Abstract
The burden of the two different diseases, “cystic echinococcosis” (CE), due to several species of Echinococcus among the E. granulosus sensu lato cluster, and “alveolar echinococcosis,” due to E. multilocularis, has long been underestimated. Other species, E. oligarthra and E. vogeli, may also cause disease in humans, similar to CE and AE, respectively. CE is usually maintained by a synanthropic domestic cycle (dog/domestic ungulates); a cycle in wild animals (fox/small mammals) allows E. multilocularis to subsist in nature, and environmental factors play a critical role. The larval stage of Echinococcus spp., the “metacestode,” is characterized by a germinal layer surrounded by a laminated layer and an adventitial layer. The germinal layer forms isolated cysts (CE) or aggregated microcysts (AE), which are filled with a water-like liquid (“hydatid fluid”). The diagnosis of both diseases in humans relies on imaging: ultrasound examination (also useful for mass screening), computed tomography, and magnetic resonance imaging, which provides pathognomonic images; incidental diagnosis is frequent. WHO-US-based classification of CE cysts (CE-1 to CE-5) and staging system for AE (PNM classification) are used to choose among a variety of therapeutic options available, including surgery to remove the lesions and nonsurgical image-guided interventions to sterilize CE cysts or treat complications in CE and AE. Benzimidazoles – with a strict monitoring to ensure optimal efficacy and avoid adverse events – are still the only antiparasitic agents available. For CE as well as AE, there is a need to find new antiparasitic compounds and evaluate therapeutic strategies.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmadinejad M, Hashemi M, Azizallahi N (2020) Evaluation of prognostic factors associated with postoperative complications following pulmonary hydatid cyst surgery. Open Respir Med J 14:16–21. https://doi.org/10.2174/1874306402014010016
Aji T, Dong J-H, Shao Y-M, Zhao J-M, Li T, Tuxun T, Shalayiadang P, Ran B, Jiang T-M, Zhang R-Q, He Y-B, Huang J-F, Wen H (2018) Ex vivo liver resection and autotransplantation as alternative to allotransplantation for end-stage hepatic alveolar echinococcosis. J Hepatol 69:1037–1046. https://doi.org/10.1016/j.jhep.2018.07.006
Akhan O, Salik AE, Ciftci T, Akinci D, Islim F, Akpinar B (2017) Comparison of long-term results of percutaneous treatment techniques for hepatic cystic echinococcosis types 2 and 3b. AJR Am J Roentgenol 208:878–884. https://doi.org/10.2214/AJR.16.16131
Akhan O, Erdoğan E, Ciftci TT, Unal E, Karaağaoğlu E, Akinci D (2020) Comparison of the long-term results of puncture, aspiration, injection and re-aspiration (PAIR) and catheterization techniques for the percutaneous treatment of CE1 and CE3a liver hydatid cysts: a prospective randomized trial. Cardiovasc Intervent Radiol 43:1034–1040. https://doi.org/10.1007/s00270-020-02477-7
Alpay L, Lacin T, Atinkaya C, Kıral H, Demir M, Baysungur V, Okur E, Yalcınkaya I (2012) Video-assisted thoracoscopic removal of pulmonary hydatid cysts. Eur J Cardiothorac Surg 42:971–975. https://doi.org/10.1093/ejcts/ezs338
Al-Saeedi M, Khajeh E, Hoffmann K, Ghamarnejad O, Stojkovic M, Weber TF, Golriz M, Strobel O, Junghanss T, Büchler MW, Mehrabi A (2019) Standardized endocystectomy technique for surgical treatment of uncomplicated hepatic cystic echinococcosis. PLoS Negl Trop Dis 13:e0007516. https://doi.org/10.1371/journal.pntd.0007516
Al-Saeedi M, Ramouz A, Khajeh E, El Rafidi A, Ghamarnejad O, Shafiei S, Ali-Hasan-Al-Saegh S, Probst P, Stojkovic M, Weber TF, Hoffmann K, Mehrabi A (2021) Endocystectomy as a conservative surgical treatment for hepatic cystic echinococcosis: A systematic review with single-arm meta-analysis. PLoS Negl Trop Dis 12;15(5):e0009365. https://doi.org/10.1371/journal.pntd.0009365. PMID: 33979343; PMCID: PMC8143402
Alvarez Rojas CA, Romig T, Lightowlers MW (2014) Echinococcus granulosus sensu lato genotypes infecting humans – review of current knowledge. Int J Parasitol 44:9–18. https://doi.org/10.1016/j.ijpara.2013.08.008
Ambregna S, Koch S, Sulz MC, Grüner B, Öztürk S, Chevaux J-B, Sulima M, de Gottardi A, Napoléon B, Abergel A, Bichard P, Boytchev I, Deprez P, Dumortier J, Frossard J-L, Kull E, Meny B, Moradpour D, Prat F, Vanbiervliet G, Thevenot T, Vuitton DA, Bresson-Hadni S, Vuitton L (2017) A European survey of perendoscopic treatment of biliary complications in patients with alveolar echinococcosis. Expert Rev Anti-Infect Ther 15:79–88. https://doi.org/10.1080/14787210.2017.1252260
Ammann RW (1991) Improvement of liver resectional therapy by adjuvant chemotherapy in alveolar hydatid disease. Swiss Echinococcosis Study Group (SESG). Parasitol Res 77:290–293
Ammann RW, Ilitsch N, Marincek B, Freiburghaus AU (1994) Effect of chemotherapy on the larval mass and the long-term course of alveolar echinococcosis. Swiss Echinococcosis Study Group. Hepatology 19:735–742
Ammann RW, Fleiner-Hoffmann A, Grimm F, Eckert J (1998) Long-term mebendazole therapy may be parasitocidal in alveolar echinococcosis. J Hepatol 29:994–998
Aydin U, Yazici P, Onen Z, Ozsoy M, Zeytunlu M, Kiliç M, Coker A (2008) The optimal treatment of hydatid cyst of the liver: radical surgery with a significant reduced risk of recurrence. Turk J Gastroenterol 19:33–39
Aydin Y, Ogul H, Turkyilmaz A, Eroglu A (2012) Surgical treatment of mediastinal cysts: report on 29 cases. Acta Chir Belg 112:281–286
Ayifuhan A, Tuerganaili A, Jun C, Ying-Mei S, Xiang-Wei L, Hao W (2012) Surgical treatment for hepatic alveolar echinococcosis: report of 50 cases. Hepato-Gastroenterology 59:790–793. https://doi.org/10.5754/hge10545
Azizi A, Blagosklonov O, Lounis A, Berthet L, Vuitton D-A, Bresson-Hadni S, Delabrousse E (2015) Alveolar echinococcosis: correlation between hepatic MRI findings and FDG-PET/CT metabolic activity. Abdom Imaging 40:56–63. https://doi.org/10.1007/s00261-014-0183-0
Bardonnet K, Vuitton DA, Grenouillet F, Mantion GA, Delabrousse E, Blagosklonov O, Miguet J-P, Bresson-Hadni S (2013) 30-yr course and favorable outcome of alveolar echinococcosis despite multiple metastatic organ involvement in a non-immune suppressed patient. Ann Clin Microbiol Antimicrob 12:1. https://doi.org/10.1186/1476-0711-12-1
Barnes TS, Deplazes P, Gottstein B, Jenkins DJ, Mathis A, Siles-Lucas M, Torgerson PR, Ziadinov I, Heath DD (2012) Challenges for diagnosis and control of cystic hydatid disease. Acta Trop 123:1–7. https://doi.org/10.1016/j.actatropica.2012.02.066
Bartholomot G, Vuitton DA, Harraga S, Shi DZ, Giraudoux P, Barnish G, Wang YH, MacPherson CNL, Craig PS (2002) Combined ultrasound and serologic screening for hepatic alveolar echinococcosis in Central China. Am J Trop Med Hyg 66:23–29
Basmaciyan L, Burlet B, Ramla S, Blot M, Mahy S, Aubriot-Lorton M-H, Valot S, Grelat M, Sautour M, Grenouillet F, Knapp J, Millon L, Piroth L, Martin L, Dalle F (2018) First case of human primary vertebral cystic echinococcosis due to Echinococcus Ortleppi. J Clin Med 7:E443. https://doi.org/10.3390/jcm7110443
Bayrak M, Altıntas Y (2019) Current approaches in the surgical treatment of liver hydatid disease: single center experience. BMC Surg 19:95. https://doi.org/10.1186/s12893-019-0553-1
Bektasoglu HK, Hasbahceci M, Tasci Y, Aydogdu I, Malya FU, Kunduz E, Dolay K (2019) Comparison of laparoscopic and conventional Cystotomy/partial cystectomy in treatment of liver Hydatidosis. Biomed Res Int 2019:1212404. https://doi.org/10.1155/2019/1212404
Beldi G, Vuitton D, Lachenmayer A, Heyd B, Dufour J-F, Richou C, Candinas D, Bresson-Hadni S (2019) Is ex vivo liver resection and autotransplantation a valid alternative treatment for end-stage hepatic alveolar echinococcosis in Europe? J Hepatol 70:1030–1031. https://doi.org/10.1016/j.jhep.2018.12.011
Bellanger A-P, Courquet S, Pallandre J-R, Godet Y, Millon L (2020) Echinococcus multilocularis vesicular fluid induces the expression of immune checkpoint proteins in vitro. Parasite Immunol 42:e12711. https://doi.org/10.1111/pim.12711
Bellanger AP, Achour K, Barkati S, Bastid C, Bresson-Hadni S, Delaere B, Dziri C, Gottstein B, Kachani M, Mantion G, Umhang G, Wallon M, Vuitton DA (2021a) Terminologie à utiliser pour l’étude et la prise en charge des échinococcoses : adaptation du consensus international à la langue française. Bull Acad Natl Med 205:1028–1059. https://doi.org/10.1016/j.banm.2021.06.016
Bellanger A-P, Wang J, Gbaguidi-Haore H, Barrera C, Bresson-Hadni S, Zlobec I, Lachenmayer A, Richou C, Turco C, Gottstein B, Millon L, Beldi G (2021b) Investigating new serological and tissue markers for the follow-up of patients operated for alveolar echinococcosis. Parasite Immunol 43:e12827. https://doi.org/10.1111/pim.12827
Ben Amor N, Gargouri M, Gharbi HA, Golvan YJ, Ayachi K, Kchouck H (1986) Trial therapy of inoperable abdominal hydatid cysts by puncture. Ann Parasitol Hum Comp 61:689–692
Ben Salah E, Barrera C, Sakly W, Mosbahi S, Balliau T, Franche N, Gottstein B, Ben Youssef S, Mekki M, Babba H, Millon L (2022) Novel biomarkers for the early prediction of pediatric cystic echinococcosis post-surgical outcomes. J Infect 84:87–93. https://doi.org/10.1016/j.jinf.2021.09.023
Bosco A, Alves LC, Cociancic P, Amadesi A, Pepe P, Morgoglione ME, Maurelli MP, Ferrer-Miranda E, Santoro KR, Nascimento Ramos RA, Rinaldi L, Cringoli G (2021) Epidemiology and spatial distribution of Echinococcus granulosus in sheep and goats slaughtered in a hyperendemic European Mediterranean area. Parasit Vectors 14:421. https://doi.org/10.1186/s13071-021-04934-9
