Parasitic food-borne and water-borne zoonoses · 2017-10-19 · Parasitic food-borne and...

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Rev. sci. tech. Off. int. Epiz., 2000,19 (1), 240-258 Parasitic food-borne and water-borne zoonoses C.N.L Macpherson(1). Gottstein (2) & S. Geerts (3) (1) Windward Islands Research and Education Foundation, St George's University, P.O. Box 7, St George's, Grenada, West Indies (2) University of Bern, Institute of Parasitology, Laenggass-Strasse 122, P.O. Box 8466, CH-3001 Berne, Switzerland (3) Institute of Tropical Medicine, Geneeskunde Prince Leopold, Nationalestraat 155,2000 Antwerp, Belgium Summary Estimates suggest that almost half of the population of the world is affected by water-borne and food-borne infections. Parasitic food-borne and water-borne zoonoses contribute to this statistic by inflicting a heavy toll on human health and causing serious direct and indirect losses to the agricultural industry. The inability of non-industrialised countries to keep pace with population growth, migration from rural to urban areas and the demand for clean, safe drinking water and proper sanitation means that water-borne zoonoses will continue to exact an increasing burden of ill health in these countries. The consumption of raw or undercooked meat, crustaceans, and fresh-water fish and vegetables facilitates transmission of large numbers of zoonotic infections. The burgeoning tourist industry, emigration and the importation of food from endemic regions has resulted in increasing diagnosis of these infections in non-endemic countries. The authors examine the epidemiology, medical and veterinary public health importance and recent developments in diagnosis, treatment and control of the most important parasitic food-borne and water-borne infections. Keywords Cestodes- Food-borne zoonoses - Nematodes - Parasites - Protozoa - Public health - Trematodes - Water-borne zoonoses - Zoonoses. Introduction The insidious nature of most food-borne and water-borne parasitic zoonoses, combined with the lack of collaboration between policy makers in the fields of human and animal health has resulted in the under-reporting of the economic and public health importance of zoonotic infections. Spectacular advances have been made in the areas of epidemiology, diagnosis, treatment, mathematical models and cost-benefit analysis. However, to make a practical difference, these advances must be combined with a clear understanding of human behaviour, cultural differences and socio-economic status (education, occupation and financial status) of individuals in different parts of the world. The low socio-economic status of non-industrialised countries in terms of medical, veterinary and diagnostic institutions, trained personnel and financial status, provides conditions for the proliferation of parasitic zoonoses. An overview of the distribution, clinical manifestations and public health importance of zoonotic protozoa and helminths is presented, along with current methods of diagnosis, treatment and control. Protozoa Toxoplasmosis Distribution and public health importance Toxoplasma gondii is possibly the most widespread and prevalent protozoan parasite on earth, infecting approximately half a billion people (26). The range of prevalence reported world-wide is great and may locally depend upon meat consumption habits and the population density of cats. In Europe, the seropositivity rate among adults varies between 10% and 80% and increases significantiy with age. In most countries of central Europe, the seroprevalence for women of child-bearing age ranges between 30% and

Transcript of Parasitic food-borne and water-borne zoonoses · 2017-10-19 · Parasitic food-borne and...

Rev. sci. tech. Off. int. Epiz., 2000,19 (1), 240-258

Parasitic food-borne and water-borne zoonoses C.N.L Macpherson(1). Gottstein ( 2 ) & S. Geerts ( 3 )

(1) Windward Islands Research and Education Foundation, St George's University, P.O. Box 7, St George's, Grenada, West Indies (2) University of Bern, Institute of Parasitology, Laenggass-Strasse 122, P.O. Box 8466, CH-3001 Berne, Switzerland (3) Institute of Tropical Medicine, Geneeskunde Prince Leopold, Nationalestraat 155,2000 Antwerp, Belgium

Summary Estimates suggest that almost half of the population of the world is affected by water-borne and food-borne infections. Parasitic food-borne and water-borne zoonoses contribute to this statistic by inflicting a heavy toll on human health and causing serious direct and indirect losses to the agricultural industry. The inability of non-industrialised countries to keep pace with population growth, migration from rural to urban areas and the demand for clean, safe drinking water and proper sanitation means that water-borne zoonoses will continue to exact an increasing burden of ill health in these countries. The consumption of raw or undercooked meat, crustaceans, and fresh-water fish and vegetables facilitates transmission of large numbers of zoonotic infections. The burgeoning tourist industry, emigration and the importation of food from endemic regions has resulted in increasing diagnosis of these infections in non-endemic countries. The authors examine the epidemiology, medical and veterinary public health importance and recent developments in diagnosis, treatment and control of the most important parasitic food-borne and water-borne infections.

Keywords Cestodes- Food-borne zoonoses - Nematodes - Parasites - Protozoa - Public health -Trematodes - Water-borne zoonoses - Zoonoses.

Introduction The insidious nature of mos t food-borne and water-borne parasitic zoonoses , c o m b i n e d with the l ack of col laborat ion b e t w e e n pol icy make r s in the fields of h u m a n and animal health has resulted in the under-reporting of the e c o n o m i c and public heal th importance of zoonot ic infections. Spectacular advances have b e e n m a d e in the areas of epidemiology, diagnosis, treatment, mathematical m o d e l s and cost-benefit analysis. However , to m a k e a practical difference, these advances must b e c o m b i n e d with a clear understanding of h u m a n behaviour, cultural differences and soc io -economic status (education, occupat ion and financial status) of individuals in different parts of the world . T h e l o w soc io -economic status of non-industrialised countries in terms of medical , veterinary and diagnostic institutions, trained personnel and financial status, provides condit ions for the proliferation of parasitic zoonoses .

An overview of the distribution, clinical manifestations and public heal th importance of zoonot ic p ro tozoa and helminths is presented, along with current m e t h o d s of diagnosis, treatment and control.

Protozoa Toxoplasmosis Distribution and public heal th impor tance Toxoplasma gondii is possibly the mos t widespread and prevalent p ro tozoan parasite o n earth, infecting approximately half a bi l l ion p e o p l e (26) . T h e range of prevalence reported world-wide is great and may locally d e p e n d u p o n mea t consumpt ion habits and the population density of cats. In Europe, the seropositivity rate among adults varies b e t w e e n 10% and 80% and increases significantiy with age. In mos t countries of central Europe, the seroprevalence for w o m e n of child-bearing age ranges b e t w e e n 30% and

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45%. Similar rates have b e e n reported f rom the United States of America (USA) and other continents (26). A m o n g animals, seroprevalence has b e e n repor ted to b e h igh in mos t l ivestock species, a l though infectious parasites have only b e e n demonstrated, at relatively h igh prevalences, in small ruminants and pigs. Beef is generally not cons idered to b e an important source of infection for humans (18, 20) . In the USA, serological surveys of cats, the definitive host , revealed that 2 5 % of h o u s e cats were seropositive for T. gondii antibodies (21) . T h e prevalence of active shedding of oocysts by cats at any given t ime is less than 2 % (21) .

Parasite biology, l i fe -cycle and epidemiology

Toxoplasma gondii is a parasite of domest ic and wild cats that potentially is capable of infecting all vertebrates (21). Cats b e c o m e infected f rom three sources, namely: b y ingesting tissues f rom animals harbouring cysts of T. gondii that contain the s low-developing organisms called bradyzoites; b y ingesting tissues f rom acutely infected animals with rapidly developing tachyzoites; and b y ingesting oocysts s h e d in the faeces of o ther cats (17). After ingestion, T. gondii enters the feline intestinal epi thel ium in w h i c h the parasite deve lops , first through asexual stages or, under certain condit ions, direcdy to the sexual stages. After fertilisation, zygotes deve lop into oocysts w h i c h enter the l u m e n of the intestine and are shed, unsporulated, in the faeces. T h e t ime f rom ingestion of cysts until shedding of oocysts is three to ten days and shedding usually lasts f rom seven to twenty-one days. Oocysts are not infectious immediate ly after shedding, but require exposure to air at r o o m temperature for approximately two days. Sporulated oocysts contain two sporocysts, e a c h of which contains four sporozoi tes . Cats can repeat oocyst shedding after reinfection, al though the number shed is far less than during the primary infection (21) .

Infection of a non-feline hos t with either oocysts or tissue cysts will a l low tachyzoites to undergo repeated, rapid multiplication b y a p rocess called endodyogeny , until, influenced b y the i m m u n e system of the host , the multiplication rate s lows and the tachyzoites transform into bradyzoites. These b e c o m e surrounded b y a cyst wall and remain dormant but infectious in the tissue for long per iods of time, somet imes for the life of the host . Bradyzoites transform b a c k into tachyzoites w h e n the cysts are ingested b y another host or w h e n the i m m u n e system of the current hos t is suppressed b y malnutrition, disease, or medicat ion.

Toxoplasmosis can b e transmitted to humans via several routes. Although a major source of infection is thought to result from contamination of the environment with oocysts shed in cat faeces, the extent of h u m a n infection resulting from this route is not k n o w n . Faeces are depos i ted in gardens, fields, lawns, pastures, playgrounds and any other locat ion available to cats. T h e oocysts measure only 10 µm to 12 µm in diameter and are dispersed easily b y wind, water, s h o e s and feet of humans or animals and numerous other routes.

Oocysts can remain infectious for a year or m o r e if protec ted from temperature extremes, intense sunlight and desiccation.

Transmission of T. gondii b y ingestion of tissue cysts in raw or u n d e r c o o k e d mea t from a variety of l ivestock and game animals has b e e n d o c u m e n t e d as another major source of h u m a n infection (21) . Specific cultural preferences for u n d e r c o o k e d or raw mea t inevitably result in a higher prevalence of infection. In France, 2 0 4 chi ldren b e c a m e infected after be ing hospital ised and fed meals of very rare or raw meat (14) . T h e risks presented b y general association wi th meat are less clear; abattoir workers in Egypt and Ghana were not found to b e at h igher risk of acquiring T. gondii than the general popula t ion, whereas abattoir workers , butchers , and mea t inspectors in J a p a n and Brazil were found to b e at higher risk (26) . Water -borne transmission of T. gondii oocysts has b e e n d o c u m e n t e d rarely and m a y not b e epidemiological ly significant.

Pathogenes is and cl inical f ea tu res

Initial clinical signs of toxoplasmosis are usually characterised b y non-specific and variable symptoms resembling those of influenza. Acute infections include dermatomyosit is , encephalitis, enteritis, hepatitis, lymphadenit is , myocarditis , placentitis, pneumonit is , retinochoroiditis, skeletal myositis, tenosynovitis, tonsillitis, vasculitis, anaemia and fever (26) . T h e pe r iod of incubation is quite variable; in mos t cases, clinical signs are manifested a few days to a few w e e k s after exposure . Duration and severity is very l imi ted among immunocompe ten t persons. In patients wi th cancer or acquired i m m u n e deficiency syndrome (AIDS), infections of long duration, fo l lowed b y death, m a y occur. A risk group of special interest is non- immune pregnant w o m e n . In Europe, congenital toxoplasmosis is repor ted in approximately 0 . 1 % to 0 .2% of pregnancies w h e r e the mothe r is seronegative prior to or during early pregnancy (23) . Approximately 2 5 % of the foetuses will exhibit pathologically distinct manifestations, for example , cerebral malformations or severe retinochoroiditis. T h e remaining 75% will exhibit sub-clinical forms of infection, w h i c h may exhibit post-natal manifestations such as chorioretinitis or mental retardation. In general, the earlier in pregnancy infection is acquired, the greater the extent of lesions in the foetus will b e .

Diagnosis

In humans and animals, direct diagnosis is b a s e d o n medica l history, tissue sections, tissue b iops ies , fluid aspirates, or other diagnostic substrates that m a y contain T. gondii organisms. T h e detect ion of parasites can b e pe r fo rmed using

•microscopical, histological or immunohis tochemica l procedures . As parasites can b e few in number , these approaches have l o w sensitivity. Alternatively, diagnostic amplification of T. gondii deoxyribonucleic acid (DNA) b y the polymerase chain reaction (PCR) has b e e n used successfully in investigations of the parasite in b o t h humans and animals (5, 58) .

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Serological tests include, among others, direct agglutination tests, the Sabin-Feldmann dye test, the indirect fluorescent ant ibody test and the enzyme- l inked immunosorbent assay (ELISA). Agglutination tests and ELISA are available commercial ly, the latter is offered to detect immunoglobul in (Ig) M, IgG and IgA and even to assess the avidity of the ant ibody binding reactivity in order to discriminate b e t w e e n recent (acute) and o ld infections. In veterinary parasitology, serological tests can only indicate that an animal has b e e n exposed to T. gondii or is currendy infected. Avidity tests to determine recent infections are under development .

