Diagnosis of Human Trematode Infections

  • J. Guillermo EstebanEmail author
  • Carla Muñoz-Antoli
  • Rafael Toledo
  • Lawrence R. Ash
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1154)


Digenetic trematodes form a major group of human parasites, affecting a large number of humans, especially in endemic foci. Over 100 species have been reported infecting humans, including blood, lung, liver, and intestinal parasites. Traditionally, trematode infections have been diagnosed by parasitological methods based on the detection and the identification of eggs in different clinical samples. However, this is complicated due to the morphological similarity between eggs of different trematode species and other factors such as lack of sensitivity or ectopic locations of the parasites. Moreover, the problem is currently aggravated by migratory flows, international travel, international trade of foods, and changes in alimentary habits. Although efforts have been made for the development of immunological and molecular techniques, the detection of eggs through parasitological techniques remains as the gold standard for the diagnosis of trematodiases. In this chapter, we review the current status of knowledge on diagnostic techniques used when examining feces, urine, and sputum and also analyze the most relevant characteristics used to identify eggs with a quick key for the identification of eggs.


Digenea Trematode Fluke Liver-, lung-, intestinal-, blood-trematodes Diagnosis Parasitological techniques Eggs 



This work was supported by the projects PROMETEO/2009/081 and PROMETEO2014-083 Fase II of Conselleria d’Educació, Generalitat Valenciana (Valencia, Spain); by project SN07.A126 of Cooperación al Desarrollo de la Universitat de València (Valencia, Spain); by projects BFU2013-41040 and BFU2016-75639-P of Ministerio de Economía y Competitividad (Madrid, Spain); and by projects No. RD12/0018/0013 (IV National Program of I+D+I 2008-2011) and RD16/0027/0023 (IV National Program of I+D+I 2017-2021) of the Red de Investigación Cooperativa en Enfermedades Tropicales-RICET, ISCIII-Subdirección General de Redes y Centros de Investigación Cooperativa of Ministerio de Sanidad y Consumo (Madrid, Spain).


  1. Aguayo V, Valdes B, Espino AM (2018) Assessment of Fasciola hepatica glutathione S-transferase as an antigen for serodiagnosis of human chronic fascioliasis. Acta Trop 186:41–49PubMedCrossRefPubMedCentralGoogle Scholar
  2. Ahn CS, Na BK, Chung DL, Kim JG, Kim JT, Kong Y (2015) Expression characteristics and specific antibody reactivity of diverse cathepsin F members of Paragonimus westermani. Parasitol Int 64:37–42PubMedCrossRefPubMedCentralGoogle Scholar
  3. Ai L, Chen MX, Alasaad S, Elsheikha HM, Li J, Li HL, Lin RQ, Zou FC, Zhu XQ, Chen JX (2011) Genetic characterization, species differentiation and detection of Fasciola spp. by molecular approaches. Parasit Vectors 4:101PubMedCrossRefPubMedCentralGoogle Scholar
  4. Alasaad S, Soriguer RC, Abu-Madi M, El Behairy A, Baños PD, Píriz A, Fickel J, Zhu XQ (2011) A fluorescence-based polymerase chain reaction-linked single-strand conformation polymorphism (F-PCR-SSCP) assay for the identification of Fasciola spp. Parasitol Res 108:1513–1517PubMedCrossRefPubMedCentralGoogle Scholar
  5. Ali NM (2012) Development and evaluation of a dipstick assay in diagnosis of human fasciolosis. Parasitol Res 110:1649–1654PubMedCrossRefPubMedCentralGoogle Scholar
  6. Allam G, Bauomy IR, Hemyeda ZM, Sakran TF (2012) Evaluation of a 14.5 kDa-Fasciola gigantica fatty acid binding protein as a diagnostic antigen for human fascioliasis. Parasitol Res 110:1863–1871PubMedCrossRefPubMedCentralGoogle Scholar
  7. Allen AVH, Ridley DS (1970) Further observations on the formol-ether concentration technique for faecal parasites. J Clin Pathol 23:545–546PubMedCrossRefPubMedCentralGoogle Scholar
  8. Alva A, Cangalaya C, Quiliano M, Krebs C, Gilman RH, Sheen P, Zimic M (2017) Mathematical algorithm for the automatic recognition of intestinal parasites. PLoS One 12(4):e0175646PubMedCrossRefPubMedCentralGoogle Scholar
  9. Arimatsu Y, Kaewkes S, Laha T, Hong SJ, Sripa B (2012) Rapid detection of Opisthorchis viverrini copro-DNA using loop-mediated isothermal amplification. Parasitol Int 61:178–182PubMedCrossRefPubMedCentralGoogle Scholar
  10. Arimatsu Y, Kaewkes S, Laha T, Sripa B (2015) Specific diagnosis of Opisthorchis viverrini using loop-mediated isothermal amplification (LAMP) targeting parasite microsatellites. Acta Trop 141(Pt B):368–371PubMedCrossRefPubMedCentralGoogle Scholar
  11. Armignacco O, Caterini L, Marucci G, Ferri F, Bernardini G, Natalini Raponi G, Ludovisi A, Bossù T, Gomez Morales MA, Pozio E (2008) Human illnesses caused by Opisthorchis felineus flukes, Italy. Emerg Infect Dis 14:1902–1905PubMedCrossRefPubMedCentralGoogle Scholar
  12. Armignacco O, Ferri F, Gomez-Morales MA, Caterini L, Pozio E (2013) Cryptic and asymptomatic Opisthorchis felineus infections. Am J Trop Med Hyg 88:364–366PubMedCrossRefPubMedCentralGoogle Scholar
  13. Aryeetey YA, Essien-Baidoo S, Larbi IA, Ahmed K, Amoah AS, Obeng BB, van Lieshout L, Yazdanbakhsh M, Boakye DA, Verweij JJ (2013) Molecular diagnosis of Schistosoma infections in urine samples of school children in Ghana. Am J Trop Med Hyg 88:1028–1031PubMedCrossRefPubMedCentralGoogle Scholar
  14. Ash LR, Orihel TC (1991) Parasites: a guide to laboratory procedures and identification. ASCP Press, American Society of Clinical Pathologists, ChicagoGoogle Scholar
  15. Ash LR, Orihel TC (2007) Atlas of human parasitology, 5th edn. American Society for Clinical Pathology Press, ChicagoGoogle Scholar
  16. Ash LR, Orihel TC, Savioli L (1994) Bench Aids for the diagnosis of intestinal parasites. World Health Organization, GenevaGoogle Scholar
  17. Ashrafi K, Bargues MD, O’Neill S, Mas-Coma S (2014) Fascioliasis: a worldwide parasitic disease of importance in travel medicine. Travel Med Infect Dis 12(6 Pt A):636–649PubMedCrossRefPubMedCentralGoogle Scholar
  18. Ashton RA, Stewart BT, Petty N, Lado M, Finn T, Brooker S, Kolaczinski JH (2011) Accuracy of circulating cathodic antigen tests for rapid mapping of Schistosoma mansoni and S. haematobium infections in Southern Sudan. Tropical Med Int Health 16:1099–1103CrossRefGoogle Scholar
  19. Atalabi TE, Adubi TO, Lawal U (2017) Rapid mapping of urinary schistosomiasis: an appraisal of the diagnostic efficacy of some questionnaire-based indices among high school students in Katsina State, northwestern Nigeria. PLoS Negl Trop Dis 11(4):e0005518PubMedCrossRefPubMedCentralGoogle Scholar
  20. Barda BD, Rinaldi L, Ianniello D, Zepherine H, Salvo F, Sadutshang T, Cringoli G, Clementi M, Albonico M (2013) Mini-FLOTAC, an innovative dirtect diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Negl Trop Dis 7:e2344PubMedCrossRefPubMedCentralGoogle Scholar
  21. Bassiouny HK, Hasab AA, El-Nimr NA, Al-Shibani LA, Al-Waleedi AA (2014) Rapid diagnosis of schistosomiasis in Yemen using a simple questionnaire and urine reagent strips. East Mediterr Health J 20:242–249PubMedCrossRefPubMedCentralGoogle Scholar
  22. Bergquist R, Johansen MV, Utzinger J (2009) Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 4:151–156CrossRefGoogle Scholar
  23. Bezerra FSM, Leal JKF, Sousa MS, Pinheiro MCC, Ramos AN Jr, Silva-Moraes V, Katz N (2018) Evaluating a point-of-care circulating cathodic antigen test (POC-CCA) to detect Schistosoma mansoni infections in a low endemic area in north-eastern Brazil. Acta Trop 182:264–270PubMedCrossRefPubMedCentralGoogle Scholar
  24. Bierman WFW, Wetsteyn JCFM, van Gool TV (2005) Presentation and diagnosis of imported schistosomiasis: relevance of eosinophilia, microscopy for ova, and serology. J Travel Med 12:9–13PubMedCrossRefPubMedCentralGoogle Scholar
  25. Blagg W, Schloegel EL, Mansour NS, Khalaf GI (1955) A new concentration technic for the demonstration of protozoa and helminth eggs in feces. Am J Trop Med Hyg 4:23–28PubMedCrossRefPubMedCentralGoogle Scholar
  26. Blair D, Xu ZB, Agatsuma T (1999) Paragonimus and paragonimiasis. Adv Parasitol 3:99–158Google Scholar
  27. 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 117–150CrossRefGoogle Scholar
  28. Bottieau E, Clerinx J, De Vega MR, Van den Enden E, Colebunders R, Van Esbroeck M, Vervoort T, Van Gompel A, Van den Ende J (2006) Imported Katayama fever: clinical and biological features at presentation and during treatment. J Infect 52:339–345PubMedCrossRefPubMedCentralGoogle Scholar
  29. Buathong S, Leelayoova S, Mungthin M, Ruang-Areerate T, Naaglor T, Suwannahitatorn P, Piyaraj P, Taamasri P, Tan-Ariya P (2017) Molecular discrimination of Opisthorchis-like eggs from residents in a rural community of central Thailand. PLoS Negl Trop Dis 11(11):e0006030PubMedCrossRefPubMedCentralGoogle Scholar
  30. Cabada MM, Malaga JL, Castellanos-Gonzalez A, Bagwell KA, Naeger PA, Rogers HK, Maharsi S, Mbaka M, White AC Jr (2017) Recombinase polymerase amplification compared to real-time polymerase chain reaction test for the detection of Fasciola hepatica in human stool. Am J Trop Med Hyg 96:341–346PubMedCrossRefPubMedCentralGoogle Scholar