Böttcher D, Bangoura B, Schmäschke R, Müller K, Fischer S, Vobis V, Meiler H, Wolf G, Koller A, Kramer S, Overhoff M, Gawlowska S, Schoon H-A (2013) Diagnostics and epidemiology of alveolar echinococcosis in slaughtered pigs from large-scale husbandries in Germany. Parasitol Res 112:629–636. https://doi.org/10.1007/s00436-012-3177-2
Boubaker G, Macchiaroli N, Prada L, Cucher MA, Rosenzvit MC, Ziadinov I, Deplazes P, Saarma U, Babba H, Gottstein B, Spiliotis M (2013) A multiplex PCR for the simultaneous detection and genotyping of the Echinococcus granulosus complex. PLoS Negl Trop Dis 7:e2017. https://doi.org/10.1371/journal.pntd.0002017
Bresson-Hadni S, Vuitton DA, Lenys D, Liance M, Racadot E, Miguet JP (1989) Cellular immune response in Echinococcus multilocularis infection in humans. I. Lymphocyte reactivity to Echinococcus antigens in patients with alveolar echinococcosis. Clin Exp Immunol 78:61–66
Bresson-Hadni S, Vuitton DA, Bartholomot B, Heyd B, Godart D, Meyer JP, Hrusovsky S, Becker MC, Mantion G, Lenys D, Miguet JP (2000) A twenty-year history of alveolar echinococcosis: analysis of a series of 117 patients from eastern France. Eur J Gastroenterol Hepatol 12:327–336
Bresson-Hadni S, Delabrousse E, Blagosklonov O, Bartholomot B, Koch S, Miguet J-P, Mantion GA, Vuitton DA (2006) Imaging aspects and non-surgical interventional treatment in human alveolar echinococcosis. Parasitol Int 55(Suppl):S267–S272. https://doi.org/10.1016/j.parint.2005.11.053
Bresson-Hadni S, Blagosklonov O, Knapp J, Grenouillet F, Sako Y, Delabrousse E, Brientini M-P, Richou C, Minello A, Antonino A-T, Gillet M, Ito A, Mantion GA, Vuitton DA (2011) Should possible recurrence of disease contraindicate liver transplantation in patients with end-stage alveolar echinococcosis? A 20-year follow-up study. Liver Transpl 17:855–865. https://doi.org/10.1002/lt.22299
Bresson-Hadni S, Montange D, Richou C, Brumpt E, Fillion A, Bartholomot B, Blagosklonov O, Delabrousse E, Grenouillet F, Vuitton D-A, Millon L (2021a) Tobacco, cannabis, and liquorice: hidden players altering albendazole metabolism in patients with hepatic alveolar echinococcosis. J Hepatol 74:471–473. https://doi.org/10.1016/j.jhep.2020.10.032
Bresson-Hadni S, Spahr L, Chappuis F (2021b) Hepatic alveolar echinococcosis. Semin Liver Dis 41:393–408. https://doi.org/10.1055/s-0041-1730925
Brumpt E, Blagosklonov O, Calame P, Bresson-Hadni S, Vuitton DA, Delabrousse E (2019) AE hepatic lesions: correlation between calcifications at CT and FDG-PET/CT metabolic activity. Infection 47:955–960. https://doi.org/10.1007/s15010-019-01328-z
Brundu D, Piseddu T, Stegel G, Masu G, Ledda S, Masala G (2014) Retrospective study of human cystic echinococcosis in Italy based on the analysis of hospital discharge records between 2001 and 2012. Acta Trop 140:91–96. https://doi.org/10.1016/j.actatropica.2014.08.011
Brunetti E, Kern P, Vuitton DA, Writing Panel for the WHO-IWGE (2010) Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 114:1–16. https://doi.org/10.1016/j.actatropica.2009.11.001
Brunetti E, Garcia HH, Junghanss T, International CE Workshop in Lima, Peru, 2009 (2011) Cystic echinococcosis: chronic, complex, and still neglected. PLoS Negl Trop Dis 5:e1146. https://doi.org/10.1371/journal.pntd.0001146
Budke CM, Deplazes P, Torgerson PR (2006) Global socioeconomic impact of cystic echinococcosis. Emerg Infect Dis 12:296–303. https://doi.org/10.3201/eid1202.050499
Buttenschoen K, Carli Buttenschoen D, Gruener B, Kern P, Beger HG, Henne-Bruns D, Reuter S (2009a) Long-term experience on surgical treatment of alveolar echinococcosis. Langenbeck’s Arch Surg / Deutsche Gesellschaft Für Chirurgie 394:689–698. https://doi.org/10.1007/s00423-008-0392-5
Buttenschoen K, Gruener B, Carli Buttenschoen D, Reuter S, Henne-Bruns D, Kern P (2009b) Palliative operation for the treatment of alveolar echinococcosis. Langenbeck’s Arch Surg 394:199–204. https://doi.org/10.1007/s00423-008-0367-6
Cai H, Zhang J, Zhang X, Guan Y, Ma X, Cao J, Ma J, Liu N, Wu H, Liu Y, Liu J, Wang W, Lei W, Shi K, Zhang Q, Zhang X, Zhan P, Shen Y (2021) Prevalence of Echinococcus species in wild foxes and stray dogs in Qinghai Province, China. Am J Trop Med Hyg:tpmd210622. https://doi.org/10.4269/ajtmh.21-0622
Caoduro C, Porot C, Vuitton DA, Bresson-Hadni S, Grenouillet F, Richou C, Boulahdour H, Blagosklonov O (2013) The role of delayed 18F-FDG PET imaging in the follow-up of patients with alveolar echinococcosis. J Nucl Med 54:358–363. https://doi.org/10.2967/jnumed.112.109942
Casulli A, Siles-Lucas M, Cretu CM, Vutova K, Akhan O, Vural G, Cortés Ruiz A, Brunetti E, Tamarozzi F (2020) Achievements of the HERACLES project on cystic echinococcosis. Trends Parasitol 36:1–4. https://doi.org/10.1016/j.pt.2019.10.009
Catalano S, Lejeune M, Liccioli S, Verocai GG, Gesy KM, Jenkins EJ, Kutz SJ, Fuentealba C, Duignan PJ, Massolo A (2012) Echinococcus multilocularis in urban coyotes, Alberta, Canada. Emerg Infect Dis 18:1625–1628. https://doi.org/10.3201/eid.1810.120119
Cattaneo L, Manciulli T, Cretu C-M, Giordani MT, Angheben A, Bartoloni A, Zammarchi L, Bartalesi F, Richter J, Chiodini P, Godbole G, Junghanss T, Stojkovic M, Sammarchi L, Dore R, Vercelli A, Benazzo F, Cuzzocrea F, Tamarozzi F, Brunetti E (2019) Cystic echinococcosis of the bone: a European Multicenter study. Am J Trop Med Hyg 100:617–621. https://doi.org/10.4269/ajtmh.18-0758
Ceballos L, Elissondo C, Sánchez Bruni S, Confalonieri A, Denegri G, Alvarez L, Lanusse C (2010) Chemoprophylactic activity of flubendazole in cystic echinococcosis. Chemotherapy 56:386–392. https://doi.org/10.1159/000316827
Ceballos L, Elissondo C, Sánchez Bruni S, Denegri G, Lanusse C, Alvarez L (2011) Comparative performances of flubendazole and albendazole in cystic echinococcosis: ex vivo activity, plasma/cyst disposition, and efficacy in infected mice. Antimicrob Agents Chemother 55:5861–5867. https://doi.org/10.1128/AAC.05105-11
Ceballos L, Virkel G, Elissondo C, Canton C, Canevari J, Murno G, Denegri G, Lanusse C, Alvarez L (2013) A pharmacology-based comparison of the activity of albendazole and flubendazole against Echinococcus granulosus metacestode in sheep. Acta Trop 127:216–225. https://doi.org/10.1016/j.actatropica.2013.05.004
Chauchet A, Grenouillet F, Knapp J, Richou C, Delabrousse E, Dentan C, Millon L, Di Martino V, Contreras R, Deconinck E, Blagosklonov O, Vuitton DA, Bresson-Hadni S, FrancEchino Network (2014) Increased incidence and characteristics of alveolar echinococcosis in patients with immunosuppression-associated conditions. Clin Infect Dis 59:1095–1104. https://doi.org/10.1093/cid/ciu520
Chen X, Chen X, Shao Y, Zhao J, Li H, Wen H (2014) Clinical outcome and immune follow-up of different surgical approaches for human cyst hydatid disease in liver. Am J Trop Med Hyg 91:801–805. https://doi.org/10.4269/ajtmh.14-0177
Chen J, Wei L, Chen T-W, Li R, Zhang X-M, Deng C-M, Zhang Y, Xiong J, Li X-Z, Li Z-H (2021) Triphase contrast-enhanced CT to evaluate indications for autologous liver transplantation in patients with end-stage hepatic alveolar echinococcosis. Sci Rep 11:22096. https://doi.org/10.1038/s41598-021-01586-8
Colpani A, Achilova O, D’Alessandro GL, Budke CM, Mariconti M, Muratov T, Vola A, Mamedov A, Giordani MT, Urukov X, De Silvestri A, Suvonkulov U, Brunetti E, Manciulli T (2021) Trends in the surgical incidence of cystic echinococcosis in Uzbekistan from 2011 to 2018. Am J Trop Med Hyg:tpmd210261. https://doi.org/10.4269/ajtmh.21-0261
Comte S, Raton V, Raoul F, Hegglin D, Giraudoux P, Deplazes P, Favier S, Gottschek D, Umhang G, Boué F, Combes B (2013) Fox baiting against Echinococcus multilocularis: contrasted achievements among two medium size cities. Prev Vet Med 111:147–155. https://doi.org/10.1016/j.prevetmed.2013.03.016
Comte S, Umhang G, Raton V, Raoul F, Giraudoux P, Combes B, Boué F (2017) Echinococcus multilocularis management by fox culling: an inappropriate paradigm. Prev Vet Med 147:178–185. https://doi.org/10.1016/j.prevetmed.2017.09.010
Conraths FJ, Deplazes P (2015) Echinococcus multilocularis: epidemiology, surveillance and state-of-the-art diagnostics from a veterinary public health perspective. Vet Parasitol 213:149–161. https://doi.org/10.1016/j.vetpar.2015.07.027
Cooney RM, Flanagan KP, Zehyle E (2004) Review of surgical management of cystic hydatid disease in a resource limited setting: Turkana, Kenya. Eur J Gastroenterol Hepatol 16:1233–1236. https://doi.org/10.1097/00042737-200411000-00024
Craig PS, Echinococcosis Working Group in China (2006) Epidemiology of human alveolar echinococcosis in China. Parasitol Int 55(Suppl):S221–S225. https://doi.org/10.1016/j.parint.2005.11.034
Craig P, Mastin A, van Kesteren F, Boufana B (2015) Echinococcus granulosus: epidemiology and state-of-the-art of diagnostics in animals. Vet Parasitol 213:132–148. https://doi.org/10.1016/j.vetpar.2015.07.028
Craig PS, Hegglin D, Lightowlers MW, Torgerson PR, Wang Q (2017) Echinococcosis: control and prevention. Adv Parasitol 96:55–158. https://doi.org/10.1016/bs.apar.2016.09.002
Crouzet J, Grenouillet F, Delabrousse E, Blagosklonov O, Thevenot T, Di Martino V, Piarroux R, Mantion GA, Bresson-Hadni S (2010) Personalized management of patients with inoperable alveolar echinococcosis undergoing treatment with albendazole: usefulness of positron-emission-tomography combined with serological and computed tomography follow-up. Clin Microbiol Infect 16:788–791. https://doi.org/10.1111/j.1469-0691.2009.02924.x
D’Alessandro A, Rausch RL (2008) New aspects of neotropical polycystic (Echinococcus vogeli) and unicystic (Echinococcus oligarthrus) echinococcosis. Clin Microbiol Rev 21:380–401. https://doi.org/10.1128/CMR.00050-07, table of contents
da Silva AM (2019) Hydatid cyst/cystic echinococcosis: anatomical and surgical nomenclature and method to quantify the cyst content solidification. - PubMed - NCBI. https://www-ncbi-nlm-nih-gov.gate2.inist.fr/pubmed/22040484. Accessed 9 Aug 2019
