PDF herunterladen
Semin Liver Dis 2021; 41(03): 393-408
DOI: 10.1055/s-0041-1730925
Review Article

Hepatic Alveolar Echinococcosis

Solange Bresson-Hadni
1   Gastroenterology and Hepatology, Faculty of Medicine, University Hospitals of Geneva, Switzerland
2   Division of Tropical and Humanitarian Medicine, Faculty of Medicine, University Hospitals of Geneva, Faculty of Medicine, Switzerland
3   Laboratory of Parasitology-Mycology, National Reference Center for Echinococcosis, University Hospital of Besançon, Besançon, France
,
Laurent Spahr
1   Gastroenterology and Hepatology, Faculty of Medicine, University Hospitals of Geneva, Switzerland
,
François Chappuis
2   Division of Tropical and Humanitarian Medicine, Faculty of Medicine, University Hospitals of Geneva, Faculty of Medicine, Switzerland
› Institutsangaben
› Weitere Informationen
    Lizenzen und Reprints

Abstract

Hepatic alveolar echinococcosis (HAE) is a rare but severe zoonosis caused by the pseudotumoral intrahepatic development of the larval stage of the tapeworm Echinococcus multilocularis. HAE is present only in the Northern Hemisphere, predominantly in China. Currently, there is a significant resurgence of cases in historically endemic areas associated with emergence of HAE in countries not previously concerned. Today, in European countries, HAE is often discovered by chance; however, clinicians should be made aware of opportunistic infections that progressively emerged recently as a result of therapeutic or pathological immunosuppression. Ultrasonography is the key first-line diagnostic procedure, with specific serology providing confirmation in 95% of the cases. Albendazole, only parasitostatic, is the mainstay for treatment. Surgical resection, if feasible, is the gold standard for treatment, and more patients are currently eligible for this option because of an earlier diagnosis. The prognosis has considerably improved but remains poor in countries where access to care is less favorable.

Keywords

Echinococcus multilocularis - alveolar echinococcosis - liver surgery - instrumental procedures - albendazole


Publikationsverlauf

Artikel online veröffentlicht:
23. Juni 2021

© 2021. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Wen H, Vuitton L, Tuxun T. et al. Echinococcosis: advances in the 21st century. Clin Microbiol Rev 2019; 32 (02) 1-39
    PubMedGoogle Scholar
  • 2 Atanasov G, Benckert C, Thelen A. et al. Alveolar echinococcosis-spreading disease challenging clinicians: a case report and literature review. World J Gastroenterol 2013; 19 (26) 4257-4261
    CrossrefPubMedGoogle Scholar
  • 3 Buttenschoen K, Carli Buttenschoen D, Gruener B. et al. Long-term experience on surgical treatment of alveolar echinococcosis. Langenbecks Arch Surg 2009; 394 (04) 689-698
    CrossrefPubMedGoogle Scholar
  • 4 Vuitton DA, Gottstein B. Echinococcus multilocularis and its intermediate host: a model of parasite-host interplay. J Biomed Biotechnol 2010; 2010: 923193
    CrossrefPubMedGoogle Scholar
  • 5 Gottstein B, Hemphill A. Echinococcus multilocularis: the parasite-host interplay. Exp Parasitol 2008; 119 (04) 447-452
    CrossrefPubMedGoogle Scholar
  • 6 Bresson-Hadni S, Vuitton D-A, Bartholomot B. et al. A twenty-year history of alveolar echinococcosis: analysis of a series of 117 patients from eastern France. Eur J Gastroenterol Hepatol 2000; 12 (03) 327-336
    CrossrefPubMedGoogle Scholar
  • 7 Beldi G, Vuitton D, Lachenmayer A. et al. Is ex vivo liver resection and autotransplantation a valid alternative treatment for end-stage hepatic alveolar echinococcosis in Europe?. J Hepatol 2019; 70 (05) 1030-1031
