Abstract
Zoonotic infections are among the most common on earth and are responsible for >60 per cent of all human infectious diseases. Some of the most important and well-known human zoonoses are caused by worm or helminth parasites, including species of nematodes (trichinellosis), cestodes (cysticercosis, echinococcosis) and trematodes (schistosomiasis). However, along with social, epidemiological and environmental changes, together with improvements in our ability to diagnose helminth infections, several neglected parasite species are now fast-becoming recognized as important zoonotic diseases of humans, e.g. anasakiasis, several fish-borne trematodiasis and fasciolosis. In the present review, we discuss the current disease status of these primary helminth zoonotic infections with particular emphasis on their diagnosis and control. Advances in molecular biology, proteomics and the release of helminth genome-sequencing project data are revolutionizing parasitology research. The use of these powerful experimental approaches, and their potential benefits to helminth biology are also discussed in relation to the future control of helminth infections of animals and humans.
References
Acuna-Soto R.& Braun-Roth G. . 1987Bleeding ulcer in the common bile duct due to Fasciola hepatica. Am. J. Gastroenterol. 82, 560–562. PubMed, ISI, Google ScholarAguilar-Díaz H., 2006The genome project of Taenia solium. Parasitol. Int. 55, S127–S130. (doi:10.1016/j.parint.2005.11.020). Crossref, PubMed, ISI, Google ScholarAllan J. C.& Craig P. S. . 2006Coproantigens in taeniasis and echinococcosis. Parasitol. Int. 55, S75–S80. (doi:10.1016/j.parint.2005.11.010). Crossref, PubMed, ISI, Google ScholarAlonso D., Muñoz J., Gascón J., Valls M. E.& Corachan M. . 2006Failure of standard treatment with praziquantel in two returned travelers with Schistosoma haematobium infection. Am. J. Trop. Med. Hyg. 74, 342–344. Crossref, PubMed, ISI, Google ScholarAlvarez L. I., Solana H. D., Mottier M. L., Virkel G. L., Fairweather I.& Lanusse C. E. . 2005Altered drug influx/efflux and enhanced metabolic activity in triclabendazole-resistant liver flukes. Parasitology 131, 501–510. (doi:10.1017/S0031182005007997). Crossref, PubMed, ISI, Google ScholarAncelle T., De Bruyne A., Poisson D.& Dupouy-Camet J. . 2005Outbreak of trichinellosis due to consumption of bear meat from Canada, France, September. Euro. Surveill. 10, E051013.3. PubMed, Google ScholarAndrews S. J. . 1999The life cycle of Fasciola hepatica. Fasciolosis (ed.& Dalton J. P. ), pp. 1–29. Oxford, UK: CABI. Google ScholarArmentia A., Martin-Gil F. J., Pascual C., Martín-Esteban M., Callejo A.& Martínez C. . 2006Anisakis simplex allergy after eating chicken meat. J. Invest. Allergol. Clin. Immunol. 16, 258–263. PubMed, ISI, Google ScholarAudicana M. T., Ansotegui I. J., de Corres L. F.& Kennedy M. W. . 2002Anisakis simplex: dangerous—dead and alive?Trends Parasitol. 18, 20–25. (doi:10.1016/S1471-4922(01)02152-3). Crossref, PubMed, ISI, Google ScholarBoa M. E., Mahundi E. A., Kassuku A. A., Willingham A. L.& Kyvsgaard N. C. . 2006Epidemiological survey of swine cysticercosis using ante-mortem and post-mortem examination tests in the southern highlands of Tanzania. Vet. Parasitol. 139, 249–255. (doi:10.1016/j.vetpar.2006.02.012). Crossref, PubMed, ISI, Google ScholarBrander K. M. . 2007Global fish production and climate change. Proc. Natl Acad. Sci. USA 104, 19 709–19 714. (doi:10.1073/pnas.0702059104). Crossref, ISI, Google ScholarBrennan G. P., 2007Understanding triclabendazole resistance. Exp. Mol. Pathol. 82, 104–109. (doi:10.1016/j.yexmp.2007.01.009). Crossref, PubMed, ISI, Google ScholarBruschi F.& Murrell K. D. . 2002New aspects of human trichinellosis: the impact of new Trichinella species. Postgrad. Med. J. 78, 15–22. (doi:10.1136/pmj.78.915.15). Crossref, PubMed, ISI, Google ScholarCaffrey C. R. . 2007Chemotherapy of schistosomiasis: present and future. Curr. Opin. Chem. Biol. 11, 433–439. (doi:10.1016/j.cbpa.2007.05.031). Crossref, PubMed, ISI, Google ScholarCai X., Yuan G., Zheng Y., Luo X., Zhang S., Ding J., Jing Z.