Serology is unreliable for diagnosis of infection in animals or meat . Diagnosis is poss ib le if the diagnostic material is inoculated into mice or fed to cats, with a subsequent demonstrat ion of infection in these animals. T o c o n f i r m transmission of organisms from suspect tissues, tachyzoites can b e detected in m o u s e peritoneal exudate after four to six days and possibly only after four w e e k s post inoculation. Toxoplasma gondii antibodies can b e found in the mice two to three w e e k s after inoculation, and cysts will b e present in the brain one m o n t h after inoculation. Oocysts can b e s h e d in cat faeces a few days or later after potential infection.

Treatment , prevent ion and control Chemotherapeut ic treatment for toxoplasmosis in humans has b e e n reviewed (36). Pyrimethamine with su lphonamides acts synergistically against the rapidly dividing tachyzoite stage and is the treatment of cho ice in many countries. Spiramycin and clindamycin, macrol ide antibiotics, are also reported to b e effective treatments. All these c o m p o u n d s have serious side-effects and must b e used with caution. In cats, monens in and toltrazuril appeared effective against the intestinal developmental stages of T. gondii, the latter drug also affects the extraintestinal stages.

Measures that reduce or eliminate contamination of the environment with oocysts from cat faeces will h e l p prevent toxoplasmosis (26). Cats should b e prevented from hunting birds and rodents, and should b e fed thoroughly c o o k e d , dry or canned food. Litter pans shou ld b e used in the h o m e and empt ied daily. Sandboxes for chi ldren should b e covered w h e n not in use and gardeners handling soil shou ld wear gloves and wash their hands thoroughly before eating or handling food . On the farm, b a m s , stalls, feed bunkers , waterers and other areas should b e k e p t free of cat faeces.

All meat should b e c o o k e d thoroughly be fo re eating. Extensive studies have b e e n conduc ted that demonstrate thermal death curves for cook ing meat , and indicate the necessary combinat ion of time versus temperature for rendering T. gondii non-infectious; 60°C or higher as minimal core temperature in meat; freezing (—15°C or lower) or gamma-irradiation (0.5 kGy) are other effective measures .

Vaccination of cats has exhibi ted 8 5 % efficacy using the mutant strain T-263 (19), and vaccination of s h e e p with the

commerc ia l live vaccine strain S-48 inhibits abort ion but does not comple te ly prevent cyst formation in infection-challenged animals.

Sarcocystiosis Sarcocystis spp . , l ike T. gondii, are cocc id ian protozoans w h i c h have a global distribution. T h e life-cycle is heter ixenous with herbivores (domest ic and wild) primarily acting as intermediate hosts, containing zoitocysts (formerly k n o w n as sarcocysts), and carnivores (domest ic and wild), including humans , serving as definitive hosts . Numerous species of Sarcocystis infect cattle, s h e e p , pigs, horses , camels, buffalo and wild game animals. Heavy infections in these intermediate hosts m a y cause abort ion, anorexia, fever, anaemia and reduced live weight gain. T w o species are recognised as zoonot ic , namely: S. hominis and S. suihominis, al though zoitocysts of u n k n o w n origin have also b e e n found in humans (87). T h e publ ic heal th implications of this are u n k n o w n but m a y indicate that the genus is a m u c h more important zoonosis than is currendy appreciated. Humans acquire S. hominis b y consumpt ion of u n c o o k e d beef containing zoitocysts. Sarcocystis hominis is only mildly pathogenic in humans , causing s tomach pains, nausea and diarrhoea, Sporocysts beg in to b e passed in the faeces after 14 to 18 days (11 to 13 days after infection with S. suihominis). Sarcocystis suihominis is acquired b y eating zoitocysts in u n d e r c o o k e d p o r k . Sarcocystis suihominis is m o r e pathogenic than S. hominis, causing s tomach pains, nausea, diarrhoea and dyspnoea within 24 hours of infection. N o effective treatment is available for either intermediate or definitive hosts . Control is possible b y avoiding eating u n d e r c o o k e d meat .

Giardiosis Distribution and public health impor tance Various genetic variants of Giardia infect humans and animals world-wide. In 1976, a survey in the USA repor ted Giardia in 3.8% of nearly 415 ,000 p e o p l e . In 1980, the parasite was found to infect from 2 % to 20% of p e o p l e in the USA (depending o n the popula t ion sampled) (11). Transmission of giardiosis f rom animals to humans remains controversial. The close association b e t w e e n humans and c o m p a n i o n animals provides opportunities for transmission. In central Europe, h igh rates of cyst excretion have b e e n reported in pet animals, including dogs (0 .5%-18%) and cats (2%-5%) and in l ivestock, including calves (27%) and l ambs (30%) (79). Untreated surface water in unpopula ted areas m a y be contaminated through reservoir hosts, including beavers (Castor fiber), racoons (Procyon lotor), muskrats (Ondatra zibethica), mouff lon (Ovis musimon) and other species (26). Evidence for direct zoonot ic transmission and the ability to attribute outbreaks to specific host species d e p e n d upon markers to identify and distinguish Giardia f rom wild animal, domest icated animal, and h u m a n sources (41).

Parasi te biology, l i fe-cycle and epidemiology Giardia intestinalis (synonyms: Giardia duodenalis, Giardia lamblia) is a flagellate exhibiting a very s imple and direct

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life-cycle. After ingestion of Giardia cysts, e a c h of w h i c h harbour two identical parasite t rophozoites , the cysts pass through the d u o d e n u m and then the organisms leave the cyst and undergo binary fission to form n e w trophozoites that continue to proliferate and establish infection in the host. The bi-nucleate, mot i le feeding stage, the t rophozoi te , attaches to the epi thel ium in the uppe r part of the small intestine b y a ventral, d isk- l ike organelle. Trophozoi tes swept into the lumen undergo mitotic division or transform into the cyst stage that passes f rom the host in faeces. Morphologically, the trophozoite has a face-l ike or pear - shaped appearance and, when v iewed with the narrow end down , the paired nuclei l o o k l ike eyes , the anterior flagella l o o p above the nuclei appears l ike eyebrows , and the m e d i a n b o d y resembles a down-turned m o u t h (26) . Trophozoi tes measure from 9 µm to 21 µm in length and from 5 µm to 15 µm in width. Giardia cysts have a visible bu t no t p rominent wall, are ellipsoidal, contain four nuclei and paired axonemes , and measure approximately 8 µm to 12 µm in length b y 7 µm to 10 µm in width. Transmission of the dormant, environmentally resistant cyst stage is via the faecal-oral route, indirecdy through contaminated water or food , or b y direct person-to-person contact. Cysts can remain infectious for several mon ths under mois t and c o o l conditions, but lose infectivity rapidly under dry, h o t condit ions. Conventional decontamination of drinking water using chlorine is ineffective against Giardia cysts. Giardia has b e e n identified more often than any other pa thogen in water-borne disease outbreaks in the USA (26) . Most outbreaks have occurred in water systems of small communit ies . Infrastructures at r isk include water supplies in campsites, parks , resorts and institutions, or individual water systems, including non-potable sources. Infection c a n also fol low ingestion of water whi le swimming or diving. A seasonal trend, especially during the summer , implies either increased contamination of non-community water supplies or use b y greater number s of susceptible persons . Most cases have b e e n attributed to contaminated surface water bu t a few represent contamination b y groundwater. F o o d - b o m e transmission of Giardia due to faecal contamination m a y occur through contaminated vegetables or salads, a l though this s e e m s to play a minor role in the ep idemio logy of giardiosis in humans (26) .

Pathogenesis and cl inical f e a t u r e s

Initial signs of illness associated with giardiosis include nausea, anorexia, discomfort in the uppe r intestine and fatigue. This is fo l lowed b y bursts of foul-smelling watery diarrhoea, flatulence and abdomina l distension, usually lasting only a few days. Occasionally, this acute stage can last for months , causing malabsorpt ion, weight loss, and debilitation (26) . Chronic infection is m a r k e d b y recurrent brief ep i sodes , or to a lesser extent, persistent ep i sodes of foul-smelling loose stools, flatulence and abdomina l distension. Lactose intolerance, c o m m o n during active infection, m a y persist for a per iod thereafter. Mortality has b e e n repor ted very rarely.

Diagnosis

Diarrhoea caused b y giardiosis must b e differentiated f rom other entero-pathogenic agents b y diagnosis. S o m e clinical indications for giardiosis are p rov ided b y the p resence of upper -abdomina l cramps, abdomina l distension, flatulence, steatorrhoea and foul-smelling faeces and b y the absence of b l o o d and mucus in the faeces. Traditionally, diagnosis is based o n identification of cysts or, less frequendy, t rophozoi tes i n faeces, or t rophozoi tes in duodena l aspirates or b iopsies . Most diagnoses can b e pe r fo rmed b y s tool examination. Fresh stools must b e examined immediately b y wet smear or preserved in buffered formalin solutions such as sodium-acetate-formalin (SAF) or merthiolate- iodine-formalin (MIF). At least three stools co l lec ted o n alternate days should b e examined before other diagnostic procedures are at tempted. W h e n organisms in faecal smears are absent, zinc sulphate solution shou ld b e used for flotation and concentration; sugar and other salts should not b e used b e c a u s e these distort the parasite, rendering it unrecognisable (26). W h e n Giardia cannot b e detected in stools of suspected cases, duodena l or jejunal fluid shou ld b e obta ined and examined b y duodena l tube, e n d o s c o p e , or duodena l content sampling b y the duodena l s t img-capsule-technique (Entero-Test). These traditional diagnostic m e t h o d s either l ack method ica l sensitivity, are difficult to perform, or involve invasive procedures , and h e n c e complementary immunological m e t h o d s have b e e n deve loped to support diagnosis. Serodiagnosis, b y detect ion of anti-Giardia antibodies is not appropriate. Conversely, immunodiagnost ic detect ion of Giardia-antigen, including immunodiffusion, immunof luorescence , counterirnmunoelectrophoresis and ELISA, has s h o w n great value and has resulted in a large commerc ia l marke t for rapid and reliable tests (80). In endemic non-industrialised countries where stool mic roscopy m a y provide the only diagnostic opt ion, a therapeutic trial m a y b e justified w h e n clinical symptoms suggest Giardia infection but repeated s tool samples remain negative.

Detection of Giardia cysts in water presents special logistical difficulties, as samples of 100 to 1,000 litres are usually used. Methodically highly sensitive techniques, such as PCR or fluorescence-activated-cell-sorting (FACS), are used for this application.

Treatment , prevent ion and control

T h e treatment of cho ice for humans varies according to country, due to differences in approved drugs. Generally, giardiosis is treated wi th nitroimidazoles (such as metronidazole, ornidazole or tinidazole) or a lbendazole . Furazolidone has b e e n r e c o m m e n d e d for children. Paromomycin has b e e n p r o p o s e d for treatment of. pregnant w o m e n . In domest ic animals, especially in dogs , the drugs u s e d are the same as for humans , excep t that fenbendazole has b e e n demonstrated to b e highly effective in dogs (but not other animals). Indication for treatment is usually restricted to

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symptomatic c o m p a n i o n animals. Symptomatic infections in l ivestock are rare and are usually self-limiting and self-healing. The mos t important measures to prevent giardiosis are personal hygiene, p roper sanitary infrastructures, and appropriate treatment of drinking water. Given the potential for virtually all surface water to b e e x p o s e d to Giardia contamination f rom h u m a n or animal sources, caution dictates that all cysts of Giardia b e regarded as potentially infective for humans . Specific guidelines, r ecommendat ions and regulations for controlling water-borne Giardia have b e e n deve loped or p r o p o s e d by various national and international organisations (26).

Cryptosporidiosis Of the eight recognised species of Cryptosporidium, all of w h i c h infect vertebrates, only one , C. parvum, is zoonotic . This species is remarkable within the genus for a l ack of hos t specificity; in addit ion to humans , infection has b e e n reported in seventy-nine species of mammals . Discovered b y Tyzeret in 1907 in asymptomatic laboratory mice , the parasite was thought to b e non-pathogenic for three-quarters of a century. T h e economic importance of the parasite b e c a m e apparent to the agricultural world w h e n an outbreak of severe diarrhoea was reported in 1955 in turkeys and a similar p r o b l e m was reported in calves in 1971 . Since then, the parasite has b e e n associated with outbreaks of diarrhoea in the young of cattle, sheep , goats, deer, horses , dogs , cats and turkeys. T h e first case of C. parvum in a h u m a n was reported in 1976, and only seven cases were repor ted prior to 1982. An increasing incidence has since b e e n reported, mainly in i m m u n o c o m p r o m i s e d patients with AIDS, in w h o m the infection is life threatening. Cryptosporidium parvum has b e e n demonstrated to b e responsible for sporadic outbreaks of water-borne illness in immunocompe ten t individuals, s o m e of wh ich have involved many thousands of p e o p l e .

