CHAPTER 9

Microbiological Hazards and Their Control: Parasites

Mike Taylor

INTRODUCTION immigration, tourism, and desire to experience the culinary dishes of other cultures may in- Many types of parasites are food-borne, and crease the incidence of in other can become infected following the in- countries. As with some helminths, protozoan gestion of infected or contaminated meat, , parasites are opportunistic infections that are of- molluscs, vegetables, or fruit, or products de- ten acquired as the result of poor hygiene or rived from these foods. In most cases, parasitic travel to foreign countries. infections are acquired by eating raw or incom- Fermented foods that use raw ingredients that pletely cooked food, or food that is partially have been contaminated or infected with infective pickled or smoked or poorly preserved. Most, if or intermediate parasite stages have the potential not all, infections are preventable if the food is to cause infection. Although food-borne prepared sufficiently to destroy the infective parasitic diseases continue to be reported globally, stages of the parasite. However, many infections reports of human infection following the ingestion are commonly associated with cultural and eat- of fermented food are sparse. Cultural dishes such ing habits that have been in practice in popula- as som fak (a fermented Thai minced fish dish) tions for generations. have been reported to result in human infection Meat from many species of has been with the helminth parasite, (see a recognized source of many helminth, and some Gnathostomosis). Infection with another proto- protozoal, infections, in man. In developed zoan parasite, Giardia, has been reported follow- countries, the introduction of meat hygiene mea- ing the ingestion of cheese dip. Fermentation sures has resulted in reduced incidences of many alone may therefore be insufficient to prevent the of the traditionally recognized helminth infec- transmission of many food-borne parasites, and tions. However, the eating of many traditional potentially infected material should be avoided raw or lightly cooked meat dishes continues, and wherever possible, or alternatively subjected to may occasionally result in infection in man. freezing or some form of heat treatment. Raw, uncooked fish dishes are also commonly Many parasites infect humans, but reference eaten in many cultures, and snails, clams, oys- is made only to those helminths and protozoa ters, and a variety of other molluscs are part of that are recognized as food-borne and a potential the diets of many people worldwide. Although source of infection in fermented foods. most food-borne helminth infections are re- ported from Third World countries, increased Source: © Crown copyright 1997. Published with the permission of the Controller of Her Britannic The nematodes are a diverse group of para- Majesty's Stationery Office. The views expressed are sitic or free-living unsegmented worms that are those of the author and do not necessarily reflect those usually cylindrical and elongate in shape. With of Her Britannic Majesty's Stationery Office or the few exceptions, the sexes of nematodes are sepa- VLA or any other government department. rate, and the life cycle may be direct or indirect, involving an intermediate . The general de- Most human infections and deaths associated scription and classification of the food-borne with A. cantonensis have been reported from nematodes discussed in this chapter are summa- Taiwan, Thailand,131'176 and some Pacific is- rized in Table 9-1. lands, but human infections have been reported in most countries where the parasite occurs and 33 Angiostrongylosis appears to be spreading. The incidence of angiostrongylosis appears to be spreading, espe- Angiostrongylus cantonensis and A. costari- cially in those areas in which snails are an im- censis are parasites of rodents (predominantly portant part of the diet. rats) that can cause disease in humans through the ingestion of infected snails. Two other species, A. Epidemiology and Transmission malaysiensis and A. mackerrasse, occur but have Humans become infected with angiostrongyl- not been associated with human infection. Most osis by intentionally or accidentally eating in- human infections are acquired by eating infected fected snails or slugs. Rodents are infected by in- snails, but can occur through eating infected gesting infected molluscs or by ingesting infective shrimp and crab, or snail- or slug-contaminated larvae present in "slime" on plants. In most en- raw vegetables. demic areas of , both land and aquatic snails (Achatina and PiId) are eaten regularly. The giant Public Health Significance African land snail, Achatina fulica, is a particular A. cantonensis can cause and menin- delicacy in many countries and is a good interme- goencephalitis with mild to moderate symptoms, diate host. Slugs and snails (which are used for often of sudden onset, with intense headaches; medicinal purposes in some cultures), land crabs, vomiting; moderate intermittent fever; and, in ap- shrimp, and paratenic hosts such as toads and proximately 50% of cases, coughing, anorexia, have also transmitted infection. Sauces pre- malaise, constipation, and somnolence.176 In se- pared from shrimp juices or unwashed contami- vere cases, coma and death may occur. Accidental nated vegetables have also been incriminated. The ingestion of the slug intermediate host of A. drinking of untreated water containing larvae re- costaricensis causes abdominal angiostrongylosis leased from dead snails has also been suggested as with symptoms similar to appendicitis, including a means of infection. Infection continues to be re- fever, abdominal pain, anorexia, diarrhea, and ported from new areas of the world, in part due to vomiting.96 Migratory larvae may cause gastroen- the dissemination of the intermediate snail hosts, teritis, tumor-like masses or abcessation of the in- but also due to transportation of infected rats on testines, liver enlargement, nervous signs, coma, ships. Most terrestrial and aquatic snails are sus- and, occasionally, death.108 Infection is normally ceptible to infection, and populations can be diagnosed by confirming the presence of parasites readily infected from carrier rats. or eggs in surgically removed tissues or fluids or by using serological assays.37'144'169 Prevention and Control Angiostrongyliosis can be prevented by edu- Life Cycle cating people in endemic areas to avoid eating Adult worms are found in the pulmonary ar- uncooked molluscs, particularly land snails. teries of rats. The life cycles of A. cantonensis Freezing will kill larvae present in snails if they and A. costaricensis are similar and are shown in are frozen at -15 0C for 12-24 hours. Paratenic Figure 9-1 . The prepatent period (from infection hosts (i.e., shrimp, prawn, crabs) should be to maturity) is 42—45 days. cooked before eating, and vegetables should be washed before eating raw. Little or no informa- Distribution tion is available on the survivability of infective The distributions of A. cantonensis and A. larvae in fermented foods such as balao-balao costaricensis are summarized in Table 9-2. (fermented shrimp). Table 9-1 Food-Borne Helminths— Classification

