either acute or chronic gastric or intestinal forms after several hours to several days, months, or even years post-infestation. The most common Anisakids in humans are Pseudoterranova, such as Pseudoterranova decipiens, and Anisakis simplex, the latter can also induce allergic problems. Moreover, some 33 allergens of Anisakis simplex are thermostable, increasing the allergic risk for consumers. Allergies can result in hives, itching, angioedema, bronchospasm, or, more rarely, anaphylactic shock. Other less common Anisakids in humans, Contracaecum spp., which can pose public health issues but remain very rare. Hysterothylacium spp. does not cause any public health problems as it is destroyed at a temperature of 37°C. However, like other genera, its presence in fish can lead to rejection by the consumer.

Indeed, anisakidosis has around 20,000 reported cases to date, with the vast majority (90%) in Japan. Human anisakidosis is usually more common than human pseudoterranovosis in Japan and Europe, although in North America, Pseudoterranova spp. is the most frequent. Cases of human pseudoterranovosis have been reported in Chile and Peru [2].

2.1.1 Morphology

For the classification and differentiation of various genera within the Anisakidae family, criteria such as the morphology of excretory and digestive systems, as well as the sexual organ (spicule), are used [2]. However, the similarity and the morphological resemblance of these worms, including size, shape, differences between males and females, the presence or not of the cuticular striations on the body, as well as the shape of the head and tail, unfortunately complicate their identification [3].

2.1.1.1 Anisakis

The name Anisakis is composed of “anis-” (a Greek prefix meaning different) and “akis” (Greek for spine or spicule). The worms belonging to the genus Anisakis are usually found in herring, which serves as the paratenic host, and in whales, which are the definitive hosts.

Anisakis, being nematodes, are unsegmented roundworms with a thick cuticle, ranging in color from light white to yellowish, measuring 2 to 6 cm in length and a few millimeters in diameter. The cuticle is characterized by large, irregular, and discontinuous transverse grooves across the body, with fine parallel ridges between the grooves. On a live larva, a visible white portion of 2 mm in length corresponds to the esophageal ventricle. At the other end, there is a triangular penetration tooth, next to which is the excretory pore followed by the excretory canal.

The larva has a ring-shaped nervous system. Regarding internal morphology, the larva possesses a complete digestive system consisting of a trilabiate mouth (one dorsal and two subventral), an esophagus with two parts (an anterior muscular and a posterior glandular), ending in the anus. The excretory system terminates in ventro-lateral lips, and numerous peri-anal papillae are present. There is no cecum or esophageal appendix [4].

The L3 larva found in fish can measure from 9 to 39 mm in length. Whitish in color, it may be coiled and encysted. Most L3 larvae are located in the body cavity, on the liver, and on the wall of the digestive tract, and less commonly, in the flesh of the fish (Figure 1).

Figure 1.

Larva of Anisakis spp. in Silver scabbardfish.

2.1.1.2 Pseudoterranova

Worms of the genus Pseudoterranova are also known as codworms or sealworms. The L3 larvae of these worms are typically found in the flesh of fish and less commonly in the visceral cavity. The larvae found in fish measure approximately 9 to 58 mm in length and can have a whitish-cream, yellow-brown, or reddish-brown color. They are coiled within irregularly shaped cysts. Morphologically, they are characterized by the presence of an anterior boring tooth near the excretory pore. The esophagus consists of a relatively long proventriculus and a ventricle. The intestine, located immediately behind the ventricle, extends forward as a cecum (retrograde) and narrows backward to enter the rectum, which opens at the anus. The posterior end of the larva bears a small spine called the mucron [5].

2.1.1.3 Contracaecum

The worms belonging to the Contracaecum spp. genus are whitish-yellow to greenish, and sometimes tinged with red. They have a length of 1.5 to 28.1 mm and a width of 0.13 to 1.18 mm. In adults, males measure between 15 and 70 mm in length and 0.8 to 1.5 mm in width, while females measure between 15 and 90 mm in length and 0.8 to 2 mm in width. The larvae have a pointed tail without a mucron. The excretory pore opens between the two subventral lips. The piercing tooth is small. The esophageal appendix is longer than the cecal appendix. The caudal papillae consist of 2 pairs subventrally and 2 to 3 pairs sublaterally [6, 7, 8].

