U. S. Food and Drug Administration
Center for Food Safety and Applied Nutrition
March 29, 2001

Scope

This section reviews methods of control of parasites that may be of concern in cold-smoked fish. Evidence suggests some fish parasites that are currently not considered human pathogens may become a human health concern in the future, but a description and the control of such parasites are beyond the scope of this report. Consequently, this report will discuss only those parasites that have been known to cause disease in humans.

A variety of parasites have been identified in raw fish. Most of the scientific literature describes methods to control the most significant parasites of concern in the western world, such as anisakid parasites. Although trematode diseases are endemic to countries other than the United States, interest in their control is increasing, given the number of diseases caused by these parasites. A number of parasites also are emerging as possible hazards in the future. For example, evidence shows that anisakids Contracaecum multipapillatum and Hysterothylacium type MB can infect primates and mammals, respectively. In addition, it is well known that recent climatological changes and expanded human activities will accelerate the global transport and dissemination of species and will accelerate host-shifts in a manner difficult to predict (Harvell and others 1999). The growing number of marine mammals, particularly seals and sea lions in the northern Pacific and Atlantic oceans, is increasing the occurrence of parasites in fish. This is expected to continue. Other phenomena that may result in an increase in marine infections are the global distribution and increasing popularity of undercooked seafood products (Overstreet 1999). The following descriptions of the life cycles of the parasites of concern have been summarized from Bier (1992), Hayunga (1997), Goldsmid and Speare (1997), Reilly and Kaferstein (1997), and Adams and Rausch (1997).

Anisakiasis is a disease that includes infections by all ascaroid nematodes having larval stages in aquatic hosts. The main nematodes known to have caused disease in humans are Anisakis simplex and Pseudoterranova decipiens. These nematodes reach sexual maturity in the intestinal tract of marine mammals. Eggs are expelled into the intestinal tract and then are expelled in the feces. In the water the eggs embryonate and undergo at least one moult. The larvae that hatch may infect a small crustacean that may in turn be ingested by a fish (that is, rockfish, herring, mackerel, and salmon). When an infected fish is consumed by another fish, the larvae may penetrate the viscera and infect the new fish host. Marine mammals (such as dolphins, seals, and so on) or humans may become infected from eating the infected intermediate host. In humans, these nematodes do not normally mature, but the worms can migrate from the gastrointestinal tract, becoming embedded in the gastrointestinal mucosa and causing tissue reaction and discomfort (that is, gastric pain, diarrhea, vomiting).

Cestodes are tapeworms and the species of major concern associated with consumption of fish are in the genus Diphyllobothrium. This tapeworm reaches sexual maturity in the intestinal tract of mammals. Eggs are excreted with the feces and develop in water into larvae that hatch into coracidium and may be eaten by a crustacean. In the crustacean body cavity it develops into the next stage, the procercoid. The larvae may then become infective to fish that ingest the crustacean. These larvae then develop into the plerocercoid. Plerocercoids may infect other fish and cease development or infect mammals when they reach sexual maturity. Humans are one of the definitive hosts. Salmon is the most common fish that transmits diphyllobothriasis, although it may also be transmitted by whitefish, trout, and pike. Because the disease is not contagious (and, in the United States, the Center for Disease Control does not require reporting the disease) often it is not reported to health authorities. Some of the symptoms include nausea, abdominal pain, diarrhea, and weakness.

Trematode (or flukes) species of concern have very similar life cycles. Depending on the species, trematodes transmitted by the ingestion of seafood may reach sexual maturity in the liver (for example, Clonorchis, Opisthorchis), intestine (for example, Nanophyetus, Heterophyes), or lungs (for example, Paragonimus) of humans and other mammals. Eggs pass out to the environment in feces and infect mollusks after being ingested. The larvae penetrate the tissue through morphologically distinct stages that asexually produce free swimming larvae. In general, they have a snail intermediate host and use various aquatic animals to harbor metacercaria, the infective stage. The clinical effects of intestinal flukes are generally not serious, although Clonorchis sinensis and Opisthorchis viverrini can cause serious liver damage to humans, and have been associated with carcinoma of the liver.