& Lu C. . 2008Effective production and purification of the glycosylated TSOL18 antigen, which is protective against pig cysticercosis. Infect. Immun. 76, 767–770. (doi:10.1128/IAI.00444-07). Crossref, PubMed, ISI, Google ScholarChai J. Y., Darwin Murrell K.& Lymbery A. J. . 2005Fish-borne parasitic zoonoses: status and issues. Int. J. Parasitol. 35, 1233–1254. (doi:10.1016/j.ijpara.2005.07.013). Crossref, PubMed, ISI, Google ScholarChen M. G.& Mott K. E. . 1990Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Trop. Dis. Bull. 87, R1–R38. Google ScholarCho P. Y., Lee M. J., Kim T. I., Kang S. Y.& Hong S. J. . 2006Expressed sequence tag analysis of adult Clonorchis sinensis, the Chinese liver fluke. Parasitol. Res. 99, 602–608. (doi:10.1007/s00436-006-0204-1). Crossref, PubMed, ISI, Google ScholarCho P. Y., Kim T. I., Whang S. M.& Hong S. J. . 2008Gene expression profile of Clonorchis sinensis metacercariae. Parasitol. Res. 102, 277–282. (doi:10.1007/s00436-007-0759-5). Crossref, PubMed, ISI, Google ScholarChoi D.& Hong S. T. . 2007Imaging diagnosis of clonorchiasis. Kor. J. Parasitol. 45, 77–85. (doi:10.3347/kjp.2007.45.2.77). Crossref, PubMed, Google ScholarColes G. C.& Stafford K. A. . 2001Activity of oxyclozanide, nitroxynil, clorsulon and albendazole against adult triclabendazole-resistant Fasciola hepatica. Vet. Rec. 148, 723–724. Crossref, PubMed, ISI, Google ScholarColes G. C., Rhodes A. C.& Stafford K. A. . 2000Activity of closantel against adult triclabendazole-resistant Fasciola hepatica. Vet. Rec. 146, 504. Crossref, PubMed, ISI, Google ScholarCraig P. S. The Echinococcosis Working Group in China. 2006Epidemiology of human alveolar echinococcosis in China. Parasitol. Int. 55, S221–S225. (doi:10.1016/j.parint.2005.11.034). Crossref, PubMed, ISI, Google ScholarCraig P. S., 2007Prevention and control of cystic echinococcosis. Lancet Infect. Dis. 7, 385–394. (doi:10.1016/S1473-3099(07)70134-2). Crossref, PubMed, ISI, Google ScholarCunningham A. A. . 2005A walk on the wild side—emerging wildlife diseases. Br. Med. J. 331, 1214–1215. (doi:10.1136/bmj.331.7527.1214). Crossref, PubMed, Google ScholarCurtale F., Hassanein Y. A.& Savioli L. . 2005Control of human fascioliasis by selective chemotherapy: design, cost and effect of the first public health, school-based intervention implemented in endemic areas of the Nile Delta, Egypt. Trans. R. Soc. Trop. Med. Hyg. 99, 599–609. (doi:10.1016/j.trstmh.2005.03.004). Crossref, PubMed, ISI, Google ScholarDai G., Wang S., Yu J., Xu S., Peng X., He Z., Liu X., Zhou S.& Liu F. . 2007Vaccination against Schistosoma japonicum infection by DNA vaccine encoding Sj22.7 antigen. Acta Biochim. Biophys. Sin. 39, 27–36. Crossref, Google ScholarDalton J. P.& Mulcahy G. . 2001Parasite vaccines—a reality?Vet. Parasitol. 98, 149–167. (doi:10.1016/S0304-4017(01)00430-7). Crossref, PubMed, ISI, Google ScholarDe Bruyne A., Ancelle T., Vallee I., Boireau P.& Dupouy-Camet J. . 2006Human trichinellosis acquired from wild boar meat: a continuing parasitic risk in France. Euro. Surveill. 11, E060914.5. PubMed, Google ScholarDespommier D. D. . 1983Biology. Trichinella and trichinosis (ed.& Campbell W. C. ), pp. 75–151. New York, NY: Plenum Press. Crossref, Google ScholarDespommier D. D. . 1998How does Trichinella spiralis make itself at home?Parasitol. Today 14, 318–323. (doi:10.1016/S0169-4758(98)01287-3). Crossref, PubMed, Google ScholarEl-On J. . 2003Benzimidazole treatment of cystic echinococcosis. Acta Trop. 85, 243–252. (doi:10.1016/S0001-706X(02)00217-6). Crossref, PubMed, ISI, Google ScholarEspinoza J. R., 2007Evaluation of Fas2-ELISA for the serological detection of Fasciola hepatica infection in humans. Am. J. Trop. Med. Hyg. 76, 977–982. Crossref, PubMed, ISI, Google ScholarEsteban J. G., 2003Hyperendemic fascioliasis associated with schistosomiasis in villages in the Nile Delta of Egypt. Am. J. Trop. Med. Hyg. 69, 429–437. Crossref, PubMed, ISI, Google ScholarFairweather I. . 