Parasitic Worms of Fishes from the Northern Part of the Sea of Okhotsk, and their Medical and Veterinary Significance

 

  

The topic under consideration is relevant for all regions of the Russian Far East, where population has been consuming fresh fish as one of the main food products for a long time.
Every year, with the start of salmon fishing season, the population and the media of the Magadan region have traditionally been puzzled by the possibility of infection with parasitic worms from fish caught or bought at the market.
Unfortunately, the educative activities among the population on the topic of infection with helminths in our country are still extremely small and incomparable with those, in the countries of Southeast Asia. For example, in Japan, where the topic of helminthosis (diseases caused by parasitic worms) from the fresh seafood is especially relevant, there are wonderful both private and state-owned parasitological museums. For example, the famous Meguro Parasitological Museum is of particular popularity, where skillfully designed stands with collection material are dedicated to each type of parasite.

Stand dedicated to the life cycle and practical significance of the cestode (tapeworm) Diphyllobothrium luxi (= D. nihonkaiense) in a private parasitological museum in Meguro (Japan)

At least 20 species of helminths with medical and (or) veterinary significance can be distinguished from salmon fish on the mainland coast of the Sea of ​​Okhotsk: cestodes (tapeworms) - Diplocotyle olrikii, Nybelinia surmenicola, Eubothrium crassum, E. salvelini, Diphyllobothrium dendriticum, D. ditremrem, D. luxi; trematodes (diagenetic flukes) - Diplostomum gasterostei, D. gavium, Ichthyocotylurus erraticus, I. pileatus, Phyllodistomum simile, Ph. umblae; nematodes (roundworms) - Hysterothylacium gadi aduncum, Anisakis simplex, Pseudoterranova decipiens, Philonema oncorhynchi, Salvelinema salmonicola and acanthocephals (acanthocephalans or spiny-headed worms) - Acanthocephalus tenuirostris, Cumnosoma.
Four species are most practically significant for the inhabitants of the coastal regions of the North Okhotsk Sea: cestodes - tapeworm D. luxi and N. surmenicola, as well as nematodes A. simplex and P. decipiens. Knowing some of the biological features of these helminths and the simple rules for cooking fresh fish allows a Far East resident to fully enjoy the taste of freshly caught Pacific salmon and anadromous char. This is the main utilitarian goal of the further narration.
Lux’es tapewormn - Diphyllobothrium luxi. The invasive larvae (plerocercoids) of the Lux’es tapeworm are white, relatively large (more than 1 cm long, both free-lying and encapsulated), are visually clearly distinguishable in the red musculature of salmon fish.

The plerocercoid Diphyllobothrium luxi in the muscles of humpback salmon (From: Vyalov, 2003)

 

In our opinion, this helminth represents the greatest threat to human and domestic animals' health, causing a helminthiasis called diphyllobothriasis. One should note, that the adult mature cestode D. luxi reaches one meter or more in the intestines of an infected mammal (brown bear, human).
Reliable information about the risk of infection of the population with tapeworms is currently known only within the Khabarovsk Territory and the Sakhalin Region, which most likely does not reflect the true modern picture of the distribution of diphyllobothriasis (D. luxi causative organism) in the Northern part of the Sea of Okhotsk.
Plerocercoids D. luxi are localized, as a rule, in the dorsal and caudal parts of the musculature of salmon fish, and one must be especially careful to detect these parasites in the prepared fish.

Localization (indicated by dots) of plerocercoids Diphyllobothrium luxi in the humpback musculature (from: Vyalov, 2003)

The natural life cycle and sources of invasion of D. luxi have not yet been completely studied. It is believed that terrestrial mammals, and to a lesser extent humans living on the coast of the Far Eastern seas and in salmon river basins, can be the sources of primary invasion. For example, in salmon spawning grounds, the main role in the distribution of this parasite may belong to its main definitive host - the brown bear, a large species that feeds on anadromous salmon during their spawning migration and largely infected with the tapeworms D. luxi.
Nematodes Anisakis simplex and Pseudoterranova decipiens. The larvae of both types of nematodes, causing a helminthiasis disease called anisacidosis, differ well even with the naked eye.
In anisakis larvae, the body is light yellow, 14–30 mm long and up to 0.5 mm in diameter, usually coiled in a thin-walled capsule into a tight spiral. The larvae of pseudoterrans, on the contrary, are dark red, much larger (25–45 mm long and up to 1.2 mm in diameter), folded in the capsule with an irregular ring or straightened, lying freely outside the capsules.

