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Current status of food-borne trematode infections

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Abstract

Food-borne trematodiases constitute an important group of the most neglected tropical diseases, not only in terms of research funding, but also in the public media. The Trematoda class contains a great number of species that infect humans and are recognized as the causative agents of disease. The biological cycle, geographical distribution, and epidemiology of most of these trematode species have been well characterized. Traditionally, these infections were limited, for the most part, in populations living in low-income countries, particularly in Southeast Asia, and were associated with poverty. However, the geographical limits and the population at risk are currently expanding and changing in relation to factors such as growing international markets, improved transportation systems, and demographic changes. The diagnosis of these diseases is based on parasitological techniques and only a limited number of drugs are currently available for treatment, most of which are unspecific. Therefore, in-depth studies are urgently needed in order to clarify the current epidemiology of these helminth infections and to identify new and specific targets for both effective diagnosis and treatment. In this review, we describe the biology, medical and epidemiological features, and current treatment and diagnostic tools of the main groups of flukes and the corresponding diseases.

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References

  1. Keiser J, Utzinger J (2005) Emerging foodborne trematodiasis. Emerg Infect Dis 11:1507–1514

    Article  PubMed  Google Scholar 

  2. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483

    Article  PubMed  PubMed Central  Google Scholar 

  3. Sripa B, Kaewkes S, Intapan PM, Maleewong W, Brindley PJ (2010) Food-borne trematodiases in Southeast Asia: epidemiology, pathology, clinical manifestation and control. Adv Parasitol 72:305–350

    Article  PubMed  Google Scholar 

  4. Toledo R, Bernal MD, Marcilla A (2011) Proteomics of foodborne trematodes. J Proteomics 74:1485–1503

    Article  PubMed  CAS  Google Scholar 

  5. Balasegaram M, Balasegaram S, Malvy D, Millet P (2008) Neglected diseases in the news: a content analysis of recent international media coverage focussing on leishmaniasis and trypanosomiasis. PLoS Negl Trop Dis 2:e234

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hotez PJ, Fenwick A, Savioli L, Molyneux DH (2009) Rescuing the bottom billion through control of neglected tropical diseases. Lancet 373:1570–1575

    Article  PubMed  Google Scholar 

  7. Moran M, Guzman J, Ropars AL, McDonald A, Jameson N, Omune B, Ryan S, Wu L (2009) Neglected disease research and development: how much are we really spending? PLoS Med 6:e30

    Article  PubMed  Google Scholar 

  8. Halton DW (2004) Microscopy and the helminth parasite. Micron 35:361–390

    Article  PubMed  CAS  Google Scholar 

  9. Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY (2005) Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis 5:31–41

    Article  PubMed  Google Scholar 

  10. World Health Organization (WHO) (1995) Control of foodborne trematode infections. Report of a WHO Study Group. World Health Organ Tech Rep Ser 849:1–157

    Google Scholar 

  11. Blair D, Agatsuma T, Wang W (2007) Paragonimiasis. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses: fish and plant-borne parasites. World class parasites, vol 11. Springer, New York, pp 117–150

    Google Scholar 

  12. Murray CJ, Lopez AD (1996) Evidence-based health policy—lessons from the Global Burden of Disease Study. Science 274:740–743

    Article  PubMed  CAS  Google Scholar 

  13. World Health Organization (WHO) (2004) The world health report 2004—changing history. WHO, Geneva, Switzerland

    Google Scholar 

  14. Hong ST, Fang Y (2012) Clonorchis sinensis and clonorchiasis, an update. Parasitol Int 61:17–24

    Article  PubMed  CAS  Google Scholar 

  15. Andrews RH, Sithithaworn P, Petney TN (2008) Opisthorchis viverrini: an underestimated parasite in world health. Trends Parasitol 24:497–501

    Article  PubMed  PubMed Central  Google Scholar 

  16. Sithithaworn P, Yongvanit P, Tesana S, Pairojkul C (2007) Liver flukes. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses: fish and plant-borne parasites. World class parasites, vol 11. Springer, New York, pp 3–52