    CrossrefPubMedGoogle Scholar
  • 8 Brunetti E, Kern P, Vuitton DA. Writing Panel for the WHO-IWGE. Expert consensus for the diagnosis and treatment of cystic and alveolar echinococcosis in humans. Acta Trop 2010; 114 (01) 1-16
    CrossrefPubMedGoogle Scholar
  • 9 Kern P, Menezes da Silva A, Akhan O. et al. The echinococcoses: diagnosis, clinical management and burden of disease. Adv Parasitol 2017; 96: 259-369
    Google Scholar
  • 10 Hemphill A, Stadelmann B, Rufener R. et al. Treatment of echinococcosis: albendazole and mebendazole--what else?. Parasite 2014; 21: 70
    CrossrefPubMedGoogle Scholar
  • 11 Bresson-Hadni S, Koch S, Miguet J-Ph. et al; European Group of Clinicians. Indications and results of liver transplantation for Echinococcus alveolar infection: an overview. Langenbecks Arch Surg 2003; 388 (04) 231-238
    CrossrefPubMedGoogle Scholar
  • 12 Aliakbarian M, Tohidinezhad F, Eslami S, Akhavan-Rezayat K. Liver transplantation for hepatic alveolar echinococcosis: literature review and three new cases. Infect Dis (Lond) 2018; 50 (06) 452-459
    CrossrefPubMedGoogle Scholar
  • 13 Aji T, Dong JH, Shao YMZ. et al. Ex vivo liver resection and autotransplantation as alternative to allotransplantation for end-stage hepatic alveolar echinococcosis. J Hepatol 2018; 69 (05) 1037-1046
    CrossrefPubMedGoogle Scholar
  • 14 Vuitton DA, Wang Q, Zhou HX. et al. 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 (Engl) 2011; 124 (18) 2943-2953
    PubMedGoogle Scholar
  • 15 Eckert J, Conraths FJ, Tackmann K. Echinococcosis: an emerging or re-emerging zoonosis?. Int J Parasitol 2000; 30 (12-13): 1283-1294
    CrossrefPubMedGoogle Scholar
  • 16 Eckert J, Thompson RCA. Historical aspects of echinococcosis. Adv Parasitol 2017; 95 (95) 1-64
    PubMedGoogle Scholar
  • 17 Tappe D, Frosch M. Rudolf Virchow and the recognition of alveolar echinococcosis, 1850s. Emerg Infect Dis 2007; 13 (05) 732-735
    PubMedGoogle Scholar
  • 18 Devleesschauwer B, Bouwknegt M, Dorny P. et al. Risk ranking of foodborne parasites: state of the art. Food Waterborne Parasitol 2017; 8-9: 1-13
    CrossrefPubMedGoogle Scholar
  • 19 Bouwknegt M, Devleesschauwer B, Graham H. et al; The Euro-FBP Workshop Participants. Prioritisation of food-borne parasite in Europe 2016. Euro Surveill 2018; 23 (09) 17-00161
    CrossrefPubMedGoogle Scholar
  • 20 Torgerson PR, Keller K, Magnotta M, Ragland N. The global burden of alveolar echinococcosis. PLoS Negl Trop Dis 2010; 4 (06) e722
    CrossrefPubMedGoogle Scholar
  • 21 World Health Organization. 2015 WHO estimates of the global burden of foodborne diseases. Foodborne disease burden epidemiology reference group 2007–2015.. Accessed January 30, 2021 at: https://apps.who.int/iris/bitstream/handle/10665/199350/9789241565165_eng.pdf;jsessionid=5B771F5A4743970E31E68CF1FD99186F?sequence=1
    Google Scholar
  • 22 Deplazes P, Rinaldi L, Alvarez Rojas CA. et al. Global distribution of alveolar and cystic echinococcosis. Adv Parasitol 2017; 95: 315-493
    CrossrefPubMedGoogle Scholar
  • 23 Combes B, Comte S, Raton V. et al. Westward spread of Echinococcus multilocularis in foxes, France, 2005–2010. Emerg Infect Dis 2012; 18: 2059-2062
    CrossrefPubMedGoogle Scholar
  • 24 Chauchet A, Grenouillet F, Knapp J. et al; FrancEchino Network. Increased incidence and characteristics of alveolar echinococcosis in patients with immunosuppression-associated conditions. Clin Infect Dis 2014; 59 (08) 1095-1104
    CrossrefPubMedGoogle Scholar
  • 25 Schweiger A, Ammann RW, Candinas D. et al. Human alveolar echinococcosis after fox population increase, Switzerland. Emerg Infect Dis 2007; 13 (06) 878-882