Phylum Class Order Family Genus Nemathelminthes Nematoda (Roundworms) Metastrongyloidae Angiostrongylus Elongate, cylindrical, unsegmented worms with fluid-filled body cavity. Sexes are separate. Anisakidae Life cycle direct or indirect. Enophida Trichinellidae Trichinella Capillaridae Capillaria Dioctophymida Dioctophymatidae Dioctophyma Thelaziidae Gnathostoma Platyhelminthes (Tapeworms) Diphyllobothridae Tape-like segmented body comprising head, neck, and strobila (proglottids). Bothria or suckers for attachment. Hermaphroditic. Indirect life cycles. Taeniidae Taenia

Trematoda (Flukes) Echinostomida Fasciolidae Fasciola Unsegmented leaf or lancet-shaped worms with two muscular suckers for attachment and well- Echinostomatidae Echinostoma developed oral sucker and pharynx. Hypoderaeum Hermaphroditic (generally). Indirect life cycles. Plagiorchiida Troglotrematidae Paragonimus Nanophyetes Opisthorchiidae Heterophyidae Heterophyes Metagonimus Opisthorciidae Opisthorcis (Clonorchis) Source: ©Crown Copyright. First-stage larvae Ingested by rat excreted in feces

Angiostrongylus cantonensis

Second- and third-stage larvae in Carriers intermediate host (slug, snail) (crabs, prawns)

Human infection through ingestion of raw or undercooked intermediate host (snails) or carriers (crabs, prawns, etc.)

Figure 9-1 Life cycle of Angiostrongylus cantonensis. Source: © Crown Copyright.

Anisakiosis worms are common parasites of marine mam- mals (Table 9-2), and the larval stages are found Anisakiosis is a parasitic gastrointestinal dis- in marine fish and squid. Humans acquire infec- ease of man that is caused by the larval stages of tions by eating the raw or improperly cooked or nematodes of the family Anisakidae. The adult preserved meat of these animals. There are many Table 9-2 Food-Borne Helminths (Nematodes, Cestodes)

Parasite Class Parasite Distribution Main Hosts (final) Source of Infection to Man Nematoda Angiostrongylus Asia and Pacific Islands, Australia, India, Rodents (rats) Molluscs (snails), shrimps, (Roundworms) Africa, Caribbean, parts of United crabs, amphibians, States contaminated vegetables and salads Anisakis simplex North and , Pacific Islands, Pinipeds (whales, dolphins, Fish Anisakis decipens parts of northern Europe porpoises) Seals, sealions, walruses Capillaria phillipinensis Phillipines, Thailand Man (several species of Fish ) Dioctophyma renale Worldwide (North and South America, Carnivores (mink, ferret, Fish southern Europe, Asia, Middle East) , , jackals), man Thailand, Japan, southeast Asia, , Carnivores (dogs and Fish , frogs, chickens, Mexico (Middle East, Africa, Baltic cats), man ducks, States, Russia) , man United States, former USSR, parts of Ruminants, pigs, dogs, Salads (insects) Europe, Middle East, China, North cats, horses, rodents, Africa, New Zealand primates, man Worldwide (except Antartica) Pigs, rodents, carnivores Meat (mink, fox, badger, bears, walrus, seals), man

