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Effects of marine mammal parasites on human health
EFFECTS OF DARING CARNAL
PARASITES
TOMOO OSHIMA AND MICHAEL
ON DUGAN
HEALTH
KLIKS
Department of Parasitology, School of Medicine, Yokohama City University, Urafune-cho, Minami-ku, Yokohama City, Japan and Division of Comparative Medicine, School of Medicine, University of Hawaii, Hawaii, USA INTRODUCTION Excellent lists of marine mammal parasites have been published by Margolis & Dailey (1972) and Dailey & Brownell (1972), and Williams & Jones (1976) have reviewed the parasites of marine origin which are hazardous to man. Although there are many parasites of marine mammals, those which are hazardous to humans are restricted to the families Anisakidae (Nematoda) and Diphyllobothriidae (Cestoda). No ectoparasites or protozoan parasites of marine mammals are known to have infected humans. Trichinellosis was once suggested to be a zoonotic disease, cycling between eskimos and walrus in the arctic region (Myers, 1970; Williams &Jones, 1976). However, its epidemiologica importance is enigmatic at present. The common characteristics of these two groups of marine mammal parasites are as follows: 1. They are parasitic in the digestive tract and their eggs are discharged over a wide area in the host faeces. 2. The primary intermediate hosts are marine crustacea and the second intermediate hosts are marine fishes and squids. 3. The infection route to the marine mammal host is oral, by way of feeding on infected second intermediate hosts. The food habits of humans are also responsible for their infections. When humans consume uncooked marine fish and squid fillets, some species of these two groups of parasites are able to develop or persist temporarily in the human gastrointestinal tract and sometimes invade its wall, causing frank disease.
ANISAKIDAE The classifications scheme for the family Anisakidae of Hartwich (1974) consists of three subfamilies: Goezinae, Anisakinae and Raphidascarinae. The most important marine mammal nematodes affecting man are found in the subfamily Anisakinae, especially in the genera Anisakis and Pseudoterranova (=Phocanema=Terranova ), The status of the latter genus was recently revised by Gibson (1983). A number of comprehensive reviews of human infection with these worms, known as anisakiasis, have appeared (Oshima, 1972; Myers, 1975; van Thiel, 1976; Margolis, 1977; Smith & Wooten, 1978). Anisakis simplex A. simplex is the most common nematode found in the stomach of Cetaceans, especially Odontoceti, throughout the world and rarely in the stomach of pinnipeds (see Dailey & Brownell, 1972 and Margolis & Dailey, 1972). As the hosts of A. simplex in the coastal waters of Japan, seven species of cetaceans and one species of pinniped were reported (Oshima, 1972). The third-stage larva of this species is the major causative agent of human anisakiasis in Japan and Europe but not North America (Smith & Wooten, 1978; Kliks, 1983). This larva was originally referred to as Anisakis Type I (Berland, 1961). Van Banning (1971) succeeded in cultivating Anisakis Type I larvae to adult worm in vitro; later Pippy & van Banning (1971) identified the cultured adult as Anisakis simplex. The cultivation of Anisakis Type I larvae has also been 415
416
T. OS~?;~?IU utrdM. Kkks
carried out in various localities with similar results. Several species of marine crustacea belonging to the Euphausiacea, Decapoda and Amphipoda are known to be the first intermediate hosts (see Smith & Wooten, 1978). The euphausiid crustacea are universally the major primary host of A. simplex (Smith, 1983) in which the larvae developed from the second to the third stage, moulting once in the haemocoel. No development of larvae of A. simplex occurs in marine fishes and squids or in humans; these animals only serve as transport or paratenic hosts. Anisakis Type II larvae
Kagei, Sano, Takahashi, Tamura & Sakamoto (1978) identified Anisakis Type II larvae as a cause of acute gastric anisakiasis. Oshima, Oya & Wakai (1982) tried to cultivate Anisakis Type I1 larvae using the same method as that used with the Type I larvae, but all the larvae died and no adult worms were obtained. The final identification of Anisakis Type I1 larvae is still pending. Larvae
of Anisakis typica
No case of human anisakiasis due to infection by A. fypica larvae has yet been reported. Bargov (1982) reported Anisakis Type IA larvae in fish from the Philippine Sea which differed from Type I larvae. He claimed that they might be the larvae of A. typica. Histopathological studies may detect human cases of Anisakis typica in the future though they will be rare. Pselfduferranova
~=Phocane~?za=Terrano~~a~ decipiens