    CrossrefPubMedGoogle Scholar
  • 26 Piarroux M, Piarroux R, Giorgi R. et al. Clinical features and evolution of alveolar echinococcosis in France from 1982 to 2007: results of a survey in 387 patients. J Hepatol 2011; 55 (05) 1025-1033
    CrossrefPubMedGoogle Scholar
  • 27 Sailer M, Soelder B, Allerberger F, Zaknun D, Feichtinger H, Gottstein B. Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J Pediatr 1997; 130 (02) 320-323
    CrossrefPubMedGoogle Scholar
  • 28 Vuitton DA, Demonmerot F, Knapp J. et al. Clinical epidemiology of human AE in Europe. Vet Parasitol 2015; 213 (3-4): 110-120
    CrossrefPubMedGoogle Scholar
  • 29 Massolo A, Klein C, Kowalewska-Grochowska K. et al. European Echinococcus multilocularis identified in patients in Canada. N Engl J Med 2019; 381 (04) 384-385
    CrossrefPubMedGoogle Scholar
  • 30 Olivier CJ, Li H, Auer RN, Dixit D. Disseminated alveolar echinococcosis in a 74-year-old woman presenting with focal seizure. CMAJ 2019; 191 (34) E940-E943
    CrossrefPubMedGoogle Scholar
  • 31 Bart JM, Knapp J, Gottstein B. et al. EmsB, a tandem repeated multi-loci microsatellite, new tool to investigate the genetic diversity of Echinococcus multilocularis . Infect Genet Evol 2006; 6 (05) 390-400
    CrossrefPubMedGoogle Scholar
  • 32 Valot B, Knapp J, Umhang G, Grenouillet F, Millon L. Genomic characterization of EmsB microsatellite loci in Echinococcus multilocularis . Infect Genet Evol 2015; 32: 338-341
    CrossrefPubMedGoogle Scholar
  • 33 Knapp J, Gottstein B, Bretagne S. et al. Genotyping Echinococcus multilocularis in human alveolar echinococcosis patients: an EmsB microsatellite analysis. Pathogens 2020; 9 (04) 282
    CrossrefPubMedGoogle Scholar
  • 34 Knapp J, Gottstein B, Saarma U, Millon L. Taxonomy, phylogeny and molecular epidemiology of Echinococcus multilocularis: from fundamental knowledge to health ecology. Vet Parasitol 2015; 213 (3-4): 85-91
    CrossrefPubMedGoogle Scholar
  • 35 Umhang G, Bastien M, Renault C. et al. A flotation/sieving method to detect Echinococcus multilocularis and Toxocara spp. eggs in soil by real-time PCR. Parasite 2017; 24: 28
    CrossrefPubMedGoogle Scholar
  • 36 Miguet JP, Bresson-Hadni S. Alveolar echinococcosis of the liver. J Hepatol 1989; 8 (03) 373-379
    CrossrefPubMedGoogle Scholar
  • 37 Vuitton DA, McManus DP, Rogan MT. et al; World Association of Echinococcosis. International consensus on terminology to be used in the field of echinococcoses. Parasite 2020; 27: 41
    CrossrefPubMedGoogle Scholar
  • 38 Gottstein B, Soboslay P, Ortona E, Wang J, Siracusano A, Vuitton DA. Immunology of alveolar and cystic echinococcosis (AE and CE). Adv Parasitol 2017; 96: 1-54
    CrossrefPubMedGoogle Scholar
  • 39 Gottstein B, Wang J, Boubaker G. et al. Susceptibility versus resistance in alveolar echinococcosis (larval infection with Echinococcus multilocularis). Vet Parasitol 2015; 213 (3-4): 103-109
    CrossrefPubMedGoogle Scholar
  • 40 Bresson-Hadni S, Laplante JJ, Lenys D. et al. Seroepidemiological screening of E. multilocularis infection in 7,884 subjects of a European endemic area for alveolar echinococcosis . Am J Trop Hyg 1994; 51: 837-846
    CrossrefPubMedGoogle Scholar
  • 41 Jensen B, Reuter S, Kratzer W. et al. Long-term seropositivity against Echinococcus multilocularis in an epidemiological follow-up study in southwestern Germany (Römerstein). Infection 2001; 29 (06) 310-314
    CrossrefPubMedGoogle Scholar
  • 42 Romig T, Kratzer W, Kimmig P. et al; Römerstein Study Group. An epidemiologic survey of human alveolar echinococcosis in southwestern Germany. Am J Trop Med Hyg 1999; 61 (04) 566-573
