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Echinococcus metacestodes as laboratory models for the screening of drugs against cestodes and trematodes

Published online by Cambridge University Press:  21 September 2009

A. HEMPHILL ,
B. STADELMANN ,
S. SCHOLL ,
J. MÜLLER ,
M. SPILIOTIS ,
N. MÜLLER ,
B. GOTTSTEIN  and
M. SILES-LUCAS
A. HEMPHILL*
Affiliation:
Institute of Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012Berne, Switzerland
B. STADELMANN
Affiliation:
Institute of Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012Berne, Switzerland
S. SCHOLL
Affiliation:
Institute of Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012Berne, Switzerland
J. MÜLLER
Affiliation:
Institute of Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012Berne, Switzerland
M. SPILIOTIS
Affiliation:
Institute of Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012Berne, Switzerland
N. MÜLLER
Affiliation:
Institute of Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012Berne, Switzerland
B. GOTTSTEIN
Affiliation:
Institute of Parasitology, University of Berne, Laenggass-Strasse 122, CH-3012Berne, Switzerland
M. SILES-LUCAS
Affiliation:
Parasitology Laboratory, Instituto de Recursos Naturales y Agrobiología de Salamanca (CSIC), Cordel de Merinas 40-52, 37008Salamanca, Spain
*
*Corresponding author: Andrew Hemphill, Institute of Parasitology Vetsuisse Faculty, University of BerneLänggass-Strasse 122, CH-3012Berne, Switzerland. Tel: +41 31 6312384. Fax: +41 31 6312477. Email: [email protected]
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Summary

Among the cestodes, Echinococcus granulosus, Echinococcus multilocularis and Taenia solium represent the most dangerous parasites. Their larval stages cause the diseases cystic echinococcosis (CE), alveolar echincoccosis (AE) and cysticercosis, respectively, which exhibit considerable medical and veterinary health concerns with a profound economic impact. Others caused by other cestodes, such as species of the genera Mesocestoides and Hymenolepis, are relatively rare in humans. In this review, we will focus on E. granulosus and E. multilocularis metacestode laboratory models and will review the use of these models in the search for novel drugs that could be employed for chemotherapeutic treatment of echinococcosis. Clearly, improved therapeutic drugs are needed for the treatment of AE and CE, and this can only be achieved through the development of medium-to-high throughput screening approaches. The most recent achievements in the in vitro culture and genetic manipulation of E. multilocularis cells and metacestodes, and the accessability of the E. multilocularis genome and EST sequence information, have rendered the E. multilocularis model uniquely suited for studies on drug-efficacy and drug target identification. This could lead to the development of novel compounds for the use in chemotherapy against echinococcosis, and possibly against diseases caused by other cestodes, and potentially also trematodes.

Keywords

Cystic echinococcosis (CE)alveolar echinococcosis (AE)Echinoccoccus granulosusEchinoccoccus multilocularisin vitro culturechemotherapy
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 569 - 587
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Ali-Khan, Z., Siboo, R., Gomersall, M. and Faucher, M. (1983). Cystolytic events and the possible role of germinal cells in metastasis in chronic alveolar hydatidosis. Annals of Tropical Medicine and Parasitology 77, 497–512.CrossRefGoogle ScholarPubMed
Ammann, R. and Eckert, J. (1995). Clinical diagnosis and treatment of echinococcosis in humans. In Echinococcosis and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 411–430. CAB International, Wallmingford.Google Scholar
Angelucci, F., Basso, A., Bellelli, A., Brunori, M., Pica Maattoccia, L. and Valle, C. (2007). The anti-schistosomal drug praziquantel is an adenosine antagonist. Parasitology 134, 215–1221.CrossRefGoogle ScholarPubMed
Becker, B., Mehlhorn, H., Andrews, P. and Thomas, H. (1981). Ultrastructural investigations on the effect of praziquantel on the tegument of five species of cestodes. Zeitschrift für Parasitenkunde 64, 257–269.CrossRefGoogle ScholarPubMed
Blanton, R. E., Wachira, T. M., Zeyhle, E., Njoroge, E. M., Magambo, J. K. and Schantz, P. M. (1988). Oxfendazole treatment of cystic hydatid disease in naturally infected animals. Antimicrobial Agents and Chemotherapy 42, 601–605.CrossRefGoogle Scholar
Brehm, K. and Spiliotis, M. (2008 a). Recent advances in the in vitro cultivation and genetic manipulation of Echinococcus multilocularis metacestodes and germinal cells. Experimental Parasitology 119, 506–515.CrossRefGoogle ScholarPubMed
Brehm, K. and Spiliotis, M. (2008 b). The influence of host hormones and cytokines on Echinococcus multilocularis signalling and development. Parasite 15, 286–289.CrossRefGoogle ScholarPubMed
Brehm, K., Spiliotis, M., Zavala-Gongora, R., Konrad, C. and Frosch, M. (2006). The molecular mechanisms of larval cestode development: first steps into an unknown world. Parasitology International 55, S15–S21.CrossRefGoogle ScholarPubMed