It has long been known that so called “codworm” was the 3rd stage larva of P. decipiens as reviewed by Margolis (1977). Between 1940 and 1981, 160 human cases of P. decipiens larvae infection were observed by endoscopy in northern Japan among people who consumed raw Pacific halibut, Pacific cod and squid (Koyama, Araki, Machida & Karasawa, 1982). After ingestion by man these worms frequently molt to the fourth-stage. In Japan larval invasion foci are restricted to the stomach; however, a worm of this type was noted as an incidental finding at laporotomy in the United States (Little & MacPhail, 1972). Kliks (1983) recently reported eight human cases from California, one of which involved infection with an adult male worm. In contrast to the situation in Japan and Holland the majority of North American cases of anisakiasis have involved this type of larva rather than Anisakis. In sensu stricto this disease should be called “pseudoterranoviasis”. However, the term anisakiasis has been widely applied to infection with any member of the family Anisakidae without causing any undue confusion. The natural definitive hosts of this species are usually Pinnipedia (seals, sea lions and walrus) and occasionally Cetacea (for precise host records see Daily & Brownell, 1972 and Margolis & Dailey, 1972). Cod and halibut are generally regarded as the most frequent paratenic hosts of 3rd stage larvae. However, many other commercial and non-commercial fish species have not been as adequately surveyed as these two popular food sources. Relatively large surveys of food fishes on the Pacific Coast of North America indicate that heavy infections with l? decipiens larvae occur in the edible portion of the flesh (Myers, 1979). Many species of inshore-dwelling rockfish (Sebastes) and anadromous salmon (Onchorhynchus) are known to have a high prevalence of infection. Both Alaskan salmon and rockfish (marketed as “Pacific red snapper”) have been implicated in human cases in California (Kiiks, 1983). Other species of Anisakid larvue potentially infective to man
Experimental infection studies indicate that several other anisakid larvae are capable of attaching to, and/or penetrating, the gastrointestinal mucosa of mammals. Deardorff, Kliks & Desowitz (1983) reported that a small Terranova-like third-stage larva recovered from the organs of wide variety of fishes (Deardoff, Kliks, Rosenthal, Rychlinski & Desowitz, 1982) caused gastric ulceration and hemorrhage when inoculated into rats. It is probable that as raw marine fishes and squids become popular food items in many parts of the world, novel species of anisakid parasites of marine mammals will be found to be capable of infecting man. Endoscopy
as a method of diagnosis and treatment
In present day Japan, when a patient visits our clinic complaining of acute abdominal symptoms after eating raw marine fish or squid, endoscopy is used to locate Anisakis or pseudoterranova larvae penetrating the stomach wall, and the larvae are removed with biopsy forceps (Sugimachi, Inokuchi, Ooiwa, Fujino & Ishii, 198.5). The use of the endoscope in clinics for the diagnosis and treatment of stomach anisakiasis has been widespread, resulting in the detection of an enormous number of patients.
Marine parasites and human health
417
Allergy in Anisakiasis
Local eosinophilia and granuloma formation of the host gastrointestinal wall at the invasion of Anisakis larvae seems to have little relation to the host’s immune status; i.e. whether the event is a primary infection or a multiple, hyperinfection of larvae. Eosinophilic phlegmonous inflammation of the host tissue around the worm may be induced by the direct influence of an eosinophil chemotactic factor (ECF) which is secreted by the invading worm (Twasaki & Torisu, 1982). This proposal required some amendments to be made to the “double hit or exacerbation” theory (see Smith & Wooten, 1978). However, cell mediated immune mechanisms clearly play some role in inducing granuloma formation with high local eosinophilia in the stomach and gut wall following the invasion of anisakid larvae (Sugane & Oshima, 1982). Raybourne, Desowitz, Kliks & Desowitz (1983) also reported the inhibition of rodent lymphoblast proliferation by excretory-secretory products of Anisakis and Pseudoterranova larvae. Larval E-S materials may modulate the granulomatous response associated with human anisakiasis. Prevalance of anisakiasis in Japan
Anisakiasis in Japan is widely distributed from Hokkaido to Okinawa. However, the incidence is highest on Kyushu Island. At the 27th meeting of the Japanese Society of Digestive Tract Endoscopy in 1984, a total of 3,141 cases of stomach anisakiasis were reported of which 2,236 cases were from Kyushu Island, 336 cases from Japan Sea coastal areas of the south-west half of Honshu Island, 489 cases from Hokkaido, 49 cases from Nagano Prefecture and 22 cases from Tokyo. According to Koyama et al. (1982) P. decipiens human infection occurs mainly in Hokkaido and occasionally in Kanazawa Prefecture and almost never on Kyushu Island. At the present moment, Kyushu Island is the main focus of stomach anisakiasis (in sensu stricto) in Japan. Hokkado is the second most important focus of gastric anisakiasis; 21.8% of patients were infected with P. pseudoterranova larvae (Koyama et al., 1982). The annual incidence of anisakiasis in Japan cannot be accurately determined. However, it is probably in excess of 1,000 symptomatic episodes per year. Intestinal anisakiasis 30 to 40% of anisakiasis cases involve the intestine, especially the ileum region (see Oshima, 1972). It is curious that no case of intestinal infection by P. decipiens has ever been reported. The pathology of intestinal anisakiasis is much more exudative and inflammatory than gastric anisakiasis and the onset of illness