  31. Cabaret J, Bayssade-Dufour C, Tami G, Albaret JL (1999) Identification of African Paragonimidae by multivariate analysis of the eggs. Acta Trop 72:79–89PubMedCrossRefPubMedCentralGoogle Scholar
  32. Cabeza-Barrera I, Cabezas-Fernández T, Salas Coronas J, Vázquez Villegas J, Cobo F (2011) Dicrocoelium dendriticum: an emerging spurious infection in a geographic area with a high level of immigration. Ann Trop Med Parasitol 105:403–406PubMedCrossRefPubMedCentralGoogle Scholar
  33. Cabrera BD (1984) Paragonimiasis in the Philippines: current status. Arzneimittelforschung 34:1188–1192PubMedPubMedCentralGoogle Scholar
  34. Cai XQ, Xu MJ, Wang YH, Qiu DY, Liu GX, Lin A, Tang JD, Zhang RL, Zhu XQ (2010) Sensitive and rapid detection of Clonorchis sinensis infection in fish by loop-mediated isothermal amplification (LAMP). Parasitol Res 106:1379–1383PubMedCrossRefPubMedCentralGoogle Scholar
  35. 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 61:183–186PubMedCrossRefPubMedCentralGoogle Scholar
  36. Calvani NED, Windsor PA, Bush RD, Slapeta J (2017) Scrambled eggs: a highly sensitive molecular diagnostic workflow for Fasciola species specific detection from faecal samples. PLoS Negl Trop Dis 11(9):e0005931PubMedCrossRefPubMedCentralGoogle Scholar
  37. Casacuberta M, Kinunghi S, Vennervald BJ, Olsen A (2016) Evaluation and optimization of the Circulating Cathodic Antigen (POC-CCA) cassette test for detecting Schistosoma mansoni infection by using image analysis in school children in Mwanza Region, Tanzania. Parasit Epidemiol Control 1:105–115CrossRefGoogle Scholar
  38. Castilla EA, Jessen R, Sheck DN, Procop GW (2003) Cavitary mass lesion and recurrent pneumothoraces due to Paragonimus kellicotti infection—North American paragonimiasis. Am J Surg Pathol 27:1157–1160PubMedCrossRefPubMedCentralGoogle Scholar
  39. Cavalcanti MG, Silva LF, Peralta RHS, Barreto MG, Peralta JM (2013) Schistosomiasis in áreas of low endemicity: a new era in diagnosis. Trends Parasitol 29:75–82PubMedCrossRefPubMedCentralGoogle Scholar
  40. 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 53–115CrossRefGoogle Scholar
  41. 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 147–183Google Scholar
  42. Chai JY (2013) Paragonimiasis. Handb Clin Neurol 114:283–296PubMedCrossRefPubMedCentralGoogle Scholar
  43. Chai JY, Lee SH (2002) Food-borne intestinal trematode infections in the Republic of Korea. Parasitol Int 51:129–154PubMedCrossRefPubMedCentralGoogle Scholar
  44. Chai JY, Yu JR, Lee SH, Jung HC, Song IS, Cho SY (1989) An egg-negative patient of acute metagonimiasis diagnosed serologically by ELISA. Seoul J Med 30:138–142Google Scholar
  45. Chai JY, Darwin Murrell K, Lymbery AJ (2005) Fish-borne parasitic zoonoses: status and issues. Int J Parasitol 35:1233–1254PubMedCrossRefPubMedCentralGoogle Scholar
  46. Chai JY, Han ET, Guk SM, Shin EH, Sohn WM, Yong TS, Eom KS, Lee KH, Jeong HG, Ryang YS, Hoang EH, Phommasack B, Insisiengmay B, Lee SH, Rim HJ (2007) High prevalence of liver and intestinal fluke infections among residents of Savannakhet Province in Laos. Korean J Parasitol 45:213–218PubMedCrossRefPubMedCentralGoogle Scholar
  47. Chai JY, Han ET, Shin EH, Sohn WM, Yong TS, Eom KS, Min DY, Um JY, Park MS, Hoang EH, Phommasack B, Insisiengmay B, Lee SH, Rim HJ (2009a) High prevalence of Haplorchis taichui, Phaneropsolus molenkampi, and other helminth infections among people in Khammouane province, Lao PDR. Korean J Parasitol 47:243–247PubMedCrossRefPubMedCentralGoogle Scholar
  48. Chai JY, Shin EH, Lee SH, Rim HJ (2009b) Foodborne intestinal flukes in Southeast Asia. Korean J Parasitol 47:S69–S102PubMedCrossRefPubMedCentralGoogle Scholar
  49. Chai JY, Yong TS, Eom KS, Min DY, Shin EH, Banouvong V, Insisiengmay B, Insisiengmay S, Phommasack B, Rim HJ (2010) Prevalence of the intestinal flukes Haplorchis taichui and H. yokogawai in a mountainous area of Phongsaly Province, Lao PDR. Korean J Parasitol 48:339–342PubMedCrossRefPubMedCentralGoogle Scholar
  50. Chai JY, Jung BK, Kim DG, Kim JL, Lim H, Shin EH, Lee KH, Kim MR, Han SJ, Yeom JH, Park SM, Hwang JS (2015) Heterophyid trematodes recovered from people residing along the Boseong River, South Korea. Acta Trop 148:142–146PubMedCrossRefPubMedCentralGoogle Scholar
  51. Chang ZS, Wu B, Blair D, Zhang YN, Hu L, Chen SH, Chen MG, Feng Z, Davis GM (2000) Gene sequencing for identification of Paragonimus eggs from a human case. Chin J Parasitol Parasit Dis 18:213–215Google Scholar
  52. Cheever AW, Neafie C (2000) Schistosomiasis. In: Meyers WM, Neafie RC, Marty AM, Wear DJ (eds) Pathology of infectious diseases, vol I. Helmintiases. Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DC, pp 23–48Google Scholar
  53. Chen M, Lu Y, Hua X, Mott KE (1994) Progress in assessment of morbidity due to Clonorchis sinensis infection: a review of recent literature. Trop Dis Bull 91:R7–R65Google Scholar
  54. 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 108:1193–1198PubMedCrossRefPubMedCentralGoogle Scholar
  55. Cheng MG (1989) Schistosomiasis control program in the People’s Republic of China: a review. Southeast Asian J Trop Med Public Health 20:511–517Google Scholar
  56. Chernet A, Neumayr A, Hatz C, Kling K, Sydow V, Rentsch K, Utzinger J, Probst-Hensch N, Marti H, Nickel B, Labhardt ND (2018) Spectrum of infectious diseases among newly arrived Eritrean refugees in Switzerland: a cross-sectional study. Int J Public Health 63:233–239PubMedCrossRefPubMedCentralGoogle Scholar
  57. Choi D, Hong ST (2007) Imaging diagnosis of clonorchiasis. Korean J Parasitol 45:77–85PubMedCrossRefPubMedCentralGoogle Scholar
  58. Choi D, Hong ST, Lim JH, Cho SY, Rim HJ, Ji Z, Yuan R, Wang S (2004a) Sonographic findings of active Clonorchis sinensis infection. J Clin Ultrasound 32:17–23PubMedCrossRefPubMedCentralGoogle Scholar
  59. Choi BI, Han JK, Hong ST, Lee KH (2004b) Clonorchiasis and cholangiocarcinoma: etiologic relationship and imaging diagnosis. Clin Microbiol Rev 17:540–552PubMedCrossRefPubMedCentralGoogle Scholar
  60. Cnops L, Tannich E, Polman K, Clerinx J, Van Esbroeck M (2012) Schistosoma real-time PCR as diagnostic tool for international travellers and migrants. Trop Med Int Health 17:1208–1216PubMedCrossRefPubMedCentralGoogle Scholar
  61. Cnops L, Soentjens P, Clerinx J, Van Esbroeck M (2013) A Schistosoma haematobium-specific real-time PCR for diagnosis of urogenital schistosomiasis in serum samples of international travelers and migrants. PLoS Negl Trop Dis 7(8):e2413PubMedCrossRefPubMedCentralGoogle Scholar
  62. Coelho PMZ, Jurberg AD, Oliveira AA, Katz N (2009) Use of a saline gradient for the diagnosis of schistosomiasis. Mem Inst Oswaldo Cruz 104:720–723PubMedCrossRefPubMedCentralGoogle Scholar
  63. Colley DG, Binder S, Campbell C, King CH, Tchuem Tchuenté LA, N’Goran EK, Erko B, Karanja DM, Kabatereine NB, van Lieshout L, Rathbun S (2013) A five-country evaluation of a point-of-care circulating cathodic antigen urine assay for the prevalence of Schistosoma mansoni. Am J Trop Med Hyg 88:426–432PubMedCrossRefPubMedCentralGoogle Scholar
  64. Corstjens PL, van Lieshout L, Zuiderwijk M, Kornelis D, Tanke HJ, Deelder AM, van Dam GJ (2008) Up-converting phosphor technology-based lateral flow assay for detection of Schistosoma circulating anodic antigen in serum. J Clin Microbiol 46:171–176PubMedCrossRefPubMedCentralGoogle Scholar
  65. Coulibaly JT, N’Gbesso YK, Knopp S, N’Guessan NA, Silué KD, van Dam GJ, N’Goran EK, Utzinger J (2013a) Accuracy of urine circulating cathodic antigen test for the diagnosis of Schistosoma mansoni in preschool-aged children before and after treatment. PLoS Negl Trop Dis 7:e2109PubMedCrossRefPubMedCentralGoogle Scholar
  66. Coulibaly JT, N’Goran EK, Utzinger J, Doenhoff MJ, Dawson EM (2013b) A new rapid diagnostic test for detection of anti-Schistosoma mansoni and anti-Schistosoma haematobium antibodies. Parasit Vectors 6:29PubMedCrossRefPubMedCentralGoogle Scholar
  67. Cringoli G (2006) FLOTAC, a novel apparatus for a multivalent faecal egg count technique. Parassitologia 48:381–384PubMedPubMedCentralGoogle Scholar
  68. Cringoli G, Rinaldi L, Maurelli MP, Utzinger J (2010) FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of intestinal parasites in animals and humans. Nat Protoc 5:503–515PubMedCrossRefPubMedCentralGoogle Scholar
  69. Devi KR, Narain K, Bhattacharya S, Negmu K, Agatsuma T, Blair D, Wickramashinghe S, Mahanta J (2007) Pleuropulmonary paragonimiasis due to Paragonimus heterotremus: molecular diagnosis, prevalence of infection and clinicoradiological features in an endemic area of northeastern India. Trans R Soc Trop Med Hyg 101:786–792PubMedCrossRefPubMedCentralGoogle Scholar
  70. 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 22:174–178PubMedPubMedCentralGoogle Scholar
  71. Ditrich O, Giboda M, Scholz T, Beer SA (1992) Comparative morphology of eggs of the Haplorchiinae (Trematoda: Heterophyidae) and some other medically important heterophyid and opisthorchiid flukes. Folia Parasitol 39:123–132PubMedPubMedCentralGoogle Scholar
  72. Doanh PN, Nawa Y (2016) Clonorchis sinensis and Opisthorchis spp. in Vietnam: current status and prospects. Trans R Soc Trop Med Hyg 110:13–20PubMedCrossRefPubMedCentralGoogle Scholar