2.1.1.4 Hysterothylacium

Worms belonging to the genus Hysterothylacium spp. are Anisakidae with a whitish to gray and highly active larva. The larva has a length of 1.5 to 2.5 mm, and the female can reach 8 cm. They have fish as definitive hosts, with the same individual hosting both larval and adult forms. Hysterothylacium does not pose health problems for humans as they are killed at low temperatures. They are very active at 10°C but die at 30°C. The survival of these larvae requires a low temperature [2].

The nematode is characterized by a three-lipped head, each with a pair of triangular ridges, and the presence of semi-interlabia and cervical wings. The worm also has a cuticle with fine transverse striations, an anterior cecum and an esophageal ventricle with a posterior appendix; the appendix and cecum are roughly equal in size, the excretory pore is located at the level of the neural ring, the tail has a terminal “cactus,” and the male spicules are approximately equal in size [9].

2.1.2 Life cycle

The Anisakidae have a heteroxenous life cycle (Figure 2). Unembryonated eggs of Anisakidae are excreted with the feces of the definitive host into the marine environment. The larvae L1, L2, and L3 mature within the egg before hatching into free-living L3 larvae in the marine environment. The hatching rate of the larvae depends on the water temperature, with higher temperatures leading to faster hatching [10].

Figure 2.

Anisakis life cycle [2].

The free-living L3 larvae are more often ingested by crustaceans (shrimp, crab, amphipod, krill, etc.), intermediate hosts. Fish and cephalopods then act as paratenic hosts by feeding on the infected crustaceans. If a fish or mollusk carrying L3 larvae is ingested by another non-definitive predator fish, the capsules containing Anisakidae larvae are digested, and the larvae encyst again in this new host, which, in turn, plays the role of a paratenic host. This is crucial from an epidemiological and food safety perspective as larvae can be transferred from one fish to another, leading to an accumulation of these parasites throughout the food chain. Some Anisakidae migrate from the digestive tract to the body cavity and reach various organs. Definitive hosts for the genera Pseudoterranova and Anisakis are marine mammals, while Contracaecum also includes piscivorous birds. Hysterothylacium has predator fish as definitive hosts.

After being ingested by this definitive host, L3 develops into L4, L5, and then reaches adulthood and sexual maturity. In some cases, L3 does not progress to the adult stage and causes definitive eosinophilic granulomas, as seen in the Balaena mysticetus [11].

Humans are accidental hosts that do not allow the normal development of the larva. Infection occurs through the ingestion of L3 larvae present in raw or undercooked fish. These larvae can cause two types of pathologies: digestive and allergic [10].

Other accidental hosts have been mentioned in the literature, including mammals such as bears, monkeys, dogs [12], cats, raccoons [13], birds, amphibians, and reptiles such as turtles [14], and crocodiles [15].

2.1.3 Impact of Anisakidae on public health

The first case of Anisakid disease was described in 1876 by Leuckart [16]; however, the disease was not widely recognized until the 1960. The larva was identified as A. simplex at the 3rd larval stage. Since that time, numerous cases of this zoonotic infestation have been described in other countries, such as Japan where the consumption of raw fish is common. Over 20,000 cases of anisakiasis had been reported worldwide by EFSA on 2010, with the highest prevalence (over 90%) coming from Japan, reporting an annual rate of 2000 to 3000 cases of anisakiasis. The adoption of diverse cuisines worldwide, the development of better diagnostic tools, and an improved understanding of Anisakis and its infestation have led to a significant increase in the reporting of anisakiasis cases. Among other countries where anisakiasis cases have been reported are Korea, China, Malaysia, Taiwan, the UK, Australia, Spain, Italy, France, Germany, Denmark, Norway, Croatia, the USA, South America, Egypt, South Africa, indicating the presence of anisakiasis on every continent except Antarctica.