is acute and severe (Ishikura, 1971). Distribution of infection foci is concentrated in the ileum. However, it occurs in any locality from the duodenum to the rectum (Oshima, 1972). A few cases of transluminal migration of anisakid larvae with tumor formation on the omentum have been reported as incidental findings after surgery (Yoshimura, Kondo, Akao, Ohnishi, Watanabe, Shinno & Aikawa, 1979). Endoscopic diagnosis is only possible when the infection site is in the colon or rectum. Immunological diagnosis is not routinely applicable at the moment. Desowitz, Raybourne & Kliks (1985) have developed a radioallergosorbent (RAST) assay for detecting parasite-specific IgE antibodies which has proven useful for confirming diagnosis of subacute cases of anisakiasis. An ELISA for detecting parasite-specific IgG antibodies has been recently developed (M.M. Kliks, unpublished data). Elucidation of the patient’s recent dietary history and clinical signs are usually sufficient to make a diagnosis of intestinal anisakiasis. As Ishikura (1968) stated, when an experienced physician is able to confirm a diagnosis of intestinal anisakiasis there is no need of surgery. A conservative allopathic treatment is indicated. The control of anisakiasis
Important sources of human anisakiasis (in sensu stricto) infection in Japan are the common mackerel, Pneumatophorus japonicus japonicus, chum salmon, Onchorhynchus keta, Pacific pollock, Theragra chalcogramma and Suumeika squid, Todarodes pacificus. Sources of Pseudoterranova larval infection are the Pacific cod, Gadus morrhua macrocephalus, and halibut, Hipoglossus stenolepis. In North America, rockfish (Sebastes spp.) and salmon are involved in transmission to humans (Kliks, 1983) and in Europe herring (&pea spp.) is the major source of human infection (van Thiel, 1976). In the Netherlands, freezing regulations were introduced in 1968 to prevent anisakiasis. Herring must be frozen within 12 hours and kept at this temperature for at least 24 hours. This regulation has resulted in a remarkable reduction in the number of cases in the Netherlands (van Thiel, 1976). Unlike the situation in Europe, in Japan legislative control of marine fishes and squids for the prevention of anisakiasis is both impractical and culturally unacceptable, but some effective measures can be taken. The holding of potentially infective marine fishes and squid at -20°C for more than 24 hours before eating raw and consistent health education of the people the dangers of anisakiasis may be possible.
418
T.
O~~~i~~~ und M K1ik.t
DIPHY ~~UB~THRII~A~ Among the family Diphyllobo&hriidae, two genera, Djp~og~?lo~orKs and Dipltyllobothriz~ln, which are normally found as parasites of cetaceans and pinnipeds, have been implicated in human infection in Alaska, North America, Hawaiian Islands, Scandinavia, Peru and Japan where peopfe are likeiy to consume raw (or slightly salted or lightly cooked) marine or estuarine fish. In contrast to the anisakid nematodes which generally affect man as the larval stage only, these very large tapeworms are capabte of growth and maturation in the human intestine. The taxonomy of these two cestode genera is still uncertain and the life cycles of most of the species are not completely known. The differential identification of the larval stages of these cestodes is almost impossible. Reports of human cases of infection with these tapeworms of marine origin often avoid specific identification of the worms and describe them as ~iph~lfobothriLlm or ~~~log~nap~rz~s sp. Di~l~g~l~~~or~s b~~~e~~~ter~e D. baf~eno~terffe was originalIy found in the intestine of a sei whale caught off Norway in 1892. ft has subsequently been recorded often from whales of the family Balenopteridae, from the coastat waters of Japan, especialiy from little piked whales (B~~~~~~nop~erue~c~stor~strfftff). In Japan, human cases of ~~~~ug~~opo~~~ infection have been known since 1894. Up to the present time there have been 91 documented cases. These were identified as D. grandis which was thought restricted to humans. However, after careful morphological study of specimens of both species, Rausch (1964) and Iwata (1%5) concluded that these two species should be regarded as synonymous. Kamo (1971) reserved both names because of the wide range of morphological variation among the two species. Generally speaking, it seems more appropriate to accept the synonymy of these species. The distribution of patients has been restricted to the coastal regions of south-western Japan (Kamo 1969; Yamane, Maejima, Yazaki & Fukumoto, 1977). Clinical symptoms included diarrhoea, abdominal pain, nausea, vomiting, anorexia and general fatigue. Spontaneous discharge of the strobila often occurs without any treatment. Symptoms and worm infections spontaneously subsided in the majority of patients. Epidemiologically, nothing is known except that the patients frequently ate raw marine fish such as sardines, Pacific mackerel, bonito and squid, Little piked whales also consume these marine fishes as food. Unfortunately, no record of the plerocercoids of D. b~l~e~upterue in fishes and squids is available, but it is most likely that both whates and humans ingest certain marine fishes which act as second intermediate hosts of D. b~~~e~~~~ter~e. Development of the worms in the human intestine seems to be incomplete and they may be spontaneously discharged. As far as the first intermediate hosts are concerned, Kamo, Iwata, Hatsushika c1:Maejima (1973) carried out experimental infections of 33 species of marine copepoda with coracidia of D. grandis and D. balaenopterae. Fully developed procercoids were recovered from the hemocoel of Oithona nanu and Labidocera japonica. Di~hyliub~thr~~m Rausch & Hiltard (1970) recovered six species of the genus ~~~~y~~~but~zr~~i~ {D. f~t~~?