Da Silva AM, Courquet S, Raoul F, Rieffel D, Giraudoux P, Millon L, Knapp J (2020) Assessment of the exposure to Echinococcus multilocularis associated with carnivore faeces using real-time quantitative PCR and flotation technique assays. Int J Parasitol 50:1195–1204. https://doi.org/10.1016/j.ijpara.2020.07.008
Deininger S, Wellinghausen N (2019) Evaluation of a new combined Western and line blot assay (EUROLINE-WB) for diagnosis and species identification of Echinococcus infection in humans. GMS Infect Dis 7:Doc01. https://doi.org/10.3205/id000041
Demir H, Halac M, Yilmaz S, Isgoren S, Sonmezoglu K, Uslu I (2008) A doughnut sign of a hydatid cyst of the liver on F-18 FDG PET/CT. Clin Nucl Med 33:876–877. https://doi.org/10.1097/RLU.0b013e31818bf2df
Deplazes P, Eckert J (2001) Veterinary aspects of alveolar echinococcosis – a zoonosis of public health significance. In: Veterinary parasitology, pp 65–87
Deplazes P, Hegglin D, Gloor S, Romig T (2004a) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol 20:77–84
Deplazes P, Hegglin D, Gloor S, Romig T (2004b) Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol 20:77–84
Deplazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J, Thompson RCA, Jenkins EJ (2017) Global distribution of alveolar and cystic echinococcosis. Adv Parasitol 95:315–493. https://doi.org/10.1016/bs.apar.2016.11.001
Duishanbai S, Geng D, Liu C, Guo H-R, Hao Y-J, Liu B, Wang Y-X, Luo K, Zhou K, Wen H, Research Group of Hydatid Diseases (2011) Treatment of intracranial hydatid cysts. Chin Med J 124:2954–2958
Dybicz M, Gierczak A, Dąbrowska J, Rdzanek Ł, Michałowicz B (2013) Molecular diagnosis of cystic echinococcosis in humans from Central Poland. Parasitol Int 62:364–367. https://doi.org/10.1016/j.parint.2013.03.005
Dziri C, Haouet K, Fingerhut A, Zaouche A (2009) Management of cystic echinococcosis complications and dissemination: where is the evidence? World J Surg 33:1266–1273. https://doi.org/10.1007/s00268-009-9982-9
Echinococcosis W-IWG on (2001) PAIR: puncture, aspiration, injection, reaspiration: an option for the treatment of cystic echinococcosis. WHO, Geneva
Eckert J, Deplazes P (2004) Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 17:107–135
Eckert J, Thompson RCA (2017) Historical aspects of echinococcosis. Adv Parasitol 95:1–64. https://doi.org/10.1016/bs.apar.2016.07.003
Eckert J, Deplazes P, Craig PS, Gemmell M, Gottstein B, Heath D, Jenkins D, Kamiya M, Lightowlers M (2001) Echinococcosis in animals: clinical aspects, diagnosis and treatment. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (eds) WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. World Organization for Animal Health (OIE), Paris, pp 72–99
Ehrhardt AR, Reuter S, Buck AK, Haenle MM, Mason RA, Gabelmann A, Kern P, Kratzer W (2007) Assessment of disease activity in alveolar echinococcosis: a comparison of contrast enhanced ultrasound, three-phase helical CT and [(18)F] fluorodeoxyglucose positron emission tomography. Abdom Imaging 32:730–736. https://doi.org/10.1007/s00261-006-9173-1
Feng X, Wen H, Zhang Z, Chen X, Ma X, Zhang J, Qi X, Bradshaw H, Vuitton D, Craig PS (2010) Dot immunogold filtration assay (DIGFA) with multiple native antigens for rapid serodiagnosis of human cystic and alveolar echinococcosis. Acta Trop 113:114–120. https://doi.org/10.1016/j.actatropica.2009.10.003
Fica A, Soto A, Slater J, Peralta M, Humeres R, Castro M, González J, Weitzel T (2012) Clinical presentation of hydatid disease during 15 years: a case series from Santiago, Chile. Rev Chil Infectol 29:183–191. https://doi.org/10.4067/S0716-10182012000200011
Firpo G, Vola A, Lissandrin R, Tamarozzi F, Brunetti E (2017) Preliminary evaluation of percutaneous treatment of Echinococcal cysts without injection of Scolicidal agent. Am J Trop Med Hyg 97:1818–1826. https://doi.org/10.4269/ajtmh.17-0468
Franchi C, Di Vico B, Teggi A (1999) Long-term evaluation of patients with hydatidosis treated with benzimidazole carbamates. Clin Infect Dis 29:304–309. https://doi.org/10.1086/520205
Frider B, Larrieu E, Odriozola M (1999) Long-term outcome of asymptomatic liver hydatidosis. J Hepatol 30:228–231
Gargouri M, Ben Amor N, Ben Chehida F, Hammou A, Gharbi HA, Ben Cheikh M, Kchouk H, Ayachi K, Golvan JY (1990) Percutaneous treatment of hydatid cysts (Echinococcus granulosus). Cardiovasc Intervent Radiol 13:169–173
Gemmell MA, Johnstone PD, Oudemans G (1977) The effect of praziquantel on Echinococcus granulosus, Taenia hydatigena and Taenia ovis infections in dogs. Res Vet Sci 23:121–123
Georges S, Villard O, Filisetti D, Mathis A, Marcellin L, Hansmann Y, Candolfi E (2004) Usefulness of PCR analysis for diagnosis of alveolar echinococcosis with unusual localizations: two case studies. J Clin Microbiol 42:5954–5956. https://doi.org/10.1128/JCM.42.12.5954-5956.2004
Gharbi HA, Hassine W, Brauner MW, Dupuch K (1981) Ultrasound examination of the hydatic liver. Radiology 139:459–463. https://doi.org/10.1148/radiology.139.2.7220891
Ghoshal AG, Sarkar S, Saha K, Sarkar U, Kundu S, Chatterjee S, Kundu S (2012) Hydatid lung disease: an analysis of five years cumulative data from Kolkata. J Assoc Physicians India 60:12–16
Giraudoux P, Craig PS, Delattre P, Bao G, Bartholomot B, Harraga S, Quéré JP, Raoul F, Wang Y, Shi D, Vuitton DA (2003) Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127(Suppl):S121–S131
Giraudoux P, Raoul F, Afonso E, Ziadinov I, Yang Y, Li L, Li T, Quéré J-P, Feng X, Wang Q, Wen H, Ito A, Craig PS (2013) Transmission ecosystems of Echinococcus multilocularis in China and Central Asia. Parasitology 140:1655–1666. https://doi.org/10.1017/S0031182013000644
Giraudoux P, Zhao Y, Afonso E, Yan H, Knapp J, Rogan MT, Shi D, Jia W, Craig PS (2019) Long-term retrospective assessment of a transmission hotspot for human alveolar echinococcosis in mid-West China. PLoS Negl Trop Dis 13:e0007701. https://doi.org/10.1371/journal.pntd.0007701
Godot V, Harraga S, Podoprigora G, Liance M, Bardonnet K, Vuitton DA (2003) IFN alpha-2a protects mice against a helminth infection of the liver and modulates immune responses. Gastroenterology 124:1441–1450
Gottstein B, Wang J, Blagosklonov O, Grenouillet F, Millon L, Vuitton DA, Müller N (2014) Echinococcus metacestode: in search of viability markers. Parasite 21:63. https://doi.org/10.1051/parasite/2014063
Gottstein B, Lachenmayer A, Beldi G, Wang J, Merkle B, Vu XL, Kurath U, Müller N (2019) Diagnostic and follow-up performance of serological tests for different forms/courses of alveolar echinococcosis. Food Waterborne Parasitol 16:e00055. https://doi.org/10.1016/j.fawpar.2019.e00055
Graeter T, Kratzer W, Oeztuerk S, Haenle MM, Mason RA, Hillenbrand A, Kull T, Barth TF, Kern P, Gruener B (2016) Proposal of a computed tomography classification for hepatic alveolar echinococcosis. World J Gastroenterol 22:3621–3631. https://doi.org/10.3748/wjg.v22.i13.3621
Graeter T, Bao H, Delabrousse E, Brumpt E, Shi R, Li W, Jiang Y, Schmidberger J, Kratzer W, Liu W, XUUB consortium (2020) Hepatic alveolar echinococcosis: comparative computed tomography study between two Chinese and two European centres. Food Waterborne Parasitol 19:e00082. https://doi.org/10.1016/j.fawpar.2020.e00082
Grenard P, Bresson-Hadni S, El Alaoui S, Chevallier M, Vuitton DA, Ricard-Blum S (2001) Transglutaminase-mediated cross-linking is involved in the stabilization of extracellular matrix in human liver fibrosis. J Hepatol 35:367–375. https://doi.org/10.1016/s0168-8278(01)00135-0
Grenouillet F, Frider B, Alvarez Rodriguez J, Amante M, Pestalardo ML, Cazorla A, Bresson-Hadni S, Millon L (2013) Molecular diagnosis of polycystic echinococcosis due to Echinococcus vogeli in a Paraguayan immigrant in Argentina. J Clin Microbiol 51:3151–3153. https://doi.org/10.1128/JCM.00871-13
Grenouillet F, Umhang G, Arbez-Gindre F, Mantion G, Delabrousse E, Millon L, Boué F (2014) Echinococcus ortleppi infections in humans and cattle, France. Emerg Infect Dis 20:2100–2102. https://doi.org/10.3201/eid2012.140641
Gruener B, Cretu C, Brunetti E, Menezes C, Haerter G, Grobusch M, Kern P (2008) Accelerated larval growth of Echinococcus spp in the immunodeficient host? Am J Trop Med Hyg 79:118
Guo B, Zhang Z, Guo Y, Guo G, Wang H, Ma J, Chen R, Zheng X, Bao J, He L, Wang T, Qi W, Tian M, Wang J, Zhou C, Giraudoux P, Marston CG, McManus DP, Zhang W, Li J (2021) High endemicity of alveolar echinococcosis in Yili prefecture, Xinjiang autonomous region, the People’s Republic of China: infection status in different ethnic communities and in small mammals. PLoS Negl Trop Dis 15:e0008891. https://doi.org/10.1371/journal.pntd.0008891
Harraga S, Godot V, Bresson-Hadni S, Pater C, Beurton I, Bartholomot B, Vuitton DA (1999) Clinical efficacy of and switch from T helper 2 to T helper 1 cytokine profile after interferon alpha2a monotherapy for human echinococcosis. Clin Infect Dis 29:205–206. https://doi.org/10.1086/520157
Haskologlu S, Dogu F, Gollu Bahadır G, Akyuzluer S, Ciftci E, Altun D, Keles S, Kologlu M, Ikinciogullari A (2020) An unexpected infection in loss-of-function mutations in STAT3: malignant alveolar echinococcosis in liver. Iran J Allergy Asthma Immunol 19:667–675. https://doi.org/10.18502/ijaai.v19i6.4936
He Y-B, Bai L, Jiang Y, Ji X-W, Tai Q-W, Zhao J-M, Zhang J-H, Liu W-Y, Wen H (2015) Application of a three-dimensional reconstruction technique in liver autotransplantation for end-stage hepatic alveolar echinococcosis. J Gastrointest Surg 19:1457–1465. https://doi.org/10.1007/s11605-015-2842-z
