Marine Mammals: A Barometer to Human Disease?
IAAAM 1987
Thomas L. Deardorff
Fishery Research Branch, U.S. Food and Drug Administration, Dauphin Island, AL

The Fishery Research Branch laboratory is located 4 miles offshore of Alabama in the Gulf of Mexico. The FDA originally operated our facility in the area of shellfish sanitation; but, in 1983, both the name and the direction of the lab were changed. We are now a research facility with our interests focused on fishery products. Our current research may be divided into 2 categories: Aquatic Chemical Hazards and Aquatic Biological Hazards. One of the newly emerging areas of public health concern being studying in the Aquatic Biological Hazards section is: Parasites and their potential to be transmitted to humans by seafood.

Researchers, to date, have implicated well-over fifty species of parasites as producing zoonotic infections resulting from eating raw seafoods. Most of these infections, fortunately, do not occur in the United States. This can be attributed to a lack of specific intermediate hosts required to complete the parasite's life cycle, improved sanitation, refined foodhandling procedures, and our traditional "meat and potatoes" diet.

Some parasitic diseases, however, do occur in the United States and the number of new case reports, as well as previously unrecognized parasitic diseases, continues to increase. One reason for this increase my be attributed to the changing dietary habits of our cosmopolitan society--a change that may permit new types of parasitic infection to be acquired. For example, some common raw fish dishes known to transmit parasitic diseases that may be served at some specialty restaurants are: poison cru, raw fish with coconut milk; lomi load, raw salmon with green pepper and tomatoes; and ceviche, raw fish in lime juice. In addition to these, one of the fastest growing types of restaurants in recent years is the Japanese sushi bar. In these restaurants, customers often dine on sushi (raw seafood usually associated with rice) and sashimi (sliced raw fish) . However, no matter how esthetically pleasing, how appetizing, or how harmless these dishes my look, as we all know, things aren't always as they appear. Sushi and sashimi are known to have caused hundreds of cases of parasitic infections in humans.

Humans my become infected with parasitic nematodes by consuming raw or inadequately prepared seafoods. When a larval stage is ingested, it may penetrate into or through the gastrointestinal tract of a host. For example, the zoonotic disease, anisakiasis, is one disease associated with the consumption of raw seafoods. The third-stage larvae of Anisakis simplex is capable of burrowing into the mucosa of a patients stomach.

The clinical features of this disease generally involve the sudden and severe onset of epigastric pain, often associated with nausea and vomiting, occurring from 1 to 12 hours after eating raw seafood. As the disease moves from the acute to the chronic stage, the epigastric distress becomes vague, occult blood may be seen in the gastric juice or stool, and hematological findings usually reveal a high eosinophil range (4 to 41%; normal is from 2 to 5%). The use of a biopsy forcep to grasp and remove the worm is extremely effective management of gastric anisakiasis.

While endoscopy is considered the most reliable diagnostic method and treatment for worm in the stomach, it is of little help if the larva enters the intestine. Presently, the only diagnostic method available for worms in the intestines, with the exception of exploratory surgery, is radiology. As a diagnostic tool, however, this techniques has a poor batting average; it is less than 50% reliable in gastric and 20% reliable in intestinal cases. Abdominal surgery remains is the only method of removing the worms from the intestine.

The greatest number of human cases occur in areas where seafood constitutes a major portion of the protein intake of a population. Most cases of human anisakiasis have been reported from Japan and The Netherlands, but since 1958, 50 cases of human anisakiasis have been reported in the U.S. Clearly, the low number of cases in the U.S. is no cause for immediate alarm; however, as I mentioned earlier, we have noted that the number of cases has been increasing. For instance, of the U.S. cases, over 70% occurred in the last 6 years; over 30% occurred in the last 2 years. Anisakiasis is not a reportable disease and it may well be that we are looking at the tip of the iceberg. We are currently taking steps to try and better document the occurrence of this disease as well as to increase our understanding of it.

Not only is the Food and Drug Administration concerned with the worm in the food that you bring to your table, but we are also concerned with worms as they impact the marine environment. We are, therefore, studying parasite life cycles. Not all antiskid nematodes have the same life cycle and, often, the final hosts differ. Clearly, a better understanding of the biology of certain parasites is to our advantage.

