Journal of the Egyptian Society of Parasitology, Vol.44, No.1, April 2014 J. . Soc. Parasitol. (JESP), 44(1), 2014: 249 – 274

THE IMPACT OF PARASITES ON HEALTH (REVIEW ARTICLE) By OMAR S.A. AMER Department of Zoology, Faculty of Science, Al-Azhar University (Assiut Branch), Egypt (email:[email protected]) Abstract One of the most important problems faced by world at the present time is food deficiency. Today the third world is facing protein deficiency as one of the major global challenges. In Egypt, the continuous population explosion requires more food production to meet the con- sequent increasing demands. However, there are many zoonotic fish parasites not onlu in Egypt but worldwide. Key words: Egypt, Fish, zoonotic heminthes, Review

Introduction be ignored keeping in mind the use of cod are considered to compensate the and sharks among patients suffering with continuous lack of such element due to its vitamin A and D deficiency (Uradzinski et comparatively low price (El-Tantawy and al, 2007) El-Sherbiny, 2010). Fishes were used even Among the , fishes are the most im- in prehistoric ages and were supposed to be portant hosts for maintenance of parasites beneficial to long life and intelligence mainly helminthes. Most of fishes have par- (Hamilton, 1971). Fish as food products asites and they not only serve as hosts of dif- have a very high nutritive value approximat- ferent parasites but also serve as carrier of ing that of red meat.Its protein is readily many larval parasitic forms that mature and available (at a level of 96%) which stems may cause serious diseases in many verte- from a low content of collagen and elastin. It brates including man.With the increasing is worth mentioning that as little as 100 g interests in aquaculture, parasitic infestations ration of fish provides a human with 1/3 to are becoming threats for fish health man- 1/2 of the daily requirement for pro- agement. It is therefore an essential area for tein. Fish constitutes an important and indis- proper attention to be given by the scientists pensable component of the human diet due for sustainable aquaculture production to the content of polyunsaturated fatty acids (Chandra, 2006). (PUFA), the so-called "Omega-3 acids". suffer from numerous parasitic They are necessary for the comprehensive food-borne zoonoses, many of which are development and functioning of the brain as caused by helminths. The helminth zoonoses well as senses of sight and hearing.A study of concern in this review are those transmit- conducted in Netherlands reported that eat- ted from fish, freshwater, brackish and ma- ing a pound of fish a week could reduce the rine. In the past, these diseases were limited coronary diseases in man. Some fish, for the most part to populations living in specially cold water species such as cod, low- and middle-income countries, but the salmon, mackerel and sardines, contain geographical limits and populations at risk some oils that are not found in other food are expanding and changing because of the and have major effects on body chemistry, growing international markets, improved which reduces the tendency of to clot transportation systems, and demographic and helps in lowering cholesterol level in the changes (Chai et al, 2005). blood. The medical value of fish oil cannot

249 WHO (1995) estimated that the number of sakis spp. Petter et al. (1985) studied teleost people currently infected with fish-borne fishes from the Bay of Kotor (Yugoslavia) trematodes exceeds 18 million, but world- for parasitic and they found sev- wide the number of people at risk, including eral species of adult or larval nematodes of those in developed countries, is more than the genus .Smith and Wootten half a billion. The recognition of the public (1987) reviewed many and varied aspects of health significance of these zoonoses, their the extensive world literature on Anisakis. links to poverty and cultural traditions, to Wootten (1978) studied the occurrence of intensification of agriculture, to environmen- larval Anisakids in small gadoids from Scot- tal degradation, and the lack of tools for con- tish waters and noted increased trol is increasing. rate with increasing age and length of fish. Fish and parasites: Although fish are a Hristovski and Jardas (1991) discussed valuable source of food, their consumption endohelminths of fishes from the mid- may contribute to food poisoning and infec- Dalmation region of the Adriatic Sea. Naid- tions as they contain pathogenic bacteria and enova and Morvinova (1997) studied the /or their toxins, parasite and chemical resi- helminth fauna of Mediterranean Sea fishes. dues (Uradzinski et al, 2007). Several stud- Diamant et al. (1999) reported several spe- ies andcomprehensive textbooks in fish par- cies of digeneans from the rabbit fish, Siga- asitology have been achieved in the last nus rivulatus, and Dzikowski et al. (2003) years, from these, the following can be reported that multi-annual changes in the drawn: parasite communities of the same spe- A- Global studies: Many protozoan para- cies.Scholz (1999) studied some parasites in sites infect fishes (opalinids, coccidea, dac- cultured and feral fish. He only selected a tylosomes, trypanosomes, Hixamida, Myxo- few parasites of each major group of fish sporea, Microspora) (Azevedo et al, 1993; parasites, i.e. protozoans, myxosporeans, Bassey, 2011; Abowei and Ezekiel, 2011, helminths and parasitic crustaceans. Stewart Eli et al, 2012) and monogenean trematodes and Bernier (1999) studied the common par- (Reed et al, 1996) but all of them were never asites, diseases and injuries of fresh water recorded from humans.Yamaguti (1937; fishes in the Northwest Territories and Nu- 1938; 1939; 1940; 1941) reported the hel- navut. Hoffman (1999) gave brief descrip- minth fauna of Japan. Tsai and Cross (1966) tions of North American freshwater fish and reported Anisakis-like larvae from the ma- their parasites. Salgado-Maldonado et al. rine fishes of . A survey on anisaki- (2005) reviewed the helminth parasites in dae larvae found in fishes and cephalopods freshwater fish from the Papaloapan river caught in the Seto Inland Sea and the Japan basin, Mexico. They presented a checklist Seawas published by Hatada (1970) while for these helminthes based on the previously the dynamics of the larvae, Ani- published records and original data. sakis simplex invasion in the South Western Chandra (2006) reviewed a parasitological Baltic herring was studied (Grabda, 1974). investigation and research in Bangladesh. Davey (1971) had given a revision of the Considerable works mainly on systematic, genus Anisakis. In 1977, Hauck discussed nature of infestation and pathology of differ- the occurrence and survival of the larval ent groups of fish parasites had been done. A nematode Anisakis spp. in the flesh of fresh total of 290 species of parasites had been frozen, brined and smoked pacific herring. recorded from freshwater and marine fishes Bhaibulaya and Siwaraksa (1979) reported in Bangladesh. Two helminth parasites of Anisakis larvae from the marine fishes of the zoonotic importance Dibothriocephalus la- Gulf of Thailand. In 1983, Bagrov described tus and spinigerum were also morphological variability of larvae of Ani- reported.

