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Food-borne Trematodiases in East Asia: Epidemiology and Burden

  • Thomas FürstEmail author
  • Puangrat Yongvanit
  • Narong Khuntikeo
  • Zhao-Rong Lun
  • Juanita A. Haagsma
  • Paul R. Torgerson
  • Peter Odermatt
  • Christine Bürli
  • Nakul Chitnis
  • Paiboon Sithithaworn
Chapter
Part of the Neglected Tropical Diseases book series (NTD)

Abstract

Food-borne trematodiases are a cluster of parasitic helminth infections in humans and animals and belong to the cluster of neglected tropical diseases. The causative helminths dispose of a complex life cycle. As with many helminth infections, most infected people may only experience mild and non-specific clinical signs and symptoms. However, repeated, heavy and long-term infections may lead to severe clinical manifestations and also potentially fatal complications such as cholangiocarcinoma. Diagnosis remains a challenge as reliable, affordable, rapid, and simple-to-use diagnostic techniques are not available. If correctly and early diagnosed, safe, cheap, efficacious, orally administered drugs are available. Globally, the disease burden of food-borne trematodiases is estimated to be well within the range of other and better known neglected tropical diseases (e.g. dengue, leishmaniasis, lymphatic filariasis, onchocerciasis, and schistosomiasis) with a concentration in East and Southeast Asia. Food-borne trematodiases are zoonoses and may also have a negative impact on agri- and aquacultural production in affected regions. Mathematical modelling and analysis of food-borne trematodiases transmission dynamics to inform control and prevention is still in a very early stage, also due to the very limited availability of essential data. The current mainstay of human food-borne trematodiases control is drug-based morbidity control. For improved control, prevention or even elimination, more integrated efforts adopting also an ecosystem and “One Health” perspective are needed.

Keywords

Food-borne trematodiases Neglected tropical diseases East and Southeast Asia Epidemiology Burden of disease Life cycle Transmission Clinical signs and symptoms Diagnosis Treatment Veterinary issues Economic issues Mathematical disease modelling Control and prevention 

Notes

Conflict of Interests

The authors have nothing to disclose.

Funding Statement

TF acknowledges financial support from the Swiss National Science Foundation (project no. P300P3-154634). PY, NK, and PS are supported by the National Research Council of Thailand through the Fluke Free Thailand Project. ZRL is supported by grants from the National Base Research programme (973 project; NO.2010CB530000) and the National Natural Science Foundation of China (project nos. #31272305 and #31472058). NC acknowledges funding from the RAPIDD program of the Science & Technology Directorate, Department of Homeland Security, and the Fogarty International Center, National Institutes of Health, USA.

References

  1. Ababouch L (2006) Assuring fish safety and quality in international fish trade. Mar Pollut Bull 53:561–568PubMedCrossRefPubMedCentralGoogle Scholar
  2. Allen EJ, Victory HD (2003) Modelling and simulation of a schistosomiasis infection with biological control. Acta Trop 87:251–267PubMedCrossRefPubMedCentralGoogle Scholar
  3. Andrews SJ (1999) The life cycle of Fasciola hepatica. In: Dalton JP (ed) Fasciolosis. CAB International, WallingfordGoogle Scholar
  4. Andrews RH, Sithithaworn P, Petney TN (2008) Opisthorchis viverrini: an underestimated parasite in world health. Trends Parasitol 24:497–501PubMedPubMedCentralCrossRefGoogle Scholar
  5. Andriamanantena D, Rey P, Perret JL, Klotz F (2005) Distomatoses. EMC-Malad Infect 2:105–118. (in French)CrossRefGoogle Scholar
  6. Anh VT, Tram NT, Klank LT, Cam PD, Dalsgaard A (2007) Faecal and protozoan parasite contamination of water spinach (Ipomoea aquatica) cultivated in urban wastewater in Phnom Penh, Cambodia. Trop Med Int Health 12:73–81CrossRefGoogle Scholar
  7. Attwood HD, Chou ST (1978) Longevity of Clonorchis sinensis. Pathology 10:153–156PubMedCrossRefPubMedCentralGoogle Scholar
  8. Aunpromma S, Tangkawattana P, Papirom P, Kanjampa P, Tesana S, Sripa B, Tangkawattana S (2012) High prevalence of Opisthorchis viverrini infection in reservoir hosts in four districts of Khon Kaen Province, an opisthorchiasis endemic area of Thailand. Parasitol Int 61:60–64PubMedCrossRefPubMedCentralGoogle Scholar
  9. Barbour AD (1978) MacDonald’s model and the transmission of bilharzia. Trans R Soc Trop Med Hyg 72:6–15PubMedCrossRefGoogle Scholar