Distribution, public health impor tance and epidemiology

In the 1990s, the number of reports of C. parvum infections has increased dramatically, including infection in i m m u n o c o m p r o m i s e d individuals and immunocompe ten t children and adults from all over the world, thereby reaffirming the global distribution of the parasite. During this period, over twenty water-borne ep idemics have b e e n reported from a number of deve loped countries, including the USA, Canada, England, Scotland and J apan (77). Many of the outbreaks involved small numbers of p e o p l e infected after contamination of swimming poo l s . Four ep idemics involved many thousands of individuals and resulted from contamination of municipal water supplies. T h e largest of these occurred in Milwaukee, in the USA, in the spring of 1993, w h e n 403 ,000 cases were reported (56) . T h e ep idemic completely ove rwhe lmed the publ ic heal th system: 44 ,000 p e o p l e sought medica l care and over 4 ,000 were hospitalised. Oocyst densities of 0.13 per litre were found in water suppl ied b y the Milwaukee treatment plant, al though the source of the

parasite remains speculative. Cattle, a slaughterhouse and h u m a n sewage were all suspected. Genetic analysis of recovered isolates has traced mos t outbreaks among humans to h u m a n infection sources; animals have rarely b e e n determined as infection sources for humans .

In immunocompe ten t individuals, the parasite is an important contributor to diarrhoea in children, with a reported prevalence of b e t w e e n 1% and 3 % in industrialised countries and b e t w e e n 4% and 17% in developing countries. Diarrhoea due to C. parvum has b e e n reported to cause mortality in infants less than one year of age, at a rate of 2.9% in Guinea-Bissau. Traveller's diarrhoea m a y also result from infection with this organism.

T h e average prevalence of C. parvum in patients with human immunodef ic iency virus (HIV) has b e e n reported to b e 27% in developing countries and 1 2 % in industrialised countries (25) . T h e life-threatening potential of C. parvum infections in i m m u n o c o m p r o m i s e d and immunosuppressed individuals has greatly enhanced the importance of cryptosporidiosis as a global public heal th p r o b l e m , al though recently, the incidence of the disease s eems to have decreased in industrialised countries, due to the introduction of triple-therapy.

Domestic animals, particularly young animals, are frequently infected and the associated symptoms cause e c o n o m i c losses to farmers. T h e role of animals in the infection of humans , and vice versa, remains unclear, but, according to genetic analyses of recovered isolates, should not b e overestimated. Sewage waste and agricultural and urban run-off have b e e n recognised as sources of water contamination. Veterinarians and animal handlers have an increased risk of contracting cryptosporidiosis.

Parasi te biology and l i fe -cycle

Transmission of C. parvum occurs via oocysts w h i c h are immediately infective w h e n passed, and may b e transmitted b y water-borne or faeco-oral routes. Water-borne epidemics are facilitated by the ability of the oocyst to withstand standard water treatments (chlorination and sand filtration) and to remain viable for long per iods in the environment. Infected hosts may shed as many as 1 0 1 0 oocysts daily. In an infected individual, b o t h th ick and thin walled oocysts m a y b e p roduced . T h e former are thought to b e responsible for transmission b e t w e e n hosts and the latter ha tch in the same hos t and are responsible for autoinfection. Once oocysts are ingested, the four sporozoi tes contained within are released in the small intestine and then immediately attach to enterocytes and b e c o m e t rophozoi tes in this intracellular but extra-cytoplasmic location. T h e t rophozoi tes b e c o m e schizonts containing merozoi tes . On release, merozoi tes may b e c o m e mic ro - or macro-gametocytes , the union of w h i c h produces a zygote w h i c h transforms into an unsporulated oocyst. In i m m u n o c o m p r o m i s e d hosts , the cycle is repeated

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continuously, whilst in i m m u n o c o m p e t e n t individuals, the cycle is self-hmiting.

Pathogenesis and cl inical f ea tu res Approximately one w e e k after ingestion of oocysts b y humans, a wide range of clinical manifestations of cryptosporidiosis are exper ienced, depending o n the age and immune status of the host . Infection with C. parvum may result in malabsorptive or secretory diarrhoea. Immunocompeten t individuals present wi th a range of symptoms w h i c h can start with abdomina l cramps, nausea, low-grade fever and anorexia. Stools are offensive, l oose to watery and are typically a brown-green colour with mucus but n o b l o o d or pus. T h e duration of symptoms is from o n e day to eight w e e k s . Stool frequency is from two to ten times per day. In i m m u n o c o m p r o m i s e d individuals, the clinical manifestations are variable: f rom asymptomatic transient infections to fulminating diarrhoea, u p to three litres a day, with vomiting and abdomina l cramps. In patients with AIDS, oocysts have also b e e n found in the biliary tract w h i c h m a y cause a sclerosing cholangiotis w h i c h may present clinically as a progressive right uppe r quadrant abdomina l pain.

Diagnosis Despite be ing relatively insensitive, detect ion of oocysts in stools b y mic roscopy remains the principal m e t h o d of diagnosis. Various staining techniques can b e emp loyed , the most widely used be ing the modi f ied Ziehl-Neelsen technique. Detection of antigen in faeces using ELISA has provided g o o d sensitivity and specificity. Polymerase chain reaction assays to detect DNA in stool samples or b iops ies have not yet b e e n appl ied in a routine clinical setting. Tools to detect C. parvum in water samples are similar to those offered for G intestinalis (see above) , and include mainly FACS and PCR.

Treatment , prevent ion and control No effective treatment or vaccine is available. Patients at h igh risk of severe cryptosporidiosis are advised to bo i l and/or filter (< 2 µm po re size) all drinking water and not to swim in public baths . W h e r e c o m p a n i o n animal p rogrammes are used for AIDS patients, the animals should also b e prov ided bo i l ed or-filtered drinking water. T h e inability of water treatment systems to control the parasite will contribute to the public health importance of cryptosporidiosis until modifications render water treatment systems m o r e effective. In Milwaukee, and in other large cities in the USA, municipal water treatment n o w includes ozonat ion of the water wh ich destroys C. parvum oocysts.

Trematodes Fasciolosis (distomatosis) Distribution and public heal th impor tance Fasciola hepatica, the c o m m o n liver fluke, affects predominandy ruminants and occurs throughout mos t

temperate regions of the world . In veterinary medic ine , the organism m a y b e a significant heal th p r o b l e m and can cause h igh e c o n o m i c losses through disease and diminution of product ion. Humans are rarely affected, al though the W o r l d Health Organization estimates that 2.4 mil l ion p e o p l e are infected wor ld-wide (89) . T h e annual incidence in Europe is estimated to b e a few cases pe r year and per country. W h i l e mos t infected p e o p l e have eaten wild watercress or other freshwater-raised plants, infective metacercariae may, in s o m e cases, b e acquired directly through drinking water. Other fasciolid flukes may also occasionally infect humans , but are cons idered to b e of minor importance.

Parasi te biology, l i fe -cycle and ep idemio logy Fasciola hepatica is a flatworm of 2 c m to 5 c m in length which , as an adult fluke, parasitises the bi le ducts. Immature eggs are s h e d in faeces and under optimal conditions, a miracidium will deve lop in, and then subsequendy b e released from, the egg. This larva will deve lop and multiply asexually in mol luscan intermediate hosts (e.g. Lymnaea truncatula in Europe) . Released cercariae adhere p redominandy to water plants w h e r e they mature to infective metacercariae. Ingestion of metacercariae will b e fo l lowed b y the release of juvenile flukes w h i c h penetrate through the intestine to reach the liver, via the peri toneal cavity. T h e juvenile flukes migrate through the liver parenchyma for six or seven w e e k s to finally reach the bi le ducts. Here the flukes mature and egg product ion c o m m e n c e s as early as two or three mon ths post infection.

Pathogenesis and cl inical f ea tu res Disease presentation is related to the intensity of exposure and stage and duration of infection. Most cases remain sub-clinical, but w h e n symptoms occur, these usually are related to the hepatobiliary system. Occasionally, aberrant migration of immature flukes leads to unusual ectopic manifestations. Heavy infections m a y result in traumatic hepatitis w h e n juveniles occur in the liver parenchyma.

Diagnosis In established infections, fasciolosis can b e diagnosed b y detecting parasite eggs in the faeces. If eggs are absent, such as in the early, tissue-invasive stage, or in exclusively ectopic disease, serology may b e useful (71). Blood eosinophil ia supports the diagnosis, but is not always present. Non-invasive imaging techniques may he lp to establish the extent of liver damage, but d o not specifically confirm the diagnosis (37). Biopsy of ectopic lesions provides a definitive diagnosis. Very occasionally, eggs appear in faeces as a result of gastro-intestinal passage in individuals w h o have consumed infected s h e e p liver.

Treatment , prevent ion and control According to preliminary veterinary clinical data and studies in ruminants, the mos t effective and least toxic drug for the treatment of fasciolosis is triclabendazole, given in a single dose of 10 mg /kg b o d y weight (91). Praziquantel has not

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proved effective in treating fasciolosis. In ectopic disease, surgery, if indicated, is b o t h diagnostic and curative; chemothe rapy is not useful. In terms of prophylactic control, consumpt ion of raw leaf vegetables and possibly contaminated water shou ld b e avoided, especially if obtained from p o n d s or streams in fields e x p o s e d to s h e e p and catde faeces.

Clonorchiosis and opisthorchiosis Clonorchis sinensis, Opisthorchis viverrini and 0. felineus, the h u m a n l i v e r flukes, are parasites of fish-eating mammals , particularly in Asia and Europe w h e r e m o r e than 20 mill ion p e o p l e are infected. In highly endemic areas, such as north-east Thailand, the prevalence of 0. viverrini may reach up to 90% (6). Clonorchis sinensis is highly prevalent in the People 's Republic of China, Taipei China and Vietnam and still occurs in J apan and the Korean peninsula. T h e main animal hosts are cats, dogs, pigs, rats and camels . Opisthorchis felineus is prevalent in Poland, eastern Germany and in parts of the former Union of Soviet Socialist. Republics. T h e adult flukes live in the bi le ducts and may occur in large numbers . Large f lask-shaped operculated eggs are shed in faeces and hatch if ingested by the appropriate intermediate snail host . Cercariae are shed w h i c h penetrate the sk in of fish of the family Cyprinidae, and eventually encyst in the muscles of these fish. Infection occurs through eating u n d e r c o o k e d or raw fish and the metacercariae reach the l i v e r b y direct migration u p the bi le duct. Raw fish dishes are a dietary habit in all countries where these flukes are c o m m o n l y found. Clinical manifestations are rare, but infection increases the risk of cholangiocarcinoma (39) . Control is possible through treatment with praziquantel, sanitation measures and educat ion to discourage consumpt ion of raw fish.

Heterophyosis Heterophyes heterophyes and Metagonimus yokogawai are probably the two mos t important of numerous different species of small (usually under 2.5 m m in length), zoonot ic intestinal flukes found in mammal s and birds w h i c h ingest encysted metacercariae in raw or u n d e r c o o k e d fish. These flukes common ly occur in Japan , Laos , Thailand, the Republic of Korea, Hawaii, the Balkans, the Philippines, the People 's Republic of China, Taipei China, Turkey and Siberia. The life-cycle is similar to that of Clonorchis and Opisthorchis spp . and the operculated eggs passed in faeces are morphological ly very similar. Clinical manifestations are rare and, if present, are usually due to eggs t rapped in various tissues (84) . Treatment and control are similar to other fish-borne t rematodes .

Paragonimosis Paragonimosis results from infection b y numerous species of lung-dwelling flukes. Over 20 mil l ion p e o p l e are infected world-wide. T h e species involved include Paragonimus westermani (the main species in the Far East), P. miyazakii, P. skryjabini and P. heterotrema in Asia, P. africanus and P. uterobilateralis in Africa and P. mexicanus and other species

in Latin America. Countries with significant number s of cases include the People 's Republic of China, Taipei China, Thailand, Japan , Nigeria, Cameroon , Peru and Ecuador. Numerous species of mammal s m a y act as definitive hosts, including dogs , cats and wild carnivores. Aquatic snails are the first intermediate hos t f rom wh ich cercariae are released, subsequently infecting crabs, crayfish or shr imp. Definitive hosts are infected b y eating raw or u n d e r c o o k e d encysted metacercariae w h i c h occur in these species . Infection m a y also occur w h e n paratenic hosts , such as wild boa r are consumed . Pulmonary infection is characterised b y a chronic productive cough and chest pain. T h e clinical signs, w h e n c o m b i n e d with an appropriate history, are relatively pa thognomonic ; other diagnostic measures may include detect ion of eggs in sputum or faeces and dot-ELISA tests. Plain radiographs are useful for detecting pulmonary masses . In addit ion to the lung, these flukes can b e found in the brain, giving rise to serious neurological symptoms. Most neurological infections have b e e n reported from the Far East, especially the Republic of Korea. Computer ised tomography (CT) scans are useful for disclosing brain lesions. Control measeres include educat ion and treatment using praziquantel.