Hemphill A, Spicher M, Stadelmann B, Mueller J, Naguleswaran A, Gottstein B, Walker M (2007) Innovative chemotherapeutical treatment options for alveolar and cystic echinococcosis. Parasitology 134:1657–1670. https://doi.org/10.1017/S0031182007003198
Hemphill A, Stadelmann B, Rufener R, Spiliotis M, Boubaker G, Müller J, Müller N, Gorgas D, Gottstein B (2014) Treatment of echinococcosis: albendazole and mebendazole – what else? Parasite 21:70. https://doi.org/10.1051/parasite/2014073
Herzig M, Maksimov P, Staubach C, Romig T, Knapp J, Gottstein B, Conraths FJ (2021) Red foxes harbor two genetically distinct, spatially separated Echinococcus multilocularis clusters in Brandenburg, Germany. Parasit Vectors 14:535. https://doi.org/10.1186/s13071-021-05038-0
Hira PR, Shweiki H, Lindberg LG, Shaheen Y, Francis I, Leven H, Behbehani K (1988) Diagnosis of cystic hydatid disease: role of aspiration cytology. Lancet 2:655–657. https://doi.org/10.1016/s0140-6736(88)90470-9
Horton J (2003) Albendazole for the treatment of echinococcosis. Fundam Clin Pharmacol 17:205–212
Hosch W, Junghanss T, Stojkovic M, Brunetti E, Heye T, Kauffmann GW, Hull WE (2008) Metabolic viability assessment of cystic echinococcosis using high-field 1H MRS of cyst contents. NMR Biomed 21:734–754. https://doi.org/10.1002/nbm.1252
Huang L, Huang Y, Wang Q, Xiao N, Yi D, Yu W, Qiu D (2011) An agent-based model for control strategies of Echinococcus granulosus. Vet Parasitol 179:84–91. https://doi.org/10.1016/j.vetpar.2011.01.047
Hüttner M, Nakao M, Wassermann T, Siefert L, Boomker JDF, Dinkel A, Sako Y, Mackenstedt U, Romig T, Ito A (2008) Genetic characterization and phylogenetic position of Echinococcus felidis (Cestoda: Taeniidae) from the African lion. Int J Parasitol 38:861–868. https://doi.org/10.1016/j.ijpara.2007.10.013
Hwang R, Liou P, Kato T (2018) Ex vivo liver resection and autotransplantation: an emerging option in selected indications. J Hepatol 69:1002–1003. https://doi.org/10.1016/j.jhep.2018.09.005
Ishizu H, Uchino J, Sato N, Aoki S, Suzuki K, Kuribayashi H (1997) Effect of albendazole on recurrent and residual alveolar echinococcosis of the liver after surgery. Hepatology 25:528–531. https://doi.org/10.1002/hep.510250305
Ito A, Craig PS (2003) Immunodiagnostic and molecular approaches for the detection of taeniid cestode infections. Trends Parasitol 19:377–381. https://doi.org/10.1016/s1471-4922(03)00200-9
Jebbawi F, Bellanger A-P, Lunström-Stadelmann B, Rufener R, Dosch M, Goepfert C, Gottstein B, Millon L, Grandgirard D, Leib SL, Beldi G, Wang J (2021) Innate and adaptive immune responses following PD-L1 blockade in treating chronic murine alveolar echinococcosis. Parasite Immunol 43:e12834. https://doi.org/10.1111/pim.12834
Jerraya H, Khalfallah M, Osman SB, Nouira R, Dziri C (2015) Predictive factors of recurrence after surgical treatment for liver hydatid cyst. Surg Endosc 29:86–93. https://doi.org/10.1007/s00464-014-3637-0
Johansen MV, Penrith M-L (2009) Has culling been properly assessed as a valid and justified control intervention measure for zoonotic diseases? PLoS Negl Trop Dis 3:e541. https://doi.org/10.1371/journal.pntd.0000541
Julien C, Le Treut YP, Bourgouin S, Palen A, Hardwigsen J (2021) Closed cyst resection for liver hydatid disease: a new standard. J Gastrointest Surg 25:436–446. https://doi.org/10.1007/s11605-019-04509-1
Junghanss T, da Silva AM, Horton J, Chiodini PL, Brunetti E (2008) Clinical management of cystic echinococcosis: state of the art, problems, and perspectives. Am J Trop Med Hyg 79:301–311
Kadry Z, Renner EC, Bachmann LM, Attigah N, Renner EL, Ammann RW, Clavien P-A (2005) Evaluation of treatment and long-term follow-up in patients with hepatic alveolar echinococcosis. Br J Surg 92:1110–1116. https://doi.org/10.1002/bjs.4998
Kantarci M, Bayraktutan U, Karabulut N, Aydinli B, Ogul H, Yuce I, Calik M, Eren S, Atamanalp SS, Oto A (2012) Alveolar echinococcosis: spectrum of findings at cross-sectional imaging. Radiographics 32:2053–2070. https://doi.org/10.1148/rg.327125708
Karpstein T, Chaudhry S, Bresson-Hadni S, Hayoz M, Boubaker G, Hemphill A, Rufener R, Kaethner M, Schindler I, Aebi Y, Cunha AS, Largiadèr CR, Lundström-Stadelmann B (2021) Maca against echinococcosis?-a reverse approach from patient to in vitro testing. Pathogens 10:1335. https://doi.org/10.3390/pathogens10101335
Kern P (2006) Medical treatment of echinococcosis under the guidance of good clinical practice (GCP/ICH). Parasitol Int 55(Suppl):S273–S282. https://doi.org/10.1016/j.parint.2005.11.040
Kern P, Wen H, Sato N, Vuitton DA, Gruener B, Shao Y, Delabrousse E, Kratzer W, Bresson-Hadni S (2006) WHO classification of alveolar echinococcosis: principles and application. Parasitol Int 55(Suppl):S283–S287. https://doi.org/10.1016/j.parint.2005.11.041
Kern PA, Abboud P, Kern W, Stich A, Bresson-Hadni S, Guérin B (2008) Critical appraisal of nitazoxanide for the treatment of alveolar echinococcosis. Am J Trop Med Hyg 79(6):125
Kern P, Menezes da Silva A, Akhan O, Müllhaupt B, Vizcaychipi KA, Budke C, Vuitton DA (2017) The Echinococcoses: diagnosis, clinical management and burden of disease. Adv Parasitol 96:259–369. https://doi.org/10.1016/bs.apar.2016.09.006
Kilic M, Yoldas O, Koc M, Keskek M, Karakose N, Ertan T, Gocmen E, Tez M (2008) Can biliary-cyst communication be predicted before surgery for hepatic hydatid disease: does size matter? Am J Surg 196:732–735. https://doi.org/10.1016/j.amjsurg.2007.07.034
Knapp J, Bart JM, Maillard S, Gottstein B, Piarroux R (2010) The genomic Echinococcus microsatellite EmsB sequences: from a molecular marker to the epidemiological tool. Parasitology 137:439–449. https://doi.org/10.1017/S0031182009991612
Knapp J, Millon L, Mouzon L, Umhang G, Raoul F, Ali ZS, Combes B, Comte S, Gbaguidi-Haore H, Grenouillet F, Giraudoux P (2014) Real time PCR to detect the environmental faecal contamination by Echinococcus multilocularis from red fox stools. Vet Parasitol 201:40–47. https://doi.org/10.1016/j.vetpar.2013.12.023
Knapp J, Giraudoux P, Combes B, Umhang G, Boué F, Said-Ali Z, Aknouche S, Garcia C, Vacheyrou M, Laboissière A, Raton V, Comte S, Favier S, Demerson J-M, Caillot C, Millon L, Raoul F (2018) Rural and urban distribution of wild and domestic carnivore stools in the context of Echinococcus multilocularis environmental exposure. Int J Parasitol 48:937–946. https://doi.org/10.1016/j.ijpara.2018.05.007
Knapp J, Gottstein B, Bretagne S, Bart J-M, Umhang G, Richou C, Bresson-Hadni S, Millon L (2020) Genotyping Echinococcus multilocularis in human alveolar echinococcosis patients: an EmsB microsatellite analysis. Pathogens 9:E282. https://doi.org/10.3390/pathogens9040282
Knapp J, Da Silva AM, Courquet S, Millon L (2021) Assessment of the genetic diversity of Echinococcus multilocularis from Copro-isolated eggs. Pathogens 10:1296. https://doi.org/10.3390/pathogens10101296
Knapp J, Lallemand S, Monnien F, Felix S, Valmary-Degano S, Courquet S, Demonmerot F, Heyd B, Turco C, Doussot A, Bourgeois L, Bresson-Hadni S, Richou C, Millon L (2022) Molecular diagnosis of alveolar echinococcosis in patients based on frozen and formalin-fixed paraffin-embedded tissue samples. Parasite 29:4. https://doi.org/10.1051/parasite/2022004. Epub 2022 Feb 2. PMID: 35113014; PMCID: PMC8812296
Koch S, Bresson-Hadni S, Miguet J-P, Crumbach J-P, Gillet M, Mantion G-A, Heyd B, Vuitton D-A, Minello A, Kurtz S, European Collaborating Clinicians (2003) Experience of liver transplantation for incurable alveolar echinococcosis: a 45-case European collaborative report. Transplantation 75:856–863. https://doi.org/10.1097/01.TP.0000054230.63568.79
Kratzer W, Gruener B, Kaltenbach TEM, Ansari-Bitzenberger S, Kern P, Fuchs M, Mason RA, Barth TFE, Haenle MM, Hillenbrand A, Oeztuerk S, Graeter T (2015) Proposal of an ultrasonographic classification for hepatic alveolar echinococcosis: echinococcosis multilocularis Ulm classification-ultrasound. World J Gastroenterol 21:12392–12402. https://doi.org/10.3748/wjg.v21.i43.12392
Kurt Y, Sücüllü I, Filiz AI, Urhan M, Akin ML (2008) Pulmonary echinococcosis mimicking multiple lung metastasis of breast cancer: the role of fluoro-deoxy-glucose positron emission tomography. World J Surg Oncol 6:7. https://doi.org/10.1186/1477-7819-6-7
La X, Zhang F, Li Y, Li J, Guo Y, Zhao H, Pang N, Ma X, Wen H, Fan H, Ding J (2015) Upregulation of PD-1 on CD4+CD25+ T cells is associated with immunosuppression in liver of mice infected with Echinococcus multilocularis. Int Immunopharmacol 26:357–366. https://doi.org/10.1016/j.intimp.2015.04.013
Lachenmayer A, Gebbers D, Gottstein B, Candinas D, Beldi G (2019) Elevated incidence of alveolar echinococcosis in immunocompromised patients. Food Waterborne Parasitol 16:e00060. https://doi.org/10.1016/j.fawpar.2019.e00060
Larrieu E, Uchiumi L, Salvitti JC, Sobrino M, Panomarenko O, Tissot H, Mercapide CH, Sustercic J, Arezo M, Mujica G, Herrero E, Labanchi JL, Grizmado C, Araya D, Talmon G, Galvan JM, Sepulveda L, Seleiman M, Cornejo T, Echenique H, Del Carpio M (2019) Epidemiology, diagnosis, treatment and follow-up of cystic echinococcosis in asymptomatic carriers. Trans R Soc Trop Med Hyg 113:74–80. https://doi.org/10.1093/trstmh/try112
Li J, Wu C, Wang H, Liu H, Vuitton DA, Wen H, Zhang W (2014) Boiling sheep liver or lung for 30 minutes is necessary and sufficient to kill Echinococcus granulosus protoscoleces in hydatid cysts. Parasite 21:64. https://doi.org/10.1051/parasite/2014064. Epub 2014 Dec 2. PMID: 25456565; PMCID: PMC4251422
Li Y-P, Ma Z-G, Tuxun T, Li Z-D, Meng Y, Chen X (2020) The application of laparoscopy combined with indocyanine green fluorescence imaging technique for hepatic cystic echinococcosis. BMC Surg 20:249. https://doi.org/10.1186/s12893-020-00911-8