  73. Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y, Le NT (2007) Description of a new lung fluke species, Paragonimus vietnamensis sp. nov. (Trematoda, Paragonimidae), found in northern Vietnam. Parasitol Res 101:1495–1501PubMedCrossRefPubMedCentralGoogle Scholar
  74. Doanh PN, Shinohara A, Horii Y, Habe S, Nawa Y (2008) Discovery of Paragonimus westermani in Vietnam and its molecular phylogenetic status in P. westermani complex. Parasitol Res 104:1149–1155PubMedCrossRefPubMedCentralGoogle Scholar
  75. 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 60:534–537PubMedCrossRefPubMedCentralGoogle Scholar
  76. Duenngai K, Sithithaworn P, Rudrappa UK, Iddya K, Laha T, Stensvold CR, Strandgaard H, Johansen MV (2008) Improvement of PCR for detection of Opisthorchis viverrini DNA in human stool samples. J Clin Microbiol 46:366–368PubMedCrossRefPubMedCentralGoogle Scholar
  77. Duenngai K, Boonmars T, Sithithaworn J, Sithithaworn P (2013) Diagnosis of early infection and post chemotherapeutic treatment by copro-DNA detection in experimental opisthorchiasis. Parasitol Res 112:271–278PubMedCrossRefPubMedCentralGoogle Scholar
  78. Dusak A, Onur MR, Cicek M, Firat U, Ren T, Dogra VS (2012) Radiological imaging features of Fasciola hepatica infection—a pictorial review. J Clin Imaging Sci 2:2PubMedCrossRefPubMedCentralGoogle Scholar
  79. Duthaler U, Rinaldi L, Maurelli MP, Vargas M, Utzinger J, Cringoli G, Keiser J (2010) Fasciola hepatica: comparison of the sedimentation and FLOTAC techniques for the detection and quantification of faecal egg counts in rats. Exp Parasitol 126:161–166PubMedCrossRefPubMedCentralGoogle Scholar
  80. Eberl M, Al-Sherbiny M, Hagan P, Ljubojevic S, Thomas AW, Wilson RA (2002) A novel and sensitive method to monitor helminth infections by faecal sampling. Acta Trop 83:183–187PubMedCrossRefPubMedCentralGoogle Scholar
  81. Ellis MK, Li Y, Hou X, Chen H, McManus DP (2008) sTNFR-II and sICAM-1 are associated with acute disease and hepatic imflammation in schistosomiasis japonica. Int J Parasitol 38:717–723PubMedCrossRefPubMedCentralGoogle Scholar
  82. Ephraim RK, Duah E, Cybulski JS, Prakash M, D’Ambrosio MV, Fletcher DA, Keiser J, Andrews JR, Bogoch II (2015) Diagnosis of Schistosoma haematobium infection with a mobile phone-mounted Foldscope and a reversed-lens CellScope in Ghana. Am J Trop Med Hyg 92:1253–1256PubMedCrossRefPubMedCentralGoogle Scholar
  83. 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 1–34Google Scholar
  84. Esteban JG, Bargues MD, Mas-Coma S (2008) Geographical distribution, diagnosis and treatment of human fascioliasis: a review. Res Rev Parasitol 58:13–42Google Scholar
  85. Figueroa-Santiago O, Delgado B, Espino AM (2011) Fasciola hepatica saposin-like protein-2-based ELISA for the serodiagnosis of chronic human fascioliasis. Diagn Microbiol Infect Dis 70:355–361PubMedCrossRefPubMedCentralGoogle Scholar
  86. Fischer PU, Curtis KC, Marcos LA, Weil GJ (2011) Molecular characterization of the North American lung fluke Paragonimus kellicotti in Missouri and its development in Mongolian gerbils. Am J Trop Med Hyg 84:1005–1011PubMedCrossRefPubMedCentralGoogle Scholar
  87. Fischer PU, Curtis KC, Folk SM, Wilkins PP, Marcos LA, Weil GJ (2013) Serological diagnosis of North American paragonimiasis by Western blot using Paragonimus kellicotti adult worm antigen. Am J Trop Med Hyg 88:1035–1040PubMedCrossRefPubMedCentralGoogle Scholar
  88. Fried B, Haseeb MA (1991) Plathyhelminthes: Aspidogastrea, Monogenea, and Digenea. In: Harrison FW, Bogitish BJ (eds) Microscopic anatomy of invertebrates, vol III. Plathyhelminthes and Nemertinea. Wiley-Liss Inc., New York, pp 141–209Google Scholar
  89. Fried B, Graczyk TK, Tamang L (2004) Food-borne intestinal trematodiases in humans. Parasitol Res 93:159–170PubMedCrossRefPubMedCentralGoogle Scholar
  90. Fritzsche C, Stachs O, Holtfreter MC, Nohr-Łuczak C, Guthoff RF, Reisinger EC (2012) Confocal laser scanning microscopy, a new in vivo diagnostic tool for schistosomiasis. PLoS One 7(4):e34869PubMedCrossRefPubMedCentralGoogle Scholar
  91. Fürst T, Keiser J, Utzinger J (2012a) Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect Dis 12:210–221PubMedCrossRefPubMedCentralGoogle Scholar
  92. Fürst T, Sayasone S, Odermatt P, Keiser J, Utzinger J (2012b) Manifestation, diagnosis, and management of foodborne trematodiasis. BMJ 344:e4093PubMedCrossRefPubMedCentralGoogle Scholar
  93. Gan X, Shi X, Wang Y, Wang P, Shen H, Zhu M, Tang Y, Zhang S (2005) Development of rapid diagnostic kit (Dot Immunogold Filtration Assay) for detection of antibodies against Paragonimus westermani. Chin J Zoonoses 21:988–990Google Scholar
  94. Glinz D, Silué KD, Knopp S, Lohourignon LK, Yao KP, Steinmann P, Rinaldi L, Cringoli G, N’Goran EK, Utzinger J (2010) Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS Negl Trop Dis 4:e754PubMedCrossRefPubMedCentralGoogle Scholar
  95. Gomes LI, Dos Santos Marques LH, Enk MJ, de Oliveira MC, Coelho PM, Rabello A (2010) Development and evaluation of a sensitive PCR-ELISA system for detection of Schistosoma infection in feces. PLoS Negl Trop Dis 4(4):e664PubMedCrossRefPubMedCentralGoogle Scholar
  96. Gomez-Morales MA, Ludovisi A, Amati M, Pozio E (2013) Validation of an excretory/secretory antigen based-Elisa for the diagnosis of Opisthorchis felineus infection in humans from low trematode endemic areas. PLoS One 8(5):e62267PubMedCrossRefPubMedCentralGoogle Scholar
  97. Gong Z, Miao R, Shu M, Zhu Y, Wen Y, Guo Q, Liao Q, Wan C (2017) Paragonimiasis in Children in Southwest China: a retrospective case reports review from 2005 to 2016. Medicine (Baltimore) 96(25):e7265CrossRefGoogle Scholar
  98. 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(9):e2414PubMedCrossRefPubMedCentralGoogle Scholar
  99. Gottstein B, Schneeberger M, Boubaker G, Merkle B, Huber C, Spiliotis M, Müller N, Garate T, Doherr MG (2014) Comparative assessment of ELISAs using recombinant saposin-like protein 2 and recombinant cathepsin L-1 from Fasciola hepatica for the serodiagnosis of human fasciolosis. PLoS Negl Trop Dis 8(6):e2860PubMedCrossRefPubMedCentralGoogle Scholar
  100. Graczyk TK, Fried B (2007) Human waterborne trematode and protozoa infections. Adv Parasitol 64:111–160PubMedCrossRefPubMedCentralGoogle Scholar
  101. Graczyk TK, Gilman RH, Fried B (2001) Fasciolopsiasis: is it a controllable food-borne disease? Parasitol Res 87:80–83PubMedCrossRefPubMedCentralGoogle Scholar
  102. Gray DJ, Ross AG, Li YS, McManus DP (2011) Diagnosis and management of schistosomiasis. BMJ 342:d2651PubMedCrossRefPubMedCentralGoogle Scholar
  103. Grenfell R, Harn DA, Tundu S, Da’dara A, Siqueira L, Coelho PM (2013) New approaches with different types of circulating cathodic antigen for the diagnosis of patients with low Schistosoma mansoni load. PLoS Negl Trop Dis 7(2):e2054PubMedCrossRefPubMedCentralGoogle Scholar
  104. Gryseels B, Polman K, Clerinx J (2006) Human schistosomiasis. Lancet 368:1106–1118PubMedCrossRefPubMedCentralGoogle Scholar
  105. Gualdieri L, Rinaldi L, Petrullo L, Morgoglione ME, Maurelli MP, Musella V, Piemonte M, Caravano L, Coppola MG, Cringoli G (2011) Intestinal parasites in immigrants in the city of Naples (southern Italy). Acta Trop 117:196–201PubMedCrossRefPubMedCentralGoogle Scholar
  106. Gupte A, Shah C, Koticha A, Shukla A, Kuyare S, Bhatia S (2014) Gastrodiscoides hominis infestation of colon: endoscopic appearance. Gastrointest Endosc 79:549–550PubMedCrossRefPubMedCentralGoogle Scholar
  107. Habtamu K, Degarege A, Ye-Ebiyo Y, Erko B (2011) Comparison of the Kato-Katz and FLOTAC techniques for the diagnosis of soil-transmitted helminth infections. Parasitol Int 60:398–402PubMedCrossRefPubMedCentralGoogle Scholar
  108. Harinasuta T, Pungpak S, Keystone J (1993) Trematode infections. Opisthorchiasis, clonorchiasis, fascioliasis and paragonimiasis. Infect Dis Clin N Am 7:699–716Google Scholar
  109. Hatz CF (2001) The use of ultrasound in schistosomiasis. Adv Parasitol 48:225–284PubMedCrossRefPubMedCentralGoogle Scholar
  110. Henry TS, Lane MA, Weil GJ, Bailey TC, Bhalla S (2012) Chest CT features of North American paragonimiasis. Am J Roentgenol 198:1076–1083CrossRefGoogle Scholar
  111. Hong ST, Fang Y (2012) Clonorchis sinensis and clonorchiasis, an update. Parasitol Int 61:17–24PubMedCrossRefPubMedCentralGoogle Scholar
  112. Huang SY, Tang JD, Song HQ, Fu BQ, Xu MJ, Hu XC, Zhang H, Weng YB, Lin RQ, Zhu XQ (2012a) A specific PCR assay for the diagnosis of Clonorchis sinensis infection in humans, cats and fishes. Parasitol Int 61:187–190PubMedCrossRefPubMedCentralGoogle Scholar
  113. Huang SY, Zhao GH, Fu BQ, Xu MJ, Wang CR, Wu SM, Zou FC, Zhu XQ (2012b) Genomics and molecular genetics of Clonorchis sinensis: current status and perspectives. Parasitol Int 61:71–76PubMedCrossRefPubMedCentralGoogle Scholar
  114. Hung NM, Madsen H, Fried B (2013) Global status of fish-borne zoonotic trematodiasis in humans. Acta Parasitol 58:231–238PubMedCrossRefPubMedCentralGoogle Scholar