250 Moles (2007) summarized the published Alkawari et al. (1996) worked on the biodi- records of parasites of freshwater and ma- versity of helminth parasites of fishes in rine fishes of Alaska and the surrounding Arabian Gulf Parasitic fish diseases in Egypt seas through 2006. Of 601 species of fish were reported by Eissa (2002). E1-Said- believed to inhabit the waters of Alaska, Hassanine (2000) reported two digenetic parasites were listed for 89 species. Ghaffar trematodes from some fishes in the Gulf of (2014) studied the seasonal variation and Aqaba. El-Labadi et al. (2006) recorded the histopathology of helminth parasites in the intestinal digenetic trematodes of some fish- fish, Lutjanus argentimaculatus (Forsk, es from the Gulf of Aqaba, Red Sea. 1775) red snapper, and reviewed some of the Mhaisen and Al-Nasiri (2012) reviewed previous works that dealt with fish parasites the parasites of fishes at Salah Al-Deen around the world especially in Pakistan. Province, Iraq. They reported 84 parasite Muzzall and Whelan (2011) presented a species; 6 ciliophorans, 21 myxozoans, 17 synopsis and literature review for fishes par- monogeneans, 6 trematodes, 9 cestodes, 10 asites of Great Lakes from 1871-2010.The nematodes, 5 acanthocephalans, 2 annelids synopsis was based on information from the and 8 arthropods. These were recorded from literature (articles, theses, dissertations, re- 21 fish species, among which 18 fish species ports) on the major parasite groups (proto- belonged to the family Cyprinidae. Mhaisen zoans, digenetic trematodes, monogeneans, et al. (2012) reviewed the fish parasites of aspidobothreans, cestodes, nematodes, acan- Al-Furat fish farm, Babylon province, Iraq. thocephalans, , copepods, molluscs). These fishes included the B- Local and Arabian studies: Digenetic (Cyprinus carpio), the grass carp (Cteno- trematodes of marine fishes from the Red pharyngodonidella) and the silver carp (Hy- Sea received great attention from several pophthalmichthys molitrix) as well as the workers. Nagaty and his group reported on mullet (Liza abu). The parasitic fauna in- these digeneans from 1930 until 1972 (Na- cluded 60 valid parasite species: 10 protozo- gaty, 1930; 1937; 1941;1942; 1948; 1954; ans, 3 myxozoans, 29 monogeneans, 1 trem- 1956; 1957; Nagaty and abdel-Aal, 1961; atode, 5 cestodes, 3 nematodes, 2 acantho- 1962a,b,c; 1964; 1972). Ramadan continued cephalans, 6 crustaceans and 1 mollusc. The working on digeneans of Red Sea fishes, common carp was found to harbour 56 spe- where he described several new species and cies of parasites, the grass carp 25 species, revised the (Ramadan, 1982; the silver carp 25 species and the mullet six 1983; 1984; 1985; 1986; 1988; Saoud and species. Ramadan, 1985). Fish parasites and human health: Fish of Al-Bassel (1997) studied the helminth par- most species are intermediate hosts of tran- asites infecting some fishes from the Medi- sient forms of a vast number of parasites. terranean Sea. He investigated 465 fish be- Muscles of fish belonging to the most valu- longing to 7 families and 9 genera caught able species are habitat of larvae, whereas from the Libian coastal waters near Misu- parasites very often occur in their gastroin- rata. Al-Bassel (2003) surveyed the helmin- testinal tract, and other internal organs, th parasites of fish from inland waters in the as well as on their skin.The most dangerous Fayoum Government, Egypt. He investigat- are those which, when ingested with courses ed 450 fishes belonging to 7 genera and 7 made of fish or marine invertebrates may species for helminth parasites. Of these, 220 undergo developmental stages in the internal fish were found to harbour Acanthocephala organs or muscles of humans, thus including (14%), cestodes (16.22%), (10.66 unpleasant influence of life threatening dis- %), Monogenea (1.77%) and nematodes eases. A risk of infection with parasites usu- (6.22%). ally occurs with the consumption of live

251 parasite-containing flesh, liver or gonads in tion-associated changes to phenotype the form of traditional courses prepared may influence the outcome of intraspecific from raw or slightly salted or marinated fish, or interspecific interactions and have im- as well as cold-smoked products, which portant consequences for individual perfor- were not frozen prior to smoking. Among mance, whether measured by an ecologist in the vast number of fish products, only a few terms of evolutionary fitness or by a fisher- are pathogenic to humans, including mainly ies manager as reductions in stock biomass. digeneans, tapeworms and nematodes. Di- Andréoletti et al. (2011) reported that for geneans use fish, shell fish and crustacea as fishery products caught from fishing grou- a second intermediate host and humans or nds in the Baltic Sea, four groups of viable other feeding on fish, as the defin- parasites present possible health risks, Ani- itive host. Tapeworms parasitizing in fish sakis simplex, Contracaecum osculatum, occur as adult forms in the gastrointestinal Pseudoterranovadecipiens and Diphyllobo- tract or in the form of larvae in various tis- thrium spp. The incidence of transmission of sues. The final host of larvae living in the disease from fish to humans is dependant muscles and organs of fish are most often upon several factors including the type of predatory fish, , mammals feeding on the parasite, the susceptibility of the host fish, and sometimes humans. Larvae of and environmental factors. some species of nematodes, parasitizing fish, All of the important Fishborne zoonotic may also be harmful to humans. The Clupe- parasites (FZPs) are helminths, the majority idae, Scombrids and Gadoid fish may be in- of which are trematode. There are strong fested with Anisakis simplex larvae. The lar- linkages of FZPs to poverty, pollution and vae, curled into flat spirals, rises primarily in population growth. For example, in some the peritoneum, liver, and gonads and some- areas, shortage of fuel in poor homes may times also in the abdominal segments of permit only partial cooking of raw fish. muscles (Sikorski, 2004). Overcrowding in endemic areas lead to dete- Adams et al. (1997) reported that the most rioration of the environment and increased important of helminths acquired by humans pollution of surface waters with sewage, from fish are the anisakid nematodes (par- night-soil, and animal excreta. Development ticularly Anisakis simplex and Pseudoterra- can also create increased risks; for example, nova decipiens), cestodes of the genus Di- dams create reservoirs highly favourable for phyllobothrium and digenetic trematodes of snail vectors, as well as fish, which are the the families , major transmitters of fishborne trematodes. and Nanophyetidae. Stewart and Bernier ; The liver flukes: The caus- (1999) mentioned that the effect of parasites ative agents of human include on the value of the fish is perhaps greater Looss, 1907 (in East than their impact on human health. Also, and Southeast Asia), viverrini they added that parasites can reduce the val- Stiles and Hassall, 1896 (in Southeast Asia), ue of fish to harvesters by damaging the O. felineus Blanchard, 1895 (in Russia and skin, infesting the meat, or spoiling the fla- Eastern Europe), and Metorchis conjunctus vour or condition of the fish. Barber and Looss, 1899 (in North America). A total of Poulin (2008) reported that some parasites 17 million people around the world are esti- may be responsible for acute, economically mated to be infected with these liver flukes important outbreaks of disease in exploited (WHO, 1995). fish populations or reduce productivity Liver flukes have long been known to through nutritional effects; others may be cause serious disease in certain areas of the responsible for chronic long-term changes in world. Cholangitis, choledocholithiasis, pan- population structure. They added that infec- creatitis and cholangiocarcinoma are the ma-

