FISH - AND SHELLFISH - BORNETREMATODE INFECTIONS IN CANADA

Brent R Dixon' and Rick B Flohr-

1Food Directorate, Health Canada, Ottawa, Ontario, Canada, KIAOL2; 2Inspection Directorate, Fisheries andOceans Canada, Ottawa, Ontario, Canada KIA OE6

Abstract. Food-borne trematode infections are endemic in various parts of tbe world, particularly Soutbeast Asia.Despite the high prevalence, morbidity and total costs of these infections, tbey remain poorly recognized by publichealth authorities and consumers. Factors such as poor sanitation and traditional metbods of food preparationhasten the spread of food-borne trematode infections in endemic regions and must be carefully examined in orderto develop effective control strategies. There is also a growing risk to consumers in non-endemic countries as aresult of international trade. A considerable quantity of freshwater fish and shellfish is imported into Canada fromendemic countries in Southest Asia. Some of these products are imported fresh or processed in such a way that theinfecti ve metacercariae may not be destroyed. Further, current inspection procedures in Canada may not detect tbepresence of all parasites in imported fish productes. Therefore, tbere may be a risk of infection if the fish orshellfish is consumed raw or lightly cooked. Many of the cases of infection in Canada involve recent immigrantsfrom endemic regions who have become infected either before arriving or through the consumption of tread it ion aIor ethnic dishes prepared from imported products. International travel and the increasing availability and interestin etbnic foods also contribute to the risk of infection in all Canadians. In addition to these imported trematodes,a number of species are found in freshwater fishes and shellfish in Nouth America and have also caused illness inhumans. Altbough the prevalence of infection remains relatively low in Canada, the need for an increased generalawareness of food-borne trematode infections and their causes is indicated.

INTRODUCTION

It has been estimated that over 50 million peopleworld-wide are currently infected with food-bornetrematodes (Lima dos Santos, 1995). The majority ofthese infections result from the consumption of raw orlightly cooked freshwater fish or shellfish (crustaceans)containing viable metcercariae. Depending on theparasite species, these infections may occur in theliver, lungs, small intestine, and occasionally thebrain or other tissues, and produce symptoms rangingin severity from mild to debilitating and life-threaten-ing. The direct or indirect cost of diseases causedby food-borne trematodes is thought to be very high(WHO, 1993a, b). In addition to medical costs, lossof income and productivity exert a heavy burden onthe economy of endemic countries such as Thailand,where the total cost of liver fluke infections alone maybe as high as USS 84.6 millon per year (Loaharanuand Sornmani, 1991).

Despite the prevalence and high cost, particularlyin Southeast Asia, food-borne trematode infections arepoorly recognizied by public health authorities andconsumers alike. This lack of information probablyrepresents the single most important obstacle in the

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effective control of this problem. A number of factorsimpact on the spread of food-borne trematode infec-tions and each of these must be carefully examined inorder to develop control strategies (Rim et al, 1994).

There is also a growing risk to consumers in non-endemic regions as a result of international trade. InCanada, an increasing quantity of freshwater fish andshellfish is being imported from endemic regions.While much of it is frozen or canned, some is importedfresh or processed in such a way that metacercariaeare not killed. Further, since current inspection proce-dures for imported freshwater fish and shellfish maynot detect the presence of all parasites, there is a riskof infection if the product is subsequently consumedraw or lightly cooked. Many of the cases of food-bornetrematode infections which have been diagnosed inCanada have involved recent immigrants from endemicregions. While most of these individuals will probablyhave become infected before arriving, some cases havedeveloped in Canada through the consumption of tra-ditional dishes prepared using products imported fromendemic regions. The increasing interest in ethnicdishes containing raw or lightly cooked fish or shell-fish, however, contributes to the risk of infection by allCanadians. Travel and tourism to endemic regions is

also increasing and constitutes a further risk to thosewho consume traditional foods during their travels.

In addition to those infections resulting from theconsumption of imported products, some trematodesare present in fish and shellfish in North America andhave also been responsible for infections in humans.