  10. Belizario VY, Bersabe MJJ, de Los Reyes ABE, de Leon WU (2004) School-based assessment of soil-transmitted helminthiasis and foodborne parasitosis (intestinal fluke infection) in Monkayo, Compostela Valley. Southeast Asian J Trop Med Public Health 35:123–139Google Scholar
  11. Belizario VY, Mallari AO, de Leon WU, Lucero AC (2007) Assessment of the efficacy, safety, and tolerability of praziquantel and triclabendazole in the treatment of paragonimiasis. Southeast Asian J Trop Med Public Health 38:97–105Google Scholar
  12. Bergquist R, Lustigman S (2010) Control of important helminthic infections: vaccine development as part of the solution. Adv Parasitol 73:297–326PubMedCrossRefPubMedCentralGoogle Scholar
  13. Blair D (2014) Paragonimiasis. Adv Exp Med Biol 766:115–152PubMedCrossRefPubMedCentralGoogle Scholar
  14. Blair D, Agatsuma T, Wang W (2007) Paragonimiasis. In: Murrell KD, Fried B (eds) World class parasites. Springer, DordrechtGoogle Scholar
  15. Bless PJ, Schär F, Khieu V, Kramme S, Muth S, Marti H, Odermatt P (2015) High prevalence of large trematode eggs in schoolchildren in Cambodia. Acta Trop 141:295–302PubMedCrossRefPubMedCentralGoogle Scholar
  16. Bondad-Reantaso MG, Subasinghe RP, Arthur JR, Ogawa K, Chinabut S, Adlard R, Tan Z, Shariff M (2005) Disease and health management in Asian aquaculture. Vet Parasitol 132:249–272PubMedCrossRefPubMedCentralGoogle Scholar
  17. Bundhamcharoen K, Odton P, Phulkerd S, Tangcharoensathien V (2011) Burden of disease in Thailand: changes in health gap between 1999 and 2004. BMC Public Health 11:53PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bürli C, Harbrecht H, Odermatt P, Sayasone S, Chitnis N (2018) Mathematical analysis of the transmission dynamics of the liver fluke, Opisthorchis viverrini. J Theor Biol 439:181–194PubMedCrossRefPubMedCentralGoogle Scholar
  19. Buzby JC, Roberts T (2009) The economics of enteric infections: human foodborne disease costs. Gastroenterology 136:1851–1862PubMedCrossRefGoogle Scholar
  20. Cabada MM, White AC (2012) New developments in epidemiology, diagnosis, and treatment of fascioliasis. Curr Opin Infect Dis 25:518–522PubMedCrossRefPubMedCentralGoogle Scholar
  21. Caban-Hernandez K, Gaudier JF, Ruiz-Jimenez C, Espino AM (2014) Development of two antibody detection enzyme-linked immunosorbent assays for serodiagnosis of human chronic fascioliasis. J Clin Microbiol 52:766–772PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cadmus SIB, Adesokan HK (2009) Causes and implications of bovine organs/offal condemnations in some abattoirs in western Nigeria. Trop Anim Health Prod 41:1455–1463PubMedCrossRefPubMedCentralGoogle Scholar
  23. Chai JY (2007) Intestinal flukes. In: Murrell KD, Fried B (eds) World class parasites. Springer, DordrechtGoogle Scholar
  24. 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 38:51–57PubMedPubMedCentralCrossRefGoogle Scholar
  25. Chai JY, Bahk YY, Sohn WM (2013a) Trematodes recovered in the small intestine of stray cats in the Republic of Korea. Korean J Parasitol 51:99–106PubMedPubMedCentralCrossRefGoogle Scholar
  26. Chai JY, Yong TS, Eom KS, Min DY, Jeon HK, Kim TY, Jung BK, Sisabath L, Insisiengmay B, Phommasack B, Rim HJ (2013b) Hyperendemicity of Haplorchis taichui infection among riparian people in Saravane and Champasak province, Lao PDR. Korean J Parasitol 51:305–311PubMedPubMedCentralCrossRefGoogle Scholar
  27. Chamadol N, Pairojkul C, Khuntikeo N, Laopaiboon V, Loilome W, Sithithaworn P, Yongvanit P (2014) Histological confirmation of periductal fibrosis from ultrasound diagnosis in cholangiocarcinoma patients. J Hepatobiliary Pancreat Sci 21:316–322PubMedCrossRefPubMedCentralGoogle Scholar
  28. Charlier J, van der Voort M, Hogeveen H, Vercruysse J (2012) ParaCalc—a novel tool to evaluate the economic importance of worm infections on the dairy farm. Vet Parasitol 184:204–211PubMedCrossRefPubMedCentralGoogle Scholar
  29. Chen JX, Chen MX, Ai L, Xu XN, Jiao JM, Zhu TJ, Su HY, Zang W, Luo JJ, Guo YH, Lv S, Zhou XN (2013) An outbreak of human fascioliasis gigantica in southwest China. PLoS One 8:e71520PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chi TT, Dalsgaard A, Turnbull JF, Tuan PA, Murrell KD (2008) Prevalence of zoonotic trematodes in fish from a Vietnamese fish-farming community. J Parasitol 94:423–428PubMedCrossRefPubMedCentralGoogle Scholar
  31. Choi MS, Choi D, Choi MH, Ji Z, Li Z, Cho SY, Hong KS, Rim HJ, Hong ST (2005) Correlation between sonographic findings and infection intensity in clonorchiasis. Am J Trop Med Hyg 73:1139–1144PubMedCrossRefPubMedCentralGoogle Scholar