2005Triclabendazole: new skills to unravel an old(ish) enigma. J. Helminthol. 79, 227–234. (doi:10.1079/JOH2005298). Crossref, PubMed, ISI, Google ScholarFairweather I.& Boray J. C. . 1999Mechanisms of fasciolicide action and drug resistance in Fasciola hepatica. Fasciolosis (ed.& Dalton J. P. ), pp. 225–276. Oxford, UK: CABI. Google ScholarFawzi M., El-Sahn A. A., Ibrahim H. F.& Shehata A. I. . 2004Vegetable-transmitted parasites among inhabitants of El-Prince, Alexandria and its relation to housewives' knowledge and practices. J. Egypt Public Health Assoc. 79, 13–12. PubMed, Google ScholarFinkelstein J. L., Schleinitz M. D., Carabin H.& McGarvey S. T. . 2008Decision-model estimation of the age-specific disability weight for schistosomiasis japonica: a systematic review of the literature. PLoS Negl. Trop. Dis. 2, e158. (doi:10.1371/journal.pntd.0000158). Crossref, PubMed, ISI, Google ScholarGarcia H. H., Moro P. L.& Schantz P. M. . 2007Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis. Curr. Opin. Infect. Dis. 20, 489–494. (doi:10.1097/QCO.0b013e3282a95e39). Crossref, PubMed, ISI, Google ScholarGauci C., Vural G., Oncel T., Varcasia A., Damian V., Kyngdon C. T., Craig P. S., Anderson G. A.& Lightowlers M. W. . 2008Vaccination with recombinant oncosphere antigens reduces the susceptibility of sheep to infection with Taenia multiceps. Int. J. Parasitol. 38, 1041–1050. (doi:10.1016/j.ijpara.2007.11.006). Crossref, PubMed, ISI, Google ScholarGavidia C. M., 2008Diagnosis of cystic echinococcosis, central Peruvian Highlands. Emerg. Infect. Dis. 14, 260–266. (doi:10.3201/eid1402.061101). Crossref, PubMed, ISI, Google ScholarGolab E., Szulc M.& Sadkowska-Todys M. . 2007Outbreak of trichinellosis in North-Western Poland. Euro. Surveill. 12, E070712.1. PubMed, Google ScholarGraham C. S., Brodie S. B.& Weller P. F. . 2001Imported Fasciola hepatica infection in the United States and treatment with triclabendazole. Clin. Infect. Dis. 33, 1–5. (doi:10.1086/320870). Crossref, PubMed, ISI, Google ScholarGryseels B., Polman K., Clerinx J.& Kestens L. . 2006Human schistosomiasis. Lancet 368, 1106–1118. (doi:10.1016/S0140-6736(06)69440-3). Crossref, PubMed, ISI, Google ScholarHaas B. J., Berriman M., Hirai H., Cerqueira G. G., Loverde P. T.& El-Sayed N. M. . 2007Schistosoma mansoni genome: closing in on a final gene set. Exp. Parasitol. 117, 225–228. (doi:10.1016/j.exppara.2007.06.005). Crossref, PubMed, ISI, Google ScholarHe Y. X., Salafsky B.& Ramaswamy K. . 2001Host–parasite relationships of Schistosoma japonicum in mammalian hosts. Trends Parasitol. 17, 320–324. (doi:10.1016/S1471-4922(01)01904-3). Crossref, PubMed, ISI, Google ScholarHien T. V., Dung T. T. K., Chi N. H., Dahn P. H.& Pham P. T. . 2001Fasciolosis in Vietnam. Southest Asian J. Trop. Med. Public Health 32, 48–50. PubMed, Google ScholarHu F., 2007Clonorchis sinensis: expression, characterization, immunolocalization and serological reactivity of one excretory/secretory antigen-LPAP homologue. Exp. Parasitol. 117, 157–164. (doi:10.1016/j.exppara.2007.04.003). Crossref, PubMed, ISI, Google ScholarIntapan P. M., Wongkham C., Imtawil K. J., Pumidonming W., Prasongdee T. K., Miwa M.& Maleewong W. . 2005Detection of Paragonimus heterotremus eggs in experimentally infected cats by a polymerase chain reaction-based method. J. Parasitol. 91, 195–198. (doi:10.1645/GE-3357RM). Crossref, PubMed, ISI, Google ScholarIrving J. A., Spithill T. W., Pike R. N., Whisstock J. C.& Smooker P. M. . 2003The evolution of enzyme specificity in Fasciola spp. J. Mol. Evol. 57, 1–15. (doi:10.1007/s00239-002-2434-x). Crossref, PubMed, ISI, Google ScholarJefferies J. R., Campbell A. M., van Rossum A. J., Barrett J.& Brophy P. M. . 2001Proteomic analysis of Fasciola hepatica excretory–secretory products. Proteomics 1, 1128–1132. (doi:10.1002/1615-9861(200109)1:9<1128::AID-PROT1128>3.0.CO;2-0). Crossref, PubMed, ISI, Google ScholarJenkins D. J. . 2006Echinococcus granulosus in Australia, widespread and doing well!. Parasitol. Int. 55, S203–S206. (doi:10.1016/j.parint.2005.11.031). Crossref, PubMed, ISI, Google ScholarJenkins D. J., Romig T.