Bresson-Hadni, S., Delabrousse, E., Blagosklonov, O., Bartholomot, B., Koch, S., Miguet, J. P., André Mantion, G. and Angèle Vuitton, D. (2006). Imaging aspects and non-surgical interventional treatment in human alveolar echinococcosis. Parasitology International 55 (Suppl.), S267–S272.CrossRefGoogle ScholarPubMed
Bresson-Hadni, S., Vuitton, D. A., Bartholomot, B., Heyd, B., Godart, D., Meyer, J. P., Hrusovsky, S., Becker, M. C., Mantion, G., Lenys, D. and Miguet, J. P. (2000). A twenty year history of alveolar echinococcosis: analysis of a series of 117 patients from eastern France. European Journal of Gasteroenterology and Hepatology 12, 327–336.CrossRefGoogle ScholarPubMed
Britos, L., Dominguez, L., Ehrlich, R. and Marin, M. (2000). Effect of praziquantel on the strobilar development of Mesocestoides corti in vitro. Journal of Helminthology 74, 295–299.CrossRefGoogle ScholarPubMed
Brunetti, E., Troia, G., Garlaschelli, A. L., Gulizia, R. and Filice, C. (2004). Twenty years of percutaneous treatments for cystic echinococcosis: a preliminary assessment of their use and safety. Parassitologia 46, 367–370.Google ScholarPubMed
Budke, C. M. (2006). Global socioeconomic impact of cystic echinococcosis. Emerging Infectious Diseases 12, 296–303.CrossRefGoogle ScholarPubMed
Chappell, L. H., Wastling, J. M. and Hurd, H. (1989). Action of cyclosporin A on the tapeworms Hymenolepis microstoma, H. diminuta and Mesocestoides corti in vivo. Parasitology 98, 291–299.CrossRefGoogle ScholarPubMed
Casado, N., Urrea-Paris, M. A., Moreno, M. J. and Rodriguez-Caabeiro, F. (2001). Combined praziquantel and albendazole chemoprophylaxis in experimental hydatidosis. Parasitology Research 87, 787–789.Google ScholarPubMed
Chai, J., Menghebat Wie, J., Deyu, S., Bin, L., Jincao, S., Chen, F., Xiong, L., Yiding, M., Xiuling, W., Dolikun, , Guliber, , Yanchun, W., Fanghua, G. and Shuhua, X. (2004). Observations on clinical efficacy of albendazole emulsion in 264 cases of hepatic cystic echinococcosis. Parasitology International 53, 3–10.CrossRefGoogle ScholarPubMed
Chinnery, J. B. and Morris, D. L. (1986). Effects of albendazole sulphoxide on viability of hydatid protoscoleces in vitro. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 815–817.CrossRefGoogle ScholarPubMed
Cobo, F., Yarnoz, C., Sesma, B., Fraile, P., Aizcorbe, M., Trujillo, R., Diaz-de-Liano, A. and Ciga, M. A. (1998). Albendazole plus praziquantel versus albendazole alone as preoperative treatment in intra-abdominal hydatidosis caused by Echinococcus granulosus. Tropical Medicine and International Health 3, 462–466.CrossRefGoogle ScholarPubMed
Colebrook, A. L., Jenkins, D. J., Jones, M. K., Tatarczuch, L. and Lightowlers, M. W. (2004). Effect of cyclosporin A on the survival and ultrastructure of Echinococcus granulosus protoscoleces in vitro. Parasitology 129, 497–504.CrossRefGoogle ScholarPubMed
Craig, P. S., McManus, D. P., Lightowlers, M. W., Chabalgoity, J. A., Garcia, H. H., Gavidia, C. M., Gilman, R. H., Gonzalez, A. E., Lorca, M., Naquira, C., Nieto, A. and Schantz, P. M. (2007). Prevention and control of cystic echinococcosis. Lancet Infectious Diseases 7, 385–394.CrossRefGoogle ScholarPubMed
Dubey, R., Abuzar, S., Sharma, S., Chatterjee, R. K. and Katiyar, J. C. (1985). Synthesis and anthelmintic activity of 5(6)-(benzimidazol-2-ylcarbamoyl) and (4-substituted piperazin-1-yl)benzimidazoles. Journal of Medical Chemistry 28, 1748–1750.CrossRefGoogle Scholar
Dueger, E. L., Moro, P. L. and Gilman, R. H. (1999). Oxfendazole treatment of sheep with naturally acquired hydatid disease. Antimicrobial Agents and Chemotherapy 43, 2263–2267.CrossRefGoogle ScholarPubMed
Eckert, J. and Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107–135.CrossRefGoogle ScholarPubMed
Eckert, J. and Pohlenz, J. (1976). On the effect of mebendazole on metacestodes of Mesocestoides corti and Echinococcus multilocularis. Tropenmedizin und Parasitologie 27, 247–262.Google ScholarPubMed
Eckert, J., Thompson, R. C. A. and Mehlhorn, H. (1983). Proliferation and metastases formation of larval Echinococcus multilocularis. I. Animal model, macroscopical and histological findings. Zeitschrift für Parasitenkunde 69, 737–748.CrossRefGoogle ScholarPubMed
Elissondo, M. C., Albani, C. M., Gende, L., Eguaras, M. and Denegri, G. (2008). Efficacy of thymol against Echinococcus granulosus protoscoleces. Parasitology International 57, 185–190.CrossRefGoogle ScholarPubMed
Elissondo, M. C., Ceballos, L., Alvarez, L., Sánchez Bruni, S., Lanusse, C. and Denegri, G. (2009). Flubendazole and ivermectin in vitro combination therapy produces a marked effect on Echinococcus granulosus protoscoleces and metacestodes. Parasitology Research. doi. 10.1007/s00436-009-1469-yCrossRefGoogle ScholarPubMed
Elissondo, M., Ceballos, L., Dopchiz, M., Andresiuk, V., Alvarez, L., Sanchez Bruni, S., Lanusse, C. and Denegri, G. (2007). In vitro and in vivo effects of flubendazole on Echinococcus granulosus metacestodes. Parasitology Research 100, 1003–1009.CrossRefGoogle ScholarPubMed
Elissondo, M. C., Dopchiz, M. C., Ceballos, L., Alvarez, L., Sanchez Bruni, S., Lanusse, C. and Denegri, G. (2006). In vitro effects of flubendazole on Echinococcus granulosus protoscoleces. Parasitology Research 98, 317–323.CrossRefGoogle ScholarPubMed