~, D. d~~dr~i~cum, D. ~~~~eolutt~rn, D. ursi, D. d&m and a. afnscense) from humans in Alaska of which D. la&m was most common. They suggested that marine and terrestria1 mammals consumed anadromous fish as a common source of infection. According to Margoljs & Dailey (1972) six species of D~~hy~~obothr~~~rn are known from marine mammals. Kamo, Maejima, Yazaki & Fukumoto (1982) listed eight species from marine mammals of the coastal waters of Japan. L1. ~u?ner~~~and I). ~~c~~cu~ are found to occur rarely as human parasites. D. cameroni was originally collected from the Hawaiian monk seal and the first record of human infection was reported by Kamo, Yamane and Kawashima (1981). L). ~~c~~c~rn is a wet1 known parasite of the northern fur seal, Stellar’s sea lion and California sea lion. Human infections have been reported from Peru (Baer, 1969), Chile (Atiass & Cattan, 1976; Sagua, Miranda, Fuetes & Vladillo, 1976) and Japan (Kamo, Maejima, Yazaki, Otsuru, Hasegawa, Kuniyoshi & Asato, 1982). All these cases are thought to be incidental infections and the infectious sources were unknown. Yamane, Kamo, Yazaki, Fukumoto & Maejima (1981) described a new species, Diphyllobathrium vonagoensis, from a human, thought to be derived from a marine mammal parasite. Four cases of human infection with an unidentified “Koga-0kamura type” d~~hyll~b~thr~~d were reported by Hasegawa, Tamaki, Asato & Otsuru (1984) and Kamo, Yamane, Maejima, Yazaki & Fukumoto (1977). No information on the Iife cycle of this worm is available.
Marine parasites and human health Diphpllobothrium D.
lattim in
419
Japan
latum
infection among Japanese people has a long history. After the 1940’s the infection rate subsided, but since 1970 diphyllobothriasis has reappeared and the number of patients is increasing. Annually about 100 new human infections have been found (Oshima, 1983). The Japanese strain of D. latum apparently has a special affinity at its plerocercoid stage for anadromous salmodidae (Onchorhynthus masou and Onchorhynchus gorbuscha) also shows some differences in adult morphology and physiology from the European strain. The latter species is transmitted in a freshwater ecosystem, while the former is associated with the marine environment. The gross adult morphology of the adult stages, however, is very similar. At the present time it is difficult to determine whether both strains belong to the same or different species. Usually D. latum is an anthropogenic cestode. However, seven species of pinnipeds (walrus, harbor seal, ringed seal, hooded seal, Mediterranean monk seal and harbor porpoise) also become infected (Dailey & Brownell, 1972). No valid record of D. latum was found in the parasites of marine mammals caught off the west coast of North America (Margolis & Dailey, 1972). A minor outbreak (51 cases) of infection with a worm resembling D. latum was recently reported from several parts of the United States (Ruttenber, Weniger, Sorvillo, Murray & Ford, 1984). Most patients had a history of eating raw salmon from Alaska. SUMMARY Marine mammals and humans have in common the consumption of raw marine fishes and squids. When man ingests these sea foods raw, juvenile stages of some marine mammal parasites are able to invade the human digestive tract, remaining temporarily or developing to the adult stage. Among these parasites, nematodes belonging to the family Anisakidae attack man severely, especially Anisakis simplex and Pseudoterranova decipiens, both of which can cause acute abdominal symptoms. In Japan more then three thousand cases have been documented and it is estimated that more than one thousand people are infected annually. Diagnosis, treatment and preventative measures are discussed. Another group of marine mammal parasites which infect humans belongs to the family Diphyllobothriidae. The most important genus is Diplogonoporus, which has been responsible for about one hundred human cases in Japan. Diphyllobothrium datum from the Far East show slight differences in morphology and biological characteristics from European and American specimens. REFERENCES ATIAS A. & CATTAN P.E. 1976. First case of human infection with Diphyllobothrium
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garage Diphyllobothrkm 30: 101-111. YOSHIMURA
(Cestoda:
Pseudophyllidea
parasites
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and ~urn~n ~ea~fh
found from a man in Japan. Japanese
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H., KONDO K., OHNISWI Y., WATANABEK., SHINNO B. & AIKAWA K. 1979. Two cases of eosinophilic granulomas formed in the large omentum and mesentery by penetration of Anisakis larvae through the gastrointestinal tract. Stomach and Intestine 14: 519-522. (In Japanese).