252 jor clinical problems, associated with the (1993) reported in 35 patients long chronic pattern of these infections. Alt- with acute gallstone pancreatitis and/or chol- hough the extent of the problem is difficult angitis whom underwent endoscopic sphinc- to assess due to the lack of comprehensive terotomy and considered its endemicity epidemiological studies, particularly in there. Morsy and Al-Mathal (2011) reported Southeast Asia, there is evidence that the C. sinensis in Egypt. greatest risk factor for humans, is the con- b- : is a particularly sumption of raw or improperly cooked or serious (Rim, 1982b; Kaewkes, processed fish, that is increasing in some 2003) and is highly prevalent in Southeast regions, facilitated partly by population mi- Asia including Thailand, Laos, Cambodia grations and partly by commercial provision and South Vietnam; about 9 million people of these products (WHO, 2004). are estimated to be infected globally a- Clonorchis sinensis: the Chinese liver (Yossepowitch et al, 2004). In Thailand, it is fluke, is the most important species of fish- widespread in the north and northeastern borne zoonotic parasite in EastAsia (Rim, regions. The number of infected people in 1990a; Hong, 2003). In 1947, the estimated the northeastern region alone was estimated number of infected people worldwide was in the 1960s to beover 3.5 million (Wykoff about19 million (Stoll, 1947), but more re- et al, 1965), and this figure seems to have cently it has been estimated to be about 7-10 changed little; the estimated number of in- million (Crompton, 1999). In Japan, this fected people is currently about 6 million parasite was formerly quite prevalent, but (Sripa et al, 2003). In Laos, the Mekong has been successfully controlled since the River basin is the most heavily infected area 1960s (Hong, 2003). (Chai et al, 2005). In Vietnam, several In , clonorchiasis is distributed in a southern provinces such as Phu Yen have total of 24 provinces, municipalities and au- reported infections, with prevalences above tonomous regions (Chen et al, 1994). 10% (De et al, 2003). Guangdong Province (including Hong c- : was first de- Kong) and Guangxi Zhuang Autonomous scribed from a naturally infected cat and Region, Heilongjiang, Jilin and Liaoning subsequently from a man in 1892 (Beaver et provinces are the areas with most reported al, 1984); it is now recognized as a natural infections (Yu et al, 2003). In a nationwide parasite of dogs, cats, foxes, and pigs in survey, the prevalence of C. sinensis was eastern and southeastern Europe and the 0.4% among almost 1.5 million people ex- Asiatic parts of Russia and common also in amined (Xu et al, 1995). In Taiwan, clonor- southern, central, and eastern Europe, Tur- chiasis was formerly endemic in three areas, key and Siberia west of the Ob River, in- Mei-Nung in the south, Sun-Moon Lake in cluding Tomsk and Tyumen. In 24 regions the center and Miao-Li in the north (Cross, of the Ukraine, the number of human infec- 1984), but the current status is unknown. In tions reported between 1952 and 1968 was Vietnam, clonorchiasis has been endemic 9340 (Rim, 1982b). The global incidence in mainly in the north, especially along the Red 1947 for this parasite was estimated to be River Delta including Haiphong and Hanoi about 1.1 million (Stoll, 1947); the incidence (Rim, 1982a). In southern parts of Vietnam, appears to have not changed significantly C. sinensis is not reported, although opis- and is now estimated to be about 1.6 million thorchiasis is reported to be endemic (De et (Yossepowitch et al, 2004). al, 2003). Besides, Morsy and El Maridi d- Metorchis conjunctus: the Canadian liv- (1978) in Jordan reported zoonotic C. sinen- er fluke, is a parasite of carnivorous mam- sis among Palestinian refugees in Al-Baqaa mals in Canada and USA (MacLean et al, Camp. In Saudi Arabia, Al Karawi et al. 1996). Human infections with this fluke

253 have occurred in Canada since 1946 (Ya- situated. The contributing factors promoting maguti, 1958), particularly in aboriginal carcinogenesis include ingestion of carcino- populations from Quebec to Saskatchewan, gensor co-carcinogens, and host endogenous and the eastern coast of Greenland (Mac- influences such as malnutrition, immunolog- Lean et al, 1996; Behr et al, 1998) ical defects, and genetic factors (Watanapa Disease and public health impact: The he- and Watanapa, 2002). patic lesions and clinical manifestations in The histopathological changes include ade- infected people are similar for all the liver nomatous hyperplasia of the biliary epitheli- fluke infections (Rim, 1982b ).Bronchial um, thickening of the bile duct wall, peri- asthma and allergic lesions are encountered ductal with eosinophils and in early stages, along with painful enlarge- round cells and fibrosis in the portal areas. ment of the liver, congestion of the spleen, A large number of flukes can cause obstruc- and local eosinophilia in the wall of bile tion of the biliary tract. Based on 70 nec- ducts in chronic and severe infections. Bile ropsy cases in Thailand, hepatomegaly was stones may form around eggs and cause remarkable in most chronic and severe cases cholecystitis and colicky pain. Carcinoma of of , with marked dilatation the bile duct or the pancreas, with metasta- and hypertrophy of the bile ducts (Sripa, ses into theepigastric lymph nodes, is re- 2003). sponsible for of some patients. Inflammation of the bile duct and cell infil- The adult worms of C. sinensis and O. vi- trations may be secondary to super imposed verriniare found commonly in the intrahe- bacterial infections; suppurative cholangitis patic bile duct, some in the gall bladder and is frequently the end result and the infection along the biliary tract of infected humans. may extend into the liver parenchyma caus- The main pathogenesis in the biliary tract is ing hepatitis. Adenomatous and fibrous hy- mechanical, chemical, and immunological perplasia, seen in the bile ducts, can also oc- irritation by the worms (Li et al, 2004). This cur in the pancreatic duct. Moderate infec- results in obstruction of the bile duct and tion levels with less than 100 worms of O. bile stasis, periductal inflammation, and viverrini are usually asymptomatic. Howev- cholangitis. Histopathologically, the enlarge- er, infections with hundreds or thousands of ment of the bile duct, periductal fibrosis, ad- worms can cause right upper quadrant pain, enomatous hyperplasia, and cystic degenera- , flatulence, fatigue, dyspepsia, pain tion are the most prominent features (Lee et over the liver, jaundice in some patients and al, 1978). In mild infections, the patient is a moderate elevation of the body tempera- usually asymptomatic. Heavy infections, ture (Mairiang and Mairiang, 2003). however, can cause significant symptoms High incidences of cholangiocarcinoma, causing the patient to seek medication. based on both necropsy and liver biopsy da- Jaundice, indigestion, epigastric discomfort, ta, have been reported for O. viverrini. For anorexia, general malaise, diarrhea and mild instance, in Khon Kaen, northeastern Thai- fever are common clinical symptoms. Com- land, the incidence of cholangiocarcinoma is plications such as pyogenic cholangitis, bili- estimated to be 129 per 100,000 males and ary calculi, cholecystitis, liver , 89 per 100,000 for females, compared with pancreatitis and cholangiocarcinoma, are one to two per 100,000 in western countries often associated with infection (Sripa, 2003). (Vatanasapt et al, 1990). Jaundice usually Among these, cholangio-carcinoma is the occurs in cases with heavy infections and most serious. It arises from metaplastic especially when there is carcinomatous changes of biliary epithelial cells and usual- transformation with an increased biliary ob- ly occurs in the secondary intrahepatic bile struction. ducts, where the flukes are preferentially