El-On, J. (2002). Benzimidazole treatment of cystic echinococcosis. Acta Tropica 85, 243–252.CrossRefGoogle Scholar
Emery, I., Bories, C., Liance, M., and Houin, R. (1995). In vitro quantitative assessment of Echinococcus multilocularis metacestode viability after in vivo and in vitro maintenance. International Journal for Parasitology 25, 275–278.CrossRefGoogle ScholarPubMed
Franchi, C., DiVico, B. and Teggi, A. (1999). Long term evaluation of patients with hydatidosis treated with benzimidazole carbamates. Clinical Infectious Diseases 29, 304–309.CrossRefGoogle ScholarPubMed
Frayha, G. J., Bikhazi, K. J. and Kachachi, T. A. (1981). Treatment of hydatid cysts (Echinococcus granulosus) by Cetrimide. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 447–450.CrossRefGoogle ScholarPubMed
Garcia, H. H., Gonzales, A. E., Evans, C. A. W. and Gilman, R. H. (2003). Taenia solium cysticercosis. The Lancet 361, 547–556.CrossRefGoogle Scholar
Garcia-Dominguez, C., Correa, D., Rabiela, M. T. and Flisser, A. (1991). Praziquantel treatment of muscle Taenia solium cysticercosis. 4. Reversible in vitro effect. Parasitology Research 77, 691–696.CrossRefGoogle ScholarPubMed
Garcia-Llamazares, J. L., Alvarez-de-Felipe, A. I., Redondo-Cardena, P., Voces-Alonso, J. A. and Prieto-Fernandez, J. G. (1997). In vivo inhibition of the regenerative capacity of hydatid material after treatment with netobimin. Parasitology Research 83, 105–108.CrossRefGoogle ScholarPubMed
Gavidia, C. M., Gonzalez, A. E., Lopera, L., Jayashi, C., Angelats, R., Barron, E. A., Ninaquispe, B., Villareal, L., Garcia, H. H., Verastegui, M. R. and Gilman, R. (2009). Evaluation of nitazoxanide and oxfendazole efficacy against cystic echinococcosis in naturally infected sheep. American Journal of Tropical Medicine and Hygiene 80, 367–372.CrossRefGoogle ScholarPubMed
Gelmedin, V., Caballero-Gamiz, R. and Brehm, K. (2008). Characterization and inhibition of a p38-like mitogen-activated protein kinase (MAPK) from Echinococcus multilocularis: Antiparasitic activities of a p38 MAPK inhibitors. Biochemical Pharmacology 76, 1068–1081.CrossRefGoogle ScholarPubMed
Gnanasekar, M., Salunkhe, A. M., Mallia, A. K., He, Y. X. and Kalyanasundaram, R. (2009). Prazquantel affects the regulatory myosin light chain of Schistosoma mansoni. Antimicrobial Agents and Chemotherapy 53, 1054–1060.CrossRefGoogle Scholar
Gottstein, B. and Hemphill, A. (1997). Immunopathology of echinococcosis. Chemical Immunology 66, 177–208.Google ScholarPubMed
Gupta, S., Katiyar, J. C. and Sen, A. B. (1981). Effect of mode of infection on the development and chemotherapeutic response of Hymenolepis nana in rats. Journal of Helminthology 55, 101–107.CrossRefGoogle ScholarPubMed
Heath, D. D., Christie, M. J. and Chevis, R. A. (1975). The lethal effect of mebendazole on secondary Echinococcus granulosus, cysticerci of Taenia pisiformis and tetrathyridia of Mesocestoides corti. Parasitology 70, 273–285.CrossRefGoogle ScholarPubMed
Hemphill, A. and Gottstein, B. (1995). Immunological and morphological studies on the proliferation of in vitro cultivated Echinococcus multilocularis metacestodes. Parasitology Research 81, 605–614.CrossRefGoogle Scholar
Hemphill, A. and Kern, P. (2008). Special issue: experimental studies in echinococcosis. Experimental Parasitology 119, 437–438.CrossRefGoogle ScholarPubMed
Hemphill, A. and Mueller, J. (2009). Alveolar and cystic echinococcosis: towards novel chemotherapeutical treatment options. Journal of Helminthology 83, 99–111.CrossRefGoogle ScholarPubMed
Hemphill, A., Mueller, J. and Esposito, M. (2006). Nitazoxanide, a broad-spectrum thiazolide anti-infective agent for the treatment of gastrointestinal infections. Expert Opinion in Pharmacotherapy 7, 953–964.CrossRefGoogle ScholarPubMed
Hemphill, A., Spicher, M., Stadelmann, B., Mueller, J., Naguleswaran, A., Gottstein, B. and Walker, M. (2007). Innovative chemotherapeutical treatment options for alveolar and cystic echinococcosis. Parasitology 134, 1657–1670.CrossRefGoogle ScholarPubMed
Hemphill, A., Stettler, M., Walker, M., Siles-Lucas, M., Fink, R. and Gottstein, B. (2002). Culture of Echinococcus multilocularis metacestodes; an alternative to animal use. Trends in Parasitology 18, 445–449.CrossRefGoogle ScholarPubMed
Holmes, E., Tsang, T. M., Huang, J. T., Leweke, F. M., Koethe, D., Gerth, C. W., Nolden, B. M., Gross, S., Schreiber, D., Nicholson, J. K. and Bahn, S. (2006). Metabolic profiling of CSF: evidence that early intervention may impact on disease progression and outcome in schizophrenia. PloS Medicine 3, e327. doi:10.1371/journal.pmed.0030327.CrossRefGoogle ScholarPubMed
Horton, R. J. (1997). Albendazole in the treatment of human cystic echinococcosis: 12 years of experience. Acta Tropica 64, 79–93.CrossRefGoogle ScholarPubMed
Hosch, W., Junghanss, T., Stojkovic, M., Brunetti, E., Heye, T., Kauffmann, G. W. and Hull, W. E. (2008). Metabolic viability assessment of cystic echinococcosis using high field 1H MRS of cyst contents. NMR in Biomedicine 21, 734–754.CrossRefGoogle ScholarPubMed