  115. Intapan PM, Sanpool O, Thanchomnang T, Imtawil K, Pongchaiyakul C, Nawa Y, Maleewong W (2012) Molecular identification of a case of Paragonimus pseudoheterotremus infection in Thailand. Am J Trop Med Hyg 87:706–709PubMedCrossRefPubMedCentralGoogle Scholar
  116. Iwagami M, Rajapakse RP, Paranagama W, Okada T, Kano S, Agatsuma T (2008) Ancient divergence of Paragonimus westermani in Sri Lanka. Parasitol Res 102:845–852PubMedCrossRefPubMedCentralGoogle Scholar
  117. Jang JS, Kim KH, Yu JR, Lee SU (2007) Identification of parasite DNA in common bile duct stones by PCR and DNA sequencing. Korean J Parasitol 45:301–306PubMedCrossRefPubMedCentralGoogle Scholar
  118. Jeandron A, Abdyldaieva G, Usubalieva J, Ensink JH, Cox J, Matthys B, Rinaldi L, Cringoli G, Utzinger J (2010) Accuracy of the Kato-Katz, adhesive tape and FLOTAC techniques for helminth diagnosis among children in Kyrgyzstan. Acta Trop 116:185–192PubMedCrossRefPubMedCentralGoogle Scholar
  119. Jeandron A, Rinaldi L, Abdyldaieva G, Usubalieva J, Steinmann P, Cringoli G, Utzinger J (2011) Human infections with Dicrocoelium dendriticum in Kyrgyzstan: the tip of the iceberg? J Parasitol 97:1170–1172PubMedCrossRefPubMedCentralGoogle Scholar
  120. 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
  121. Johansen MV, Lier T, Sithithaworn P (2015) Towards improved diagnosis of neglected zoonotic trematodes using a One Health approach. Acta Trop 141(Pt B):161–169PubMedCrossRefPubMedCentralGoogle Scholar
  122. Jurberg AD, de Oliveira AA, Lenzi HL, Coelho PM (2008) A new miracidia hatching device for diagnosing schistosomiasis. Mem Inst Oswaldo Cruz 103:112–114PubMedCrossRefPubMedCentralGoogle Scholar
  123. 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
  124. Kaewkong W, Intapan PM, Sanpool O, Janwan P, Thanchomnang T, Laummaunwai P, Lulitanond V, Doanh PN, Maleewong W (2013) Molecular differentiation of Opisthorchis viverrini and Clonorchis sinensis eggs by multiplex real-time PCR with high resolution melting analysis. Korean J Parasitol 51:689–694PubMedCrossRefPubMedCentralGoogle Scholar
  125. Kang S, Sultana T, Loktev VB, Wongratanacheewin S, Sohn WM, Eom KS, Park JK (2008) Molecular identification and phylogenetic analysis of nuclear rDNA sequences among three opisthorchiid liver fluke species (Opisthorchiidae: Trematoda). Parasitol Int 57:191–197PubMedCrossRefPubMedCentralGoogle Scholar
  126. Katz N, Chaves A, Pellegrino J (1972) A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Säo Paulo 14:397–400PubMedPubMedCentralGoogle Scholar
  127. Kazantseva L, García Lázaro MDP, Herrera-Velit P, Espinoza JR (2017) Anti-Fas2 IgM antibodies in Fasciola hepatica infected patients with positive IgG serology. Trans R Soc Trop Med Hyg 111:102–106PubMedCrossRefPubMedCentralGoogle Scholar
  128. Keiser J, Utzinger J (2005) Emerging foodborne trematodiasis. Emerg Infect Dis 11:1507–1514PubMedCrossRefGoogle Scholar
  129. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483PubMedCrossRefPubMedCentralGoogle Scholar
  130. Keiser J, Duthaler U, Utzinger J (2010) Update on the diagnosis and treatment of food-borne trematode infections. Curr Opin Infect Dis 23:513–520PubMedCrossRefPubMedCentralGoogle Scholar
  131. Khan MAH, Ullah R, Rehman A, Rehman L, Shareef PA, Abidi SMA (2017) Immunolocalization and immunodetection of the excretory/secretory (ES) antigens of Fasciola gigantica. PLoS One 12(10):e0185870PubMedCrossRefPubMedCentralGoogle Scholar
  132. Kim TI, Na BK, Hong SJ (2009) Functional genes and proteins of Clonorchis sinensis. Korean J Parasitol 47:S59–S68PubMedCrossRefGoogle Scholar
  133. Kim YJ, Lee SM, Choi GE, Hwang SH, Kim HH, Lee EY, Chang CL (2010) Performance of an enzyme-linked immunosorbent assay for detection of Clonorchis sinensis infestation in high- and low-risk groups. J Clin Microbiol 48:2365–2367PubMedCrossRefPubMedCentralGoogle Scholar
  134. Kim KU, Lee K, Park HK, Jeong YJ, Yu HS, Lee MK (2011) A pulmonary paragonimiasis case mimicking metastatic pulmonary tumor. Korean J Parasitol 49:69–72PubMedCrossRefPubMedCentralGoogle Scholar
  135. Knight WB, Hiatt RA, Cline BL, Ritchie LS (1976) A modification of the formol-ether concentration technique for increased sensitivity in detecting Schistosoma mansoni. Am J Trop Med Hyg 55:818–823CrossRefGoogle Scholar
  136. Knopp S, Rinaldi L, Khamis IS, Stothard JR, Rollinson D, Maurelli MP, Steinmann P, Marti H, Cringoli G, Utzinger J (2009a) A single FLOTAC is more sensitive than triplicate Kato-Katz for the diagnosis of low-intensity soil-transmitted helminth infections. Trans R Soc Trop Med Hyg 103:347–354PubMedCrossRefGoogle Scholar
  137. Knopp S, Glinz D, Rinaldi L, Mohammed KA, N’Goran EK, Stothard JR, Marti H, Cringoli G, Rollinson D, Utzinger J (2009b) FLOTAC: a promising technique for detecting helminth eggs in human faeces. Trans R Soc Trop Med Hyg 103:1190–1194PubMedCrossRefGoogle Scholar
  138. Knopp S, Corstjens PL, Koukounari A, Cercamondi CI, Ame SM, Ali SM, de Dood CJ, Mohammed KA, Utzinger J, Rollinson D, van Dam GJ (2015) Sensitivity and specificity of a urine circulating anodic antigen test for the diagnosis of Schistosoma haematobium in low endemic settings. PLoS Negl Trop Dis 9(5):e0003752PubMedCrossRefPubMedCentralGoogle Scholar
  139. Koh EJ, Kim SK, Wang KC, Chai JY, Chong S, Park SH, Cheon JE, Phi JH (2012) The return of an old worm: cerebral paragonimiasis presenting with intracerebral hemorrhage. J Korean Med Sci 27:1428–1432PubMedCrossRefPubMedCentralGoogle Scholar
  140. Lall M, Sahni AK, Rajput AK (2013) Pleuropulmonary paragonimiasis: mimicker of tuberculosis. Pathog Glob Health 107:40–42PubMedCrossRefPubMedCentralGoogle Scholar
  141. Lamaningao P, Kanda S, Laimanivong S, Shimono T, Darcy AW, Phyaluanglath A, Mishima N, Nishiyama T (2017) Development of a PCR assay for diagnosing trematode (Opisthorchis and Haplorchis) infections in human stools. Am J Trop Med Hyg 96:221–228PubMedCrossRefPubMedCentralGoogle Scholar
  142. Lambertucci JR, dos Santos Silva LC, Andrade LM, de Queiroz LC, Carvalho VT, Voieta I, Antunes CM (2008) Imaging techniques in the evaluation of morbidity in schistosomiasis mansoni. Acta Trop 108:209–217PubMedCrossRefPubMedCentralGoogle Scholar
  143. Lane MA, Marcos LA, Onen NF, Demertzis LM, Hayes EV, Davila SZ, Nurutdinova DR, Bailey TC, Weil GJ (2012) Paragonimus kellicotti flukes in Missouri, USA. Emerg Infect Dis 18:1263–1267PubMedCrossRefPubMedCentralGoogle Scholar
  144. Le TH, Van De N, Blair D, Sithithaworn P, McManus DP (2006a) Clonorchis sinensis and Opisthorchis viverrini: development of a mitochondrial-based multiplex PCR for their identification and discrimination. Exp Parasitol 112:109–114PubMedCrossRefGoogle Scholar
  145. Le TH, Van De N, Blair D, McManus DP, Kino H, Agatsuma T (2006b) Paragonimus heterotremus Chen and Hsia (1964), in Viet Nam: a molecular identification and relationships of isolates from different hosts and geographical origins. Acta Trop 98:25–33PubMedCrossRefPubMedCentralGoogle Scholar
  146. Le TH, Hguyen NTB, Truong NH, De NV (2012a) Development of mitochondrial loop-mediated isothermal amplification for detection of the small liver fluke Opisthorchis viverrini (Opisthorchiidae; Trematoda; Platyhelminthes). J Clin Microbiol 50:1178–1184PubMedCrossRefPubMedCentralGoogle Scholar
  147. Le TH, Nguyen KT, Nguyen NT, Doan HT, Le XT, Hoang CT, De NV (2012b) Development and evaluation of a single-step duplex PCR for simultaneous detection of Fasciola hepatica and Fasciola gigantica (family Fasciolidae, class Trematoda). J Clin Microbiol 50:2720–2726PubMedCrossRefPubMedCentralGoogle Scholar
  148. Lee SH, Hwang SW, Chai JY, Seo BS (1984) Comparative morphology of eggs of heterophyids and Clonorchis sinensis causing human infections in Korea. Korean J Parasitol 22:171–180CrossRefGoogle Scholar
  149. Lee SC, Chung YB, Kong Y, Kang SY, Cho SY (1993) Antigenic protein fractions of Metagonimus yokogawai reacting with patient sera. Korean J Parasitol 31:43–48PubMedCrossRefPubMedCentralGoogle Scholar
  150. Lee EG, Na BK, Bae YA, Kim SH, Je EY, Ju JW, Cho SH, Kim TS, Kang SY, Cho SY, Kong Y (2006) Identification of immunodominant excretory-secretory cysteine proteases of adult Paragonimus westermani by proteome analysis. Proteomics 6:1290–1300PubMedCrossRefPubMedCentralGoogle Scholar
  151. 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 100:677–681PubMedCrossRefPubMedCentralGoogle Scholar
  152. Lee JJ, Jung BK, Lim H, Lee MY, Choi SY, Shin EH, Chai JY (2012a) Comparative morphology of minute intestinal fluke eggs that occur in human stools in the Republic of Korea. Korean J Parasitol 50:207–213PubMedCrossRefPubMedCentralGoogle Scholar
  153. Lee MR, Kim YJ, Kim DW, Yoo WG, Cho SH, Hwang KY, Ju JW, Lee WJ (2012b) The identification of antigenic proteins: 14-3-3 protein and propionyl-CoAcarboxylase in Clonorchis sinensis. Mol Biochem Parasitol 182:1–6PubMedCrossRefPubMedCentralGoogle Scholar
  154. Lengeler C, Utzinger J, Tanner M (2002) Screening for schistosomiasis with questionnaires. Trends Parasitol 18:375–377PubMedCrossRefPubMedCentralGoogle Scholar
  155. Levy C, Lymp J, Angulo P, Gores GJ, Larusso N, Lindor KD (2005) The value of serum CA 19-9 in predicting cholangiocarcinomas in patients with primary sclerosing colangitis. Dig Dis Sci 50:1734–1740PubMedCrossRefPubMedCentralGoogle Scholar
