World Distribution of Trichinella Spp. Infections in Animals and Humans

Veterinary Parasitology 149 (2007) 3–21 www.elsevier.com/locate/vetpar

World distribution of Trichinella spp. infections in animals and humans Edoardo Pozio * Department of Infectious, Parasitic and Immunomediated Diseases, Istituto Superiore di Sanita`, viale Regina Elena 299, 00161 Rome, Italy

Abstract The etiological agents of human trichinellosis show virtually worldwide distribution in domestic and/or wild animals, with the exception of Antarctica, where the presence of the parasite has not been reported. This global distribution of Trichinella and varying cultural eating habits represent the main factors favouring human infections in industrialised and non-industrialised countries. Human trichinellosis has been documented in 55 (27.8%) countries around the world. In several of these countries, however, trichinellosis affects only ethnic minorities and tourists because the native inhabitants do not consume uncooked meat or meat of some animal species. Trichinella sp. infection has been documented in domestic animals (mainly pigs) and in wildlife of 43 (21.9%) and 66 (33.3%) countries, respectively. Of the 198 countries of the world, approximately 40 (20%) are small islands far from the major continents, or city–states where Trichinella sp. cannot circulate among animals for lack of local fauna (both domestic and wild). Finally, information on the occurrence of Trichinella sp. infection in domestic and/or wildlife is still lacking for 92 countries. # 2007 Elsevier B.V. All rights reserved.

Keywords: Trichinella sp.; Epidemiology; Global; Domestic animals; Wild animals

1. Introduction (Murrell and Pozio, 2000; Bolpe and Bofﬁ, 2001; Marinculic et al., 2001; Djordjevic et al., 2003). Nematode worms of the genus Trichinella are one of Reliable epidemiological information on animal and the most widespread zoonotic pathogens in the world. human infections is not uniformly collected around the Infection by Trichinella spp. has been detected in world. Only a limited number of countries have domestic and/or wild animals of all continents, with the implemented an ofﬁcial recording system for human exception of Antarctica, where there is no record of the and/or animal infections in the last 50 years. In most parasite (Pozio and Murrell, 2006). This global countries, reporting of infection has been and continues distribution of Trichinella, together with different to be on a voluntary basis and relies on physicians, cultural eating habits, represents the main factor veterinarians, biologists, zoologists or epidemiologists favouring human infections in industrialised and non- who are working on these parasites. This often results in industrialised countries. Major political and economic fragmentary information. changes, revolutions and wars can contribute to an The occurrence of trichinellosis in humans is strictly increase in prevalence among the human population related to cultural food practices, including the consumption of raw or undercooked meat of different animal origin. Therefore, most of the epidemiological * Tel.: +39 06 4990 2304; fax: +39 06 4990 3561. data and ad hoc surveys on Trichinella spp. in domestic E-mail address: [email protected]. and/or wild animals are related to outbreaks in humans.

In fact, the presence of the parasite in domestic and wild 2.2. Congo DR (Zaire) animals is not sufficient in itself for the infection to occur in the human population. Only a single report of Trichinella sp. larvae in the Until recently, all Trichinella infections occurring in muscles of a spotted hyena (Crocuta crocuta)of animals and humans were attributed to Trichinella Marunga in the province of Katanga was documented in spiralis. Today, eight species (T. spiralis, Trichinella 1948 by Thienpont (Young and Kruger, 1967). In nativa, Trichinella britovi, Trichinella pseudospiralis, addition, an infection suggestive of trichinellosis was Trichinella murrelli, Trichinella nelsoni, Trichinella diagnosed in a man who had visited Congo (Levy et al., papuae, and Trichinella zimbabwensis) and three 1960). Even if these two reports are incomplete, they genotypes (Trichinella T6, T8 and T9) within two suggest that Trichinella sp. is circulating in this country. clades (encapsulated and non-encapsulated) are recognised in this genus (Pozio and Murrell, 2006; Zarlenga 2.3. Egypt et al., 2006). The aim of the present work is to review the In this predominantly Muslim country, the only information from the scientific and grey literature on the human outbreak of trichinellosis was documented in occurrence of Trichinella spp. infections in animals and French tourists following the consumption of pork from humans by country and to integrate the published a domestic pig in 1975 (Therizol et al., 1975), while a information with the most recent knowledge of the single human case was reported in Tanta (Antonios and parasite. The data is reported, in an alphabetical order, Salem, 1989). At the time of the outbreak, a prevalence by continent and country. When the information of of 4.5% was detected in domestic pigs slaughtered at the Trichinella species circulating in a country is available Cairo abattoir. During the period 1995–1999, the on the web site of the International Trichinella prevalence dropped to 1.7%. However, risk of infection Reference Center (ITRC), this is reported at the country can still be considered high because hundreds of level. In countries where Trichinella sp. infections have infected pigs correspond to this percentage (Morsy been documented in animals and/or humans, but the et al., 2000). Furthermore, high prevalence rates of aetiological agent has never been identified at the infection (up to 13.3%) have been detected in species level, the most probable species circulating in synanthropic rats from Alexandria abattoirs (Loutfy the country is suggested on the basis of the present et al., 1999). T. spiralis was identified in two stray dogs knowledge of the distribution area of Trichinella species (Mikhail et al., 1994) and in domestic pigs (La Rosa (Pozio and Murrell, 2006). et al., 1992; ITRC). Trichinella sp. larvae were detected in wolves from Sinai (Barakat et al., 1982), and the 2. Africa species may have been T. britovi. This epidemiological data suggest that both a domestic and a sylvatic cycle 2.1. Algeria occur in Egypt.