Echinostomosis These t rematodes are of minor zoonot ic importance but a h igh prevalence has b e e n repor ted in endemic countries, such as the Republic of Korea , the Philippines, Indonesia, Malaysia and Thailand. T h e mos t prevalent species include Echinostoma ilocanum, E. revolutum, E. malayanum, E. echinatum and E. hortense (42). Human infection is by ingestion of metacercariae encysted in freshwater snails and fish. Heavy infections m a y result in diarrhoea, anorexia and abdomina l discomfort. T h e eggs are similar to Fasciola and Fasciolopsis. For control, recourse is m a d e to educat ion and treatment using praziquantel.

Cestodes Taeniosis and cysticercosis Distribution and public health impor tance Taenia solium and T. saginata have cosmopol i tan distributions with the former being m o r e widespread in the rural areas of Latin America, Africa and Asia. Prevalence and incidence data among humans is lacking, as the species are often not identified. In general, the prevalence of Taenia spp . is low, even in (hyper) endemic areas in Latin America (0 .2% to 2.8%) (76).

Bovine and porc ine cysticercosis are reported world-wide. Although the official figures for T. saginata cysticercosis in Western Europe vary b e t w e e n 0 .2% and 2 % , detailed examination of the heads and hearts of cattle revealed that approximately 10% are infected with cysticerci (30) . Bovine cysticercosis remains very c o m m o n in East Africa, whereas h igh prevalences of porc ine cysticercosis are reported from Latin America and s o m e regions of Africa and Asia (30, 76).

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The publ ic heal th impor tance of T. solium cysticercosis has b e e n seriously underest imated in many regions of the wor ld (82). Wor ld -wide , the n u m b e r of deaths due to neurocysticercosis is estimated at approximately 50 ,000 (75). The ep idemic of cysticercosis in a communi ty of o r thodox Jews in Los Angeles has highlighted the risk of T. solium for those living in non-endemic areas (76) .

Parasite biology, l i fe -cycle and epidemiology In addit ion to Taenia saginata and Taenia solium, a n e w species of Taenia has b e e n discovered in Asia w h i c h is considered b y s o m e as a separate species , Taenia asiatica, and by others as a subspecies of T. saginata, T. saginata asiatica (24). T h e cysticerci of this Taenia are. not present in the muscles, but deve lop essentially in the liver. T h e pig is the principal intermediate host , but cattle, goats and m o n k e y s can also harbour the cysticerci. People b e c o m e infected b y eating raw or u n d e r c o o k e d p o r k liver, w h i c h s e e m s to b e a fairly widespread habi t in s o m e areas of the region. W h e t h e r or not the eggs of the Asian Taenia are also infective for humans is still unclear, but available circumstantial evidence, and the fact that the eggs d id not deve lop in b a b o o n s , rather suggest that h u m a n cysticercosis due to this Taenia sp . is p robab ly not a concern. Molecular analyses have s h o w n that the Asian Taenia is distinct, but very closely related to T. saginata (55) .

In Latin America, the ep idemio logy of T. solium has b e e n studied intensively. Risk factors associated with higher levels of seropositivity for cysticercosis in humans inc luded l o w levels of sanitary infrastructure, personal hygiene, a history of taeniosis and an age of over twenty years (76) . Clustering of seropositive cases of cysticercosis in h o u s e h o l d s of p e o p l e with a history of, or current taeniosis, has also b e e n reported.

The ep idemio logy of T. saginata has received m u c h less attention than T. solium. In Denmark, case control studies of cattle with cysticercosis f rom lightiy or heavily infected farms were pe r fo rmed to examine sources of infection. T h e mos t important source of T. saginata eggs for lightly infected farms appeared to b e the use of effluent from sewage treatment plants as drinking water for the cattle, whereas the origin of infection in heavily infected farms was related to the use of sludge from septic tanks (47) .

Pathogenesis and cl inical f e a t u r e s Taenia saginata carriers m a y suffer from abdominal pain, nausea, weakness , loss of appetite or increased appetite, headache , constipation, dizziness, diarrhoea, anal pruritus and hyperexcitability. Similar symptoms have b e e n repor ted for T. solium. Taenia saginata proglottids are usually passed in or outside stools whereas T. solium proglottids are generally eliminated with the faeces. Thus, T. solium infections m a y go unnoticed.

In pigs and cattle, infection with cysticerci is generally asymptomatic. Only in massive infections have s o m e clinical symptoms b e e n descr ibed. Symptoms due to

neurocysticercosis in humans vary considerably according to the number and locat ion of cysticerci, the status of the Cysticercus (living or dead) and the immune response of the hos t (86). In m a n y patients, infection may remain asymptomatic despite long-term and even severe infections. T h e deve lopment of subcutaneous cysticerci s eems to b e less c o m m o n in Latin America than e lsewhere . Neurocysticercosis is cons idered to b e one of the mos t important causes of epilepsy, especially late-onset seizures, in developing countries. In severe cases it is an acute life-threatening disease, but m o r e often it is a long-lasting infection affecting the quality of life of the patient.

Diagnosis Taeniosis Important progress has b e e n achieved in the field of diagnosis b o t h of taeniosis and cysticercosis in the 1990s. T h e classical coprological techniques are recognised to l ack sensitivity for the detect ion of t apeworm ova in the faeces, unless repeated several times. T h e perianal swab technique is m o r e sensitive, certainly for T. saginata, but patients are often reluctant to undergo this k i n d of sampling. A commercia l ly available ELISA test allowing the detect ion of parasite antigens in stool samples has a h igh sensitivity and specificity, but is not able to distinguish b e t w e e n T. saginata and T. solium (1). Differentiation b e t w e e n the species is poss ible , however , using DNA p r o b e s or PCR assays (33) .

Bovine cysticercosis Compar i son of the efficacy of the classical meat inspection (incisions in the so-cal led predilect ion sites) with detailed examination of the carcass has s h o w n that only 10% to 20% of cysticercosis cases are detected at the abattoir (30) . As an alternative to these m e t h o d s , ant ibody detect ion techniques were deve loped . However, these serological tests were not able to reliably identify naturally infected animals, or to distinguish animals carrying living cysts from those harbouring dead ones . T h e latter could b e achieved b y monoc lona l ant ibody-based antigen detect ion ELISAs (4, 38) . These tests are highly specific and al low the detect ion of cattle harbouring a m i n i m u m of thirty to fifty cysts.

Porcine cysticercosis Classical meat or tongue inspection lacks sensitivity for the diagnosis of T. solium cysticercosis in pigs. T h e immunob lo t assay using purified glycoproteins of T. solium cysticerci has b e e n demonstrated to b e very sensitive and specific. Promising results have also b e e n obtained in ELISA using purified fractions of the cyst fluid or excretory-secretory products of T. solium cysticerci. T h e antigen detect ion ELISAs are also useful to detect pigs harbouring living cysticerci of T. solium or the Asian Taenia (4, 38) .

Human cysticercosis Contrasted CT and magnetic resonance imaging (MRI) are the techniques of cho ice to confirm neurocysticercosis. For mos t forms of the disease (with the except ion of mic ro -calcifications), the latter is m o r e sensitive and specific (76) .

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However , these sophisticated techniques are usually not available in rural areas where mos t cases of neurocysticercosis occur. Using purified glycoproteins of T. solium, a highly sensitive and specific immunoblot t ing technique has b e e n deve loped (81) . T h e test detects 9 8 % of the proven cases with two or m o r e cysts and is able to identify 60% to 8 0 % of the patients with only a single cyst. An ELISA using these antigens was s h o w n to b e as sensitive and specific as the immunoblot t ing (45). A monoc lona l ant ibody-based ELISA was able to detect circulating antigen in a h igh percentage of patients wi th neurocysticercosis o n the basis of serum or classical swine fever samples (4). T h e advantage of this test is that only active infections (with living cysts) are detected.

Treatment, prevention and control The eradication of taeniosis/cysticercosis, especially due to T. solium, is poss ib le for the following reasons:

- t apeworm infections in humans are the only source of infection for intermediate hosts

- domest ic animal intermediate host populat ions can b e managed to avoid infection

- n o significant wildlife reservoir exists

- effective treatment is available for tapeworms (75) .

Praziquantel or niclosamide remain the drugs of cho ice for all mtestinal Taenia infections. T h e poss ib le exacerbat ion of symptoms i n persons with concomitant neurocysticercosis suggests that use of niclosamid might b e preferable in e n d e m i c areas of cysticercosis.

Treatment of bovine or porc ine cysticercosis is poss ib le using antbelmintics at a higher dosage. T h e treatment of c h o i c e for 7. saginata cysticercosis in cattle is praziquantel at 50 mg /kg (preferably repeated twice) . This dosage kills all cysticerci, but several mon ths are required for the cysts to b e resorbed and disappear. Porcine cysticercosis can b e treated reliably with a single d o s e of oxfendazole (30 mg/kg), wh i ch offers the opportunity of including the treatment of cysticercotic pigs as a poss ib le intervention in any cysticercosis contro programme.

Albendazole and to a lesser extent, praziquantel, are cons idered the treatment of c h o i c e for cysticercosis in humans, especially w h e n steroid drugs are used simultaneously (86) . While a general decrease in the frequency of seizures was r e c o r d e d in patients w h o received anthelmintic therapy, many studies cannot b e interpreted correctly due to the l a c k of appropriate controls and patient selection b ias (86) . Doubt still remains as to whe the r the course of neurocysticercosis is modi f i ed b y anthelmintic treatment.

A recombinant vaccine h a s b e e n d e v e l o p e d w h i c h provides protect ion against T. saginata cysticercosis in m o r e than 9 9 % of the immunised animals (51) . Since T. solium oncospheres contain a protein, w h i c h is h o m o l o g o u s to the host-protective

18 kDa antigens in T. ovis and T. saginata, a vaccine against T. solium cysticercosis in pigs (and possibly humans) can b e expec ted in the near future.

Echinococcosis Echinococcosis is a group of infectious diseases caused b y the tapeworms of the genus Echinococcus. T w o species, E. granulosus, the causative organism of cystic echinococcosis (CE), and E. multilocularis, w h i c h causes alveolar ech inococcos is (AE) are of significant publ ic health importance. T w o additional species , E. vogeli and E. oligarthrus, rarely infect humans and are geographically limited to Central America and the northern region of South America.

Cystic echinococcosis Distribution and public health importance Infections wi th E. granulosus occur wor ld-wide . A so-called European form, primarily involving synanthropic hosts in the life-cycle, has a nearly cosmopol i tan distribution (67) . This form is related to major public heal th or e c o n o m i c problems in many rural areas of the world. Another form is prevalent in northern parts of the North American continent and Eurasia (67) . Globally, little data exist o n the overall prevalence of CE. Regions with g o o d documentat ion where a relatively high prevalence i n defined geographical areas has b e e n reported include the entire Mediterranean area, the semi-arid areas of East Africa (Kenya, Sudan, Ethiopia, Tanzania); large foci also exist in many countries in South America and parts of the People 's Republic of China.

T h e main economic losses in l ivestock occur in the families Bovidae, Suidae, Equidae and Camelidae and are due to condemnat ion of infected viscera, decreased l i v e weight gain and mi lk and w o o l product ion. Unfortunately, reliable data o n the economic repercussions for l ivestock product ion are lacking for all countries.

Parasite biology, life-cycle and epidemiology Echinococcus granulosus is a small t apeworm (7 m m in length), found in the small intestine of carnivores, predominantly dogs . Ungulates, and rarely s o m e other animals, and humans are intermediate hosts . In definitive hosts , sexual maturity of adult t apeworms is r eached within five to six w e e k s . Gravid proglottids, e a c h containing several hundreds of eggs, and eggs l iberated f rom disrupted proglottids are s h e d in faeces. Fol lowing ingestion of E granulosus eggs by susceptible intermediate hosts, a primary larva (the oncosphere ) ha tches from the egg and penetrates the intestinal epithelium into the lamina propria. T h e oncosphere is subsequently transported to primary target organs, such as the liver and lungs, and less frequently to other organs. At these sites, hydatid cyst maturation occurs, w h i c h m a y result in the formation of protoscoleces . Once ingested b y a definitive host , such protoscoleces g row into adult tapeworms.

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The route of transmission of eggs to humans is diverse; taeniid eggs in general are k n o w n to adhere to the fur of the definitive host. C lose contact wi th infected dogs creates r isk of infection (85). Defaecation sites of dogs in areas in w h i c h E. granulosus is prevalent are h igh risk, especially for chi ldren or any p e o p l e in contact with the contaminated soil. Secondary contamination of f o o d p r o d u c e d o n soil or w h i c h has b e e n putatively contaminated b y faeces of carnivores m a y b e a significant source of infection. Faecal contamination of drinking water m a y occur in areas w h e r e dogs have access to drinking water sources.