  156. Li Y, Hu X, Liu X, Huang Y, Xu J, Zhao J, Wu Z, Yu X (2012) Serological diagnosis of clonorchiasis: using a recombinant propeptide of cathepsin L proteinase from Clonorchis sinensis as a candidate antigen. Parasitol Res 110:2197–2203PubMedCrossRefGoogle Scholar
  157. Liang T, Liang G, Du Y, Wang X, Wang Y, Chen A, Chen Z, Du J, Li H, Yu L (2018) Scrotal Paragonimiasis in adults: two case reports and review of literature. Medicine (Baltimore) 97(14):e0328CrossRefGoogle Scholar
  158. Lier T, Simonsen GS, Wang T, Lu D, Haukland HH, Vennervald BJ, Johansen MV (2009a) Low sensitivity of the formol-ethyl acetate sedimentation concentratiom technique in low-intensity Schistosoma japonicum infections. PLoS Negl Trop Dis 3(2):e386PubMedCrossRefPubMedCentralGoogle Scholar
  159. Lier T, Simonsen GS, Wang T, Lu D, Haukland HH, Vennervald BJ, Hegstad J, Johansen MV (2009b) Real-time polymerase chain reaction for detection of low-intensity Schistosoma japonicum infections in China. Am J Trop Med Hyg 81:428–432PubMedCrossRefPubMedCentralGoogle Scholar
  160. Lim JH, Mairiang E, Ahn GH (2008) Biliary parasitic diseases including clonorchiasis, opisthorchiasis and fascioliasis. Abdom Imaging 33:157–165PubMedCrossRefGoogle Scholar
  161. Linder E, Lundin M, Thors C, Lebbad M, Winiecka-Krusnell J, Helin H, Leiva B, Isola J, Lundin J (2008) Web-based virtual microscopy for parasitology: a novel tool for education and quality assurance. PLoS Negl Trop Dis 2(10):e315PubMedCrossRefPubMedCentralGoogle Scholar
  162. Linder E, Grote A, Varjo S, Linder N, Lebbad M, Lundin M, Diwan V, Hannuksela J, Lundin J (2013) On-chip imaging of Schistosoma haematobium eggs in urine for diagnosis by computer vision. PLoS Negl Trop Dis 7(12):e2547PubMedCrossRefPubMedCentralGoogle Scholar
  163. Liu GH, Yan HB, Otranto D, Wang XY, Zhao GH, Jia WZ, Zhu XQ (2014) Dicrocoelium chinensis and Dicrocoelium dendriticum (Trematoda: Digenea) are distinct lancet fluke species based on mitochondrial and nuclear ribosomal DNA sequences. Mol Phylogenet Evol 79:325–331PubMedCrossRefGoogle Scholar
  164. Long Y, Qin Z, Duan M, Li S, Wu X, Lin W, Li J, Zhao Z, Liu J, Xiong D, Huang Y, Hu X, Yang C, Ye M, Tan W (2016) Screening and identification of DNA aptamers toward Schistosoma japonicum eggs via SELEX. Sci Rep 6:24986PubMedCrossRefPubMedCentralGoogle Scholar
  165. López-Caballero J, Oceguera-Figueroa A, León-Règagnon V (2013) Detection of multiple species of human Paragonimus from Mexico using morphological data and molecular barcodes. Mol Ecol Resour 13(6):1125–1136PubMedPubMedCentralGoogle Scholar
  166. Lovis L, Mak TK, Phongluxa K, Soukhathammavong P, Sayasone S, Akkhavong K, Odermatt P, Keiser J, Felger I (2009) PCR diagnosis of Opisthorchis viverrini and Haplorchis taichui infections in a Lao community in an area of endemicity and comparison of diagnostic methods for parasitological field surveys. J Clin Microbiol 47:1517–1523PubMedCrossRefPubMedCentralGoogle Scholar
  167. Lumbreras H, Cantella R, Burga R (1962) Acerca de un procedimiento de sedimentación rápida para investigar huevos de Fasciola hepatica en las heces, su evaluación y su uso en el campo. Rev Méd Perú 31:167–174. (in Spanish).Google Scholar
  168. 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
  169. Maleewong W (1997) Recent advances in diagnosis of paragonimiasis. Southeast Asian J Trop Med Public Health 28(Suppl 1):134–138PubMedPubMedCentralGoogle Scholar
  170. Marchese V, Beltrame A, Angheben A, Monteiro GB, Giorli G, Perandin F, Buonfrate D, Bisoffi Z (2018) Schistosomiasis in immigrants, refugees and travellers in an Italian referral centre for tropical diseases. Infect Dis Poverty 7:55PubMedCrossRefPubMedCentralGoogle Scholar
  171. Marco-Flores V, Marcos-Raymundo L, Terashima Iwashita A, Samalvides-Cuba F, Miranda-Sanchez E, Espinoza-Babilon J, Gotuzzo-Herencia E (2002) Fas-2 ELISA and the rapid sedimentation technique modified by Lumbreras for Fasciola hepatica infection diagnosis. Rev Méd Herediana 13:49–57CrossRefGoogle Scholar
  172. Martínez-Sernández V, Muiño L, Perteguer MJ, Gárate T, Mezo M, González-Warleta M, Muro A, Correia da Costa JM, Romarís F, Ubeira FM (2011) Development and evaluation of a new lateral flow immunoassay for serodiagnosis of human fasciolosis. PLoS Negl Trop Dis 5:e1376PubMedCrossRefPubMedCentralGoogle Scholar
  173. Marty AM, Neafie RC (2000) Paragonimiasis. In: Meyers WM, Neafie RC, Marty AM, Wear DJ (eds) Pathology of infectious diseases, vol I. Helmintiases. Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DC, pp 49–67Google Scholar
  174. Mas-Coma S, Bargues MD (1997) Human liver flukes: a review. Res Rev Parasitol 57:145–218Google Scholar
  175. Mas-Coma S, Bargues MD, Esteban JG (1999) Human fasciolosis. In: Dalton JP (ed) Fasciolosis. CAB International, Wallingford, Oxon, pp 411–434Google Scholar
  176. Mas-Coma S, Bargues MD, Marty AM, Neafie RC (2000) Hepatic trematodiases. In: Meyers WM, Neafie RC, Marty AM, Wear DJ (eds) Pathology of infectious diseases, vol 1. Helminthiases. Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DC, pp 69–92Google Scholar
  177. Mas-Coma S, Bargues MD, Valero MA (2005) Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol 35:1255–1278PubMedCrossRefPubMedCentralGoogle Scholar
  178. Mas-Coma S, Bargues MD, Valero MA (2007) Plant-borne trematode zoonoses: fascioliasis and fasciolopsiasis. In: Murrell KD, Fried B (eds) Food-borne parasitic zoonoses: fish and plant-borne parasites, world class parasites, vol 11. Springer, New York, pp 293–334CrossRefGoogle Scholar
  179. 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 69:41–146PubMedCrossRefPubMedCentralGoogle Scholar
  180. Mas-Coma S, Bargues MD, Valero MA (2014a) Diagnosis of human fascioliasis by stool and blood techniques: update for the present global scenario. Parasitology 141:1918–1946PubMedCrossRefPubMedCentralGoogle Scholar
  181. Mas-Coma S, Valero MA, Bargues MD (2014b) Fascioliasis. In: Toledo R, Fried B (eds) Digenetic trematodes, 1st edn. Springer Science + Business Media, New York, pp 77–114CrossRefGoogle Scholar
  182. Mas-Coma S, Bargues MD, Valero MA (2018) Human fascioliasis infection sources, their diversity, incidence factors, analytical methods and prevention measures. Parasitology 145:1665–1699PubMedCrossRefPubMedCentralGoogle Scholar
  183. 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 61:203–207PubMedCrossRefPubMedCentralGoogle Scholar
  184. McManus DP, Gray DJ, Li Y, Feng Z, Williams GM, Stewart D, Rey-Ladino J, Ross AG (2010) Schistosomiasis in the People’s Republic of China: the era of the Three Gorges Dam. Clin Microbiol Rev 23:442–466PubMedCrossRefPubMedCentralGoogle Scholar
  185. Meyers WM, Neafie RC, Marty AM, Wear DJ (2000) Pathology of infectious diseases, vol I. Helmintiases. Armed Forces Institute of Pathology, American Registry of Pathology, Washington, DCGoogle Scholar
  186. Mirzadeh A, Valadkhani Z, Yoosefy A, Babaie J, Golkar M, Esmaeili Rastaghi AR, Kazemi-Rad E, Ashrafi K (2017) Expression, purification and in vitro refolding of the recombinant truncated Saposin-like protein 2 antigen for development of diagnosis of human fascioliasis. Acta Trop 171:163–171PubMedCrossRefPubMedCentralGoogle Scholar
  187. Mokhtarian K, Akhlaghi L, Mohammadi M, Meamar AR, Razmjou E, Khoshmirsafa M, Falak R (2016a) Evaluation of anti-Cathepsin L1: a more reliable method for serodiagnosis of human fasciolosis. Trans R Soc Trop Med Hyg 110:542–550PubMedCrossRefPubMedCentralGoogle Scholar
  188. Mokhtarian K, Akhlaghi L, Meamar AR, Razmjou E, Manouchehri Naeini K, Gholami S, Najafi Samei M, Falak R (2016b) Serodiagnosis of fasciolosis by fast protein liquid chromatography-fractionated excretory/secretory antigens. Parasitol Res 115:2957–2965PubMedCrossRefPubMedCentralGoogle Scholar
  189. Mordvinov VA, Yurlova NI, Ogorodova LM, Katokhin AV (2012) Opisthorchis felineus and Metorchis bilis are the main agents of liver fluke infection of humans in Russia. Parasitol Int 61:25–31PubMedCrossRefPubMedCentralGoogle Scholar
  190. Moure Z, Zarzuela F, Espasa M, Pou D, Serre-Delcor N, Treviño B, Bocanegra C, Molina I, Pumarola T, Sulleiro E (2017) Dicrocoelium dendriticum: an unusual parasitological diagnosis in a reference international health unit. Am J Trop Med Hyg 96:355–357PubMedCrossRefPubMedCentralGoogle Scholar
  191. Mulvenna J, Yonglitthipagon SB, Sripa B, Brindley PJ, Loukas A, Bethony JM (2012) Banking on the future: biobanking for “omics” approaches to biomarker discovery for Opisthorchis-induced cholangiocarcinoma in Thailand. Parasitol Int 61:173–177PubMedCrossRefPubMedCentralGoogle Scholar
  192. Muth S, Sayasone S, Odermatt-Biays S, Phompida S, Duong S, Odermatt P (2010) Schistosoma mekongi in Cambodia and Lao People’s Democratic Republic. Adv Parasitol 72:179–203PubMedCrossRefPubMedCentralGoogle Scholar
  193. Mwangi IN, Agola EL, Mugambi RM, Shiraho EA, Mkoji GM (2018) Development and evaluation of a loop-mediated isothermal amplification assay for diagnosis of Schistosoma mansoni infection in faecal samples. J Parasitol Res 2018:1267826PubMedCrossRefPubMedCentralGoogle Scholar