The majority of the human population is Muslim and 2.4. Ethiopia does not consume pork or meat from carnivores (i.e., the most important reservoir of Trichinella worms), and The Coptic religion is practiced by 35–40% of the trichinellosis has only been documented in 50 Ethiopian population and four outbreaks of trichinel- expatriates from France. There were six outbreaks losis have been documented following the consumption associated with the consumption of a domestic pig of warthog meat (Phacochoerus aethiopicus)(Perdomo (Gerard, 1946) and of wild boars (Sus scrofa)(Lanoire Gonzalez et al., 1986; Kefenie et al., 1988; Kefenie and et al., 1963; Verdaguer et al., 1963; Memin et al., 1968; Bero, 1992; Gelnew, personal communication). Non- Barabe et al., 1977; Michel et al., 1986). Only a single encapsulated larvae of Trichinella sp., probably T. case was documented in an Algerian person who zimbabwensis, have been detected in a farmed Nile consumed meat from a jackal (Canis aureus) infected crocodile (Crocodilus niloticus) from Lake Abaja with T. britovi (Nezri et al., 2006; ITRC). These reports (Pozio et al., 2007; ITRC). suggest that T. britovi infection occurs among wildlife of Algeria, although no surveys have been conducted. 2.5. Guinea The infection in the domestic pig could be related to the poor hygienic conditions of the time and to transmission T. britovi larvae were detected in a true civet (Viverra from wildlife to the domestic pig. civetta) and two African palm civets (Nandinia E. Pozio / Veterinary Parasitology 149 (2007) 3–21 5 binotata) from the Fouta Djallon Massif, Pilimini 2.10. South Africa Subprefecture (Pozio et al., 2005a; ITRC). No other data are available for either human or domestic animal Most epidemiological investigations have been infections. carried out on wildlife from the Kruger National Park, where Trichinella T8 has been detected in a spotted hyena 2.6. Kenya and in a lion, T. nelsoni in a lion and a mixed infection T. nelsoni and Trichinella T8 in another lion (Pozio et al., There have been several reports of Trichinella sp. 1994; ITRC). Trichinella sp. larvae were also detected in infections in humans in this country. Nearly 40 cases, an African civet (Civettictis civetta), black-backed jackal one fatal, were documented from 1959 to 1987 (Canis mesomelas) and in a multimammate rat (Praomys (Forrester et al., 1961; Forrester, 1964; Nelson, 1970; natalensis)(Young and Kruger, 1967; Young and Whyte, Hutcheon and Pamba, 1972; Okelo and Bhatt, 1987)in 1975). This infection has not been documented in either five outbreaks due to the consumption of pork from humans or domestic animals. bush pigs (Potamochoerus larvatus), probably infected with T. nelsoni. Another case report was the infection in 2.11. Tanzania UR a Japanese tourist, but it was not possible to identify the source due to the wide range of game meats he had A human outbreak with several deaths occurred from consumed (Nakamura et al., 2003). T. nelsoni has been the consumption of a warthog (Bura and Willett, 1977). detected in a wide spectrum of carnivorous mammals, T. nelsoni is widespread among wildlife, lion, leopard, including lion (Panthera leo), serval (Felis serval), bat-eared fox (Otocyon megalotis), cheetah (Acinonyx leopard (Panthera pardus), bush pig, spotted hyena, jubatus), spotted hyena, black-backed jackal and side-striped jackal (Canis adustus), striped hyena warthog (Sachs, 1970; Pozio et al., 1997; ITRC). This (Hyena hyena) and in a domestic dog (Nelson, 1970; infection has not been documented in domestic animals. Sachs, 1970; ITRC). The domestic cycle has never been 2.12. Tunisia documented. T. zimbabwensis could also be present in reptiles and mammals. Encapsulated larvae of Trichinella sp. (probably T. britovi 2.7. Mozambique ) were detected in wild carnivores, including genet (Genetta genetta), jackal (C. aureus), and mongoose (Herpestes ichneumon)(Fassbender and T. zimbabwensis has been detected in 20% of wild Mayer, 1974). This infection has not been documented Nile crocodiles of the lake Cahora Bassa (Pozio et al., either in humans or domestic animals. 2007). 2.13. Zimbabwe 2.8. Namibia In 1995, T. zimbabwensis was found in 256 of 648 Nile The genotype Trichinella T8 has been detected in a crocodiles (39.5%) farmed in 18 farms (62.1%) of the 29 lion of the Etosha park (Pozio et al., 1994; ITRC). In the existing in Zimbabwe at that time. In 2002, 11 (40.7%) of same area, Trichinella sp. larvae were detected in a the 27 crocodile farms still had infected animals (Pozio spotted hyena and in a black-backed jackal (Pozio et al., et al., 2002). Of 28 wild Nile monitor lizards (Varanus 1994). This infection has been never documented in niloticus) tested, T. zimbabwensis larvae were also humans and domestic animals. detected in five (17.6%) (Pozio et al., 2007; ITRC). Non-encapsulated larvae of Trichinella sp., probably T. 2.9. Senegal zimbabwensis, were detected in a lion of the Harare zoo (Chris Foggin, unpublished data). The infection has not Almost 90% of the Senegalese population is been documented either in humans or domestic animals. Muslim. Trichinellosis was reported however in nine Europeans in Dakar following the consumption of 3. America pork from a warthog (Gretillat and Vassiliades, 1967). Trichinella sp. infection, probably T. britovi,has 3.1. Argentina been detected in jackals and warthogs (Gretillat, 1970). There is no report of infection in domestic T. spiralis is widespread in domestic, synanthopic animals. and wild animals of Argentina and human outbreaks 6 E. Pozio / Veterinary Parasitology 149 (2007) 3–21 occur every year (Ribicich et al., 2005; ITRC). Reports domestic pigs, farmed wild boars and occasionally in of human infection were infrequent during the period wildlife (Appleyard et al., 1998). Control of infection at 1960–1990. However, between 1990 and 1999, 5217 slaughter is compulsory only for exported meat of pigs cases were documented. Ninety-one percent of these and horses. In addition, an innovative trichinellosis occurred in the central provinces of Buenos Aires, prevention program has been developed among Inuit Cordoba and Santa Fe (Bolpe and Boffi, 2001), where communities in Nunavik (northern Quebec) aimed at the highest prevalence in domestic pigs has been testing meat samples from harvested walrus at a reported, ranging from 0.01% to 0.03%. Today, the regional laboratory and rapid dissemination of results yearly incidence of trichinellosis in humans is around to the communities (Proulx et al., 2002). 1000 infections (Ribicich et al., 2005). This parasite has also been detected in wild boars (S. scrofa), foxes of the 3.4. Chile genus Pseudalopex and pumas (Puma concolor), in synanthropic brown rats (Rattus norvegicus) and High rates of human infection were common in the armadillos (Chaetophractus villosus)(Minoprio et al., early 1900s, but prevalence has progressively declined. 1967; Negme and Schenone, 1970; Ribicich et al., During the period 1991–2000, a total of 631 clinical 2005). At present, all slaughtered pigs are subjected to cases with four deaths (0.6%) were recorded. The HCl–pepsin digestion according the current legislation; incidence declined from 0.7 Â 100,000 in 1991 to however, backyard and free-roaming pigs escape from 0.2 Â 100,000 in 2000. During the same period, this control and represent the most important source of infection rates in pigs decreased from 0.017% in infection for humans. 1991 to 0.004% in 1998–2000 (Schenone et al., 2002). No infection has been detected in wildlife (carnivores 3.2. Bolivia and rodents) (Alvarez et al., 1970), but a single case of trichinellosis has recently been documented following Trichinella sp. larvae have never been reported in consumption of pork from a wild boar (Garcia et al., animals or humans from this country. Anti-Trichinella 2005). T. spiralis has been detected in synanthropic antibodies were detected in sera from domestic pigs brown rats and in cats and dogs (Ortega-Pierres et al., from different country regions (Bjorland et al., 1993; 2000; ITRC). Brown et al., 1996) and in the sera of seven asymptomatic people (Bartoloni et al., 1999). However, 3.5. Greenland (Denmark) the lack of documented infections in both humans and animals suggests the need for further investigation to T. nativa is widespread in both terrestrial and marine confirm the circulation of Trichinella sp. in animals and wildlife of Greenland (polar bears, arctic foxes, humans in Bolivia. walruses, and seals) and in sled dogs (Henriksen et al., 1994; La Rosa and Pozio, 1990; ITRC). 3.3. Canada Trichinellosis outbreaks occur for the consumption of walrus meat (Bohm, 1985; Moller et al., 2005). Trichinella spp. is widespread in Canadian both terrestrial and marine wildlife, but prevelance varies 3.6. Mexico considerably from one province to another (Rausch, 1970; Kim, 1983; Appleyard et al., 1998; Polley et al., Human trichinellosis frequently occurs in Mexico 2000). The yearly incidence of infections in humans is from the consumption of pork from domestic pigs. about 10–15 cases, due to the consumption of game According to published information, 766 infections meat from black bears (Ursus americanus) and walruses with 14 deaths were documented between 1952 and (Odobenus rosmarus). There has been no documented 1997 (Ortega-Pierres et al., 2000). The number of report of Trichinella sp. infection in domestic pigs in the infections has likely been underestimated as suggested last 10 years (Appleyard et al., 2002). T. nativa and by a serological survey where 1.9% of 954 serum Trichinella T6 are predominant in wildlife (ITRC), samples randomly collected in a rural area in 1997 were whereas T. murrelli has been detected only in the positive (De La Rosa Arana et al., 1998). The Vancouver area close to the border with the United prevalence of infection in domestic pigs detected by States. Non-encapsulated larvae, probably T. pseudos- artificial digestion in different Mexican states, ranged piralis, were detected in a bird (Alvin Gajadhar, between 0.0% and 6.0% from 1986 to 1999 (Ortega- unpublished data). T. spiralis has been detected in Pierres et al., 2000). Trichinella sp. infection is also E. Pozio / Veterinary Parasitology 149 (2007) 3–21 7 present in domestic and stray dogs and cats and in In Alaska, trichinellosis has been documented in synanthropic rats living nearby foci of porcine infection humans for the consumption of bear and walrus meat (Ortega-Pierres et al., 2000). T. spiralis was detected in (Margolis et al., 1979; Woodard, 1988). High pre- slaughtered horses in the State of Mexico (Arriaga et al., valence rates of T. nativa infections were documented 1995). No information is available on Trichinella sp. among terrestrial wildlife (polar, brown and black infection in Mexican wildlife. baears, arctic foxes, wolves, lynxes, and in some rodents), whereas low prevalence rates were documen- 3.7. United States ted among marine mammals (walruses and seals) (Rausch, 1970; La Rosa et al., 2003). Before the Second World War, the prevalence of trichinellosis reached 36% in examined human cadavers 4. Asia and the main source of infection was pork from domestic pigs where the prevalence of T. spiralis infection was as 4.1. Afghanistan high as 11.0% in garbage-fed pigs and up to 0.95% in farm-raised pigs (Zimmermann, 1970). Only 72 cases Trichinella sp. infection has been detected in several were reported during the period 1997–2001. The source wildlife species, including lynx, wolf, jackal, red fox, of infection was identified or suspected for 52 infected mongoose (Herpestes auropunctatus) and in Afghan people: 30 (43%) cases were associated with eating wild hedgehogs (Hemiechinus megalotis)(Kullmann, 1970). game (bear, cougar or wild boar meat), 12 (17%) cases Human infection has not been reported due to religious were associated with eating commercial pork products, practices which prohibit consumption of pork. No and nine (13%) cases were associated with eating non- infection has been documented in domestic animals. commercial pork from home-raised or direct-from-farm swine where U.S. commercial pork production industry 4.2. Cambodia standards and regulations do not apply (Roy et al., 2003; Nelson et al., 2003). Trichinella spp. infections are Anti-Trichinella antibodies have been detected in widespread in wildlife (e.g. black and brown bears, serum samples from persons of a rural population from cougar, raccoon, coyote, red and grey foxes, wolverine, this country (Pozio, 2001). The lack of documented fisher, mink, skunk badger, weasel, river otter, and wild infections in humans and animals suggests the need for boar) but the prevalence of infection varies considerably further investigation to confirm the circulation of these from one state to another. The domestic cycle is currently nematodes. very rare and infected pigs are usually from organic farms or from farms with very poor hygienic conditions. T. 4.3. China murrelli is the main etiological agent of infection in wildlife, although T. spiralis is still present, attesting to Trichinellosis is one of the most important food- the existence of the domestic cycle in the past. The borne parasitic zoonoses in China and many outbreaks freezing resistant species T. nativa and Trichinella T6 are with deaths are reported each year. Most of the present in wildlife from states close to the Canadian outbreaks occur in 10 provinces, including Yunnan, border. However, both T. nativa and Trichinella T6 have Henan, Tibet, Hubei, Sichuan, Guangxi, Jilin, Liaoning, been also detected in wildlife living in the Rocky Helongjiang, Neimonggol and Jiangxi. In these areas, Mountains and Appalachians (Pozio and Murrell, 2006; the domestic cycle is present and the prevalence of T. ITRC). T. pseudospiralis was detected in a vulture spiralis in pigs reaches 50%. Over 20,000 infections (Coragypus atratus) from Alabama and in a wild pig (S. were documented in the Yunnan province between 1964 scrofa) from Texas (Lindsay et al., 1995; Gamble et al., and 1997, with 213 deaths. In some regions, more than 2005). The only legislation in the U.S. regarding 10% of the local population have anti-Trichinella Trichinella are the processed product rules which govern antibodies (Takahashi et al., 2000). The most important cooking, freezing and curing methods for ready-to-eat source of infection is pork from domestic pigs, but pork and pork products. Special agreements exist with the infections are also related to the consumption of bear, European Union, Russia, Japan and several other dog, and goat meat (Takahashi et al., 2000; Liu and countries which allows to test pork intended for export Boireau, 2002). T. nativa has been detected in cats and using artificial digestion methods. A pilot ‘‘Trichinae dogs from northern regions of China (ITRC). The Certification Program’’ is currently in progress in 50 ‘‘Western Region Development of China’’ programme, farms. starting in the 1990s, provoked the migration and 8 E. Pozio / Veterinary Parasitology 149 (2007) 3–21 settlement of large numbers of people from central to one in 1962 and another in1972, of T. spiralis the western areas, which led in turn to an increased infections (note that at that time all Trichinella sp. quantity of pork products being taken from central to larvae were identified as T. spiralis) have been reported western regions, either commercially or privately. The in domestic swine from Tapanuli, the northern region areas of central China where potentially infected meat is of the island of Sumatra, where the local custom of exported to other provinces have high prevalence rates cooking or roasting meat greatly hinders the transmis- of T. spiralis infection in pigs, for example 6.8% in sion to humans (Holz, 1962, 1966). Since Indonesia is Hubei and 4.3% in Henan. This has led to a dramatic averylargecountryspreadoutamongmanyislands,T. increase in the size of the human population at risk for papuae could be present in domestic and wild pigs and trichinellosis in the western areas of China (Wang et al., other mammals as well as in crocodiles and monitor 2006). Canine trichinellosis has been recorded in 13 lizards. provinces, autonomous regions or municipalities and the average prevalence of infection in dogs slaughtered 4.6. Iran Islamic Rep in abattoirs was 16.2% (from 1.2% to 44.8%), with the highest prevalence located in northeast China. The Trichinella sp. infection has been documented in prevalence in dog meat sold at markets was 3.5% (988/ jackals, red foxes, stray dogs, brown bears, wild cats 27,898). The prevalence of Trichinella sp. infection in and wild boars of the Caspian region (Mobedi et al., brown rats varied from 1.1% to 15.1%. Trichinella sp. 1973; Hamidi, 1979). In the Isfahan region, Trichinella larvae were detected in 1.5% of black rats (R. sp. infection was detected in stray dogs, jackals, red norvegicus) and in 0.8% of wild mice (Apodemus foxes, stripped hyena and in one rodent (Meriones chevrieri). Trichinella sp. larvae have also been persicus)(Sadighian et al., 1973). Both T. spiralis and detected in foxes, bears, wild boars, weasels (Mustela T. britovi have been documented (Shaikenov and Boev, sibirica), raccoon dogs, bamboo rats (Rhizomys 1983). A single doubtful human infection from the sinensis), shrews (Tupaia belangeri) and moles (Para- consumption of pork from a wild boar has been also scapter leucurus)(Wang et al., 2007). reported (Mobedi et al., 1973). No information is available on Trichinella sp. infection in domestic 4.4. India animals.

