{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T18:46:14Z","timestamp":1790793974372,"version":"4.1.0"},"reference-count":45,"publisher":"American Society for Microbiology","issue":"5","license":[{"start":{"date-parts":[[1999,5,1]],"date-time":"1999-05-01T00:00:00Z","timestamp":925516800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["Antimicrob Agents Chemother"],"published-print":{"date-parts":[[1999,5]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    The metacestode stage of\n                    <jats:italic>Echinococcus multilocularis<\/jats:italic>\n                    is the causative agent of alveolar echinococcosis (AE), a parasitic disease affecting the liver, with occasional metastasis into other organs. Benzimidazole carbamate derivatives such as mebendazole and albendazole are currently used for chemotherapeutic treatment of AE. Albendazole is poorly resorbed and is metabolically converted to its main metabolite albendazole sulfoxide, which is believed to be the active component, and further to albendazole sulfone. Chemotherapy with albendazole has been shown to have a parasitostatic rather than a parasitocidal effect; it is not effective in all cases, and the recurrence rate is rather high once chemotherapy is stopped. Thus, development of new means of chemotherapy of AE is needed. This could include modifications of benzimidazoles and elucidiation of the respective biological pathways. In this study we performed in vitro drug treatment of\n                    <jats:italic>E. multilocularis<\/jats:italic>\n                    metacestodes with albendazole sulfoxide and albendazole sulfone. High-performance liquid chromatography analysis of vesicle fluids showed that the drugs were taken up rapidly by the parasite. Transmission electron microscopic investigation of parasite tissues and nuclear magnetic resonance spectroscopy of vesicle fluids demonstrated that albendazole sulfoxide and albendazole sulfone had similar effects with respect to parasite ultrastructure and changes in metabolites in vesicle fluids. This study shows that the in vitro cultivation model presented here provides an ideal first-round test system for screening of antiparasite drugs.\n                  <\/jats:p>","DOI":"10.1128\/aac.43.5.1052","type":"journal-article","created":{"date-parts":[[2018,10,8]],"date-time":"2018-10-08T20:34:57Z","timestamp":1539030897000},"page":"1052-1061","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":79,"title":["Efficacies of Albendazole Sulfoxide and Albendazole Sulfone against In Vitro-Cultivated\n                    <i>Echinococcus multilocularis<\/i>\n                    Metacestodes"],"prefix":"10.1128","volume":"43","author":[{"given":"Katrin","family":"Ingold","sequence":"first","affiliation":[{"name":"<!--label omitted: 1-->Institute of Parasitology,1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Bigler","sequence":"additional","affiliation":[{"name":"<!--label omitted: 2-->Department of Chemistry and Biochemistry,2 and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wolfgang","family":"Thormann","sequence":"additional","affiliation":[{"name":"<!--label omitted: 3-->Department of Clinical Pharmacology,3 University of Berne, Berne, and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tania","family":"Cavaliero","sequence":"additional","affiliation":[{"name":"<!--label omitted: 4-->Institute of Parasitology, University of Zu\u0308rich, Zu\u0308rich,4 Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bruno","family":"Gottstein","sequence":"additional","affiliation":[{"name":"<!--label omitted: 1-->Institute of Parasitology,1"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew","family":"Hemphill","sequence":"additional","affiliation":[{"name":"<!--label omitted: 1-->Institute of Parasitology,1"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"crossref","first-page":"506","DOI":"10.4269\/ajtmh.1990.43.506","article-title":"Recurrence rate after discontinuation of long-term mebendazole therapy in alveolar echinococcosis (preliminary results).","volume":"43","author":"Ammann R. W.","year":"1990","unstructured":"Ammann R. W. Hirsbrunner R. Cotting J. Steiger U. Jacquier P. Eckert J. Recurrence rate after discontinuation of long-term mebendazole therapy in alveolar echinococcosis (preliminary results). Am. J. Trop. Med. Hyg. 43 1990 506 515","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"e_1_3_2_3_2","doi-asserted-by":"crossref","first-page":"735","DOI":"10.1002\/hep.1840190328","article-title":"Effect of chemotherapy on the larval mass and the long-term course of alveolar echinococcosis.","volume":"19","author":"Ammann R. W.","year":"1994","unstructured":"Ammann R. W. Ilitsch N. Marincek B. Freiburghaus A. U. Effect of chemotherapy on the larval mass and the long-term course of alveolar echinococcosis. Hepatology 19 1994 735 742","journal-title":"Hepatology"},{"key":"e_1_3_2_4_2","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1007\/BF00930903","article-title":"Improvement of liver resectional therapy by adjuvant chemotherapy in alveolar hydatid disease.","volume":"77","author":"Ammann R. W.","year":"1991","unstructured":"Ammann R. W. Swiss Echinococcosis Study Group Improvement of liver resectional therapy by adjuvant chemotherapy in alveolar hydatid disease. Parasitol. Res. 77 1991 290 293","journal-title":"Parasitol. Res."