Human pathogenic parasites occur in several species of fish that may be cold-smoked, including gadoids, salmonids, sole or flounder, grouper, halibut (Hippoglossus spp and Paralichthys sp.), herring, mackerel, mullet, sablefish, sprat, small tunas, and turbot. Parasites are also identified as a potential hazard in some invertebrates that may be cold-smoked or cold-smoked and dried, including octopus, squid, snails, and crabs/crayfish. Several species of salmonid parasites, such as Anisakis spp. (a nematode or roundworm), Diphyllobothrium spp. (a cestode or tapeworm) and Nanophyetus salmincola are of public health concern (Turner and others 1981; Eastburn and others 1987).

All wild-caught Pacific salmon (Oncorhynchus spp.) are considered to have A. simplex larvae present. Prevalence reached more than 75% in fresh U.S. commercial sockeye salmon (O. nerka), chum salmon (O. keta), coho salmon (O. kisutch), and king salmon (O. tschawyscha) (Myers 1979; Deardoff and Overstreet 1991). High incidence was also reported from U.S. supermarkets (Rosset and others 1982). There seems to be a high prevalence of larvae in Atlantic salmon, particularly in the muscle (39%) and intestinal cavity (64%) (Beverley-Burton and Pippy 1978; Bristow and Berland 1991). Anisakis simplex larvae were detected at a high incidence (78-97%) in herring (Clupea harengus) during 1981-86 in the Mancha Channel (Declerck 1988) and in smoked herring from a French supermarket (Lagoin 1980). Pacini and others (1993) tested commercial samples of fresh, frozen and smoked fish on the Italian market for presence of anisakid larvae. They observed that 54% of fresh, 28% of frozen, and 75% of smoked fish samples contained nematodes belonging to Anisakidae; all larvae detected in frozen fish products were dead.

In contrast to wild-caught salmon, farmed salmon, particularly Atlantic salmon (Salmo salar), are not considered to be hosts of Anisakis spp. when fed normal pelleted feed. When 2,832 Norwegian-farmed Atlantic salmon and 876 Scottish-farmed Atlantic smoked salmon fillets were analyzed for anisakid larvae infestation, none were detected (Angot and Brasseur 1993). This result is in agreement with results from previous studies that indicated that farmed salmon (Atlantic, coho, and chinook species) are virtually free from anisakid larvae (Bristow and Berland 1991; Deardoff and Kent 1989). Nevertheless, it should be emphasized that aquacultured fish can become hosts of anisakids if fed moist feeds (that is, raw fish).

Other nematodes, including Gnathostoma spp., Eustrongylides spp., and Pseudoterranova spp., may cause disease in humans. Diphyllobothrium spp. has been reported in salmonids and has caused human illness. These cestodes should be considered a possible hazard in all environments and cannot be ruled out from aquaculture systems. The majority of trematode infections occurs endemically in some countries of Eastern Asia, South America, Eastern Europe, and West Africa and derive mostly from wild-caught fish; however, with an increasing global fish trade, trematodes or flukes, including Heterophyes spp., Metagonimus spp., Opisthorchis spp., Clonorchis sinensis, Echinostoma spp, and N. salmincola, could become a public health concern.

While normally not fatal, parasitic worms can cause intestinal discomfort and other more serious symptoms (Turner and others 1981). Although few cases of anisakiasis have been documented in the United States, many cases have been reported in Japan (Oshima 1972), principally resulting from the consumption of cold-smoked or raw salmon. A recent study on the occurrence of anisakiasis in 27 countries revealed 33,747 cases of anisakiasis, estimated from Japanese and other databases from 1968 to 1998. In Japan, eight of those cases were from Pseudoterranova decipiens (Ishikura and others 1998).

At least two known outbreaks of diphyllobothriasis associated with salmon consumption have been documented in the United States (Turner and others 1981). Interestingly, the disease is thought to be more prevalent than anisakiasis, but it is not usually reported. It has been estimated that there are 13 million carriers globally (Crompton and Joyner 1980), with greater prevalence in Eastern Europe.

Fish trematode infections, particularly chlonorchiasis, opistorchiasis, and paragonimiasis, may also be derived from the consumption of raw or underprocessed fish. Trematode infections are a public health issue mainly in Eastern and Southern Asia. Although the source was not identified, it has been estimated that 50 million people are affected throughout the world (Lima dos Santos 1997). For example, between 1974 and 1985, 8 out of 10 patients in Oregon reported either gastrointestinal complaints or unexplained peripheral blood eosinophilia and had eggs typical for N. salmincola recovered from their stools. They also recalled eating fish prior to the onset of symptoms and had a history of ingestion of raw, incompletely cooked, or smoked salmon (Onchorhynhcus sp.), steelhead trout (Salmon gairdneri), or steelhead eggs. The authors point out that this problem exists West of the Cascade mountain range from Northern California to the Olympic Peninsula in Washington State, United States (Eastburn and others 1987).