Pathogenesis and clinical features Cases of CE usually present with well-delineated spherical primary cysts (35) . Although variations occur geographically, approximately 6 5 % of cysts occur in the liver, 2 5 % in the lungs and the remainder c a n occur in a lmost any locat ion (35). Cysts cause pathological damages in, or dysfunction of, infected organs mainly b y the gradual process of space-occupying repression or displacement of vital organs, tissues or vessels. Cyst rupture may b e a cause of anaphylactic or acute inflammatory pathology. Clinical manifestations are primarily determined by the site, size and number of cysts. Success of surgical removal of hydatid cysts is variable, depending o n the facilities available. In countries with m o d e m medica l facilities, case-fatality rates are l ow , varying be tween 1% and 4 % for first surgical intervention cases (35). This mortality rate is m u c h higher in countries w h e r e operating and post-operative care facilities are not optimal. Under non-opt imal conditions, recurrence rates of over 15% have b e e n reported (due to the growth of pro toscoleces or other larval material be ing left in the patient during surgery and subsequendy developing into multiple cysts) (56). Secondary infections are usually multiple and result in a higher mortality rate. T h e public heal th importance is reflected mainly b y the n u m b e r of infected persons and their diminished functional capacity, the direct and indirect costs of hospitalisation and recovery from surgery, and any residual disability or clinical sequelae (74) . In highly endemic regions, fear of b e c o m i n g infected causes an immeasurable soc io -economic cost.

Diagnosis Diagnosis of E. granulosus infections in definitive hosts is based o n the recovery and identification of proglottids and the detection of the characteristic eggs. An important feature is that morpholog ica l speciat ion of Taenia spp . and £ granulosus eggs is not poss ible . More specific and sensitive diagnostic approaches for E. granulosus in carnivores include copro-antigen detect ion (13) , and species-specific egg identification b y monoc lona l antibodies (9), or m o r e recendy by PCR (12 , 13, 16). For the diagnosis of larval infections in humans, imaging procedures together with serology will yield the diagnosis. Ultrasonography (US) is the primary diagnostic procedure of c h o i c e (57) . False positive results can occur in up to 10% of cases due to misidentification of benign serous cysts and abscesses (35) . For the detect ion of extrahepatic

disease and volumetric fol low-up assessment, CT is the superior technique whilst MRI adds diagnostic benefit b y identifying changes of the intra- and extra-hepatic venous system. Ultrasonography is also useful in longitudinal studies, such as following u p treated patients w h e r e successfully treated cysts b e c o m e hyperechogen ic . Aspiration cytology appears particularly helpful in detecting pulmonary, renal and other non-hepat ic lesions for w h i c h imaging techniques and serology d o not provide appropriate diagnostic support .

Immunodiagnost ic tests for the detect ion of serum antibodies are used to support the clinical diagnosis of CE (35, 49 ) . T h e indirect haemagglutination tests and ELISA using E. granulosus hydat id fluid antigen are relatively sensitive for hepat ic cases (85%-98%) . For pulmonary cyst localisation, the diagnostic sensitivity is marked ly lower (50%-60%) , for multiple organs, localisation is very h igh (90%-100%) . These tests are usually used for a primary serological screening. Specificity is l o w with regard to other ces tode infection and relatively l o w for non-ces tode parasitoses. In order to increase specificity, primary seropositive sera are retested in a confirmation test such as antigen-5-precipitation (arc-5-test) or immunoblot t ing for a relatively specific 8kDa/12kDa hydatid fluid po lypep t ide antigen (40, 4 3 , 4 8 , 60) .

Treatment, prevention and control Surgery and puncture-aspiration-injection-reaspiration (PAIR), somet imes c o m p l e m e n t e d or replaced b y chemotherapy , represent the principal treatment (90) . Perioperative chemothe rapy with a lbendazole or m e b e n d a z o l e is indicated for reducing the risk of secondary echinococcos is . Treatment shou ld c o m m e n c e at latest four days prior to surgery and continue for one or m o r e months . Treatment of non-resectable cysts with a lbendazole or m e b e n d a z o l e results in cyst disappearance in 3 0 % of cases, another 3 0 % - 5 0 % of patients demonstrate degenerat ion of cysts or significant size reductions, and the cysts of b e t w e e n 2 0 % and 4 0 % of patients under chemotherapy s h o w n o morpholog ica l change (35) .

Prevention of CE focuses primarily o n veterinary aspects to control the intensity and extensity of infection in definitive host populat ions. This includes regular treatment of definitive hosts with praziquantel and meat inspection to prevent access of dogs to cysts (88). A vaccine for ruminant intermediate hosts is be ing d e v e l o p e d (50, 51) .

Alveolar echinococcosis Distribution and public health importance T h e geographical distribution of E. multilocularis is l imited to the northern hemisphere . In North America, the ces tode is mainly present in sub-arctic regions of Alaska and Canada (35) . In Europe, areas with relatively frequent reports of alveolar ech inococcos i s in humans are central and eastern France, Switzerland, Austria and Germany (2). More recent data suggest that neighbouring countries, such as the Netherlands, Belgium, Poland and Chechenya , are also

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infected relatively frequently. Areas of Asia with a h igh prevalence of E. multilocularis include the entire zone of tundra f rom the Whi te Sea eastwards to the Bering Strait, covering large areas of the former Union of Socialist Soviet Republics, the north of the People 's Republic of China and parts of other countries. Similarly to CE, little data exists o n the overall prevalence of AE in humans . In Switzerland, France, Germany and Austria, the annual morbidity rates range b e t w e e n 0.2-1.0 case per 100,000 inhabitants (2). T h e importance of the disease is not due to the large number of cases reported but rather to the severity of the clinical disease in the individual patient, with a frequently lethal ou t come for non-treated cases. Mortality reached 9 2 % within ten years of diagnosis in cases without radical surgery. Mortality rates have recendy significanüy decreased to b e t w e e n 10% and 14% wh ich may b e attributable to m a r k e d improvements in diagnosis, surgery and chemotherapy (3).

Parasite biology, l i fe-cycle and epidemiology

The life-cycle of E. multilocularis is similar to that of E. granulosus. Echinococcus multilocularis occurs as adult tapeworms mainly in red and arctic foxes (Vulpes spp. ) , but dogs and cats can also b e involved incidentally as definitive hosts. Dogs and cats may play a significant role in the transmission of parasites to humans, due to close contact. Small mammals (microtine and arvicolid rodents and occasionally other species) are intermediate hosts for E. multilocularis. In contrast to E. granulosus, E. multilocularis is predominandy maintained b y a wildlife cycle. F o x and dog fur contaminated with E. multilocularis eggs is considered to b e an important heal th hazard to fox hunters and dog owners and to their family m e m b e r s . Vegetables grown outdoors , forest fruits, and windfall fruit contaminated b y fox or dog faeces or eggs stripped from fox fur are considered to b e the major source of infection for humans . Exact data are still unavailable and are very difficult to obtain since retrospective studies cannot accurately provide the information required. The time b e t w e e n infection and occurrence of the first symptoms has b e e n estimated to average b e t w e e n five and fifteen years (31).

Pathogenesis and cl inical fea tures

The primary location of AE is the liver. Rarely, lesions may also metastacise to the lungs, brain, and other organs (35). In contrast to the CE, AE is characterised b y a hepat ic lesion consisting of a dispersed, firm, pale tissue, subsegmented b y scattered small cysts and vesicles. T h e lesions m a y have focal, non-peripheral zones of calcification. In contrast to the infection in rodent hosts, lesions in humans rarely exhibit the formation of protoscoleces and b r o o d capsules w i t h i n vesicles.

Clinical symptoms are usually non-specific with mi ld upper quadrant and epigastric pain. Hepatomegaly l inked with obstructive jaundice has b e e n reported.

Diagnosis Among the imaging procedures , US and CT are of greatest diagnostic value (2, 35) . Irregularly dispersed clusters of calcifications o n plain abdomina l radiographs may give the initial clues. For mass screening programmes , US is the preferred imaging p rocedure (10) . Magnetic resonance imaging d o e s not visualise microcalcifications but reveals intrahepatic changes or obstruction of the inferior vena cava or the portal venous system. Diagnostic b iops ies can b e used to investigate speciat ion using direct immunof luorescence or PCR (15, 46, 69) .

Complementary to imaging procedures , immunodiagnosis represents a secondary diagnostic tool w h i c h is useful in confirming the nature of the aetiological agent (35, 51) . The use of purified E. multilocularis antigens, such as the Em2-antigen, the Eml8-an t igen or recombinant antigens II/3-10 or EM 10 or others, provide diagnostic sensitivities ranging b e t w e e n 9 1 % and 100%, with overall specificities of be tween 9 8 % and 100% (27, 34 , 44 , 59 , 72 , 73) . These antigens allow discrimination b e t w e e n AE and CE with a reliability of 95%. Test operating characteristics enable reliable seroepidemiological studies, and thus detect ion of asymptomatic pre-clinical cases of AE, in addit ion to unique cases in w h i c h the metaces tode les ion dies at an apparentiy early stage of infection (31 , 68) . Serological tests are of limited value for the assessment of the efficacy of treatment and chemotherapy (32, 53 , 54) .

Treatment , prevent ion and control T h e treatment of cho ice is radical surgical resection of the entire parasitic les ion from the liver and other affected organs. Excision of the parasitic les ion follows the principles of radical tumour surgery. Concomitant chemotherapy is r e c o m m e n d e d in all cases after radical surgery or after non-surgical p rocedures (90). Long-term chemotherapy is mandatory in inoperable or only partially resectable cases and in all patients after liver transplantation. Presurgical chemotherapy is not indicated in cases of AE (90) . Liver transplantation has b e e n p r o p o s e d for a selected group of patients with extensive lesions restricted to the liver or with secondary liver disease leading to chronic liver failure (90).

The efficacy of treatment p rogrammes b y fox baiting with praziquantel is under evaluation as a potential control measure. In highly endemic areas, month ly treatment of cats and dogs with praziquantel m a y significanüy reduce infection risk.

Diphyllobothriasis Within the group of tapeworms belonging to the genus Diphyllobothrium, D. latum is the predominant species with regard to numbers of cases: approximately 20 mil l ion people are estimated to b e infected (23) . Diphyllobothrium latum has a world-wide distribution with major foci in the freshwater lakes of Europe, in areas of the former Union of Soviet

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Socialist Republics, Finland, Scandinavia, the alpine zone , and in Asia and America.

The life-cycle includes c o p e p o d s as first intermediate hosts and freshwater fish as s e c o n d intermediate hosts , the latter harbour a n u m b e r of p le rocerco id larvae (66) . Fol lowing ingestion b y definitive hosts , such as humans , the larvae will mature to adult t apeworms that can reach 10 m or m o r e in length and m a y contain u p to 3,000 proglottids. Egg production starts approximately thirty-five days after infection. Intestinal infection with D. latum is usually asymptomatic. In s o m e cases, mi ld gastrointestinal obstruction, rarely diarrhoea and abdomina l pain, and occasionally leukocytosis with eosinophil ia are present. Anaemia occurs in approximately 2 % of the patients, as shown in studies pe r fo rmed in Finland. T h e cause is related to a high affinity of the t apeworm surface for vitamin B 1 2 , w h i c h is then abso rbed f rom the host . As infection is acquired b y the consumption of raw freshwater fish, preventive measures include appropriate cook ing of fish and treatment with praziquantel. In areas with h igh freshwater fish and carnivore population densities, regular treatment with praziquantel of domestic carnivores, especially those be ing fed raw fish, can reduce environmental contamination of natural water resources with parasite eggs. This m a y b e particularly useful in relation to freshwater fish aquacultures. Preventing access of wild carnivores to such facilities b y appropriate fencing may also provide g o o d results.

Nematodes Trichinellosis Distribution and public heal th impac t Trichinellosis is a cosmopol i tan he lminth zoonosis , wh ich can occur where humans eat raw or improper ly c o o k e d meat or meat products f rom infected pigs, wild boars , horses , walruses, dogs and many other domest ic or wild mammals . Trichinella spp . have b e e n repor ted f rom approximately 150 mammalian species (7) and even from birds and marsupials in the case of T. pseudospiralis. Recently, Trichinella spp . have been reported in crocodi les in Z imbabwe (C.M.O. Kapel , personal communicat ion) . Although sylvatic trichinellosis is still endemic in western Europe, pigs raised o n industrial farms are n o longer at risk. Porcine and h u m a n trichinellosis still occurs in a few regions in Spain and southern Finland, where traditional pig rearing practices still prevail (61) . Most cases of h u m a n trichinellosis (more than 2 ,600 since 1975) in the European Union (EU) have b e e n caused b y the consumption of horse mea t originating f rom eastern Europe or North America. Furthermore, b e t w e e n 1975 and 1998, an estimated 1,200 h u m a n infections with trichinellosis in the EU were due to the consumpt ion of wild boa r meat . In eastern Europe, precise figures are not available, but it is generally accepted that in recent years an increase of animal and h u m a n trichinellosis has occurred due to political changes and the resulting soc io - economic p rob lems .