Hrckova, G. and Velebny, S. (1995). Effects of free and liposomized praziquantel on worm burden and antibody response in mice infected with Mesocestoides corti tetrathyridia. Journal of Helminthology 69, 213–221.CrossRefGoogle ScholarPubMed
Hrckova, G. and Velebny, S. (1997). Effect of praziquantel and liposome-incorporated praziquantel on peritoneal macrophage activation in mice infected with Mesocestoides corti tetrathyridia (Cestoda). Parasitology 114, 475–482.CrossRefGoogle ScholarPubMed
Hrckova, G., Velebny, S. and Corba, J. (1998). Effects of free and liposomized praziquantel on the surface morphology and motility of Mesocestoides vogae tetrathyridia (syn. M. corti; Cestoda: Cyclophyllidea) in vitro. Parasitology Research 84, 230–238.Google Scholar
Hurd, H., Mackenzie, K. S. and Chappell, L. H. (1993). Anthelmintic effects of cyclosporin A on protoscoleces and secondary hydatid cysts of Echinococcus granulosus in the mouse. International Journal for Parasitology 23, 315–320.CrossRefGoogle ScholarPubMed
Ingold, K., Bigler, P., Thormann, W., Cavaliero, T., Gottstein, B. and Hemphill, A. (1999). Efficacies of albendazole sulfoxide and albendazole sulfone against in vitro cultivated Echinococcus multilocularis metacestodes. Antimicrobial Agents and Chemotherapy 43, 1052–1061.CrossRefGoogle ScholarPubMed
Jain, M. K., Gupta, S., Katiyar, J. C., Maitra, S. C., Singh, J. and Bhakuni, D. S. (1989). Methyl 5(6)-(alpha-hydroxyphenyl methyl) benzimidazole-2-carbamate and cysticercosis: chemotherapeutic and electron microscopic studies. Indian Journal of Experimental Biology 27, 454–459.Google Scholar
Jeziorski, M. C. and Greenberg, R. M. (2006). Voltage-cated calcium channel subunits from platyhelminths: potential role in praziquantel action. International Journal for Parasitology 36, 625–632.CrossRefGoogle ScholarPubMed
Jura, H., Bader, A. and Frosch, M. (1998). In vitro activities of benzimidazoles against Echinococcus multilocularis metacestodes. Antimicrobial Agents and Chemotherapy 42, 1052–1056.CrossRefGoogle ScholarPubMed
Jura, H., Bader, A., Hartmann, M., Maschek, H. and Frosch, M. (1996). Hepatic tissue culture model for study of host-parasite interactions in alveolar echinococcosis. Infection and Immunity 64, 3484–3490.CrossRefGoogle ScholarPubMed
Kammerer, W. S. and Perez-Esandi, M. V. (1975). Chemotherapy of experimental Echinococcus granulosus infection. Trials in CF1 mice and jirds (Meriones unguiculatus). American Journal of Tropical Medicine and Hygiene 24, 90–95.CrossRefGoogle ScholarPubMed
Keiser, J., Chollet, J., Xiao, S. H., Mei, J. Y., Jiao, P. Y., Utzinger, J. and Tanner, M. (2009). Mefloquine – an aminoalcohol with promising antischistosomal properties in mice. PLOS Neglected Tropical Diseases 3, 1–10.CrossRefGoogle ScholarPubMed
Keiser, J. and Utzinger, J. (2007 a). Food-borne trematodiasis: current chemotherapy and advance with artemisinins and synthetic trioxolanes. Trends in Parasitology 23, 555–562.CrossRefGoogle ScholarPubMed
Keiser, J. and Utzinger, J. (2007 b). Artemisinins and synthetic trioxolanes in the treatment of helminthic infections. Current Opinions in Infectious Diseases 20, 605–612.CrossRefGoogle Scholar
Kern, P. (2003). Echinococcus granulosus infection: clinical presentation, medical treatment and outcome. Langenbecks Archives of Surgery 388, 413–420.CrossRefGoogle ScholarPubMed
Kern, P. (2006). Medical treatment of echinococcosis under the guidance of Good Clinical Practice (GCP/ICH). Parasitology International 55 (Suppl.), S273–S282.CrossRefGoogle ScholarPubMed
Kern, P., Abboud, P., Kern, W. V., Stich, A., Bresson-Hadni, S., Guerin, B., Buttenschoen, K., Gruener, B., Reuter, S. and Hemphill, A. (2008). Critical appraisal of nitazoxanide for the treatment of alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 79, 119.Google Scholar
King, C. H. (2007). Lifting the burden of schistosomiasis – defining elements of infection-associated disease and the benefits of anti-parasite treatment. Journal of Infectious Diseases 196, 653–655.CrossRefGoogle Scholar
Kohn, A. B., Roberts-Misterly, J. M., Anderson, P. A. V., Khan, N. and Greenberg, R. M. (2003). Specific sites in the beta interaction domain of schistosome Ca2+ channel -subunit are key to its role in sensitivity to the anti-schistosomal drug praziquantel. Parasitology 127, 349–356.CrossRefGoogle Scholar
Launchbury, A. P. and Habboubi, N. (1993). Epirubicin and doxorubicin: a comparison of their characteristics, therapeutic activity and toxicity. Cancer Treatment Reviews 19, 197–228.CrossRefGoogle ScholarPubMed
Lawton, P., Hemphill, A., Deplazes, P., Gottstein, B., and Sarciron, M. E. (1997). Echinococcus multilocularis metacestodes: immunological and immunocytochemical analysis of the relationships between alkaline phosphatase and the Em2 antigen. Experimental Parasitology 87, 142–149.CrossRefGoogle ScholarPubMed
Lawton, P., Walchshofer, N. and Sarciron, M. E. (2001). In vitro effects of isoprinosine and a dipeptide methyl ester on Echinococcus multilocularis protoscoleces. Journal of Helminthology 75, 251–257.Google Scholar
Li, J. V., Wang, Y. L., Saric, J., Nicholson, J. K., Dirnhofer, S., Singer, B. H., Tanner, M., Wittlin, S., Holmes, E. and Utzinger, J. (2008). Gobal metabolic responses of NMRI mice to an experimental Plasmodium berghei infection. Journal of Proteome Research 7, 3948–3956.CrossRefGoogle Scholar