Cestoda Diphyllobothrium latum Northern Hemisphere (northern Europe, , fox, mink, , , Fish (Tapeworms) Russia, North America, South America, bear, seals Asia, Africa) Central Africa, Asia, South and West Man Meat (beef) (Cysticercus bovis) Africa, parts of Europe, southeast Asia, Central and South America; also reported in United States, Canada, Australia and Pacific Islands Central and South America, central and Man Meat (pork) (Cysticercus east Africa, southeast Asia, southern cellulosae) Europe Source: © Crown Copyright. species of anisakid nematodes, but those most Humans acquire A. simplex by eating raw or often associated with human illness are Anisakis poorly salted, pickled, or smoked herring, cod, simplex, Pseudoterranova decipiens, Phoca- mackerel, salmon, or squid, and P. decipiens nema, and Contracaecum spp. from cod, halibut, flatfish, and red snapper. Such traditional preparations as green herring, Public Health Significance lomi lomi salmon, seviche, sushi, and sashimi Anisakis causes acute or chronic gastrointesti- (i.e., seasoned fish fillets), all of which use raw nal disease in man. Migrating larvae cause a for- or uncooked fish, are major sources of infec- eign-body reaction and eventually necrosis and tions.34 In the Netherlands, the occurrence of the hemorrhage of the stomach, occasionally creat- disease was due to the habit of consuming raw ing tunnels and burrows in the stomach mu- or lightly salted herring (green herring).162 Al- cosa,139 causing pain, nausea, and vomiting. The though the habit persists, the incidence of hu- acute symptoms subside in a few days, but a man anisakiosis has been drastically reduced by vague abdominal pain with intermittent nausea freezing fish before marketing. In recent years, and vomiting persists for weeks, with symptoms the highest incidence of the disease has been re- resembling those of a peptic ulcer. The condition corded in Japan, where many fish dishes are is often misdiagnosed because of its similarity to eaten raw (sashimi); pickled in vinegar other acute gastrointestinal conditions (e.g., gas- (sunomono)\ or fermented in rice, rice bran, or tric ulcers or neoplasm, appendicitis, diverticuli- koji (sushi and zuke). In the United States, at tis, Crohn's disease, gallstones, etc.). Diagnosis least two cases have been linked to eating is normally only made following biopsy and seviche (i.e., pieces of raw fish seasoned in confirmed on histopathology. lemon juice for several hours), and others to eat- ing Japanese raw fish dishes. Life Cycle Adult anisakid worms are located in the Prevention and Control stomach of marine cetaceans and pinnipeds but The risk of human infection with anisakiosis do not develop in humans. The life cycle of increases in countries where fish are eaten these worms is shown in Figure 9-2. Humans raw.172 Anisakiosis is preventable by ensuring become infected if an intermediate fish host that only well-cooked marine fish, octopus, and containing infective third-stage larvae is eaten squid are eaten. Larvae are killed by cooking at uncooked. 60 0C or above. Freezing fish at -20 0C for 24 hours will kill the larvae, with the exception of Distribution some North American species that can survive Fish infections are found in most oceans and freezing at that temperature for 52 hours. Clean- seas but are highest in areas in which there are ing and eviscerating fish immediately after they high marine mammal populations, such as are caught prevents larvae migrating from the coastal Japan and Alaska. Many species of fish intestine to the muscles. Salt curing, marinating, are naturally infected with anisakiosis, and the microwaving, and smoking temperatures are in- prevalence of infection can be very high. In sufficient to kill the parasite.34 Marination of Japanese waters, 123 species of marine fish have herring has been a long tradition in parts of been found to harbor the parasite.118 The global northern Europe,85'106 involving the preservation distribution of anisakiosis is summarized in of herring fillets in salt and acetic acid. The salt/ Table 9-2. The highest levels of infection have acetic acid marination process produces the typi- been reported from Japan and the Netherlands.88 cal flavor as a result of denaturing of the fish proteins, lowering of the pH, and addition of Epidemiology and Transmission sugar and spices.158 The salt/acid treatment may The main source of infection from anisakid take up to 42 days to kill Anisakis larvae, and at worms for man is marine fish, many species of low concentrations may not kill larvae at all.85 which are highly parasitized by anisakid larvae. Larvae have also been shown to survive in izushi Eggs in feces

Anisakis simplex First- or second-stage larvae ingested by

Infective larvae in fish

Human infection through ingestion of raw, undercooked, or poorly preserved fish

Figure 9-2 Life cycle of Anisakis simplex. Source: © Crown Copyright.

