CHAPTER 9

Microbiological Hazards andTheir Control: Parasites

Mike Taylor

INTRODUCTION

Many types of parasites are food-borne, andhumans can become infected following the in-gestion of infected or contaminated meat, fish,molluscs, vegetables, or fruit, or products de-rived from these foods. In most cases, parasiticinfections are acquired by eating raw or incom-pletely cooked food, or food that is partiallypickled or smoked or poorly preserved. Most, ifnot all, infections are preventable if the food isprepared sufficiently to destroy the infectivestages of the parasite. However, many infectionsare commonly associated with cultural and eat-ing habits that have been in practice in popula-tions for generations.

Meat from many species of animals has beena recognized source of many helminth, and someprotozoal, infections, in man. In developedcountries, the introduction of meat hygiene mea-sures has resulted in reduced incidences of manyof the traditionally recognized helminth infec-tions. However, the eating of many traditionalraw or lightly cooked meat dishes continues, andmay occasionally result in infection in man.Raw, uncooked fish dishes are also commonlyeaten in many cultures, and snails, clams, oys-ters, and a variety of other molluscs are part ofthe diets of many people worldwide. Althoughmost food-borne helminth infections are re-ported from Third World countries, increased

Source: © Crown copyright 1997. Published withthe permission of the Controller of Her BritannicMajesty's Stationery Office. The views expressed arethose of the author and do not necessarily reflect thoseof Her Britannic Majesty's Stationery Office or theVLA or any other government department.

immigration, tourism, and desire to experiencethe culinary dishes of other cultures may in-crease the incidence of parasitic disease in othercountries. As with some helminths, protozoanparasites are opportunistic infections that are of-ten acquired as the result of poor hygiene ortravel to foreign countries.

Fermented foods that use raw ingredients thathave been contaminated or infected with infectiveor intermediate parasite stages have the potentialto cause human infection. Although food-borneparasitic diseases continue to be reported globally,reports of human infection following the ingestionof fermented food are sparse. Cultural dishes suchas som fak (a fermented Thai minced fish dish)have been reported to result in human infectionwith the helminth parasite, Gnathostoma (seeGnathostomosis). Infection with another proto-zoan parasite, Giardia, has been reported follow-ing the ingestion of cheese dip. Fermentationalone may therefore be insufficient to prevent thetransmission of many food-borne parasites, andpotentially infected material should be avoidedwherever possible, or alternatively subjected tofreezing or some form of heat treatment.

Many parasites infect humans, but referenceis made only to those helminths and protozoathat are recognized as food-borne and a potentialsource of infection in fermented foods.

NEMATODES

The nematodes are a diverse group of para-sitic or free-living unsegmented worms that areusually cylindrical and elongate in shape. Withfew exceptions, the sexes of nematodes are sepa-rate, and the life cycle may be direct or indirect,

involving an intermediate host. The general de-scription and classification of the food-bornenematodes discussed in this chapter are summa-rized in Table 9-1.

Angiostrongylosis

Angiostrongylus cantonensis and A. costari-censis are parasites of rodents (predominantlyrats) that can cause disease in humans through theingestion of infected snails. Two other species, A.malaysiensis and A. mackerrasse, occur but havenot been associated with human infection. Mosthuman infections are acquired by eating infectedsnails, but can occur through eating infectedshrimp and crab, or snail- or slug-contaminatedraw vegetables.

Public Health Significance

A. cantonensis can cause meningitis and menin-goencephalitis with mild to moderate symptoms,often of sudden onset, with intense headaches;vomiting; moderate intermittent fever; and, in ap-proximately 50% of cases, coughing, anorexia,malaise, constipation, and somnolence.176 In se-vere cases, coma and death may occur. Accidentalingestion of the slug intermediate host of A.costaricensis causes abdominal angiostrongylosiswith symptoms similar to appendicitis, includingfever, abdominal pain, anorexia, diarrhea, andvomiting.96 Migratory larvae may cause gastroen-teritis, tumor-like masses or abcessation of the in-testines, liver enlargement, nervous signs, coma,and, occasionally, death.108 Infection is normallydiagnosed by confirming the presence of parasitesor eggs in surgically removed tissues or fluids orby using serological assays.37'144'169

Life Cycle

Adult worms are found in the pulmonary ar-teries of rats. The life cycles of A. cantonensisand A. costaricensis are similar and are shown inFigure 9-1 . The prepatent period (from infectionto maturity) is 42—45 days.

Distribution

The distributions of A. cantonensis and A.costaricensis are summarized in Table 9-2.

Most human infections and deaths associatedwith A. cantonensis have been reported fromTaiwan, Thailand,131'176 and some Pacific is-lands, but human infections have been reportedin most countries where the parasite occurs andappears to be spreading.33 The incidence ofangiostrongylosis appears to be spreading, espe-cially in those areas in which snails are an im-portant part of the diet.