Liance M, Janin V, Bresson-Hadni S, Vuitton DA, Houin R, Piarroux R (2000) Immunodiagnosis of Echinococcus infections: confirmatory testing and species differentiation by a new commercial Western Blot. J Clin Microbiol 38:3718–3721. https://doi.org/10.1128/JCM.38.10.3718-3721.2000
Liccioli S, Giraudoux P, Deplazes P, Massolo A (2015) Wilderness in the “city” revisited: different urbes shape transmission of Echinococcus multilocularis by altering predator and prey communities. Trends Parasitol 31:297–305. https://doi.org/10.1016/j.pt.2015.04.007
Lightowlers MW, Gasser RB, Hemphill A, Romig T, Tamarozzi F, Deplazes P, Torgerson PR, Garcia HH, Kern P (2021) Advances in the treatment, diagnosis, control and scientific understanding of taeniid cestode parasite infections over the past 50 years. Int J Parasitol 51:1167–1192. https://doi.org/10.1016/j.ijpara.2021.10.003
Lissandrin R, Tamarozzi F, Piccoli L, Tinelli C, De Silvestri A, Mariconti M, Meroni V, Genco F, Brunetti E (2016) Factors influencing the serological response in hepatic Echinococcus granulosus infection. Am J Trop Med Hyg 94:166–171. https://doi.org/10.4269/ajtmh.15-0219
Lissandrin R, Tamarozzi F, Mariconti M, Manciulli T, Brunetti E, Vola A (2018) Watch and wait approach for inactive Echinococcal cyst of the liver: an update. Am J Trop Med Hyg 99:375–379. https://doi.org/10.4269/ajtmh.18-0164
Liu W, Delabrousse É, Blagosklonov O, Wang J, Zeng H, Jiang Y, Wang J, Qin Y, Vuitton DA, Wen H (2014) Innovation in hepatic alveolar echinococcosis imaging: best use of old tools, and necessary evaluation of new ones. Parasite 21:74. https://doi.org/10.1051/parasite/2014072
Luong LT, Chambers JL, Moizis A, Stock TM, St Clair CC (2018) Helminth parasites and zoonotic risk associated with urban coyotes (Canis latrans) in Alberta. Canada J Helminthol 94:e25. https://doi.org/10.1017/S0022149X1800113X
Lv H, Jiang Y, Peng X, Zhang S, Wu X, Yang H, Zhang H (2015) Subadventitial cystectomy in the management of biliary fistula with liver hydatid disease. Acta Trop 141:223–228. https://doi.org/10.1016/j.actatropica.2014.06.006
Lymbery AJ (2017) Phylogenetic pattern, evolutionary processes and species delimitation in the genus Echinococcus. Adv Parasitol 95:111–145. https://doi.org/10.1016/bs.apar.2016.07.002
Macpherson CNL, Bartholomot B, Frider B (2003) Application of ultrasound in diagnosis, treatment, epidemiology, public health and control of Echinococcus granulosus and E. multilocularis. Parasitology 127(Suppl):S21–S35
Magistri P, Pecchi A, Franceschini E, Pesi B, Guadagni S, Catellani B, Assirati G, Guidetti C, Guerrini GP, Tarantino G, Ballarin R, Codeluppi M, Morelli L, Coratti A, Di Benedetto F (2019) Not just minor resections: robotic approach for cystic echinococcosis of the liver. Infection 47:973–979. https://doi.org/10.1007/s15010-019-01333-2
Maitiseyiti A, Ma Z, Meng Y, Tian G, Kalifu B, Lu S, Chen X (2020) Mid-term outcomes of laparoscopic Total cystectomy versus open surgery for complicated liver hydatid cysts. Surg Laparosc Endosc Percutan Tech 31:44–50. https://doi.org/10.1097/SLE.0000000000000822
Malik AA, Bari SU, Amin R, Jan M (2010) Surgical management of complicated hydatid cysts of the liver. World J Gastrointest Surg 2:78–84. https://doi.org/10.4240/wjgs.v2.i3.78
Manciulli T, Vola A, Mariconti M, Lissandrin R, Maestri M, Budke CM, Tamarozzi F, Brunetti E (2018) Shortage of Albendazole and its consequences for patients with cystic echinococcosis treated at a referral Center in Italy. Am J Trop Med Hyg 99:1006–1010. https://doi.org/10.4269/ajtmh.18-0245
Marcinkutė A, Šarkūnas M, Moks E, Saarma U, Jokelainen P, Bagrade G, Laivacuma S, Strupas K, Sokolovas V, Deplazes P (2015) Echinococcus infections in the Baltic region. Vet Parasitol 213:121–131. https://doi.org/10.1016/j.vetpar.2015.07.032
Mariconti M, Vola A, Manciulli T, Genco F, Lissandrin R, Meroni V, Rosenzvit M, Tamarozzi F, Brunetti E (2019) Role of microRNAs in host defense against Echinococcus granulosus infection: a preliminary assessment. Immunol Res 67:93–97. https://doi.org/10.1007/s12026-018-9041-4
Massolo A, Liccioli S, Budke C, Klein C (2014) Echinococcus multilocularis in North America: the great unknown. Parasite 21:73. https://doi.org/10.1051/parasite/2014069
Massolo A, Klein C, Kowalewska-Grochowska K, Belga S, MacDonald C, Vaughan S, Girgis S, Giunchi D, Bramer SA, Santa MA, Grant DM, Mori K, Duignan P, Slater O, Gottstein B, Müller N, Houston S (2019) European Echinococcus multilocularis identified in patients in Canada. N Engl J Med 381:384–385. https://doi.org/10.1056/NEJMc1814975
McManus DP (2013) Current status of the genetics and molecular taxonomy of Echinococcus species. Parasitology 140:1617–1623. https://doi.org/10.1017/S0031182013000802
Mohamed AE, Yasawy MI, Al Karawi MA (1998) Combined albendazole and praziquantel versus albendazole alone in the treatment of hydatid disease. Hepato-Gastroenterology 45:1690–1694
Mohkam K, Belkhir L, Wallon M, Darnis B, Peyron F, Ducerf C, Gigot J-F, Mabrut J-Y (2014) Surgical management of liver hydatid disease: subadventitial cystectomy versus resection of the protruding dome. World J Surg 38:2113–2121. https://doi.org/10.1007/s00268-014-2509-z
Monge-Maillo B, Chamorro Tojeiro S, López-Vélez R (2017) Management of osseous cystic echinococcosis. Expert Rev Anti-Infect Ther 15:1075–1082. https://doi.org/10.1080/14787210.2017.1401466
Monge-Maillo B, Olmedo Samperio M, Pérez-Molina JA, Norman F, Mejía CR, Tojeiro SC, López-Vélez R (2019) Osseous cystic echinococcosis: a case series study at a referral unit in Spain. PLoS Negl Trop Dis 13:e0007006. https://doi.org/10.1371/journal.pntd.0007006
Mori K, Liccioli S, Marceau D, Massolo A (2019) A community analysis approach to parasite transmission in multi-host systems: assemblages of small mammal prey and Echinococcus multilocularis in an urban area in North America. Int J Parasitol Parasites Wildl 9:49–55. https://doi.org/10.1016/j.ijppaw.2019.03.012
Mustapayeva A, Manciulli T, Zholdybay Z, Juskiewicz K, Zhakenova Z, Shapiyeva Z, Medetov Z, Vola A, Mariconti M, Brunetti E, Budke CM, Khalykova M, Duisenova A (2020) Incidence rates of surgically managed cystic echinococcosis in Kazakhstan, 2007–2016. Am J Trop Med Hyg 102:90–95. https://doi.org/10.4269/ajtmh.19-0572
Mustapayeva A, Luca D’Alessandro G, Doszhanova G, Colpani A, Sadybekov N, Baimakhanov Z, Assanov E, Salybekov S, Kaniyev S, Serikuly E, Tagabayeva L, Budke CM, Vola A, Mariconti M, De Silvestri A, Yalisheva S, Sadykova A, Zholdybay Z, Katarbayev A, Zhakenova Z, Brunetti E, Juszkiewicz K, Duisenova A, Manciulli T (2021) Ultrasound-based evaluation of the prevalence of abdominal cystic echinococcosis in the Turkestan region of Kazakhstan. Trans R Soc Trop Med Hyg:trab105. https://doi.org/10.1093/trstmh/trab105
Nakao M, McManus DP, Schantz PM, Craig PS, Ito A (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134:713–722. https://doi.org/10.1017/S0031182006001934
Nakao M, Lavikainen A, Yanagida T, Ito A (2013) Phylogenetic systematics of the genus Echinococcus (Cestoda: Taeniidae). Int J Parasitol 43:1017–1029. https://doi.org/10.1016/j.ijpara.2013.06.002
Nakao M, Lavikainen A, Hoberg E (2015) Is Echinococcus intermedius a valid species? Trends Parasitol 31:342–343. https://doi.org/10.1016/j.pt.2015.04.012
Neumayr A, Troia G, de Bernardis C, Tamarozzi F, Goblirsch S, Piccoli L, Hatz C, Filice C, Brunetti E (2011) Justified concern or exaggerated fear: the risk of anaphylaxis in percutaneous treatment of cystic echinococcosis-a systematic literature review. PLoS Negl Trop Dis 5:e1154. https://doi.org/10.1371/journal.pntd.0001154
Ocak S, Poyanlı A, Güllüoğu M, İbiş C, Tekant Y, Özden İ (2021) Dramatic response to albendazole in transplantation candidates with unresectable hepatic alveolar hydatid disease. Clin Case Rep 9:e04666. https://doi.org/10.1002/ccr3.4666
Otero-Abad B, Torgerson PR (2013) A systematic review of the epidemiology of echinococcosis in domestic and wild animals. PLoS Negl Trop Dis 7:e2249. https://doi.org/10.1371/journal.pntd.0002249
Paternoster G, Boo G, Wang C, Minbaeva G, Usubalieva J, Raimkulov KM, Zhoroev A, Abdykerimov KK, Kronenberg PA, M onenber B, Furrer R, Deplazes P, Torgerson PR (2020) Epidemic cystic and alveolar echinococcosis in Kyrgyzstan: an analysis of national surveillance data. Lancet Glob Health 8:e603–e611. https://doi.org/10.1016/S2214-109X(20)30038-3
Pawlowski Z, Eckert J, Vuitton D, Ammann R, Kern P, Craig P, Dar K, De Rosa F, Filice C, Gottstein B, Grimm F, MacPherson C, Sato N, Todorov T, Uchino J, von Sinner W, Wen H (2001) Echinococcosis in humans: clinical aspects, diagnosis and treatment. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (eds) WHO/OIE manual on Echinococcosis in humans and animals: a public health problem of global concern. World Organization for Animal Health (OIE), Paris, pp 20–72
Peng X, Zhang S, Niu J (2002) Total subadventitial cystectomy for the treatment of 30 patients with hepatic hydatid cysts. Chin J General Surg (Chin) 17:529–530
Peng X, Li J, Wu X, Zhang S, Niu J, Chen X, Yao J, Sun H (2006) Detection of Osteopontin in the pericyst of human hepatic Echinococcus granulosus. Acta Trop 100:163–171. https://doi.org/10.1016/j.actatropica.2006.08.013
Petrone L, Vanini V, Petruccioli E, Ettorre GM, Busi Rizzi E, Schininà V, Girardi E, Ludovisi A, Gómez-Morales MÁ, Pozio E, Teggi A, Goletti D (2015) IL-4 specific-response in whole blood associates with human cystic echinococcosis and cyst activity. J Infect 70:299–306. https://doi.org/10.1016/j.jinf.2014.10.009
Petrone L, Tamarozzi F, Vola A, Gomez Morales MA, Ludovisi A, Najafi Fard S, Mariconti M, Brunetti E, Goletti D (2021) Accuracy of an experimental whole-blood test for detecting reactivation of echinococcal cysts. PLoS Negl Trop Dis 15:e0009648. https://doi.org/10.1371/journal.pntd.0009648