254 Patients with cholangiocarcinoma may pre- mans. Human infections were also recorded sent obstructive jaundice, fever, and acute from Siberia, Europe, China, and Taiwan. complications such as cholangitis, acalcu- In Japan, prevalence has decreased since the lous cholecystitis and generalized bile peri- 1970 s, except in a few foci as areas sur- tonitis. Using hamsters as an experimental rounding the Hamana Lake (Ito et al, 1991). animal model, it was shown that chemical- In Russia, M. yokogawai is endemic in the carcinogens such as dimethynitrosamine Amur and Ussuri valleys of Khabarovsk ter- which is present in fermented fish including ritory, where the prevalence in ethnic minor- ‘Pla ra’ plays the role of an‘initiator’, and O. ity groups varies between 20-70% (Yu and viverrini acts as a ‘promoter’ for the devel- Mott, 1994). Intestinal histopathology is opment of cholangio-carcinoma (Thamavit characterized by villous atrophy and crypt et al, 1994). hyperplasia, with variable degrees of in- Intestinal flukes; heterophyids: These mi- flammatory reactions (Chai, 1979). In light nute intestinal flukes of the family Hetero- infections, fatigue and mild gastrointestinal phyidae are parasites of birds and mammals. troubles such as epigastric pain, diarrhea and A large number of species have been report- anorexia are present; while in heavy infec- ed from humans, among which Metagoni- tions, abdominal cramps, malabsorption and mus yokogawai and heterophy- weight loss may occur. es are generally considered the most im- Other Metagonimus spp. infecting man: M. portant species (Yu and Mott, 1994). The takahashii Suzuki, 1930 was reported in Ja- importance of these flukes is being increas- pan from mice and dogs fed with metacer- ingly recognized through recent studies from cariae encysted in fresh water fish other than the (Belizario et al, 2001), from sweetfish (Chai and Lee, 2002). M. miyatai Thailand on Haplorchis taichui (Waikagul, was first found in Japan in 1941, but its tax- 1991; Sukontason et al, 2001) and from Ko- onomic significance was later established to rea on several species including Heterophyes be a distinct species (Saito et al, 1997). nocens and Metagonimus spp.(Chai and Lee, b- (v. Siebold, 1991; 2002). Although generally not consid- 1852) Stiles and Hassal, 1990. It was first ered of significant clinical importance rela- found by Bilharz in 1852 in the intestine of a tive to the liver flukes, several heterophyid child in Egypt. This species is seen in Nile species, including Stellantchasmus falcatus, Delta, Middle East and Turkey. It is parasitic Haplorchis spp., and Procerovum spp., can in humans and fish-eating birds and animals. cause significant pathology, often fatal, in It is characterized by having 70-80 digitate the heart, brain, and of humans spines on the genital sucker. First intermedi- (Africa et al, 1940). The exact mechanisms ate host is the brackish water snail Pirenella of pathogenesis responsible are not clear but conica and the second is Mugil and Tilapia may be related to invasion of the circulatory fishes. Khalil Bey (1924, 1933) was the first system by worm eggs. Disease is usually Egyptian scientist who discovered Hetero- related to worm burdens, which in some phyes Heterophyes life history in Egypt. The cases can be very heavy (MacLean et al, infection was common in northern parts of 1999). the Nile Delta especially in lakes as Idku, a- (Katsurada, Maryut and Manzala (Youssef et al., 1987). 1912): The genus Metagonimus is character- Kuntz and Chandler (1956) found that in the ized by a laterally deviated ventral sucker Nile Delta H. heterophyes infected man, and absence of ventrogenital apparatus or dogs, cats, rodents and birds. Then after, genital sucker. Four species, namely M. many authors dealt with H. heterophyes and yokogawai, M. takahashii, M. minutus, and heterophyiasis. Nagaty and Khalil (1961) M. miyatai, have been reported from hu- and Khalil et al. (1964) used Yomesan in

255 treating heterophyiasis. Sheir and Aboul- armed with gonotyl and chitinous spines Enein (1970) used Niclosamide in treating (Yamaguti, 1958). Five species, namely Ha- heterophyiasis. Paperna et al. (1978) report- plorchis taichui, H. pumilio, H. yokogawai, ed microsporidian infection in the cyst wall H. pleurolophocerca, and H. vanissimus, are of Heterophyes metacercariae encysted in responsible for human infections (Yu and fish. Rifaat et al. (1980) in villages on the Mott, 1994); the first three are the most im- lakes of Borollos and Manzalla reported a portant. H. taichui Chen, 1936 was first de- rate of 2.4% heterophyiasis. The mean prev- scribed from birds and mammals from cen- alence of heterophyid infections in the vil- tral Taiwan (Faust and Nishigori, 1926). lages of Khuzestan, southwest Iran, was Human infections are now commonly found found to be 8% (2-24% in range). In post- throughout Asia (Velasquez, 1982). H. pu- mortem examination of carnivores in the milio (Looss, 1986) was originally described same areas, 14.2% of jackals, 33.3% of fox- from birds and mammals in Egypt; it is also es, and 2.5% of dogs were infected with H. now known to be distributed in Asia (Yu heterophyes and M. yokogawai (Massoud et and Mott, 1994). H. yokogawai (Katsuta, al, 1981). Human infections were also re- 1932) was described from dogs and cats fed ported in Japan (Kagei et al., 1980) and the with metacercariae from mullet in Taiwan; Republic of (Chai et al, 1986; Chai human infections have now been reported and Lee, 2002). from many Asian countries, Australia, and c- Heterophyes nocens Onji and Nishio, Egypt (Velasquez, 1982). Haplorchid infec- 1916 was first reported in Japan from exper- tions are known to be asymptomatic or of imental dogs and cats fed with metacercariae very mild intestinal manifestations. from the mullet M. cephalus, and it is now The intestinal flukes-echinostomes: Trem- known to occur elsewhere in the Far East. atodes of family (Poche, This species is distinguished from H. heter- 1926) are intestinal parasites of birds and ophyes by the smaller number (50-62) of mammals. At least 30 genera and more than spines on the gonotyl. The snail and fish 200 species are known; about 15 species in- hosts are brackish water species (Chai and fect humans (Yamashita, 1964 and Huffman Lee, 2002). In April 1990, a highly endemic and Fried, 1990). There are 11 reported fish- focus was discovered on a southwestern borne echinostome species of which Echi- coastal island, where 42 (43%) of 98 resi- nostoma hortense and Echinochasmus ja- dents examined were infected (Chai et al, ponicus are the most important (Yu and 1994a). Another endemic area with a preva- Mott, 1994 and Chai and Lee, 2002). Most lence of 75% was later found in a western human echinostome infections have been coastal village (Chai et al, 1997). Several reported from Asia and the Western Pacific, other coastal areas and many islands have but infections probably occur also in Africa been added to the list of endemic areas (Chai (Yu and Mott, 1994).The disease is general- et al, 2004). In Japan, human H. nocens in- ly mild, but ulcerations and bleeding in the fections were reported from Kochi, Chiba, stomach or may occur, as in E. Yamaguchi, Chugoku and Hiroshima Pre- hortense infection (Chai et al, 1994b). fectures. Recently, two lakeside villages of a- hortense (Asada, 1926): Mikkabi-cho, at the north end of Hamana The genus Echinostoma Rudolphi, 1809 is Lake, Shizuoka Prefecture, were found to characterized by an elongated body and have prevalences of 7.5 and 10.5% (Kino et presence of a head collar with dorsally unin- al, 2002a; b). terrupted crown of spines. More than 95 d- Haplorchis spp.: The genus Haplorchis species are known (Yamaguti, 1958), and is characterized by the presence of only one seven species infect humans (Yamashita, testis and a ventro-genital-sucker complex 1964; Yu and Mott, 1994). E. hortense has