  194. Navaratnam AM, Mutumba-Nakalembe MJ, Stothard JR, Kabatereine NB, Fenwick A, Sousa-Figueiredo JC (2012) Notes on the use of urine-CCA dipsticks for detection of intestinal schistosomiasis in preschool children. Trans R Soc Trop Med Hyg 106:619–622PubMedCrossRefPubMedCentralGoogle Scholar
  195. Nkouawa A, Okamoto M, Mabou AK, Edinga E, Yamasaki H, Sako Y, Nakao M, Nakaya K, Blair D, Agatsuma T, Enyong P, Shibahara T, Moyou-Somo R, Ito A (2009) Paragonimiasis in Cameroon: molecular identification, serodiagnosis and clinical manifestations. Trans R Soc Trop Med Hyg 103:255–261PubMedCrossRefPubMedCentralGoogle Scholar
  196. Obeng BB, Aryeetey YA, de Dood CJ, Amoah AS, Larbi IA, Deelder AM, Yazdanbakhsh M, Hartgers FC, Boakye DA, Verweij JJ, van Dam GJ, van Lieshout L (2008) Application of a circulating-cathodic-antigen (CCA) strip test and real-time PCR, in comparison with microscopy, for the detection of Schistosoma haematobium in urine samples from Ghana. Ann Trop Med Parasitol 102:625–633PubMedCrossRefPubMedCentralGoogle Scholar
  197. Ochodo EA, Gopalakrishna G, Spek B, Reitsma JB, van Lieshout L, Polman K, Lamberton P, Bossuyt PM, Leeflang MM (2015) Circulating antigen tests and urine reagent strips for diagnosis of active schistosomiasis in endemic areas. Cochrane Database Syst Rev (3):CD009579Google Scholar
  198. Ohmae H, Sinuon M, Kirinoki M, Matsumoto J, Chigusa Y, Socheat D, Matsuda H (2004) Schistosomiasis mekongi: from discovery to control. Parasitol Int 53:135–142PubMedCrossRefPubMedCentralGoogle Scholar
  199. Olveda DU, Olveda RM, Lam AK, Chau TN, Li Y, Gisparil AD II, Ross AG (2014) Utility of diagnostic imaging in the diagnosis and management of Schistosomiasis. Clin Microbiol 3(2):142–155PubMedCrossRefPubMedCentralGoogle Scholar
  200. Orihel TC, Ash LR (1995) Parasites in human tissues. ASCP Press, American Society of Clinical Pathologists, ChicagoGoogle Scholar
  201. Ortu G, Ndayishimiye O, Clements M, Kayugi D, Campbell CH, Lamine MS, Zivieri A, Magalhaes RS, Binder S, King CH, Fenwick A, Colley DG, Jourdan PM (2017) Countrywide reassessment of Schistosoma mansoni infection in Burundi using a urine-circulating cathodic antigen rapid test: informing the National Control Program. Am J Trop Med Hyg 96:664–673PubMedPubMedCentralGoogle Scholar
  202. Osakunor DNM, Woolhouse MEJ, Mutapi F (2018) Paediatric schistosomiasis: what we know and what we need to know. PLoS Negl Trop Dis 12(2):e0006144PubMedCrossRefPubMedCentralGoogle Scholar
  203. Pagès JR, Jourdane J, Southgate VR, Tchuem Tchuenté LA (2003) Reconnaissance de deux espèces jumelles au sein du taxon Schistosoma intercalatum Fisher, 1934, agent de la schistosomose humaine rectale en Afrique. Description de Schistosoma guineensis n. sp. In: Combes C, Jourdane J (eds) Taxonomy, ecology and evolution of metazoan parasites, vol II. Presses Universitaires de Perpignan, Perpignan, pp 139–146Google Scholar
  204. Patel NU, Bang TJ, Dodd GD 3rd (2016) CT findings of human Fasciola hepatica infection: case reports and review of the literature. Clin Imaging 40:251–255PubMedCrossRefPubMedCentralGoogle Scholar
  205. Pauly A, Schuster R, Steuber S (2003) Molecular characterization and differentiation of opisthorchiid trematodes of the species Opisthorchis felineus (Rivolta, 1884) and Metorchis bilis (Braun, 1790) using polymerase chain reaction. Parasitol Res 90:409–414PubMedCrossRefPubMedCentralGoogle Scholar
  206. Petney TN, Andrews RH, Saijuntha W, Wenz-Mücke A, Sithithaworn P (2013) The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverrini. Int J Parasitol 43:1031–1046PubMedCrossRefPubMedCentralGoogle Scholar
  207. Polman K, Diakhate MM, Engels D, Nahimana S, Van Dam GJ, Falcão Ferreira ST, Deelder AM, Gryseels B (2000) Specificity of circulating antigen detection for schistosomiasis mansoni in Senegal and Burundi. Trop Med Int Health 5:534–537PubMedCrossRefPubMedCentralGoogle Scholar
  208. Pozio E, Armignacco O, Ferri F, Gomez Morales MA (2013) Opisthorchis felineus an emerging infection in Italy and its implication for the European Union. Acta Trop 126:54–62PubMedCrossRefPubMedCentralGoogle Scholar
  209. Prasad PK, Goswami LM, Tandon V, Chatterjee A (2011) PCR-based molecular characterization and insilico analysis of food-borne trematode parasites Paragonimus westermani, Fasciolopsis buski and Fasciola gigantica from Northeast India using ITS2 rDNA. Bioinformation 6:64–68PubMedCrossRefPubMedCentralGoogle Scholar
  210. Procop GW (2009) North American paragonimiasis (caused by Paragonimus kellicotti) in the context of global paragonimiasis. Clin Microbiol Rev 22:415–446PubMedCrossRefPubMedCentralGoogle Scholar
  211. Qiu XG, Nakamura-Uchiyama F, Nawa Y, Itoh M (2016) A tool for mass-screening of paragonimiasis: an enzyme-linked immunosorbent assay with urine samples. Trop Med Health 44:19. Scholar
  212. Quiao TQ, Zheng PM, Ma RH, Luo XB, Luo ZL (2012) Development of a real-time PCR assay for the detection of Clonorchis sinensis DNA in gallbladder bile and stone samples from patients with cholecystolithiasis. Parasitol Res 111:1497–1503CrossRefGoogle Scholar
  213. Rahimi MT, Ashrafi K, Koosha S, Abdi J, Rokni MB (2011) Evaluation of Fast-ELISA versus standard-ELISA to diagnose human fasciolosis. Arch Iran Med 14:18–21Google Scholar
  214. Rim HJ (1982) Opisthorchiasis. In: Hillyer GV, Hopla CE (eds) Handbook series in zoonoses. Section C: Parasite zoonoses, vol III. CRC Press, Boca Raton, pp 109–121Google Scholar
  215. Rim HJ (2005) Clonorchiasis: an update. J Helminthol 79:269–281PubMedCrossRefPubMedCentralGoogle Scholar
  216. Ritchie LS (1948) An ether sedimentation technique for routine stool examinations. Bull U S Army Med Dep 8:326PubMedPubMedCentralGoogle Scholar
  217. Robijn ML, Planken J, Kornelis D, Hokke CH, Deelder AM (2008) Mass spectrometric detection of urinary oligosaccharides as markers of Schistosoma mansoni infection. Trans R Soc Trop Med Hyg 102:79–83PubMedCrossRefPubMedCentralGoogle Scholar
  218. Rokni MB, Mirhendi H, Mizani A, Mohebali M, Sharbatkhori M, Kia EB, Abdoli H, Izadi S (2010) Identification and differentiation of Fasciola hepatica and Fasciola gigantica using a simple PCR-restriction enzyme method. Exp Parasitol 124:209–213PubMedCrossRefPubMedCentralGoogle Scholar
  219. Ross AGP, Sleigh AC, Li Y, Davis GM, Williams GM, Jiang Z, Feng Z, McManus DP (2001) Schistosomiasis in the People’s Republic of China: prospects and challenges for the 21st century. Clin Microbiol Rev 14:270–295PubMedCrossRefPubMedCentralGoogle Scholar
  220. Ross AGP, Bartley PB, Sleigh AC, Olds GR, Li Y, Williams GM, McManus DP (2002) Schistosomiasis. N Engl J Med 346:1212–1220PubMedCrossRefPubMedCentralGoogle Scholar
  221. Sandoval H, Manga-González MY, Castro JM (2013) A tool for diagnosis of Dicrocoelium dendriticum infection: hatching eggs and molecular identification of the miracidium. Parasitol Res 112:1589–1595PubMedCrossRefPubMedCentralGoogle Scholar
  222. Sanneh B, Joof E, Sanyang AM, Renneker K, Camara Y, Sey AP, Jagne S, Baldeh I, Ceesay SJ, Sambou SM, Ogoussan K (2017) Field evaluation of a schistosome circulating cathodic antigen rapid test kit at point-of-care for mapping of schistosomiasis endemic districts in The Gambia. PLoS One 12(8):e0182003PubMedCrossRefPubMedCentralGoogle Scholar
  223. Sanpool O, Intapan PM, Thanchomnang T, Janwan P, Lulitanond V, Doanh PN, Van Hien H, Dung do T, Maleewong W, Nawa Y (2012) Rapid detection and differentiation of Clonorchis sinensis and Opisthorchis viverrini eggs in human fecal samples using a duplex real-time fluorescence resonance energy transfer PCR and melting curve analysis. Parasitol Res 111:89–96PubMedCrossRefPubMedCentralGoogle Scholar
  224. Sarkari B, Khabisi SA (2017) Immunodiagnosis of human fascioliasis: an update of concepts and performances of the serological assays. J Clin Diagn Res 11:OE05–OE10PubMedPubMedCentralGoogle Scholar
  225. Sato M, Thaenkham U, Dekumyoy P, Waikagul J (2009) Discrimination of O. viverrini, C. sinensis, H. pumilio and H. taichui using nuclear DNA-based PCR targeting ribosomal DNA ITS regions. Acta Trop 109:81–83PubMedCrossRefPubMedCentralGoogle Scholar
  226. Sato M, Pongvongsa T, Sanguankiat S, Yoonuan T, Dekumyoy P, Kalambaheti T, Keomoungkhoun M, Phimmayoi I, Boupha B, Moji K, Waikagul J (2010) Copro-DNA diagnosis of Opisthorchis viverrini and Haplorchis taichui infection in an endemic area of Lao PDR. Southeast Asian J Trop Med Public Health 41:28–35PubMedPubMedCentralGoogle Scholar
  227. Sawangsoda P, Sithithaworn J, Tesana S, Pinlaor S, Boonmars T, Mairiang E, Yongvanit P, Duenngai K, Sithithaworn P (2012) Diagnostic values of parasite-specific antibody detections in saliva and urine in comparison with serum in opisthorchiasis. Parasitol Int 61:196–202PubMedCrossRefPubMedCentralGoogle Scholar
  228. Shafiei R, Sarkari B, Sadjjadi SM (2015) Performance of a 27 kDa Fasciola hepatica antigen in the diagnosis of human fascioliasis. J Lab Phys 7:17–20Google Scholar
  229. Shalaby S, El-Bahy M, Hassan A, Shalaby H, Gupta N (2015) Diagnotic value of some Fasciola gigantica antigens. J Parasit Dis 39:479–486PubMedCrossRefPubMedCentralGoogle Scholar