    CrossrefPubMedGoogle Scholar
  • 43 Rausch RL, Wilson JF, Schantz PM, McMahon BJ. Spontaneous death of Echinococcus multilocularis: cases diagnosed serologically (by Em2 ELISA) and clinical significance. Am J Trop Med Hyg 1987; 36 (03) 576-585
    CrossrefPubMedGoogle Scholar
  • 44 Beldi G, Müller N, Gottstein B. Alveolar echinococcosis. Swiss medical. Forum 2017; 17 (36) 760-766
    PubMedGoogle Scholar
  • 45 Ricard-Blum S, Bresson-Hadni S, Vuitton DA, Ville G, Grimaud JA. Hydroxypyridinium collagen cross-links in human liver fibrosis: study of alveolar echinococcosis. Hepatology 1992; 15 (04) 599-602
    CrossrefPubMedGoogle Scholar
  • 46 Ricard-Blum S, Bresson-Hadni S, Guerret S. et al. Mechanism of collagen network stabilization in human irreversible granulomatous liver fibrosis. Gastroenterology 1996; 111 (01) 172-182
    CrossrefPubMedGoogle Scholar
  • 47 Vuitton DA. The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite?. Acta Trop 2003; 85 (02) 119-132
    CrossrefPubMedGoogle Scholar
  • 48 Vuitton DA. Echinococcosis and allergy. Clin Rev Allergy Immunol 2004; 26 (02) 93-104
    CrossrefPubMedGoogle Scholar
  • 49 Vuitton DA, Zhang SL, Yang Y. et al. Survival strategy of Echinococcus multilocularis in the human host. Parasitol Int 2006; 55 (Suppl): S51-S55
    CrossrefPubMedGoogle Scholar
  • 50 Wang J, Gottstein B. Immunoregulation in larval Echinococcus multilocularis infection. Parasite Immunol 2016; 38 (03) 182-192
    CrossrefPubMedGoogle Scholar
  • 51 Ma X, Zhang X, Liu J. et al. The correlations between Th1 and Th2 cytokines in human alveolar echinococcosis. BMC Infect Dis 2020; 20 (01) 414
    CrossrefPubMedGoogle Scholar
  • 52 Nono JK, Lutz MB, Brehm K. Expansion of host regulatory T cells by secreted products of the tapeworm Echinococcus multilocularis . Front Immunol 2020; 11: 798
    CrossrefPubMedGoogle Scholar
  • 53 Wang J, Müller S, Lin R. et al. Depletion of FoxP3+ Tregs improves control of larval Echinococcus multilocularis infection by promoting co-stimulation and Th1/17 immunity. Immun Inflamm Dis 2017; 5 (04) 435-447
    CrossrefPubMedGoogle Scholar
  • 54 Wang J, Cardoso R, Marreros N. et al. Foxp3+ T regulatory cells as a potential target for immunotherapy against primary infection with Echinococcus multilocularis eggs. Infect Immun 2018; 86 (10) e00542-e18
    CrossrefPubMedGoogle Scholar
  • 55 Godot V, Harraga S, Beurton I. et al. Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. II. Influence of the HLA B8, DR3, DQ2 haplotype. Clin Exp Immunol 2000; 121 (03) 491-498
    CrossrefPubMedGoogle Scholar
  • 56 Gottstein B, Bettens F. Association between HLA-DR13 and susceptibility to alveolar echinococcosis. J Infect Dis 1994; 169 (06) 1416-1417
    CrossrefPubMedGoogle Scholar
  • 57 Eiermann TH, Bettens F, Tiberghien P. et al. HLA and alveolar echinococcosis. Tissue Antigens 1998; 52 (02) 124-129
    CrossrefPubMedGoogle Scholar
  • 58 Zhang S, Penfornis A, Harraga S. et al. Polymorphisms of the TAP1 and TAP2 genes in human alveolar echinococcosis. Eur J Immunogenet 2003; 30 (02) 133-139
    CrossrefPubMedGoogle Scholar
  • 59 Magy N, Bresson-Hadni S, Augé B, Toussirot E, Wendling D. Polyarthritis accompanying alveolar echinococcosis or the icing on the cake [in French]. Rev Med Interne 2000; 21 (05) 460-461
    CrossrefPubMedGoogle Scholar
  • 60 Bresson-Hadni S, Humbert P, Paintaud G. et al. Skin localization of alveolar echinococcosis of the liver. J Am Acad Dermatol 1996; 34 (5, Pt 2): 873-877
    CrossrefPubMedGoogle Scholar
  • 61 Beaussant-Cohen S, Richou C, Lenoir M. et al. MR imaging features of peritoneal alveolar echinococcosis. Diagn Interv Imaging 2018; 99 (7–8): 511-512