PARASITES
TOMOO OSHIMA AND MICHAEL
ON DUGAN
HEALTH
KLIKS
Department of Parasitology, School of Medicine, Yokohama City University, Urafune-cho, Minami-ku, Yokohama City, Japan and Division of Comparative Medicine, School of Medicine, University of Hawaii, Hawaii, USA INTRODUCTION Excellent lists of marine mammal parasites have been published by Margolis & Dailey (1972) and Dailey & Brownell (1972), and Williams & Jones (1976) have reviewed the parasites of marine origin which are hazardous to man. Although there are many parasites of marine mammals, those which are hazardous to humans are restricted to the families Anisakidae (Nematoda) and Diphyllobothriidae (Cestoda). No ectoparasites or protozoan parasites of marine mammals are known to have infected humans. Trichinellosis was once suggested to be a zoonotic disease, cycling between eskimos and walrus in the arctic region (Myers, 1970; Williams &Jones, 1976). However, its epidemiologica importance is enigmatic at present. The common characteristics of these two groups of marine mammal parasites are as follows: 1. They are parasitic in the digestive tract and their eggs are discharged over a wide area in the host faeces. 2. The primary intermediate hosts are marine crustacea and the second intermediate hosts are marine fishes and squids. 3. The infection route to the marine mammal host is oral, by way of feeding on infected second intermediate hosts. The food habits of humans are also responsible for their infections. When humans consume uncooked marine fish and squid fillets, some species of these two groups of parasites are able to develop or persist temporarily in the human gastrointestinal tract and sometimes invade its wall, causing frank disease.
ANISAKIDAE The classifications scheme for the family Anisakidae of Hartwich (1974) consists of three subfamilies: Goezinae, Anisakinae and Raphidascarinae. The most important marine mammal nematodes affecting man are found in the subfamily Anisakinae, especially in the genera Anisakis and Pseudoterranova (=Phocanema=Terranova ), The status of the latter genus was recently revised by Gibson (1983). A number of comprehensive reviews of human infection with these worms, known as anisakiasis, have appeared (Oshima, 1972; Myers, 1975; van Thiel, 1976; Margolis, 1977; Smith & Wooten, 1978). Anisakis simplex A. simplex is the most common nematode found in the stomach of Cetaceans, especially Odontoceti, throughout the world and rarely in the stomach of pinnipeds (see Dailey & Brownell, 1972 and Margolis & Dailey, 1972). As the hosts of A. simplex in the coastal waters of Japan, seven species of cetaceans and one species of pinniped were reported (Oshima, 1972). The third-stage larva of this species is the major causative agent of human anisakiasis in Japan and Europe but not North America (Smith & Wooten, 1978; Kliks, 1983). This larva was originally referred to as Anisakis Type I (Berland, 1961). Van Banning (1971) succeeded in cultivating Anisakis Type I larvae to adult worm in vitro; later Pippy & van Banning (1971) identified the cultured adult as Anisakis simplex. The cultivation of Anisakis Type I larvae has also been 415
416
T. OS~?;~?IU utrdM. Kkks
carried out in various localities with similar results. Several species of marine crustacea belonging to the Euphausiacea, Decapoda and Amphipoda are known to be the first intermediate hosts (see Smith & Wooten, 1978). The euphausiid crustacea are universally the major primary host of A. simplex (Smith, 1983) in which the larvae developed from the second to the third stage, moulting once in the haemocoel. No development of larvae of A. simplex occurs in marine fishes and squids or in humans; these animals only serve as transport or paratenic hosts. Anisakis Type II larvae
Kagei, Sano, Takahashi, Tamura & Sakamoto (1978) identified Anisakis Type II larvae as a cause of acute gastric anisakiasis. Oshima, Oya & Wakai (1982) tried to cultivate Anisakis Type I1 larvae using the same method as that used with the Type I larvae, but all the larvae died and no adult worms were obtained. The final identification of Anisakis Type I1 larvae is still pending. Larvae
of Anisakis typica
No case of human anisakiasis due to infection by A. fypica larvae has yet been reported. Bargov (1982) reported Anisakis Type IA larvae in fish from the Philippine Sea which differed from Type I larvae. He claimed that they might be the larvae of A. typica. Histopathological studies may detect human cases of Anisakis typica in the future though they will be rare. Pselfduferranova
~=Phocane~?za=Terrano~~a~ decipiens