(i.e., pickled rice with cod roe, fillets of salmon, other countries.32'34'93 Man is the main definitive and cod) and in sashimi.118 host for the parasite, but several species of birds are now believed to be a natural host and are able 35 Capillariosis to transmit the infection. Intestinal capillariosis is caused by a tiny Public Health Significance , Capillaria philippinensis. The dis- Infections with C. philippinensis can cause di- ease was first recognized in the Philippines in arrhea, anorexia, weight loss, and, if left un- the 1960s and has subsequently been reported in treated, death. The parasites cause damage to the mucosa of the small intestine, leading to fluid, whether they are known to survive in fermented protein, and electrolyte loss. Clinical symptoms fish products. include abdominal pain and diarrhea. If treat- ment is not initiated rapidly, patients die because Dioctophymosis of the irreversible effects of the electrolyte loss, Dioctophyma (Dioctophyme) renale is a large heart failure, or septicemia. In endemic areas, a di- kidney-dwelling nematode of carnivores. Infec- agnosis can be made on patients based on clinical tion is acquired by ingesting raw or undercooked signs. In chronic infections, there is weight loss, fish or frogs. It has only rarely been reported in wasting, and intractable diarrhea. Infection is con- man. firmed by identifying eggs, larvae, and adults mi- croscopically in the feces. Serological tests are not Public Health Significance sufficiently specific for routine use. Infection in man can cause renal damage and associated symptoms of renal colic, hematuria, Life Cycle or urinary obstruction. In humans and dogs, Dio- C. philippinensis is a small nematode that is ctophyma usually locates in only one kidney, found in the small intestines of man. Further de- most often the right one, and in most cases only velopment occurs in fish. A number of species of one parasite is found, causing little or no clinical freshwater fish are suspected to serve as inter- symptoms. Infection is diagnosed by the pres- mediate hosts for the parasite. The fish are usu- ence of the characteristic thick, bipolar eggs in ally small and are eaten whole in the Philippines urine (only if female worms are present). and Thailand, leading to human infection. Life Cycle Distribution D. renale is a large, blood-red nematode that is The distribution of intestinal capillariosis is found in the kidneys of carnivores (Table 9-2). summarized in Table 9-2. Nearly 2,000 cases of The size of the parasite depends on the size of the capillariosis have been recorded in the Philip- host species; in dogs, the adult female of the para- pines, with more than 100 deaths. In Thailand, site can reach up to 1 m in length. The intermediate there have been only a few hundred cases, with host is a free-living, aquatic segmented worm (oli- an unknown number of deaths recorded.36 gochaete) in which further development to an in- fective occurs. Transmission to a final host Epidemiology and Transmission occurs following ingestion of the annelid interme- Sanitation facilities are poor in many rural ar- diate host, or more usually following ingestion of a eas of southeast Asia and defecation in the fields fish or a , which act as transport hosts. The is a common practice. During the monsoon prepatent period is from 3]/2 to 6 months. rains, the feces are broken down and washed away to streams and ponds, resulting in infection Distribution of freshwater fish. These and many other foods D. renale is found on all continents with the are eaten uncooked, especially in the endemic possible exception of Africa and Oceania (Table areas of the Philippines and in Thailand. 9-2). The most frequently reported form of in- fection is canine dioctophymosis, with the high- Prevention and Control est prevalence of infection in Canadian wild Educating both the local population and visi- mink (Mustela vison), where 18% of the animals tors of the dangers of eating uncooked freshwa- are infected. The disease is very rare in man, ter fish can help prevent intestinal capillariosis. with only a few reports worldwide. Improvement of sanitation and the control of in- discriminate disposal of feces would also be Epidemiology and Transmission beneficial. No information is available on the In North America, mustelids, especially mink, conditions that kill the parasite in fish and appear to be the main reservoir. In other areas, it is likely that other species of mustelids or wild based on history, symptoms, or serology and can canids serve as main definitive hosts. These be confirmed following the recovery and identi- hosts are infected by ingesting frogs or fish fication of parasitic larvae.114 (paratenic hosts) and aquatic oligochaetes (inter- mediate hosts) that contain the third-stage lar- Life Cycle vae. Dogs and humans are accidental hosts and Adult worms of G. spinigerum are found in are infected by ingesting raw fish and frogs, and tumor-like masses in the stomach wall of fish- almost always harbor only one parasite. The rar- eating mammals. The life cycle of G. spinigerum ity of human infection can be explained by the is shown in Figure 9-3. The prepatent period is fact that larvae are located in the mesentery and approximately six months. liver of fish and frogs, which generally are not eaten by man. Distribution The distribution of human gnathostomiosis is Prevention and Control summarized in Table 9-2. Infection can be prevented, both in humans and dogs, by avoiding the consumption of raw or Epidemiology and Transmission undercooked fish and frogs. It is not known what The main source of human infection of conditions result in larval death. gnathostomosis in Thailand is the -headed fish, Ophicephalus spp., which is one of the Gnathostomosis used in som-fak, a rice-fermented fish dish with widespread popularity. In Japan, freshwa- Gnathostomosis is caused by infection with ter Ophicephalus species are eaten raw as the larval or immature adult stages of nematodes sashimi. The ingestion of raw or inadequately of the genus Gnathostoma. Adult parasites are cooked fish is the major source of infection in reported in dogs, cats, and other carnivorous ani- other areas reporting the disease. Infections in mals worldwide. In Thailand, more than 40 spe- Mexico are attributed to eating raw cycloid fish as cies of have been reported to be natu- ceviche." Human infections are also reported rally infected. These include freshwater fish, from eating raw or poorly cooked catfish, eels, frogs, snakes, chickens, ducks and other birds, frogs, chickens, ducks, and snakes.39 Dogs, cats, rats, mongooses, and tree shrews.38 Four species, and several species of wild mammals are reser- G. spinigerum and G. hispidum, and more re- voirs of the parasite. These definitive hosts be- cently, G. doloresi and G. nipponicum, have come infected primarily through eating infected been reported in humans in Japan.111'152 fish or other animals that serve as paratenic hosts. Public Health Significance Prevention and Control Man is an abnormal host, with infection re- Health education programs in endemic areas sulting in a larval migrans causing red, itchy, of Asia are required to control this type of infec- and edematous subcutaneous swellings that usu- tion. Ensuring that people eat only well-cooked ally last approximately one week but can recur fish, eels, or other intermediate hosts such as weeks or months later. More rarely, the parasite snakes, frogs, and poultry can prevent infec- may enter the eye, causing subconjunctival tions. Potentially -infested water should edema, exopthalmus, impaired vision or blind- be boiled or treated. ness through hemorrhage, and retinal damage. Invasion of the central nervous system (CNS) Gongylonemosis can produce headaches, neck stiffness, drowsi- ness, or coma and death. Brain hemorrhage and Gongylonema pulchrum is a spiruroid nema- transitory obstructive hydrocephalus have also tode of the Thelaziidae family (Table 9-1). It is been reported.140 Diagnosis in endemic areas is found in all domesticated mammals, but is most Adults worms in stomach