& Thompson R. C. A. . 2005Emergence/re-emergence of Echinococcus spp.—a global update. Int. J. Parasitol. 35, 1205–1219. (doi:10.1016/j.ijpara.2005.07.014). Crossref, PubMed, ISI, Google ScholarJongwutiwes S., 1998First outbreak of human trichinellosis caused by Trichinella pseudospiralis. Clin. Infect. Dis. 26, 111–115. (doi:10.1086/516278). Crossref, PubMed, ISI, Google ScholarKeiser J.& Utzinger J. . 2005Emerging foodborne trematodiasis. Emerg. Infect. Dis. 11, 1507–1514. Crossref, PubMed, ISI, Google ScholarKeiser J., Utzinger J., Vennerstrom J. L., Dong Y., Brennan G.& Fairweather I. . 2007Activity of artemether and OZ78 against triclabendazole-resistant Fasciola hepatica. Trans. R. Soc. Trop. Med. Hyg. 101, 1219–1222. (doi:10.1016/j.trstmh.2007.07.012). Crossref, PubMed, ISI, Google ScholarKim T. S., de Guzman J. V., Kong H. H.& Chung D. I. . 2006Comparison of gene representation between diploid and triploid Paragonimus westermani by expressed sequence tag analyses. J. Parasitol. 92, 803–816. (doi:10.1645/GE-723R.1). Crossref, PubMed, ISI, Google ScholarKing C. H., Dickman K.& Tisch D. J. . 2005Reassessment of the cost of chronic helminthic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 1561–1569. (doi:10.1016/S0140-6736(05)66457-4). Crossref, PubMed, ISI, Google ScholarKobayashi Y., Shimakura K., Ishizaki S., Nagashima Y.& Shiomi K. . 2007Purification and cDNA cloning of a new heat-stable allergen from Anisakis simplex. Mol. Biochem. Parasitol. 155, 138–145. (doi:10.1016/j.molbiopara.2007.06.012). Crossref, PubMed, ISI, Google ScholarKraft R. . 2007Cysticercosis: an emerging parasitic disease. Am. Fam. Phys. 76, 91–96. PubMed, ISI, Google ScholarLaha T., Pinlaor P., Mulvenna J., Sripa B., Sripa M., Smout M. J., Gasser R. B., Brindley P. J.& Loukas A. . 2007Gene discovery for the carcinogenic human liver fluke, Opisthorchis viverrini. BMC Genom. 8, 189. (doi:10.1186/1471-2164-8-189). Crossref, PubMed, ISI, Google ScholarLahmar S., Lahmar S., Boufana B., Bradshaw H.& Craig P. S. . 2007Screening for Echinococcus granulosus in dogs: comparison between arecoline purgation, coproELISA and coproPCR with necropsy in pre-patent infections. Vet. Parasitol. 144, 287–292. (doi:10.1016/j.vetpar.2006.10.016). Crossref, PubMed, ISI, Google ScholarLateef M., Zargar S. A., Khan A. R., Nazir M.& Shoukat A. . 2008Successful treatment of niclosamide- and praziquantel-resistant beef tapeworm infection with nitazoxanide. Int. J. Infect. Dis. 12, 80–82. (doi:10.1016/j.ijid.2007.04.017). Crossref, PubMed, ISI, Google ScholarLe T. H., De N. V., Agatsuma T., Thi , Nguyen T. G., Nguyen Q. D., McManus D. P.& Blair D. . 2008Human fascioliasis and the presence of hybrid/introgressed forms of Fasciola hepatica and Fasciola gigantica in Vietnam. Int. J. Parasitol. 38, 725–730. Crossref, PubMed, ISI, Google ScholarLee J. S., Lee J., Park S. J.& Yong T. S. . 2003Analysis of the genes expressed in Clonorchis sinensis adults using the expressed sequence tag approach. Parasitol. Res. 91, 283–289. (doi:10.1007/s00436-003-0962-y). Crossref, PubMed, ISI, Google ScholarLee J. S., Kim I. S., Sohn W. M., Lee J.& Yong T. S. . 2006aVaccination with DNA encoding cysteine proteinase confers protective immune response to rats infected with Clonorchis sinensis. Vaccine 24, 2358–2366. (doi:10.1016/j.vaccine.2005.11.062). Crossref, PubMed, ISI, Google ScholarLee J. S., Kim I. S., Sohn W. M., Lee J.& Yong T. S. . 2006bA DNA vaccine encoding a fatty acid-binding protein of Clonorchis sinensis induces protective immune response in Sprague-Dawley rats. Scand. J. Immunol. 63, 169–176. (doi:10.1111/j.1365-3083.2006.01721.x). Crossref, PubMed, ISI, Google ScholarLee J. S., Lee J., Kim S. H.& Yong T. S. . 2007Molecular cloning and characterization of a major egg antigen in Paragonimus westermani and its use in ELISA for the immunodiagnosis of paragonimiasis. Parasitol. Res. 100, 677–681. (doi:10.1007/s00436-006-0324-7). Crossref, PubMed, ISI, Google ScholarLier T., Johansen M. V., Hjelmevoll S. O., Vennervald B. J.