Epidemiology and Transmission

Humans become infected with angiostrongyl-osis by intentionally or accidentally eating in-fected snails or slugs. Rodents are infected by in-gesting infected molluscs or by ingesting infectivelarvae present in "slime" on plants. In most en-demic areas of Asia, both land and aquatic snails(Achatina and PiId) are eaten regularly. The giantAfrican land snail, Achatina fulica, is a particulardelicacy in many countries and is a good interme-diate host. Slugs and snails (which are used formedicinal purposes in some cultures), land crabs,shrimp, and paratenic hosts such as toads andfrogs have also transmitted infection. Sauces pre-pared from shrimp juices or unwashed contami-nated vegetables have also been incriminated. Thedrinking of untreated water containing larvae re-leased from dead snails has also been suggested asa means of infection. Infection continues to be re-ported from new areas of the world, in part due tothe dissemination of the intermediate snail hosts,but also due to transportation of infected rats onships. Most terrestrial and aquatic snails are sus-ceptible to infection, and populations can bereadily infected from carrier rats.

Prevention and Control

Angiostrongyliosis can be prevented by edu-cating people in endemic areas to avoid eatinguncooked molluscs, particularly land snails.Freezing will kill larvae present in snails if theyare frozen at -15 0C for 12-24 hours. Paratenichosts (i.e., shrimp, prawn, crabs) should becooked before eating, and vegetables should bewashed before eating raw. Little or no informa-tion is available on the survivability of infectivelarvae in fermented foods such as balao-balao(fermented shrimp).

Table 9-1 Food-Borne Helminths— Classification

Genus

Angiostrongylus

AnisakisTrichinellaCapillariaDioctophymaGongylonemaGnathostomaDiphyllobothrium

Taenia

FasciolaFasciolopsisEchinostomaHypoderaeumParagonimusNanophyetesHeterophyesMetagonimusOpisthorcis(Clonorchis)

Family

Metastrongyloidae

AnisakidaeTrichinellidaeCapillaridaeDioctophymatidaeThelaziidaeGnathostomatidaeDiphyllobothridae

Taeniidae

Fasciolidae

Echinostomatidae

Troglotrematidae

Heterophyidae

Opisthorciidae

Order

Strongylida

AscarididaEnophida

DioctophymidaSpirurida

Pseudophyllidea

Cyclophyllidea

Echinostomida

Plagiorchiida

Opisthorchiidae

Class

Nematoda (Roundworms)Elongate, cylindrical, unsegmented worms withfluid-filled body cavity. Sexes are separate.Life cycle direct or indirect.

Cestoda (Tapeworms)Tape-like segmented body comprising head,neck, and strobila (proglottids). Bothria or suckersfor attachment. Hermaphroditic. Indirect life cycles.

Trematoda (Flukes)Unsegmented leaf or lancet-shaped worms withtwo muscular suckers for attachment and well-developed oral sucker and pharynx.Hermaphroditic (generally). Indirect life cycles.

Phylum

Nemathelminthes

Platyhelminthes

Source: ©Crown Copyright.

Anisakiosis

Anisakiosis is a parasitic gastrointestinal dis-ease of man that is caused by the larval stages ofnematodes of the family Anisakidae. The adult

worms are common parasites of marine mam-mals (Table 9-2), and the larval stages are foundin marine fish and squid. Humans acquire infec-tions by eating the raw or improperly cooked orpreserved meat of these animals. There are many

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

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

Carriers(crabs, prawns)

Second- and third-stage larvae inintermediate host (slug, snail)

Angiostrongylus cantonensis

Ingested by rat

First-stage larvaeexcreted in feces

Table 9-2 Food-Borne Helminths (Nematodes, Cestodes)

Source of Infection to Man

Molluscs (snails), shrimps,crabs, amphibians,contaminated vegetablesand salads

Fish

Fish

Fish

Fish , frogs, chickens,ducks, snakes

Salads (insects)

Meat

Fish

Meat (beef)

Meat (pork)

Main Hosts (final)

Rodents (rats)

Pinipeds (whales, dolphins,porpoises)

Seals, sealions, walrusesMan (several species of

birds)Carnivores (mink, ferret,

dogs, cats, jackals), manCarnivores (dogs and

cats), manPigs, manRuminants, pigs, dogs,

cats, horses, rodents,primates, man

Pigs, rodents, carnivores(mink, fox, badger,bears, walrus, seals),man

Dog, fox, mink, cat, pig,bear, seals

Man

Man

Distribution

Asia and Pacific Islands, Australia, India,Africa, Caribbean, parts of UnitedStates

North and South America, Pacific Islands,parts of northern Europe

Phillipines, Thailand

Worldwide (North and South America,southern Europe, Asia, Middle East)

Thailand, Japan, southeast Asia, China,Mexico (Middle East, Africa, BalticStates, Russia)

United States, former USSR, parts ofEurope, Middle East, China, NorthAfrica, New Zealand

Worldwide (except Antartica)

Northern Hemisphere (northern Europe,Russia, North America, South America,Asia, Africa)

Central Africa, Asia, South and WestAfrica, parts of Europe, southeast Asia,Central and South America; alsoreported in United States, Canada,Australia and Pacific Islands

Central and South America, central andeast Africa, southeast Asia, southernEurope

Parasite

Angiostrongylus

Anisakis simplexAnisakis decipens

Capillaria phillipinensis

Dioctophyma renale

Gnathostoma spinigerum

Gnathostoma hispidumGongylonema pulchrum

Trichinella spiralis

Diphyllobothrium latum

Taenia saginata(Cysticercus bovis)

Taenia solium(Cysticercuscellulosae)

Parasite Class

Nematoda(Roundworms)

Cestoda(Tapeworms)

Source: © Crown Copyright.

species of anisakid nematodes, but those mostoften associated with human illness are Anisakissimplex, Pseudoterranova decipiens, Phoca-nema, and Contracaecum spp.