Eggs passed in feces Hatched larvae ingested by

Final Host (fish-eating mammals)

Gnathostoma spinigerum

Cyclops, crustacean intermediate host

Encysted larvae in fish, amphibians, or reptiles

Human infection through ingestion of raw or undercooked fish

Figure 9-3 Life cycle of Gnathostoma spinigerum, Source: © Crown Copyright.

prevalent in ruminants (Table 9-2). Cases of hu- palate, soft palate, and tonsils, with pharyngitis man infection are rare. and stomatitis reported. Diagnosis is based on history, clinical signs of mouth irritation, and Public Health Significance microscopic identification of the parasite. Occa- In humans, gongylonemosis parasites have sionally, the parasite has been found emerging been found in the submucosa of lips, gums, hard from the mouth. Infection in animals is usually asymptomatic, but may sometimes cause lesions populations of the parasite are the same, and five of the mouth or pharynx.29 In pigs, the parasite is species have recently been proposed.24 T. found in the tongue mucosa and may cause oc- spiralis is the most important species, with clusion of the esophagus.179 widespread distribution in domestic pigs. Life Cycle Public Health Significance Adult Gongylonemosis worms live in the Trichinellosis is a cosmopolitan zoonotic, mouth, esophagus, or rumen of the final hosts. The food-borne, parasitic disease resulting from the life cycle of G. pulchrum involves coprophagic ingestion of meat harboring the infective larvae beetles of the genera Aphodius, Ontophagus, and of Trichinella. Intestinal trichinellosis is usually Blaps as intermediate hosts. Ruminants become mild and therefore not often diagnosed, but may infected by ingestion of the beetles with grass or cause diarrhea and abdominal discomfort, some- other infested food. times accompanied by nausea and vomiting, leavy infections can be severe, causing ex- Distribution tremely painful muscles, and even fatalities in Although G. pulchrum is widely distributed man. The illness typically begins one to four geographically, human infection is rare. The dis- weeks after ingestion of infective meat, and is tribution of G. pulchrum is summarized in Table characterized by muscle aches and fever. Muscle 9-2. Infection in domestic ruminants varies con- pain, which may be severe and incapacitating, is siderably, with high levels of infection reported an outstanding feature, with the jaw muscles fre- in the Ukraine (e.g., 32-94% of adult cattle, 39- quently involved. The infection of heart muscle 95% of sheep, and 0-37% of pigs infected),29 may induce severe, even fatal, myocarditis. and Iran (e.g., 49.7% of the cattle).4 In the Death may also result from encephalitis or pneu- United States, the parasite was found in 5.9% of monitis. In most parts of the world, the probabil- pigs, varying from O to 21% according to geo- ity of contracting the disease is now low, and its graphic origin.179 decline, certainly throughout the western world, can be attributed to the introduction of a number Epidemiology and Transmission of control measures discussed later. Diagnosis Man is an accidental host and is probably in- may be based on a clinical history of prior con- fected by ingesting beetles on salads and raw sumption of raw or undercooked meat, but this vegetables. aspect may be missed, particularly in countries where the disease rarely occurs. Clinical signs of Prevention and Control muscle aches, fever, and periorbital edema are Because the Gongylonemosis parasite is rare indicative of the disease. Infection is usually di- in humans and causes only mild symptoms, spe- agnosed by demonstrating larvae in muscle bi- cial control measures are usually not recom- opsy specimens. mended. Individual protection can be obtained by observing the rules of personal, food, and en- Life Cycle vironmental hygiene. T. spiralis is a small, nematode parasite that is found in the small intestine of man, pig, rat, and Trichinellosis () other mammals (Table 9-2). The life cycle of T. spiralis is shown in Figure 9-4. Encysted larvae Trichinellosis (trichinosis) is a food-borne remain infective for months, even years. In some disease that is caused by infection with parasitic hosts, especially man, they eventually die and nematodes of the genus, Trichinella. Infection become calcified. Trichinella is remarkable results from ingesting meat harboring infective among parasitic nematodes in having neither a larvae. Until recently, T. spiralis was accepted free-living stage between individual hosts nor an as the sole representative of the genus Tri- intermediate host. The spread of larvae through- chinella. It has now become clear that not all out the host musculature permits transmission to luman infection via raw or Human infection Jiercooked pork, sausages, etc. from game meat

Domestic cycle

Pig-to-pig transmission via cannibalism, tail-biting, etc.