& Simonsen G. S. . 2008Real-time PCR for detection of low intensity Schistosoma japonicum infections in a pig model. Acta Trop. 105, 74–80. (doi:10.1016/j.actatropica.2007.10.004). Crossref, PubMed, ISI, Google ScholarLightlowlers M. W. . 2006Cestode vaccines: origins, current status and future prospects. Parasitology 133, S27–S42. (doi:10.1017/S003118200600179X). Crossref, PubMed, ISI, Google ScholarLun Z. R., Gasser R. B., Lai D. H., Li A. X., Zhu X. Q., Yu X. B.& Fang Y. Y. . 2005Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect. Dis. 5, 31–41. (doi:10.1016/S1473-3099(04)01252-6). Crossref, PubMed, ISI, Google ScholarMafojane N. A., Appleton C. C., Krecek R. C., Michael L. M.& Willingham A. L. . 2003The current status of neurocysticercosis in Eastern and Southern Africa. Acta Trop. 87, 25–33. Crossref, PubMed, ISI, Google ScholarMagambo J., Njoroge E.& Zeyhle E. . 2006Epidemiology and control of echinococcosis in sub-Saharan Africa. Parasitol. Int. 55, S193–S195. (doi:10.1016/j.parint.2005.11.029). Crossref, PubMed, ISI, Google ScholarMalakauskas A., Paulauskas V., Järvis T., Keidans P., Eddi C.& Kapel C. M. . 2007Molecular epidemiology of Trichinella spp. in three Baltic countries: Lithuania, Latvia, and Estonia. Parasitol. Res. 100, 687–693. (doi:10.1007/s00436-006-0320-y). Crossref, PubMed, ISI, Google ScholarMalenganisho W. L., Magnussen P., Friis H., Siza J., Kaatano G., Temu M.& Vennervald B. J. . 2008Schistosoma mansoni morbidity among adults in two villages along Lake Victoria shores in Mwanza District, Tanzania. Trans. R. Soc. Trop. Med. Hyg. 102, 532–541. (doi:10.1016/j.trstmh.2008.03.006). Crossref, PubMed, ISI, Google ScholarMalone J. B. . 1997The landscape epidemiology of Fasciolosis: geographic determinants of disease risk. Immunology, pathobiology and control of fasciolosis (ed.& Boray J. C. ). Rahway, NJ: MSD AGVET. Google ScholarMarcilla A., 2008Leucine aminopeptidase is an immunodominant antigen of Fasciola hepatica excretory and secretory products in human infections. Clin. Vaccine Immunol. 15, 95–100. (doi:10.1128/CVI.00338-07). Crossref, PubMed, Google ScholarMas-Coma S., Anglés R., Esteban J. G., Bargues M. D., Buchon P., Franken M.& Strauss W. . 1999aThe Northern Bolivian Altiplano: a region highly endemic for human fascioliasis. Trop. Med. Int. Health 4, 454–467. (doi:10.1046/j.1365-3156.1999.00418.x). Crossref, PubMed, ISI, Google ScholarMas-Coma S., Bargues M. D.& Esteban J. G. . 1999bHuman fasciolosis. Fasciolosis (ed.& Dalton J. P. ), pp. 411–434. Oxford, UK: CABI. Google ScholarMas-Coma S., Bargues M. D.& Valero M. A. . 2005Fascioliasis and other plant-borne trematode zoonoses. Int. J. Parasitol. 35, 1255–1278. (doi:10.1016/j.ijpara.2005.07.010). Crossref, PubMed, ISI, Google ScholarMayta H., Gilman R. H., Prendergast E., Castillo J. P., Tinoco Y. O., Garcia H. H., Gonzalez A. E.& Sterling C. R. . 2008Nested PCR for specific diagnosis of Taenia solium Taeniasis. J. Clin. Microbiol. 46, 286–289. (doi:10.1128/JCM.01172-07). Crossref, PubMed, ISI, Google ScholarMcCarthy J.& Moore T. A. . 2000Emerging helminth zoonoses. Int. J. Parasitol. 30, 1351–1360. (doi:10.1016/S0020-7519(00)00122-3). Crossref, PubMed, ISI, Google ScholarMcConville M., Brennan G. P., McCoy M., Castillo R., Hernandez-Campos A., Ibarra F.& Fairweather I. . 2007Immature triclabendazole-resistant Fasciola hepatica: tegumental responses to in vitro treatment with the sulphoxide metabolite of the experimental fasciolicide compound alpha. Parasitol. Res. 100, 365–377. (doi:10.1007/s00436-006-0270-4). Crossref, PubMed, ISI, Google ScholarMcGarry J. W., Ortiz P. L., Hodgkinson J. E., Goreish I.& Williams D. J. . 2007PCR-based differentiation of Fasciola species (Trematoda: Fasciolidae), using primers based on RAPD-derived sequences. Ann. Trop. Med. Parasitol. 101, 415–421. (doi:10.1179/136485907X176508). Crossref, PubMed, Google ScholarMcGonigle L., Mousley A., Marks N. J., Brennan G. P., Dalton J. P., Spithill T. W., Day T. A.& Maule A. G. . 