Trichinella sp. infection has been documented rarely 4.7. Israel in India. Few reports showed the presence of encapsulated larvae of Trichinella sp. in domestic cats, Six human outbreaks of trichinellosis among the in a wild toddy cat (Paradoxurus hermaphroditus), in a Christian Arab population and immigrants from Thai- wild civet cat (Viverricula indica), and in domestic pigs land have been documented following consumption of (Kalapesi and Rao, 1954; Maplestone and Bhaduri, pork from wild boars (Eisenman and Einat, 1992; 1942; Parmeter et al., 1968; Schad and Chowdhury, Shimshony, 1997; Hefer et al., 2004; Marva et al., 1967; Schad et al., 1967). The non-encapsulated species 2005). Trichinella sp. (most probably T. britovi) T. pseudospiralis was detected in an Indian mole rat infection was documented in wild boars and up to (Bandicota bengalensis)(Shaikenov and Boev, 1983). 40% of jackals (Alex Marcovics, personal communica- Human trichinellosis was documented only once tion). No information is available on Trichinella sp. (Alipuria et al., 1996), but infection is likely under- infection in domestic animals. diagnosed in humans. 4.8. Japan 4.5. Indonesia Both T. nativa and Trichinella T9 are present in red Though most people are Muslims and do not eat foxes, raccoon dogs, Japanese black bears, brown bears pork, the island of Bali is one of the few areas of the and domestic dog (Kanai et al., 2006; ITRC). country where the majority of people are Hindu and Trichinellosis in humans was ﬁrst reported due to anti-Trichinella sp. antibodies were detected in 19.5% consumption of dog meat in 1957, then, three outbreaks of young children and teenagers (Chomel et al., 1993). occurred from the consumption of game meat (black Three Italian tourists visiting the island acquired and brown bears) (Yamaguchi, 1991; Takahashi et al., trichinellosis from the consumption of pork (de 2000). There is no information on the occurrence of Carneri and Di Matteo, 1989). Only two reports, these parasites in domestic pigs. E. Pozio / Veterinary Parasitology 149 (2007) 3–21 9