Liance, M., Bresson-Hadni, S., Vuitton, D. A., Lenys, D., Carbillet, J. P. and Houin, R. (1992). Effects of cyclosporin A on the course of murine alveolar echinococcosis and on specific cellular and humoral immune responses against Echinococcus multilocularis. International Journal for Parasitology 22, 23–28.CrossRefGoogle ScholarPubMed
Liance, M., Nemati, F., Bories, C. and Couvreur, P. (1993). Experience with doxorubicin-bound polyisohexylcyanoacrylate nanoparticles on murine alveolar echinococcosis of the liver. International Journal for Parasitology 23, 427–429.CrossRefGoogle ScholarPubMed
Maki, J. and Yanagisawa, T. (1985). Anthelmintic effects of bithionol, paromomycin sulphate, flubendazole and mebendazole on mature and immature Hymenolepis nana in mice. Journal of Helminthology 59, 211–216.CrossRefGoogle ScholarPubMed
Martin, F. P. J., Verdu, E. F., Wang, Y. L., Dumas, M. E., Yap, I. K. S., Cloarec, O., Bergonzelli, G. E., Corthesy-Theulaz, I., Kochhar, S., Holmes, E., Lindon, J. C., Collins, S. M. and Nicholson, J. K. (2006). Transgenomic interactions in a mouse disease model: interaction of Trichinella spiralis infection with dietary Lactobacillus paracasei supplementation. Journal of Proteome Research 5, 2185–2193.CrossRefGoogle Scholar
Martinez, J., Perez-Serrano, J., Bernadina, W. E. and Rodriguez-Caabeiro, F. (1999). Echinococcus granulosus: in vivo effects of ivermectin and praziquantel on hsp60 and hsp70 levels. Experimental Parasitology 93, 171–180.CrossRefGoogle Scholar
Martinez Zedillo, G., Hoyo Badillo, C., Amezcua, J. and Gonzalez Barranco, D. (1992). Verapamil does not block the spastic response of praziquantel on the larvae of Taenia pisiformis. Archives of Medical Research 23, 73–77.Google Scholar
Marchiondo, A. A., Ming, R., Andersen, F. L., Slusser, J. H. and Conder, G. A. (1994). Enhanced larval cyst growth of Echinococcus multilocularis in praziquantel-treated jirds (Meriones unguiculatus). American Journal of Tropical Medicine and Hygiene 50, 120–127.CrossRefGoogle ScholarPubMed
Mathis, A., Wild, P., Boettger, E. C., Kapel, C. M. O. and Deplazes, P. (2005). Mitochondrial ribosome as the target for the macrolide antibiotic clarithromycin in the helminth Echinococus multilocularis. Antimicrobial Agents and Chemotherapy 49, 3251–3255.CrossRefGoogle Scholar
Matsumoto, J., Müller, N., Hemphill, A., Oku, Y., Kamiya, M. and Gottstein, B. (2006). 14-3-3- and II/3-10 gene expression as molecular markers to address viability and growth activity of Echinococcus multilocularis metacestodes. Parasitology 392, 98–105.Google Scholar
Matsumoto, J., Sakamoto, K., Shiniyo, N., Kido, Y., Yamamoto, N., Yagi, K., Miyoshi, H., Nonaka, N., Katakura, K., Kita, K. and Oku, Y. (2008). Anaerobic NADH-fumarate reductase system is predominant in the respiratory chain of Echinococcus multilocularis providing a novel target for the chemotherapy of alveolar echinococcosis. Antimicrobial Agents and Chemotherapy 52, 164–170.CrossRefGoogle ScholarPubMed
McManus, D. P., Wenbao, Z., Jun, L. and Bartley, P. B. (2003). Echinococcosis. The Lancet 362, 1295–1304.CrossRefGoogle ScholarPubMed
McTigue, M. A., Williams, D. R. and Tainer, J. A. (1995). Crystal structures of a schistosomal drug and vaccine target: glutathione S-transferase from Schistosoma japonica and its complex with the leading anti-schistosomal drug praziquantel. Journal of Molecular Biology 246, 21–27.CrossRefGoogle Scholar
Mehlhorn, H., Eckert, J. and Thompson, R. C. A. (1983). Proliferation and metastases formation of larval Echinococcus multilocularis II. Ultrastructural investigations. Zeitschrift für Parasitenkunde 69, 749–763.CrossRefGoogle ScholarPubMed
Miyaji, S., Katakura, K., Matsufuji, S., Murakami, Y., Hayashi, S., Oku, Y., Okamoto, M. and Kamiya, M. (1993). Failure of treatment with alpha-difluoromethylornithine against secondary multilocular echinococcosis in mice. Parasitology Research 79, 75–76.CrossRefGoogle ScholarPubMed
Moreno, M. J., Casado, N., Urrea-París, M. A. and Rodríguez-Caabeiro, F. (2002). Could ivermectin have a synergic effect with albendazole in hydatidosis therapy? Parasitology Research 88, 563–567.CrossRefGoogle ScholarPubMed
Morris, D. L., Chinnery, J. B. and Ubhi, C. (1987). A comparison of the effects of albendazole, its sulphone metabolite, and mebendazole on the viability of protoscoleces of Echinococcus granulosus in an in vitro culture system. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 804–806.CrossRefGoogle Scholar
Morris, D. L., Richards, K. S. and Chinnery, J. B. (1986). Protoscolicidal action of praziquantel – in vitro and electron microscopical studies on Echinococcus granulosus. Journal of Antimicrobial Chemotherapy 18, 687–691.CrossRefGoogle Scholar
Morseth, D. J. (1967). Fine structure of the hydatid cyst and protoscolex of Echinococcus granulosus. Journal of Parasitology 53, 312–325.CrossRefGoogle ScholarPubMed
Müller, J., Naguleswaran, A., Müller, N. and Hemphill, A. (2008 a). Neospora caninum: functional inhibition of protein disulfide isomerase by the broad-spectrum anti-parasitic drug nitazoxanide and other thiazolides. Experimental Parasitology 118, 80–88.CrossRefGoogle ScholarPubMed