Public Health Significance

Anisakis causes acute or chronic gastrointesti-nal disease in man. Migrating larvae cause a for-eign-body reaction and eventually necrosis andhemorrhage of the stomach, occasionally creat-ing tunnels and burrows in the stomach mu-cosa,139 causing pain, nausea, and vomiting. Theacute symptoms subside in a few days, but avague abdominal pain with intermittent nauseaand vomiting persists for weeks, with symptomsresembling those of a peptic ulcer. The conditionis often misdiagnosed because of its similarity toother acute gastrointestinal conditions (e.g., gas-tric ulcers or neoplasm, appendicitis, diverticuli-tis, Crohn's disease, gallstones, etc.). Diagnosisis normally only made following biopsy andconfirmed on histopathology.

Life Cycle

Adult anisakid worms are located in thestomach of marine cetaceans and pinnipeds butdo not develop in humans. The life cycle ofthese worms is shown in Figure 9-2. Humansbecome infected if an intermediate fish hostcontaining infective third-stage larvae is eatenuncooked.

Distribution

Fish infections are found in most oceans andseas but are highest in areas in which there arehigh marine mammal populations, such ascoastal Japan and Alaska. Many species of fishare naturally infected with anisakiosis, and theprevalence of infection can be very high. InJapanese waters, 123 species of marine fish havebeen found to harbor the parasite.118 The globaldistribution of anisakiosis is summarized inTable 9-2. The highest levels of infection havebeen reported from Japan and the Netherlands.88

Epidemiology and Transmission

The main source of infection from anisakidworms for man is marine fish, many species ofwhich are highly parasitized by anisakid larvae.

Humans acquire A. simplex by eating raw orpoorly salted, pickled, or smoked herring, cod,mackerel, salmon, or squid, and P. decipiensfrom cod, halibut, flatfish, and red snapper.Such traditional preparations as green herring,lomi lomi salmon, seviche, sushi, and sashimi(i.e., seasoned fish fillets), all of which use rawor uncooked fish, are major sources of infec-tions.34 In the Netherlands, the occurrence of thedisease was due to the habit of consuming rawor lightly salted herring (green herring).162 Al-though the habit persists, the incidence of hu-man anisakiosis has been drastically reduced byfreezing fish before marketing. In recent years,the highest incidence of the disease has been re-corded in Japan, where many fish dishes areeaten raw (sashimi); pickled in vinegar(sunomono)\ or fermented in rice, rice bran, orkoji (sushi and zuke). In the United States, atleast two cases have been linked to eatingseviche (i.e., pieces of raw fish seasoned inlemon juice for several hours), and others to eat-ing Japanese raw fish dishes.

Prevention and Control

The risk of human infection with anisakiosisincreases in countries where fish are eatenraw.172 Anisakiosis is preventable by ensuringthat only well-cooked marine fish, octopus, andsquid are eaten. Larvae are killed by cooking at60 0C or above. Freezing fish at -20 0C for 24hours will kill the larvae, with the exception ofsome North American species that can survivefreezing at that temperature for 52 hours. Clean-ing and eviscerating fish immediately after theyare caught prevents larvae migrating from theintestine to the muscles. Salt curing, marinating,microwaving, and smoking temperatures are in-sufficient to kill the parasite.34 Marination ofherring has been a long tradition in parts ofnorthern Europe,85'106 involving the preservationof herring fillets in salt and acetic acid. The salt/acetic acid marination process produces the typi-cal flavor as a result of denaturing of the fishproteins, lowering of the pH, and addition ofsugar and spices.158 The salt/acid treatment maytake up to 42 days to kill Anisakis larvae, and atlow concentrations may not kill larvae at all.85

Larvae have also been shown to survive in izushi

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

(i.e., pickled rice with cod roe, fillets of salmon,and cod) and in sashimi.118

Capillariosis

Intestinal capillariosis is caused by a tinynematode, Capillaria philippinensis. The dis-ease was first recognized in the Philippines inthe 1960s and has subsequently been reported in

other countries.32'34'93 Man is the main definitivehost for the parasite, but several species of birdsare now believed to be a natural host and are ableto transmit the infection.35

Public Health Significance

Infections with C. philippinensis can cause di-arrhea, anorexia, weight loss, and, if left un-treated, death. The parasites cause damage to the

Anisakis simplex

Eggs in feces

First- or second-stage larvaeingested by crustacean

Infective larvae in fish

Human infection through ingestionof raw, undercooked, or poorlypreserved fish

mucosa of the small intestine, leading to fluid,protein, and electrolyte loss. Clinical symptomsinclude abdominal pain and diarrhea. If treat-ment is not initiated rapidly, patients die becauseof the irreversible effects of the electrolyte loss,heart failure, or septicemia. In endemic areas, a di-agnosis can be made on patients based on clinicalsigns. In chronic infections, there is weight loss,wasting, and intractable diarrhea. Infection is con-firmed by identifying eggs, larvae, and adults mi-croscopically in the feces. Serological tests are notsufficiently specific for routine use.

Life Cycle

C. philippinensis is a small nematode that isfound in the small intestines of man. Further de-velopment occurs in fish. A number of species offreshwater fish are suspected to serve as inter-mediate hosts for the parasite. The fish are usu-ally small and are eaten whole in the Philippinesand Thailand, leading to human infection.