  32. Choi MH, Park SK, Li Z, Ji Z, Yu G, Feng Z, Xu L, Cho SY, Rim HJ, Lee SH, Hong ST (2010) Effect of control strategies on prevalence, incidence and reinfection of clonorchiasis in endemic areas of China. PLoS Negl Trop Dis 4:e601PubMedPubMedCentralCrossRefGoogle Scholar
  33. Clausen JH, Madsen H, Murrell KD, Van PT, Thu HNT, Do DT, Thi LAN, Manh HN, Dalsgaard A (2012) Prevention and control of fishborne zoonotic trematodes in fish nurseries, Vietnam. Emerg Infect Dis 18:1438–1445PubMedCentralCrossRefPubMedGoogle Scholar
  34. Copeman DB, Copland RS (2008) Importance and potential impact of liver fluke in cattle and buffalo. In: Gray GD, Copland RS, Copeman DB (eds) Overcoming liver fluke as a constraint to ruminant production in Southeast Asia. ACIAR, CanberraGoogle Scholar
  35. Elkins DB, Sithithaworn P, Haswell-Elkins MR, Kaewkes S, Awacharagan P, Wongratanacheewin S (1991) Opisthorchis viverrini: relationships between egg counts, worms recovered and antibody-levels within an endemic community in northeast Thailand. Parasitology 102:283–288PubMedCrossRefPubMedCentralGoogle Scholar
  36. Elkins DB, Mairiang E, Sithithaworn P, Mairiang P, Chaiyakum J, Chamadol N, Loapaiboon V, Haswell-Elkins MR (1996) Cross-sectional patterns of hepatobiliary abnormalities and possible precursor conditions of cholangiocarcinoma associated with Opisthorchis viverrini infection in humans. Am J Trop Med Hyg 55:295–301PubMedCrossRefPubMedCentralGoogle Scholar
  37. Espinoza JR, Terashima A, Herrera-Velit P, Marcos LA (2010) Human and animal fascioliasis in Peru: impact in the economy of endemic zones. Rev Peru Med Exp Salud Publica 27:604–612. (in Spanish)PubMedCrossRefPubMedCentralGoogle Scholar
  38. Fairweather I (2011) Reducing the future threat from (liver) fluke: realistic prospect or quixotic fantasy? Vet Parasitol 180:133–143PubMedCrossRefGoogle Scholar
  39. FAO (1994) Diseases of domestic animals caused by flukes: epidemiology, diagnosis and control of Fasciola, paramphistome, Dicrocoelium, Eurytrema and schistosome infections of ruminants in developing countries. FAO, RomeGoogle Scholar
  40. Fried B, Graczyk TK, Tamang L (2004) Foodborne intestinal trematodiases in humans. Parasitol Res 93:159–170PubMedCrossRefPubMedCentralGoogle Scholar
  41. Fuentes MV (2006) Remote sensing and climate data as a key for understanding fasciolosis transmission in the Andes: review and update of an ongoing interdisciplinary project. Geospat Health 1:59–70PubMedCrossRefPubMedCentralGoogle Scholar
  42. Fuentes MV (2007) Is the El Niño Southern Oscillation likely to increase the risk of Fasciola transmission? Ann Trop Med Parasitol 101:555–557PubMedCrossRefPubMedCentralGoogle Scholar
  43. Fürst T, Duthaler U, Sripa B, Utzinger J, Keiser J (2012a) Trematode infections: liver and lung flukes. Infect Dis Clin North Am 26:399–419PubMedCrossRefPubMedCentralGoogle Scholar
  44. Fürst T, Keiser J, Utzinger J (2012b) Global burden of human foodborne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis 12:210–221PubMedCrossRefPubMedCentralGoogle Scholar
  45. Fürst T, Sayasone S, Odermatt P, Keiser J, Utzinger J (2012c) Manifestation, diagnosis, and management of foodborne trematodiasis. BMJ 344:e4093PubMedCrossRefPubMedCentralGoogle Scholar
  46. Global Burden of Disease 2013 DALYs and HALE Collaborators (2015) Global, regional, and national disability-adjusted life-years (DALYs) for 306 diseases and injuries and healthy life expectancy (HALE) for 188 countries, 1990–2013: quantifying the epidemiological transition. Lancet 386:2145–2191CrossRefGoogle Scholar
  47. Global Burden of Disease 2015 DALYs and HALE Collaborators (2016) Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388:1603–1658CrossRefGoogle Scholar
  48. Global Burden of Disease 2016 DALYs and HALE Collaborators (2017) Global, regional, and national disability-adjusted life-years (DALYs) for 333 diseases and injuries and haealthy life expectancy (HALE) for 195 countries and territories, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet 390:1260–1344CrossRefGoogle Scholar
  49. Gonzales Santana B, Dalton JP, Vasquez Camargo F, Parkinson M, Ndao M (2013) The diagnosis of human fascioliasis by enzyme-linked immunosorbent assay (ELISA) using recombinant cathepsin L protease. PLoS Negl Trop Dis 7:e2414PubMedPubMedCentralCrossRefGoogle Scholar
  50. Graczyk TK, Fried B (2007) Human waterborne trematode and protozoan infections. Adv Parasitol 64:111–160PubMedCrossRefPubMedCentralGoogle Scholar
  51. Gutierrez Y (2000) Diagnostic parasitology of parasitic infections with clinical correlations. Lea & Febiger, Philadelphia, PAGoogle Scholar