2008The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration. Int. J. Parasitol. 38, 149–155. (doi:10.1016/j.ijpara.2007.10.007). Crossref, PubMed, ISI, Google ScholarMcManus D. P.& Dalton J. P. . 2006Vaccines against the zoonotic trematodes Schistosoma japonicum, Fasciola hepatica and Fasciola gigantica. Parasitology 133, S43–S61. (doi:10.1017/S0031182006001806). Crossref, PubMed, ISI, Google ScholarMoghaddam A. S., Massoud J., Mahmoodi M., Mahvi A. H., Periago M. V., Artigas P., Fuentes M. V., Bargues M. D.& Mas-Coma S. . 2004Human and animal fascioliasis in Mazandaran province, northern Iran. Parasitol. Res. 94, 61–69. (doi:10.1007/s00436-004-1169-6). Crossref, PubMed, ISI, Google ScholarMoneo I., Caballero M. L., Rodriguez-Perez R., Rodriguez-Mahillo A. I.& Gonzalez-Muñoz M. . 2007Sensitization to the fish parasite Anisakis simplex: clinical and laboratory aspects. Parasitol. Res. 101, 1051–1055. (doi:10.1007/s00436-007-0587-7). Crossref, PubMed, ISI, Google ScholarMoro P.& Schantz P. M. . 2006Cystic echinococcosis in the Americas. Parasitol. Int. 55, S181–S186. (doi:10.1016/j.parint.2005.11.048). Crossref, PubMed, ISI, Google ScholarMorphew R. M., Wright H. A., LaCourse E. J., Woods D. J.& Brophy P. M. . 2007Comparative proteomics of excretory-secretory proteins released by the liver fluke Fasciola hepatica in sheep host bile and during in vitro culture ex host. Mol. Cell. Proteom. 6, 963–972. (doi:10.1074/mcp.M600375-MCP200). Crossref, ISI, Google ScholarMoskwa B., Bień J., Cabaj W., Korinkova K., Koudela B., Kacprzak E.& Stefaniak J. . 2006The estimation of different ELISA procedures for serodiagnosis of human trichinellosis. Wiad Parazytol. 52, 231–238. PubMed, Google ScholarMottier L., Alvarez L., Fairweather I.& Lanusse C. . 2006Resistance-induced changes in triclabendazole transport in Fasciola hepatica: ivermectin reversal effect. J. Parasitol. 92, 1355–1360. (doi:10.1645/GE-922R.1). Crossref, PubMed, ISI, Google ScholarO'Neill S. M., Parkinson M., Dowd A. J., Strauss W., Angles R.& Dalton J. P. . 1999Short report: immunodiagnosis of human fascioliasis using recombinant Fasciola hepatica cathepsin L1 cysteine proteinase. Am. J. Trop. Med. Hyg. 60, 749–517. Crossref, PubMed, ISI, Google ScholarOliveira G. . 2007The Schistosoma mansoni transcriptome: an update. Exp. Parasitol. 117, 229–235. (doi:10.1016/j.exppara.2007.06.001). Crossref, PubMed, ISI, Google ScholarParkinson M., O'Neill S. M.& Dalton J. P. . 2007Endemic human fasciolosis in the Bolivian Altiplano. Epidemiol. Infect. 135, 669–674. (doi:10.1017/S095026880600728X). Crossref, PubMed, ISI, Google ScholarParvathi A., 2007Clonorchis sinensis: development and evaluation of a nested polymerase chain reaction (PCR) assay. Exp. Parasitol. 115, 291–295. (doi:10.1016/j.exppara.2006.09.010). Crossref, PubMed, ISI, Google ScholarPawlowski Z., Allan J.& Sarti E. . 2005Control of Taenia solium taeniasis/cysticercosis: from research towards implementation. Int. J. Parasitol. 35, 1221–1232. (doi:10.1016/j.ijpara.2005.07.015). Crossref, PubMed, ISI, Google ScholarPetavy A. F., 2008An oral recombinant vaccine in dogs against Echinococcus granulosus, the causative agent of human hydatid disease: a pilot study. PLoS Negl. Trop. Dis. 2, e125. (doi:10.1371/journal.pntd.0000125). Crossref, PubMed, ISI, Google ScholarPozio E. . 2001New patterns of Trichinella infection. Vet. Parasitol. 98, 133–148. (doi:10.1016/S0304-4017(01)00427-7). Crossref, PubMed, ISI, Google ScholarPozio E. . 2007World distribution of Trichinella spp. infections in animals and humans. Vet. Parasitol. 149, 3–21. (doi:10.1016/j.vetpar.2007.07.002). Crossref, PubMed, ISI, Google ScholarPozio E., Gomez Morales M. A.& Dupouy-Camet J. . 2003Clinical aspects, diagnosis and treatment of trichinellosis. Expert Rev. Anti Infect. Ther. 1, 471–482. (doi:10.1586/14787210.1.3.471). Crossref, PubMed, Google ScholarPrakash A., Kumar G. S., Rout M., Nagarajan K.& Kumar R. . 