256 27 or 28 collar spines around the oral sucker, c- Nanophyetus salmincola, Chapin, 1927: and two tandem slightly lobulated testes. It It belongs to the Nanophyetidae Dollfus, was first described from synanthropic in 1939, and infects various mammals includ- Japan, and then from humans and rodents in ing humans, the dog, cat, raccoon, and fox, the Republic of Korea (Chai and Lee, 2002) and three species of birds on the Pacific and China (Yu and Mott, 1994). An infec- coast of NorthAmerica and Canada, and tion rate of 22.4% has been reported among Eastern Siberia. It is minute, pyriform, and residents of Cheongsong-gun, Republic possesses two large testes in the posterior ofKorea (Chai and Lee, 2002). In a survey in half of thebody. Its snail host is Oxytrema Liaoning province, northeast China, 6 out of silicula and the second hosts are salmonid 10 hospitalized patients with hepatitis who (trout, salmon) and non-salmonid fish (Mil- had eaten raw loach were found to be infect- lemann and Knapp, 1970). Nanophyetiasis is ed, and 69.7% of loach, Misgurnus anguilli- endemic in the far-eastern part of Russia in- caudatus, examined from a local market cluding Amur and Ussurivalleys of Khaba- were infected (Yu and Mott, 1994). rovsk territory and north Sakhalin (Yu and In experimental rats, infection produces Mott, 1994). In local ethnic minorities, the villous atrophy, crypt hyperplasia, inflam- prevalence is 20%, and reaches up to 60% in mation of the stroma, and decreased vil- some localities. In the USA, 20 human cases lus/crypt ratios (Chai and Lee, 2002). Muco- have been reported since 1974 (Eastburn et sal damage is generally more severe than in al, 1987). Infected people may experience heterophyid infections. Abdominal pain, di- mild diarrhea, abdominal discomfort, and arrhea, and fatigue are the major symptoms. eosinophilia. Chai et al. (1994b) reported that a patient Cestodiases: : This is with E. hortense infection suffered from se- the most important fish-borne zoonosis vere ulcerative lesions and bleeding in the caused by a cestode parasite. Species of the duodenum. genus (Order Pseudophyl- b- Echinochasmus japonicus (Tanabe, lidae, Family Diphyllobothriidae) are re- 1926): The genus Echinochasmus Dietz, sponsible for most reported cestode infec- 1909 is characterizedby a plump, sometimes tions in humans. The zoonosis occurs most elongated, body and the presence of a head commonly in countries where it is a frequent collar with a dorsally interrupted crown of practice to consume raw or marinated fish. spines (Yamaguti, 1958). Among the 40 At least 13 of about 50 species of Diphyllo- species known, only four species have been bothrium have been reported from humans. found infecting humans; Ech. japonicus, All are gastrointestinal parasites as adults in Ech. perfoliatus, Ech. liliputanus and Ech. a variety of piscivorous birds and mammals. fujianensis (Yu and Mott, 1994). Ech. ja- Diphyllobothriasis is considered a mild ill- ponicus was first reported in Japan from ex- ness and is not normally reportable; the un- perimental animals fed metacercariae from derstanding of the global distribution of this freshwater fish; it is now known to be dis- parasite infection is somewhat fragmentary tributed widely in the Far East, particularly and based on limited human and fish surveys in humans in the Republic of Korea (Chai or clinical case reports. Sturchler (1988) es- and Lee, 2002) and Anhui, Fujian, Guang- timated that there were about 9 million hu- dong,Guangxi, and Jiangsu provinces of man infections in the 1970s, but the accura- China (Lin et al, 1985). In six counties of cy of this figure currently is doubtful, and Fujian and Guangdong provinces, China, the may even be an underestimate. Although infection rate among residents was 4.9% Diphyllo-bothrium is generally associated (178/3639) (Yu and Mott, 1994). with cold water intermediate and definitive hosts, there are sporadic case reports from

257 warm localites including the Middle East zoonosis has declined overall, especially in and Malaysia (Abo-Shehada and Ziyadeh, the former ‘hotspot’ Scandinavian countries, 1991; Rohela et al, 2002), although the it persists in several regions (Dupouy-Camet sources are not clear; confusion with sparga- and Peduzzi, 2004). Currently Switzerland, num infections makes reports from such are- Sweden, Finland and Estonia reported more as somewhat problematical. than 10 cases per year, while Lithuania, Po- Globally, the incidence of human infec- land, Hungary, Italy and France average 2– tions has declined in recent years, particular- 10 cases annually.Only sporadic cases occur ly in North America (Kingston and Kil- in Norway, Austria, and Spain. Most of the bourn, 1989; Dick et al, 2001) and Europe cases in Switzerland, France and Italy occur (Dupouy-Camet and Peduzzi, 2004). Until in the Alpine Lakes region. In Finland, the 1982, diphyllobothriasis was a reportable national prevalence has declined since 1981 disease in the USA and CDC estimated that when it was 1–4% (Raisanen and Puska, about 125-200 cases occurred during the pe- 1984).Diphyllobothriasis is a common infec- riod 1977–1981 (Ruttenber et al, 1984). tion in Far-East Russia, where D. kleba- CDC estimates only several dozen cases oc- novskii is considered the important zoonotic curring annually in the USA (Deardorff, species (Muratov and Posokhov, 1988; 1991). During 1981, CDC reported that 52 Lloyd, 1998 and Muratov, 1990). The para- people residing in the west coast states of site is widespread in all the major river the USA became infected with Diphyllo- drainages east of the Urals, including those bothrium, apparently from fresh salmon of the Lena, Kolyma and Indigirka rivers shipped from Alaska. Surprisingly, 1% of (Suvorina and Simonova, 1993). school children in Baton Rouge, Louisiana The Amur River region is also an endemic carried D. Latum according to a survey area (Khodakova et al, 1996), as are the (Christian and Perret, 1974). A recent dis- coastal area of the Okhotsk Sea where hu- covery reported in France revealed that a man prevalences range from 1.0 to 3.3%. A patient became infected with D. nihon- major new focus has apparently developed kaiense from a salmon (Oncorhynchusketa) during the 10 years since the completion of imported from the Pacific Coast of Canada the Krasnoyaek Reservoir on the Enisel Riv- (Chai et al, 2005). er; one survey revealed a prevalence of 7.7% Most reported human infections in South in people living along the reservoirs hore America occur in Chile, Peru and Argentina (Ko, 1995). Diphyllobothriasis was fre- (Von Bonsdorff, 1977). The first case in quently reported in Japan, especially along Chile was reported by Neghme et al. (1950). the coast of the Sea of Japan, averaging The prevalence of diphyllobothriids in some about 100 cases per year since the 1970s Chilean lake districts ranges from 0.1 to (Oshima, 1984). Until recently, most infec- 2.8% (Torres et al, 2004). The presence of tions were considered due to D.latum. How- the marine species D. pacificum in humans ever, recent taxonomic studies strongly sug- in Peru has been estimated to be about 1.6% gest that the majority of infections are due to (Miranda et al, 1967), which is in line with D.nihonkaiense (Yamane et al, 1989). Infec- recent findings from the analysis of ancient tions by other species also cannot be ruled coprolites of the Chiribaya Culture popula- out, such as D. yonagoensis are known in tions (700-1476AD) in southern Peru (Holi- the region (Yamane et al, 1981; Kamo et al, day et al, 2003), suggesting that this zoono- 1988). tic species has persisted in the region for a As an example, in 1996 a large outbreak in very long time. Shizuoka Prefecture was discovered to be Analysis of 20 years of diphyllobothriasis caused by another diphyllobothriid, Diplog- survey in Europe indicated that while this onoporus grandis. Since 1894 there have