  52. Habbema JDF, van Oortmarssen GJ, Plaisier AP (1996) The ONCHOSIM model and its use in decision support for river blindness control. In: Isham V, Medley G (eds) Models for infectious human diseases: their structure and relation to data. Cambridge University Press, CambridgeGoogle Scholar
  53. Haridy FM, Morsy TA, Gawish NI, Antonios TN, Abdel Gawad AG (2002) The potential reservoir role of donkeys and horses in zoonotic fascioliasis in Gharbia Governorate, Egypt. J Egypt Soc Parasitol 32:561–571PubMedPubMedCentralGoogle Scholar
  54. Haswell-Elkins MR, Satarug S, Tsuda M, Mairiang E, Esumi H, Sithithaworn P, Mairiang P, Saitoh M, Yongvanit P, Elkins DB (1994) Liver fluke infection and cholangiocarcinoma: model of endogenous nitric oxide and extragastric nitrosation in human carcinogenesis. Mutat Res 305:241–252PubMedCrossRefPubMedCentralGoogle Scholar
  55. Hethcote HW (2000) The mathematics of infectious diseases. SIAM Rev 42:599–653CrossRefGoogle Scholar
  56. Hillyer GV, Apt W (1997) Foodborne trematode infections in the Americas. Parasitol Today 13:87–88CrossRefGoogle Scholar
  57. Hisakane N, Kirinoki M, Chigusa Y, Sinuon M, Socheat D, Matsuda H, Ishikawa H (2008) The evaluation of control measures against Schistosoma mekongi in Cambodia by a mathematical model. Parasitol Int 57:379–385PubMedCrossRefPubMedCentralGoogle Scholar
  58. Hong ST, Fang Y (2012) Clonorchis sinensis and clonorchiasis, an update. Parasitol Int 61:17–24PubMedCrossRefPubMedCentralGoogle Scholar
  59. Hotez PJ, Ehrenberg JP (2010) Escalating the global fight against neglected tropical diseases through interventions in the Asia Pacific region. Adv Parasitol 72:31–53PubMedCrossRefPubMedCentralGoogle Scholar
  60. Hu H, Gong P, Xu B (2010) Spatially explicit agent-based modelling for schistosomiasis transmission: human-environment interaction simulation and control strategy assessment. Epidemics 2:49–65PubMedCrossRefPubMedCentralGoogle Scholar
  61. Huffman JE, Fried B (1990) Echinostoma and echinostomiasis. Adv Parasitol 29:215–269PubMedCrossRefPubMedCentralGoogle Scholar
  62. Institute for Health Metrics and Evaluation (2017) GBD compare [Online]. Institute for Health Metrics and Evaluation. http://vizhub.healthdata.org/gbd-compare. Accessed 24 Nov 2017
  63. Johansen MV, Sithithaworn P, Bergquist R, Utzinger J (2010) Towards improved diagnosis of zoonotic trematode infections in Southeast Asia. Adv Parasitol 73:171–195PubMedCrossRefPubMedCentralGoogle Scholar
  64. Johansen MV, Lier T, Sithithaworn P (2015) Towards improved diagnosis of neglected zoonotic trematodes using a one health approach. Acta Trop 141:161–169PubMedCrossRefPubMedCentralGoogle Scholar
  65. Kaewkes S, Elkins DB, Sithithaworn P, Haswell-Elkins MR (1991) Comparative studies on the morphology of the eggs of Opisthorchis viverrini and lecithodendriid trematodes. Southeast Asian J Trop Med Public Health 22:623–630PubMedPubMedCentralGoogle Scholar
  66. Kaewpitoon N, Kaewpitoon SJ, Pengsaa P (2008a) Opisthorchiasis in Thailand: review and current status. World J Gastroenterol 14:2297–2302PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kaewpitoon N, Kaewpitoon SJ, Pengsaa P, Sripa B (2008b) Opisthorchis viverrini: the carcinogenic human liver fluke. World J Gastroenterol 14:666–674PubMedPubMedCentralCrossRefGoogle Scholar
  68. Keiser J, Utzinger J (2004) Chemotherapy for major foodborne trematodes: a review. Expert Opin Pharmacother 5:1711–1726PubMedCrossRefPubMedCentralGoogle Scholar
  69. Keiser J, Utzinger J (2005) Emerging foodborne trematodiasis. Emerg Infect Dis 11:1507–1514PubMedPubMedCentralCrossRefGoogle Scholar
  70. Keiser J, Utzinger J (2009) Foodborne trematodiases. Clin Microbiol Rev 22:466–483PubMedPubMedCentralCrossRefGoogle Scholar
  71. Keiser J, Xiao SH, Xue J, Chang 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 28:370–373PubMedCrossRefPubMedCentralGoogle Scholar
  72. Khan SA, Davidson BR, Goldin RD, Heaton N, Karani J, Pereira SP, Rosenberg WM, Tait P, Taylor-Robinson SD, Thillainayagam AV, Thomas HC, Wasan H (2012) Guidelines for the diagnosis and treatment of cholangiocarcinoma: an update. Gut 61:1657–1669PubMedCrossRefPubMedCentralGoogle Scholar
  73. Khuntikeo N, Pugkhem A, Titapun A, Bhudhisawasdi V (2014) Surgical management of perihilar cholangiocarcinoma: a Khon Kaen experience. J Hepatobiliary Pancreat Sci 21:521–524PubMedCrossRefPubMedCentralGoogle Scholar
  74. Kopolrat K, Sithithaworn P, Tesana S, Andrews RH, Petney TN (2015) Susceptibility, metacercarial burden, and mortality of juvenile silver barb, common carp, mrigal and tilapia following exposure to Haplorchis taichui. Parasitol Res 114:1433–1442PubMedCrossRefPubMedCentralGoogle Scholar