It has long been known that so called “codworm” was the 3rd stage larva of P. decipiens as reviewed by Margolis (1977). Between 1940 and 1981, 160 human cases of P. decipiens larvae infection were observed by endoscopy in northern Japan among people who consumed raw Pacific halibut, Pacific cod and squid (Koyama, Araki, Machida & Karasawa, 1982). After ingestion by man these worms frequently molt to the fourth-stage. In Japan larval invasion foci are restricted to the stomach; however, a worm of this type was noted as an incidental finding at laporotomy in the United States (Little & MacPhail, 1972). Kliks (1983) recently reported eight human cases from California, one of which involved infection with an adult male worm. In contrast to the situation in Japan and Holland the majority of North American cases of anisakiasis have involved this type of larva rather than Anisakis. In sensu stricto this disease should be called “pseudoterranoviasis”. However, the term anisakiasis has been widely applied to infection with any member of the family Anisakidae without causing any undue confusion. The natural definitive hosts of this species are usually Pinnipedia (seals, sea lions and walrus) and occasionally Cetacea (for precise host records see Daily & Brownell, 1972 and Margolis & Dailey, 1972). Cod and halibut are generally regarded as the most frequent paratenic hosts of 3rd stage larvae. However, many other commercial and non-commercial fish species have not been as adequately surveyed as these two popular food sources. Relatively large surveys of food fishes on the Pacific Coast of North America indicate that heavy infections with l? decipiens larvae occur in the edible portion of the flesh (Myers, 1979). Many species of inshore-dwelling rockfish (Sebastes) and anadromous salmon (Onchorhynchus) are known to have a high prevalence of infection. Both Alaskan salmon and rockfish (marketed as “Pacific red snapper”) have been implicated in human cases in California (Kiiks, 1983). Other species of Anisakid larvue potentially infective to man
Experimental infection studies indicate that several other anisakid larvae are capable of attaching to, and/or penetrating, the gastrointestinal mucosa of mammals. Deardorff, Kliks & Desowitz (1983) reported that a small Terranova-like third-stage larva recovered from the organs of wide variety of fishes (Deardoff, Kliks, Rosenthal, Rychlinski & Desowitz, 1982) caused gastric ulceration and hemorrhage when inoculated into rats. It is probable that as raw marine fishes and squids become popular food items in many parts of the world, novel species of anisakid parasites of marine mammals will be found to be capable of infecting man. Endoscopy
as a method of diagnosis and treatment
In present day Japan, when a patient visits our clinic complaining of acute abdominal symptoms after eating raw marine fish or squid, endoscopy is used to locate Anisakis or pseudoterranova larvae penetrating the stomach wall, and the larvae are removed with biopsy forceps (Sugimachi, Inokuchi, Ooiwa, Fujino & Ishii, 198.5). The use of the endoscope in clinics for the diagnosis and treatment of stomach anisakiasis has been widespread, resulting in the detection of an enormous number of patients.
Marine parasites and human health
417
Allergy in Anisakiasis
Local eosinophilia and granuloma formation of the host gastrointestinal wall at the invasion of Anisakis larvae seems to have little relation to the host’s immune status; i.e. whether the event is a primary infection or a multiple, hyperinfection of larvae. Eosinophilic phlegmonous inflammation of the host tissue around the worm may be induced by the direct influence of an eosinophil chemotactic factor (ECF) which is secreted by the invading worm (Twasaki & Torisu, 1982). This proposal required some amendments to be made to the “double hit or exacerbation” theory (see Smith & Wooten, 1978). However, cell mediated immune mechanisms clearly play some role in inducing granuloma formation with high local eosinophilia in the stomach and gut wall following the invasion of anisakid larvae (Sugane & Oshima, 1982). Raybourne, Desowitz, Kliks & Desowitz (1983) also reported the inhibition of rodent lymphoblast proliferation by excretory-secretory products of Anisakis and Pseudoterranova larvae. Larval E-S materials may modulate the granulomatous response associated with human anisakiasis. Prevalance of anisakiasis in Japan
Anisakiasis in Japan is widely distributed from Hokkaido to Okinawa. However, the incidence is highest on Kyushu Island. At the 27th meeting of the Japanese Society of Digestive Tract Endoscopy in 1984, a total of 3,141 cases of stomach anisakiasis were reported of which 2,236 cases were from Kyushu Island, 336 cases from Japan Sea coastal areas of the south-west half of Honshu Island, 489 cases from Hokkaido, 49 cases from Nagano Prefecture and 22 cases from Tokyo. According to Koyama et al. (1982) P. decipiens human infection occurs mainly in Hokkaido and occasionally in Kanazawa Prefecture and almost never on Kyushu Island. At the present moment, Kyushu Island is the main focus of stomach anisakiasis (in sensu stricto) in Japan. Hokkado is the second most important focus of gastric anisakiasis; 21.8% of patients were infected with P. pseudoterranova larvae (Koyama et al., 1982). The annual incidence of anisakiasis in Japan cannot be accurately determined. However, it is probably in excess of 1,000 symptomatic episodes per year. Intestinal anisakiasis 30 to 40% of anisakiasis cases involve the intestine, especially the ileum region (see Oshima, 1972). It is curious that no case of intestinal infection by P. decipiens has ever been reported. The pathology of intestinal anisakiasis is much more exudative and inflammatory than gastric anisakiasis and the onset of illness is acute and severe (Ishikura, 1971). Distribution of