Distribution

The distribution of intestinal capillariosis issummarized in Table 9-2. Nearly 2,000 cases ofcapillariosis have been recorded in the Philip-pines, with more than 100 deaths. In Thailand,there have been only a few hundred cases, withan unknown number of deaths recorded.36

Epidemiology and Transmission

Sanitation facilities are poor in many rural ar-eas of southeast Asia and defecation in the fieldsis a common practice. During the monsoonrains, the feces are broken down and washedaway to streams and ponds, resulting in infectionof freshwater fish. These and many other foodsare eaten uncooked, especially in the endemicareas of the Philippines and in Thailand.

Prevention and Control

Educating both the local population and visi-tors of the dangers of eating uncooked freshwa-ter fish can help prevent intestinal capillariosis.Improvement of sanitation and the control of in-discriminate disposal of feces would also bebeneficial. No information is available on theconditions that kill the parasite in fish and

whether they are known to survive in fermentedfish products.

Dioctophymosis

Dioctophyma (Dioctophyme) renale is a largekidney-dwelling nematode of carnivores. Infec-tion is acquired by ingesting raw or undercookedfish or frogs. It has only rarely been reported inman.

Public Health Significance

Infection in man can cause renal damage andassociated symptoms of renal colic, hematuria,or urinary obstruction. In humans and dogs, Dio-ctophyma usually locates in only one kidney,most often the right one, and in most cases onlyone parasite is found, causing little or no clinicalsymptoms. Infection is diagnosed by the pres-ence of the characteristic thick, bipolar eggs inurine (only if female worms are present).

Life Cycle

D. renale is a large, blood-red nematode that isfound in the kidneys of carnivores (Table 9-2).The size of the parasite depends on the size of thehost species; in dogs, the adult female of the para-site can reach up to 1 m in length. The intermediatehost is a free-living, aquatic segmented worm (oli-gochaete) in which further development to an in-fective larva occurs. Transmission to a final hostoccurs following ingestion of the annelid interme-diate host, or more usually following ingestion of afish or a frog, which act as transport hosts. Theprepatent period is from 3]/2 to 6 months.

Distribution

D. renale is found on all continents with thepossible exception of Africa and Oceania (Table9-2). The most frequently reported form of in-fection is canine dioctophymosis, with the high-est prevalence of infection in Canadian wildmink (Mustela vison), where 18% of the animalsare infected. The disease is very rare in man,with only a few reports worldwide.

Epidemiology and Transmission

In North America, mustelids, especially mink,appear to be the main reservoir. In other areas, it

is likely that other species of mustelids or wildcanids serve as main definitive hosts. Thesehosts are infected by ingesting frogs or fish(paratenic hosts) and aquatic oligochaetes (inter-mediate hosts) that contain the third-stage lar-vae. Dogs and humans are accidental hosts andare infected by ingesting raw fish and frogs, andalmost always harbor only one parasite. The rar-ity of human infection can be explained by thefact that larvae are located in the mesentery andliver of fish and frogs, which generally are noteaten by man.

Prevention and Control

Infection can be prevented, both in humansand dogs, by avoiding the consumption of raw orundercooked fish and frogs. It is not known whatconditions result in larval death.

Gnathostomosis

Gnathostomosis is caused by infection withthe larval or immature adult stages of nematodesof the genus Gnathostoma. Adult parasites arereported in dogs, cats, and other carnivorous ani-mals worldwide. In Thailand, more than 40 spe-cies of vertebrates have been reported to be natu-rally infected. These include freshwater fish,frogs, snakes, chickens, ducks and other birds,rats, mongooses, and tree shrews.38 Four species,G. spinigerum and G. hispidum, and more re-cently, G. doloresi and G. nipponicum, havebeen reported in humans in Japan.111'152

Public Health Significance

Man is an abnormal host, with infection re-sulting in a larval migrans causing red, itchy,and edematous subcutaneous swellings that usu-ally last approximately one week but can recurweeks or months later. More rarely, the parasitemay enter the eye, causing subconjunctivaledema, exopthalmus, impaired vision or blind-ness through hemorrhage, and retinal damage.Invasion of the central nervous system (CNS)can produce headaches, neck stiffness, drowsi-ness, or coma and death. Brain hemorrhage andtransitory obstructive hydrocephalus have alsobeen reported.140 Diagnosis in endemic areas is

based on history, symptoms, or serology and canbe confirmed following the recovery and identi-fication of parasitic larvae.114

Life Cycle

Adult worms of G. spinigerum are found intumor-like masses in the stomach wall of fish-eating mammals. The life cycle of G. spinigerumis shown in Figure 9-3. The prepatent period isapproximately six months.

Distribution

The distribution of human gnathostomiosis issummarized in Table 9-2.

Epidemiology and Transmission

The main source of human infection ofgnathostomosis in Thailand is the snake-headedfish, Ophicephalus spp., which is one of thefishes used in som-fak, a rice-fermented fish dishwith widespread popularity. In Japan, freshwa-ter Ophicephalus species are eaten raw assashimi. The ingestion of raw or inadequatelycooked fish is the major source of infection inother areas reporting the disease. Infections inMexico are attributed to eating raw cycloid fish asceviche." Human infections are also reportedfrom eating raw or poorly cooked catfish, eels,frogs, chickens, ducks, and snakes.39 Dogs, cats,and several species of wild mammals are reser-voirs of the parasite. These definitive hosts be-come infected primarily through eating infectedfish or other animals that serve as paratenic hosts.