Larvae of the third stage from salmon muscles: Anisakissimplex on the left, Pseudoterranovadecipiens on the right (From: Vyalov, 2003)

Almost every resident of the Far East is well aware of the appearance of anisakis larvae from fresh, smoked, salted and pickled herring, in which the surface of internal organs is often covered with a layer of these parasites.

Larvae of the nematode Anisakis simplex on the internal organs of herring (from the title page of the advertising leaflet of a private parasitological museum in Meguro, Japan)

Initially, the beginning of a wide study of anisakisis was connected with herring: in the last century a serious human disease was revealed in Holland for the first time, which in some cases ended in death. This disease was called the "eosinophilic phlegmon" of the intestine. Its causative organism was the larvae of Anisakis sp. from the Atlantic herring. Since that time, the problem of anisacidosis has been attracting close attention of specialists and has become one of the world problems of medical parasitology.
The life cycle of A. simplex, which is similar to the life cycle of representatives of other species of the anisacid family, including Pseudoterranova decipiens, is the most completely studied by the present time. Mature nematodes in the gastrointestinal tract of whales and seals produce a huge number of eggs. In sea water, the larvae of the first and second stages are successively formed inside the egg. Such eggs or larvae emerging from them are swallowed by the first intermediate hosts - various crustaceans, in the body cavity of which the development of the second stage is finally completed and the formation of larvae of the third stage begins. Their further development is necessarily associated with fish and cephalopods (including squids) - the second intermediate hosts. Being localized in the body cavity, internal organs and muscles, the third stage larvae become invasive (capable of infecting) for definitive (final) hosts. In the stomach and intestines of the latter, they molt twice, grow and turn into adult worms.
It should be noted that, regardless of the species, the role of the main causative organism of anisacidosis all over the world is played by the third-stage larvae from fish that reliably belong to two genera: Anisakis and Pseudoterranova. Unconditional "leadership" in this regard within the Pacific basin, including the Sea of ​​Okhotsk, belongs to the species A. simplex, a mass parasite of almost all species of anadromous salmon and char. This group of salmon fish is of paramount importance in the epidemiology of anisacidosis in the northern part of the Sea of Okhotsk, as it is a favorite food item in fresh and salted form among the population. However, in the Far East of Russia, there is the only documented case of human anisidosis (A. simplex) described in the scientific literature until now. Obviously, this does not reflect the true picture of the spread of human anisakidosis in the region, and usually cases of infection with anisakisis are not advertised or are diagnosed simply as intestinal food poisoning.
From year to year, there is a high infection rate of anadromous salmon with anisakis larvae in the northern part of the coast of the Sea of ​​Okhotsk, where mass species of salmon – chum salmon, humpback, coho and sockeye salmon, which have the highest epidemiological significance for anisacidosis in the region, are particularly distinguished. At the same time, the question of the intravital distribution of anisakis larvae in salmon fish is of particular importance. Thus, there is a certain pattern can be observed. It was clearly established that in humpback, studied immediately after catching, the abdominal muscles turned out to be the most infected with larvae of A. simplex; lower rates are noted for the spinal muscles. This indicates unidirectional migrations of anisakis larvae in the fish body (here, salmonids) towards the organs and tissues most saturated with fats, which is also confirmed by our practice.
To detect anisakis larvae in freshly caught salmon or char, first of all, it is necessary to examine the abdominal muscles of the fish, dissecting them into thin slices for visual detection of parasites. In the absence of anisakisis in the abdomen of the fish, the probability of their detection in the deep muscle layers is reduced to zero. And this is important for choosing the subsequent procedure for using (cooking) fresh fish - weak or strong salting, frying, smoking or completely freezing.
No wonder that every salmon fishing season in all regions of the Russian Far East starts with the issue of prevention of diphyllobothriasis and anisacidosis raditionally raised in print and electronic media. The scientific and popular literature describes various methods of disinfestation fish from dangerous helminths – causal organisms of diphyllobothriasis, anisacidosis and many other helminthiases. However, the simplest, well-known preventive action for epidemiologically significant parasitic worms (both in industrial production and in everyday life) is prolonged preliminary freezing of fish at low temperature until it is completely disinfested from live helminths, which can be successfully implemented by the modern refrigeration appliances.
The following series of action is usually recommended: freezing the whole fish (or its pieces) at a temperature of - 20°С (temperature in the body of the fish) for 24 hours, followed by storage at - 18°С for 7 days, or boil or fry for 20 minutes, or salting in strong pickle for 14 days. And here we strongly recommend the book by A. V. Gaevskaya (2005), where the professional morphological, systematic and environmental analysis of the representatives of the Anisakida family (Anisakidae), including A. simplex and P. decipiens, and all the information about them existing in literature and practice is given in a readily understandable format.
Finally, it is necessary to mention once again helminths that spoil the market condition of fish products both in fresh and in canned form. First of all, this concerns the larvae (plerocercoids) of the cestode Nybelinia surmenicola.
The main final host of Nibelinia in the Pacific basin is the pollock Theragra chalcogramma. That is why for many years this currently valuable commercial species of marine fish has been unjustifiably used mainly for the production of mineral fertilizer and feed for fur animals. As a rule, Nibelinia are localized in the cavity of the fish’s body and, in large quantities (hundreds of specimens), accumulate in its caudal part above the anus, where they form a whole lump covered with connective tissue membranes.