  75. Krull WH (1941) The number of cercariae of Fasciola hepatica developing in snails infected with a single miracidium. In: Christie JR (ed) Proceedings of the Helminthological Society of Washington. Helminthological Society of Washington, Washington, DCGoogle Scholar
  76. Li T, He S, Zhao H, Zhao G, Zhu XQ (2010) Major trends in human parasitic diseases in China. Trends Parasitol 26:264–270PubMedCrossRefPubMedCentralGoogle Scholar
  77. Lin RQ, Tang JD, Zhou DH, Song HQ, Huang SY, Chen JX, Chen MX, Zhang H, Zhu XQ, Zhou XN (2011) Prevalence of Clonorchis sinensis infection in dogs and cats in subtropical southern China. Parasit Vectors 4:180PubMedPubMedCentralCrossRefGoogle Scholar
  78. Loaharanu P, Sornmani S (1991) Preliminary estimates of economic impact of liver fluke infection in Thailand and the feasibility of irradiation as a control measure. Southeast Asian J Trop Med Public Health 22:384–390PubMedPubMedCentralGoogle Scholar
  79. 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 5:31–41PubMedCrossRefPubMedCentralGoogle Scholar
  80. Mairiang E, Laha T, Bethony JM, Thinkhamrop B, Kaewkes S, Sithithaworn P, Tesana S, Loukas A, Brindley PJ, Sripa B (2012) Ultrasonography assessment of hepatobiliary abnormalities in 3359 subjects with Opisthorchis viverrini infection in endemic areas of Thailand. Parasitol Int 61:208–211PubMedCrossRefGoogle Scholar
  81. Mas-Coma S, Bargues MD, Esteban JG (1999) Human fasciolosis. In: Dalton JP (ed) Fasciolosis. CAB International, WallingfordGoogle Scholar
  82. Mas-Coma S, Bargues MD, Valero MA (2005) Fascioliasis and other plantborne trematode zoonoses. Int J Parasitol 35:1255–1278PubMedCrossRefGoogle Scholar
  83. Mas-Coma S, Bargues MD, Valero MA (2007) Plantborne trematode zoonoses: fascioliasis and fasciolopsiasis. In: Murrell KD, Fried B (eds) World class parasites. Springer, DordrechtGoogle Scholar
  84. Mas-Coma S, Bargues MD, Valero MA (2014) Diagnosis of human fascioliasis by stool and blood techniques: update for the present global scenario. Parasitology 141:1918–1946PubMedCrossRefGoogle Scholar
  85. Monis PT, Andrews RH (1998) Molecular epidemiology: assumptions and limitations of commonly applied methods. Int J Parasitol 28:981–987PubMedCrossRefGoogle Scholar
  86. Montresor A, Cong DT, Sinuon M, Tsuyuoka R, Chanthavisouk C, Strandgaard H, Velayudhan R, Capuano CM, Le Anh T, Dato AST (2008) Large-scale preventive chemotherapy for the control of helminth infection in Western Pacific countries: six years later. PLoS Negl Trop Dis 2:e278PubMedPubMedCentralCrossRefGoogle Scholar
  87. Murray CJL, Vos T, Lozano R, Naghavi M, Flaxman AD, Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S, Aboyans V, Abraham J, Ackerman I, Aggarwal R, Ahn SY, Ali MK, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Bahalim AN, Barker-Collo S, Barrero LH, Bartels DH, Basanez MG, Baxter A, Bell ML, Benjamin EJ, Bennett D, Bernabe E, Bhalla K, Bhandari B, Bikbov B, Bin Abdulhak A, Birbeck G, Black JA, Blencowe H, Blore JD, Blyth F, Bolliger I, Bonaventure A, Boufous S, Bourne R, Boussinesq M, Braithwaite T, Brayne C, Bridgett L, Brooker S, Brooks P, Brugha TS, Bryan-Hancock C, Bucello C, Buchbinder R, Buckle G, Budke CM, Burch M, Burney P, Burstein R, Calabria B, Campbell B, Canter CE, Carabin H, Carapetis J, Carmona L, Cella C, Charlson F, Chen H, Cheng AT, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, de Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahiya M, Dahodwala N, Damsere-Derry J, Danaei G, Davis A, de Leo D, Degenhardt L, Dellavalle R, Delossantos A, Denenberg J, Derrett S, Des Jarlais DC, Dharmaratne SD et al (2012) Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2197–2223PubMedCrossRefGoogle Scholar
  88. Nakagawa J, Ehrenberg JP, Nealon J, Fürst T, Aratchige P, Gonzales G, Chanthavisouk C, Hernandez LM, Fengthong T, Utzinger J, Steinmann P (2015) Towards effective prevention and control of helminth neglected tropical diseases in the Western Pacific Region through multi-disease and multi-sectoral interventions. Acta Trop 141:407–418PubMedCrossRefGoogle Scholar
  89. Nakamura-Uchiyama F, Nawa Y (2003) Efficacy of triclabendazole in patients with fascioliasis and paragonimiasis westermani. Clin Parasitol 14:207–209Google Scholar
  90. Nakamura-Uchiyama F, Onah DN, Nawa Y (2001) Clinical features of paragonimiasis cases recently found in Japan: parasite-specific immunoglobulin M and G antibody classes. Clin Infect Dis 32:e151–e153PubMedCrossRefPubMedCentralGoogle Scholar