Although A. simplex seems to be sensitive to salt, the high salt concentrations and times needed for its elimination make salting an inadequate method of inactivation. For example, Karl and others (1995) reported that in herring processed with the traditional German and Danish procedures, larvae were killed only after being marinated for 5-6 wk in 8-9% salt. When salt concentration was lowered to 4.3%, the time to kill all the larvae increased to 7 wk. Similarly, Fan (1998) reported that metacercariae of Clonorchis sinensis from fresh water fish (Pseudorasbora parva) were killed if kept in heavy salt. These results clearly demonstrate that the more typical water phase salt contents of 3 - 3.5% in cold-smoked fish would not be sufficient to kill the organisms. In addition, dry salting does tend to kill those parasites residing on fish surfaces, but generally does not do so for those imbedded within the tissue.

Several studies have reported temperatures and times needed to kill parasites. For example, Bier (1976) indicated that 60 ^oC (140 ^oF) for 1 min was needed to kill the anisakid larvae. These temperatures are not achieved during cold-smoking of fish and therefore parasites are not eliminated by the cold-smoking process. Gardiner (1990) reported that neither cold-smoking for 12 h at 25.6 ^oC (78 ^oF) nor refrigeration for 27 d reduced the amount of larvae in salmon. This analysis indicated that fresh salmon and cold-smoked salmon had 1 - 3 and 1 - 5 Anisakis spp. viable larvae / 200 g of fish, respectively. A similar result was found in whole Pacific herring (Clupea harengus pallasi), where Hauck (1977) reported that Anisakis larval viability after brining and smoking at an average temperature of 19 ^oC (66 ^oF) for 24 h was 100% and 87.5%, respectively.

Unlike bacteria, molds, and viruses, most parasites are relatively easy to destroy by holding the raw material or finished product at freezing temperatures for a specified period of time; of course, this is dependent upon the internal temperature of the material. The Fish and Fishery Products Hazards and Controls Guide recommends a temperature below -4 ^oF (-20 ^oC) for 7 d or -31 ^oF (-35 ^oC) (internal) for 15 h to kill the parasites of concern (FDA 1998). Although, based on the data currently available, these recommendations may appear stringent, it is because they were developed for the parasites that are considered most resistant to freezing (G. Hoskin 2001; personal communication; unreferenced). Already in 1975 (Food Chemical News, October 1975) Dr. G. J. Jackson cautioned that the anisakid nematodes vary in their ability to survive at low temperatures. For instance, certain species of anisakids have been reported to survive up to 52 h at -4 ^oF. A number of other time and temperature regimes have been prescribed to accomplish the inactivation of parasites. Another such option prescribes holding the fish at -10 ^oF (-23 ^oC) for 60 h (Ching 1984). Alternatively, E.U. regulations require freezing at a temperature of no more than -4 ^oF (-20 ^oC) in all parts of the product for not less than 24 h in order to control parasites in fish.

Some published studies support the effectiveness in controlling parasites by freezing at -4 ^oF (-20 ^oC) in all parts of the product for not less than 24 h. Very early studies by Gustafson (1953) demonstrated that temperatures of less than -17 0C (1.4 ^oF) for 24 h could kill Anisakis larvae. Higher temperatures or shorter times were not as effective. Studies in herring (Houwing 1969) demonstrated that at -4 ^oF, nematodes were killed in 24 h, but if the product temperature reached -30 0C (-22 ^oF) by a cryogenic method, the inactivation was immediate, and no further storage was necessary. A more recent study by Deardoff and Throm (1988) used blast freezing to freeze salmon and rockfish at -31 ^oF (-35 0C). Fish were stored frozen for 15 h and then at -18 0C (0 ^oF) for up to 48 h. Out of 3,545, they found no viable larvae after 1 h of storage at -18 0C. Similar results were found in herring by Karl and Leinemann (1989). They investigated the effect of freezing and cold storage on survival of Anisakix simplex in herring and herring fillets at -20 0C (-4 0F) for 24 h and found no surviving parasites. Although Hauck (1977) reported no viable Anisakis after freezing, the conditions were not detailed. The use of freezing has also been investigated for the control of other parasites of human health concern. Although the World Health Organization (1979) indicated that freezing fish at -10 0C (14 0F) for 5 d would kill all trematodes of concern, later research data indicate that longer times may be needed. For instance, Fan (1998) reported that metacercariae of Clonorchis sinensis from fresh water fish (Pseudorasbora parva) remained viable after frozen storage at -12 0C (10 0F) for 10-18 d and -20 0C for 3-7 d. As mentioned previously, clonorchiasis is not common in Western countries. The metacercariae of Heterophyes are also very resistant to freezing; since they survived 30 h of storage at -10 or -20 0F (Hamed and Elias 1970).