Piarroux M, Piarroux R, Giorgi R, Knapp J, Bardonnet K, Sudre B, Watelet J, Dumortier J, Gérard A, Beytout J, Abergel A, Mantion G, Vuitton DA, Bresson-Hadni S (2011) Clinical features and evolution of alveolar echinococcosis in France from 1982 to 2007: results of a survey in 387 patients. J Hepatol 55:1025–1033. https://doi.org/10.1016/j.jhep.2011.02.018
Qin Y, Li X, Zhang Q, Xie B, Ji X, Li Y, Yiblayan A, Wen H (2016) Analysis of the clinical value of (18)F-FDG PET/CT in hepatic alveolar echinococcosis before and after autologous liver transplantation. Exp Ther Med 11:43–48. https://doi.org/10.3892/etm.2015.2857
Qiu Y, Yang X, Wang T, Shen S, Yang Y, Huang B, Wang W (2021) Learning curve of ex vivo liver resection and autotransplantation in treating end-stage hepatic alveolar echinococcosis: a RA-CUSUM analysis. Front Surg 8:753968. https://doi.org/10.3389/fsurg.2021.753968
Ran B, Wang M, Jian W, Jiang T, Zhang R, Guo Q, Zhang W, Wen H, Shao Y, Aji T (2019) Simultaneous occurrence of hepatic alveolar and cystic echinococcosis. J Helminthol 94:e80. https://doi.org/10.1017/S0022149X19000385
Rausch RL, Wilson JF, Schantz PM (1990) A programme to reduce the risk of infection by Echinococcus multilocularis: the use of praziquantel to control the cestode in a village in the hyperendemic region of Alaska. Ann Trop Med Parasitol 84:239–250. https://doi.org/10.1080/00034983.1990.11812463
Rehmann P, Gröne A, Gottstein B, Völlm J, Sager H, Janovsky M, Bacciarini LN (2005) Detection of Echinococcus multilocularis infection in a colony of cynomolgus monkeys (Macaca fascicularis) using serology and ultrasonography. J Vet Diagn Investig 17:183–186
Reuter S, Jensen B, Buttenschoen K, Kratzer W, Kern P (2000) Benzimidazoles in the treatment of alveolar echinococcosis: a comparative study and review of the literature. J Antimicrob Chemother 46:451–456
Reuter S, Buck A, Grebe O, Nüssle-Kügele K, Kern P, Manfras BJ (2003) Salvage treatment with amphotericin B in progressive human alveolar echinococcosis. Antimicrob Agents Chemother 47:3586–3591. https://doi.org/10.1128/AAC.47.11.3586-3591.2003
Reuter S, Buck A, Manfras B, Kratzer W, Seitz HM, Darge K, Reske SN, Kern P (2004) Structured treatment interruption in patients with alveolar echinococcosis. Hepatology 39:509–517. https://doi.org/10.1002/hep.20078
Reuter S, Manfras B, Merkle M, Härter G, Kern P (2006) In vitro activities of itraconazole, methiazole, and nitazoxanide versus Echinococcus multilocularis larvae. Antimicrob Agents Chemother 50:2966–2970. https://doi.org/10.1128/AAC.00476-06
Ricard-Blum S, Bresson-Hadni S, Vuitton DA, Ville G, Grimaud JA (1992) Hydroxypyridinium collagen cross-links in human liver fibrosis: study of alveolar echinococcosis. Hepatology 15:599–602. https://doi.org/10.1002/hep.1840150408
Ricard-Blum S, Bresson-Hadni S, Guerret S, Grenard P, Volle PJ, Risteli L, Grimaud JA, Vuitton DA (1996) Mechanism of collagen network stabilization in human irreversible granulomatous liver fibrosis. Gastroenterology 111:172–182. https://doi.org/10.1053/gast.1996.v111.pm8698196
Richards KS, Riley EM, Taylor DH, Morris DL (1988) Studies on the effect of short term, high dose praziquantel treatment against protoscoleces of ovine and equine Echinococcus granulosus within the cyst, and in vitro. Trop Med Parasitol 39:269–272
Rinaldi F, Brunetti E, Neumayr A, Maestri M, Goblirsch S, Tamarozzi F (2014) Cystic echinococcosis of the liver: a primer for hepatologists. World J Hepatol 6:293–305. https://doi.org/10.4254/wjh.v6.i5.293
Robardet E, Giraudoux P, Caillot C, Boue F, Cliquet F, Augot D, Barrat J (2008) Infection of foxes by Echinococcocus multilocularis in urban and suburban areas of Nancy, France: influence of feeding habits and environment. Parasite 15:77–85. https://doi.org/10.1051/parasite/2008151077
Robardet E, Giraudoux P, Caillot C, Augot D, Boue F, Barrat J (2011) Fox defecation behaviour in relation to spatial distribution of voles in an urbanised area: an increasing risk of transmission of Echinococcus multilocularis? Int J Parasitol 41:145–154. https://doi.org/10.1016/j.ijpara.2010.08.007
Roberts MG, Aubert MF (1995) A model for the control of Echinococcus multilocularis in France. Vet Parasitol 56:67–74. https://doi.org/10.1016/0304-4017(94)00655-v
Roelfsema JH, Nozari N, Pinelli E, Kortbeek LM (2016) Novel PCRs for differential diagnosis of cestodes. Exp Parasitol 161:20–26. https://doi.org/10.1016/j.exppara.2015.12.010
Rogan MT, Hai WY, Richardson R, Zeyhle E, Craig PS (2006) Hydatid cysts: does every picture tell a story? Trends Parasitol 22:431–438. https://doi.org/10.1016/j.pt.2006.07.003
Romig T, Dinkel A, Mackenstedt U (2006) The present situation of echinococcosis in Europe. Parasitol Int 55(Suppl):S187–S191. https://doi.org/10.1016/j.parint.2005.11.028
Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, Wassermann M, Takahashi K, de la Rue M (2017) Ecology and life cycle patterns of Echinococcus species. Adv Parasitol 95:213–314. https://doi.org/10.1016/bs.apar.2016.11.002
Sailer M, Soelder B, Allerberger F, Zaknun D, Feichtinger H, Gottstein B (1997) Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J Pediatr 130:320–323
Sato N, Namieno T, Furuya K, Takahashi H, Yamashita K, Uchino J, Suzuki K (1997) Contribution of mass screening system to resectability of hepatic lesions involving Echinococcus multilocularis. J Gastroenterol 32:351–354
Scharf G, Deplazes P, Kaser-Hotz B, Borer L, Hasler A, Haller M, Flückiger M (2004) Radiographic, ultrasonographic, and computed tomographic appearance of alveolar echinococcosis in dogs. Vet Radiol Ultrasound 45:411–418
Schipper HG, Laméris JS, van Delden OM, Rauws EA, Kager PA (2002) Percutaneous evacuation (PEVAC) of multivesicular echinococcal cysts with or without cystobiliary fistulas which contain non-drainable material: first results of a modified PAIR method. Gut 50:718–723. https://doi.org/10.1136/gut.50.5.718
Schmidberger J, Steinbach J, Schlingeloff P, Kratzer W, Grüner B (2019) Surgery versus conservative drug therapy in alveolar echinococcosis patients in Germany – a health-related quality of life comparison. Food Waterborne Parasitol 16:e00057. https://doi.org/10.1016/j.fawpar.2019.e00057
Schneider R, Gollackner B, Edel B, Schmid K, Wrba F, Tucek G, Walochnik J, Auer H (2008) Development of a new PCR protocol for the detection of species and genotypes (strains) of Echinococcus in formalin-fixed, paraffin-embedded tissues. Int J Parasitol 38:1065–1071. https://doi.org/10.1016/j.ijpara.2007.11.008
Shen S, Kong J, Qiu Y, Zhang S, Qin Y, Wang W (2019) Ex vivo liver resection and autotransplantation versus allotransplantation for end-stage hepatic alveolar echinococcosis. Int J Infect Dis 79:87–93. https://doi.org/10.1016/j.ijid.2018.11.016
Siles-Lucas M, Casulli A, Conraths FJ, Müller N (2017) Laboratory diagnosis of Echinococcus spp. in human patients and infected animals. Adv Parasitol 96:159–257. https://doi.org/10.1016/bs.apar.2016.09.003
Siles-Lucas M, Casulli A, Cirilli R, Carmena D (2018) Progress in the pharmacological treatment of human cystic and alveolar echinococcosis: compounds and therapeutic targets. PLoS Negl Trop Dis 12:e0006422. https://doi.org/10.1371/journal.pntd.0006422
Simsek S, Kaplan M, Ozercan IH (2011) A comprehensive molecular survey of Echinococcus granulosus in formalin-fixed paraffin-embedded tissues in human isolates in Turkey. Parasitol Res 109:411–416. https://doi.org/10.1007/s00436-011-2269-8
Skuhala T, Trkulja V, Runje M, Vukelic D, Desnica B (2014) Albendazolesulphoxide concentrations in plasma and hydatid cyst and prediction of parasitological and clinical outcomes in patients with liver hydatidosis caused by Echinococcus granulosus. Croat Med J 55:146–155. https://doi.org/10.3325/cmj.2014.55.146
Smego RA, Bhatti S, Khaliq AA, Beg MA (2003) Percutaneous aspiration-injection-reaspiration drainage plus albendazole or mebendazole for hepatic cystic echinococcosis: a meta-analysis. Clin Infect Dis 37:1073–1083. https://doi.org/10.1086/378275
Sokouti M, Sadeghi R, Pashazadeh S, Abadi SEH, Sokouti M, Rezaei-Hachesu P, Ghojazadeh M, Sokouti B (2017) A systematic review and meta-analysis on the treatment of liver hydatid cyst: comparing laparoscopic and open surgeries. Arab J Gastroenterol 18:127–135. https://doi.org/10.1016/j.ajg.2017.09.010
Sokouti M, Sadeghi R, Pashazadeh S, Abadi SEH, Sokouti M, Ghojazadeh M, Sokouti B (2019) A systematic review and meta-analysis on the treatment of liver hydatid cyst using meta-MUMS tool: comparing PAIR and laparoscopic procedures. Arch Med Sci 15:284–308. https://doi.org/10.5114/aoms.2018.73344
Solomon N, Kachani M, Zeyhle E, Macpherson CNL (2017) The natural history of cystic echinococcosis in untreated and albendazole-treated patients. Acta Trop 171:52–57. https://doi.org/10.1016/j.actatropica.2017.03.018
Staebler S, Steinmetz H, Keller S, Deplazes P (2007) First description of natural Echinococcus multilocularis infections in chinchilla (Chinchilla laniger) and Prevost’s squirrel (Callosciurus prevostii borneoensis). Parasitol Res 101:1725–1727. https://doi.org/10.1007/s00436-007-0717-2
Stefanić S, Shaikenov BS, Deplazes P, Dinkel A, Torgerson PR, Mathis A (2004) Polymerase chain reaction for detection of patent infections of Echinococcus granulosus (“sheep strain”) in naturally infected dogs. Parasitol Res 92:347–351. https://doi.org/10.1007/s00436-003-1043-y
Stettler M, Rossignol JF, Fink R, Walker M, Gottstein B, Merli M, Theurillat R, Thormann W, Dricot E, Segers R, Hemphill A (2004) Secondary and primary murine alveolar echinococcosis: combined albendazole/nitazoxanide chemotherapy exhibits profound anti-parasitic activity. Int J Parasitol 34:615–624. https://doi.org/10.1016/j.ijpara.2004.01.006