Rats infected from Infection via dead pork scraps infected rats

Trichinella spiralis

Wildlife infection from carrion feeding

Game meat Sylvatic cycle

Figure 9-4 Life cycle of Trichinella spiralis. Source: © Crown Copyright. another individual host, but only after the death eas, its prevalence in man and pigs has been re- of the first host. duced to a low level, but persists at higher levels in wildlife. Prevalence rates are higher in large Distribution carnivorous or scavenging species such as bears, Trichinella has been recorded on every conti- mink, fox, badger, wild boar, and rodents. Infor- nent except Antarctica (Table 9-2). In many ar- mation on the global incidence of clinical trichinellosis in man is not readily available, but to pigs. In some countries, laws requiring waste it is evident that there has been a striking reduc- food (swill) to be cooked before being fed to tion in western Europe and the United States. pigs have been introduced to help control a num- Several outbreaks in France and Italy have been ber of important viral pig diseases. Good hus- associated with eating horse meat that was bandry and rat-proofing piggeries also help con- thought to have become infected by intention- trol infection. In many countries, meat ally or inadvertently eating fodder that was con- inspection procedures have been introduced to taminated with the bodies of dead rats or mice. identify infection. Outbreaks of varying severity continue to occur Ethnic or cultural practices in which meat is in eastern Europe, the former Soviet Union, eaten undercooked or raw are a particular risk Asia, and occasionally elsewhere. area and may call for special educational mea- sures. Traditional types of sausage (including Epidemiology and Transmission fermentated sausage) that receive little cooking have long been associated with human disease. Two distinctive epidemiological cycles of T. Education draws attention to the need to freeze spiralis are recognized, domestic and sylvatic. or cook such foodstuffs. Freezing may be more The domestic cycle involves pigs and rats, acceptable because it has less effect on flavor through either the feeding of uncooked pork and taste than cooking. To be effective, meat scraps (e.g., in waste feed) to pigs, cannibalism must be frozen throughout and stored for suffi- among pigs (e.g., scavenging of dead carcasses cient time to ensure death of encysted larvae. and possibly tail biting of live pigs), or infection The thermal death point of T. spiralis is approxi- of rats by disposal of uncooked pork and the sub- mately 57 0C, and cooking pork so that it reaches sequent infection of pigs by the ingestion of in- a temperature of 77 0C gives a margin of safety fected rats. Human infection occurs when without destroying the taste of the meat. Slightly undercooked or raw pig meat is eaten. lower temperatures may be adequate provided In the sylvatic cycle, Trichinella is transmit- the temperature is achieved uniformly through- ted among species of wildlife. Man becomes in- out the meat. It can be assumed that pork will be fected by consuming game meat. The two cycles safe if it is cooked until there is no red or pink col- may be interrelated by the fact that domestic oration throughout. In the United States, fer- pigs may scavenge on dead wild animals and mented pork sausages must either originate from vice versa. Rats can also be of significance in Trichinella-CQrtified meat or be heated to 58.3 0C this respect in that they may become infected ei- at the end of the fermentation process.89 Although ther through eating pork scraps or by scavenging certain factors such as pH may affect survivability wildlife carcasses. Rats may in turn be hunted of trichinae in fermented sausage, prescribed heat and eaten by wildlife predators, or when they treatment is considered necessary.31 die, be eaten by wild carrion feeders or pigs. Crossover of Trichinella from one transmission cycle to another may occur, with domestic to CESTODES (TAPEWORMS) sylvatic cycle the more likely109 as wildlife There are a number of food-borne tapeworms strains may have low infectivity for rats or pigs. that infect humans, of which a few are acquired by eating meat or fish. A general description and Prevention and Control classification of food-borne tapeworm species is Human infection by trichinae is linked to the provided in Table 9-1. consumption of undercooked pork or game meat. A number of measures can therefore be Diphyllobothriosis taken to control infection. These involve a com- bination of consumer education and control of Although there are various species of fish infection in pigs. Pig herds can be kept free of tapeworm reported in humans, the most impor- infection by ensuring that pork scraps are not fed tant is Diphyllobothrium latum. Public Health Significance mented, then freezing at -10 0C for 1-3 days Diphyllobothriosis is usually asymptomatic, should kill pleurocercoid larvae in the fish tis- but long-term infection with the tapeworm may sue. Sewage from lakeside hotels and from lei- produce vitamin B 12 deficiency leading to anemia. sure boats should be treated before release into The presence of several worms may cause intesti- the lakes. nal obstruction. CNS signs of peripheral and spi- nal nerve degeneration have been reported. Diag- Taeniosis () nosis is based on identifying the presence of the characteristic eggs in human feces. Taeniosis is intestinal infection with a pre- adult or adult stage of a tapeworm of the genus Life Cycle Taenia. Only two species, T. saginata and T. solium, infect human intestines as adult tape- The fish tapeworms are among the largest worms, and man is the only known final host. worms to infect humans. Adult tapeworms are Intermediate stages of these human tapeworms found in the small intestine, ranging from 2 m to infect the tissues of meat-producing animals. 15 m in length and living as long as 10 years. Tissue infection with a metacestode stage of Many species offish such as pike, perch, turbot, Taenia is referred to as cysticercosis. The inter- salmon, and trout serve as second intermediate mediate hosts of T. saginata and T. solium are hosts. The life cycle of D. latum is shown in Fig- domesticated cattle and pigs, respectively, but ure 9-5. several other ruminants, including sheep, goats, Distribution and llamas, have been recorded as carriers of C. bovis, although the validity of these hosts has The distribution of D. latum is widespread in been questioned. The reindeer, Rangifer the temperate and subarctic regions of the North- tarandus, has been shown to act as an intermedi- ern Hemisphere where freshwater fish are eaten. ate host in Russia. Cysticerci thought to be C. Distribution is summarized in Table 9-2. cellulosae have been reported in monkeys, wild Epidemiology and Transmission pigs, bush babies, camels, rabbits, hares, bears, dogs, foxes, cats, rats, and mice. Four species Diphyllobothriosis is transmitted by the in- (i.e., T. solium, T. saginata, T. multiceps, and T. gestion of infected, raw, or improperly cooked hydatigena) parasitize human organs as cys- freshwater fish. Human cultures with prefer- ticerci; the last three species invading man only ences for smoked, pickled, or raw fish (such as exceptionally.163 Other species, T. serialis, T. sashimi or sushi) are at particular risk. longihamatus, T. crassiceps, and T. taeniae- Endemnicity is maintained where there is formis, have occasionally been diagnosed as a poor sanitation, or, due to the practice of lake- cause of cysticercosis in man.12'14'92 side hotels, pumping of raw sewage into fresh- water lakes. The parasite may have been spread Public Health Significance by the emigration of infected people from en- Taeniosis itself causes little if any disability demic areas into lake regions in which suscep- and morbidity. Conversely, human cysticercosis tible and fish were present. Scandina- has a definite public health significance, causing vian and Russian immigrants are thought to have disability and death in infected people. Cys- introduced the parasite into the Great Lakes re- ticerci may be found in every organ of the body gion of North America and Alaska. of man, but are most common in the subcutane- ous tissue, eye, and brain. In the brain Prevention and Control (neurocysticercosis), the tissue reaction that oc- Human infection is easily prevented by ensur- curs may cause a variety of CNS disorders, some ing that freshwater fish is well cooked or by of which may be fatal. In endemic areas, changing dietary habits through education. If neurocysticercosis may be responsible for 30- fish is to be eaten raw, smoked, pickled, or fer- 60% of cases of epilepsy, and mortality may Human infection through ingestion of raw, uncooked, or poorly preserved fish containing plerocercoids