Müller, J., Sidler, D., Nachbur, U., Wastling, J., Brunner, T. and Hemphill, A. (2008 b). Thiazolides inhibit growth and induce glutathione-S-transferase Pi (GSTP1)-dependent cell death in human colon cancer cells. International Journal of Cancer 123, 1797–1806.CrossRefGoogle ScholarPubMed
Naguleswaran, A., Spicher, M., Vonlaufen, N., Ortega-Mora, L. M., Torgerson, P., Gottstein, B. and Hemphill, A. (2006). In vitro metacestodicidal activities of genistein and other isoflavones against Echinococcus multilocularis and Echinococcus granulosus. Antimicrobial Agents and Chemotherapy 50, 3770–3778.CrossRefGoogle ScholarPubMed
Nakao, M., McManus, D. P., Schantz, P. M., Craig, P. S. and Ito, A. (2007) A molecular phylogeny of the genus Echinococcus inferred from complete mitochondrial genomes. Parasitology 134, 713–722.CrossRefGoogle ScholarPubMed
Nessim, N. G., Hassan, S. I., William, S. and El-Baz, H. (2000). Efffect of the broad spectrum antheminthic drug flubenadazole upon Schistosoma mansoni experimentally infected mice. Arztneimittelforschung 50, 1129–1133.Google Scholar
Nogi, T., Zhang, D., Chan, J. D., and Marchant, J. S. (2009). A novel bological activity of praziqunatel requiring voltage-operated Ca2+ channel beta subunits: subversion of flatworm regenerative polarity. PloS Neglected Tropical Diseases 3, e464.CrossRefGoogle Scholar
Novak, M. and Blackburn, B. J. (1985). Comparison of the effects of imidazo[1,2-a]pyridine-2-carbamates and benzimidazole-2-carbamates on the development of Hymenolepis nana in Tribolium confusum. Experientia 41, 687–689.CrossRefGoogle ScholarPubMed
Ochieng'-Mitula, P. J. and Burt, M. D. (1996). The effects of ivermectin on the hydatid cyst of Echinococcus granulosus after direct injection at laparotomy. Journal of Parasitology 82, 155–157.CrossRefGoogle ScholarPubMed
Ordovas, J. M. and Mooser, V. (2006). Metagenomics: the role of the microbiome in cardivascular diseases. Current Opinion in Lipidology 17, 157–161.CrossRefGoogle Scholar
Palomares-Alonso, F., Piliado, J. C., Palencia, G., Ortiz-Plata, A. and Jung-Cook, H. (2007). Efficacy of nitazoxanide, tizoxanide, and tizoxanide/albendazole sulphoxide combination against Taenia crassiceps cysts. Journal of Antimicrobial Chemotherapy 59, 212–218.CrossRefGoogle ScholarPubMed
Perez Serrano, J., Casado, N., Guillermo, , Denegri, , Rodriguez-Caabeiro, F. (1994). The effects of albendazole and albendazole sulphoxide combination-therapy on Echinococcus granulosus in vitro. International Journal for Parasitology 24, 219–224.CrossRefGoogle ScholarPubMed
Rausch, R. L. (1995). Life cycle patterns and geographic distribution of Echinococcus species. In Echinococcosis and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.), pp. 89–99. Wallmingford: CAB International.Google Scholar
Reuter, S., Buck, A., Grebe, O., Nüssle-Kügele, K., Kern, P. and Manfras, B. (2003 b). Salvage treatment with amphotericin B in progressive human alveolar echinococcosis. Antimicrobial Agents and Chemotherapy 47, 3586–3591.CrossRefGoogle ScholarPubMed
Reuter, S., Buck, A., Manfras, B., Kratzer, W., Seitz, H. M., Darge, K., Reske, S. N. and Kern, P. (2004). Structured treatment interuption in patients with alveolar echinococcosis. Hepatology 39, 509–517.CrossRefGoogle Scholar
Reuter, S., Jensen, B., Buttenschoen, K., Kratzer, W. and Kern, P. (2000). Benzimidazoles in the treatment of alveolar echinococcosis. Journal of Antimicrobial Chemotherapy 46, 451–460.CrossRefGoogle ScholarPubMed
Reuter, S., Manfras, B., Merkle, M., Harter, G. and Kern, P. (2006). In vitro activities of itraconazole, methiazole, and nitazoxanide versus Echinococcus multilocularis larvae. Antimicrobial Agents and Chemotherapy 50, 2966–2970.CrossRefGoogle ScholarPubMed
Reuter, S., Merkle, M., Brehm, K., Kern, P. and Manfras, B. (2003 a). Effect of amphotericin B on larval growth of Echinococcus multilocularis. Antimicrobial Agents and Chemotherapy 47, 620–625.CrossRefGoogle ScholarPubMed
Robinson, M. W., Hoev, E. M., Fairweather, I., Dalton, J. P., McGonigle, S. and Trudgett, A. (2001). Characterization of a beta tubulin gene from the liver fluke Fasciola hepatica. International Journal for Parasitology 31, 1264–1268.CrossRefGoogle ScholarPubMed
Rodriguez-Caabeiro, F., Casado, N. and Juarez-Pelaez, E. (1989). Efecto in vitro de praziquantel, mebendazole y oxfendazole sobre protoscolex de Echinococcus granulosus. Revista Iberica Parasitologica 49, 77–83.Google Scholar
Rogan, M. T. and Richards, K. S. (1986). Echinococcus granulosus: in vivo effect of monensin on the tegument of the protoscolex. Parasitology 93, 347–355.CrossRefGoogle ScholarPubMed
Saldana, J., Marin, M., Fernandez, C. and Dominguez, L. (2001). In vitro taurocholate-induced segmentation and clustering of Mesocestoides vogae (syn. corti) tetrathyridia (Cestoda) – inhibition by cestocidal drugs. Parasitology Research 87, 281–286.CrossRefGoogle ScholarPubMed