4.9. Kazakhstan animals and the etiological agent has not been identiﬁed, although T. britovi could be the etiological T. nativa and T. britovi circulate among red and agent circulating among wildlife. corsac foxes, wolves, jackals, martens, wild cats, lynxes and wild boars (Shaikenov and Boev, 1983; ITRC). T. 4.14. Malaysia pseudospiralis was documented in a corsac fox, in two crows, and in an eagle (Shaikenov and Boev, 1983; There is no published report of Trichinella sp. Pozio, 2005; ITRC). Trichinellosis in humans has been infection in animals or humans from Malaysia. documented following the consumption of pork from However, 84 students and teachers from Singapore wild boars (Boev et al., 1966; Genis, 1971). No acquired trichinellosis in 1998 while visiting a information is available on Trichinella sp. infection in neighbouring Malaysian island (Pozio, 2001), suggest- domestic animals. ing that the parasite is circulating among local swine.

4.10. Korea Republic (South) 4.15. Myanmar (Burma)

Trichinellosis was documented in three persons who Trichinella sp. infection occurs among domestic consumed raw meat from a badger (Meles meles) pigs, but the prevalence of infection is unknown and the infected with T. spiralis (Sohn et al., 2000; 2003; etiological agent has not been identified (Watt et al., ITRC). T. spiralis was also detected in a wild boar (Sohn 2000). No information is available on Trichinella sp. et al., 2003). No information is available on Trichinella infection in wildlife and humans. sp. infection in domestic animals. 4.16. Syrian AR 4.11. Kyrgyzstan Limited outbreaks of trichinellosis have been T. nativa was detected in a red fox (Shaikenov and reported in Christian villages due to consumption of Boev, 1983). No information is available on Trichinella wild boars (Pozio and Murrell, 2006). No information is spp. infection in humans and domestic animals. available on Trichinella sp. infection in wildlife and domestic animals. 4.12. Laos 4.17. Tajikistan Three trichinellosis outbreaks have been documented in humans from consumption of pork from domestic T. britovi was documented in a red fox (Shaikenov pigs (Sicard et al., 1976; Sayasone et al., 2006; and Boev, 1983). No information is available on these Barennes et al., 2006). The last outbreak involving parasites infection in domestic animals and humans. approximately 600 people occurred in the Udomxay province in the northern region of the country in 2005 4.18. Thailand (Barennes et al., 2006). T. spiralis is likely quite common in free-ranging pigs mainly in the Northern T. spiralis infection occurs frequently in domestic region of the country even if the information is very animals (pigs and dogs) and humans primarily in limited and only two isolates from an infected person northern mountain minority tribes. More than 7500 and from a domestic pig have been identified (ITRC). infections with 97 deaths occurred in about 130 outbreaks No information is available on Trichinella sp. infection (morbidity rate 0.04 per 100,000 people), since 1962; in wildlife. however, this figure is considered an underestimation of the number of cases (Kaewpitoon et al., 2006). 4.13. Lebanon Approximately 200–600 human infections occur annually in northern Thailand during communal feasts Large outbreaks have occurred in Christian villages celebrating the Thai New Year, though few of them have from the consumption of pork from wild boars and been documented. This parasite sometimes occur in domestic pigs (Merab et al., 1952; Matossian et al., synanthropic rats and wild pigs (S. scrofa) and have been 1974; Blondheim et al., 1984; Olaison and Ljungstrom, also reported in a black bear (Ursus thibetanus) and in a 1992; Haim et al., 1997). No information is available on squirrel (the species is unknown) which was the source of Trichinella sp. infection in wildlife and domestic an human outbreak (Khamboonruang, 1991). The 10 E. Pozio / Veterinary Parasitology 149 (2007) 3–21 occurrence of this infection in a squirrel is not surprising, 1970, 2002 and 2004 (Van De et al., 2006). The last since these rodents eat carrion when starved. A human outbreak occurred in Quai To (Tuan Giao district, Dien outbreak for the consumption of pork from a wild pig was Bien province) suggesting the occurrence of the reported to have been caused by T. pseudospiralis domestic cycle in the northern areas of the country (Jongwutiwes et al., 1998; ITRC). Recently, T. papuae (Nhan and Van De, 2004). No information is available was identified as the etiological agent of trichinellosis on the prevalence of this infection in wildlife and involving 19 people after eating raw wild pig (Kusolsuk domestic animals. et al., 2006). Even if the identification of T. papuae needs further confirmation, it is noteworthy to mention that two 5. Europe outbreaks occurred in Thailand for the consumption of meat from a monitor lizard (Varanus nebulosus) and a 5.1. Austria turtle (the species name is unknown) (Khamboonruang, 1991). The last human outbreak of trichinellosis occurred in 1970 following the consumption of a pig from a family 4.19. Turkey farm fed with the flesh of an infected fox (Hinaidy, 1978). Between 1952 and 1982, Trichinella infection Limited human outbreaks of trichinellosis have been was detected in 12 backyard or free-ranging pigs documented following the consumption of pork from (Hinaidy, 1978, 1983). No infected pigs reared in wild boars in Istanbul (13 cases), in Antalya (more than Austria have been detected in the last 24 years. Both T. 40 people) and Bursa (seven people) (Merdivenci et al., spiralis and T. britovi infections occur in wild boars and 1977; Heper et al., 2005; Pozio and Zarlenga, 2005). red foxes (ITRC). The largest outbreak (about 500 infected people) occurred in Izmir for the consumption of meatballs 5.2. Azerbaijan made with beef and pork from domestic pigs (Ozdemir et al., 2005; Turk et al., 2006). T. britovi was the T. britovi infection has been documented in one red causative agent (Ozdemir et al., 2005; ITRC). Trichi- fox, one wolf and one jackal (Shaikenov and Boev, nella sp. larvae were detected in domestic and wild pigs 1983). No information is available on the prevalence of and pork products (Nazli and Inal, 1987). No infection in wildlife and domestic animals and humans. information is available on the prevalence of infection in wildlife and domestic animals. 5.3. Belarus