  230. Shane HL, Verani JR, Abudho B, Montgomery SP, Blackstock AJ, Mwinzi PN, Butler SE, Karanja DM, Secor WE (2011) Evaluation of urine CCA assays for detection of Schistosoma mansoni infection in Western Kenya. PLoS Negl Trop Dis 5:e951PubMedCrossRefPubMedCentralGoogle Scholar
  231. Shim SS, Kim Y, Lee JK, Lee JH, Song DE (2012) Pleuropulmonary and abdominal paragonimiasis: CT and ultrasound findings. Br J Radiol 85:403–410PubMedCrossRefPubMedCentralGoogle Scholar
  232. Shin SH, Hsu A, Chastain HM, Cruz LA, Elder ES, Sapp SG, McAuliffe I, Espino AM, Handali S (2016) Development of two FhSAP2 recombinant-based assays for immunodiagnosis of human chronic fascioliasis. Am J Trop Med Hyg 95:852–855PubMedCrossRefPubMedCentralGoogle Scholar
  233. 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 3–52CrossRefGoogle Scholar
  234. Slesak G, Inthalad S, Basy P, Keomanivong D, Phoutsavath O, Khampoui S, Grosrenaud A, Amstutz V, Barennes H, Buisson Y, Odermatt P (2011) Ziehl-Neelsen staining technique can diagnose paragonimiasis. PLoS Negl Trop Dis 5(5):e1048. Scholar
  235. Slusarewicz P, Pagano S, Mills C, Popa G, Chow KM, Mendenhall M, Rodgers DW, Nielsen MK (2016) Automated parasite faecal egg counting using fluorescence labelling, smartphone image capture and computational image analysis. Int J Parasitol 46:485–493PubMedCrossRefPubMedCentralGoogle Scholar
  236. Sohn WM, Yong TS, Eom KS, Min DY, Lee D, Jung BK, Banouvong V, Insisiengmay B, Phommasack B, Rim HJ, Chai JY (2014) Prevalence of Haplorchis taichui among humans and fish in Luang Prabang Province, Lao PDR. Acta Trop 136:74–80PubMedCrossRefPubMedCentralGoogle Scholar
  237. Sowerby SJ, Crump JA, Johnstone MC, Krause KL, Hill PC (2016) Smartphone microscopy of parasite eggs accumulated into a single field of view. Am J Trop Med Hyg 94:227–230PubMedCrossRefPubMedCentralGoogle Scholar
  238. 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 4:1148–1155CrossRefGoogle Scholar
  239. 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 72:305–350PubMedCrossRefPubMedCentralGoogle Scholar
  240. 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 120S:S158–S168CrossRefGoogle Scholar
  241. Sripa J, Brindley PJ, Sripa B, Loukas A, Kaewkes S, Laha T (2012) Evaluation of liver fluke recombinant cathepsin B-1 protease as a serodiagnostic antigen for human opisthorchiasis. Parasitol Int 61:191–195PubMedCrossRefPubMedCentralGoogle Scholar
  242. Stensvold CR, Saijuntha W, Sithithaworn P, Wongratanacheewin S, Strandgaard H, Ornbjerg N, Johansen MV (2006) Evaluation of PCR based coprodiagnosis of human opisthorchiasis. Acta Trop 97:26–30PubMedCrossRefPubMedCentralGoogle Scholar
  243. Stoll NR (1923) Investigations on the control of hookworm disease. XV. An effective method of counting hookworm eggs in feces. Am J Hyg 3:59–70Google Scholar
  244. Sukontason K, Piangjai S, Sukontason K, Chaithong U (1999) Potassium permanganate staining for differentiation the surface morphology of Opisthorchis viverrini, Haplorchis taichui and Phaneropsolus bonnie eggs. Southeast Asian J Trop Med Public Health 30:371–374PubMedPubMedCentralGoogle Scholar
  245. Sun J, Xu J, Liang P, Mao Q, Huang Y, Lv X, Deng C, Liang C, de Hoog GS, Yu X (2011) Molecular identification of Clonorchis sinensis and discrimination with other opisthorchid liver fluke species using multiple ligation-depended probe amplification (MLPA). Parasit Vectors 4:98PubMedCrossRefPubMedCentralGoogle Scholar
  246. Tang ZL, Huang Y, Yu XB (2016) Current status and perspectives of Clonorchis sinensis and clonorchiasis: epidemiology, pathogenesis, omics, prevention and control. Infect Dis Poverty 5:71PubMedCrossRefPubMedCentralGoogle Scholar
  247. Tantrawatpan C, Intapan PM, Janwan P, Sanpool O, Lulitanond V, Srichantaratsamee C, Anamnart W, Maleewong W (2013) Molecular identification of Paragonimus species by DNA pyrosequencing technology. Parasitol Int 62:341–345PubMedCrossRefPubMedCentralGoogle Scholar
  248. Tantrawatpan C, Intapan PM, Thanchomnang T, Sanpool O, Janwan P, Lulitanond V, Sadaow L, Maleewong W (2014) Development of a PCR assay and pyrosequencing for identification of important human fish-borne trematodes and its potential use for detection in fecal specimens. Parasit Vectors 7:88PubMedCrossRefPubMedCentralGoogle Scholar
  249. Tantrawatpan C, Saijuntha W, Manochantr S, Kheolamai P, Thanchomnang T, Sadaow L, Intapan PM, Maleewong W (2016) A singleplex real-time fluorescence resonance energy transfer PCR with melting curve analysis for the differential detection of Paragonimus heterotremus, Echinostoma malayanum and Fasciola gigantica eggs in faeces. Trans R Soc Trop Med Hyg 110:74–83PubMedCrossRefPubMedCentralGoogle Scholar
  250. Tchuem Tchuenté LA, Kueté Fouodo CJ, Kamwa Ngassam RI, Sumo L, Dongmo Noumedem C, Kenfack CM, Gipwe NF, Nana ED, Stothard JR, Rollinson D (2012) Evaluation of circulating cathodic antigen (CCA) urine-tests for diagnosis of Schistosoma mansoni infection in Cameroon. PLoS Negl Trop Dis 6:e1758PubMedCrossRefPubMedCentralGoogle Scholar
  251. Teimoori S, Arimatsu Y, Laha T, Kaewkes S, Sereerak P, Tangkawattana S, Brindley PJ, Sripa B (2015) Immunodiagnosis of opisthorchiasis using parasite cathepsin F. Parasitol Res 114:4571–4578PubMedCrossRefPubMedCentralGoogle Scholar
  252. Teixera CF, Neuhauss E, Ben R, Romanzini J, Graeff-Teixeira C (2007) Detection of Schistosoma mansoni eggs in feces through their interaction with paramagnetic beads in a magnetic field. PLoS Negl Trop Dis 1:e73CrossRefGoogle Scholar
  253. ten Hove RJ, Verweij JJ, Vereecken K, Polman K, Dieye L, van Lieshout L (2008) Multiplex real-time PCR for the detection and quantification of Schistosoma mansoni and S. haematobium infection in stool samples collected in northern Senegal. Trans R Soc Trop Med Hyg 102:179–185PubMedCrossRefPubMedCentralGoogle Scholar
  254. Terashima A, Marcos L, Maco V, Canales M, Samalvides F, Tello R (2009) Spontaneous sedimentation in tuve technique (SSTT) for diagnosis of intestinal parasites. Rev Gastroenterol Peru 29:305–310PubMedPubMedCentralGoogle Scholar
  255. Tesana S, Srisawanwonk T, Kaewkes S, Sithithaworn P, Kanla P, Arunyanart C (1991) Egg shell morphology of the small eggs of human trematodes in Thailand. Southeast Asian J Trop Med Public Health 22:631–636PubMedPubMedCentralGoogle Scholar
  256. Thaenkham U, Visetsuk K, Dung DT, Waikagul J (2007) Discrimination of Opisthorchis viverrini from Haplorchis taichui using COI sequence marker. Acta Trop 103:26–32PubMedCrossRefGoogle Scholar
  257. Toledo R, Esteban JG (2016) An update on human echinostomiasis. Trans R Soc Trop Med Hyg 110:37–45PubMedCrossRefGoogle Scholar
  258. Toledo R, Esteban JG, Fried B (2006) Immunology and pathology of intestinal trematodes in their definitive hosts. Adv Parasitol 63:285–365PubMedCrossRefPubMedCentralGoogle Scholar
  259. Toledo R, Esteban JG, Fried B (2012) Current status of food-borne trematode infections. Eur J Clin Microbiol Infect Dis 31:1705–1718PubMedCrossRefGoogle Scholar
  260. Toledo R, Muñoz-Antolí C, Esteban JG (2014) Intestinal trematode infections. In: Toledo R, Fried B (eds) Digenetic trematodes, 1st edn. Springer Science + Business Media, New York, pp 201–240CrossRefGoogle Scholar
  261. 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:e367PubMedCrossRefPubMedCentralGoogle Scholar
  262. Ubeira FM, Muiño L, Valero MA, Periago MV, Pérez-Crespo I, Mezo M, González-Warleta M, Romarís F, Paniagua E, Cortizo S, Llovo J, Más-Coma S (2009) MM3-ELISA detection of Fasciola hepatica coproantigens in preserved human stool samples. Am J Trop Med Hyg 81:156–162PubMedCrossRefGoogle Scholar
  263. Upatham ES, Viyanant V (2003) Opisthorchis viverrini and opisthorchiasis: a historical review and future perspective. Acta Trop 88:171–176PubMedCrossRefPubMedCentralGoogle Scholar
  264. Utzinger J, Rinaldi L, Lohourignon LK, Rohner F, Zimmermann MB, Tschannen AB, N’Goran EK, Cringoli G (2008) FLOTAC: a new sensitive technique for the diagnosis of hookworm infections in humans. Trans R Soc Trop Med Hyg 102:84–90PubMedCrossRefPubMedCentralGoogle Scholar
  265. Valero MA, Pérez-Crespo I, Periago MV, Khoubbane M, Mas-Coma S (2009a) Fluke egg characteristics for the diagnosis of human and animal fascioliasis by Fasciola hepatica and F. gigantica. Acta Trop 111:150–159PubMedCrossRefGoogle Scholar
  266. Valero MA, Ubeira FM, Khoubbane M, Artigas P, Muiño L, Mezo M, Pérez-Crespo I, Periago MV, Mas-Coma S (2009b) MM3-ELISA evaluation of coproantigen release and serum antibody production in sheep experimentally infected with Fasciola hepatica and F. gigantica. Vet Parasitol 159:77–81PubMedCrossRefPubMedCentralGoogle Scholar
  267. Valero MA, Periago MV, Pérez-Crespo I, Rodríguez E, Perteguer MJ, Gárate T, González-Barberá EM, Mas-Coma S (2012a) Assessing the validity of an ELISA test for the serological diagnosis of human fascioliasis in different epidemiological situations. Tropical Med Int Health 17:630–636CrossRefGoogle Scholar