},{"key":"e_1_3_2_5_2","doi-asserted-by":"crossref","unstructured":"Barret\n              J.\n          Biochemical pathways in parasites\n          Analytical parasitology.\n              Rogan\n              M.\n          1997\n          1\n          31\n          Springer Verlag\n          Heidelberg Germany","DOI":"10.1007\/978-3-642-60345-7_1"},{"key":"e_1_3_2_6_2","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1016\/0020-7519(87)90100-7","article-title":"Studies on glucose metabolism in Hymenolepis diminuta using 13C nuclear magnetic resonance.","volume":"17","author":"Behm C. A.","year":"1987","unstructured":"Behm C. A. Bryant C. Jones A. J. Studies on glucose metabolism in Hymenolepis diminuta using 13C nuclear magnetic resonance. Int. J. Parasitol. 17 1987 1333 1341","journal-title":"Int. J. 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Hyg."},{"key":"e_1_3_2_12_2","doi-asserted-by":"crossref","first-page":"773","DOI":"10.1016\/0020-7519(87)90058-0","article-title":"The susceptibility of the mongolian gerbil (Meriones unguiculatus) and the OFa mouse strain to Echinococcus multilocularis\u2014ultrastructural aspects of the cysts.","volume":"17","author":"Delabre I.","year":"1987","unstructured":"Delabre I. Gabrion C. Contant F. Petavy A.-F. Deblock S. The susceptibility of the mongolian gerbil (Meriones unguiculatus) and the OFa mouse strain to Echinococcus multilocularis\u2014ultrastructural aspects of the cysts. Int. J. Parasitol. 17 1987 773 780","journal-title":"Int. J. Parasitol."},{"key":"e_1_3_2_13_2","unstructured":"Eckert\n              J.\n          Prospects for treatment of the metacestode stage of Echinococcus The biology of Echinococcus and hydatid disease.\n              Thompson\n              R. C. A.\n          1986\n          250\n          284\n          Allen & Unwin\n          London United Kingdom"},{"key":"e_1_3_2_14_2","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1007\/s004360050420","article-title":"Echinococcus granulosus: membrane permeability of secondary hydatid cysts to albendazolesulfoxide.","volume":"84","author":"Garcia-Llamazares J. L.","year":"1998","unstructured":"Garcia-Llamazares J. L. Alvarez-de-Felipe A. I. Redondo-Cardena P. A. Prieto-Fernandez J. G. Echinococcus granulosus: membrane permeability of secondary hydatid cysts to albendazolesulfoxide. Parasitol. Res. 84 1998 417 420","journal-title":"Parasitol. Res."},{"key":"e_1_3_2_15_2","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1016\/0140-6736(93)92361-V","article-title":"Randomized controlled trial of efficacy of albendazole in intra-abdominal hydatid disease.","volume":"342","author":"Gil-Grande L. A.","year":"1993","unstructured":"Gil-Grande L. A. Rodriguez-Caabeiro F. Prieto J. G. Sanchez-Ruano J. J. Brasa C. Aguilar L. Garcia-Hoz F. Casada N. Barcena R. Alvarez A. I. Randomized controlled trial of efficacy of albendazole in intra-abdominal hydatid disease. Lancet 342 1993 1269 1272","journal-title":"Lancet"},{"key":"e_1_3_2_16_2","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/S0065-308X(08)60024-X","article-title":"Echinococcus multilocularis infection: immunology and immunodiagnosis.","volume":"31","author":"Gottstein B.","year":"1992","unstructured":"Gottstein B. Echinococcus multilocularis infection: immunology and immunodiagnosis. Adv. Parasitol. 31 1992 321 379","journal-title":"Adv. Parasitol."},{"key":"e_1_3_2_17_2","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1017\/S0031182000049738","article-title":"The lethal effect of mebendazole on secondary Echinococcus granulosus cysticerci and Taenia pisiformis and tetrahydria of Mesocestoides corti.","volume":"70","author":"Heath D. 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In vitro cultivation and proliferation of Echinococcus multilocularis metacestode\n          Alveolar echinococcosis strategy for eradication of alveolar echinococcosis of the liver.\n              Urchino\n              J.\n              Sato\n              N.\n          1996\n          79\n          84\n          Fuji Shoin\n          Sapporo Japan"},{"key":"e_1_3_2_20_2","doi-asserted-by":"crossref","unstructured":"Hemphill\n              A.