4.20. Turkmenistan Both domestic and sylvatic cycles occur in this country. Trichinella sp. infection has been detected T. britovi infection was documented in a jackal mainly in carnivores (red fox, wolf, raccoon dog, black (Shaikenov and Boev, 1983). No information is polecat, marten), but also in wild boars and in yellow- available on the prevalence of infection in wildlife necked mice. In the 1980s, the prevalence of infection in and domestic animals and humans. domestic pigs was 0.0005% (Skripova et al., 1992). Both T. spiralis and T. britovi have been reported in 4.21. Uzbekistan domestic pigs (Shaikenov and Boev, 1983). Between 1980 and 1989, the prevalence of human trichinellosis T. britovi was found in a jackal (Shaikenov and Boev, was 0.55 per 100,000 inhabitants (Skripova and 1983). A large outbreak of trichinellosis was reported Kovchur, 1994). for the consumption of pork from a wild boar (Kairov, 1965; Nadzhimiddinov et al., 1965). No information is 5.4. Belgium available on the occurrence of infection in domestic animals. Trichinella sp. infection has not been detected in domestic animals and only one outbreak was docu- 4.22. Vietnam mented in humans following the consumption of pork from a wild boar (Famere´e et al., 1979). Famere´e et al. Three trichinellosis outbreaks involving 68 people (1981) found Trichinella sp. larvae in 6.7% of wild who consumed raw pork from domestic pigs, have been boars, 2.2% of muskrats (Ondatra zibethica), 6.5% of documented in the northern region of the country in brown rats and 11.1% of black rats (Rattus rattus). E. Pozio / Veterinary Parasitology 149 (2007) 3–21 11

However, the parasite was not identified at the species slaughterhouse, however, none has been identified as level. Today, the sylvatic cycle seems to be rare, but belonging to the genus Trichinella. In 1996, a recently T. britovi larvae were detected in a wild boar prevalence of 0.1% was detected in red foxes from a (Schynts et al., 2006; ITRC). small area of Jutland, but the few recovered larvae were not identified at the species level (Enemark et al., 2000). 5.5. Bosnia-Herzegovina Today, this country has made an application to the European Commission to be recognised as a country Trichinella sp. infection is common in wildlife and in with a negligible risk for trichinellosis. free-roaming and backyard pigs. Human trichinellosis occurs quite frequently for the consumption of pork from 5.10. Estonia wild boars and pigs, with a yearly incidence ranging from 0.1 (in 2002) to 12 (in 1998) cases per 100,000 There is a high prevalence of infection of both inhabitants. More than 51 outbreaks (775 infected T. nativa and T. britovi in wildlife (badger, brown bear, people) have been reported in the last 14 years, with lynx, raccoon dog, red fox, wild boar and wolf) (Pozio several fatalities (Ravlija et al., 2006). Probably, both T. et al., 1998; ITRC). T. nativa was documented in two spiralis and T. britovi are circulating among animals. wild boars (Pozio and Kapel, 1999). However, infection in domestic pigs and humans is rare. From 1992 to 1999, 5.6. Bulgaria T. britovi infection was documented in six backyard pigs from small farms, one of which was the source of Both T. spiralis and T. britovi are widespread in infection for three people (Jarvis et al., 2001). wildlife (red fox, badger, wild cat, field mouse, wolf, Trichinella sp. infection also occurs in farmed fur brown bear, jackal, black rat stone marten, otter and animals (Miller et al., 2006). wild boar) and in free-roaming and backyard pigs (Kurdova et al., 2004; ITRC). T. pseudospiralis has been 5.11. Finland detected in one wild boar, red fox and badger (ITRC). Hundreds of infections in humans occur yearly for the The domestic cycle is still endemic in this country consumption of pork from wild boars and pigs. although the yearly incidence in swine is very low. The number of Trichinella-positive swine and swine herds 5.7. Croatia increased from the beginning of the 1980s until mid 1990s. Recently, there was a reduction in the number of There is a high prevalence of both T. spiralis and T. cases, and during the last few years the condemnation britovi in wildlife. Recently, a control program has rate was around 0.0001%. A high prevalence (up to strongly reduced the prevalence in domestic swine from 53%) of T. spiralis, T. nativa, T. britovi, and T. 3.6% to 0.0001%. T. pseudospiralis was detected in a pseudospiralis was detected in wild boars, lynxes, domestic pig (ITRC). About 30–50 cases of trichinel- wolves, brown bears, raccoon dogs, red foxes and losis are diagnosed in humans every year (Marinculic badgers (Oivanen et al., 2002; ITRC). Infections in et al., 2001). Currently, Croatia is following EU humans were not documented in the last 50 years. guidelines for the control of Trichinella sp. infection in susceptible animals for human consumption. 5.12. France