    Google Scholar 

  17. Chai JY (2007) Intestinal flukes. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses: fish and plant-borne parasites. World class parasites, vol 11. Springer, New York, pp 53–115

    Google Scholar 

  18. Fried B, Abruzzi A (2010) Food-borne trematode infections of humans in the United States of America. Parasitol Res 106:1263–1280

    Article  PubMed  Google Scholar 

  19. Rim HJ (2005) Clonorchiasis: an update. J Helminthol 79:269–281

    Article  PubMed  Google Scholar 

  20. International Agency for Research on Cancer (IARC) (1994) IARC monographs on the evaluation of carcinogenic risks to humans: schistosomes, liver flukes and Helicobacter pylori. IARC Monographs 61:9–175

    Google Scholar 

  21. Choi BI, Han JK, Hong ST, Lee KH (2004) Clonorchiasis and cholangiocarcinoma: etiologic relationship and imaging diagnosis. Clin Microbiol Rev 17:540–552

    Article  PubMed  PubMed Central  Google Scholar 

  22. Mayer DA, Fried B (2007) The role of helminth infections in carcinogenesis. Adv Parasitol 65:239–296

    Article  PubMed  Google Scholar 

  23. Sripa B, Pairojkul C (2008) Cholangiocarcinoma: lessons from Thailand. Curr Opin Gastroenterol 24:349–356

    Article  PubMed  Google Scholar 

  24. Malone JB (1997) The landscape epidemiology of fasciolosis: geographic determinants of disease risk. In: Boray JC (ed) Immunology, pathobiology and control of fasciolosis. MSD AGVET, Rahway, NJ, pp 65–81

    Google Scholar 

  25. Andrews SJ (1999) The life cycle of Fasciola hepatica. In: Dalton JP (ed) Fasciolosis. CABI Publishing, Oxford, pp 1–29

    Google Scholar 

  26. Robinson MW, Dalton JP (2009) Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philos Trans R Soc Lond B Biol Sci 364:2763–2776

    Article  PubMed  Google Scholar 

  27. Mas-Coma S, Valero MA, Bargues MD (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69:41–146

    Article  PubMed  Google Scholar 

  28. Mas-Coma S (2004) Human fascioliasis. In: Cotruvo JA, Dufour A, Rees G, Bartram J, Carr R, Cliver DO, Craun GF, Fayer R, Gannon VPJ (eds) Waterborne zoonoses: identification, causes and control. World Health Organization. IWA Publishing, London, UK, pp 305–322

    Google Scholar 

  29. Esteban JG, González C, Bargues MD, Angles R, Sánchez C, Náquira C, Mas-Coma S (2002) High fascioliasis infection in children linked to a man-made irrigation zone in Peru. Trop Med Int Health 7:339–348

    Article  PubMed  Google Scholar 

  30. Mas-Coma S, Bargues MD, Valero MA (2005) Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol 35:1255–1278

    Article  PubMed  CAS  Google Scholar 

  31. Esteban JG, Flores A, Angles R, Mas-Coma S (1999) High endemicity of human fascioliasis between Lake Titicaca and La Paz valley, Bolivia. Trans R Soc Trop Med Hyg 93:151–156

    Article  PubMed  CAS  Google Scholar 

  32. Esteban JG, González C, Curtale F, Muñoz-Antoli C, Valero MA, Bargues MD, el-Sayed M, el-Wakeel AA, Abdel-Wahab Y, Montresor A, Engels D, Savioli L, Mas-Coma S (2003) Hyperendemic fascioliasis associated with schistosomiasis in villages in the Nile Delta of Egypt. Am J Trop Med Hyg 69:429–437

    PubMed  Google Scholar 

  33. Rokni MB, Massoud J, O’Neill SM, Parkinson M, Dalton JP (2002) Diagnosis of human fasciolosis in the Gilan province of Northern Iran: application of cathepsin L-ELISA. Diagn Microbiol Infect Dis 44:175–179

    Article  PubMed  CAS  Google Scholar 

  34. Garcia HH, Moro PL, Schantz PM (2007) Zoonotic helminth infections of humans: echinococcosis, cysticercosis and fascioliasis. Curr Opin Infect Dis 20:489–494