A strong tradition of consuming raw or undercooked fish, through traditional recipes such as “ceviche” in South America, marinated anchovies in Spain, and raw fish prepared in traditional Japanese dishes like “sushi” and “sashimi,” coupled with an exponential increase in the number of restaurants worldwide, are the major risk factors for the spread of anisakiasis [17].

2.1.3.1 Pathogenic power

Humans are accidental hosts of the Anisakis parasite. Infestation occurs through the consumption of fish and marine crustaceans contaminated with third-stage larvae. Two main mechanisms are believed to be responsible for anisakiasis: allergic reactions and direct tissue damage resulting from the penetration of larvae into the site of the target organ [2].

The survival duration of Anisakis in humans is very short, and they are typically expelled or destroyed within a few days or weeks. However, a few hours after ingesting this parasite through an infested fish, the worm burrows into the human intestinal wall, causing an acute and transient infection with symptoms such as abdominal pain, vomiting, or diarrhea. The invasion of the intestinal wall by the parasite sometimes leads to the development of a granuloma or perforation, causing direct tissue damage.

The part of the gastrointestinal tract in which the Anisakis larva lodges, and the type of Anisakis spp. ingested, largely determine the clinical manifestations of observed anisakiasis. Penetration of the gastric mucosa leads to inflammation, giving rise to some of the symptoms. Anisakis can cause gastrointestinal infections, which can be classified into acute, chronic, ectopic, or allergic reactions [17].

2.1.3.2 Gastric form

In gastric anisakiasis, a predilection for penetration into the greater curvature of the stomach has been suggested. The larva burrows into the walls of the stomach. Typically, significant edema of the gastric mucosa around the penetration site is observed through endoscopy. The typical clinical presentation is often reported as acute and severe epigastric pain, nausea, vomiting, mild fever, excessive salivation, and heartburn occurring a few hours after the consumption of infected fish, with symptoms developing within 12 hours [8].

2.1.3.3 Intestinal form

Intestinal anisakiasis presents with non-specific clinical features such as nausea, vomiting, or diarrhea, typically developing 1 to 5 days after the consumption of infected fish. It is known to take more time for symptoms of intestinal anisakiasis to manifest as the incubation period is longer (3 to 72 hours). However, it has been recognized that patients are often misdiagnosed with other diseases such as intestinal inflammation, intestinal obstruction, ulcer, acute appendicitis, diverticulitis, mad cow disease, etc. [6].

2.1.3.4 Allergic reaction

In all cases, the body responds to the intrusion of the parasite with an eosinophil-mediated immune reaction. When the parasite lodges in the organism, it secretes biochemical substances foreign to the immune system, triggering the migration of eosinophils towards the parasite, forming a granuloma around it and isolating it from the organism. This immune response is responsible for the inflammatory reaction in the host, manifested by hives, rhinitis, bronchoconstriction, coughing, asthma, conjunctivitis, contact dermatitis, gastrointestinal symptoms (epigastric pain and nausea), intestinal edema, and potentially anaphylactic shock [2].

2.2 Gymnorhynchus gigas

Pomfret, among the most consumed fish by humans worldwide, exhibits a high level of parasitism by Gymnorhynchus gigas. However, since it is not transmissible to humans, and its potential relevance to human health has not been questioned, and it poses no hazard to consumers, it is noteworthy that this parasite, despite its abundance in nature, has not been studied to date [18].

2.2.1 Morphology

Gymnorhynchus gigas is a flatworm visible to the naked eye. When young, it is dark white, almost transparent, and as it ages, it becomes larger, with its color shifting towards yellowish-white and becoming more opaque. G. gigas consists of three distinct parts:

• Anterior or cephalic part: It contains the scolex, usually invaginated, measuring approximately 11 × 1.9–2 mm. It has four botryoids at the apical end and four proboscides enclosed in a sheath that can be reversible from the scolex, containing hooks at the end of the stalk.

• Central part: Formed by an ovoid vesicle, about 12 × 12 cm in diameter.

• Caudal part: Its length and width are highly variable, sometimes measuring up to 1 m long. It performs complex convolutions within the fish’s musculature, making the parasite difficult to remove in its entirety (Figure 3) [18].

Figure 3.

Larva of Gymnorhynchus gigas in Pomfret.