TREMATODES OF PUBLIC HEALTH CONCERN

1. Liver flukes

Clonorchis sinensis

Human infections with the Chinese liver fluke arehighly prevalent in China (Li, 199 I), Korea (Chungand Soh, 1991; Soh, 1991), Taiwan (Chen, 199Ia,b),Vietnam and Japan. Over 5 million people are infectedin China alone (WHO, 1993a,b). It is also an impor-tant parasitic infection in Chinese communitiesoverseas (WHO, 1993a,b). An increasing number ofhuman cases are being diagnosed and reported innon-endemic areas such as North America and west-ern Europe (Sirisinha et ai, 199 I). In Canada, Duchastel(1984) reported that C. sinensis was the most commonparasitic infection among Hong Kong residents whoapplied to emigrate during 1979-1981. Of the 25,095individuals examined, 13.4% yielded a positive stoolsample for C. sinensis ova. This parasite was also listedamong the ten most prevalent parasites detected inimmigrants to Quebec in 1976 and 1977 (Gyorkos,1978). Most of these infections occurred in immigrantsfrom Hong Kong and China. Croll and Gyorkos (1979)reported that C. sinensis is not transmitted in Canadaand is found, most frequently, in immigrants to Canadafrom the Far East. Unspecified trematodes of theClonorchis/Opisthorchis group have also been identi-fied in 30 states in the United States, and were the mostfrequently identified trematode in a recent nationalsurvey (Kappus et ai, 1991, 1994). A total of 1,226stool specimens, out of 216,275 examined, were posi-tive for this trematode group.

Opisthorchis spp

Opisthorchis viverrini is prevalent in SoutheastAsia, particularly in Thailand, Lao PDR, and Cambo-dia (Khamboonruang, 1991; Scholz et ai, 1991; WHOI993a,b). Over 7 Million people are thought to beinfected in Thailand alone (WHO, 1993a). The preva-lence is particularly high in northeast Thailand wherefreshwater fish is the most common source of animalprotein. Another species, O.felineus, is found mostlyin eastem Europe and the former Soviet Union, whereapproximately 2 million people are infected (WHO,

1993a,b). Although they are not always distinguishedfrom clonorchiasis, infections with Opisthorchis sppare apparently being reported more frequently inNorth America and western Europe.

Metorchis conjunctus

The Canadian liver fluke was recently identifiedin an outbreak situation in Quebec (McLean et ai,1996). A group of Korean nationals consumed rawwhite sucker, Catostomus commersoni, freshly caughtin a small river north of Montreal. After an incubationperiod of 1-15 days, 17 of the 19 individuals becamesymptomatic. Symptoms included abdominal pain,fever, headache, anorexia, diarrhea, nausea, and back-ache. Symptoms resolved spontaneously or followingtreatment with praziquantel. A direct relationship wasfound between the quantity of fish eaten and the sever-ity of symptoms. An examination of unconsumed fishrevealed an average of over 7 metacercariae per gramof flesh.

A number of earlier incidents of infection inCanada have also been documented. Eaton (1975)reported the presence of M. conjunctus eggs in agroup of native Indians in northern Saskatchewan.Much of the fish consumed by these people was smokedover an open fire witout any further cooking. Aboutone third of the members ofthis group (24 cases) werefound to be infected, with some families having allmembers infected. Sucker was a regular item in thediet of these people. All of the cases reported weresub-clinical. Several cases of infection withM. conjunctus were diagnosed at the Toronto PublicHealth Laboratory (Scholten and Yang, 1975). Naimanet al (1980) reported one case of infection in a nativeIndian child who had intermittent bouts of milddiarrhea. Presumably, the infection was acquireddurring one of his summer visits to a reservation innorthern Manitoba.

M. conjunctus has been found in Canada fromSaskatchewan to the Atlantic coast and from theArctic to the US border (Eaton, 1975). It has also beenreported from the Eastern United States as far south asNorth Carolina.

2. Lung flukes

Paragonimus spp are lung flukes which occur inhumans and numerous other mammals. Humanparagonimiasis may be caused by several differentspecies of Paragonimus (WHO, 1993a). This diseasehas been reported from 39 countries (Rim et ai,1994). These parasites are endemic in most Asiancountries, including Thailand (Ekarohit et ai, 1991;