    Article  PubMed  Google Scholar 

  35. Chen MG, Mott KE (1990) Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Trop Dis Bull 87:R1–R38

    Google Scholar 

  36. Aka NA, Adoubryn K, Rondelaud D, Dreyfuss G (2008) Human paragonimiasis in Africa. Ann Afr Med 7:153–162

    Article  PubMed  Google Scholar 

  37. Procop GW (2009) North American paragonimiasis (caused by Paragonimus kellicotti) in the context of global paragonimiasis. Clin Microbiol Rev 22:415–446

    Article  PubMed  PubMed Central  Google Scholar 

  38. Cribb TH, Bray RA, Olson PD, Littlewood DT (2003) Life cycle evolution in the digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254

    Article  PubMed  Google Scholar 

  39. Chai JY, Lee SH (2002) Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 51:129–154

    Article  PubMed  Google Scholar 

  40. Fried B, Graczyk TK, Tamang L (2004) Food-borne intestinal trematodiases in humans. Parasitol Res 93:159–170

    Article  PubMed  Google Scholar 

  41. Hong ST, Chai JY, Lee SH (1986) Ten human cases of Fibricola seoulensis infection and mixed one with Stellantchasmus and Metagonimus. Korean J Parasitol 24:95–97

    Article  Google Scholar 

  42. Esteban JG, Muñoz-Antolí C (2009) Echinostomes: systematics and life cycles. In: Fried B, Toledo R (eds) The biology of echinostomes. From the molecule to the community. Springer, New York, pp 1–34

    Google Scholar 

  43. Huffman JE, Fried B (1990) Echinostoma and echinostomiasis. Adv Parasitol 29:215–269

    Article  PubMed  CAS  Google Scholar 

  44. Toledo R, Esteban JG, Fried B (2009) Recent advances in the biology of echinostomes. Adv Parasitol 69:147–204

    Article  PubMed  Google Scholar 

  45. Graczyk TK, Fried B (2007) Human waterborne trematode and protozoan infections. Adv Parasitol 64:111–160

    Article  PubMed  Google Scholar 

  46. Chai JY (2009) Echinostomes in humans. In: Fried B, Toledo R (eds) The biology of echinostomes. From the molecule to the community. Springer, New York, pp 147–183

    Google Scholar 

  47. Haseeb MA, Eveland LK (2000) Human echinostomiasis: mechanisms of pathogenesis and host resistance. In: Fried B, Graczyk TK (eds) Echinostomes as experimental models for biological research. Kluwer Academic Publishers, Dordrecht, the Netherlands, pp 83–98

    Google Scholar 

  48. Sohn WM, Kim HJ, Yong TS, Eom KS, Jeong HG, Kim JK, Kang AR, Kim MR, Park JM, Ji SH, Sinuon M, Socheat D, Chai JY (2011) Echinostoma ilocanum infection in Oddar Meanchey Province, Cambodia. Korean J Parasitol 49:187–190

    Article  PubMed  PubMed Central  Google Scholar 

  49. Toledo R (2009) Immunology and pathology of echinostome infections in the definitive host. In: Fried B, Toledo R (eds) The biology of echinostomes. From the molecule to the community. Springer, New York, pp 185–206

    Google Scholar 

  50. Toledo R, Esteban JG, Fried B (2006) Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 63:285–365

    Article  PubMed  Google Scholar 

  51. Toledo R, Monteagudo C, Espert A, Fried B, Esteban JG, Marcilla A (2006) Echinostoma caproni: intestinal pathology in the golden hamster, a highly compatible host, and the Wistar rat, a less compatible host. Exp Parasitol 112:164–171

    Article  PubMed  CAS  Google Scholar 

  52. Graczyk TK, Fried B (1998) Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg 58:501–504

    PubMed  CAS  Google Scholar 

  53. Chattopadyay UK, Das MS, Pal D, Das S, Mukherjee A (1990) A case of echinostomiasis in a tribal community in Bengal. Ann Trop Med Parasitol 84:193