    CrossrefPubMedGoogle Scholar
  • 62 Caire Nail L, Reimundes ER, Weibel Galluzo C. et al. Disseminated alveolar echinococcosis resembling metastatic malignancy: a case report. J Med Case Rep 2017; 11 (01) 113
    CrossrefPubMedGoogle Scholar
  • 63 Algros MP, Majo F, Bresson-Hadni S. et al. Intracerebral alveolar echinococcosis. Infection 2003; 31 (01) 63-65
    CrossrefPubMedGoogle Scholar
  • 64 Yang YR, Vuitton DA, Jones MK, Craig PS, McManus DP. Brain metastasis of alveolar echinococcosis in a hyperendemic focus of Echinococcus multilocularis infection. Trans R Soc Trop Med Hyg 2005; 99 (12) 937-941
    CrossrefPubMedGoogle Scholar
  • 65 Reuter S, Seitz HM, Kern P, Junghanss T. Extrahepatic alveolar echinococcosis without liver involvement: a rare manifestation. Infection 2000; 28 (03) 187-192
    CrossrefPubMedGoogle Scholar
  • 66 Faucher JF, Descotes-Genon C, Hoen B. et al. Hints for control of infection in unique extrahepatic vertebral alveolar echinococcosis. Infection 2017; 45 (03) 365-368
    CrossrefPubMedGoogle Scholar
  • 67 Frossard JL, Armenian B, Gottstein B. et al. A case of alveolar echinococcosis restricted to the pancreas. Am J Gastroenterol 1997; 92 (11) 2117-2119
    PubMedGoogle Scholar
  • 68 Grüner B, Kern P, Mayer B. et al. Comprehensive diagnosis and treatment of alveolar echinococcosis: a single-center, long-term observational study of 312 patients in Germany. GMS Infect Dis 2017; 5: Doc01
    PubMedGoogle Scholar
  • 69 Graeter T, Bao HH, Shi R. et al; XUUB Consortium. Evaluation of intrahepatic manifestation and distant extrahepatic disease in alveolar echinococcosis. World J Gastroenterol 2020; 26 (29) 4302-4315
    CrossrefPubMedGoogle Scholar
  • 70 Bartholomot G, Vuitton DA, Harraga S. et al. Combined ultrasound and serologic screening for hepatic alveolar echinococcosis in central China. Am J Trop Med Hyg 2002; 66 (01) 23-29
    CrossrefPubMedGoogle Scholar
  • 71 Bresson-Hadni S, Delabrousse E, Blagosklonov O. et al. Imaging aspects and non-surgical interventional treatment in human alveolar echinococcosis. Parasitol Int 2006; 55 (Suppl): S267-S272
    CrossrefPubMedGoogle Scholar
  • 72 Liu W, Delabrousse E, Blagosklonov O. et al. Innovation in hepatic alveolar echinococcosis imaging: best use of old tools, and necessary evaluation of new ones. Parasite 2014; 21: 74
    CrossrefPubMedGoogle Scholar
  • 73 Brumpt E, Blagosklonov O, Calame P. et al. Alveolar echinococcosis hepatic lesions: correlation between calcifications at CT and FDG-PET/CT metabolic activity. Infection 2019; 47 (06) 955-960
    CrossrefPubMedGoogle Scholar
  • 74 Graeter T, Kratzer W, Oeztuerk S. et al. Proposal of a computed tomography classification for hepatic alveolar echinococcosis. World J Gastroenterol 2016; 22 (13) 3621-3631
    CrossrefPubMedGoogle Scholar
  • 75 Rubini-Campagna A, Kermarrec E, Laurent V, Régent D. Hepatic and extrahepatic alveolar echinococcosis: CT and MR imaging features [in French]. J Radiol 2008; 89 (06) 765-774
    CrossrefPubMedGoogle Scholar
  • 76 Reuter S, Nüssle K, Kolokythas O. et al. Alveolar liver echinococcosis: a comparative study of three imaging techniques. Infection 2001; 29 (03) 119-125
    CrossrefPubMedGoogle Scholar
  • 77 Kodama Y, Fujita N, Shimizu T. et al. Alveolar echinococcosis: MR findings in the liver. Radiology 2003; 228 (01) 172-177
    CrossrefPubMedGoogle Scholar
  • 78 Azizi A, Blagosklonov O, Lounis A. et al. Alveolar echinococcosis: correlation between hepatic MRI findings and FDG-PET/CT metabolic activity. Abdom Imaging 2015; 40 (01) 56-63