Localization of Nybelinia surmenicola larvae in the body of freshly caught pollock. The places of the largest accumulation of nibelinia are shaded. The dotted line shows the recommended cut line for fish processing for food purposes (according to: Oshmarin et al., 1961)

It is believed that Nibelia is completely harmless for a human, in adult state they parasitize only in sharks and stingrays. Their larvae are relatively rare or in small quantities in anadromous salmon fish. However, by appearance and size they are resemble larvae of meat flies (Fig. 7) and are very mobile in a living state, which causes an aversion of a handler to the infested fish (for example, an amateur fisherman or a cook).

Larvae (plerocercoids) of Nybeliniasurmenicola. Photo by G. Atrashkevich

If the caught infested fish is not immediately processed or frozen as a whole, the Nibelian larvae, which for a long time maintain viability, are able to migrate from the cavity of the fish’s body into its muscles. Nibelines remain alive for up to 22 hours in gutted fish stored in a domestic refrigerator to at - 7 ° C. However (and this is important), the larvae of nibelia become inactive and do not change their localization in the cavity of the body of the fish under such conditions neither during its further storage in the refrigerator, nor during defrostation.
In conclusion, we would like to advise fish processors, primarily amateur fishermen and cooks, not to give in to the first feeling of disgust at the sight of a fish infested with helminths, which often leads to its culling and discarding, and try to calmly deal with the species composition and localization of the observed helminths.

 

Adult cestodes of Eubothriumcrassum, causing blockage of chum intestines. Photo by V. Pospekhov

Then the appropriate measures should be taken depending on the degree of infestation of the fish, by single helminths or a multitude of them, posing risks to humans and animals or only spoiling the market condition of the fish. In the latter case, it is enough just to remove the helminths (out of sight) and you can immediately use fresh fish as intended. Otherwise, for guaranteed disinfestation of fish, it is necessary to use the well-known methods of freezing, salting or high temperature exposure, mentioned above.


 
Authors: Atrashkevich G.I., Cand. of Biol. Scien. (Ph.D.), head of the Laboratory of Helminths’ Ecology; Pospekhov V.V., researcher