In the USA, Trichinella infections gradually decl ined during the 1990s, but have not yet comple te ly disappeared. In Latin America, several countries have a relatively high prevalence of trichinellosis. In Chile, T. spiralis larvae were found in 2 % of the autopsies carried out during 1992. In Asia and Africa, few data are available o n the prevalence of trichinellosis. Trichinellosis in pigs and humans s eems to b e widespread in regions of the People 's Republic of China, Laos , Thailand and Vietnam, whereas in sub-Saharan Africa, less than 100 h u m a n cases have b e e n reported. T h e cases in Africa were due to T. nelsoni, w h i c h has a l o w infectivity for humans and domest ic pigs. Little is k n o w n about the publ ic heal th importance of T. pseudospiralis. After the description of the first h u m a n case in 1993 , a few outbreaks due to T. pseudospiralis were reported, in w h i c h serious clinical symptoms and e v e n mortality were observed .

Parasi te biology, l i fe -cycle and ep idemio logy Trichinella is a unique n e m a t o d e having b o t h the adult and larval stages present w i t h i n the same host . The larvae are encapsulated in muscles , except for T. pseudospiralis, w h e r e the capsule around the larvae is absent. T h e latter parasite also has a wider hos t range and infects b o t h m a m m a l s and birds. Humans and animals b e c o m e infected with Trichinella spp . through the ingestion of mea t containing viable larvae. Carnivores with cannibalistic or scavenger habits are the mos t important reservoir hosts of Trichinella spp . However , herbivores such as horses , cattle, s h e e p and reindeer can also b e c o m e infected. T h e large n u m b e r of outbreaks of h u m a n trichinellosis due to infected horse meat shows that infection of horses with Trichinella is n o longer exceptional (22) .

Five spec ies are currentiy recognised within the genus Trichinella and three pheno types (T5, T6 and T8) have an uncertain taxonomic status (62) . S o m e authorities consider that T5, w h i c h has b e e n n a m e d T. murrelli, should b e classed as a separate species (65) . T h e pheno type T8 is closely related to T. britovi and T6 is m o r e closely related to T. nativa (62) .

T h e ep idemio logy of trichinellosis in Europe has b e e n studied in detail b y Pozio and colleagues (61 , 63) . Three species with different epidemiologica l features are present, namely: T. spiralis, T. britovi and T. nativa. T h e transmission of these species occurs only through a sylvatic cycle for T. britovi and T. nativa, whereas T. spiralis is transmitted, according to the region, either through a sylvatic cycle alone, or through b o t h sylvatic and domest ic cycles. T h e domest ic cycle of T. spiralis, with domest ic pigs and synanthropic rats as the mos t important sources of infection, still exists in eastern Europe and in a few regions of western/northern Europe (for example Extremadura, Spain and southern Finland), w h e r e pig rearing is still very traditional (i.e. small farms, p o o r hygiene, contact with rats, etc.). In these regions, the prevalence of trichinellosis in wild boars is often higher than e lsewhere . This is p robably due to uncontrol led garbage d u m p s including remnants of infected pig and wild game carcasses. T h e sylvatic cycle of T. britovi and T. nativa is maintained b y

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wild carnivores, mainly foxes, living in natural ecosystems; rodents d o not play a significant role in transmission of the disease. The prevalence of trichinellosis in foxes has b e e n s h o w n to increase with increasing altitude. This is thought to b e due to the presence of an ecologically less disturbed ecosystem in mounta in areas and to a m o r e p ronounced cannibalistic behaviour of foxes in these regions. Trichineila britovi and T. nativa can pass from sylvatic (fox) to domest ic (pig) cycles, although they may not b e maintained in the latter cycle (63).

Pathogenesis and cl inical f ea tu res

Trichinellosis in pigs is generally asymptomatic, except in heavily infected animals, where loss of appetite, malaise, diarrhoea, h ind l imb paralysis and incontinence have b e e n observed. In horses experimentally infected with larvae of T. spiralis, a transient muscle disorder has b e e n reported.

Clinical symptoms caused b y Trichinella spp . in humans d e p e n d o n the number of infective larvae ingested, the immune status of the host (first infection or reinfection) and the species of Trichineila. Clinical signs comprise a transient intestinal stage fol lowed b y a longer lasting extra-intestinal stage (8). High eosinophilia in combinat ion with fever, muscle pain and orbital o e d e m a are suggestive for trichinellosis, especially if the history shows that the patient has eaten raw or improperly c o o k e d meat from potentially infected animals.

Diagnosis

Using r andom amplified po lymorphic DNA-polymerase chain reaction (RAPD-PCR), identification of the five species and three taxa (T5, T6 and T8) of Trichineila is n o w possible. The sensitivity of this technique is 100% for a single larva if the DNA is not damaged. The specificity increases from 88% to 100% if up to five larvae are examined (64).

In animals, trichinoscopy, artificial digestion of one gram samples and ELISA using excretory-secretory (ES) antigens were s h o w n to have a sensitivity of 3 larvae per gram of tissue (LPG), 1 LPG and 0.01 LPG, respectively. Recent investigations have demonstrated that the p o o l e d sample of 1 g of muscle wh ich is artificially digested detects only be tween 3 LPG and 5 LPG (28). In order to detect an infection level of 1 LPG of T. spiralis, w h i c h is generally considered a potentially dangerous public heal th threat, examination of 5 g samples of tongue or diaphragm has b e e n r e c o m m e n d e d (28). In horses, 1 g samples were demonstrated to b e unreliable in detecting infection levels of < 3 LPG (29). After the multi­focal outbreak of h u m a n trichinellosis in 1993 in France, due to the consumption of horse meat wh ich h a d b e e n declared free of Trichineila using the former technique in North America, the EU dec ided to increase the sample size from 1 g to 5 g. In horses , larvae accumulate preferentially in the tongue, fol lowed b y the masseter, n e c k , suprasprnatus, trapezius and diaphragm muscles .

The ELISA, using ES antigens (ES-ELISA), is a highly sensitive technique w h i c h is very useful for epidemiological surveillance of porcine trichinellosis, al though false negatives may occur in infected pigs prior to seroconvers ion (28). The ES-ELISA may also fail to detect infected horses , especially those with older infections, because the antibodies disappear m u c h m o r e rapidly than in pigs (78) .

In humans , muscle b i o p s y and consecutive artificial digestion of the sample is the m e t h o d of cho ice for the parasitological confirmation of trichinellosis (52) . T h e species of Trichineila involved can b e identified using RAPD-PCR as ment ioned earlier (64) . Although s o m e progress has b e e n m a d e in the field of antigen detect ion, ant ibody detect ion tests (especially the IgG-ELISA) are generally m o r e useful, because specific antibodies remain present for a long pe r iod after infection (8).

Treatment , prevent ion and control

Treatment of animal and h u m a n trichinellosis is possible using benzimidazole c o m p o u n d s . Mebendazo le and albendazole are the anthelmintics of cho ice (8, 52) .

Since trichinellosis is only transmitted through ingestion of infected meat , the following preventive measures should be employed :

- waste f o o d and swill containing mea t should b e heated (100°C for 30 minutes) before use as pig feed

- architectural barriers should b e created to avoid the entrance of rodents and other synanthropic animals to animal premises and food-stores

- animal carcasses should b e p r o m p d y and properly d i sposed of (52, 83) .

Although these measures are difficult to implement in some regions of the wor ld due to cultural, soc io -economic or historical reasons, many large industrialised farms in the EU, the USA and elsewhere have used these measures with success. The risk of contracting trichinellosis from these farms is very low. Nevertheless, the EU laws require that all pigs for export b e examined for Trichineila, at a cost of US$3 per pig. Since 190 mil l ion pigs are slaughtered per year, it has been calculated that the EU could save US$420 mill ion and simultaneously improve Trichineila control b y restricting examination to those pigs originating in small farms or in regions with traditional pig rearing practices (61) . Proposals for alternative Trichineila control w i t h i n the EU are currently being discussed. These suggest that pigs from large commercia l farms, wh ich are situated in non-endemic Trichineila areas and w h i c h take the necessary measures to avoid infection, should n o longer have to undergo Trichineila control at the slaughterhouse (83) . In these areas, a representative sample of indicator animals, e.g. foxes, could b e examined in order to moni tor the evolution of trichinellosis.

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In countries w h e r e mea t inspect ion for Trichinella is not obligatory (e.g. the USA) or w h e r e the detect ion techniques used in abattoirs are not sufficiendy reliable, the mos t reliable me thod to avoid trichinellosis infection is to ensure that meat reaches an internal temperature of 60°C for at least a minute during cooking . Freezing at —15°C for twenty days kills Trichinella larvae, except T. nativa. Since this species has b e e n found in domest ic pigs, frozen p o r k can n o longer b e considered safe for the consumer, or at least p o r k originating from T. nativa endemic regions. Another m e t h o d of killing Trichinella larvae, is l o w level g a m m a irradiation (< 1 kGy) . Prevention of trichinellosis might also b e achieved b y vaccination. Several reports indicate that h igh protect ion levels against re-infection can b e obta ined after experimental immunisation of swine.

Capillariosis Capillaria philippinensis occurs over a w i d e geographical area extending from the Philippines, w h e r e infection occurs as small ep idemics along rivers, to Egypt where individual cases have b e e n reported. Infection arises from eating raw or unde rcooked fish w h i c h serve as intermediate hosts. T h e adults live in the uppe r small intestine where autoinfection is responsible for maintaining infection over many years. A chronic malabsorpt ion syndrome m a y deve lop , w h i c h has occasionally b e e n repor ted to b e fatal. Monkeys appear to b e the usual definitive hosts . Control is pe r fo rmed b y treatment with m e b e n d a z o l e and through educat ion. T h e parasite has been greatly reduced in areas where the practice of consuming unde rcooked fish has b e e n discontinued.

Gnathostomosis Zoonotic infections occur with several species of the genus Gnaihostoma. Mammalian carnivores such as cats, dogs , tigers and leopards usually serve as definitive hosts . C o p e p o d s serve as initial intermediate hosts. W h e n infected c o p e p o d s are ingested b y fish or frogs, these species serve as secondary intermediate hosts in w h i c h infective L 3 larvae deve lop . Infection in definitive hosts occurs b y eating raw or unde rcooked fresh-water fish (G. spinigerum). Most repor ted cases have occurred in Thailand and Japan . A cutaneous or visceral larva migrans condi t ion m a y arise in humans w h e n infected fish or frogs are eaten. Treatment for superficially occurring larvae may b e surgical removal .

Anisakiosis This condi t ion arises in humans infected with the larvae of Pseudoterranova decipiens, a c o m m o n n e m a t o d e parasite of marine mammals , c o d and other sea fish, or with larvae of species of Anisakis, w h i c h infect sea fish such as herring and mackerel . Infection is acquired b y consuming u n c o o k e d or raw fish filets c o m m o n l y sold in stores. Clinical manifestations may include 'tingling throat syndrome ' or ulceration of the gut (70). Therapy includes surgical removal of larvae. No appropriate chemothe rapy has b e e n repor ted as yet, a l though ivermectin is assumed to exhibit reasonable efficacy.

Parastrongylosis (angiostrongylosis) T h e species Angiostrongylus cantonensis and A. costaricensis have b e e n reclassified in the genus Parastrongylus. T h e term 'angiostrongylosis' should , therefore, n o w b e rep laced b y 'parastrongylosis'. Thousands of h u m a n infections occur with the larval stage of the rodent n e m a t o d e Parastrongylus cantonensis. Infection occurs b y eating infected molluscs or f o o d contaminated b y contact with snails. Infection causes eosinophi l ic meningitis. This parasite has spread in recent years, with the dissemination of one of the intermediate hosts , the giant African land snail (Achatina fulica), w h i c h is a popular f o o d i t em in s o m e countries. Chemothe rapy m a y include a lbendazole or ivermectin, but always requires concomitant medica t ion with steroids.