\n              Croft\n              S. L.\n          Electron microscopy in parasitology\n          Analytical parasitology.\n              Rogan\n              M.\n          1997\n          227\n          268\n          Springer Verlag\n          Heidelberg Germany","DOI":"10.1007\/978-3-642-60345-7_7"},{"key":"e_1_3_2_21_2","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1016\/0035-9203(89)90724-4","article-title":"Chemotherapy of Echinococcus infection in man with albendazole.","volume":"83","author":"Horten R. J.","year":"1989","unstructured":"Horten R. J. Chemotherapy of Echinococcus infection in man with albendazole. Trans. R. Soc. Trop. Med. Hyg. 83 1989 97 102","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"e_1_3_2_22_2","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1017\/S0031182098002406","article-title":"Identification of a novel laminated layer-associated protein in Echinococcus multilocularis metacestodes.","volume":"116","author":"Ingold K.","year":"1998","unstructured":"Ingold K. Gottstein B. Hemphill A. Identification of a novel laminated layer-associated protein in Echinococcus multilocularis metacestodes. Parasitology 116 1998 363 372","journal-title":"Parasitology"},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1128\/AAC.42.5.1052"},{"key":"e_1_3_2_24_2","first-page":"B1857","article-title":"Klinik und Therapie der alveol\u00e4ren Echinokokkose.","volume":"91","author":"Kern P.","year":"1994","unstructured":"Kern P. Wechsler J. G. Lauchart W. Kunz R. Klinik und Therapie der alveol\u00e4ren Echinokokkose. Deutsches Aerzteblatt-Aerztliche Mitteilungen 91 1994 B1857 B1863","journal-title":"Deutsches Aerzteblatt-Aerztliche Mitteilungen"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1016\/0169-4758(90)90227-U"},{"key":"e_1_3_2_26_2","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1006\/expr.1997.4190","article-title":"Echinococcus multilocularis metacestodes: immunological and immunocytochemical analysis of the relationships between alkaline phosphatase and the Em2 antigen.","volume":"87","author":"Lawton P.","year":"1997","unstructured":"Lawton P. Hemphill A. Deplazes P. Gottstein B. Sarciron M. E. Echinococcus multilocularis metacestodes: immunological and immunocytochemical analysis of the relationships between alkaline phosphatase and the Em2 antigen. Exp. Parasitol. 87 1997 142 149","journal-title":"Exp. Parasitol."},{"key":"e_1_3_2_27_2","unstructured":"L\u00f6scher\n              T.\n              von Sonnenburg\n              F.\n              Nothdurft\n              H. D.\n          Epidemiology and therapy of human echinococcosis in central Europe. 8th International Congress for Tropical Medicine and Malaria\n          1992"},{"key":"e_1_3_2_28_2","unstructured":"Mesarini-Wicki\n              B.\n          Long-term course of alveolar echinococcosis in 70 patients treated by benzimidazol derivates (mebendazole and albendazole) (1976\u20131989). Inaugural dissertation.\n          1991\n          Universit\u00e4tsspital Z\u00fcrich\n          Z\u00fcrich Switzerland"},{"key":"e_1_3_2_29_2","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1136\/gut.28.1.75","article-title":"Penetration of albendazolesulphoxide into hydatid cysts.","volume":"28","author":"Morris D. L.","year":"1987","unstructured":"Morris D. L. Chinnery J. B. Georgiou G. Stamatakis G. Golematis B. Penetration of albendazolesulphoxide into hydatid cysts. Gut 28 1987 75 80","journal-title":"Gut"},{"key":"e_1_3_2_30_2","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1007\/BF00931518","article-title":"Metabolites of alveolar Echinococcus as determined by 31P- and 1H-nuclear magnetic resonance spectroscopy.","volume":"78","author":"Novak M.","year":"1992","unstructured":"Novak M. Hameed N. Buist R. Backburn B. J. Metabolites of alveolar Echinococcus as determined by 31P- and 1H-nuclear magnetic resonance spectroscopy. Parasitol. Res. 78 1992 665","journal-title":"Parasitol. Res."},{"key":"e_1_3_2_31_2","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1007\/BF00931507","article-title":"Anti-tubulin immunohistochemistry study of Echinococcus granulosus protoscolices incubated with albendazole and albendazolesulphoxide in vitro.","volume":"81","author":"Perez-Serrano J.","year":"1995","unstructured":"Perez-Serrano J. Denegri G. Casado N. Bodega G. Rodriguez-Caabeiro F. Anti-tubulin immunohistochemistry study of Echinococcus granulosus protoscolices incubated with albendazole and albendazolesulphoxide in vitro. Parasitol. Res. 81 1995 438 440","journal-title":"Parasitol. Res."