infection foci is concentrated in the ileum. However, it occurs in any locality from the duodenum to the rectum (Oshima, 1972). A few cases of transluminal migration of anisakid larvae with tumor formation on the omentum have been reported as incidental findings after surgery (Yoshimura, Kondo, Akao, Ohnishi, Watanabe, Shinno & Aikawa, 1979). Endoscopic diagnosis is only possible when the infection site is in the colon or rectum. Immunological diagnosis is not routinely applicable at the moment. Desowitz, Raybourne & Kliks (1985) have developed a radioallergosorbent (RAST) assay for detecting parasite-specific IgE antibodies which has proven useful for confirming diagnosis of subacute cases of anisakiasis. An ELISA for detecting parasite-specific IgG antibodies has been recently developed (M.M. Kliks, unpublished data). Elucidation of the patient’s recent dietary history and clinical signs are usually sufficient to make a diagnosis of intestinal anisakiasis. As Ishikura (1968) stated, when an experienced physician is able to confirm a diagnosis of intestinal anisakiasis there is no need of surgery. A conservative allopathic treatment is indicated. The control of anisakiasis
Important sources of human anisakiasis (in sensu stricto) infection in Japan are the common mackerel, Pneumatophorus japonicus japonicus, chum salmon, Onchorhynchus keta, Pacific pollock, Theragra chalcogramma and Suumeika squid, Todarodes pacificus. Sources of Pseudoterranova larval infection are the Pacific cod, Gadus morrhua macrocephalus, and halibut, Hipoglossus stenolepis. In North America, rockfish (Sebastes spp.) and salmon are involved in transmission to humans (Kliks, 1983) and in Europe herring (&pea spp.) is the major source of human infection (van Thiel, 1976). In the Netherlands, freezing regulations were introduced in 1968 to prevent anisakiasis. Herring must be frozen within 12 hours and kept at this temperature for at least 24 hours. This regulation has resulted in a remarkable reduction in the number of cases in the Netherlands (van Thiel, 1976). Unlike the situation in Europe, in Japan legislative control of marine fishes and squids for the prevention of anisakiasis is both impractical and culturally unacceptable, but some effective measures can be taken. The holding of potentially infective marine fishes and squid at -20°C for more than 24 hours before eating raw and consistent health education of the people the dangers of anisakiasis may be possible.
418
T.
O~~~i~~~ und M K1ik.t
DIPHY ~~UB~THRII~A~ Among the family Diphyllobo&hriidae, two genera, Djp~og~?lo~orKs and Dipltyllobothriz~ln, which are normally found as parasites of cetaceans and pinnipeds, have been implicated in human infection in Alaska, North America, Hawaiian Islands, Scandinavia, Peru and Japan where peopfe are likeiy to consume raw (or slightly salted or lightly cooked) marine or estuarine fish. In contrast to the anisakid nematodes which generally affect man as the larval stage only, these very large tapeworms are capabte of growth and maturation in the human intestine. The taxonomy of these two cestode genera is still uncertain and the life cycles of most of the species are not completely known. The differential identification of the larval stages of these cestodes is almost impossible. Reports of human cases of infection with these tapeworms of marine origin often avoid specific identification of the worms and describe them as ~iph~lfobothriLlm or ~~~log~nap~rz~s sp. Di~l~g~l~~~or~s b~~~e~~~ter~e D. baf~eno~terffe was originalIy found in the intestine of a sei whale caught off Norway in 1892. ft has subsequently been recorded often from whales of the family Balenopteridae, from the coastat waters of Japan, especialiy from little piked whales (B~~~~~~nop~erue~c~stor~strfftff). In Japan, human cases of ~~~~ug~~opo~~~ infection have been known since 1894. Up to the present time there have been 91 documented cases. These were identified as D. grandis which was thought restricted to humans. However, after careful morphological study of specimens of both species, Rausch (1964) and Iwata (1%5) concluded that these two species should be regarded as synonymous. Kamo (1971) reserved both names because of the wide range of morphological variation among the two species. Generally speaking, it seems more appropriate to accept the synonymy of these species. The distribution of patients has been restricted to the coastal regions of south-western Japan (Kamo 1969; Yamane, Maejima, Yazaki & Fukumoto, 1977). Clinical symptoms included diarrhoea, abdominal pain, nausea, vomiting, anorexia and general fatigue. Spontaneous discharge of the strobila often occurs without any treatment. Symptoms and worm infections spontaneously subsided in the majority of patients. Epidemiologically, nothing is known except that the patients frequently ate raw marine fish such as sardines, Pacific mackerel, bonito and squid, Little piked whales also consume these marine fishes as food. Unfortunately, no record of the plerocercoids of D. b~l~e~upterue in fishes and squids is available, but it is most likely that both whates and humans ingest certain marine fishes which act as second intermediate hosts of D. b~~~e~~~~ter~e. Development of the worms in the human intestine seems to be incomplete and they may be spontaneously discharged. As far as the first intermediate hosts are concerned, Kamo, Iwata, Hatsushika c1:Maejima (1973) carried out experimental infections of 33 species of marine copepoda with coracidia of D. grandis and D. balaenopterae. Fully developed procercoids were recovered from the hemocoel of Oithona nanu and Labidocera japonica. Di~hyliub~thr~~m Rausch & Hiltard (1970) recovered six species of the genus ~~~~y~~~but~zr~~i~ {D. f~t~~?