    PubMed  CAS  Google Scholar 

  54. Lee SH, Chai JY (2001) A review of Gymnophalloides seoi (Digenea: Gymnophallidae) and human infections in the Republic of Korea. Korean J Parasitol 39:85–118

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  55. Scholz T (2002) Family Gymnophallidae Odhner, 1905. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI Publishing, Wallingford, pp 345–351

    Google Scholar 

  56. Chai JY, Choi MH, Yu JR, Lee SH (2003) Gymnophalloides seoi: a new human intestinal trematode. Trends Parasitol 19:109–112

    Article  PubMed  Google Scholar 

  57. Chai JY, Lee GC, Park YK, Han ET, Seo M, Kim J, Guk SM, Shin EH, Choi MH, Lee SH (2000) Persistent endemicity of Gymnophalloides seoi infection in a southwestern coastal village of Korea with special reference to its egg laying capacity in the human host. Korean J Parasitol 38:51–57

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  58. Marty AM, Andersen EM (2000) Fasciolopsiasis and other intestinal trematodiasis. In: Meyers WM, Neafie RC, Marty AM, Wear DJ (eds) Pathology of infectious diseases, vol I helminthiases. Washington DC: Armed Forces Institute of Pathology (AFIP) and American Registry of Pathology, pp 93–105

    Google Scholar 

  59. Johansen MV, Sithithaworn P, Bergquist R, Utzinger J (2010) Towards improved diagnosis of zoonotic trematode infections in Southeast Asia. Adv Parasitol 73:171–195

    Article  PubMed  Google Scholar 

  60. Wongratanacheewin S, Pumidonming W, Sermswan RW, Pipitgool V, Maleewong W (2002) Detection of Opisthorchis viverrini in human stool specimens by PCR. J Clin Microbiol 40:3879–3880

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  61. Chaicumpa W, Ruangkunaporn Y, Kalambaheti T, Limavongpranee S, Kitikoon V, Khusmith S, Pungpak S, Chongsa-nguan M, Sornmani S (1991) Specific monoclonal antibodies to Opisthorchis viverrini. Int J Parasitol 21:969–974

    Article  PubMed  CAS  Google Scholar 

  62. Sirisinha S, Chawengkirttikul R, Haswell-Elkins MR, Elkins DB, Kaewkes S, Sithithaworn P (1995) Evaluation of a monoclonal antibody-based enzyme linked immunosorbent assay for the diagnosis of Opisthorchis viverrini infection in an endemic area. Am J Trop Med Hyg 52:521–524

    PubMed  CAS  Google Scholar 

  63. Mazidur Rahman SM, Choi MH, Bae YM, Hong ST (2012) Coproantigen capture ELISA for detection of Clonorchis sinensis infection in experimentally infected rats. Parasitol Int 61:203–207

    Article  PubMed  CAS  Google Scholar 

  64. Huang SY, Tang JD, Song HQ, Fu BQ, Xu MJ, Hu XC, Zhang H, Weng YB, Lin RQ, Zhu XQ (2012) A specific PCR assay for the diagnosis of Clonorchis sinensis infection in humans, cats and fishes. Parasitol Int 61:187–190

    Article  PubMed  CAS  Google Scholar 

  65. Kim EM, Verweij JJ, Jalili A, Van Lieshout L, Choi MH, Bae YM, Lim MK, Hong ST (2009) Detection of Clonorchis sinensis in stool samples using real-time PCR. Ann Trop Med Parasitol 103:513–518

    Article  PubMed  CAS  Google Scholar 

  66. Arimatsu Y, Kaewkes S, Laha T, Hong SJ, Sripa B (2012) Rapid detection of Opisthorchis viverrini copro-DNA using loop-mediated isothermal amplification (LAMP). Parasitol Int 61:178–182

    Article  PubMed  CAS  Google Scholar 

  67. Espinoza JR, Maco V, Marcos L, Saez S, Neyra V, Terashima A, Samalvides F, Gotuzzo E, Chavarry E, Huaman MC, Bargues MD, Valero MA, Mas-Coma S (2007) Evaluation of Fas2-ELISA for the serological detection of Fasciola hepatica infection in humans. Am J Trop Med Hyg 76:977–982