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Khamboonruang, 1991) Japan (Kamiya and Ooi,1991; Nawa, 1991), Korea (Chung and Soh,1991;Soh, 1991), and China (Xu, 1991), as well as a fewcountries in West Africa (Sachs and Cumberlidge,1990; Pozio, 1991). Approximately 22 million peopleare thought to be infected in these regions (WHO,1993a,b). In the western hemisphere, it has beenreported from most countries, but most notably fromEcuador and Peru (WHO, I993a,b ). In Canada, Belandet al (1969) described four cases of paragonimiasisin the province of Quebec. One of these patientshad never been outside of Quebec. Through question-ing, it was revealed that he had sold live snailsand crustaceans from an exotic food section of adepartment store. Although he did not consumethese items, he may have accidentally ingested watercontaminated with these animals. Another caseinvolved an Italian man who had immigrated toCanada three years earlier. As in the first case, thedefinite source of this infection could not bedetermined. Two other cases involved immigrantsfrom endemic regions who had, presumably, acquiredinfections there. One patient had immigrated toCanada from Malaysis a year before hospitalization.The other patient was a Filipino woman who hadimmigrated to the United States, and eventually toCanada, a few years before hospitalization. Whilestudying these cases, Beland et al (1969) examinedseveral snails from the St Lawrence River in Quebec.A large number of sporocysts were observed in thetissues of a number of these snails. As a result ofthese findings, and some earlier studies reportingParagonimus metacercariae in crayfish from Michi-gan, these authors concluded that there was apossibility of further domestic cases occurring inNorth America. In the United States, Johnson et al(1982) described several cases of paragonimiasisamong Laotian refugees in Minnesota. Pachucki et al(1984) reported on an infection of Paragonimus inan American man who had no history of travel outsidethe United States. This individual was apparentlyinfected after eating raw crayfish in Missouri. Thisinfection was described as American paragonimiasisand appeared to be caused by a species other thanP. westermani, which is common in Asia.

3. Intestinal flukes

Echinostoma spp

At least 16 species of echinostomes have beenreported in human infections (Cayney, 1991). The mostcommon species reported in Southeast Asia includeE. malayanum and E. ilocanum (Waikagul, 1991).

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Infections with E. hortense and E. cinetorchis have beenreported in Korea and Japan (Chai and Lee, 1991).Human infections occur in Asia, North Africa, andin the Americas (WHO, 1993a). Although they areconsidered rare, several cases of infection withEchinostoma spp have been diagnosed in Canada atthe Toronto Public Health Laboratory (Scholten andYang, 1975). One other case was reported in a 6 yearsold boy in the province of Alberta (Eaton, 1972). Anoutbreak of gastroenteritis occurred among a group ofAmerican tourists returning from a trip to Kenya andTanzania in 1983 (Poland et ai, 1985). A diagnosis ofechinostomiasis was based on the presence ofechinostome-Iike eggs in stools.

Metagonimus spp

Metagonimus yokogawai is the most commonspecies of intestinal trematode reported in Korea(Chung and Sho 1991; Chai and Lee, 1991). Endemicfoci include streams in coastal areas of Korea wheresweetfish are found. In Canada, Beare (1978) reportedtwo cases of infection with M. yokogawai out of 144overseas immigrants to the province of Alberta. Gold-smith (1978) reported a case of metagonimiasis in awoman from California who first developed symptomsduring travel in Southeast Asia. This patient enduredrecurrent diarrhea for one and a half years before adiagnosis was made. As she had been careful to avoideating raw fish during her travels, the source ofher infection was not clear, although salad contami-nated with metacercariae from a cutting surface wassuggested.

Heterophyes spp

Human infections occur in Asia, North Africa, andin the Americas (WHO, 1993a). H. heterophyes isprevalent in Egypt and the Middle East, while H. nocenshas been reported in Korea and Japan (Chai and Lee,1991). Very few cases have been reported in Canada.SekIe et al (1978) reported one case of infection withHeterophyes sp. out of 140 recent immigrants toManitoba. Similarly, Beare (1978) found two casesof infection with H. heterophyes out of 144 overseasimmigrants to the province of Alberta. A single casewas reported in the United States (Adams et al. 1986).While this individual had never travelled outsideof the continental United States, she had apparentlybecome infected while eating sushi at a local Japaneserestaurant which served a variety of freshwater andsaltwater fishes flown in from the Orient.