2.2.2 Life cycle

Life cycle involving at least two hosts. Fish can serve as final or intermediate hosts for these tapeworms, which are oviparous, and their eggs are transmitted in the feces of the final host. The eggs hatch in water to release free-swimming larvae, propelled by cilia. In the order Trypanorhyncha, these larvae are called coracidium and must be ingested by a suitable invertebrate intermediate host, typically a crustacean, mollusk, clupeid, or scombrid. The tapeworm larva penetrates through the intestinal wall of the host and undergoes a transformation process in the abdominal cavity to the procercoid stage, capable of infecting the fish host. If the procercoid is ingested by a suitable fish host, it penetrates the intestinal wall and encysts in the viscera or musculature, where it develops into the plerocercoid stage.

Fish in which a plerocercoid stage is formed act as second intermediate hosts, such as teleosts. The life cycle completes when an infected fish is eaten by a definitive host, which is an elasmobranch (rays and sharks), in whose intestine the tapeworm develops to maturity.

The plerocercoids of Gymnorhynchus gigas are often found in the musculature of the Ray’s bream (Brama raii), causing a mass invasion in the fish muscles. The mode of infection appears to be either through the fish’s skin or by ingesting zooplankton or parasitized crustaceans [19].

2.2.3 Health aspect

The parasite Gymnorhynchus gigas is capable of causing significant changes in the musculature. These changes are sometimes visible in freshly caught fish, appearing as grayish spots that become more evident when the parasite is in the superficial layers of the musculature, closer to the skin. The muscle tissue around the parasite may have a yellowish color compared to the pinkish-white color of healthy muscle and histologically shows interstitial myositis. The parasite itself and these lesions are likely to reduce the shelf life and assessment of fish inspection, directly affecting organoleptic characteristics; the muscle is less firm, and analytical parameters (chemical and microbiological) used for freshness evaluation are indirectly disrupted [20].

This parasite contributes to the fish’s unpleasant taste and poses an economic issue by being a reason for rejecting Moroccan fish intended for export.

2.3 Protozoa

Protozoa are commonly encountered in fish, with major groups including ciliates, flagellates, microsporidia, and myxosporidia. They can accumulate in large numbers in fish, leading to weight loss, debilitation, and mortality. Ciliates and flagellates have direct life cycles and particularly affect fish populations raised in ponds. Some of these protozoans can cause more or less pathogenic effects in their fish hosts. This is the case for myxosporidia and microsporidia.

2.3.1 Kudoa spp

The genus Kudoa belongs to the phylum Myxospora, class Myxosporea, order Multivalvulida, and family Kudoidae.

Myxosporean parasites affect many fish families and are common in cichlids, cyprinids, and mugilids [21]. In Africa, more than 135 species of Myxosporea are known to infect freshwater, brackish, and marine fish [22].

Kudoa spp. have a global distribution and infect a wide range of host species. One of the main concerns is that these species are responsible for economic losses in the fishing sector by causing post-mortem myoliquefaction.

K. septempunctata was recently identified as the causative agent of a previously unidentified foodborne illness associated with the consumption of olive flounder (Paralichthys olivaceus) in Japan. Since 2003, outbreaks of unidentified foodborne illnesses associated with the consumption of raw fish have increased, and this Myxosporean is implicated as the etiological agent, demonstrating the pathogenic potential of Kudoa spores. Clinical symptoms include severe diarrhea and vomiting 2–20 hours after ingesting raw, parasitized fish. In a study, anti-Kudoa spp. IgE antibodies were observed in patients experiencing allergic reactions after consuming fish. In experimental models, oral administration of pseudocysts to mice induced specific IgE antibodies. These IgE responses confirm the possible allergenic nature of certain parasite components [23].

Depending on the site of infestation, two forms of Myxosporea have been defined:

Coelozoic forms are free in the lumen of organs such as the gall bladder and urinary bladder.

Hystozoic forms are localized in host tissues where they generally induce cyst formation. Hystozoic species are the most pathogenic. In severe infestations, they can lead to the destruction of parasitized tissues and result in the death of the host. Additionally, Myxosporea infestation can expose fish to secondary contamination by other microorganisms such as viruses or bacteria (Figure 4) [24].