258 been more than 100 cases caused by this 2001). Despite its apparent global decline, species in Japan (Kino et al, 2002a; b).Until diphyllobothriasis appears to have increased recently, diphyllobothriasis has not been in some countries (Torres et al, 2004). The considered common in the Republic of Ko- reasons for its persistence or re-emergence rea. Between 1921and 2001, only 28 cases are not always clear. Zoonoses such as that were reported and the results of a national caused by Diphyllobothrium spp. exist with- prevalence survey for parasites revealed a in a continuum that links animal and human prevalence of only 0.004%. However, the populations, and this equilibrium may be growing demand for fresh salmon, and the disturbed by activities such as the intensifi- strong cultural fondness for raw fish may cation of fish production, environmental al- alter the status of this zoonosis in the future terations, translocation of human and animal (Lee et al, 2001). As with Japan, the system- populations, tourism, changes in fish mar- atics of diphyllobothrids recovered in Korea keting (export and distribution) systems, and are uncertain because most cases are at- cultural changes in eating habits (Dazak et tributed to D. latum, although the fish al, 2000; Murrell, 2002). sources (salmonids) are not typical for this Certain projections indicate that the future species.Because of their generally broad worldwide demand for fish and fish- host specificities, Diphyllobothrium life cy- products will increase substantially (FAO, cles are maintained primarily in nature inde- 1992), creating increasing pressure to ex- pendent of humans, and therefore the ces- ploit the marine environment for food tode is not affected much by elimination (Deardorff, 1991). The growing awareness from the human population (Torres et al, of the nutritional benefits of fish and fish 2004). The host preferences of the various products, the preferences in many countries marine or freshwater diphyllobothriid spe- for raw or lightly cooked foods, and the ris- cies may be relatively specific for either pis- ing affluence in both developing and devel- civorous birds or a specific spectrum of oped countries make this a reasonable pre- mammals such as bears, cetaceans, pinni- diction. This increased demand may increase peds or humans, and this can be very im- the risk of diphyllobothriids entering the portant in transmission and dissemination human food chain by increasing the harvest- (Dupouy-Camet and Peduzzi, 2004).Other ing and export of fish from areas of high en- risk factors associated with infection are oc- demicity. Higher risks for urban populations cupation, age and gender (Sagua et al., may also arise because of the incentive for 2000). Although infection rates are usually exporters to ship fresh (non-frozen) fish by highest in adults, especially males, there are air to gain a competitive edge in the market reports of high rates in children (Khodakova (Deardorff and Overstreet, 1990; Kaferstein, et al, 1996). 1994; Nawa et al, 2001). The global market An increasingly important factor in intro- in fish exports is quite large. For example, ducing or sustaining the zoonosis in human Europe and Canada, both endemic for di- communities is the contamination of the lo- phyllobothriids, supply about one-third of cal aquatic environment with faeces (Cross, the USA demand for seafood. In Korea, the 2001). The discharge of improperly treated demand for salmonids has increased with sewage from lake-side dwellings, hotels and rising per capita incomes, and this has ships is an important source of contamina- stimulated increased production of farmed tion with eggs. Domestic animals, especially salmonids. This increase in production con- dogs, are another important source of envi- cerns public health workers because of its ronmental contamination and may help to link to the risk of diphyllobothriasis, which maintain a natural D. latum cycle, which can has occurred more frequently in the country be amplified by human activities (Dick et al, in recent years (Lee et al, 2001).

259 It should be emphasized here, however, vironment with eggs. This led eventually to that there is little to implicate farm-raised substantial areas becoming endemic for di- salmonids in transmission of diphyllobothri- phyllobothriasis (Torres et al., 2004). How- ids to humans; wild salmonids are at highest ever, the identity of the Diphyllobothrium risk of becoming infected with diphylloboth- reported from salmonid fish in Chile has riids and represent a major reservoir of in- been questioned because elsewhere D. latum fection. Freshwater non-salmonids are also fish intermediate hosts are typically non- important in certain regions, especially for salmonids (e.g. pike, perch) and it has been infection of D. latum. Even among salmonid suggested that the Diphyllobothrium infect- hosts not all species play a similar role. For ing trout and humans in Chile may be anoth- example, Oncorhynchus nerka that spends er species, which is endemic to the region, extended periods in freshwater lacustrine such as D. dendriticum (Dick et al, 2001). systems prior to descending to the ocean, They concluded that based on existing data may be more important than other species of and the results from their own experimental Pacific salmon in transmitting Diphylloboth- and field work, the life cycle of D. latum rium ursi because of its greater vulnerability became well established in Canadian wil- to human and animal fishing. derness lakes without the participation of Seemingly unrelated environmental chan- humans, and that distribution has changed ges may also have unexpected effects on the little during the past 100 years, giving an epidemiology of this zoonosis. It has been evidence that favors a pre-European intro- suggested that the increase in infections by duction in NorthAmerica. They suggested, D. pacificum during the 1975-2000 period in however, that phylogenetic analysis of the Northern Chile was related to the cyclic ap- genotypes of D. latum from Alaska, Siberia pearance of ElNino phenomena in the East- and Europe may be the best means for set- ern Pacific, which not only affect fish popu- tling the issue. lations but also that of the primary definitive There is general agreement among experts host, the sea lion (Sagua et al, 2000). Anoth- in this field that the overriding obstacle to er example is the increased risk of diphyllo- clarifying the distribution, host-associations, bothriid infection of fish because of growing and epidemiology of diphyllobothriids, es- marine populations in the North- pecially D. latum, is the poor state of the west Pacific, a result of the 1972 Marine systematics of the genus (Holiday et al, Mammal protection Act (Deardorff, 1991). 2003).The great difficulty in differentiating Effects of climate changes like these re- morphologically the plerocercoids and the flect the complexity of the aquatic food adult strobila or proglottids of the various webs and the unpredictability of responses species, has produced confusion among re- by biological systems. The stocking of im- searchers about the specific host ranges of ported fish in new aquatic habitats may be a the species, and therefore hindered the un- significant risk for spreading diphyllobothri- derstanding of the epidemiology of the zo- ids, by providing potential intermediate onoses in North and South America, Far- hosts in the event of egg contamination. The East Asia and Eurasia (Torres et al, 2004). appearance of D. latum in Argentina and Misunderstandings of the host associations Chile has been attributed to the introduction for the freshwater species, D. latum and D. of rainbow trout (Oncorhynchus mykiss) and dendriticum have caused misinterpretations brown trout (Salmo trutta) in the early 20th of their epidemiology in specific locales. century from North America. Research carried out in recent years has Later these fish became infected by immi- convincingly demonstrated that the fish in- grants and tourists who, through poor sani- termediate hosts for D. latum are primarily tary practices, contaminated the aquatic en- nonsalmonidfish such as pike and perches,

260 while D. dendriticum utilizes salmonid and Life cycle and distribution: The higher- coregonid species. The sites of pleurocer- level taxonomy of the superfamily Asca- coid infection within the fish also differ be- ridoidia is uncertain (Fagerholm,1991; An- tween the two species (Andersen and Gib- derson, 1992), but molecular studies using son, 1989; Dick et al, 2001). mitochondrial DNA (mtDNA) and nuclear Confusion over D. latum in Japan was re- ribosomal DNA (rDNA) sequences provide solved when careful study of the diphyllo- provisional support for a monophyletic bothriids from man was identified as a new origin of the family Anisakidae, which in- species, D. nihonkaiense, from salmon (On- cludes genera Anisakis and Pseudoterranova corhynchus gerbuscha and Oncorhynchus (Nadler and Hudspeth, 2000). Anisakids typ- masu) and the species D. yonagoensis from ically utilise marine mammals or piscivorous marine fish (Yamane et al, 1986; Kamo et birds as definitive hosts, with aquatic inver- al, 1988). In Siberia in the 1980s, it was tebrates and fish as intermediate or paratenic also discovered that diphyllobothriasis hosts. Adults of Anisakis spp. are found transmitted from salmonid fish (O. gor- mainly in the of ceta- buscha and O. keta) was not, as long be- ceans (dolphins, porpoises and whales), and lieved, D. latum but a new species, D. adults of Pseudoterranova spp. in pinnipeds klebanovskii (Muratov and Posokhov, 1988). (seals, sea lions and walrus), although the The discovery of D. nihonkaiense in salmon definitive host range of most species is still (O. keta) from the Canadian Pacific Coast incompletely known (Anderson, 1992). Eggs (Gulf of Alaska) is a good example of why are shed in the faces and embryonate and the current taxonomy and mapped distribu- hatch in the ocean, releasing free swimming, tions of the diphyllobothriids are questiona- and apparently third stage larvae (Køie et al, ble, since this species may have long been 1995). The larvae are ingested by crusta- present in this region-just undetected be- ceans, such as decapods, copepods or am- cause of confusion with other Diphylloboth- phipods, where they grow within the haemo- rium species. coel. Fish and cephalopod molluscs become Nematodiasis: a- Anisakiasis: Anisakiasis infected by eating crustaceans containing refers to infection of people with larval stag- third stage larvae, which penetrate the intes- es of nematodes belonging to the families tine and invade the tissues of the paratenic Anisakidae or Raphidascarididae. Although host, where they may continue to grow or human infection have been reported with become, encapsulated (Anderson, 1992). worms from a number of species within the- Definitive hosts are usually infected by eat- se families (Bouree et al, 1995), the two ing fish or cephalopods containing the lar- genera most often associated with ani- vae. As people usually become infected with sakiasis are Anisakis and Pseudoterranova. anisakids by eating larvae contained within Anisakiasis occurs when people ingest third the paratenic host, the distribution of larval stage larvae found in the viscera or muscle nematodes within the tissues of the host is of a wide range of fish and cephalopod mol- epidemiologically important. This distribu- lusc species.Humans are accidental hosts in tion appears to be very variable, and may be the life cycle, and the parasites almost never affected by the species of parasite (Ander- develop further within the human gastroin- son, 1992), the fish species infected and the testinal tract. Nevertheless, anisakiasis is a environmental conditions to which the fish serious zoonotic disease, and there has been are subjected after capture (Roepstorff et al, a dramatic increase in its reported preva- 1993). lence throughout the world in the last two Some studies have found that larval nema- decades. todes migrate from the visceral organs to the muscle after the death of the paratenic host,