Adult worm in small intestine

Diphyllobothrium latum

First intermediate host ingested by fish Gravid Proglottid (second intermediate host) in feces

Procercoid develops within Egg hatches in water, first intermediate host releasing coracidium

Coracidium ingested by crustacean (first intermediate host) Figure 9-5 Life cycle of Diphyllobothrium latum. Source: © Crown Copyright. range from 1% to 2% of all causes of death. For a matic improvement in therapy. Diagnosis of hu- long time, treatment of taeniosis was neither safe man taeniosis is not always straightforward and nor satisfactorily effective; however, the intro- is based on clinical symptoms and the identifica- duction of effective taenicides has seen a dra- tion of tapeworm proglottids or eggs during stool or anal swab examination.72 Repeated fecal cystercerci. The life span of cysticerci varies, examinations increase the chances of finding probably due to parasite or host strain variations, eggs, and diagnosis can be improved by taking different infection doses, and host immunologi- perianal swabs using sticky cellophane tape. A cal responses. C. bovis in cattle, for example, re- fecal antigen test has also been reported.3'41 main viable for nine months to three years. Numbers of cysticerci depend not just on the de- Life Cycle gree of exposure to infective and viable tape- Adult tapeworms of T. saginata measure 4-12 worm eggs, but also on the level of host immu- m in length and take approximately three months nity that can effectively reduce the number of to become fully grown. T. solium is shorter, 1.5 m developing cysticerci. to 8 m, and takes 62-72 days to mature. Both Adult tapeworms have a high biotic potential. tapeworms are found in the small intestine of Within infected human populations, the total man and may live for up to 25 years. The life production of eggs can be enormous. The eggs cycles are similar, involving cattle and pigs re- are sensitive to temperatures higher than 38 0C spectively (Figure 9-6). and to desiccation, but are capable of surviving European winters for 35 days58 and of surviving Distribution in sea or brackish waters for some time. The T. saginata (C. bovis) occurs in many cattle- eggs are also relatively resistant to chemicals. T. breeding regions and especially where beef is saginata eggs remain infective for calves after eaten raw or undercooked. Distribution of T. 16 days in sewage, up to 71 days in sludge, and solium (C cellulosae) is usually confined to poor for several months in pastures.110 countries because it is mainly related to the low husbandry practices, human eating sanitation in pigs' breeding areas. Human migra- habits, sanitary education, and willingness to co- tion and increased consumption of pork increases operate in control programs are all factors that the spread of taeniosis/cysticercosis from the en- may further influence the transmission of demic rural areas into urban areas. Bovine cys- taeniosis. Poverty, ignorance, and some local ticercosis has a high prevalence in western and customs of eating raw pork or raw meat or vis- eastern Central Africa and some Asian countries.60 cera may also play an important transmission Moderate infections are seen in other coun- role. The habit of eating raw meat or semi-raw tries125'173 and are summarized in Table 9-2. The sausages is strongly rooted in some cultures. prevalence of bovine cysticercosis in Europe and the United States has decreased throughout the Prevention and Control twentieth century, through the introduction of Control measures include improved diagnosis meat inspection procedures in these countries. and treatment of human taeniosis as well as Fluctuations in prevalence in Europe have oc- proper pig and cattle husbandry and the instiga- curred as a result of the migration of people fol- tion of meat inspection procedures. However, lowing World War II and increased tourism,124 and routine meat inspection may be inadequate for in the United States, occasional outbreaks have light infections and may miss more than half of been attributed to Mexican immigrant workers.141 the infected animals.165 In cattle, the heart is The distribution of pig cysticercosis is also most frequently infected; in pigs, the tongue is summarized in Table 9-2. In countries that are the most commonly infected organ.125 Poor local supposed to be free of T. solium infections, human sanitation is largely responsible for the ease of cysticercosis may occur sporadically, mainly due transmission in rural endemic areas. to contact with infected migrants or tourists.76 Food transmission can be controlled by avoid- ing the consumption of raw pork or beef or semi- Epidemiology and Transmission raw meat products. Freezing infected pork or Man becomes infected with taeniosis by eat- beef can kill the cysticerci when the internal ing raw or undercooked meat containing viable temperature of meat or a carcass is less than -5 Taenia saginata