2007Neurocysticercosis in free roaming pigs–a slaughterhouse survey. Trop. Anim. Health Prod. 39, 391–394. (doi:10.1007/s11250-007-9040-2). Crossref, PubMed, ISI, Google ScholarRajshekhar V., Raghava M. V., Prabhakaran V., Oommen A.& Muliyil J. . 2006Active epilepsy as an index of burden of neurocysticercosis in Vellore district, India. Neurology 67, 2135–2139. (doi:10.1212/01.wnl.0000249113.11824.64). Crossref, PubMed, ISI, Google ScholarReiterová K., Kinceková J., Snábel V., Marucci G., Pozio E.& Dubinský P. . 2007Trichinella spiralis-outbreak in the Slovak Republic. Infection 35, 89–93. (doi:10.1007/s15010-007-6122-z). Crossref, PubMed, ISI, Google ScholarRiley S., 2008Multi-host transmission dynamics of Schistosoma japonicum in Samar province, the Philippines. PLoS Med. 5, e18. (doi:10.1371/journal.pmed.0050018). Crossref, PubMed, ISI, Google ScholarRobinson M. W.& Connolly B. . 2005Proteomic analysis of the excretory-secretory proteins of the Trichinella spiralis L1 larva, a nematode parasite of skeletal muscle. Proteomics 5, 4525–4532. (doi:10.1002/pmic.200402057). Crossref, PubMed, ISI, Google ScholarRobinson M. W., Trudgett A., Hoey E. M.& Fairweather I. . 2002Triclabendazole-resistant Fasciola hepatica: β-tubulin and response to in vitro treatment with triclabendazole. Parasitology 124, 325–338. (doi:10.1017/S003118200100124X). Crossref, PubMed, ISI, Google ScholarRobinson M. W., Lawson J., Trudgett A., Hoey E. M.& Fairweather I. . 2004The comparative metabolism of triclabendazole sulphoxide by triclabendazole-susceptible and triclabendazole-resistant Fasciola hepatica. Parasitol. Res. 92, 205–210. (doi:10.1007/s00436-003-1003-6). Crossref, PubMed, ISI, Google ScholarRobinson M. W., Gare D.& Connolly B. . 2005Profiling excretory-secretory proteins of Trichinella muscle larvae by 2-dimensional gel electrophoresis and mass spectrometry. Vet. Parasitol. 132, 37–41. (doi:10.1016/j.vetpar.2005.05.019). Crossref, PubMed, ISI, Google ScholarRobinson M. W., Greig R., Beattie K., Lamont D.& Connolly B. . 2007Comparative analysis of the excretory–secretory proteome of the muscle larva of Trichinella pseudospiralis and Trichinella spiralis. Int. J. Parasitol. 37, 139–148. (doi:10.1016/j.ijpara.2006.08.007). Crossref, PubMed, ISI, Google ScholarRobinson M. W., 2008Proteomic and phylogenetic analysis of the cathepsin L protease family of the helminth pathogen, Fasciola hepatica: expansion of a repertoire of virulence-associated factors. Mol. Cell. Proteom. 7, 1111–1123. (doi:10.1074/mcp.M700560-MCP200). Crossref, ISI, Google ScholarRodríguez E., Anadón A. M., García-Bodas E., Romarís F., Iglesias R., Gárate T.& Ubeira F. M. . 2008Novel sequences and epitopes of diagnostic value derived from the Anisakis simplex Ani s 7 major allergen. Allergy 63, 219–225. Crossref, PubMed, ISI, Google ScholarRokni M. B., Massoud J., O'Neill S. M., Parkinson M.& Dalton J. P. . 2002Diagnosis of human fasciolosis in the Gilan province of Northern Iran: application of cathepsin L-ELISA. Diagn. Microbiol. Infect. Dis. 44, 175–179. (doi:10.1016/S0732-8893(02)00431-5). Crossref, PubMed, ISI, Google ScholarRomig T., Dinkel A.& Mackenstedt U. . 2006The present situation of echinococcosis in Europe. Parasitol. Int. 55, S187–S191. (doi:10.1016/j.parint.2005.11.028). Crossref, PubMed, ISI, Google ScholarRussell S. L., McFerran N. V., Hoey E. M., Trudgett A.& Timson D. J. . 2007Characterisation of two calmodulin-like proteins from the liver fluke, Fasciola hepatica. Biol. Chem. 388, 593–599. (doi:10.1515/BC.2007.076). Crossref, PubMed, ISI, Google ScholarSadjjadi S. M. . 2006Present situation of echinococcosis in the Middle East and Arabic North Africa. Parasitol. Int. 55, S197–S202. (doi:10.1016/j.parint.2005.11.030). Crossref, PubMed, ISI, Google ScholarShimoni Z., Klein Z., Weiner P., Assous M. V.& Froom P. . 2007The use of prednisone in the treatment of trichinellosis. Isr. Med. Assoc. J. 9, 537–539. PubMed, ISI, Google ScholarSorvillo F. J., DeGiorgio C.& Waterman S. H. . 