  91. Nakamura-Uchiyama F, Mukae H, Nawa Y (2002) Paragonimiasis: a Japanese perspective. Clin Chest Med 23:409–420PubMedCrossRefPubMedCentralGoogle Scholar
  92. Nåsell I, Hirsch WM (1973) The transmission dynamics of schistosomiasis. Commun Pur Appl Math 26:395–453CrossRefGoogle Scholar
  93. Nawa Y, Hatz C, Blum J (2005) Sushi delights and parasites: the risk of fishborne and foodborne parasitic zoonoses in Asia. Clin Infect Dis 41:1297–1303PubMedCrossRefPubMedCentralGoogle Scholar
  94. Nguyen TH, Nguyen VD, Murrell D, Dalsgaard A (2007) Occurrence and species distribution of fishborne zoonotic trematodes in wastewater-fed aquaculture in northern Vietnam. Trop Med Int Health 12:66–72PubMedCrossRefPubMedCentralGoogle Scholar
  95. Nguyen TLA, Nguyen TP, Johansen MV, Murrell KD, Phan TV, Dalsgaard A, Luong TT, Thamsborg SM (2009) Prevalence and risks for fishborne zoonotic trematode infections in domestic animals in a highly endemic area of North Vietnam. Acta Trop 112:198–203PubMedCrossRefPubMedCentralGoogle Scholar
  96. Over HJ, Jansen J, van Olm PW (1992) Distribution and impact of helminth diseases of livestock in developing countries. FAO Animal Production and Health Paper 96. FAO, Rome. http://www.fao.org/docrep/004/T0584E/T0584E00.htm#TOC. Accessed 24 Nov 2017
  97. Patel T (2014) New insights into the molecular pathogenesis of intrahepatic cholangiocarcinoma. J Gastroenterol 49:165–172PubMedCrossRefPubMedCentralGoogle Scholar
  98. Pitaksakulrat O, Sithithaworn P, Laoprom N, Laha T, Petney TN, Andrews RH (2013) A cross-sectional study on the potential transmission of the carcinogenic liver fluke Opisthorchis viverrini and other fishborne zoonotic trematodes by aquaculture fish. Foodborne Pathog Dis 10:35–41PubMedCrossRefPubMedCentralGoogle Scholar
  99. Pungpak S, Riganti M, Bunnag D, Harinasuta T (1985) Clinical features in severe opisthorchiasis viverrini. Southeast Asian J Trop Med Public Health 16:405–409PubMedPubMedCentralGoogle Scholar
  100. Pungpak S, Viravan C, Radomyos B, Chalermrut K, Yemput C, Plooksawasdi W, Ho M, Harinasuta T, Bunnag D (1997) Opisthorchis viverrini infection in Thailand: studies on the morbidity of the infection and resolution following praziquantel treatment. Am J Trop Med Hyg 56:311–314PubMedCrossRefPubMedCentralGoogle Scholar
  101. Qian MB, Yap P, Yang YC, Liang H, Jiang ZH, Li W, Tan YG, Zhou H, Utzinger J, Zhou XN, Keiser J (2013) Efficacy and safety of tribendimidine against Clonorchis sinensis. Clin Infect Dis 56:e76–e82PubMedCrossRefPubMedCentralGoogle Scholar
  102. Rim HJ (1986) The current pathobiology and chemotherapy of clonorchiasis. Korean J Parasitol 24:1–141CrossRefGoogle Scholar
  103. Rim HJ (2005) Clonorchiasis: an update. J Helminthol 79:269–281PubMedCrossRefPubMedCentralGoogle Scholar
  104. Rim HJ, Lee YM, Lee JS, Joo KH (1982) Therapeutic field trial with praziquantel (Biltricide) in a rural population infected with Clonorchis sinensis. Kisaengchunghak Chapchi 20:1–8PubMedPubMedCentralGoogle Scholar
  105. Robinson MW, Dalton JP (2009) Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philos Trans R Soc Lond B Biol Sci 364:2763–2776PubMedPubMedCentralCrossRefGoogle Scholar
  106. Ronoharjo P, Wilson AJ, Partoutomo S, Hirst RG (1985) Some aspects of the epidemiology and economics of important disease of large ruminants in Indonesia. Proceedings of the 4th international symposium on veterinary epidemiology and economics, Singapore, 18–22 November 1985Google Scholar
  107. Ross R (1905) The logical basis of the sanitary policy of mosquito reduction. Science 22:689–699PubMedCrossRefGoogle Scholar
  108. Sabarez MT, Ancheta LM, Maniwang DC (1981) Prevalence and economic importance of liver fluke infestation in slaughtered caraboas and cattle in the Philippines. Ann Trop Res 3:223–228Google Scholar
  109. Saijuntha W, Sithithaworn P, Kaitsopit N, Andrews RH, Petney TN (2014) Liver flukes: Clonorchis and Opisthorchis. Adv Exp Med Biol 766:153–199PubMedCrossRefPubMedCentralGoogle Scholar
  110. Saleha AA (1991) Liver fluke disease (fascioliasis): epidemiology, economic impact and public health significance. Southeast Asian J Trop Med Public Health 22:361–364PubMedPubMedCentralGoogle Scholar
  111. Sato M, Sanguankiat S, Pubampen S, Kusolsuk T, Maipanich W, Waikagul J (2009) Egg laying capacity of Haplorchis taichui (Digenea: Heterophyidae) in humans. Korean J Parasitol 47:315–318PubMedPubMedCentralCrossRefGoogle Scholar
  112. Sayasone S, Vonghajack Y, Vanmany M, Rasphone O, Tesana S, Utzinger J, Akkhavong K, Odermatt P (2009) Diversity of human intestinal helminthiasis in Lao PDR. Trans R Soc Trop Med Hyg 103:247–254PubMedCrossRefPubMedCentralGoogle Scholar