Sarciron, E. M., Bresson-Hadni, S., Mercier, M., Lawton, P., Duranton, C., Lenys, D., Petavy, A. F. and Vuitton, D. A. (1997). Antibodies against Echinococcus multi locularis phosphatase as markers for the specific diagnosis and the serological monitoring of alveolar echinococcosis. Parasite Immunology 19, 61–68.CrossRefGoogle Scholar
Sarciron, M. E., Hamoud, W., Azzar, G., and Petavy, A. F. (1991). Alkaline phosphatase from Echinococcus multilocularis: purification and characterization. Compendium of Biochemistry and Physiology 100, 253–258.Google ScholarPubMed
Saric, J., Li, J. V., Wang, Y., Keiser, J., Bundy, J. G., Holmes, E. and Utzinger, J. (2008). Metabolic profiling of an Echinostoma caproni infection in the mouse for biomarker discovery. PloS Neglected Tropcial Diseases 2, e254. doi: 10.1371/journal.pntd.0000254CrossRefGoogle ScholarPubMed
Schantz, P. M., Chai, J., Craig, P. S., Eckert, J., Jenkins, D. J., Macpherson, C. N. L. and Thakur, A. (1995). Epidemiology and control of hydatid disease. In Echinococcosis and Hydatid Disease (ed. Thompson, R. C. A. and Lymbery, A. J.),pp. 233–245. Wallmingford: CAB International.Google Scholar
Schipper, H. G., Koopmans, R. P., Nagy, J., Butter, J. J., Kaeger, P. A. and Van Boxtel, C. J. (2000). Effect of dose increase or cimetidine co-administration on albendazole bioavailability. American Journal of Trpocial Medicine and Hygiene 63, 270–273.CrossRefGoogle ScholarPubMed
Schmidt, J. (1998). Effects of benzimidazole antheminthics as microtubule-active drugs on the synthesis of surface glycoconjugates in Echinostoma caproni, Hymenolepis microstoma and Schistosoma mansoni. Parasitology Research 84, 362–368.CrossRefGoogle Scholar
Schumacher, G. and Neuhaus, P. (2001). The physiological estrogen metabolite 2-methoxyestradiol reduces tunor growth and induces apoptosis in human solid tunors. Journal of Cancer Research and Clinical Oncology 127, 405–410.CrossRefGoogle Scholar
Shandera, W. X. and Kass, J. S. (2006). Neurocysticercosis: current knowledge and advances. Current Neurology and Neuroscience Reports 6, 453–459.CrossRefGoogle ScholarPubMed
Siles-Lucas, M. and Hemphill, A. (2002). Cestode parasites: Application of in vivo and in vivo models for studies on the host-parasite relationship. Advances in Parasitology 51, 133–230.CrossRefGoogle ScholarPubMed
Spicher, M., Naguleswaran, A., Ortega-Mora, L. M., Mueller, J., Gottstein, B. and Hemphill, A. (2008 a). In vitro and in vivo effects of 2-methoxyestradiol, either alone, or combined with albendazole, against Echinococcus metacestodes. Experimental Parasitology 119, 475–482.CrossRefGoogle ScholarPubMed
Spicher, M., Roethlisberger, C., Lany, C., Stadelmann, B., Keiser, J., Ortega-Mora, L. M., Gottstein, B. and Hemphill, A. (2008 b). In vitro and in vivo treatments of Echinococcus protoscoleces and metacestodes with artemisinin derivatives. Antimicrobial Agents and Chemotherapy 52, 3447–3450.CrossRefGoogle ScholarPubMed
Spiliotis, M. and Brehm, K. (2008). Axenic in vitro cultivation of Echinococcus multilocularis metacestode vesicles and the generation of primary cell cultures. In Host Pathogen Interactions (ed. Rupp, S. and Sohn, K.),pp. 245–262. Humana Press.Google Scholar
Spiliotis, M., Lechner, S., Tappe, D., Scheller, D., Krohne, G. and Brehm, K. (2008). Transient tranfection of Echinococcus multilocularis primary cells and complete in vitro regeneration of metacestode vesicles. International Journal for Parasitology 38, 1025–1039.CrossRefGoogle Scholar
Spiliotis, M., Tappe, D., Sesterhenn, L. and Brehm, K. (2004). Long-term in vitro cultivation of Echinococcus multilocularis metacestodes under axenic conditions. Parasitology Research 92, 430–432.CrossRefGoogle ScholarPubMed
Stettler, M., Fink, R., Walker, M., Gottstein, B., Geary, T. G., Rossignol, J. F. and Hemphill, A. (2003). In vivo parasiticidal effect of nitazoxanide against Echinococcus multilocularis metacestodes. Antimicrobial Agents and Chemotherapy 47, 467–474.CrossRefGoogle Scholar
Stettler, M., Rossignol, J. F., Fink, R., Walker, M., Gottstein, B., Merli, M., Theurillat, R., Thormann, W., Dricot, E., Segers, R. and Hemphill, A. (2004). Secondary and primary murine alveolar echinococcosis: combined albendazole/nitazoxanide chemotherapy exhibits profound anti-parasitic activity. International Journal for Parasitology 34, 615–624.CrossRefGoogle ScholarPubMed
Stettler, M., Siles-Lucas, M., Sarciron, E., Lawton, P., Gottstein, B. and Hemphill, A. (2001). Echinococcus multilocularis alkaline phosphatase as a marker for metacestode damage induced by in vitro drug treatment with albendazole sulphoxide and albendazole sulfone. Antimicrobial Agents and Chemotherapy 45, 2256–2262.CrossRefGoogle ScholarPubMed
Stey, C. and Jost, R. (1993). Rezidivierende, lebensbedroliche Anaphylaxie als Erstmanifestation eines Echinococcus cysticus (granulosus) der Leber. Schweizerische Medizinische Wochenzeitschrift 123, 1445–1450.Google Scholar
Tallima, H. and El Ridi, R. (2007). Praziquantel binds Schistosoma mansoni adult worm actin. International Journal of Antimicrobial Agents 29, 570–575.CrossRefGoogle ScholarPubMed
Taylor, D. H. and Morris, D. L. (1988). In vitro culture of Echinococcus multilocularis: protoscolicidal action of praziquantel and albendazole sulphoxide. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 265–267.CrossRefGoogle ScholarPubMed