Conclusion Parasitic p ro tozoan water-borne zoonoses , particularly Giardia and Cryptosporidium, w h i c h cause diarrhoea in animals and humans , are estimated to infect m o r e than 300 mil l ion p e o p l e annually. T h e cysts and oocysts of these pro tozoa are resistant to standard water treatment systems and spectacular e p i d e m i c s have b e e n repor ted in d e v e l o p e d countries. T h e inability of non-industrialised countries to k e e p p a c e with popula t ion growth, migration to urban areas and the d e m a n d for clean, safe, drinking water means that water-borne zoonoses will continue to exact an increasing b u r d e n of ill heal th. T h e same scenario is true for sanitation and, in addit ion to p ro tozoan zoonoses , numerous he lmin th infections, including T. solium, T. saginata, and numerous t rematode species will continue to proliferate. Close association wi th cats and dogs facilitates the transmission of T. gondii and Echinococcus s pp . Eating habits and access to flora and fauna w h i c h contain infective parasitic stages for humans are important in determining h u m a n infections, in addit ion to increasing definitive host populat ions, w h i c h was the case with foxes and E. multilocularis in central Europe. F o o d - b o r n e zoonoses transmitted through the consumpt ion of raw or u n d e r c o o k e d mea t include such organisms as Sarcocystis, T. gondii, T. solium, T. saginata, and Trichinella spp . Consumpt ion of raw, improper ly c o o k e d or p i ck l ed fresh-water fish facilitates transmission of a large number of zoonot ic infections, and an estimated 70-100 mill ion p e o p l e have b e e n infected with parasitic t rematodes such as Clonorchis spp . , Opisthorchis spp . , H. heterophyes, M. yokogawai, E. ilocanum, E. revolutum, E. malayanum, E. echinatum and E. hortense. Fish also serve as intermediate hosts for the ces tode D. latum and the nema todes C. philippinensis and G. spinigerum. Anisakis infections arise f rom eating salt-water fish. Eating raw crabs, w h i c h are somet imes p i c k l e d in wine or brine, may result in Paragonimus spp . infection and the consumpt ion of molluscs m a y e x p o s e humans to infection with P. cantonensis and P. costaricensis. T h e proliferation of f o o d i tems in the average supermarket in the USA (from a selection of about 300 i tems in the 1950s to over 3,000 today) has resulted from the

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importation of foods from many different parts of the world. Tourists travel in ever increasing numbers from industrialised countries to the tropics and the consumpt ion of local foods , presented in a traditional way, contributes to the occurrence of exotic zoonoses in non-endemic countries. Most parasitic zoonoses can b e treated but a lasting reduction in infection will require the combinat ion of a number of different approaches to control. Changing h u m a n behaviour through education, to encourage the proper cook ing of food, w h i c h

m a y have cultural and social significance, will remain as challenging as the provision of safe drinking water and sanitation for the control of zoonot ic parasitic diseases. Further studies are also required o n the veterinary importance of parasitic zoonoses .

Zoonoses parasitaires d'origine alimentaire ou hydrique C.N.L. Macpherson, B. Gottstein & S. Geerts

Résumé

Selon les dernières estimations, près de la moitié de la population mondiale serait affectée par des infections d'origine alimentaire ou hydrique. Parmi ces infections, les zoonoses parasitaires ont des conséquences graves pour la santé publique et occasionnent des pertes directes et indirectes sévères à l'agriculture. Étant donné que les pays non industrialisés ne parviennent pas à apporter une réponse adaptée à la croissance démographique et à l'exode rural, ni à fournir une eau potable de bonne qualité ou des systèmes d'assainissement efficaces, les zoonoses d'origine hydrique vont sans doute devenir un fardeau de plus en plus lourd pour la santé publique de ces pays. La consommation de viandes, de crustacés, de poissons d'eau douce et de légumes crus ou mal cuits favorise la transmission d'un grand nombre de zoonoses. Le développement de l'industrie du tourisme, l'émigration des populations humaines et l'importation de denrées alimentaires en provenance de régions endémiques se traduisent par un accroissement du nombre de ces infections dans les pays qui en sont indemnes. Les auteurs étudient l'épidémiologie des principales infections parasitaires transmises par les aliments ou par l'eau, ainsi que leur importance pour la santé publique et animale et l'évolution récente en matière de diagnostic, de traitement et de prophylaxie.

Mots-clés Cestodes - Nématodes - Protozoaires - Santé publique - Trématodes - Zoonoses -Zoonoses d'origine alimentaire - Zoonoses d'origine hydrique.

Zoonosis parasitarias transmitidas por vía hídrica o alimentaria C.N.L. Macpherson, B. Gottstein & S. Geerts

Resumen

Las estimaciones actuales sugieren que casi la mitad de la población mundial se ve afectada por infecciones que se transmiten a través del agua o los alimentos. Las zoonosis parasitarias contribuyen a esa estadística imponiendo un duro tributo en términos de salud humana y causando, directa o indirectamente, grandes pérdidas en el sector agrícola. La incapacidad de los países no industrializados para responder adecuadamente al crecimiento demográfico, la

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migración de zonas rurales a núcleos urbanos y la creciente demanda de agua potable limpia y segura y de infraestructuras de saneamiento apropiadas se traduce por un incremento previsible del impacto de las zoonosis transmitidas por el agua en el estado de salud de aquellos países. La ingestión de carne, crustáceos, pescado de agua dulce o vegetales crudos o insuficientemente cocinados facilita la transmisión de un gran número de infecciones zoonóticas. La floreciente industria del turismo, las migraciones y la importación de alimentos desde regiones endémicas han resultado en un aumento del número de diagnósticos de esas infecciones en países donde no son endémicas. Los autores examinan la epidemiología de las infecciones parasitarias más importantes que se transmiten por vía hídrica o alimentaria, así como sus repercusiones en materia de salud pública y veterinaria y los últimos avances realizados para el diagnóstico, tratamiento y control de esas enfermedades.

Palabras clave Cestodos - Nemátodos - Protozoos - Salud pública - Tremátodos - Zoonosis - Zoonosis transmitidas por vía alimentaria - Zoonosis transmitidas por vía hídrica.

References

1. Allan J . C , Velasquez-Tohom M., Torres-Alvarez R., Yurrita P. & Garcia-Noval J. (1996). - Field trial of the coproantigen-based diagnosis of Taenia solium taeniasis by enzyme-linked immunosorbent assay. Am. ] . trop. Med. Hyg., 54, 352-356.

2. Ammann R.W. & Eckert J. (1996). - Cestodes. Echinococcus. Gastroenterol. Clin. North Am., 25 (3), 655-689.

3. Ammann R.W., Fleiner-Hoffmann A., Grimm F. & Eckert J. (1998). - Long-term mebendazole therapy may be parasitocidal in alveolar echinococcosis. J. Hepatol., 29, 994-998.

4. Brandt J.R.A., Geerts S., De Deken R., Kumar V., Ceulemans F., Brijs L. & Falla N. (1992). - A monoclonal antibody-based ELISA for the detection of circulating excretory secretory antigens in Taenia sagpiata cysticercosis. Int.J. Parasitol, 22, 471-477.

5. Bretagne S., Costa J.M., Vidaud M., Nhieu J.T.V. & Fleury-Feith J. (1993). - Detection of Toxoplasma gondii by competitive DNA amplification of bronchoalveolar lavage samples. J. inject. Dis., 168, 1585-1588.

6. Brockelman W.Y., Upatham E.S., Vìyanant V. & Hirunkraks A. (1987). - Measurement of incidence of the human live fluke, Opisthorchis viverrini in northeast Thailand. Trans. roy. Soc. trop. Med. Hyg, 81 , 327-335.

7. Campbell W.C. (1988). - Trichinosis revisited: another look at modes of transmission. Parasitol. Today, 4, 83-86.

8. Capo V. & Despommier D.D. (1996). - Clinical aspects of infection with Trichineila spp. Clin. Microbiol Rev., 9, 47-54.

9. Craig P.S., Macpherson C.N.L. & Nelson G.S. (1986). - The identification of eggs of Echinococcus by immunofluorescence using a specific monoclonal antibody. Am. J. trop. Med. Hyg., 35, 152-158.

10. Craig P.S., Deshan L., Macpherson C.N., Dazhong S., Reynolds D., Barnish G., Gottstein B. & Zhirong W. (1992). - A large focus of alveolar echinococcosis in central China, Lancet, 340 (8823), 826-831.

11. Craun G.F. (1990). - Waterbome giardiasis. In Giardiasis (E.A. Meyer, ed.). Elsevier, New York, 267-293.

12. Deplazes P., Gottstein B., Eckert J., Jenkins D.J., Ewald D. & Jimenez-Palacios S. (1992). - Detection of Echinococcus coproantigens by enzyme-linked immunosorbent assay in dogs, dingoes and foxes. Parasitol. Res., 78, 303-308.

13. Deplazes P. & Eckert J. (1996). - Diagnosis of the Echinococcus multilocularis infection in final hosts. Appl. Parasitol, 37, 245-252.

256 Rev. sci. tech. Off. int. Epiz., 19 (1)

14. Desmonts G., Couvreur J., Alision F., Baudelot J., Gerbeaux J. & Lelong M. (1965). - Etude épidémiologique SUT la toxoplasmose : de l'influence de la cuisson des viandes de boucherie sur la fréquence de l'infection humaine. Rev. fr. Etud. clin. Biol, 10, 952-958.

15. Diebold-Berger S., Khan H., Gottstein B., Puget E., Frossard J.L. & Remadi S. (1997). - Cytologic diagnosis of isolated pancreatic alveolar hydatid disease with immunologic and PCR analyses: a case report. Acta cytologica, 41,1381-1386.

16. Dinkel A., von Nickisch Roseneck M., Bilger B., Merli M., Lucius R. & Romig T. (1998). - Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. J. clin. Microbiol., 36, 1871-1876.

17. Dubey J.P. (1970). - The Toxoplasma gondii oocyst from cat feces. J. experim. Med., 132, 636-662.

18. Dubey J.P. (1986). - A review of toxoplasmosis in cattle. Vet. Parasitol, 22, 177-202.

19. Dubey J.P. (1998). - Toxoplasmosis, sarcocystiosis, isosporosis and cyclosporosis. In Zoonoses: biology, clinical practice, and public health control (S.R. Palmer, E.J.L. Soulsby & D.I.H. Simpson, eds). Oxford University Press, Oxford, 579-597.

20. Dubey J.P., Fayer R. & Schad G.A. (1986). - Distribution of Toxoplasma gondii cysts in commercial cuts of pork. J. Am. vet. med. Assoc., 188,1035.

21. Dubey J.P. & Beattie CP. (1988). - Toxoplasmosis of animal and man. CRC Press, Boca Raton, Florida, 220 pp.

22. Dupouy-Camet J., Soulé C L . & Ancelle T. (1994). - Recent news on trichinellosis: another outbreak due to horsemeat consumption in France in 1993. Parasite, 1, 99-103.

23. Eckert J. (1998). - Parasiten in Nahrungsketten. Nova acta leopoldina, 79, 99-120.

24. Fan P.C. (1988). - Taiwan Taenia and taeniasis. Parasitol. Today, 4, 86-88.

25. Farthing M.J.G., Cevallos A.M. & Kelly P. (1995). -Intestinal protozoa. In Manson's tropical diseases, 20th Ed. (G.C. Cook, ed.) . W.B. Saunders Co., London, 1255-1298.

26. Fayer R. (1994). - Foodbome and waterborne zoonotic protozoa. In Foodbome disease handbook. Volume 2: Diseases caused by viruses, parasites, and fungi (Y.H. Hui, J.R. Gorham, K.D. Murrell & D.O. Oliver, eds). Marcel Dekker, New York, 331-362.

27. Frosch P.M., Frosch M., Pfister T., Schaad V. & Bitter-Suermann D. (1991). - Cloning and characterization of an immunodominant major surface antigen of Echinococcus multilocularis. Molec. biochem. Parasitol., 48, 121-130.

28. Gamble H.R. (1998). - Sensitivity of artificial digestion and enzyme immunoassay methods of inspection for trichinae in pigs. J. Food Protec, 61, 339-343.

29. Gamble R.H., Gahadjar A.A. & Solomon M.B. (1996). -Methods for the detection of trichinellosis in horses. J. Food Protec, 59, 420-425.

30. Geerts S. (1993). - The taeniasis-cysticercosis complex in Africa. Bull Séances Acad. roy. Sci. Outre-Mer, 38, 245-264.

31. Gottstein B., Lengeier C , Bachmann P., Hagemann P., Kocher P., Brassard M., Witassek F. & Eckert J. (1987). -Sero-epidemiological survey for alveolar echinococcosis (by Em2-ELISA) of blood donors in an endemic area of Switzerland. Trans, roy. Soc. trop. Med. Hyg, 81, 960-964.

32. Gottstein B., Tschudi K., Eckert J. & Ammann R. (1989). -Em2-ELISA for the follow-up of alveolar echinococcosis after complete surgical resection of liver lesions. Trans. roy. Soc. trop. Med. Hyg, 83, 389-393.

33. Gottstein B., Deplazes P., Tanner I. & Skaggs J.S. (1991). -Diagnostic identification of Taenia saginata with the polymerase chain reaction. Trans. roy. Soc. trop. Med. Hyg., 85, 248-249.

34. Gottstein B., Jacquier P., Bresson-Hadni S. & Eckert J. (1993). - Improved primary immunodiagnosis of alveolar echinococcosis in humans by an enzyme-linked immunosorbent assay using the Em2plus antigen. J. clin. Microbiol, 31 (2), 373-376.

35. Gottstein B. & Reichen J. (1996). - Echinococcosis/ hydatidosis. In Manson's tropical diseases, 20th Ed. (G.C. Cook , ed.) . W.B. Saunders Co., London, 1486-1508.

36. Haberkom A. (1996). - Chemotherapy of human and animal coccidioses: state and perspectives. Parasitol. Res., 82, 193-199.

37. Han J.K., Han D., Choi B.I. & Han M.C. (1996). - MR findings in human fascioliasis. Trop. Med. int. Hlth, 1, 367-372.