~, D. d~~dr~i~cum, D. ~~~~eolutt~rn, D. ursi, D. d&m and a. afnscense) from humans in Alaska of which D. la&m was most common. They suggested that marine and terrestria1 mammals consumed anadromous fish as a common source of infection. According to Margoljs & Dailey (1972) six species of D~~hy~~obothr~~~rn are known from marine mammals. Kamo, Maejima, Yazaki & Fukumoto (1982) listed eight species from marine mammals of the coastal waters of Japan. L1. ~u?ner~~~and I). ~~c~~cu~ are found to occur rarely as human parasites. D. cameroni was originally collected from the Hawaiian monk seal and the first record of human infection was reported by Kamo, Yamane and Kawashima (1981). L). ~~c~~c~rn is a wet1 known parasite of the northern fur seal, Stellar’s sea lion and California sea lion. Human infections have been reported from Peru (Baer, 1969), Chile (Atiass & Cattan, 1976; Sagua, Miranda, Fuetes & Vladillo, 1976) and Japan (Kamo, Maejima, Yazaki, Otsuru, Hasegawa, Kuniyoshi & Asato, 1982). All these cases are thought to be incidental infections and the infectious sources were unknown. Yamane, Kamo, Yazaki, Fukumoto & Maejima (1981) described a new species, Diphyllobathrium vonagoensis, from a human, thought to be derived from a marine mammal parasite. Four cases of human infection with an unidentified “Koga-0kamura type” d~~hyll~b~thr~~d were reported by Hasegawa, Tamaki, Asato & Otsuru (1984) and Kamo, Yamane, Maejima, Yazaki & Fukumoto (1977). No information on the Iife cycle of this worm is available.
Marine parasites and human health Diphpllobothrium D.
lattim in
419
Japan
latum
infection among Japanese people has a long history. After the 1940’s the infection rate subsided, but since 1970 diphyllobothriasis has reappeared and the number of patients is increasing. Annually about 100 new human infections have been found (Oshima, 1983). The Japanese strain of D. latum apparently has a special affinity at its plerocercoid stage for anadromous salmodidae (Onchorhynthus masou and Onchorhynchus gorbuscha) also shows some differences in adult morphology and physiology from the European strain. The latter species is transmitted in a freshwater ecosystem, while the former is associated with the marine environment. The gross adult morphology of the adult stages, however, is very similar. At the present time it is difficult to determine whether both strains belong to the same or different species. Usually D. latum is an anthropogenic cestode. However, seven species of pinnipeds (walrus, harbor seal, ringed seal, hooded seal, Mediterranean monk seal and harbor porpoise) also become infected (Dailey & Brownell, 1972). No valid record of D. latum was found in the parasites of marine mammals caught off the west coast of North America (Margolis & Dailey, 1972). A minor outbreak (51 cases) of infection with a worm resembling D. latum was recently reported from several parts of the United States (Ruttenber, Weniger, Sorvillo, Murray & Ford, 1984). Most patients had a history of eating raw salmon from Alaska. SUMMARY Marine mammals and humans have in common the consumption of raw marine fishes and squids. When man ingests these sea foods raw, juvenile stages of some marine mammal parasites are able to invade the human digestive tract, remaining temporarily or developing to the adult stage. Among these parasites, nematodes belonging to the family Anisakidae attack man severely, especially Anisakis simplex and Pseudoterranova decipiens, both of which can cause acute abdominal symptoms. In Japan more then three thousand cases have been documented and it is estimated that more than one thousand people are infected annually. Diagnosis, treatment and preventative measures are discussed. Another group of marine mammal parasites which infect humans belongs to the family Diphyllobothriidae. The most important genus is Diplogonoporus, which has been responsible for about one hundred human cases in Japan. Diphyllobothrium datum from the Far East show slight differences in morphology and biological characteristics from European and American specimens. REFERENCES ATIAS A. & CATTAN P.E. 1976. First case of human infection with Diphyllobothrium
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garage Diphyllobothrkm 30: 101-111. YOSHIMURA
(Cestoda:
Pseudophyllidea
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and ~urn~n ~ea~fh
found from a man in Japan. Japanese
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H., KONDO K., OHNISWI Y., WATANABEK., SHINNO B. & AIKAWA K. 1979. Two cases of eosinophilic granulomas formed in the large omentum and mesentery by penetration of Anisakis larvae through the gastrointestinal tract. Stomach and Intestine 14: 519-522. (In Japanese).