Taylor, D. H., Richards, K. S. and Morris, D. L. (1989). Rapid recovery of Echinococcus granulosus following ‘successful’ albendazole therapy in a gerbil model. Journal of Helminthology 63, 349–352.CrossRefGoogle Scholar
Tellez-Giron, E., Ramos, M. C. and Montante, M. (1981). Effect of flubendazole on Cysticercus cellulosae in pigs. American Journal of Tropical Medicine and Hygiene 30, 135–138.CrossRefGoogle ScholarPubMed
Tellez-Giron, E., Ramos, M. C., Dufour, L., Montante, M., Tellez, E. Jr.Rodriguez, J., Gomez-Mendez, F. and Mireles, E. (1984). Treatment of neurocysticercosis with flubendazole. American Journal of Tropical Medicine and Hygiene 33, 627–631.CrossRefGoogle ScholarPubMed
Terenina, N. V., Kosovatova, L. A., Gerasimova, E. I. and Shalaeva, N. M. (1998). The effect of anthelmintics on the serotonin content of cestodes. Meditsinskaia parazitologiia i parazitarnye bolezni 1, 10–15.Google Scholar
Thompson, R. C. A. (1986). Biology and systematics of Echinococcus. In The Biology of Echinococcus and Hydatid Disease (ed. Thompson, R. C. A.), pp. 5–17. Allen & Unwin, London.Google Scholar
Urrea-Paris, M. A., Casado, N., Moreno, M. J. and Rodriguez-Caabeiro, F. (2001). Chemoprophylactic praziquantel treatment in experimental hydatidosis. Parasitology Research 87, 510–512.Google ScholarPubMed
Urrea-Paris, M. A., Moreno, M. J., Casado, N. and Rodriguez-Caabeiro, F. (1999). Echinococcus granulosus: praziquantel treatment against the metacestode stage. Parasitology Research 85, 999–1006.CrossRefGoogle ScholarPubMed
Utzinger, J., Chollet, J., Tu, Z., Xiao, S. and Tanner, M. (2002). Comparative study of the effects of artemether and artesunate on juvenile and adult Schistosoma mansoni in experimentally infected mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 318–323.CrossRefGoogle ScholarPubMed
Varcasia, A., Garippa, G., Pipia, A. P., Scala, A., Brianti, E., Giannetto, S., Battelli, G., Poglayen, G. and Micagni, G. (2008) Cystic echinococcosis in equids in Italy. Parasitology Research 102, 815–818.CrossRefGoogle ScholarPubMed
Verheyen, A., Vanparijs, O., Borgers, M. and Thienpont, D. (1978). Scanning electron microscopic observations of Cysticercus fasciolaris (=Taenia taeniaeformis) after treatment of mice with mebendazole. Journal of Parasitology 64, 411–425.CrossRefGoogle ScholarPubMed
Voelker, R. (2009). Attention sought for negelected diseases. Journal of the American Medical Association 301, 1755–1756.CrossRefGoogle Scholar
Vuitton, D. (2009). Benzimidazoles for the treatment of cystic and alveolar echinococcosis: what is the consensus? Expert Review in Anti-Infective Therapy 7, 145–149.CrossRefGoogle ScholarPubMed
Vutova, K., Mechkov, G., Vachkov, P., Petkov, R., Georgiev, P., Handjiev, S., Ivanov, A. and Todorov, T. (1999). Effect of mebendazole on human cystic echinococcosis: the role of dosage and treatment duration. Annals of Tropical Medicine and Parasitology 93, 357–365.CrossRefGoogle ScholarPubMed
Walker, M., Rossignol, J. F., Torgerson, P. and Hemphill, A. (2004). In vivo effects of nitazoxanide on Echinococcus granulosus protoscoleces and metacestodes. Journal of Antimicrobial Chemotherapy 54, 609–616.CrossRefGoogle Scholar
Wang, Y. L., Holmes, E., Nicholson, J. K., Cloarec, O., Chollet, J., Tanner, M., Singer, B. H. and Utzinger, J. (2004). Metabolomic investigations in mice infected with Schistosoma mansoni: an approach for biomarker identification. Proceedings of the National Academy of Sciences, USA 101, 12676–12681.CrossRefGoogle Scholar
Wang, Y. L., Utzinger, J., Saric, J., Li, J. V., Burckhardt, J., Dirnhofer, S., Nicholson, J. K., Singer, B. H., Brun, R. and Holmes, E. (2008). Global metabolic responses of mice to Trypanosoma brucei brucei infection. Proceedings of the National Academy of Sciences, USA 105, 6127–6132.CrossRefGoogle ScholarPubMed
Wang, Y. L., Utzinger, J., Xiao, S. H., Xue, J., Nicholson, J. K., Tanner, M., Singer, B. H. and Holmes, E. (2006). System level metabolic effects of a Schistosoma japonicum infection in the Syrian hamster. Molecular and Biochemical Parasitology 146, 1–9.CrossRefGoogle ScholarPubMed
Wen, H., New, R. R., Muhmut, M., Wang, J. H., Wang, Y. H., Zhang, J. H., Shao, Y. M. and Craig, P. S. (1996). Pharmacology and efficacy of liposome-entrapped albendazole in experimental secondary alveolar echinococcosis and effect of co-administration with cimetidine. Parasitology 113, 111–121.CrossRefGoogle ScholarPubMed
Wiest, P. M., Li, Y., Olds, R. and Bowen, W. D. (1992). Inhibition of phosphoinositide turnover by praziquantel in Schistosoma mansoni. Journal of Parasitology 78, 753–755.CrossRefGoogle ScholarPubMed
Williams, S., Guirgus, F. and Nessim, N. G. (2003). Effect of simultaneous and/or consective administration of the broad spectrum anthelminthic flubendazole together with praziquantel in experimental Schistosoma mansoni infection. Arztneimittelforschung 53, 532–537.Google Scholar
Winning, A., Braslins, P. and McCarthy, J. S. (2009). Case report: nitazoxanide for the treatment of refractory bony hydatid disease. American Journal of Tropical Medicne and Hygiene 80, 176–178.CrossRefGoogle ScholarPubMed