5.8. Czech Republic Both T. spiralis and T. britovi circulate in the red foxes and wild boars. Between 2000 and 2005, the No human infection has been documented in this seroprevalence for Trichinella sp. infection in 8000 wild country in the last 50 years, nor have infected pigs been boars ranged from 2% and 14% according to the detected. T. britovi was documented in the red fox and different departments; however, Trichinella sp. larvae wild boar (ITRC). were detected in less than 0.01% of the inspected animals (Boireau, 2005). In 2004, T. britovi was 5.9. Denmark detected in free-ranging pigs and wildlife (wild boar and red fox) of a remote area of Corsica (Boireau and Vallee, There is no report of Trichinella sp. infection in pigs 2004; ITRC). Human infections occur yearly from the since 1930. Occasionally, single nematode larvae have consumption of pork from wild boars (135 cases in 20 been detected after HCl–pepsin digestion at the outbreaks from 1975 to 2006) (De Bruyne et al., 2006); 12 E. Pozio / Veterinary Parasitology 149 (2007) 3–21 however, the most important source of infection for the 5.18. Italy French population was horse meat imported from abroad (2296 cases from 1975 to 1999) (Boireau et al., Currently, only the sylvatic cycle (T. britovi) occurs 2000; ITRC). The etiological agent of a human outbreak among wildlife (e.g. red fox, wolf, badger, marten and from the consumption of pork from a wild boar in the wild boar) and the parasite is seldom transmitted to Camargue was identiﬁed as T. pseudospiralis (Ranque backyard or free-ranging pigs (ITRC). In the last 58 et al., 2000; ITRC). In humans, trichinellosis has been years, only 13 backyard or free-roaming pigs were also documented for the consumption of game meat detected positive at the abattoir or were the source of imported from abroad (Ancelle et al., 2005). infection for humans (Pozio et al., 2001). T. pseudospiralis was documented once in two birds (Pozio et al., 5.13. Georgia 1999). Since 1948, infections in humans have been documented from the consumption of pork from wild Trichinella sp. infection has been documented in stone boars (198 cases) or backyard and free-ranging pigs martens, jackals, red foxes and corsac foxes and domestic (165 cases) and meat from the red fox (11 cases) (Pozio cats as well as in humans (Kurashvili et al., 1970). In the et al., 2001). The most important source of infection has last several years, cases of human trichinellosis have been been horse meat imported from abroad (1038 cases in increasing, with hundreds of infections per year (Iashvili the course of six outbreaks which occurred between Nino, personal communication). 1975 and 2005) (Pozio and Murrell, 2006). In 2005, a new focus of trichinellosis in humans due to the 5.14. Germany consumption of free-ranging pigs was reported on the island of Sardinia, previously considered free from this Only the sylvatic cycle (T. spiralis, T. britovi, T. pathogen (Pozio et al., 2006). pseudospiralis) currently exists, with a prevalence of 0.08–0.22% in the red fox, 5% in the raccoon dog, and 5.19. Latvia 0.009% in the wild boar (ITRC). Sporadic infections occur among people from the consumption of pork from Both the domestic and sylvatic cycles are present in wild boars and backyard pigs, originating always from Latvia. A high prevalence of the infection was found in the sylvatic cycle (Littman et al., 2006). wildlife (e.g. in 16–60% of red foxes), where T. spiralis, T. nativa and T. britovi were detected (ITRC). A 5.15. Greece signiﬁcant increase of T. spiralis infection was observed in domestic pigs from 1984 to 1990. Human trichi- Trichinella sp. infection has been documented only nellosis also increased dramatically during late 1980s in wildlife, stray dogs and rarely in backyard or free- and early 1990s, with hundreds of human infections and ranging pigs. Very few human cases have been fatal cases. This was caused by pork from backyard or documented since World War II and the last outbreak free-ranging pigs and wild boars (Viksna et al., 2002; occurred in 1982 (Sotiraki et al., 2001). Perevoscikovs et al., 2005).

5.16. Hungary 5.20. Lithuania

Today, only the sylvatic cycle (T. britovi and T. Both the domestic and sylvatic cycles have been spiralis) occurs among red foxes and wild boars (Sreter documented. Significant increases in Trichinella sp. et al., 2003; ITRC) and seldom in backyard or free- infection in pigs, from 0.0027% during 1981–1985 to ranging pigs. Human trichinellosis has been sporadi- 0.1% in 1993 has been reported. Today, the prevalence cally documented for the consumption of pork from in domestic pigs is 0.001%. There is a high prevalence wild boars from 1998 to 2003 (Tamos Sreter, personal of infection (T. spiralis, T. britovi T. nativa) in red foxes, communication). raccoon dogs, wolves, martens and wild boars (Malakauskas et al., 2007). Human trichinellosis 5.17. Ireland increased dramatically during late 1980s and early 1990s, with hundreds of human infections and at least T. spiralis infection occurs only in red foxes. No 14 fatal cases. It was primarily caused by pork, mostly infection has been documented in domestic pigs or from pigs grown in small family farms and not humans in the last 38 years (Rafter et al., 2005; ITRC). inspected for Trichinella sp. The number of human E. Pozio / Veterinary Parasitology 149 (2007) 3–21 13 infections has decreased significantly to an average of consumption of pork from domestic pigs and wild 30–50 cases per year (Bartuliene et al., 2005). boars. The yearly incidence, however, is currently decreasing (Sadkowska-Todys and Golab, 2005). 5.21. Macedonia 5.26. Portugal T. britovi was detected in a free-roaming pig (ITRC). Human infections from the consumption of pork from The sylvatic cycle (T. britovi) is present in Portugal wild boars, free-roaming and backyard pigs are sporadic. in both the red fox and in wolf (ITRC), whereas infection was only detected in a single backyard pig 5.22. Montenegro from Montalegre in 1966. There are only two reports of trichinellosis (five people in 1962 and one single person In the last several years, Trichinella sp. infection in 1967) caused by the consumption of pork from two increased in domestic pigs due to the importation of backyard pigs (Vieira, 1983). infected animals from Serbia. A large outbreak of trichinellosis occurred for the consumption of pork 5.27. Romania from a domestic pig in 2004. Small outbreaks occur for the consumption of pork from wild boars (Nebojsa Both the sylvatic (T. britovi) and the domestic (T. Kavaric, personal communication). spiralis) cycles occur (ITRC). Between 1990 and 1999, the yearly incidence of trichinellosis was 5.5 cases/105 5.23. Netherlands inhabitants, whereas the incidence was 0.15% in domestic pigs and 1.3% in wild boars (Olteanu, The sylvatic cycle (T. spiralis, T. britovi and T. 2001; Blaga et al., 2007). The main source of infection pseudospiralis) has been documented with a low for humans is pork from backyard and free-ranging pigs prevalence in the red fox and in wild boar populations and from wild boars (Blaga et al., 2007). (van der Giessen et al., 1998; ITRC). Trichinella sp. infection has not occurred in the Dutch pig population 5.28. Russia since 1979 (van der Giessen et al., 2001). There is no documented case of human trichinellosis in The T. spiralis, T. nativa, T. britovi and T. pseudospiralis Netherlands from the consumption of pork or pork infections are widespread in both wildlife and free- products from pigs reared in this country, nor for the roaming and backyard pigs, with prevalences varying by consumption of game meat. region and host species (Bessonov, 1994; Dovgalev et al., 1997; Apanova et al., 2004; ITRC). Trichinellosis is quite 5.24. Norway common with 4920 documented cases between 1996 and 2002. The main source of infection is pork from domestic Both T. nativa and T. britovi circulate among wildlife pigs and wild boars, meat from badgers, jackal, bears and (4.8% in red foxes, 11% in minks) (Davidson et al., 2006; domestic and stray dogs (Ozeretskovskaya et al., 2005). ITRC). Infections have also been documented in dogs and cats. There is no report of Trichinella sp. in domestic 5.29. Serbia pigs. No human case has been documented since 1940. A dozen cases of Trichinella sp. infections in pigs 5.25. Poland and 30–50 human cases occur each year. Fortunatley, this represents a decrease when compared to previous High prevalences of T. spiralis and T. britovi has years (for example, 232 human trichinellosis cases in been observed in the red fox, raccoon dog and wild boar 2002). Both T. spiralis and T. britovi have been detected (ITRC). Prevalence in wild boars is reported to be in red foxes and wild boars (Cuperlovic et al., 2005). 0.25%. The yearly incidence of T. spiralis in domestic pigs ranges from 0.0032 to 0.00036% (i.e., from 66 to 5.30. Slovakia 465 infected pigs per year) (Ramisz et al., 2001). Human trichinellosis due to the consumption of Trichinellosis and infections in domestic pigs are backyard pigs is reported every year (from 15 to about quite rare in this country. Between 1962 and 1999, only 100 cases/year) (Ramisz et al., 2001). From 1993 to one outbreak was related to the consumption of pork 2000, a total of 1178 human cases were linked to the from a pig fed with offal of wild animals and a large 14 E. Pozio / Veterinary Parasitology 149 (2007) 3–21