  268. Valero MA, Periago MV, Pérez-Crespo I, Angles R, Villegas F, Aguirre C, Strauss W, Espinoza JR, Herrera P, Terashima A, Tamayo H, Engels D, Gabrielli AF, Mas-Coma S (2012b) Field evaluation of a coproantigen detection test for fascioliasis diagnosis and surveillance in human hyperendemic areas of Andean countries. PLoS Negl Trop Dis 6(9):e1812PubMedCrossRefPubMedCentralGoogle Scholar
  269. van Gool T, Vetter JCM, Vervoort T, Doenhoff MJ, Wetsteyn J, Overbosch D (2002) Serodiagnosis of imported schistosomiasis by a combination of a commercial indirect hemagglutination test with Schistosoma mansoni adult worm antigens and enzyme-linked immunosorbent assay with S. mansoni egg antigens. J Clin Microbiol 40:3232–3237CrossRefGoogle Scholar
  270. van Grootveld R, van Dam GJ, de Dood C, de Vries JJC, Visser LG, Corstjens PLAM, van Lieshout L (2018) Improved diagnosis of active Schistosoma infection in travellers and migrants using the ultra-sensitive in-house lateral flow test for detection of circulating anodic antigen (CAA) in serum. Eur J Clin Microbiol Infect Dis 37:1709–1716PubMedCrossRefPubMedCentralGoogle Scholar
  271. Vanijanonta S, Radomyos P, Bunnag D, Harinasuta T (1981) Pulmonary paragonimiasis with expectoration of worms: a case report. Southeast Asian J Trop Med Public Health 12:104–106PubMedPubMedCentralGoogle Scholar
  272. Wang W, Li Y, Li H, Xing Y, Qu G, Dai J, Liang Y (2012) Immunodiagnostic efficacy of detection of Schistosoma japonicum human infections in China: a meta-analysis. Asian Pac J Trop Med 5:15–23PubMedCrossRefPubMedCentralGoogle Scholar
  273. Watwiengkam N, Sithithaworn J, Duenngai K, Sripa B, Laha T, Johansen MV, Sithithaworn P (2013) Improved performance and quantitative detection of copro-antigens by a monoclonal antibody based ELISA to diagnose human opisthorchiasis. Acta Trop 128:659–665PubMedCrossRefPubMedCentralGoogle Scholar
  274. Webb CM, Cabada MM (2018) Recent developments in the epidemiology, diagnosis, and treatment of Fasciola infection. Curr Opin Infect Dis 31:409–414PubMedCrossRefPubMedCentralGoogle Scholar
  275. Webster BL, Southgate VR, Littlewood DTJ (2006) A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. Int J Parasitol 36:947–955PubMedCrossRefPubMedCentralGoogle Scholar
  276. Weerakoon KG, Gobert GN, Cai P, McManus DP (2015) Advances in the diagnosis of human schistosomiasis. Clin Microbiol Rev 28:939–967PubMedCrossRefPubMedCentralGoogle Scholar
  277. Weerakoon KG, Gordon CA, McManus DP (2018) DNA diagnostics for schistosomiasis control. Trop Med Infect Dis 3(3):E81PubMedCrossRefPubMedCentralGoogle Scholar
  278. WHO (1991) Basic laboratory methods in medical parasitology. World Health Organization, GenevaGoogle Scholar
  279. Wichmann D, Panning M, Quack T, Kramme S, Burchard GD, Grevelding C, Drosten C (2009) Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma. PLoS Negl Trop Dis 3:e422PubMedCrossRefPubMedCentralGoogle Scholar
  280. Wichmann D, Poppert S, Von Thien H, Clerinx J, Dieckmann S, Jensenius M, Parola P, Richter J, Schunk M, Stich A, Zanger P, Burchard GD, Tannich E (2013) Prospective European-wide multicentre study on a blood based real-time PCR for the diagnosis of acute schistosomiasis. BMC Infect Dis 13:55PubMedCrossRefPubMedCentralGoogle Scholar
  281. Wolfe MS (2007) Dicrocoelium dendriticum or Dicrocoelium hospes. Clin Infect Dis 44:1522PubMedCrossRefPubMedCentralGoogle Scholar
  282. Wongkham C, Intapan PM, Maleewong W, Miwa M (2005) Evaluation of human IgG subclass antibodies in the serodiagnosis of Paragonimiasis heterotremus. Asian Pac J Allergy Immunol 23:205–211PubMedGoogle Scholar
  283. Wongratanacheewin S, Pumidonming W, Sermswan RW, Pipitgool V, Maleewong W (2002) Detection of Opisthorchis viverrini in human stool specimens by PCR. J Clin Microbiol 40:3879–3880PubMedCrossRefPubMedCentralGoogle Scholar
  284. Wongratanacheewin S, Sermswan RW, Sirisinha S (2003) Immunology and molecular biology of Opisthorchis viverrini infection. Acta Trop 88:195–207PubMedCrossRefPubMedCentralGoogle Scholar
  285. Wongsawad P, Wongsawad C (2009) Development of PCR-based diagnosis of minute intestinal fluke, Haplorchis taichui. Southeast Asian J Trop Med Public Health 40:919–923PubMedPubMedCentralGoogle Scholar
  286. Wongsawad C, Wongsawad P (2012) Opisthorchis viverrini and Haplorchis taichui: development of a multiple PCR assay for their detection and differentiation using specific primers derived from HAT-RAPD. Exp Parasitol 132:237–242PubMedCrossRefGoogle Scholar
  287. Wongsawad C, Wongsawad P, Chai JY, Anuntalabhochai S (2009a) Haplorchis taichui, Witenberg, 1930: development of a HAT-RAPD marker for the detection of minute intestinal fluke infection. Exp Parasitol 123:158–161PubMedCrossRefPubMedCentralGoogle Scholar
  288. Wongsawad C, Wongsawad P, Chuboon S, Anuntalabhochai S (2009b) Copro-diagnosis of Haplorchis taichui infection using sedimentation and PCR-based methods. Southeast Asian J Trop Med Public Health 40:924–928PubMedPubMedCentralGoogle Scholar
  289. Wongsawad C, Phalee A, Noikong W, Chuboon S, Nithikathkul C (2012) Co-infection with Opisthorchis viverrini and Haplorchis taichui detected by human fecal examination in Chomtong district, Chiang mai province, Thailand. Parasitol Int 61:56–59PubMedCrossRefPubMedCentralGoogle Scholar
  290. Xia Y, Chen J, Ju Y, You C (2016) Characteristic CT and MR imaging findings of cerebral paragonimiasis. J Neuroradiol 43:200–206PubMedCrossRefPubMedCentralGoogle Scholar
  291. Xu J, Rong R, Zhang HQ, Shi CJ, Zhu XQ, Xia CM (2010) Sensitive and rapid detection of Schistosoma japonicum DNA by loop-mediated isothermal amplification (LAMP). Int J Parasitol 40:327–331PubMedCrossRefPubMedCentralGoogle Scholar
  292. Yahiro S, Habe S, Duong V, Odermatt P, Barennes H, Strobel M, Nakamura S (2008) Identification of the human paragonimiasis causative agent in Lao People’s Democratic Republic. J Parasitol 94:1176–1177PubMedCrossRefPubMedCentralGoogle Scholar
  293. Yang SH, Park JO, Lee JH, Jeon BH, Kim WS, Kim SI, Yun KJ, Jeong ET, Lee KW, Kim YM, Lee MH, Park H (2004) Cloning and characterization of a new cysteine proteinase secreted by Paragonimus westermani adult worms. Am J Trop Med Hyg 71:87–92PubMedCrossRefPubMedCentralGoogle Scholar
  294. Yang Y, Li M, Pan C, Yang Y, Chen X, Yao C, Du A (2018) A duplex PCR for the simultaneous detection of Fasciola hepatica and Clonorchis sinensis. Vet Parasitol 259:1–5PubMedCrossRefPubMedCentralGoogle Scholar
  295. Yoonuan T, Nuamtanong S, Dekumyoy P, Phuphisut O, Adisakwattana P (2016) Molecular and immunological characterization of cathepsin L-like cysteine protease of Paragonimus pseudoheterotremus. Parasitol Res 115:4457–4470PubMedCrossRefPubMedCentralGoogle Scholar
  296. Yossepowitch O, Gotesman T, Assous M, Marva E, Zimlichman R, Dan M (2004) Opisthorchiasis from imported raw fish. Emerg Infect Dis 10:2122–2126PubMedCrossRefPubMedCentralGoogle Scholar
  297. Yu S, Mott K (1994) Epidemiology and morbidity of food-borne intestinal trematode infections. Trop Dis Bull 91:R125–R152Google Scholar
  298. Yu Q, Yang H, Feng Y, Zhu Y, Yang X (2012) Magnetic affinity enzyme-linked immunoassay for diagnosis of schistosomiasis japonicum in persons with low-intensity infection. Am J Trop Med Hyg 87:689–693PubMedCrossRefPubMedCentralGoogle Scholar
  299. Yu S, Zhang X, Chen W, Zheng H, Ai G, Ye N, Wang Y (2017) Development of an immunodiagnosis method using recombinant PsCP for detection of Paragonimus skrjabini infection in human. Parasitol Res 116:377–385PubMedCrossRefPubMedCentralGoogle Scholar
  300. Zarrin-Khameh N, Citron DR, Stager CE, Laucirica R (2008) Pulmonary paragonimiasis diagnosed by fine-needle aspiration biopsy. J Clin Microbiol 46:2137–2140PubMedCrossRefPubMedCentralGoogle Scholar
  301. Zhao GH, Li J, Blair D, Li XY, Elsheikha HM, Lin RQ, Zou FC, Zhu XQ (2012) Biotechnological advances in the diagnosis, species differentiation and phylogenetic analysis of Schistosoma spp. Biotechnol Adv 30:1381–1389PubMedCrossRefPubMedCentralGoogle Scholar
  302. Zhou BJ, Yang BB, Doanh PN, Yang ZQ, Xiang Z, Li CY, Shinohara A, Horii Y, Nawa Y (2008) Sequence analyses of ITS2 and CO1 genes of Paragonimus proliferus obtained in Yunnan province, China and their similarities with those of P. hokuoensis. Parasitol Res 102:1379–1383PubMedCrossRefPubMedCentralGoogle Scholar
  303. Zhou YB, Zheng HM, Jiang QW (2011) A diagnostic challenge for schistosomiasis japonica in China: consequences on praziquantel-based morbidity control. Parasit Vectors 4:194PubMedCrossRefPubMedCentralGoogle Scholar
  304. Zhu HP, Yu CH, Xia X, Dong G, Tang J, Fang L, Du Y (2010) Assessing the diagnostic accuracy of immunodiagnostic techniques in the diagnosis of schistosomiasis japonica: a meta-analysis. Parasitol Res 107:1067–1073PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • J. Guillermo Esteban
    • 1
    Email author
  • Carla Muñoz-Antoli
    • 1
  • Rafael Toledo
    • 1
  • Lawrence R. Ash
    • 2
  1. 1.Área de Parasitología, Departamento de Farmacia y Tecnología Farmacéutica y Parasitología, Facultad de FarmaciaUniversidad de ValenciaValenciaSpain
  2. 2.Infectious and Tropical Diseases, Fielding School of Public HealthUniversity of California, Los AngelesLos AngelesUSA

Personalised recommendations