Nanophyetus salmincola

Nanophyetus salmincola occur as adults in the gut

of humans and other fish-eating mammals and birds.In dogs the parasites themselves rarely cause clinicaldisease but may act as vectors of an often fatal rickett-sial disease. Cercariae are shed from snails andpenetrate the skin of the second intermediate hosts,which include freshwater fishes such as salmon or trout.The flesh and viscera of these fishes may becomeheavily infected with metacercariae. Human infectionswith N. salmineola have been reported for manyyears in parts of the former Soviet Union, and morerecently in the northwestern United States. Eastburnet al (1987) reported 10 cases of infection in the stateof Oregon in which eggs typical for N. salmineolawere recovered from stool specimens. Eight of theten patients had a history of consumption of raw,incompletely cooked, or smoke salmon, steelheadtrout, or steelhead eggs. The adult flukes recoveredfrom a treated patient were subsequently identifiedas N. salmineo/a. Deardorff and Kent (1989) indicatedthat within one year of the original report, the numberof human cases in the United States had increasedto greater than 20.

EPIDEMIOLOGY AND CONTROL

While the majority of infections with fish-andshellfish-borne trematode occur in Southeast Asia,other endemic regions exist in the former Soviet Union,South America and Africa. A variety of conditions haveallowed these infections to become established inthese areas. Many of these endemic regions are im-poverished and have poor sanitation systems, leadingto the fecal contamination of natural water sourcesused for fishing. Aquacultural fish ponds, which areanother very important source of freshwater fish andshellfish in many of these regions, may also becomecontaminated by means of poor sanitation, or throughthe intentional use of night soil. In many endemiccountries, this use of excreta from domestic animalsand from humans is becoming increasingly importantfor the fertilization of ponds used in aquaculture(Naegel, 1990). It provides an inexpensive source ofnutrients to promote zoo- and phytoplankton growth,and a direct feed for some fish species. However, italso represents an important source of pathogens whichcan be transmitted via aquatic organisms to humans.In China for example, Ling et at ( 1993) reported thatup to 10,000 parasite eggs per I()() ml of pond waterand sludge were found where ponds had been fertil-ized with raw night soil. Further fecal contaminationof surface waters may result from the proximity of wildand domestic animals which serve as reservoir hosts.Each of these sources of fecal contamination can

contribute to the prevalence of metacercariae in theflesh and viscera of freshwater fish and shellfish.Improved sanitation and a reduction in the use ofnight soil in aquaculture will be important factors inany effective control strategies.

Traditional methods of food preparation involv-ing raw or lightly cooked fish or shellfish are directlyresponsible for the transmission of viable metacercariaeto humans. Prevention of infection may best be accom-plished by informing consumers and food handlers ofthe hazards involved in eating raw and lightly cookedfoods and of the methods which should be adopted toreduce the risk of infection. For example, temperatureare very effective in destroying parasites in fish andshellfish. Cooking, roasting, grilling, frying, etc are alleffective in killing metacercariae if the flesh becomeswhite or pale in color and assumes a firm texture(Abdussalam et al , 1995). When cooking is notdesired, through freezing can also be effective. Othermethods of processing fish and shellfish such as salt-ing, drying, smoking, fermenting and marinating arecommon in endemic regions but are unreliable in thedestruction of metacercariae. Long-standing traditionsof food preparations are, however, very difficult tobreak and ongoing public health education programswill be required.

While improved sanitation and public health edu-cation are very important they can only be consideredlong term measures. Loaharanu and Sommani (1991)concluded that, at present, screening and mass treat-ment is the only feasible control measure in endemicregions. Currently, praziquantel is the drug of choiceand has been used successfully on most trematodes(Eastbum et al, 1987; WHO, 1993a). Treatment is,however, often complicated by misdiagnosis due to theambiguity of symptoms. For example, paragonimiasisis often misdiagnosed as tuberculosis, epilepsy ormeningitis (Maurice, 1994).

Some endemic countries have already establishedmodels for the control of food-borne trematodes.through identification of infected people, treatmentwith praziquantel, health education, and legislationregarding food safety and the sanitary disposal of sew-age (Lima dos Santos, 1995; WHO, 1995). These con-trol programs have proven to be very effective in re-ducing the prevalence of food-borne trematode infec-tions. As a result, the World Health Organization hascalled for collaboration among various sectors, includ-ing public health, agriculture, fisheries, food industry,food safety, and education, in an effort to reduce thesuffering and expense imposed by these infections(WHO, 1995). The concept of Hazard Analysis and

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Critical Control Point (HACCP) is presently beingevaluated with respect to its feasibility and efficiencyin the prevention and control of food-borne trematodeinfections (Rim et al, 1994; Lima dos Santos, 1995).

Incorporation of HACCP-based control measuresin aquaculture could significantly reduce the risk ofhuman infection by focusing on a variety of criticalcontrol points throughout the production and process-ing of fish and shellfish.