Figure 4.

Xenoparasite formation in Axillary seabream.

2.3.2 Glugea spp

The genus Glugea spp. is a microsporidian belonging to the phylum Microsporidia, class Microsporea, order Glugeida, and family Glugeidae [25]. They are strict intracellular parasites that infect both vertebrates and invertebrates. There are more than 1300 species of microsporidia worldwide. Their classification is primarily based on morpho-anatomical characteristics obtained through light and electron microscopy. All microsporidia exhibit a form of resistance and dissemination, the spore, which is often small (1 to 5 μm long, rarely reaching 20 μm) and usually ovoid or spherical [24].

Fish hosts become infected by ingesting infectious spores from contaminated fish or food. Infected cells generally enlarge (xenomes) to accommodate proliferating parasites, which develop through merogony and sporogony inside the xenomes, leading to spore production. Infected cells hypertrophy and can reach macroscopic sizes, often resulting in characteristic pathological signs, such as multiple whitish nodules in tissues or, in the case of the bladder, significant thickening of the walls. The impact of microsporidia infestation on fish hosts varies. Some fish hosts seem to survive even in the presence of huge xenomes exerting pressure on organs, while in others, microsporidia have a morbid effect. Intranuclear infection of hematopoietic cells is often associated with acute anemia [22].

2.4 Parasitic crustaceans

Crustacean parasites are arthropods characterized by two pairs of antennae and branchial respiration. In higher forms, their chitin is calcified. Their adaptation to parasitism often leads to significant regression of organs and limbs, and they are classified as crustaceans mainly based on their characteristic larval stages [26].

They pose increasingly serious problems in both farmed and wild fish populations. These ectoparasites attach to the gills, body, and fins of fish hosts [22].

2.4.1 Copepods

Copepods are a group of small crustaceans found in almost all freshwater and saltwater habitats. There are planktonic species (living in seawater) and benthic species (living on the ocean floor). Their size varies considerably, but they generally measure 1 to 2 mm in length, with a tear-shaped body and large antennae. Like other crustaceans, they have a tough exoskeleton, but they are so small that in most species, this fine armor and the entire body are almost entirely transparent.

Parasitic copepods are characterized by monoxenous and heteroxenous cycles, going through several larval stages (molts) to reach the adult stage. Nauplius, copepodite, chalimus, and preadult stages are characteristic stages of the copepod development cycle. Parasites with a complex life cycle, using multiple hosts, are generally less specific than those with a direct cycle. Parasites with a direct life cycle often actively search for their host, while the transfer of parasitic stages in species with a complex cycle occurs passively, mainly through predation interactions [27].

Copepods have a pathogenic effect that manifests as tissue destruction during parasite penetration, anemia, extensive damage to the gills, and skin erosion. Generally, the attachment points are marked by a circular red depression, while the peripheral area becomes hemorrhagic and inflamed, sometimes ulcerated with partial loss of the epithelium. Pathogenic copepods include the Pennellidae and Sphyridae families (Figure 5) [24].

Figure 5.

Ergasilus sp. (a genus of copepod crustaceans) females, each carrying a pair of eggs on the gills.

2.4.2 Isopods

Parasitic isopods measure from 1 to 100 mm in length and are easily distinguished from other crustaceans by their body segmentation (seven thoracic segments and six posterior segments). The most significant ones belong to the family Cymothoidae, the adult forms are found in the mouth or gill cavities. Juveniles are swimming forms looking for a host, on which they attach, transform into males, and later into females [26].

These parasites often cause various pathologies in their hosts, such as epithelial erosions, inflammation, and necrosis of the dermis developing at the attachment point of the parasite to the skin, as well as deformations of gill filaments, and sometimes significant mortality. Infested individuals become unsuitable for consumption [24].