261 and that migration may be enhanced by the ing (Acha and Szyfres, 1987; Oshima, cold storage or processing of ungutted fish. 1987). Others, however, have not been able to A. simplex can cause different diseases in demonstrate post-mortem migration of lar- humans. Acute anisakidosis is probably vae in the paratenic host (Cattan and Carva- caused by an inflammatory and/or allergic jal, 1984; Roepstorff et al, 1993). At least response in the digestive tract mucosa with three species have been described within the abdominal pain. It can also induce IgE me- A. simplex: A. simplex (sensustricto), found diated reactions with several clinical mani- in the northern Atlantic, A. simplex complex festations ranging from urticaria and angi- found in the northern Pacific and southern oedema to anaphylaxis. Chronic anisakidosis waters and Anisakis pegreffi, found in the results from abscesses or eosinophilic granu- Mediterranean Sea (Mattiucci et al, 1997). lomas caused by parasite invasion (Alonso Paggi et al. (1991) also described three spe- et al, 1997; Audicana et al, 2002; Farahnak cies within the Pseudoterranova complex: et al, 2002). Anisakiasis occurs through the P. decipiensA in the north east Atlantic and world, with foci in north Asia and western Norwegian Sea, P. decipiens Cin the north Europe.Over 90% of about 20,000 cases of west Atlantic and Barents Sea, and P. decip- anisakiasis were reported from Japan (where iens B throughout northern waters. Further approximately 2000 cases are diagnosed an- genetic studies are required to confirm the nually),with most of the rest from the Neth- geographical and host ranges of these spe- erlands, Germany, France and Spain (Feld- cies, and to establish their relationships with meier et al, 1993). As diagnostic methods other species of Anisakis and Pseudoterra- improve, however, more cases are being re- nova, which have been described on mor- ported from other areas of the world, includ- phological criteria. A very large number of ing the USA (Amin et al., 2000), Canada fish species act as paratenic hosts for species (Couture et al, 2003), Chile (Mercado et al, of Anisakis and Pseudoterranova. 2001), New Zealand (Paltridge et al, 1984) Pathology and epidemiology: Clinically, and Egypt (Cocheton et al, 1991). human anisakiasis can take a number of In the last 30 years, there has been a forms, depending on the location and histo- marked increase in the prevalence of ani- pathological lesions caused by the larvae. sakiasis worldwide. This is probably due to Larvae may remain in the gastrointestinal a number of factors. First, the increase in tract, without penetrating the tissues, causing reported cases coincides with new diagnostic an asymptomatic infection, which may only techniques, particularly endoscopy; prior to be discovered when the worms are expelled the development of the gastrofiberscope by coughing, vomiting or defecating (Acha many cases of gastric anisakiasis were prob- and Szyfres, 1987). In invasive anisakiasis, ably misdiagnosed (Oshima, 1987). Second, larvae penetrate the gastric or intestinal mu- the increasing global demand for seafood cosa, or more rarely other sites such as the and a growing preference for raw or lightly throat (Amin et al, 2000). There is some ev- cooked food, especially in many western idence that gastric invasion is more often countries, increase the risk of parasite expo- associated with infections by Pseudoterra- sure. Third, there has been speculation that nova spp.and intestinal invasion with infec- greater regulatory controls over the exploita- tions by Anisakis spp. (Oshima, 1987). tion of marine mammals has led to increas- Symptoms of gastric anisakiasis usually ap- ing population sizes of potential definitive pear 1-7 hr after consumption of fish, while hosts (McCarthy and Moore, 2000), alt- intestinal anisakiasis usually manifests 5-7 hough it should be recognised that the rela- days after fish consumption. In both cases, tionship between definitive host population there is severe pain, with nausea and vomit- size and parasite population size is not

262 straightforward for parasites such as ani- in the Philippines and Thailand, and sporad- sakid nematodes, which have a complex, ic cases have been reported in Korea, Japan, multi-host life cycle. Taiwan, India, Iran, Italy, the United Arab b- Capillariasis: Capillariasis is a zoonotic Emirates, Spain, and the United Kingdom parasite caused by two different species: C. (Cross, 1998; Austin et al, 1999). hepatica and C. philippinensis. C. hepati- In Egypt, the first case of intestinal capil- ca is transferred through the fecal matter of lariasis was reported by Youssef et al. infected animals and can lead to hepatitis. C. (1989) in a 41-year-old female from Cairo, philippinensis is transferred through ingest- the second case was a 38-year-old female ing infected small freshwater fish and can living in Lower Egypt reported by Mansour lead to diarrhea and emaciation. According et al. (1990). Many subsequent caseshave to Cross (1992), 1884 confirmed cases of the been reported from different parts of Egypt, disease caused by this nematode were doc- including Cairo (El-Dib et al, 1992; Ahmed umented in human beings from 1967 to the et al, 1999) and the Menouf area (Austin et end of 1990; 110 cases were fatal. Moravec al, 1999; Anis et al,1998). In Upper Egypt, (2001) redescribed and evaluated the sys- the first reported case was a female patientin tematic status of C. philippinensis. the Assiut Governorate (Khalifa et al, 2000) Typically, unembryonated eggs are passed and the second case was two sisters from the in the human stool and become embryonated El Menia Governorate (El-Karaksy et al, in the external environment; after ingestion 2004). Attia et al. (2012) presented an over- by freshwater fish, larvae hatch, penetrate view of human infections with Capillaria the intestine, and migrate to the tissues. In- philippinensis and a newemerging parasite gestion of raw or undercooked fish results in in Upper Egypt. infection of the human host. The adults of C. Pathology and epidemiology: Intestinal philippinensis (males: 2.3 to 3.2 mm; fe- capillariasis is a life-threatening disease in males: 2.5 to 4.3 mm) reside in the human humans which causes severe enteropathy , where they burrow in the (Cross, 1998). Worms can be found in the mucosa .The females deposit unembryonat- lumen, the mucosa, or in the crypts of ed eggs. Some of these become embryonated Lieberkuhn in the human jejunum. The most in the intestine, and releaselarvae that can common pathological features are the thick- cause autoinfection. This leads to hyperin- ening of the intestinal wall, the prominence fection (a massive number of adult worms). of the vessels, the atrophy of the crypts, and C. philippinesis is currently considered a the flattening of the villi (Sangcha et al, parasite of fish eating birds, which seem to 2007). The infestation of the small bowel by be the natural definitive host http://www. this parasite results in the severe derange- cdc.gov/parasites/capillaria/biology_c_phili- ment of intestinal functions, which leads to ppinensis.html). This highly pathogenic par- weight loss, chronic (continuous or intermit- asite, that causes serious illness in human tent) diarrhea, abdominal pain, borborygmi, beings, is known to be distributed in eastern, muscle wasting, cachexia, weakness, and southern, and southeastern Asia and north- edema (Lu et al, 2006; Saichua et al, 2008). ern Africa (Philippines, Thailand, Japan, Diagnosis of fish zoonotic parasites: Diag- Korea, Taiwan, India, Iran, Egypt) (e.g., nosis of liver fluke infections can be made Chitwood et al, 1968; Pradatsundarasar et by the recovery of eggs from feces by cello- al, 1973; Mukai et al, 1983; Hoghooghi-Rad phane thick smear (Chai et al, 1982) or et al, 1987; Chen et al, 1989; Youssef et al, Kato-Katz techniques (Hong et al, 2003). 1989; Lee et al, 1993; Kang et al, 1994; However, the eggs must be differentiated Khalifa et al, 2000). More than 2,000 cases from those of heterophyids and from various of have been reported other opisthorchiid species, a task which re-