    PubMed  CAS  Google Scholar 

  68. Marcilla A, De la Rubia JE, Sotillo J, Bernal D, Carmona C, Villavicencio Z, Acosta D, Tort J, Bornay FJ, Esteban JG, Toledo R (2008) Leucine aminopeptidase is an immunodominant antigen of Fasciola hepatica excretory and secretory products in human infections. Clin Vaccine Immunol 15:95–100

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  69. O’Neill SM, Parkinson M, Strauss W, Angles R, Dalton JP (1998) Immunodiagnosis of Fasciola hepatica infection (fascioliasis) in a human population in the Bolivian Altiplano using purified cathepsin L cysteine proteinase. Am J Trop Med Hyg 58:417–423

    PubMed  Google Scholar 

  70. Lee JS, Lee J, Kim SH, Yong TS (2007) Molecular 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

    Article  PubMed  Google Scholar 

  71. Maleewong W, Intapan PM, Wongkham C, Wongsaroj T, Kowsuwan T, Pumidonming W, Pongsaskulchoti P, Kitikoon V (2003) Detection of Opisthorchis viverrini in experimentally infected bithynid snails and cyprinoid fishes by a PCR-based method. Parasitology 126:63–67

    Article  PubMed  CAS  Google Scholar 

  72. Doanh PN, Dung do T, Thach DT, Horii Y, Shinohara A, Nawa Y (2011) Human paragonimiasis in Viet Nam: epidemiological survey and identification of the responsible species by DNA sequencing of eggs in patients’ sputum. Parasitol Int 60:534–537

    Article  PubMed  CAS  Google Scholar 

  73. Chen MX, Ai L, Zhang RL, Xia JJ, Wang K, Chen SH, Zhang YN, Xu MJ, Li X, Zhu XQ, Chen JX (2011) Sensitive and rapid detection of Paragonimus westermani infection in humans and animals by loop-mediated isothermal amplification (LAMP). Parasitol Res 108:1193–1198

    Article  PubMed  CAS  Google Scholar 

  74. Lee SC, Chung YB, Kong Y, Kang SY, Cho SY (1993) Antigenic protein fractions of Metagonimus yokogawai reacting with patient sera. Korean J Parasitol 31:43–48

    Article  PubMed  CAS  Google Scholar 

  75. Ditrich O, Kopacek P, Giboda M, Gutvirth J, Scholz T (1991) Serological differentiation of human small fluke infections using Opisthorchis viverrini and Haplorchis taichui antigens. Southeast Asian J Trop Med Public Health 22:174–178

    PubMed  Google Scholar 

  76. Sohn WM (2009) Fish-borne zoonotic trematode metacercariae in the Republic of Korea. Korean J Parasitol 47:S103–S113

    Article  PubMed  PubMed Central  Google Scholar 

  77. Fried B (1994) Metacercarial excystment of trematodes. Adv Parasitol 33:91–144

    Article  PubMed  CAS  Google Scholar 

  78. Fried B, Peoples RC (2009) Maintenance, cultivation and excystation of echinostomes: 2000–2007. In: Fried B, Toledo R (eds) The biology of echinostomes. From the molecule to the community. Springer, New York, pp 111–128

    Google Scholar 

  79. Hertel J, Haberl B, Hamburger J, Haas W (2003) Description of a tandem repeated DNA sequence of Echinostoma caproni and methods for its detection in snail and plankton samples. Parasitology 126:443–449

    Article  PubMed  CAS  Google Scholar 

  80. Cai XQ, Yu HQ, Bai JS, Tang JD, Hu XC, Chen DH, Zhang RL, Chen MX, Ai L, Zhu XQ (2012) Development of a TaqMan based real-time PCR assay for detection of Clonorchis sinensis DNA in human stool samples and fishes. Parasitol Int 61:183–186

    Article  PubMed  CAS  Google Scholar 

  81. Keiser J, Utzinger J (2004) Chemotherapy for major food-borne trematodes: a review. Expert Opin Pharmacother 5:1711–1726