The life cycle of species in the genus Anisakis start and end in marine mammals. Basically, eggs are expelled by a mature female nematode into the gastrointestinal tract of the mammalian host (e.g., whales, seals, dolphins) and passed out with the feces into the water. Development to the first-stage larva occurs within the egg with the second-stage larva is released a few days later. This free-swimming larva may be eaten by a crustacean. These crustaceans (i.e., copepods or shrimp) usually act as a transport host because no larval development occurs in this animal. The crustacean merely acts as a means of transporting the worm to its next host. When the crustacean is ingested by an acceptable intermediate host (invertebrates and fishes in which the parasite develops but not to maturity) and migrates to the hemocal or mesentaries where it develops into a third stage larva. The third-stage larva is the infective stage for marine mammals and humans. It will molt to fourth-stage larva and then to its adult form when eaten by an acceptable definitive host. Humans may become infected by interrupting the cycle by eating the intermediate host. Humans, however, have not been shown to serve as a definitive host for these parasites.

Because these worms mature in marine mammals, it is generally assumed that fish are more infected in area where mammals are plentiful. Thus, marine mammals may be a barometer to predict invasive worms in fish. surveys for helmiths of marine fishes and invertebrates, supported the U.S. Food and Drug administration, have been completed for the Atlantic Coast (Cheng, 1976; Jackson et al. 1978), the Gulf Coast (Norris and Overstreet, 1976; Deardorff and Overstreet, 1981), the Pacific Coast (Meyers, 1979),and the waters near the Hawaiian Islands (Deardorff et al., 1982). These studies showed that fishes caught off the Pacific Coast have a greater worm burden than fishes caught in the other survey areas have more marine mammals compared with the Atlantic, Gulf, or Hawaiian regions. Therefore, there appears to be some correlation between the numbers of invasive worms and the presence of marine mammals.

The FDA's research interests with these worms are not only limited to their invasive potential. Deardorff et al. (1983) observed significant gastric erosion associated with the larval nematodes as they penetrated into the stomach of the inoculated animals. If mechanical methods of penetration where used by worms (i.e., via the boring tooth), we would have expected a more clean cut, rather than a rough, furrow. We speculated that the worms must be releasing excretory-secretory (ES) products to aid in the penetration process.

To investigate the possibility of ES products, Rayborn et al. (1983) isolated worms from fish tissue and maintained in culture media. The ES products were collected from supernatants of these in vitro cultures and were found to be potent inhibitors of rodent lymphocyte blast transformation (Rayborne et al., 1983). The inhibition of the cell blast transformation was correlated to the amount of protein in the ES products. This bioactive substance was later shown by Rayborne et al. (1986) to exert a similar effect on lymphoid and epitheloid cell lines; cell lines that where not mitogen-stimulated.

It has generally been assumed that removing the worms from the edible musculature of a fish would eliminate the health risks. The finding of bioactive substances eliminated by these parasites suggests that this may not be the case. The worm's products, released while encysted, may remain in the tissues. Also, the ES materials may be carried by the circulatory system of the infected fish. If so, the presence of worms in nonedible area of fish (e.g., viscera) may allow for contamination of the whole fish. We are currently examining this possibility.

The fishery industry in the Gulf of Mexico is one of the most productive in the world. This important fishery, plus our location on Dauphin Island, makes the Fishery Research Branch an ideal facility to examine these as well as other potential areas of health concern associated with seafoods.

For example, the scientists at the Fishery Research Branch are studying the third-stage larvae of a species belonging to the genus Hysterothylacium. These worms are commonly found in shrimp, flounder, and numerous other marine organisms (Norris and Overstreet, 1976; Deardorff and Overstreet, 1981). This worm has been demonstrated to possess the ability to penetrate into and through the stomach wall of laboratory animals in less than 15 minutes. The life cycle of species in this genus is similar to that of Anisakis but with a different final host. Species belonging to this genus mature in fish --- not marine manuals. Consequently, using the presence or absence of marine mammals as a barometer to indicate the presence or absence of invasive nematodes in fish is not always accurate. Such findings emphasis the importance of understanding parasite life cycles.