In non-endemic countries such as Canada, theprevalence of food-borne trematode infections remainsrelatively low and. while there is some indication thatsuitable intermediate hosts may be available, it dosenot appear likely that these parasites could become wellestablished. This is due primaily to the efficientsanitation systems, the use of commercial feed ratherthan night soil in aquaculture, and. particularly. thecommon practice of cooking fish and shellfish beforeconsumption. Further, a consumer recommendationby Fisheries and Oceans Canada states that any fishto consumed raw should be prepared from frozenproduct. Nevertheless, the importation of freshwaterfish and shellfish from endemic regions, the interest inethnic dishes, and increasing immigration and travelhave all contributed to the risk of infection in Canada.

While much of the fish and shellfish imported intoCanada from South est Asia is frozen or canned, therebykilling any metacercariae present, there is a dangerthat producers in endemic regions wishing to gain acompetitive edge could begin shipping fresh, unfro-zen fish by air (Maurice, 1994). In fact, betweenApril I, 1994 and March 31, 1995, over 1,700 kg offreshwater fish were imported into Canada as "fresh"product from various countries in Southeast Asia. Theseimports included some fishes, such as carp. mullet,and goby, which are common intermediate hosts fortrematodes. During this same period. over 40,000 kgof freshwater fish was imported as "other" (cooked.cured. dried, salted. pickled, smoked, spiced, tlavored,etc) and over 400 kg was imported as "semi-preserved"(brine, vinegar. sugar. spices, etc). Depending upon thetreatment, some of these products could also containviable metacercariae. Therefore, as the current inspec-tion procedures for imported freshwater fish intoCanada may not detect the presence of all parasites.there may be some risk of infection from theseproducts if they are consumed raw or lightly cooked.In addition to fish, there is also some importation offreshwater crustaceans (crabs, crayfish) into Canadafrom endemic regions. In an effort to reduce thelikelihood of human infection with Paragonimuswestermani, all imports of live freshwater crabs of

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the genus Eriocheir are prohibited under the CanadianFish Inspection Regulations.

In Canada, and other non-endemic countries, thereis an increasing availability and interest in ethnic andtraditional foods. Whether these foods are eaten athome or in ethnic restaurants, they may represent arisk to consumers if they are prepared using raw orlightly cooked freshwater fish or shellfish importedfrom endemic regions. In addition to these importedproducts. a number oftrematodes including Metorchisconjunctus, Nanophyetus salmincola, and Paragoni-mus spp are found in freshwater fishes and shellfishin North America and have also been responsiblefor human infections following the consumption oftraditional or ethnic dishes.

The incidence of food-borne trematode infectionsin immigrants and refugees from Southest Asia isrelatively high and probably accounts for the majorityof infections in Canada. While many of these infec-tions originated before arriving. some may havedeveloped in Canada. International trevel is alsopartially responsible for the increased prevalenceof food-borne trematode infections in developedcountries. The number of tourists to Southeast Asia isincreasing rapidly and there is a risk of infection tothose individuals who partake in traditional or ethnicfoods during their travels.

CONCLUSIONS

Despite the high cost and prevalence of infectionin some areas of the world. the public health signifi-cance of food-borne trematode infections is poorlyrecognized, and dissemination of information andcontinued discussion will be necessary for the devel-opment of effective control strategies. Control offood-borne trematodes in endemic regions willinvol ve screening the population and treatinginfected individuals. as well as the long-term measuresof public health education, and legislation regardingfood safety and sanitation.

A significant quantity of freshwater fish andshellfish is being imported into Canada from endemicregions and the consumption of these products in araw or lightly cooked form represents a moderatehealth risk. While general cooking habits as well aseffective sanitation and water treatment systems willprobably prevent the establishment of these fish andshellfish-borne trematode in Canada, factors suchas immigration, international travel, and the increas-ing interest in ethnic foods, contribute to the risk ofinfection. In addition to these imported trematodes, a

number of species are found in freshwater fishes andshellfish in North America and have also causedillness in humans. Although the prevalence ofinfection remains relatively low in Canada, the needfor an increased general awareness of food-bornetrematode infections and their causes is indicated.

ACKNOWLEDGEMENTS

We wish to thank Dr Theresa Gyorkos, Divisionof Clinical Epidemiology, Montreal General Hospital,for information on cases of food-borne trematode in-fections in Canada.

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