Prevention and Control

Health education programs in endemic areasof Asia are required to control this type of infec-tion. Ensuring that people eat only well-cookedfish, eels, or other intermediate hosts such assnakes, frogs, and poultry can prevent infec-tions. Potentially copepod-infested water shouldbe boiled or treated.

Gongylonemosis

Gongylonema pulchrum is a spiruroid nema-tode of the Thelaziidae family (Table 9-1). It isfound in all domesticated mammals, but is most

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 pharyngitisman infection are rare. and stomatitis reported. Diagnosis is based on

history, clinical signs of mouth irritation, andPublic Health Significance microscopic identification of the parasite. Occa-

In humans, gongylonemosis parasites have sionally, the parasite has been found emergingbeen found in the submucosa of lips, gums, hard from the mouth. Infection in animals is usually

Human infection throughingestion of raw orundercooked fish

Encysted larvae in fish,amphibians, or reptiles

Cyclops, crustaceanintermediate host

Gnathostoma spinigerum

Hatched larvaeingested by Cyclops

Final Host(fish-eating mammals)

Eggs passedin feces

Adults worms in stomach

asymptomatic, but may sometimes cause lesionsof the mouth or pharynx.29 In pigs, the parasite isfound in the tongue mucosa and may cause oc-clusion of the esophagus.179

Life Cycle

Adult Gongylonemosis worms live in themouth, esophagus, or rumen of the final hosts. Thelife cycle of G. pulchrum involves coprophagicbeetles of the genera Aphodius, Ontophagus, andBlaps as intermediate hosts. Ruminants becomeinfected by ingestion of the beetles with grass orother infested food.

Distribution

Although G. pulchrum is widely distributedgeographically, human infection is rare. The dis-tribution of G. pulchrum is summarized in Table9-2. Infection in domestic ruminants varies con-siderably, with high levels of infection reportedin the Ukraine (e.g., 32-94% of adult cattle, 39-95% of sheep, and 0-37% of pigs infected),29

and Iran (e.g., 49.7% of the cattle).4 In theUnited States, the parasite was found in 5.9% ofpigs, varying from O to 21% according to geo-graphic origin.179

Epidemiology and Transmission

Man is an accidental host and is probably in-fected by ingesting beetles on salads and rawvegetables.

Prevention and Control

Because the Gongylonemosis parasite is rarein humans and causes only mild symptoms, spe-cial control measures are usually not recom-mended. Individual protection can be obtainedby observing the rules of personal, food, and en-vironmental hygiene.

Trichinellosis (Trichinosis)

Trichinellosis (trichinosis) is a food-bornedisease that is caused by infection with parasiticnematodes of the genus, Trichinella. Infectionresults from ingesting meat harboring infectivelarvae. Until recently, T. spiralis was acceptedas the sole representative of the genus Tri-chinella. It has now become clear that not all

populations of the parasite are the same, and fivespecies have recently been proposed.24 T.spiralis is the most important species, withwidespread distribution in domestic pigs.

Public Health Significance

Trichinellosis is a cosmopolitan zoonotic,food-borne, parasitic disease resulting from theingestion of meat harboring the infective larvaeof Trichinella. Intestinal trichinellosis is usuallymild and therefore not often diagnosed, but maycause diarrhea and abdominal discomfort, some-times accompanied by nausea and vomiting,leavy infections can be severe, causing ex-

tremely painful muscles, and even fatalities inman. The illness typically begins one to fourweeks after ingestion of infective meat, and ischaracterized by muscle aches and fever. Musclepain, which may be severe and incapacitating, isan outstanding feature, with the jaw muscles fre-quently involved. The infection of heart musclemay induce severe, even fatal, myocarditis.Death may also result from encephalitis or pneu-monitis. In most parts of the world, the probabil-ity of contracting the disease is now low, and itsdecline, certainly throughout the western world,can be attributed to the introduction of a numberof control measures discussed later. Diagnosismay be based on a clinical history of prior con-sumption of raw or undercooked meat, but thisaspect may be missed, particularly in countrieswhere the disease rarely occurs. Clinical signs ofmuscle aches, fever, and periorbital edema areindicative of the disease. Infection is usually di-agnosed by demonstrating larvae in muscle bi-opsy specimens.

Life Cycle

T. spiralis is a small, nematode parasite that isfound in the small intestine of man, pig, rat, andother mammals (Table 9-2). The life cycle of T.spiralis is shown in Figure 9-4. Encysted larvaeremain infective for months, even years. In somehosts, especially man, they eventually die andbecome calcified. Trichinella is remarkableamong parasitic nematodes in having neither afree-living stage between individual hosts nor anintermediate host. The spread of larvae through-out the host musculature permits transmission to

Figure 9-4 Life cycle of Trichinella spiralis. Source: © Crown Copyright.

another individual host, but only after the deathof the first host.