Stojkovic M, Rosenberger K, Kauczor H-U, Junghanss T, Hosch W (2012) Diagnosing and staging of cystic echinococcosis: how do CT and MRI perform in comparison to ultrasound? PLoS Negl Trop Dis 6:e1880. https://doi.org/10.1371/journal.pntd.0001880
Stojkovic M, Rosenberger KD, Steudle F, Junghanss T (2016) Watch and wait Management of Inactive Cystic Echinococcosis - does the path to inactivity matter – analysis of a prospective patient cohort. PLoS Negl Trop Dis 10:e0005243. https://doi.org/10.1371/journal.pntd.0005243
Stojkovic M, Adt H-M, Rosenberger K, Boubaker G, Hernandez-Gonzalez A, Junghanss T, Zwahlen M, Siles-Lucas M (2017) Follow-up of surgically treated patients with cystic echinococcosis: can novel recombinant antigens compete with imaging? Analysis of a patient cohort. Tropical Med Int Health 22:614–621. https://doi.org/10.1111/tmi.12859
Stojković M, Weber TF, Junghanss T (2018) Clinical management of cystic echinococcosis: state of the art and perspectives. Curr Opin Infect Dis 31:383–392. https://doi.org/10.1097/QCO.0000000000000485
Tamarozzi F, Sako Y, Ito A, Piccoli L, Grisolìa A, Itoh S, Gatti S, Meroni V, Genco F, Brunetti E (2013) Recombinant AgB8/1 ELISA test vs. commercially available IgG ELISA test in the diagnosis of cystic echinococcosis. Parasite Immunol 35:433–440. https://doi.org/10.1111/pim.12050
Tamarozzi F, Vuitton L, Brunetti E, Vuitton DA, Koch S (2014) Non-surgical and non-chemical attempts to treat echinococcosis: do they work? Parasite 21:75. https://doi.org/10.1051/parasite/2014071
Tamarozzi F, Horton J, Muhtarov M, Ramharter M, Siles-Lucas M, Gruener B, Vuitton DA, Bresson-Hadni S, Manciulli T, Brunetti E (2020a) A case for adoption of continuous albendazole treatment regimen for human echinococcal infections. PLoS Negl Trop Dis 14:e0008566. https://doi.org/10.1371/journal.pntd.0008566
Tamarozzi F, Legnardi M, Fittipaldo A, Drigo M, Cassini R (2020b) Epidemiological distribution of Echinococcus granulosus s.l. infection in human and domestic animal hosts in European Mediterranean and Balkan countries: a systematic review. PLoS Negl Trop Dis 14:e0008519. https://doi.org/10.1371/journal.pntd.0008519
Tamarozzi F, Silva R, Fittipaldo VA, Buonfrate D, Gottstein B, Siles-Lucas M (2021) Serology for the diagnosis of human hepatic cystic echinococcosis and its relation with cyst staging: a systematic review of the literature with meta-analysis. PLoS Negl Trop Dis 15:e0009370. https://doi.org/10.1371/journal.pntd.0009370
Tao S, Qin Z, Hao W, Yongquan L, Lanhui Y, Lei Y (2011) Usefulness of gray-scale contrast-enhanced ultrasonography (SonoVue®) in diagnosing hepatic alveolar echinococcosis. Ultrasound Med Biol 37:1024–1028. https://doi.org/10.1016/j.ultrasmedbio.2011.04.014
Tappe D, Frosch M, Sako Y, Itoh S, Grüner B, Reuter S, Nakao M, Ito A, Kern P (2009) Close relationship between clinical regression and specific serology in the follow-up of patients with alveolar echinococcosis in different clinical stages. Am J Trop Med Hyg 80:792–797
Tappe D, Sako Y, Itoh S, Frosch M, Grüner B, Kern P, Ito A (2010) Immunoglobulin G subclass responses to recombinant Em18 in the follow-up of patients with alveolar echinococcosis in different clinical stages. Clin Vaccine Immunol 17:944–948. https://doi.org/10.1128/CVI.00026-10
Taylor DH, Morris DL (1989) Combination chemotherapy is more effective in postspillage prophylaxis for hydatid disease than either albendazole or praziquantel alone. Br J Surg 76:954. https://doi.org/10.1002/bjs.1800760927
Teggi A, Giattino M, Franchi C, Lastilla M (1997) A hypothesis on the significance of an increase in serum transaminases in patients with hydatidosis treated with benzimidazole carbamates. Recenti Prog Med 88:452–458
Thompson RC, Eckert J (1983) Observations on Echinococcus multilocularis in the definitive host. Z Parasitenkd 69:335–345
Torgerson PR, Deplazes P (2009) Echinococcosis: diagnosis and diagnostic interpretation in population studies. Trends Parasitol 25:164–170. https://doi.org/10.1016/j.pt.2008.12.008
Torgerson P, Macpherson C, Vuitton D (2011) Cystic echinococcosis. In: Palmer SR, Soulsby L, Torgerson P, Brown DWG (eds) Oxford textbook on Zoonoses. Biology, clinical practice, and public control, 2nd edn. Oxford University Press, Oxford, pp 1–62
Trachsel D, Deplazes P, Mathis A (2007) Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134:911–920. https://doi.org/10.1017/S0031182007002235
Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sánchez-Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso G, Sciutto E, Aslett M, Beasley H, Bennett HM, Cai X, Camicia F, Clark R, Cucher M, De Silva N, Day TA, Deplazes P, Estrada K, Fernández C, Holland PWH, Hou J, Hu S, Huckvale T, Hung SS, Kamenetzky L, Keane JA, Kiss F, Koziol U, Lambert O, Liu K, Luo X, Luo Y, Macchiaroli N, Nichol S, Paps J, Parkinson J, Pouchkina-Stantcheva N, Riddiford N, Rosenzvit M, Salinas G, Wasmuth JD, Zamanian M, Zheng Y, Taenia solium Genome Consortium, Cai J, Soberón X, Olson PD, Laclette JP, Brehm K, Berriman M (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496:57–63. https://doi.org/10.1038/nature12031
Tuxun T, Zhang J-H, Zhao J-M, Tai Q-W, Abudurexti M, Ma H-Z, Wen H (2014) World review of laparoscopic treatment of liver cystic echinococcosis--914 patients. Int J Infect Dis 24:43–50. https://doi.org/10.1016/j.ijid.2014.01.012
Ueno M, Kuroda N, Yahagi K, Ohtaki T, Kawanaka M (2012) Analysis of antibody responses by commercial western blot assay in horses with alveolar echinococcosis. J Vet Med Sci 74:813–815
Umhang G, Lahoreau J, Hormaz V, Boucher J-M, Guenon A, Montange D, Grenouillet F, Boue F (2016) Surveillance and management of Echinococcus multilocularis in a wildlife park. Parasitol Int 65:245–250. https://doi.org/10.1016/j.parint.2016.01.008
Umhang G, Possenti A, Colamesta V, d’Aguanno S, La Torre G, Boué F, Casulli A (2019) A systematic review and meta-analysis on anthelmintic control programs for Echinococcus multilocularis in wild and domestic carnivores. Food Waterborne Parasitol 15:e00042. https://doi.org/10.1016/j.fawpar.2019.e00042
Valot B, Rognon B, Prenel A, Baraquin A, Knapp J, Anelli M, Richou C, Bresson-Hadni S, Grenouillet F, Wang J, Vuitton DA, Gottstein B, Millon L (2017) Screening of antigenic vesicular fluid proteins of Echinococcus multilocularis as potential viability biomarkers to monitor drug response in alveolar echinococcosis patients. Proteomics Clin Appl 11. https://doi.org/10.1002/prca.201700010
van Kesteren F, Qi X, Tao J, Feng X, Mastin A, Craig PS, Vuitton DA, Duan X, Chu X, Zhu J, Wen H (2015) Independent evaluation of a canine echinococcosis control programme in Hobukesar County, Xinjiang, China. Acta Trop 145:1–7. https://doi.org/10.1016/j.actatropica.2015.01.009
Velasco-Tirado V, Romero-Alegría Á, Belhassen-García M, Alonso-Sardón M, Esteban-Velasco C, López-Bernús A, Carpio-Perez A, Jimenez López MF, Muñoz Bellido JL, Muro A, Cordero-Sanchez M, Pardo-Lledias J, Muñoz-Bellvis L (2017) Recurrence of cystic echinococcosis in an endemic area: a retrospective study. BMC Infect Dis 17:455. https://doi.org/10.1186/s12879-017-2556-9
Velasco-Tirado V, Alonso-Sardón M, Lopez-Bernus A, Romero-Alegría Á, Burguillo FJ, Muro A, Carpio-Pérez A, Muñoz Bellido JL, Pardo-Lledias J, Cordero M, Belhassen-García M (2018) Medical treatment of cystic echinococcosis: systematic review and meta-analysis. BMC Infect Dis 18:306. https://doi.org/10.1186/s12879-018-3201-y
Virchow R (1855) Die multilokuläre, ulzerierende Echinokokkengeschwulst der Leber. Verhandlungen der Physikalisch-Medizinischen Gesellschaft, pp 84–95
Vola A, Manciulli T, De Silvestri A, Lissandrin R, Mariconti M, Siles-Lucas M, Brunetti E, Tamarozzi F (2019) Diagnostic performances of commercial ELISA, indirect Hemagglutination, and Western Blot in differentiation of hepatic Echinococcal and non-Echinococcal lesions: a retrospective analysis of data from a single referral Centre. Am J Trop Med Hyg 101:1345–1349. https://doi.org/10.4269/ajtmh.19-0556
Vola A, Mariconti M, Lissandrin R, Cuzzocrea F, Bortolotto C, Sammarchi L, Vercelli A, Rinaldi P, Maestri M, Manciulli T, Brunetti E (2022) Prospective collection of clinical data on cystic echinococcosis: experience with the European registry of cystic echinococcosis in Pavia, Italy. Trans R Soc Trop Med Hyg 116:157–162. https://doi.org/10.1093/trstmh/trab097
Vuitton DA (2003) The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Trop 85:119–132
Vuitton DA (2009a) Benzimidazoles for the treatment of cystic and alveolar echinococcosis: what is the consensus? Expert Rev Anti-Infect Ther 7:145–149. https://doi.org/10.1586/14787210.7.2.145
Vuitton DA (2009b) Benzimidazoles for the treatment of cystic and alveolar echinococcosis: what is the consensus? Expert Rev Anti-Infect Ther 7:145–149. https://doi.org/10.1586/14787210.7.2.145
Vuitton D, Bresson-Hadni S (2014) Alveolar echinococcosis: evaluation of therapeutic strategies. Expert Opin Orphan Drugs 2:67–86
Vuitton DA, Gottstein B (2010) Echinococcus multilocularis and its intermediate host: a model of parasite-host interplay. J Biomed Biotechnol 2010:923193. https://doi.org/10.1155/2010/923193
Vuitton DA, Zhou H, Bresson-Hadni S, Wang Q, Piarroux M, Raoul F, Giraudoux P (2003) Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127(Suppl):S87–S107
Vuitton DA, Wang Q, Zhou H-X, Raoul F, Knapp J, Bresson-Hadni S, Wen H, Giraudoux P (2011) A historical view of alveolar echinococcosis, 160 years after the discovery of the first case in humans: part 1. What have we learnt on the distribution of the disease and on its parasitic agent? Chin Med J 124:2943–2953