We also are studying another type of larval nematode principally found in commercially important species from the Gulf of Mexico which does not appear to be invasive but the presence of this larval helminth represents adulteration of the seafood product. The third-stage larvae of Contracaecum multipapillatum is commonly found in the liver, kidney and less often the muscle of the striped mullet. When mullet are eviscerated, the worms in the kidney often remain with the edible portion. If the fish is to be cooked, the worms represent no health risk because they will die when exposed to extreme heat. The worms merely become additional protein. However, if the mullet is destined to be smoked, and an insufficient amount of heat is used, the worm will survive. Shorebirds serve as the final host for Contracaecum multipapillatum. Again, a crustacean probably serves as the transport host and mullet serve as the intermediate host. In areas where pelicans, cormorants, and herons are commonly found, mullet generally harbor larger worm burdens.

The Food and Drug Administration supports the Disease Prevention Programs of the Public Health Service; certainly with respect to eating less beef and more fish. Therefore, we are interested in preventive measures to neutralize the invasive potential of parasites in fish. Temperature extremes appear to be most effective. The heat from thoroughly cooking seafoods kills the parasites. However, heating the seafood products is not always desirable (i.e., sushi products). Freezing is currently regarded as the most promising preventive measure against infection with anisakid larvae. Our preliminary findings suggest that -20°C for at least five days would be effective in killing all the worms in most whole fish (see Deardorff et al., 1984). -20°C is a temperature that is attainable with standard domestic freezers. We have recently completed an experiment that demonstrated that commercial blast-freezing (-40°C for 15 hr) is effective in killing larvae in salmon and rockfish. Thus, blast-freezing fish or other seafood products intended to be eaten raw would neutralized the invasive potential of these nematodes and better insure the safety of the consumer against the disease.

While thorough cooking or adequate freezing of seafoods are good preventive measures against anisakiasis and other parasitic diseases, these practices will not always be followed and are difficult to enforce. Prevention of this disease is probably best accomplished by educating the public to the health risks of eating raw seafoods. The consumer should know the risks and evaluate the potential consequences. He is more than likely aware that raw beef (i.e., steak tartar) may be the vector for the beef tapeworm or be the cause of toxoplasmosis and that raw pork may transmit the pork tapeworm or be the cause of trichinosis. When he chooses to eat these foods, he has considered the risks.

As with beef and pork, the vast majority of seafood products are safe to eat; however, the importance of consumer awareness concerning the possible hazards of eating raw seafoods cannot be over emphasized.

References

1.  Cheng, T.C. 1976. The natural history of anisakiasis in animals. Journal of Milk and Food Technology 39:32-46.

2.  Deardorff, T.L. and R.M. Overstreet. 1981. Larval Hysterothylacium (Thynnascaris) (Nematoda: Anisakidae) from the northern Gulf of Mexico. Proceedings of the Helminthological Society of Washington 48:113-126.

3.  Deardorff, T.L., M.M. Kliks, M.E. Rosenfeld, R.A. Rychlinski, and R.S. Desowitz. 1982. Larval ascaridoid nematodes from fishes near the Hawaiian Islands, with comments on pathogenicity experiments. Pacific Science 36:187-201.

4.  Deardorff, T.L., R.B. Raybourne, and R.S. Desowitz. 1984. Behavior and viability of third-stage larvae of Terranova sp. (type HA) and Anisakis simplex (type I) under coolant conditions. Journal of Food Protection 47:49-52.

5.  Jackson, G.J., J.W. Bier, W.L. Payne, T.A. Gerding, and W.G. Knollenberg. 1978. Nematodes in fresh market fish of Washington, D.C. area. Journal of Food Protection 41:613-620.

6.  Myers, B.J. 1979. Anisakine nematodes in fresh commercial fish from waters along the Washington, Oregon and California coasts. Journal of Food Protection 42:380-384.

7.  Norris, D.E., and R.M. Overstreet. 1976. The public health implications of larval Thynnascaris nematodes from shellfish. Journal of Milk and Food Technology 39:47-54.

8.  Raybourne, R.B., R.S. Desowitz, M.M. Kliks, and T.L. Deardorff. 1983. Anisakis simplex and Terranova sp.: Inhibition by larval excretory-secretory products of mitogen-induced rodent lymphoblast proliferation. Experimental Parasitology 55:289-298.

9.  Raybourne, R.B., T.L. Deardorff, and J.W. Bier. 1986. Anisakis simplex: Larval excretory-secretory protein production and cytostatic action in mammalian cell cultures. Experimental Parasitology 62:92-97.

Speaker Information
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Thomas L. Deardorff, PhD


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