T. britovi outbreak for the consumption of dog meat of Agriculture Annual Reports, 1970–2003). T. spiralis, (Dubinsky et al., 2001; Reiterova et al., 2007; ITRC). T. T. nativa and T. britovi were detected in red foxes and pseudospiralis was detected during routine examination T. pseudospiralis in a lynx and wild boars (Pozio et al., at the slaughterhouse in four swine from a farm of 2004; ITRC). eastern Slovakia, where synanthropic rats and one cat were also infected (Hurnikova et al., 2005). T. britovi is 5.34. Switzerland prevalent in the red fox population, whereas, T. spiralis was detected only twice in red foxes. T. britovi infection has been detected in 0.9% of red foxes (Gottstein et al., 1997; ITRC). This parasite 5.31. Slovenia species was also found in lynxes and in a wolf, which have recently colonised the area (Gottstein Bruno, Neither cases of human trichinellosis, nor reports of personal communication). No infection was documen- Trichinella infection in domestic pigs have been ted in humans or domestic pigs in the last 50 years. All documented in the last 50 years. Red foxes and wild Trichinella sp. susceptible animals are tested at the boars, bears and badgers were found infected with T. slaughterhouse according to the EU legislation. britovi and T. spiralis was detected in a red fox (Albert Marinculic, personal communication; ITRC). 5.35. United Kingdom

5.32. Spain There has been no documented case of trichinellosis due to the consumption of pork or pork products from Human outbreaks (about 50–100 cases per year) pigs reared in this country for the last 50 years. The last caused by both T. spiralis and T. britovi, occur every year outbreak caused by the consumption of a local pig due to the consumption of pork or pork products from occurred in Liverpool in 1953 (Semple et al., 1954). In backyard pigs or pigs from organic farms. From 1990 to 2000, members of four households consumed pork 2001, seven outbreaks occurred due to the consumption salami illegally imported from Serbia and resulted in of autochthonous pigs; whereas from 1995 to 1998, a eight cases of trichinellosis (Milne et al., 2001). In total of 192 cases were linked to the consumption of wild England, Scotland, and Wales Trichinella sp. infection boar meat (Rodriguez-Osorio et al., 1999; Rodriguez de has not been detected either in swine reared in this las Parras et al., 2004). In 1998–99, Trichinella-infected countries, nor in wildlife as well in the last 50 years raw pork of unknown Spanish origin, imported to (Smith et al., 2003); however, the number of surveys in Germany, caused a human outbreak with 52 cases. wildlife is limited and only a small percentage of Trichinella sp. infection in swine is still present in many slaughtered pigs have been tested. In Northern Ireland, regions of Spain, and a dozen of cases are detected every Trichinella sp. infection was detected in two waste food year, but all infected animals are backyard or free- feeder pigs in 1975 and again in two pigs of the same ranging pigs. In wildlife, T. spiralis and T. britovi are farm in 1979, and T. spiralis larvae were detected in a highly prevalent and have been found in 3% of red foxes red fox in the County of Fermanagh in 2007 (Keith and 0.003% of wild boars (Pozio et al., 1996; ITRC). Hunt, personal communication; ITRC).

5.33. Sweden 5.36. Ukraine

Ten outbreaks of trichinellosis, involving a total of T. britovi and T. nativa are present in wildlife 504 persons, were reported between 1917 and 1969 and and T. spiralis in free-roaming and backyard pigs a few sporadic cases were also reported until 1978 (Kondratev et al., 1977; ITRC). Human outbreaks occur (Ringertz et al., 1962; Odelram, 1973; Rone´us, 1983; quite frequently, but no information is available on the Pozio et al., 2004). Most outbreaks were caused by the prevalence (Shelemba, 1997, 1999). consumption of pork or pork products (sausages) from small family farms of Sweden, and only one was due to 6. Paciﬁc the consumption of wild boar meat. In the past 30 years, among the approximately 3.5–4 million pigs slaugh- 6.1. Australia tered per year, sporadic cases of infection have been reported: 52 in 1970–1979, 67 in 1980–1989, eight in T. pseudospiralis was detected in marsupials and 1990–1999, and no cases in 2000–2003 (National Board birds of Tasmania (Obendorf et al., 1990; Obendorf and E. Pozio / Veterinary Parasitology 149 (2007) 3–21 15

Clarke, 1992; ITRC). The mainland of Australia, 7. Discussion however, has always been considered Trichinella-free and no autochthonous case has ever been documented in No information is available on Trichinella sp. humans, but this status is not based on any extensive infection in humans and domestic or wild animals epidemiological investigation on wildlife, but on from any other country of the world not reported above. limited investigations on synanthropic rats, domestic However, the lack of information for a country does not cats, pigs, dingoes and red foxes from Victoria and New mean that these zoonotic parasites are absent, but may South Wales (Waddell, 1969; Pozio and Murrell, 2006). instead reflect the lack of investigation. In the author’s Because T. papuae is widespread in wild pigs and opinion, Trichinella spp. could be ubiquitous in the saltwater crocodiles of Papua New Guinea, which is wildlife fauna (mammals, reptiles or birds) of these very close to Australia (less than 180 km of sea separate countries, whereas their presence in domestic animals the two countries) and the saltwater crocodile is also a and humans is relatively rare. In many cases, where marine animal, the status as Trichinella-free should be human infection is not reported, it could exist but may modified until more extensive studies are conducted. not be recognised by physicians. The list of hosts reported in the present review 6.2. Hawaii (USA) reflects only those, which play the most important role as reservoir of Trichinella spp., because they are at the In these islands, Trichinella sp. infection, probably T. top of the food chain or because their meat is consumed spiralis, was imported by the colonizers and trichi- either raw or semi-raw by humans. However, the host nellosis cases were documented in humans for the spectrum is much larger, even if in some cases infection consumption of pork from wild pigs (Barrett-Conner in other animal species occurs only sporadically (Pozio, et al., 1976; Satta, 1988). Trichinella sp. larvae were 2005). detected in several rodent species, mongooses (Her- Trichinella sp. infection has never been documented pestes javanicus) and in wild pigs (Alicata, 1970). on the islands reported below and they can be concluded Infection in domestic pigs is considered rare. As far as it that these parasites are not present, and may only be is know, the Hawaiian Islands are the only ones where passively introduced by humans: Trichinella sp. infection has been documented among the hundred small Pacific Islands. Africa (Cape Verde, Comoros, Madagascar, Maur- itius, Sao Tome´-Principe and Seychelles). 6.3. New Zealand America (the Caribbean islands Antigua-Barbuda, Bahamas, Barbados, Cuba, Dominica, Dominican T. spiralis, introduced during European coloniza- Rep, Grenada, Haiti, Jamaica, Neth Antilles, Puerto tion, was repeatedly documented in domestic pigs in Rico, St Kitts-Nevis, St Lucia, St Vincent-Grenadines 1965, 1968, 1974, 1997 and in 2001, in brown rats in and Trinidad-Tobago). 1965 and 2001 and in cats in 1965, 1974 and 2001 Asia (East Timo, Maldives, Philippines, Singapore, (Buncic, 1997; Paterson et al., 1997; ITRC). Sporadic Sri Lanka and Taiwan-China). infections were documented in humans following Europe (Cyprus, Iceland, and Malta). consumption of pork from domestic pigs as recently Pacific (Fiji, Kiribati, Marshall Is, Micronesia FS, as 2001 (Liberona and MacDiarmid, 1988; Pozio and Nauru, Palau, Samoa, Solomon Is, Tokelau, Tonga, Murrell, 2006). The control for Trichinella sp. infection Tuvalu, and Vanuatu). in pigs is only compulsory for exported pork and only a random sampling from 300 sows per year is performed In addition, there is a number of city–states (e.g. at slaughter for products destined for the domestic Andorra, Liechtenstein, San Marino, Singapore, Vati- market. can), where Trichinella sp. cannot circulate among animals for the lack of local fauna (both domestic and 6.4. Papua New Guinea sylvatic). According to the Commission regulation of the T. papuae was documented in wild and domestic pigs European Union (2005), all pigs, horses, wild boars and of several localities and in farmed saltwater crocodiles other susceptible animals slaughtered in the 27 member (Pozio et al., 2005b; ITRC). Anti-T. papuae antibodies states and intended for the EU market, should be tested were detected among human populations living in the for Trichinella sp. larvae. In addition, each member Western region (Owen et al., 2005). state should implement a monitoring program on 16 E. Pozio / Veterinary Parasitology 149 (2007) 3–21