Distribution

Trichinella has been recorded on every conti-nent except Antarctica (Table 9-2). In many ar-

eas, its prevalence in man and pigs has been re-duced to a low level, but persists at higher levelsin wildlife. Prevalence rates are higher in largecarnivorous or scavenging species such as bears,mink, fox, badger, wild boar, and rodents. Infor-mation on the global incidence of clinical

Sylvatic cycleGame meat

Wildlife infection fromcarrion feeding

Trichinella spiralis

Infection via deadinfected rats

Rats infected frompork scraps

Pig-to-pig transmission viacannibalism, tail-biting, etc.

Domestic cycle

Jluman infection via raw oriercooked pork, sausages, etc.

Human infectionfrom game meat

trichinellosis in man is not readily available, butit is evident that there has been a striking reduc-tion in western Europe and the United States.Several outbreaks in France and Italy have beenassociated with eating horse meat that wasthought to have become infected by intention-ally or inadvertently eating fodder that was con-taminated with the bodies of dead rats or mice.Outbreaks of varying severity continue to occurin eastern Europe, the former Soviet Union,Asia, and occasionally elsewhere.

Epidemiology and Transmission

Two distinctive epidemiological cycles of T.spiralis are recognized, domestic and sylvatic.The domestic cycle involves pigs and rats,through either the feeding of uncooked porkscraps (e.g., in waste feed) to pigs, cannibalismamong pigs (e.g., scavenging of dead carcassesand possibly tail biting of live pigs), or infectionof rats by disposal of uncooked pork and the sub-sequent infection of pigs by the ingestion of in-fected rats. Human infection occurs whenundercooked or raw pig meat is eaten.

In the sylvatic cycle, Trichinella is transmit-ted among species of wildlife. Man becomes in-fected by consuming game meat. The two cyclesmay be interrelated by the fact that domesticpigs may scavenge on dead wild animals andvice versa. Rats can also be of significance inthis respect in that they may become infected ei-ther through eating pork scraps or by scavengingwildlife carcasses. Rats may in turn be huntedand eaten by wildlife predators, or when theydie, be eaten by wild carrion feeders or pigs.Crossover of Trichinella from one transmissioncycle to another may occur, with domestic tosylvatic cycle the more likely109 as wildlifestrains may have low infectivity for rats or pigs.

Prevention and Control

Human infection by trichinae is linked to theconsumption of undercooked pork or gamemeat. A number of measures can therefore betaken to control infection. These involve a com-bination of consumer education and control ofinfection in pigs. Pig herds can be kept free ofinfection by ensuring that pork scraps are not fed

to pigs. In some countries, laws requiring wastefood (swill) to be cooked before being fed topigs have been introduced to help control a num-ber of important viral pig diseases. Good hus-bandry and rat-proofing piggeries also help con-trol infection. In many countries, meatinspection procedures have been introduced toidentify infection.

Ethnic or cultural practices in which meat iseaten undercooked or raw are a particular riskarea and may call for special educational mea-sures. Traditional types of sausage (includingfermentated sausage) that receive little cookinghave long been associated with human disease.Education draws attention to the need to freezeor cook such foodstuffs. Freezing may be moreacceptable because it has less effect on flavorand taste than cooking. To be effective, meatmust be frozen throughout and stored for suffi-cient time to ensure death of encysted larvae.The thermal death point of T. spiralis is approxi-mately 57 0C, and cooking pork so that it reachesa temperature of 77 0C gives a margin of safetywithout destroying the taste of the meat. Slightlylower temperatures may be adequate providedthe temperature is achieved uniformly through-out the meat. It can be assumed that pork will besafe if it is cooked until there is no red or pink col-oration throughout. In the United States, fer-mented pork sausages must either originate fromTrichinella-CQrtified meat or be heated to 58.3 0Cat the end of the fermentation process.89 Althoughcertain factors such as pH may affect survivabilityof trichinae in fermented sausage, prescribed heattreatment is considered necessary.31

CESTODES (TAPEWORMS)

There are a number of food-borne tapewormsthat infect humans, of which a few are acquiredby eating meat or fish. A general description andclassification of food-borne tapeworm species isprovided in Table 9-1.

Diphyllobothriosis

Although there are various species of fishtapeworm reported in humans, the most impor-tant is Diphyllobothrium latum.

Public Health Significance

Diphyllobothriosis is usually asymptomatic,but long-term infection with the tapeworm mayproduce vitamin B 12 deficiency leading to anemia.The presence of several worms may cause intesti-nal obstruction. CNS signs of peripheral and spi-nal nerve degeneration have been reported. Diag-nosis is based on identifying the presence of thecharacteristic eggs in human feces.

Life Cycle

The fish tapeworms are among the largestworms to infect humans. Adult tapeworms arefound in the small intestine, ranging from 2 m to15 m in length and living as long as 10 years.Many species offish such as pike, perch, turbot,salmon, and trout serve as second intermediatehosts. The life cycle of D. latum is shown in Fig-ure 9-5.

Distribution

The distribution of D. latum is widespread inthe temperate and subarctic regions of the North-ern Hemisphere where freshwater fish are eaten.Distribution is summarized in Table 9-2.

Epidemiology and Transmission

Diphyllobothriosis is transmitted by the in-gestion of infected, raw, or improperly cookedfreshwater fish. Human cultures with prefer-ences for smoked, pickled, or raw fish (such assashimi or sushi) are at particular risk.