2007Deaths from cysticercosis, United States. Emerg. Infect. Dis. 13, 230–235. Crossref, PubMed, ISI, Google ScholarSripa B., 2007Liver fluke induces cholangiocarcinoma. PLoS Med. 4, e201. (doi:10.1371/journal.pmed.0040201). Crossref, PubMed, ISI, Google ScholarSteinmann P., Keiser J., Bos R., Tanner M.& Utzinger J. . 2006Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 6, 411–425. (doi:10.1016/S1473-3099(06)70521-7). Crossref, PubMed, ISI, Google ScholarStrauss W., O'Neill S. M., Parkinson M., Angles R.& Dalton J. P. . 1999Short report: Diagnosis of human fascioliasis: detection of anti-cathepsin L antibodies in blood samples collected on filter paper. Am. J. Trop. Med. Hyg. 60, 746–748. Crossref, PubMed, ISI, Google ScholarSumitani M., Mikawa T., Miki Y., Nisida K., Tochino Y., Kamimori T., Fujiwara H., Fujikawa T.& Nakamura F. . 2005A case of chronic pleuritis by Paragonimus Westermani infection resistant to standard chemotherapy and cured by three additional cycles of chemotherapy. Nihon Kokyuki Gakkai Zasshi 43, 427–431. PubMed, Google ScholarThuwajit C., Thuwajit P., Kaewkes S., Sripa B., Uchida K., Miwa M.& Wongkham S. . 2004Increased cell proliferation of mouse fibroblast NIH-3T3 in vitro induced by excretory/secretory product(s) from Opisthorchis viverrini. Parasitology 129, 455–464. (doi:10.1017/S0031182004005815). Crossref, PubMed, ISI, Google ScholarTinga N., De N., Vien H. V., Chau L., Toan N. D., Kager P. A.& Vries P. J. . 1999Little effect of praziquantel or artemisinin on clonorchiasis in Northern Vietnam. A pilot study. Trop. Med. Int. Health 4, 814–818. (doi:10.1046/j.1365-3156.1999.00499.x). Crossref, PubMed, ISI, Google Scholarvan Hellemond J. J., van Balkom B. W.& Tielens A. G. . 2007Schistosome biology and proteomics: progress and challenges. Exp. Parasitol. 117, 267–274. Crossref, PubMed, ISI, Google Scholarvan Thiel P., Kuipers F. C.& Roskam R. T. . 1960A nematode parasitic to herring, causing acute abdominal syndromes in man. Trop. Geogr. Med. 12, 97–113. PubMed, Google ScholarVorou R. M., Papavassiliou V. G.& Tsiodras S. . 2007Emerging zoonoses and vector-borne infections affecting humans in Europe. Epidemiol. Infect. 135, 1231–1247. (doi:10.1017/S0950268807008527). Crossref, PubMed, ISI, Google ScholarWongratanacheewin S., Pumidonming W., Sermswan R. W., Pipitgool V.& Maleewong W. . 2002Detection of Opisthorchis viverrini in human stool specimens by PCR. J. Clin. Microbiol. 40, 3879–3880. (doi:10.1128/JCM.40.10.3879-3880.2002). Crossref, PubMed, ISI, Google ScholarWu Z., Pagano I., Pozio E.& Takahashi Y. . 1999Polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) for the identification of Trichinella isolates. Parasitology 118, 211–218. (doi:10.1017/S0031182098003679). Crossref, PubMed, ISI, Google ScholarYoon W. J., Lee S. M., Lee S. H.& Yoon Y. B. . 2004Gastric anisakiasis. Gastrointest. Endosc. 59, 400. (doi:10.1016/S0016-5107(03)02591-4). Crossref, PubMed, ISI, Google ScholarYu H. S., Park S. K., Lee K. H., Lee S. J., Choi S. H., Ock M. S.& Jeong H. J. . 2007aAnisakis simplex: analysis of expressed sequence tags (ESTs) of third-stage larva. Exp. Parasitol. 117, 51–56. (doi:10.1016/j.exppara.2007.03.009). Crossref, PubMed, ISI, Google ScholarYu J. M., de Vlas S. J., Jiang Q. W.& Gryseels B. . 2007bComparison of the Kato-Katz technique, hatching test and indirect hemagglutination assay (IHA) for the diagnosis of Schistosoma japonicum infection in China. Parasitol. Int. 56, 45–49. (doi:10.1016/j.parint.2006.11.002). Crossref, PubMed, ISI, Google ScholarZarlenga D. S., Chute M. B., Martin A.& Papel C. M. . 2001A single, multiplex PCR for differentiating all species of Trichinella. Parasite 8, S24–S26. Crossref, PubMed, ISI, Google ScholarZhao Q. P., Moon S. U., Na B. K., Kim S. H., Cho S. H., Lee H. W., Kong Y., Sohn W. M., Jiang M. S.& Kim T. S. . 2007Paragonimus westermani: biochemical and immunological characterizations of paramyosin. Exp. Parasitol. 115, 9–18. (doi:10.1016/j.exppara.2006.05.004). Crossref, PubMed, ISI, Google ScholarZhou X. N., 2007Epidemiology of schistosomiasis in the People's Republic of China, 2004. Emerg. Infect. Dis. 13, 1470–1476. Crossref, PubMed, ISI, Google Scholar