Table 1 Number of countries by continent with documented Trichinella sp. infections in domestic animals, wildlife and humans Continent No. of countries with No. of countries with No. of countries with (no. of countries) infections in domestic animals (%) infections in wildlife (%) infections in humans (%) Africa (53) 3 (5.7) 13 (24.5) 7a (13.2) America (37) 5 (13.5) 3 (8.1) 5 (13.5) Asia (45) 9 (20.0) 14 (31.1) 18 (40.0) Europe (48) 24 (50.0) 34 (70.8) 23 (47.9) Paciﬁc (15) 2 (13.3) 2 (13.3) 2 (13.3) Total (198) 43 (21.9) 66 (33.3) 55 (27.8) a In four of these seven countries, trichinellosis was documented only in ethnic minorities and tourists.

Trichinella sp. infection in wildlife. This information Apanova, V.I., Badmaev, B.E., Boloshinov, A.B., Nomnoeva, L.K., will greatly increase our knowledge on this zoonosis in Ian, M.A., 2004. Trichinosis in the Republic of Buriatiia. Med. Parazitol. (Mosk) 2, 34–35 in Russian. the European Union in the course of the following years. Appleyard, G.D., Conboy, G., Gajadhar, A.A., 1998. Trichinella In conclusion, Trichinella sp.infectioninhumans spiralis in sylvatic hosts from Prince Edward Island. J. Wildl. was documented in 55 (27.8%) countries, but in some Dis. 34, 158–160. of these countries trichinellosis occurred only among Appleyard, G.D., Forbes, L.B., Gajadhar, A.A., 2002. National ser- ethnic minorities and tourists, because the native ologic survey for trichinellosis in sows in Canada 1996–1997. Can. Vet. J. 43, 271–273. inhabitants do not consume uncooked meat or meat of Arriaga, C., Yepez-Mulia, L., Viveros, N., Adame, L.A., Zarlenga, some animal species (Table 1). The average yearly D.S., Lichtenfels, J.R., Benitez, E., Ortega-Pierres, M.G., 1995. incidence of the disease in humans worldwide is Detection of Trichinella spiralis muscle larvae in naturally probably close to ten-thousand cases with a mortality infected horses. J. Parasitol. 81, 781–783. rate of about 0.2%; however, the number of infections is Barabe, P., Motte, M., Larbi, M., Thomas, D., Bobin, P., Foullon, X., 1977. La trichinose aigue, a propos de deux observations alge underreported in many countries due to the lack of riennes. Medecine et Armies 5, 37–40. appropriate serological tests and the knowledge of the Barakat, R.M., El-Sawy, M.F., Selim, M.K., Rashwan, A., 1982. disease on the part of physicians (Pozio, 2007). Trichinosis in some carnivores and rodents from Alexandria, Trichinella sp. infection was documented in domestic Egypt. J. Egypt Soc. Parasitol. 12, 445–451. animals (mainly pigs) of 43 (21.9%) countries and in Barennes, H., Sayasone, S., De Bruyned, A., Hongsakhone, S., Odermatt, P., Vonprhachanhae,P., Martinez-Aussela, B., Newtonf, wildlife of 66 (33.3%) countries (Table 1). Information P.N., Chaicumpah, W., Strobela, M., Dupouy-Camet, J. 2006. ontheoccurrenceofTrichinella sp. infection in Severe outbreak of trichinellosis in Udomxay province, Lao domestic and/or wildlife is still lacking for 92 PDR, 2005. In: Proceedings of the 5th Food and Waterborne countries. Parasitic Zoonoses. Bangkok, Thailand, 28–30 November, abstract book, p. 46. Barrett-Conner, E., Davis, C.F., Hamburger, R.N., Kagan, I., 1976. An Acknowledgement epidemic of trichinosis after ingestion of wild pig in Hawaii. J. Infect. Dis. 133, 473–477. This work was in part supported by the MED-VET- Bartoloni, A., Cancrini, G., Bartalesi, F., Nicoletti, A., Mendez Prado, NET project of the European Commission contract G., Rosado, J., Roselli, M., Paradisi, F., 1999. Antibodies against FOOD-CT-2004-506122. Trichinella spiralis in the rural population of the Province of Cordillera, Bolivia. Rev. Panam. Salud Publica 5, 97–99 in Spanish. Bartuliene, A., Jasulaitiene, V., Malakauskas, A., 2005. Human References trichinellosis in Lithuania, 1990–2004. Euro Surveill. 10 E050714.6. Alicata, J., 1970. Trichinosis in the paciﬁc islands and adjacent areas. Bessonov, A.S., 1994. Trichinellosis in the former USSR. Epidemic In: Gould, S.E. (Ed.), Trichinosis in Man and Animals. Charles C. situation (1988–1992). In: Campbel, C.W., Bruschi, F., Pozio, E. Thomas Publisher, Springﬁeld, Illinois, pp. 465–472. (Eds.), Trichinellosis. Istituto Superiore di Sanita` press, Rome, Alipuria, S., Sangha, H.K., Singh, G., Pandhi, S., 1996. Trichinosis—a pp. 505–510. case report. Indian J. Pathol. Microbiol. 39, 231–232. Bjorland, J., Brown, D., Gamble, H.R., McAuley, J.B., 1993. Trichi- Alvarez, V., Rivera, G., Neghme, A., Schenone, H., 1970. Trichinosis nella spiralis infection in pigs in the Bolivian Altiplano. Vet. in animals in Chile. Bol. Chil. Parasitol. 25, 83–86 in Spanish. Parasitol. 47, 349–354. Ancelle, T., De Bruyne, A., Poisson, D., Dupouy-Camet, J., 2005. Blaga, R., Durand, B., Antoniu, S., Gherman, C., Cretu, C.M., Cozma, Outbreak of trichinellosis due to consumption of bear meat from V., Boireau, P., 2007. Dramatically increase of human trichinel- Canada, France, September 2005. Euro. Surveill. 10 E051013.3. losis incidence in Romania over the last 25 years: Impact of Antonios, S.N., Salem, S.A., 1989. A case report of human trichinosis political changes or regional food habits? Am. J. Trop. Med. Hyg. in Tanta. J. Egypt Soc. Parasitol. 19, 363–364. 76, 983–986. E. Pozio / Veterinary Parasitology 149 (2007) 3–21 17

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