38. Harrison L.J.S., Joshua G.W.P., Wright S.H. & Parkhouse R.M.E. (1989). - Specific detection of circulating surface/secreted glycoproteins of viable cysticerci in Taenia saginata cysticercosis. Parasite Immunol, 11, 351-370.

39. Haswell-Elkins M.R., Mairiang E., Mairiang P., Chaiyakum J., Chamadol N., LoapaiboonV., Sithithaworn P. & Elkins D.B. (1994). - Cross-sectional study of Opisthorchis viverrini infection and cholangiocarcinoma in communities within a high-risk area in Northeast Thailand. Int. f. Cancer, 59 (4), 505-509.

40. Hira P.R., Bahr G.M.,. Schweiki H.M. & Behbehani K. (1990). - An enzyme-linked immunosorbent assay using an arc 5 antigen for the diagnosis of cystic hydatid disease. Ann. trop. Med. Parasitol, 84, 157-162.

41 . Hopkins R.M., Meloni B.P., Grotti D.M., Wetherall J.D., Reynoldson J.A. & Thompson R.C.A. (1997). - Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. J. Parasitol, 83, 44-51.

42. Huffman J.E. & Fried B. (1990). - Echinostoma and echinostomiasis. Adv. Parasitol., 29, 215-269.

Rev. sci. tech. Off. int. Epiz., 19 (1) 2 5 7

43. Ioppolo S., Notargiacomo S., Profumo E., Franchi C , Ortona E., Rigano R. & Siracusano A. (1996). -Immunological responses to antigen B from Echinococcus granulosus cyst fluid in hydatid patients. Parasite Immunol., 18, 571-578.

44. Ito A., Wen H., Craig P.S., Ma L , Nakao M., Horii T., Pang X.L., Okamoto M., Itoh M., Osawa Y., Wang X.G. & Liu Y.H. (1997). - Antibody responses against Eml8 and Em 16 serodiagnostic markers in alveolar and cystic echinococcosis patients from northwest China. Jpn. J. med. Sci. Biol, 50, 19-26.

45. Ito A., Plancarte A., Ma L., Kong Y., Flisser A., Cho S.Y., Liu Y.H., Kamhawi S., Lightowlers M.W. & Schantz P.M. (1998). - Novel antigens for neurocysticercosis: simple method for preparation and evaluation for serodiagnosis. Am. J. trop. Med. Hyg., 59, 291-294.

46. Kern P., Frosch P., Helbig M., Wechsler J.G., Usadel S., Beckh K., Kunz R., Lucius R. & Frosch M. (1995). -Diagnosis of Echinococcus multilocularis infection by reverse-transcription polymerase chain reaction. Gastroenterology, 109, 596-600.

47. Kyvsgaard N.C., Ilsoe B., Willeberg P., Nansen P. & Henriksen S.A. (1991). - A case-control study of risk factors in light Taenia saginata cysticercosis in Danish cattle. Acta vet. scand., 32, 243-252.

48. Leggatt G.R. & McManus D.P. (1994). - Identification and diagnostic value of a major antibody epitope on the 12 kDa antigen from Echinococcus granulosus (hydatid disease) cyst fluid. Parasite Immunol, 16, 87-96.

49. Lightowlers M. & Gottstein B. (1995). - Immunodiagnosis of echinococcosis. In Echinococcus and hydatid disease (R.C.A. Thompson & A.J. Lymbery, eds). CAB International, Wallingford, 355-410.

50. Lightowlers M.W., Lawrence S.B., Gauci C.G., Young J., Ralston M.J., Maas D. & Health D.D. (1996). - Vaccination against hydatidosis using a defined recombinant antigen. Parasite Immunol, 18, 457-462.

51. Lightowlers M.W., Rolfe R. & Gauci C.G. (1996). - Taenia saginata: vaccination against cysticercosis in cattle with recombinant oncosphere antigens. Experim. Parasitai, 84, 330-338.

52. Ljungström I., Murrell D., Pozio E. & Wakelin D. (1998). -Trichinellosis. In Zoonoses: biology, clinical practice, and public health control (S.R. Palmer, E.J.L. Soulsby & D.I.H. Simpson, eds). Oxford University Press, Oxford, 789-802.

53. Ma L , Ito A. Liu Y.H., Wang X.G., Yao Y.Q., Yu D.G, & Chen Y.T. (1997). - Alveolar echinococcosis: Em2plus-ELISA and Eml8-westem blots for follow-up after treatment with albendazole. Trans. roy. Soc. trop. Med. Hyg., 91 (4), 476-478.

54. Mac Kenzie W.R., Hoxie N.J., Proctor M.E., Grodus M.S., Blair K.A., Peterson D.E., Kazmierczak J.J., Addiss D.G., Fox K.R., Rose J .B. & Davis J.P. (1994). - A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. New Engl. J. Med., 331 (3),'161-167.

55. McManus D.P. & Bowles J. (1994). - Asian (Taiwan) Taenia: species or strain? Parasi tol . Today, 10, 273-275.

56. Macpherson C.N.L. (1983). - An active intermediate host role for man in the life cycle of Echinococcus granulosus in Turkana, Kenya. Am.J. trop. Med. Hyg., 32 , 397-404.

57. Macpherson C.N.L., Romig T., Zeyhle E., Rees P.H. & Were J.B.O. (1987). - Portable ultrasound scanner versus serology in screening for hydatid cysts in a nomadic population. Lancet, 2, 259-261.

58. Müller N., Zimmermann V., Hentrich B. & Gottstein B. (1996). - Diagnosis of Neospora canium and Toxoplasma gondii infection by PCR and DNA hybridization immunoassay. J. clin. Microbiol, 34 (11), 2850-2852.

59. Nirmalan N. & Craig P.S. (1997). - Immunoblot evaluation of the species-specificity of Eml8 and Eml6 antigens for serodiagnosis of human alveolar echinococcosis. Trans. roy. Soc. trop. Med. Hyg., 91 , 484-486.

60. Porretti D., Felleisen E., Grimm F., Pfister M., Teuscher F., Zuercher C , Reichen J. & Gottstein B. (1999). - Differential immunodiagnosis between cystic hydatid disease and other cross-reactive pathologies. Am. J. trop. Med. Hyg., 60, 193-198.

61. Pozio E. (1998). - Trichinellosis in the European Union: epidemiology, ecology and economic impact. Parasi tol . Today, 14, 35-38.

62. Pozio E., La Rosa G., Murrell K.D. & Lichtenfels J.R. (1992). - Taxonomic revision of the genus Trichinella. J. Parasitai, 78, 654-659.

63. Pozio E., La Rosa G., Serrano F.J., BarratJ. & Rossi L. (1996). - Environmental and human influence on the ecology of Trichinella spiralis and Trichinella britovi in western Europe. Parasitai, 113,527-533.

64. Pozio E., Kapel C.M.O. & Gamble H.R. (1999). - Specificity and sensitivity of random amplified polymorphic DNA analysis for the identification of single larvae of Trichinella after experimental infection of pigs. Parasi tol Res., 85, 504-506.

65. Pozio E. & La Rosa G. (2000). - Trichinella murreli n. sp.: etiological agent of sylvatic trichinellosis in temperate areas of North America. J. Parasi tol . (in press).

66. Rahkonen R. & Valtonen E.T. (1997). - Infection of brown trout with Diphyi/obothrium dendriticum procercoids. Int. ] . Parasitai, 27, 1315-1318.

67. Rausch R.L. (1986). - Life-cycle patterns and geographic distribution of Echinococcus species. In The biology of Echinococcus and hydatid disease ( R C A . Thompson, ed.) . Allen and Unwin, London, 44-80.

2 5 8 Rev. sci. tech. Off. int. Epiz., 19 (1)

68. Rausch R.L, Wilson J.F., Schantz P.M. & McMahon B.J. (1987). - Spontaneous death of Echinococcus multilocularis: cases diagnosed serologically by Em2-ELISA and clinical significance. Am. J. trop. Med. Hyg., 36, 576-585.

69. Sailer M., Soelder B., Allerberger. F., Zaknun D., Feichtinger H. & Gottstein B. (1997). - Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J. Pediatr., 130, 320-323.

70. Sakanari J.A. & McKerrow J.H. (1989). - Anasakiasis. Clin. Microbiol. Rev., 2, 278-284.

71. Sampaio-Silva M.L., Da Costa J.M., Da Costa A.M., Pires M.A., Lopes S.A., Castro A.M. & Monjour L. (1996). -Antigenic components of excretory-secretory products of adult Fasciola hepatica recognized in human infections. Am. J. trop. Med. Hyg., 54, 146-148.

72. Sarciron E.M., Bresson-Hadni S., Mercier M., Lawton P., Duranton C, Lenys D., PetavyA.F. & Vuitton D.A. ( 1 9 9 7 ) . -Antibodies against Echinococcus multilocularis alkaline phosphatase as markers for the specific diagnosis and the serological monitoring of alveolar echinococcosis. Parasite Immunol, 19 (2), 61-68.

73. Sato C. & Furaya K. (1994). - Isolation and characterization of a diagnostic polysaccharide antigen from larval Echinococcus multilocularis. Jpn. J. med. Sci. Biol, 47, 65-71.

74. Schantz P.M., von Reyn C.F., Welty T. & Schultz M. (1976). - Echinococcosis in Arizona and New Mexico. Survey of hospital records, 1969-1974. Am. J. trop. Med. Hyg., 25, 312-317.

75. Schantz P.M., Cruz M., Sarti E. & Pawlowski Z. (1993). -Potential eradicability of taeniasis and cysticercosis. Bull. PAHO, 27, 397-403.

76. Schantz P.M., Wilkins P.P. & Tsang V.C.W. (1998). -Immigrants, imaging and immunoblots: the emergence of neurocysticercosis as a significant health problem. In Emerging infections 2 (W.M. Scheid, D. Armstrong & J.B. Hughes, eds). ASM Press, Washington, 213-242.

77. Smith H.V. & Rose J .B. (1998). - Waterborne cryptosporidiosis: current status. Parasitol Today, 14, 14-22.

78. Soulé C.H., Dupouy-Camet J., Georges P., Ancelle T., Gillet J.P., Vaissaire J., Delvigne A. & Plateau E. (1989). -Experimental trichinellosis in horses: biological and parasitological evaluation. Vet. Parasitol, 31 , 19-36.

79. Taminelli V. & Eckert J. (1989). - Häufigkeit und geographische Verbreitung des Giardia-Befalles bei Wiederkäuern in der Schweiz [The frequency and geographic distribution of Giardia infections in ruminants in Switzerland], Schweizer Arch. Tierheilkd., 131 (5), 251-258.

80. Tee G.H., Moody A.H., Cooke A.H. & Chiodini P.L. (1993). - Comparison of techniques for detecting antigens of Giardia lamblia and Cryptosporidium parvum in faeces. J. din. Pathol, 46, 555-558.

81. Tsang V.C.W., Brand J.A. & Boyer A.E. (1989). - An enzyme-linked immunoelectrotransfer blot assay and glycoprotein antigens for diagnosing human .cysticercosis. J. inject. Dis., 159, 51-59.

82. Tsang V.C.W. & Wilson M. (1995). - Taenia solium cysticercosis: an under-recognized but serious public health problem. Parasitol. Today, 11, 124-126.

83. Van Knapen F. (1998). - European proposal for alternative Trichinella control in domestic pigs. Fleischwirtschajt, 78, 338-339.

84. Velasquez C.C. (1982). - Heterophyidiasis. In Parasitic zoonoses, Vol. III, Section C (G.V. Hillyer & C E . Hopla, eds). CRC Press, Boca Raton, Florida, 99-107.

85. Watson-Jones D.L. & Macpherson C.N.L. (1988). - Hydatid disease in the Turkana district of Kenya. VI. Man:dog contact and its role in the transmission and control of hydatidosis amongst the Turkana. Ann. trop. Med. Parasitol, 82 (4), 343-356.

86. White A.C. (1997). - Neurocysticercosis: a major cause of neurological disease worldwide. Clin. inject. Dis., 24, 101-115.

87. Wong K.T. & Pathmanathan R. (1992). - High prevalence of human skeletal muscle Sarcocystis in south-east Asia. Trans, roy. Soc. trop. Med. Hyg., 86, 631-632.

88. World Health Organization (WHO) (1992). - Guidelines for diagnosis, surveillance and control of echinococcosis. WHOA/PH/ECH.92. WHO, Geneva, 92 pp.

89. World Health Organization (WHO) (1995). - Control of foodbome trematode infections. WHO Technical Report Series, No. 849. WHO, Geneva, 157 pp.

90. World Health Organization (WHO) (1996). - Guidelines for treatment of cystic and alveolar echinococcosis in humans. WHO Informal Working Group on Echinococcosis. Bull. WHO, 74, 231-242.

91. Yilmaz H., Oner A.F., Akdeniz H. & Arslan S. (1998). - The effect of triclabendazole (Fasinex) in children with fasciolosis. J. Egypt. Soc. Parasitol, 28, 497-502.