  113. Schratz A, Pineda MF, Reforma LG, Fox NM, Le Anh T, Tommaso Cavalli-Sforza L, Henderson MK, Mendoza R, Utzinger J, Ehrenberg JP, Tee AS (2010) Neglected diseases and ethnic minorities in the Western Pacific Region: exploring the links. Adv Parasitol 72:79–107PubMedCrossRefPubMedCentralGoogle Scholar
  114. Sithithaworn P, Haswell-Elkins MR (2003) Epidemiology of Opisthorchis viverrini. Acta Trop 88:187–194PubMedCrossRefPubMedCentralGoogle Scholar
  115. Sithithaworn P, Tesana S, Pipitgool V, Kaewkes S, Pairojkul C, Sripa B, Paupairoj A, Thaiklar K (1991) Relationship between faecal egg count and worm burden of Opisthorchis viverrini in human autopsy cases. Parasitology 102:277–281PubMedCrossRefPubMedCentralGoogle Scholar
  116. Sithithaworn P, Yongvanit P, Tesana S, Pairojkul C (2007) Liver flukes. In: Murrell KD, Fried B (eds) World class parasites. Springer, DordrechtGoogle Scholar
  117. Sithithaworn P, Sripa B, Kaewkes S, Haswell-Elkins MR (2009) Foodborne trematodes. In: Cook GC, Zumla AI (eds) Manson’s tropical diseases. WB Saunders, LondonGoogle Scholar
  118. Sithithaworn P, Yongvanit P, Duenngai K, Kiatsopit N, Pairojkul C (2014) Roles of liver fluke infection as risk factor for cholangiocarcinoma. J Hepatobiliary Pancreat Sci 21:301–308PubMedCrossRefPubMedCentralGoogle Scholar
  119. Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, Mckenzie FE (2012) Ross, MacDonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog 8:e1002588PubMedPubMedCentralCrossRefGoogle Scholar
  120. Smout MJ, Laha T, Mulvenna J, Sripa B, Suttiprapa S, Jones A, Brindley PJ, Loukas A (2009) A granulin-like growth factor secreted by the carcinogenic liver fluke, Opisthorchis viverrini, promotes proliferation of host cells. PLoS Pathog 5:e1000611PubMedPubMedCentralCrossRefGoogle Scholar
  121. Smout MJ, Mulvenna JP, Jones MK, Loukas A (2011) Expression, refolding and purification of Ov-GRN-1, a granulin-like growth factor from the carcinogenic liver fluke, that causes proliferation of mammalian host cells. Prot Expr Purif 79:263–270CrossRefGoogle Scholar
  122. Song KW, Kang SY, Lee SH (1979) A mathematical approach to the mode of transmission of clonorchiasis in the inhabitants of Nak-Dong and Han River basin. Korean J Parasitol 17:114–120CrossRefGoogle Scholar
  123. Soukhathammavong P, Odermatt P, Sayasone S, Vonghachack Y, Vounatsou P, Hatz C, Akkhavong K, Keiser J (2011) Efficacy and safety of mefloquine, artesunate, mefloquine-artesunate, tribendimidine, and praziquantel in patients with Opisthorchis viverrini: a randomised, exploratory, open-label, phase 2 trial. Lancet Infect Dis 11:110–118PubMedCrossRefGoogle Scholar
  124. Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, Pairojkul C, Bhudhisawasdi V, Tesana S, Thinkamrop B, Bethony JM, Loukas A, Brindley PJ (2007) Liver fluke induces cholangiocarcinoma. PLoS Med 4:e201PubMedPubMedCentralCrossRefGoogle Scholar
  125. Sripa B, Bethony JM, Sithithaworn P, Kaewkes S, Mairiang E, Loukas A, Mulvenna J, Laha T, Hotez PJ, Brindley PJ (2011) Opisthorchiasis and Opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Trop 120:S158–S168PubMedCrossRefGoogle Scholar
  126. Sripa B, Brindley PJ, Mulvenna J, Laha T, Smout MJ, Mairiang E, Bethony JM, Loukas A (2012) The tumorigenic liver fluke Opisthorchis viverrini—multiple pathways to cancer. Trends Parasitol 28:395–407PubMedPubMedCentralCrossRefGoogle Scholar
  127. Sripa B, Tangkawattana S, Laha T, Kaewkes S, Mallory FF, Smith JF, Wilcox BA (2015) Toward integrated opisthorchiasis control in northeast Thailand: the Lawa project. Acta Trop 141:361–367PubMedCrossRefGoogle Scholar
  128. Tesana S, Srisawangwonk T, Kaewkes S, Sithithaworn P, Kanla P, Arunyanart C (1991) Eggshell morphology of the small eggs of human trematodes in Thailand. Southeast Asian J Trop Med Public Health 22:631–636PubMedGoogle Scholar
  129. Torgerson PR, Claxton J (1999) Epidemiology and control. In: Dalton JP (ed) Fasciolosis. CAB International, WallingfordGoogle Scholar
  130. Torgerson PR, Devleesschauwer B, Praet N, Speybroeck N, Willingham AL, Kasuga F, Rokni MB, Zhou XN, Fèvre EM, Sripa B, Gargouri N, Fürst T, Budke BM, Carabin H, Kirk MD, Angulo FJ, Havelaar A, de Silva N (2015) World Health Organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: a data synthesis. PLoS Med 12:e1001920PubMedPubMedCentralCrossRefGoogle Scholar
  131. Upatham ES, Viyanant V (2003) Opisthorchis viverrini and opisthorchiasis: a historical review and future perspective. Acta Trop 88:171–176PubMedCrossRefPubMedCentralGoogle Scholar