Endemnicity is maintained where there ispoor sanitation, or, due to the practice of lake-side hotels, pumping of raw sewage into fresh-water lakes. The parasite may have been spreadby the emigration of infected people from en-demic areas into lake regions in which suscep-tible copepods and fish were present. Scandina-vian and Russian immigrants are thought to haveintroduced the parasite into the Great Lakes re-gion of North America and Alaska.

Prevention and Control

Human infection is easily prevented by ensur-ing that freshwater fish is well cooked or bychanging dietary habits through education. Iffish is to be eaten raw, smoked, pickled, or fer-

mented, then freezing at -10 0C for 1-3 daysshould kill pleurocercoid larvae in the fish tis-sue. Sewage from lakeside hotels and from lei-sure boats should be treated before release intothe lakes.

Taeniosis (Cysticercosis)

Taeniosis is intestinal infection with a pre-adult or adult stage of a tapeworm of the genusTaenia. Only two species, T. saginata and T.solium, infect human intestines as adult tape-worms, and man is the only known final host.Intermediate stages of these human tapewormsinfect the tissues of meat-producing animals.Tissue infection with a metacestode stage ofTaenia is referred to as cysticercosis. The inter-mediate hosts of T. saginata and T. solium aredomesticated cattle and pigs, respectively, butseveral other ruminants, including sheep, goats,and llamas, have been recorded as carriers of C.bovis, although the validity of these hosts hasbeen questioned. The reindeer, Rangifertarandus, has been shown to act as an intermedi-ate host in Russia. Cysticerci thought to be C.cellulosae have been reported in monkeys, wildpigs, bush babies, camels, rabbits, hares, bears,dogs, foxes, cats, rats, and mice. Four species(i.e., T. solium, T. saginata, T. multiceps, and T.hydatigena) parasitize human organs as cys-ticerci; the last three species invading man onlyexceptionally.163 Other species, T. serialis, T.longihamatus, T. crassiceps, and T. taeniae-formis, have occasionally been diagnosed as acause of cysticercosis in man.12'14'92

Public Health Significance

Taeniosis itself causes little if any disabilityand morbidity. Conversely, human cysticercosishas a definite public health significance, causingdisability and death in infected people. Cys-ticerci may be found in every organ of the bodyof man, but are most common in the subcutane-ous tissue, eye, and brain. In the brain(neurocysticercosis), the tissue reaction that oc-curs may cause a variety of CNS disorders, someof which may be fatal. In endemic areas,neurocysticercosis may be responsible for 30-60% of cases of epilepsy, and mortality may

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 along time, treatment of taeniosis was neither safenor satisfactorily effective; however, the intro-duction of effective taenicides has seen a dra-

matic improvement in therapy. Diagnosis of hu-man taeniosis is not always straightforward andis based on clinical symptoms and the identifica-tion of tapeworm proglottids or eggs during

Procercoid develops withinfirst intermediate host

Egg hatches in water,releasing coracidium

Gravid Proglottidin feces

First intermediate host ingestedby fish

(second intermediate host)

Diphyllobothrium latum

Adult worm insmall intestine

Human infection through ingestionof raw, uncooked, or poorlypreserved fish containingplerocercoids

stool or anal swab examination.72 Repeated fecalexaminations increase the chances of findingeggs, and diagnosis can be improved by takingperianal swabs using sticky cellophane tape. Afecal antigen test has also been reported.3'41

Life Cycle

Adult tapeworms of T. saginata measure 4-12m in length and take approximately three monthsto become fully grown. T. solium is shorter, 1.5 mto 8 m, and takes 62-72 days to mature. Bothtapeworms are found in the small intestine ofman and may live for up to 25 years. The lifecycles are similar, involving cattle and pigs re-spectively (Figure 9-6).

Distribution

T. saginata (C. bovis) occurs in many cattle-breeding regions and especially where beef iseaten raw or undercooked. Distribution of T.solium (C cellulosae) is usually confined to poorcountries because it is mainly related to the lowsanitation in pigs' breeding areas. Human migra-tion and increased consumption of pork increasesthe spread of taeniosis/cysticercosis from the en-demic rural areas into urban areas. Bovine cys-ticercosis has a high prevalence in western andeastern Central Africa and some Asian countries.60

Moderate infections are seen in other coun-tries125'173 and are summarized in Table 9-2. Theprevalence of bovine cysticercosis in Europe andthe United States has decreased throughout thetwentieth century, through the introduction ofmeat inspection procedures in these countries.Fluctuations in prevalence in Europe have oc-curred as a result of the migration of people fol-lowing World War II and increased tourism,124 andin the United States, occasional outbreaks havebeen attributed to Mexican immigrant workers.141

The distribution of pig cysticercosis is alsosummarized in Table 9-2. In countries that aresupposed to be free of T. solium infections, humancysticercosis may occur sporadically, mainly dueto contact with infected migrants or tourists.76

Epidemiology and Transmission

Man becomes infected with taeniosis by eat-ing raw or undercooked meat containing viable

cystercerci. The life span of cysticerci varies,probably due to parasite or host strain variations,different infection doses, and host immunologi-cal responses. C. bovis in cattle, for example, re-main viable for nine months to three years.Numbers of cysticerci depend not just on the de-gree of exposure to infective and viable tape-worm eggs, but also on the level of host immu-nity that can effectively reduce the number ofdeveloping cysticerci.