263 quires considerable training and experience, recently been applied to the diphyllobothri- and even then the lack of specific diagnostic ids. Molecular investigations have shown tools such as molecular probes presents a that the morphological variation seen within challenge (Lee et al, 1984; Ditrich et al, D. dendriticum populations has a genetic 1992). Serological tests such as ELISA us- basis (De Vos et al, 1990). Ribosomal genes ing excretory-secretory antigens are helpful have been identified that can differentiate in some cases (Choi et al, 2003). There is between the two most important freshwater interest in developing specific molecular or species, D. latum and D. dendriticum (De immunological methods to aid this task, but Vos and Dick, 1989). Molecular markers for such methods have not yet appeared or differentiating D. latum and D. nihonkaiense gained acceptance (Wongratanacheewin et have also been reported (Matsuura et al, al, 2003). However, progress in this area is 1992). Further efforts towards developing encouraging, for example, a PCR-based molecular tools for diagnostic use and for technique to detect snail and fish infections phylogenetic analysis should be strongly with O. viverrini, often a difficult task, has encouraged if many of the issues associated been reported (Maleewong et al, 2003). with this zoonosis, such as the origins and There are a number of gene sequences now distributions of D. latum are to be resolved. published in GenBank, which should spur Anaskiasis: Endoscopic examination can development of needed diagnostic tools. often be used to provide a definitive diagno- Intestinal flukes: The diagnosis is made by sis for gastric anisakiasis, but clinical diag- recovery of eggs in fecal examinations.Very nosis of intestinal anisakiasis is difficult and important issue related to heterophyids is the requires careful examination of clinical difficulty of differentiating the eggs from symptoms and patient history. From clinical those of the liver flukes in human fecal ex- symptoms, gastric anisakiasis is often misdi- aminations, which may cause inaccurate es- agnosed as a peptic ulcer, and intestinal ani- timates of the prevalences of both trema- sakiasis as appendicitis or peritonitis (Acha todes groups (Chai and Lee, 2002). New and Szyfres, 1987; Oshima, 1987). Although diagnostic techniques including PCR are immunological diagnosis of anisakid infec- needed to improve specific diagnosis of the- tion shows potential, it is complicated by se flukes. antigenic cross-reactivity with other ascarids Diphyllobothriasis: Human infection can (Iglesias et al, 1996). be easily identified by finding characteristic Capillariasis: Diagnosis of human infec- eggs or proglottids in feces. When species tion depends mainly on stool examination needs to be determined, restriction fragment for finding characteristic eggs, larvae or length polymorphisms PCR can be effective- adults in feces (Khalifa et al, 2000) or detec- ly used (Schotz et al, 2009). Although the tion of coproantigen by ELISA (El-Dib et identification of plerocercoids from fish by al, 2004),immunodiagnosis (Intapan et al, morphological criteria is very difficult 2010) or intestinal aspiration or biopsy (Lu (Margolis and Arthur, 1979), progress in et al, 2006). overcoming this obstacle has been made, Control and prevention: Strategies for pre- particularly for the freshwater species (Dick vention and control approaches are similar and Poole, 1985; Yamane et al, 1986; An- for all the liver flukes. The traditional hu- dersen et al, 1987; Andersen and Gibson, man habit of eating raw or improperly 1989). However, identifications based on cooked freshwater fish is a major reason for morphological characters for marine species sustaining the zoonosis in endemic areas and remain troublesome. Molecular approaches a seemingly intractable obstacle to control; that have proved so powerful in resolving health education efforts aimed at changing other parasite taxonomic problems have only such habits have not been very successful

264 (Guoqing et al, 2001; WHO, 2004). Current- et al, 1993); however, feasibility of the ly, the major strategies for community pre- method economically, and consumer ac- vention and control include fecal examina- ceptance appear to be obstacles to the use of tion and treatment of individual cases with this prevention method. Strategies such as (25 mg/kg, three times daily, use of chemotherapy to reduce morbidity, for 2–3 days), health education to instill the interrupting transmission, and reducing risky need to consume only cooked fish, and envi- human behavior (WHO, 2004) are reasona- ronmental sanitation through the building ble and logical. However, because of local and use of latrines in endemic areas. More constraints, deeply embedded cultural traits, recently, WHO (2004) has recommended and inadequate national priorities, it is prob- mass chemotherapy of people at risk in en- lematic whether this strategy will be imple- demic areas as the most practical and imme- mented sufficiently to have significant pub- diately effective control strategy. Mass lic health impact any time soon. Compound- chemotherapy with praziquantel (40 mg/kg ing this difficulty is a number of gaps in in a single dose) is highly efficient and gen- knowledge and technology that should be erally feasible to distribute (Lee, 1984). addressed to facilitate implementation of any Until more such control programs are im- control efforts: i- Improved diagnostic tools plemented, however, and followed over are badly needed, especially those that can time, the long-term effectiveness of this ap- differentiate various species; ii- Guidelines proach maybe problematic. Efforts to inter- for designing and implementing epidemio- rupt transmission at the intermediate host logical studies are needed in order to obtain level apparently have not been extensive to the impact data required by public health date, judging by published reports. Several agencies insetting priorities; iii- The role of projects have been conducted on pond fish reservoir hosts in maintaining transmission production in China, utilizing snail control in the absence of infected humans needs in- and drug treatment of infected members of vestigation in order to design sustainable the household, along with intensive health control strategies; iv- Social/anthropological education of the community on the risks of studies are needed to better understand the eating raw fish. cultural and behavioral traits of people with The effect on transmission over 2 years regard to food choices in order to develop was mixed, however, with a decline in prev- education strategies aimed at influencing alence in people, but only a modest impact risky behavior; v-Development of improved on snail populations, on the use of human aquaculture systems that can prevent or mit- feces as pond fertilizer and on the habit of igate the transmission of trematodes and vi- eating raw fish (Guoqing et al, 2001). In Long-term pilot control projects are needed Thailand, a FAO led HAACP approach to to compare efforts targeted at multiple high fish pond management was carried out that risk factors identified in risk assessment focused on water supply, fish fry, fish feed studies with the current mass chemotherapy and pond conditions to eliminate contamina- strategy. tion of the ponds with O.viverrini eggs and Control measures include treatment of in- snail infections. fected people, environmental sanitation, and A preliminary report indicated some suc- health education. The drug of choice is pra- cess with this intensive effort, but a full as- ziquantel; the efficacy of a single oral dose sessment of its sustainability over a period of10-20 mg/kg is satisfactory. Irradiation of of years is needed (Khamboonraung et al, the sweetfish by 200 Gy is highly effective 1997). Irradiation of fish to control infectivi- in controlling infectivity of metacercariae ty of metacercariae was tried for C. sinensis (Chai et al, 1995). The infection can be pre- (Lee et al, 1989) and O. viverrini (Sornmani vented by the avoidance of eating uncooked

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