    CrossrefPubMedGoogle Scholar
  • 79 Reuter S, Buck A, Manfras B. et al. Structured treatment interruption in patients with alveolar echinococcosis. Hepatology 2004; 39 (02) 509-517
    CrossrefPubMedGoogle Scholar
  • 80 Reuter S, Schirrmeister H, Kratzer W, Dreweck C, Reske SN, Kern P. Pericystic metabolic activity in alveolar echinococcosis: assessment and follow-up by positron emission tomography. Clin Infect Dis 1999; 29 (05) 1157-1163
    CrossrefPubMedGoogle Scholar
  • 81 Caoduro C, Porot C, Vuitton DA. et al. The role of delayed 18F-FDG PET imaging in the follow-up of patients with alveolar echinococcosis. J Nucl Med 2013; 54 (03) 358-363
    CrossrefPubMedGoogle Scholar
  • 82 Carmena D, Benito A, Eraso E. The immunodiagnosis of Echinococcus multilocularis infection. Clin Microbiol Infect 2007; 13 (05) 460-475
    CrossrefPubMedGoogle Scholar
  • 83 Ito A, Nakao M, Sako Y. Echinococcosis: serological detection of patients and molecular identification of parasites. Future Microbiol 2007; 2 (04) 439-449
    CrossrefPubMedGoogle Scholar
  • 84 Gottstein B, Lachenmayer A, Beldi G. et al. Diagnostic and follow-up performance of serological tests for different forms/courses of alveolar echinococcosis. Food Waterborne Parasitol 2019; 16: e00055
    CrossrefPubMedGoogle Scholar
  • 85 Georges S, Villard O, Filisetti D. et al. Usefulness of PCR analysis for diagnosis of alveolar echinococcosis with unusual localizations: two case studies. J Clin Microbiol 2004; 42 (12) 5954-5956
    CrossrefPubMedGoogle Scholar
  • 86 Roelfsema JH, Nozari N, Pinelli E, Kortbeek LM. Novel PCRs for differential diagnosis of cestodes. Exp Parasitol 2016; 161: 20-26
    CrossrefPubMedGoogle Scholar
  • 87 Kern P, Wen H, Sato N. et al. WHO classification of alveolar echinococcosis: principles and application. Parasitol Int 2006; 55 (Suppl): S283-S287
    CrossrefPubMedGoogle Scholar
  • 88 Vuitton DA, Bresson-Hadni S. Alveolar echinococcosis: evaluation of therapeutic strategies. Expert Opin Orphan Drugs 2014; 2 (01) 67-86
    Google Scholar
  • 89 Salm LA, Lachenmayer A, Perrodin SF, Candinas D, Beldi G. Surgical treatment strategies for hepatic alveolar echinococcosis. Food Waterborne Parasitol 2019; 15: e00050
    CrossrefPubMedGoogle Scholar
  • 90 Buttenschoen K, Schorcht P, Reuter S, Buttenschoen DC, Kern P, Beger HG. Surgical therapy of alveolar echinococcosis and long-term outcome [in German]. Chirurg 2001; 72 (05) 566-572
    CrossrefPubMedGoogle Scholar
  • 91 Sato N, Namieno T, Furuya K. et al. Contribution of mass screening system to resectability of hepatic lesions involving Echinococcus multilocularis . J Gastroenterol 1997; 32 (03) 351-354
    CrossrefPubMedGoogle Scholar
  • 92 Hillenbrand A, Gruener B, Kratzer W. et al. Impact of safe distance on long-term outcome after surgical therapy of alveolar echinococcosis. World J Surg 2017; 41 (04) 1012-1018
    CrossrefPubMedGoogle Scholar
  • 93 Joliat GR, Melloul E, Petermann D. et al. Outcomes after liver resection for hepatic alveolar echinococcosis: a single-center cohort study. World J Surg 2015; 39 (10) 2529-2534
    CrossrefPubMedGoogle Scholar
  • 94 Ishizu H, Uchino J, Sato N, Aoki S, Suzuki K, Kuribayashi H. Effect of albendazole on recurrent and residual alveolar echinococcosis of the liver after surgery. Hepatology 1997; 25 (03) 528-531
    CrossrefPubMedGoogle Scholar
  • 95 Tamarozzi F, Horton J, Muhtarov M. et al. A case for the adoption of continuous albendazole treatment regimen for human echinococcal infections. Plos Neglect Trop Dis 2020; 14 (09) e0008566
    CrossrefPubMedGoogle Scholar