While the parasites can be killed by freezing the finished product, it is generally considered more appropriate to freeze the raw material prior to processing. Nematodes in particular will attempt to depart the gut during processing and will then establish themselves in the muscle during salting or smoking (Hauck 1977). The result may be the presence of nematodes on the surface of the finished product, often perpendicular to the surface. Their presence becomes a quality issue resulting in an aesthetically unwholesome (although safe) product. For this reason, it is a good practice to freeze susceptible raw material, even for hot-smoked fish.

Visual inspection of the product before brining or smoking is also advised. This measure, however, is effective only to ensure that visible parasites are not present rather than to ensure inactivation of viable organisms. Similarly, inspection of fish after slicing will also assist in producing a quality product but cannot be relied upon for assurance against the presence of live parasites in product from commercial operations.

Some recent research has shown that the current regulation and production practice for fishery products does not protect the consumers against allergic hazards due to the ingestion of killed parasites. Audicana and others (1997) have reported that freezing of fish may not protect against allergenic reactions to ingested Anisakis simplex antigens in humans. This issue was discussed in an opinion paper from the Scientific Committee on Veterinary Measures Relating to Public Health (EC 1998) that identified parasite antigens (what is left of the parasite in the fish after it is frozen to kill the parasite) as a possible human health hazard.

Irradiation of fish is an effective method of eliminating metacercariae and other parasites (WHO 1995). For example, low-dose irradiation (0.15 kGy or less) was sufficient to inactivate metacercariae of C. sinensis and O. viverrini without affecting the sensory qualities of the fish (FAO/IAEA 1992). Hamster infectivity of O. viverrini metacercariae was prevented with 0.5 kGy (Bhaibulaya 1985). Trematodes, however, appear to be more sensitive to irradiation than other parasites. Earlier studies indicated that in order to kill A. simplex in salted herring, doses of as high as 6-10 kGy were necessary (van Mameren and Houwing 1968). Similarly, another study found A. simplex larvae to be highly resistant to irradiation doses of 2 kGy or 10 kGy (FAO/IAEA 1992). Data from studies on sensory characteristics of such products are inconsistent. The reason that anisakid larvae require much higher doses of irradiation than other parasites (for example, metacercariae, Trichinella larvae, coccidian protozoa) is that anisakiasis results from infection by the larvae. The doses of irradiation must be high enough to kill the larvae. For the other parasites just mentioned, irradiation prevents the parasitic worms from developing into adults that cause the respective diseases.

The applicability and consumer acceptability of irradiation of fish as well as any organoleptic effects should be considered and evaluated before attempting commercialization of this process and these products.

The following conclusions are based on a thorough analysis and evaluation of the current science on control methods of parasites that may be associated with the consumption of cold-smoked fish.

• Some of the fish species used for cold-smoked processing are either intermediate or final hosts to parasites. For this reason, assuring the harvesting of parasite-free fish in the wild is difficult.
• Some aquacultured fish are considered free of parasites (if their feeding regime has not been supplemented with raw fish) because their diet can be controlled using net-pens, closed recycled systems or their equivalent, and commercially pelleted diets. Consequently, these control measures must be carefully considered and applied. An analysis of the potential control points for parasites in aquacultured fish is beyond the scope of this report.
• Freezing raw fish prior to smoking remains the most effective way to ensure that viable parasites are not present in cold-smoked products consumed by the public. It is essential, therefore, that raw fish potentially containing viable parasites be frozen and held in that state for a period of time that assures destruction of all viable parasites in that fish species.

The following is a list of research areas that the panel suggests need further attention:

• Describe possible alternative freezing procedures that are or could be effective for inactivation of various fish parasites.
• Establish the kinetics and lethal effect of specific regimes of freezing on various fish parasites.
• Evaluate alternative processing procedures, such as high pressure and X-ray or e-beam irradiation for control of various fish parasites.
• Investigate the possible human health risks of allergic reactions due to parasite antigens remaining after freezing the fish to inactivate the live parasites.

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