},{"key":"e_1_3_2_32_2","doi-asserted-by":"crossref","first-page":"576","DOI":"10.4269\/ajtmh.1987.36.576","article-title":"Spontaneous death of Echinococcus multilocularis: cases diagnosed by Em2 ELISA and clinical significance.","volume":"36","author":"Rausch R. L.","year":"1987","unstructured":"Rausch R. L. Wilson J. F. Schantz P. M. McMahon B. J. Spontaneous death of Echinococcus multilocularis: cases diagnosed by Em2 ELISA and clinical significance. Am. J. Trop. Med. Hyg. 36 1987 576 585","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"e_1_3_2_33_2","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1017\/S0031182000001116","article-title":"Echinococcus granulosus equinus: variation in the germinal layer of murine hydatids and evidence of autophagy.","volume":"89","author":"Richards K. S.","year":"1984","unstructured":"Richards K. S. Arme C. Bridges J. F. Echinococcus granulosus equinus: variation in the germinal layer of murine hydatids and evidence of autophagy. Parasitology 89 1984 35 37","journal-title":"Parasitology"},{"key":"e_1_3_2_34_2","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1080\/00034983.1989.11812375","article-title":"Echinococcus multilocularis: ultrastructural effect of in vivo albendazole and praziquantel therapy, singly and in combination.","volume":"83","author":"Richards K. S.","year":"1989","unstructured":"Richards K. S. Morris D. L. Taylor D. H. Echinococcus multilocularis: ultrastructural effect of in vivo albendazole and praziquantel therapy, singly and in combination. Ann Trop. Med. Parasitol. 83 1989 479 484","journal-title":"Ann Trop. Med. Parasitol."},{"key":"e_1_3_2_35_2","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1155\/1990\/47243","article-title":"Effect of albendazole on human hydatid cysts: an ultrastructural study.","volume":"2","author":"Richards K. S.","year":"1990","unstructured":"Richards K. S. Morris D. L. Effect of albendazole on human hydatid cysts: an ultrastructural study. HPB. Surg. 2 1990 105 112","journal-title":"HPB. Surg."},{"key":"e_1_3_2_36_2","doi-asserted-by":"crossref","first-page":"1437","DOI":"10.1016\/0020-7519(95)00055-0","article-title":"Development of an injectable formulation of albendazole and in vivo evaluation of its efficacy against Echinococcus multilocularis metacestode.","volume":"12","author":"Rodriguez J. M.","year":"1995","unstructured":"Rodriguez J. M. Bories C. Emery I. Fessi H. Devissaguet J. P. Liance M. Development of an injectable formulation of albendazole and in vivo evaluation of its efficacy against Echinococcus multilocularis metacestode. Int. J. Parasitol. 12 1995 1437 1441","journal-title":"Int. J. Parasitol."},{"key":"e_1_3_2_37_2","doi-asserted-by":"crossref","first-page":"226","DOI":"10.4269\/ajtmh.1997.56.226","article-title":"Increases in the effects of albendazole on Echinococcus multilocularis metacestodes by the dipeptide methyl ester (Phe-Phe-OMe).","volume":"56","author":"Sarciron M. E.","year":"1997","unstructured":"Sarciron M. E. Walchshofer N. Walbaum S. Arsac C. Descotes J. Petavy A.-F. Paris J. Increases in the effects of albendazole on Echinococcus multilocularis metacestodes by the dipeptide methyl ester (Phe-Phe-OMe). Am. J. Trop. Med. Hyg. 56 1997 226 230","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"e_1_3_2_38_2","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1093\/infdis\/162.6.1403","article-title":"Effects of albendazole on Echinococcus multilocularis infection in the Mongolian jird.","volume":"162","author":"Schantz P. M.","year":"1996","unstructured":"Schantz P. M. Brandt F. H. Dickinson C. M. Allen C. R. Robert J. M. Eberhard M. L. Effects of albendazole on Echinococcus multilocularis infection in the Mongolian jird. J. Infect. Dis. 162 1996 1403 1407","journal-title":"J. Infect. Dis."},{"key":"e_1_3_2_39_2","doi-asserted-by":"crossref","unstructured":"Siles-Lucas M. R. Felleisen A. Hemphill W. Wilson and B. Gottstein. Stage-specific expression of Echinococcus multilocularis protein 14-3-3. Mol. Biochem. Parasitol. 91: 281\u2013293.","DOI":"10.1016\/S0166-6851(97)00208-9"},{"key":"e_1_3_2_40_2","doi-asserted-by":"crossref","first-page":"1374","DOI":"10.1038\/2111374a0","article-title":"Factors controlling the differentiation of the hydatid organism, Echinococcus granulosus, into cystic or strobilar stages in vitro.","volume":"211","author":"Smyth J. D.","year":"1966","unstructured":"Smyth J. D. Howkins A. B. Barton M. Factors controlling the differentiation of the hydatid organism, Echinococcus granulosus, into cystic or strobilar stages in vitro. Nature 211 1966 1374 1377","journal-title":"Nature"},{"key":"e_1_3_2_41_2","doi-asserted-by":"crossref","unstructured":"Smyth\n              J. D.\n              McManus\n              D. 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