Vuitton DA, Demonmerot F, Knapp J, Richou C, Grenouillet F, Chauchet A, Vuitton L, Bresson-Hadni S, Millon L (2015) Clinical epidemiology of human AE in Europe. Vet Parasitol 213:110–120. https://doi.org/10.1016/j.vetpar.2015.07.036
Vuitton DA, Azizi A, Richou C, Vuitton L, Blagosklonov O, Delabrousse E, Mantion GA, Bresson-Hadni S (2016) Current interventional strategy for the treatment of hepatic alveolar echinococcosis. Expert Rev Anti-Infect Ther 14:1179–1194. https://doi.org/10.1080/14787210.2016.1240030
Vuitton DA, Bresson-Hadni S, Chauchet A, Richou C, Grenouillet F, Delabrousse E, Millon L, Mantion G (2019) L’échinococcose alvéolaire au XXIe siècle: une maladie infectieuse opportuniste? Bulletin De l’Academie Nationale De Medecine 203:94–101
Vuitton DA, McManus DP, Rogan MT, Romig T, Gottstein B, Naidich A, Tuxun T, Wen H, Menezes da Silva A, World Association of Echinococcosis (2020) International consensus on terminology to be used in the field of echinococcoses. Parasite 27:41. https://doi.org/10.1051/parasite/2020024
Wang Y, Zhang X, Bartholomot B, Liu B, Luo J, Li T, Wen X, Zheng H, Zhou H, Wen H, Davaadorj N, Gambolt L, Mukhar T, al-Qaoud K, Abdel-Hafez S, Giraudoux P, Vuitton DA, Fraser A, Rogan MT, Craig PS (2003) Classification, follow-up and recurrence of hepatic cystic echinococcosis using ultrasound images. Trans R Soc Trop Med Hyg 97:203–211. https://doi.org/10.1016/s0035-9203(03)90121-0
Wang Q, Vuitton DA, Qiu J, Giraudoux P, Xiao Y, Schantz PM, Raoul F, Li T, Yang W, Craig PS (2004) Fenced pasture: a possible risk factor for human alveolar echinococcosis in Tibetan pastoralist communities of Sichuan, China. Acta Trop 90:285–293. https://doi.org/10.1016/j.actatropica.2004.02.004
Wang Q, Vuitton DA, Xiao Y, Budke CM, Campos-Ponce M, Schantz PM, Raoul F, Yang W, Craig PS, Giraudoux P (2006a) Pasture types and Echinococcus multilocularis, Tibetan communities. Emerg Infect Dis 12:1008–1010
Wang Y, He T, Wen X, Li T, Waili A, Zhang W, Xu X, Vuitton DA, Rogan MT, Wen H, Craig PS (2006b) Post-survey follow-up for human cystic echinococcosis in Northwest China. Acta Trop 98:43–51
Wang L, Wen H, Feng X, Jiang X, Duan X (2012) Analysis of economic burden for patients with cystic echinococcosis in five hospitals in Northwest China. Trans R Soc Trop Med Hyg 106:743–748. https://doi.org/10.1016/j.trstmh.2012.09.003
Wang Q, Yu W-J, Zhong B, Shang J-Y, Huang L, Mastin A, Renqingpengcuo null, Huang Y, Zhang G-J, He W, Giraudoux P, Wu W-P, Craig PS (2016) Seasonal pattern of Echinococcus re-infection in owned dogs in Tibetan communities of Sichuan, China and its implications for control. Infect Dis Poverty 5:60. https://doi.org/10.1186/s40249-016-0155-4
Wang J, Jebbawi F, Bellanger A-P, Beldi G, Millon L, Gottstein B (2018) Immunotherapy of alveolar echinococcosis via PD-1/PD-L1 immune checkpoint blockade in mice. Parasite Immunol 40:e12596. https://doi.org/10.1111/pim.12596
Wang S, Ma Y, Wang W, Dai Y, Sun H, Li J, Wang S, Li F (2021) Status and prospect of novel treatment options toward alveolar and cystic echinococcosis. Acta Trop 226:106252. https://doi.org/10.1016/j.actatropica.2021.106252
Wen H, Yang WG (1997) Public health importance of cystic echinococcosis in China. Acta Trop 67:133–145. https://doi.org/10.1016/s0001-706x(97)00051-x
Wen H, Tian WL, Zou PF, Xiang MX (1992) A rare case of mixed cystic and alveolar hydatidosis. Trans R Soc Trop Med Hyg 86:290–291
Wen H, Dong J-H, Zhang J-H, Zhao J-M, Shao Y-M, Duan W-D, Liang Y-R, Ji X-W, Tai Q-W, Aji T, Li T (2011) Ex vivo liver resection followed by autotransplantation for end-stage hepatic alveolar echinococcosis. Chin Med J 124:2813–2817
Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP (2019) Echinococcosis: advances in the 21st century. Clin Microbiol Rev 32. https://doi.org/10.1128/CMR.00075-18
WHO Informal Working Group (2003) International classification of ultrasound images in cystic echinococcosis for application in clinical and field epidemiological settings. Acta Trop 85:253–261
WHO Informal Working Group on Echinococcosis (WHO-IWGE) (1996) Guidelines for treatment of cystic and alveolar echinococcosis in humans. Bull World Health Organ 74:231–242
Xiao N, Qiu J, Nakao M, Li T, Yang W, Chen X, Schantz PM, Craig PS, Ito A (2005) Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. Int J Parasitol 35:693–701. https://doi.org/10.1016/j.ijpara.2005.01.003
Yaghi M, Zorkot M, Kanso M, Faraj W (2021) Robotic resection for hydatid disease of the liver. BMJ Case Rep 14:e241681. https://doi.org/10.1136/bcr-2021-241681
Yang YR, Liu XZ, Vuitton DA, Bartholomot B, Wang YH, Ito A, Craig PS, McManus DP (2006a) Simultaneous alveolar and cystic echinococcosis of the liver. Trans R Soc Trop Med Hyg 100:597–600. https://doi.org/10.1016/j.trstmh.2005.09.016
Yang YR, Sun T, Li Z, Zhang J, Teng J, Liu X, Liu R, Zhao R, Jones MK, Wang Y, Wen H, Feng X, Zhao Q, Zhao Y, Shi D, Bartholomot B, Vuitton DA, Pleydell D, Giraudoux P, Ito A, Danson MF, Boufana B, Craig PS, Williams GM, McManus DP (2006b) Community surveys and risk factor analysis of human alveolar and cystic echinococcosis in Ningxia Hui autonomous region, China. Bull World Health Organ 84:714–721
Yang YR, Craig PS, Ito A, Vuitton DA, Giraudoux P, Sun T, Williams GM, Huang Z, Li Z, Wang Y, Teng J, Li Y, Huang L, Wen H, Jones MK, McManus DP (2007) A correlative study of ultrasound with serology in an area in China co-endemic for human alveolar and cystic echinococcosis. Tropical Med Int Health 12:637–646. https://doi.org/10.1111/j.1365-3156.2007.01834.x
Yang YR, Craig PS, Vuitton DA, Williams GM, Sun T, Liu TX, Boufana B, Giraudoux P, Teng J, Li Y, Huang L, Zhang W, Jones MK, McManus DP (2008) Serological prevalence of echinococcosis and risk factors for infection among children in rural communities of southern Ningxia, China. Tropical Med Int Health 13:1086–1094. https://doi.org/10.1111/j.1365-3156.2008.02101.x
Yang C, He J, Yang X, Wang W (2019) Surgical approaches for definitive treatment of hepatic alveolar echinococcosis: results of a survey in 178 patients. Parasitology 146:1414–1420. https://doi.org/10.1017/S0031182019000891
Yang C, Yang H-J, Deng S-P, Zhang Y (2020) Current status of ex-vivo liver resection and autologous liver transplantation for end-stage hepatic alveolar echinococcosis. Ann. Palliat Med 9(2271–2278):10.21037/apm-20-184
Yangdan C-R, Wang C, Zhang L-Q, Ren B, Fan H-N, Lu M-D (2021) Recent advances in ultrasound in the diagnosis and evaluation of the activity of hepatic alveolar echinococcosis. Parasitol Res 120:3077–3082. https://doi.org/10.1007/s00436-021-07262-0
Zammarchi L, Gobbi F, Angheben A, Spinicci M, Buonfrate D, Calleri G, De Paola M, Bevilacqua N, Carrara S, Attard L, Vanino E, Gulletta M, Festa E, Iacovazzi T, Grimaldi A, Sepe A, Salomone Megna A, Gaiera G, Castagna A, Parodi P, Albonico M, Bisoffi Z, Castelli F, Olliaro P, Bartoloni A (2020) Schistosomiasis, strongyloidiasis and Chagas disease: the leading imported neglected tropical diseases in Italy. J Travel Med 27:taz100. https://doi.org/10.1093/jtm/taz100
Zavoikin VD, Zelya OP, Tumolskaya NI (2020) The importance of uninterrupted albendazole treatment in patients with unresectable alveolar echinococcosis undergoing liver transplantation. Transpl Infect Dis 22:e13291. https://doi.org/10.1111/tid.13291
Zhang W, Wen H, Li J, Lin R, McManus DP (2012) Immunology and immunodiagnosis of cystic echinococcosis: an update. Clin Dev Immunol 2012:101895. https://doi.org/10.1155/2012/101895
Zhang C, Lin R, Li Z, Yang S, Bi X, Wang H, Aini A, Zhang N, Abulizi A, Sun C, Li L, Zhao Z, Qin R, Li X, Li L, Aji T, Shao Y, Vuitton DA, Tian Z, Wen H (2019) Immune exhaustion of T cells in alveolar echinococcosis patients and its reversal by blocking checkpoint receptor TIGIT in a murine model. Hepatology. https://doi.org/10.1002/hep.30896
Zhang C, Lin R, Li Z, Yang S, Bi X, Wang H, Aini A, Zhang N, Abulizi A, Sun C, Li L, Zhao Z, Qin R, Li X, Li L, Aji T, Shao Y, Vuitton DA, Tian Z, Wen H (2020) Immune exhaustion of T cells in alveolar echinococcosis patients and its reversal by blocking checkpoint receptor TIGIT in a murine model. Hepatology 71:1297–1315. https://doi.org/10.1002/hep.30896
Zhang C, Wang H, Li J, Hou X, Li L, Wang W, Shi Y, Li D, Li L, Zhao Z, Li L, Aji T, Lin R, Shao Y, Vuitton DA, Tian Z, Sun H, Wen H (2021) Involvement of TIGIT in natural killer cell exhaustion and immune escape in patients and mouse model with liver Echinococcus multilocularis infection. Hepatology 74:3376–3393. https://doi.org/10.1002/hep.32035
Zhao Z-M, Yin Z-Z, Meng Y, Jiang N, Ma Z-G, Pan L-C, Tan X-L, Chen X, Liu R (2020) Successful robotic radical resection of hepatic echinococcosis located in posterosuperior liver segments. World J Gastroenterol 26:2831–2838. https://doi.org/10.3748/wjg.v26.i21.2831
Zingg W, Renner-Schneiter EC, Pauli-Magnus C, Renner EL, van Overbeck J, Schläpfer E, Weber M, Weber R, Opravil M, Gottstein B, Speck RF, Swiss HIV Cohort Study (2004) Alveolar echinococcosis of the liver in an adult with human immunodeficiency virus type-1 infection. Infection 32:299–302
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 Springer Nature Switzerland AG
About this entry
Cite this entry
Vuitton, D.A., Millon, L., Manciulli, T., Brunetti, E. (2022). Cystic and Alveolar Echinococcosis: Fraternal Twins Both in Search of Optimal Treatment. In: Sing, A. (eds) Zoonoses: Infections Affecting Humans and Animals. Springer, Cham. https://doi.org/10.1007/978-3-030-85877-3_29-1
Download citation
DOI: https://doi.org/10.1007/978-3-030-85877-3_29-1
Received:
Accepted:
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-85877-3
Online ISBN: 978-3-030-85877-3
eBook Packages: Springer Reference MedicineReference Module Medicine