  • 96 Pawluk SA, Roels CA, Wilby KJ, Ensom MH. A review of pharmacokinetic drug-drug interactions with the anthelmintic medications albendazole and mebendazole. Clin Pharmacokinet 2015; 54 (04) 371-383
    CrossrefPubMedGoogle Scholar
  • 97 Bresson-Hadni S, Montange D, Richou C. et al. Tobacco, cannabis, and liquorice: hidden players altering albendazole metabolism in patients with hepatic alveolar echinococcosis. J Hepatol 2021; 74 (02) 471-473
    CrossrefPubMedGoogle Scholar
  • 98 Tamarozzi F, Vuitton L, Brunetti E, Vuitton DA, Koch S. Non-surgical and non-chemical attempts to treat echinococcosis: Do they work?. Parasite 2014; 21 (75) 75
    CrossrefPubMedGoogle Scholar
  • 99 Vuitton DA, Azizi A, Richou C. et al. Current interventional strategy for the treatment of hepatic alveolar echinococcosis. Expert Rev Anti Infect Ther 2016; 14 (12) 1179-1194
    CrossrefPubMedGoogle Scholar
  • 100 Stojkovic M, Junghanss T, Veeser M, Weber TF, Sauer P. Endoscopic treatment of biliary stenosis in patients with alveolar echinococcosis. Report of 7 consecutive patients with serial ERC approach. PLoS Negl Trop Dis 2016; 10 (02) e0004278
    CrossrefPubMedGoogle Scholar
  • 101 Ambregna S, Koch S, Sulz MC. et al. A European survey of perendoscopic treatment of biliary complications in patients with alveolar echinococcosis. Expert Rev Anti Infect Ther 2017; 15 (01) 79-88
    CrossrefPubMedGoogle Scholar
  • 102 Koch S, Bresson-Hadni S, Miguet JP. et al; European Collaborating Clinicians. Experience of liver transplantation for incurable alveolar echinococcosis: a 45-case European collaborative report. Transplantation 2003; 75 (06) 856-863
    CrossrefPubMedGoogle Scholar
  • 103 Bresson-Hadni S, Blagosklonov O, Knapp J. et al. Should possible recurrence of disease contraindicate liver transplantation in patients with end-stage alveolar echinococcosis? A 20-year follow-up study. Liver Transpl 2011; 17 (07) 855-865
    CrossrefPubMedGoogle Scholar
  • 104 Aydinli B, Ozturk G, Arslan S. et al. Liver transplantation for alveolar echinococcosis in an endemic region. Liver Transpl 2015; 21 (08) 1096-1102
    CrossrefPubMedGoogle Scholar
  • 105 Chen KF, Tang YY, Wang R. et al. The choose of different surgical therapies of hepatic alveolar echinococcosis: a single-center retrospective case-control study. Medicine (Baltimore) 2018; 97 (08) e0033
    CrossrefPubMedGoogle Scholar
  • 106 Bresson-Hadni S, Koch S, Beurton I. et al. Primary disease recurrence after liver transplantation for alveolar echinococcosis: long-term evaluation in 15 patients. Hepatology 1999; 30 (04) 857-864
    CrossrefPubMedGoogle Scholar
  • 107 Tappe D, Frosch M, Sako Y. et al. 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 2009; 80 (05) 792-797
    CrossrefPubMedGoogle Scholar
  • 108 Gottstein B, Wang J, Blagosklonov O. et al. Echinococcus metacestode: in search of viability markers. Parasite 2014; 21: 63
    CrossrefPubMedGoogle Scholar
  • 109 Bardonnet K, Vuitton DA, Grenouillet F. et al. 30-yr course and favorable outcome of alveolar echinococcosis despite multiple metastatic organ involvement in a non-immune suppressed patient. Ann Clin Microbiol Antimicrob 2013; 12: 1
    CrossrefPubMedGoogle Scholar
  • 110 Crouzet J, Grenouillet F, Delabrousse E. et al. 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 2010; 16 (06) 788-791
    CrossrefPubMedGoogle Scholar
  • 111 Amman RW, Stumpe KD, Grimm F. et al. Outcome after long-term benzimidazole treatment in 11 patients with non-resectable alveolar echinococcosis with negative FDG-PET/CT and anti-Emll/3–10 serology. PLoS Negl Trop Dis 2015; ; (epub ahead of print) DOI: 10.1371/journal.pntd.0003964.