    Article  PubMed  CAS  Google Scholar 

  82. Tinga N, De N, Vien HV, Chau L, Toan ND, Kager PA, Vries PJ (1999) Little effect of praziquantel or artemisinin on clonorchiasis in Northern Vietnam. A pilot study. Trop Med Int Health 4:814–818

    Article  PubMed  CAS  Google Scholar 

  83. Ibarra VF, García SE, Fernández RM, Vera MY, Castillo BR, Hernández CA (1997) Eficacia de dos compuestos de síntesis química in vitro e in vivo en ovinos. Vet Méx 28:291–296

    Google Scholar 

  84. Ibarra VF, Vera MY, Hernández CA, Castillo BR (1997) Eficacia fasciolicida del compuesto “alfa” contra estadios juveniles y adultos en ovinos. Vet Méx 28:297–301

    Google Scholar 

  85. Rivera FN, Ibarra VF, Olazarán JS, Vera MY, Castillo BR, Hernández CA (2002) Efficacy of 5-2-chloro-methylthio-6-(1-naftiloxi)-ih-benzimidazole against different stages of Fasciola hepatica in Pelibuey sheep. Vet Méx 33:55–61

    Google Scholar 

  86. Vera MY, Ibarra VF, Quiroz RH, Hernández CA, Castillo R (2003) Field trial on the efficacy of an experimental fasciolicide compared with some commercial compounds in naturally infected cattle. Parasitol Res 91:1–4

    Article  Google Scholar 

  87. Vera MY, Ibarra VF, Liébano HE, Quiroz RH, Castillo BR, Hernández CA, Ochoa GP (2004) Efficacy of an experimental fasciolicide against immature and mature Fasciola hepatica in artificially infected calves. Parasitol Res 92:211–214

    Article  Google Scholar 

  88. McConville M, Brennan GP, Flanagan A, Edgar HW, Hanna REB, McCoy M, Gordon AW, Castillo R, Hernández-Campos A, Fairweather I (2009) An evaluation of the efficacy of compound alpha and triclabendazole against two isolates of Fasciola hepatica. Vet Parasitol 162:75–88

    Article  PubMed  CAS  Google Scholar 

  89. McConville M, Hanna REB, Brennan GP, McCoy M, Edgar HWJ, McConnell S, Castillo R, Hernández-Campos A, Fairweather I (2010) Fasciola hepatica: disruption of spermatogenesis by the fasciolicide compound alpha. Parasitol Res 106:311–323

    Article  PubMed  Google Scholar 

  90. McConville M, Brennan GP, McCoy M, Castillo R, Hernández-Campos A, Ibarra F, Fairweather I (2006) Adult triclabendazole-resistant Fasciola hepatica: surface and subsurface tegumental responses to in vitro treatment with the sulphoxide metabolite of the experimental fasciolicide compound alpha. Parasitology 133:195–208

    Article  PubMed  CAS  Google Scholar 

  91. Hanna REB, Edgar HWJ, McConnell S, Toner E, McConville M, Brennan GP, Devine C, Flanagan A, Halferty L, Meaney M, Shaw L, Moffett D, McCoy M, Fairweather I (2010) Fasciola hepatica: histological changes in the reproductive structures of triclabendazole (TCBZ)-sensitive and TCBZ-resistant flukes after treatment in vivo with TCBZ and the related benzimidazole derivative, Compound Alpha. Vet Parasitol 168:240–254

    Article  PubMed  CAS  Google Scholar 

  92. Keiser J, Utzinger J (2007) Food-borne trematodiasis: current chemotherapy and advances with artemisinins and synthetic trioxolanes. Trends Parasitol 23:555–562

    Article  PubMed  CAS  Google Scholar 

  93. Keiser J, Xiao SH, Xue J, Chan ZS, Odermatt P, Tesana S, Tanner M, Utzinger J (2006) Effect of artesunate and artemether against Clonorchis sinensis and Opisthorchis viverrini in rodent models. Int J Antimicrob Agents 28:370–373

    Article  PubMed  CAS  Google Scholar 

  94. Xiao SH, Xue J, Tanner M, Zhang YN, Keiser J, Utzinger J, Quiang HQ (2008) Artemether, artesunate, praziquantel and tribendimidine administered singly at different dosages against Clonorchis sinensis: a comparative in vivo study. Acta Trop 106:54–59