Eggs (hexacanth embryo) ingested by intermediate hosts

Taenia solium Cysticerci in intermediate hosts

cysticercus Human cysticercosis following ingestion of eggs

proglottids Cysticercus evaginates T. saginata T. solium

Gravid proglottids in feces Adult worms in small intestine

Figure 9-6 Life cycle of Taenia solium and Taenia saginata. Source: © Crown Copyright. 0C for at least four days or around -20 0C for at spread in China, Taiwan, and Korea. The preva- least 12 hours. It is not known if cysterci can sur- lence and distribution of infection is associated vive meat fermentation conditions, but it would with the presence of susceptible snail and fish seem sensible to freeze or heat treat flesh ingre- intermediate hosts and habits of the indigenous dients wherever possible. populations. It has been suggested that close to 25 million people are infected in Asia, mostly in TREMATODES (FLUKES) southern China and North Korea. Trematodes or flukes are unsegmented, Epidemiology and Transmission dorso-ventrally flattened, leaf- or lancet-shaped Infection by flukes in man occurs by eating parasitic worms. The life cycles of the parasitic raw, undercooked, or poorly preserved infected flukes discussed in the text are indirect, involv- fish. In some areas where the parasite occurs, ing a variety of intermediate hosts. A general fish is eaten raw in thin slices with rice (congee). description of food-borne flukes and their classi- The eating of raw freshwater fish has become fication is provided in Table 9—1. increasingly popular in several Far Eastern countries, and consequently the prevalence of Clonorchiosis human infection is increasing. Infections outside of Asia are usually imported. In most endemic (Opisthorchis sinensis), the areas, cats and dogs are infected in high num- Chinese , is a trematode infection that is bers. Levels of infection are maintained by the found throughout southeast Asia. The parasite is practice of fertilizing ponds used to raise fish acquired by eating raw or poorly cooked or pre- with human excrement. served freshwater fish, particularly carp, and can Diagnosis is based on the identification of the infect a range of mammals, including man. characteristic eggs in fecal samples, which have to be differentiated from other trematode eggs Public Health Significance such as , Metagonimus Human infections may be present for many yokogawi, Haplorchis taichui, and Opisthorchis years without causing overt signs of clinical dis- species (Table 9-^). Several serologic tests have ease. The development of clinical signs depends been developed, but most are nonspecific. A re- on the number of worms present, which can num- ported enzyme-linked immunosorbent assay ber several thousands in heavy infections. Large (ELISA) may be of value.30 numbers of flukes in the bile ducts can cause cho- langitis (inflammation of the bile ducts) and gall- Prevention and Control stones in man,115 and may possibly predispose to In endemic areas, treatment of all infected cholangiocarcinoma.143 The parasite may on occa- persons and improved sanitation would help sions enter the pancreatic ducts, causing dilatation, control infection by flukes. In areas where fish fibrosis, and pancreatic stones. are raised in ponds, human and animal feces should be composted or sterilized before they Life Cycle are applied as fertilizer to ponds. Adult flukes, which may live as long as 30 Thorough cooking of all freshwater fish is the years, inhabit the bile ducts of man and other fish- most effective means of controlling infection by eating mammals. More than 100 species offish are flukes. Clonorchiosis can be prevented by avoid- reported hosts for the parasite in Asia. The life ing eating raw, undercooked or improperly pick- cycle of adult fluke is shown in Figure 9-7. led, salted, dried, smoked, or fermented fish in endemic areas. There is little or no information Distribution on conditions affecting the survivability of the The parasite distribution of flukes is shown in encysted infective stages in fish flesh. Education Table 9-3. Infection rates have decreased in Ja- projects are of some benefit, but the eating of pan in recent years, but infections remain wide- raw or fermented freshwater fish has been a Next Page