    CrossrefPubMedGoogle Scholar
  • 112 Torgerson PR, Schweiger A, Deplazes P. et al. Alveolar echinococcosis: from a deadly disease to a well-controlled infection. Relative survival and economic analysis in Switzerland over the last 35 years. J Hepatol 2008; 49 (01) 72-77
    CrossrefPubMedGoogle Scholar
  • 113 Cairang Y, Zhang L, Ren B. et al. Efficacy and safety of ultrasound-guided percutaneous microwave ablation for the treatment of hepatic alveolar echinococcosis: a preliminary study. Medicine (Baltimore) 2017; 96 (27) e7137
    CrossrefPubMedGoogle Scholar
  • 114 Zheng Y. Strategies of Echinococcus species responses to immune attacks: implications for therapeutic tool development. Int Immunopharmacol 2013; 17 (03) 495-501
    CrossrefPubMedGoogle Scholar
  • 115 Siles-Lucas M, Casulli A, Cirilli R, Carmena D. Progress in the pharmacological treatment of human cystic and alveolar echinococcosis: compounds and therapeutic targets. PLoS Negl Trop Dis 2018; 12 (04) e0006422
    CrossrefPubMedGoogle Scholar
  • 116 Lundström-Stadelmann B, Rufener R, Ritler D. et al. The importance of being parasiticidal. An update on drug development for the treatment of alveolar echinococcosis. Food Waterborne Parasitol 2019; 15: e00040
    CrossrefPubMedGoogle Scholar
  • 117 Kern P, Abboud P, Kern WV. et al. Critical appraisal of nitazoxanide for the treatment of alveolar echinococcosis. Am J Trop Med Hyg 2008; 79 (6, Suppl): 125
    PubMedGoogle Scholar
  • 118 Reuter S, Buck A, Grebe O, Nüssle-Kügele K, Kern P, Manfras BJ. Salvage treatment with amphotericin B in progressive human alveolar echinococcosis. Antimicrob Agents Chemother 2003; 47 (11) 3586-3591
    CrossrefPubMedGoogle Scholar
  • 119 Rufener R, Ritler D, Zielinski J. et al. Activity of mefloquine and mefloquine derivatives against Echinococcus multilocularis . Int J Parasitol Drugs Drug Resist 2018; 8 (02) 331-340
    CrossrefPubMedGoogle Scholar
  • 120 Harraga S, Godot V, Bresson-Hadni S. et al. 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 1999; 29 (01) 205-206
    CrossrefPubMedGoogle Scholar
  • 121 Godot V, Harraga S, Podoprigora G, Liance M, Bardonnet K, Vuitton DA. IFN alpha-2a protects mice against a helminth infection of the liver and modulates immune responses. Gastroenterology 2003; 124 (05) 1441-1450
    CrossrefPubMedGoogle Scholar
  • 122 Wang J, Jebbawi F, Bellanger AP, Beldi G, Millon L, Gottstein B. Immunotherapy of alveolar echinococcosis via PD-1/PD-L1 immune checkpoint blockade in mice. Parasite Immunol 2018; 40 (12) e12596
    CrossrefPubMedGoogle Scholar
  • 123 Zhang C, Lin R, Li Z. et al. Immune exhaustion of T Cells in alveolar echinococcosis patients and its reversal by blocking checkpoint receptor TIGIT in a murine model. Hepatology 2020; 71 (04) 1297-1315
    CrossrefPubMedGoogle Scholar
  • 124 Lachenmayer A, Gebbers D, Gottstein B. et al. Elevated incidence of alveolar echinococcosis in immunocompromised patients. Food Waterborne Parasito 2019; 16: e00060
    CrossrefPubMedGoogle Scholar
  • 125 Gottstein B, Stojkovic M, Vuitton DA, Millon L, Marcinkute A, Deplazes P. Threat of alveolar echinococcosis to public health--a challenge for Europe. Trends Parasitol 2015; 31 (09) 407-412
    CrossrefPubMedGoogle Scholar
  • 126 Knapp J, Giraudoux P, Combes B. et al. Rural and urban distribution of wild and domestic carnivore stools in the context of Echinococcus multilocularis environmental exposure. Int J Parasitol 2018; 48 (12) 937-946
    CrossrefPubMedGoogle Scholar
  • 127 Bastien M, Vaniscotte A, Combes B. et al. High density of fox and cat faeces in kitchen gardens and resulting rodent exposure to Echinococcus multilocularis and Toxoplasma gondii. Folia Parasitol (Praha) 2018; 65: 65
    CrossrefPubMedGoogle Scholar