    Article  PubMed  CAS  Google Scholar 

  95. Keiser J, Brun R, Fried B, Utzinger J (2006) Trematocidal activity of praziquantel and artemisinin derivatives: in vitro and in vivo investigations with adult Echinostoma caproni. Antimicrob Agents Chemother 50:803–805

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  96. Fathy FM (2011) Anthelmintic effect of artesunate in experimental heterophyid infection. J Egypt Soc Parasitol 41:469–483

    PubMed  Google Scholar 

  97. Keiser J, Utzinger J, Vennerstrom JL, Dong Y, Brennan G, Fairweather I (2007) Activity of artemether and OZ78 against triclabendazole-resistant Fasciola hepatica. Trans R Soc Trop Med Hyg 101:1219–1222

    Article  PubMed  CAS  Google Scholar 

  98. Keiser J, Rinaldi L, Veneziano V, Mezzino L, Tanner M, Utzinger J, Cringoli G (2008) Efficacy and safety of artemether against a natural Fasciola hepatica infection in sheep. Parasitol Res 103:517–522

    Article  PubMed  Google Scholar 

  99. Hien TT, Truong NT, Minh NH, Dat HD, Dung NT, Hue NT, Dung TK, Tuan PQ, Campbell JI, Farrar JJ, Day JN (2008) A randomized controlled pilot study of artesunate versus triclabendazole for human fascioliasis in central Vietnam. Am J Trop Med Hyg 73:388–392

    Google Scholar 

  100. Keiser J, Sayed H, el-Ghanam M, Sabry H, Anani S, el-Wakeel A, Hatz C, Utzinger J, el-Din SS, el-Maadawy W, Botros S (2011) Efficacy and safety of artemether in the treatment of chronic fascioliasis in Egypt: exploratory phase-2 trials. PLoS Negl Trop Dis 5:e1285

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  101. Keiser J, Utzinger J, Tanner M, Dong Y, Vennerstrom JL (2006) The synthetic peroxide OZ78 is effective against Echinostoma caproni and Fasciola hepatica. J Antimicrob Chemother 58:1193–1197

    Article  PubMed  CAS  Google Scholar 

  102. Keiser J, Kirchhofer C, Haschke M, Huwyler J, Dong Y, Vennerstrom JL, Vanhoff K, Kaminsky R, Malikides N (2010) Efficacy, safety and pharmacokinetics of 1,2,4-trioxolane OZ78 against an experimental infection with Fasciola hepatica in sheep. Vet Parasitol 173:228–235

    Article  PubMed  CAS  Google Scholar 

  103. Keiser J, Shu-Hua X, Chollet J, Tanner M, Utzinger J (2007) Evaluation of the in vivo activity of tribendimidine against Schistosoma mansoni, Fasciola hepatica, Clonorchis sinensis, and Opisthorchis viverrini. Antimicrob Agents Chemother 51:1096–1098

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  104. Soliman MI, Taha HA (2011) Tegumental alterations of Fasciola gigantica due to in vitro treatment with Ro-354. Trop Biomed 28:283–292

    PubMed  CAS  Google Scholar 

  105. Kerboeuf D, Riou M, Guégnard F (2008) Flavonoids and related compounds in parasitic disease control. Mini Rev Med Chem 8:116–128

    Article  PubMed  CAS  Google Scholar 

  106. Ferreira JFS, Peaden P, Keiser J (2011) In vitro trematocidal effects of crude alcoholic extracts of Artemisia annua, A. absinthium, Asimina triloba, and Fumaria officinalis. Trematocidal plant alcoholic extracts. Parasitol Res 109:1585–1592

    Article  PubMed  Google Scholar 

  107. Traub RJ, Macaranas J, Mungthin M, Leelayoova S, Cribb T, Murrell KD, Thompson RC (2009) A new PCR-based approach indicates the range of Clonorchis sinensis now extends to Central Thailand. PLoS Negl Trop Dis 3:e367