  132. Upatham ES, Viyanant V, Brockelman WY, Kurathong S, Lee P, Kraengraeng R (1988) Rate of reinfection by Opisthorchis viverrini in an endemic northeast Thai community after chemotherapy. Int J Parasitol 18:643–649PubMedCrossRefPubMedCentralGoogle Scholar
  133. Uttaravichien T, Bhudhisawasdi V, Pairojkul C, Pugkhem A (1999) Intrahepatic cholangiocarcinoma in Thailand. J Hepatobiliary Pancreat Surg 6:128–135PubMedCrossRefPubMedCentralGoogle Scholar
  134. Valero MA, de Renzi M, Panova M, Garcia-Bodelon MA, Periago MV, Ordonez D, Mas-Coma S (2006) Crowding effect on adult growth, prepatent period and egg shedding of Fasciola hepatica. Parasitology 133:453–463PubMedCrossRefPubMedCentralGoogle Scholar
  135. Vonghachack Y, Odermatt P, Taisayyavong K, Phounsavath S, Akkhavong K, Sayasone S (2017) Transmission of Opisthorchis viverrini, Schistosoma mekongi and soil-transmitted helminths on the Mekong Islands, Southern Lao PDR. Infect Dis Poverty 6:131PubMedPubMedCentralCrossRefGoogle Scholar
  136. WHO (1995) Control of foodborne trematode infections. WHO Tech Rep Ser 849:1–157Google Scholar
  137. WHO (2006) Wastewater and excreta use in aquaculture. WHO, GenevaGoogle Scholar
  138. WHO & FAO (2004) Report of the joint WHO/FAO workshop on foodborne trematode infections in Asia. WHO, ManilaGoogle Scholar
  139. Williams GM, Sleigh AC, Li Y, Feng Z, Davis GM, Chen H, Ross AGP, Bergquist R, McManus DP (2002) Mathematical modelling of schistosomiasis japonica: comparison of control strategies in the People’s Republic of China. Acta Trop 82:253–262PubMedCrossRefPubMedCentralGoogle Scholar
  140. Woolhouse MEJ (1991) On the application of mathematical models of schistosome transmission dynamics. I. Natural transmission. Acta Trop 49:241–270PubMedCrossRefPubMedCentralGoogle Scholar
  141. Woolhouse MEJ (1992) On the application of mathematical models of schistosome transmission dynamics. II. Control. Acta Trop 50:189–204PubMedCrossRefPubMedCentralGoogle Scholar
  142. Woolhouse MEJ, Watts CH, Chandiwana SK (1991) Heterogeneities in transmission rates and the epidemiology of schistosome infection. Proc Biol Sci 245:109–114PubMedCrossRefPubMedCentralGoogle Scholar
  143. Woolhouse MEJ, Hasibeder G, Chandiwana SK (1996) On estimating the basic reproduction number for Schistosoma haematobium. Trop Med Int Health 1:456–463PubMedCrossRefPubMedCentralGoogle Scholar
  144. Woolhouse MEJ, Etard JF, Dietz K, Ndhlovu PD, Chandiwana SK (1998) Heterogeneities in schistosome transmission dynamics and control. Parasitol Int 117:475–482CrossRefGoogle Scholar
  145. Yi D, Qiang D, Wenjie C (2014) Neuroimaging findings in a woman with brainstem paragonimiasis: a case report and review of the literature. J Med Case Rep 8:36PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yongvanit P, Pinlaor S, Bartsch H (2012) Oxidative and nitrative DNA damage: key events in opisthorchiasis-induced carcinogenesis. Parasitol Int 61:130–135PubMedCrossRefPubMedCentralGoogle Scholar
  147. Yoshida Y (2005) Clonorchis sinensis and clonorchiasis in Japan. In: Arizono N, Chai JY, Nawa Y, Takahasi Y (eds) Asian parasitology, volume 1: Foodborne helminthiasis in Asia. Federation of Asian Parasitologists, ChibaGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Thomas Fürst
    • 1
    • 2
    • 3
    • 4
    Email author
  • Puangrat Yongvanit
    • 5
    • 6
    • 7
  • Narong Khuntikeo
    • 5
    • 6
    • 8
  • Zhao-Rong Lun
    • 9
  • Juanita A. Haagsma
    • 10
  • Paul R. Torgerson
    • 11
  • Peter Odermatt
    • 3
    • 4
  • Christine Bürli
    • 3
    • 4
  • Nakul Chitnis
    • 3
    • 4
  • Paiboon Sithithaworn
    • 5
    • 6
    • 12
  1. 1.Centre for Health PolicyImperial College LondonLondonUK
  2. 2.Department of Infectious Disease EpidemiologyImperial College LondonLondonUK
  3. 3.Swiss Tropical and Public Health InstituteBaselSwitzerland
  4. 4.University of BaselBaselSwitzerland
  5. 5.Cholangiocarcinoma Research InstituteKhon Kaen UniversityKhon KaenThailand
  6. 6.Cholangiocarcinoma Screening and Care ProgramKhon Kaen UniversityKhon KaenThailand
  7. 7.Department of BiochemistryKhon Kaen UniversityKhon KaenThailand
  8. 8.Department of SurgeryKhon Kaen UniversityKhon KaenThailand
  9. 9.Center for Parasitic Organisms, State Key Laboratory of BiocontrolSchool of Life Sciences, Sun Yat-Sen UniversityGuangzhouPeople’s Republic of China
  10. 10.Department of Public HealthErasmus University Medical CenterRotterdamThe Netherlands
  11. 11.Section of Veterinary EpidemiologyUniversity of ZürichZürichSwitzerland
  12. 12.Department of ParasitologyKhon Kaen UniversityKhon KaenThailand

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