Adult tapeworms have a high biotic potential.Within infected human populations, the totalproduction of eggs can be enormous. The eggsare sensitive to temperatures higher than 38 0Cand to desiccation, but are capable of survivingEuropean winters for 35 days58 and of survivingin sea or brackish waters for some time. Theeggs are also relatively resistant to chemicals. T.saginata eggs remain infective for calves after16 days in sewage, up to 71 days in sludge, andfor several months in pastures.110

Animal husbandry practices, human eatinghabits, sanitary education, and willingness to co-operate in control programs are all factors thatmay further influence the transmission oftaeniosis. Poverty, ignorance, and some localcustoms of eating raw pork or raw meat or vis-cera may also play an important transmissionrole. The habit of eating raw meat or semi-rawsausages is strongly rooted in some cultures.

Prevention and Control

Control measures include improved diagnosisand treatment of human taeniosis as well asproper pig and cattle husbandry and the instiga-tion of meat inspection procedures. However,routine meat inspection may be inadequate forlight infections and may miss more than half ofthe infected animals.165 In cattle, the heart ismost frequently infected; in pigs, the tongue isthe most commonly infected organ.125 Poor localsanitation is largely responsible for the ease oftransmission in rural endemic areas.

Food transmission can be controlled by avoid-ing the consumption of raw pork or beef or semi-raw meat products. Freezing infected pork orbeef can kill the cysticerci when the internaltemperature of meat or a carcass is less than -5

Figure 9-6 Life cycle of Taenia solium and Taenia saginata. Source: © Crown Copyright.

Adult worms in smallintestine

Gravid proglottids in feces

T. saginata T. solium

proglottids

Cysticercus evaginates

Human cysticercosisfollowing ingestion ofeggs

cysticercus

Taenia soliumCysticerci in intermediate hosts

Taenia saginata

Eggs (hexacanthembryo) ingested byintermediate hosts

0C for at least four days or around -20 0C for atleast 12 hours. It is not known if cysterci can sur-vive meat fermentation conditions, but it wouldseem sensible to freeze or heat treat flesh ingre-dients wherever possible.

TREMATODES (FLUKES)

Trematodes or flukes are unsegmented,dorso-ventrally flattened, leaf- or lancet-shapedparasitic worms. The life cycles of the parasiticflukes discussed in the text are indirect, involv-ing a variety of intermediate hosts. A generaldescription of food-borne flukes and their classi-fication is provided in Table 9—1.

Clonorchiosis

Clonorchis sinensis (Opisthorchis sinensis), theChinese liver fluke, is a trematode infection that isfound throughout southeast Asia. The parasite isacquired by eating raw or poorly cooked or pre-served freshwater fish, particularly carp, and caninfect a range of mammals, including man.

Public Health Significance

Human infections may be present for manyyears without causing overt signs of clinical dis-ease. The development of clinical signs dependson the number of worms present, which can num-ber several thousands in heavy infections. Largenumbers of flukes in the bile ducts can cause cho-langitis (inflammation of the bile ducts) and gall-stones in man,115 and may possibly predispose tocholangiocarcinoma.143 The parasite may on occa-sions enter the pancreatic ducts, causing dilatation,fibrosis, and pancreatic stones.

Life Cycle

Adult flukes, which may live as long as 30years, inhabit the bile ducts of man and other fish-eating mammals. More than 100 species offish arereported hosts for the parasite in Asia. The lifecycle of adult fluke is shown in Figure 9-7.

Distribution

The parasite distribution of flukes is shown inTable 9-3. Infection rates have decreased in Ja-pan in recent years, but infections remain wide-

spread in China, Taiwan, and Korea. The preva-lence and distribution of infection is associatedwith the presence of susceptible snail and fishintermediate hosts and habits of the indigenouspopulations. It has been suggested that close to25 million people are infected in Asia, mostly insouthern China and North Korea.

Epidemiology and Transmission

Infection by flukes in man occurs by eatingraw, undercooked, or poorly preserved infectedfish. In some areas where the parasite occurs,fish is eaten raw in thin slices with rice (congee).The eating of raw freshwater fish has becomeincreasingly popular in several Far Easterncountries, and consequently the prevalence ofhuman infection is increasing. Infections outsideof Asia are usually imported. In most endemicareas, cats and dogs are infected in high num-bers. Levels of infection are maintained by thepractice of fertilizing ponds used to raise fishwith human excrement.

Diagnosis is based on the identification of thecharacteristic eggs in fecal samples, which haveto be differentiated from other trematode eggssuch as Heterophyes heterophyes, Metagonimusyokogawi, Haplorchis taichui, and Opisthorchisspecies (Table 9-^). Several serologic tests havebeen developed, but most are nonspecific. A re-ported enzyme-linked immunosorbent assay(ELISA) may be of value.30

Prevention and Control

In endemic areas, treatment of all infectedpersons and improved sanitation would helpcontrol infection by flukes. In areas where fishare raised in ponds, human and animal fecesshould be composted or sterilized before theyare applied as fertilizer to ponds.

Thorough cooking of all freshwater fish is themost effective means of controlling infection byflukes. Clonorchiosis can be prevented by avoid-ing eating raw, undercooked or improperly pick-led, salted, dried, smoked, or fermented fish inendemic areas. There is little or no informationon conditions affecting the survivability of theencysted infective stages in fish flesh. Educationprojects are of some benefit, but the eating ofraw or fermented freshwater fish has been a

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