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  108. Kim TY, Chung EJ, Sohn WM, Hong SH, Yong TS (2011) Molecular characterization of Clonorchis sinensis tetraspanin 2 extracellular loop 2. Parasitol Res (in press)

  109. Chen W, Wang X, Li X, Lv X, Zhou C, Deng C, Lei H, Men J, Fan Y, Liang C, Yu X (2011) Molecular characterization of cathepsin B from Clonorchis sinensis excretory/secretory products and assessment of its potential for serodiagnosis of clonorchiasis. Parasit Vectors 4:149

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  110. Wang X, Chen W, Li X, Zhou C, Deng C, Lv X, Fan Y, Men J, Liang C, Yu X (2011) Identification and molecular characterization of a novel signaling molecule 14-3-3 epsilon in Clonorchis sinensis excretory/secretory products. Parasitol Res (in press)

  111. Lee MR, Kim YJ, Kim DW, Yoo WG, Cho SH, Hwang KY, Ju JW, Lee WJ (2011) The identification of antigenic proteins: 14-3-3 protein and propionyl-CoA carboxylase in Clonorchis sinensis. Mol Biochem Parasitol (in press)

  112. Wu W, Chen J, Zeng S, Zhang Z, Gan W, Yu X, Hu X (2011) Molecular cloning, expression, and characterization of cyclophilin A from Clonorchis sinensis. Parasitol Res 109:345–351

    Article  PubMed  Google Scholar 

  113. Zhou Z, Xia H, Hu X, Huang Y, Li Y, Li L, Ma C, Chen X, Hu F, Xu J, Lu F, Wu Z, Yu X (2008) Oral administration of a Bacillus subtilis spore-based vaccine expressing Clonorchis sinensis tegumental protein 22.3 kDa confers protection against Clonorchis sinensis. Vaccine 26:1817–1825

    Article  PubMed  CAS  Google Scholar 

  114. Huang SY, Zhao GH, Fu BQ, Xu MJ, Wang CR, Wu SM, Zou FC, Zhu XQ (2012) Genomics and molecular genetics of Clonorchis sinensis: current status and perspectives. Parasitol Int 61:71–76

    Article  PubMed  CAS  Google Scholar 

  115. Wang X, Chen W, Huang Y, Sun J, Men J, Liu H, Luo F, Guo L, Lv X, Deng C, Zhou C, Fan Y, Li X, Huang L, Hu Y, Liang C, Hu X, Xu J, Yu X (2011) The draft genome of the carcinogenic human liver fluke Clonorchis sinensis. Genome Biol 12:R107

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  116. Yoo WG, Kim DW, Ju JW, Cho PY, Kim TI, Cho SH, Choi SH, Park HS, Kim TS, Hong SJ (2011) Developmental transcriptomic features of the carcinogenic liver fluke, Clonorchis sinensis. PLoS Negl Trop Dis 5:e1208

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by the projects CGL2005-0231/BOS from the Ministerio de Ciencia e Innovación and FEDER (European Union), SAF2010-16236 from Ministerio de Ciencia y Innovación (Spain), PROMETEO/2009/081 from Conselleria d’Educació, Generalitat Valenciana (Valencia, Spain), PS09/ 02355 from the Fondo de Investigación Sanitaria (FIS) del Ministerio de Ciencia e Innovación (Madrid, Spain) and FEDER, and UV-AE-10- 23739 from the Universitat de València (Valencia, Spain).

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  1. Departamento de Parasitología, Facultad de Farmacia, Universidad de Valencia, Av. Vicente Andrés Estellés s/n, 46100, Burjassot, Valencia, Spain

    R. Toledo & J. G. Esteban

  2. Department of Biology, Lafayette College, Easton, PA, 18042, USA

    B. Fried

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  1. R. Toledo
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  2. J. G. Esteban
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  3. B. Fried
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Correspondence to R. Toledo.

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Toledo, R., Esteban, J.G. & Fried, B. Current status of food-borne trematode infections. Eur J Clin Microbiol Infect Dis 31, 1705–1718 (2012). https://doi.org/10.1007/s10096-011-1515-4

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  • DOI: https://doi.org/10.1007/s10096-011-1515-4

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