3. Search for parasites in fish

We adopted a fieldwork approach, examining 354 pieces of fish belonging to 29 different species. This examination involves looking by eye, firstly for ectoparasites on the skin, oral cavity and fins, and secondly for internal parasites in the abdominal cavity and flesh. At the end of this research, we found 60 pieces of infested fish containing 657 parasites of different species, thus giving an overall prevalence of 16.94%, an overall abundance of 1.86, and an absolute intensity of 10.95. These infestation parameters vary depending on the species of fish and the type of parasite.

The L3 infesting larva of the Anisakis nematode dominates with a prevalence of 11.30%. The plerocercoid larva of the cestode Gymnorhynchus gigas was found with a prevalence of 3.11% and appears to exclusively infest the pomfret (Brama brama), in which the prevalence is 100%. Xenomas, a whitish nodular formation, were found only in species of the sparid family, with a prevalence of 1.42%. Isopod parasitic crustaceans were found in the pomfret and the Axillary seabream (Pagellus acarne) with a prevalence of 1.12%. The pomfret and the Silver scabbardfish (Lepidopus caudatus), show a higher level of risk for parasitism with respective prevalences of 100 and 76.92%.

A positive correlation was demonstrated between the total length, the weight of the fish and the intensity of parasitism.

Fish caught off the Moroccan coast as everywhere in the world are infested by nematodes, trematodes and cestodes with varying prevalence depending on the species of fish and therefore constitutes a subject of concern to the consumer and a challenge for the health authorities and professionals in a co-regulatory framework. These parasites are responsible for emerging zoonotic diseases and can be transmissible to humans despite being generally neglected in discussions on the safety of fish products [28] . These zoonosis were considered specific to low-income populations, but tend to evolve due to the diversification of international markets, the development of means of transport and demographic changes [29] . According to the Health Organization World, more than 18 million people are infected with fish-borne parasites; worldwide, more than half a billion people are at risk of being infected [30]. Prioritization of public health systems in countries must give more resources and attention to these parasitic zoonosis of fish and must overcome the lack of data on their health and economic impact. Fish parasites are transmitted to humans following the consumption of raw or undercooked fish, inducing a form of morbidity rather than mortality [31]. Food inspection and control rules vary from country to country and are often inadequate [32]. Indeed, European Union legislation specifies in Commission Regulation No. 1276/2011 of December 8 [33], 2011 amending Annex III to Regulation (EC) No. 853/2004 of the European Parliament and of the Council [34], the axes measures to combat these parasites, namely their removal when they are visible and the application of a sanitizing treatment for products intended to be consumed raw, making it possible to kill any parasites that may have escaped visual inspection. Regulation (EC) No. 2074/2005 defines the visual inspection of fishery products as non-destructive, and specifies the methods of carrying it out in terms of sampling [35]. The visual inspection is carried out with the naked eye, and can be supplemented by the candling technique when the latter is adapted to the products subject to inspection (thin-thickness parts). However, despite the sanitizing treatment, the presence of dead larvae has been associated with allergenicity in sensitive people, due to the thermostability of certain allergens, notably Anisakis [36].

4. Conclusions

The phenomenon of fish parasitism remains a serious health problem (Fish products that are visibly parasitized can transmit parasitic diseases to humans), also leading to significant economic losses since it is considered as main reason for refoulement and seizure. Controlling the hazard of parasites in fish is based on a shared responsibility between professionals in the fishing industry and the competent health authorities. In this regard, the search for parasites in fish should be systematically conducted before their commercialization in markets. Raising consumer awareness about methods to kill parasites, namely: freezing (−20°C for 24 hours or −35°C for 15 hours), cooking, or hot smoking.

Among the perspectives to be considered in future research for parasites, the molecular analysis of larvae collected from the Moroccan coasts to better understand their distribution, their origins and their infectious power. This would help to better assess the risk for sensitized people. Furthermore, training on parasites in fishery products should be considered and carried out to reach the maximum number of professionals within the fish supply chain, in order to avoid the marketing of fishery products containing parasites and to prevent human infection.

Furthermore, it is crucial to observe the “One Health” concept by training students at universities, research centers and cross-sectoral organizations to regulate and prevent zoonoses by integrating all levels to achieve the desired public health outcomes examining the relationships between people, animals and plants and their shared environment.

Conflict of interest

The authors declare no conflict of interest.