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Successful intestinal Echinococcus multilocularis oncosphere invasion and subsequent hepatic metacestode establishment in resistant RccHan™:WIST rats after pharmacological immunosuppression

Published online by Cambridge University Press:  18 May 2016

MARIA TERESA ARMUA-FERNANDEZ ,
DEBORAH JOEKEL ,
ALEXANDER SCHWEIGER ,
RAMON MARC EICHENBERGER ,
JUN MATSUMOTO  and
PETER DEPLAZES
MARIA TERESA ARMUA-FERNANDEZ
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
DEBORAH JOEKEL
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
ALEXANDER SCHWEIGER
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
RAMON MARC EICHENBERGER
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
JUN MATSUMOTO
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zurich, Switzerland Laboratory of Medical Zoology, Department of Veterinary Medicine, Faculty of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252-0880, Japan
PETER DEPLAZES*
Affiliation:
Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zurich, Switzerland
*
*Corresponding author: Institute of Parasitology, University of Zurich, Winterthurerstrasse 266a, 8057 Zurich, Switzerland. Phone: +41 (0) 44 635 85 02. Fax: +41 (0) 44 635 89 07. E-mail: deplazesp@access.uzh.ch
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Summary

Susceptibility/resistance to larval Echinococcus multilocularis infection varies greatly depending on host species and strains. Whereas several mice strains and non-human primates are highly susceptible to alveolar echinococcosis, rats and most of humans are considered as more resistant. In this study, we aimed to elucidate factors responsible for host resistance in rats (Experiments A–D). (A) The parasite establishment was not observed in immunocompetent Wistar rats orally inoculated with sodium hypochlorite resistant eggs with/without pig bile, or activated/non-activated oncospheres (NAO). Peritoneal inoculation with NAO or metacestode tissue allowed the parasite establishment in rats. (B) T-cell-deficient athymic nude rats showed complete resistance against the metacestode establishment after oral inoculation with parasite eggs. This finding suggests that T-cell-independent parasite clearance occurred in the animals during early phase of the parasite invasion. Finally, Wistar rats that received pharmacological immunosuppression using either dexamethasone (DMS) alone or methotrexate (MTX) i.p. alone or a combination of these compounds were orally inoculated with the parasite's eggs. As a result (D), successful establishment of metacestode with protoscoleces was observed in all 3 rats treated with DMS (s.c.) alone or in all 6 rats treated with DMS (s.c.) plus MTX but not in 8 rats with MTX alone, suggesting that factors affected by DMS treatment are responsible to regulate the parasite invasion and establishment.

Keywords

alveolar echinococcosisEchinococcus multilocularisimmunosuppressionmetacestoderatresistance
Type
Research Article
Information
Parasitology , Volume 143 , Issue 10 , September 2016 , pp. 1252 - 1260
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Baron, R. W. and Tanner, C. E. (1976). The effect of immunosuppression on secondary Echinococcus multilocularis infections in mice. International Journal for Parasitology 6, 37–42.CrossRefGoogle ScholarPubMed
Bresson-Hadni, S., Laplante, J. J., Lenys, D., Rohmer, P., Gottstein, B., Jacquier, P., Mercet, P., Meyer, J. P., Miguet, J. P. and Vuitton, D. A. (1994). Seroepidemiologic screening of Echinococcus multilocularis infection in a European area endemic for alveolar echinococcosis. The American Journal of Tropical Medicine and Hygiene 51, 837–846.CrossRefGoogle Scholar
Ciesielski, C. J., Mei, J. and Piccinini, L. A. (1998). Effects of cyclosporine A and methotrexate on CD18 expression in recipients of rat cardiac allografts. Transplant Immunology 6, 122–133.Google Scholar
Dentan, C., Mazet, R., Gilson, M., Marchou-Lopez, S. and Gaudin, P. (2012). Rheumatoid arthritis, alveolar echinococcosis, and rituximab: a case report. Joint, Bone, Spine 79, 325–327.Google Scholar
Deplazes, P. and Eckert, J. (2001). Veterinary aspects of alveolar echinococcosis – a zoonosis of public health significance. Veterinary Parasitology 98, 65–87.CrossRefGoogle ScholarPubMed
Deplazes, P. and Gottstein, B. (1991). A monoclonal antibody against Echinococcus multilocularis Em2-antigen. Parasitology 103, 41–49.CrossRefGoogle ScholarPubMed
Deplazes, P., Grimm, F., Sydler, T., Tanner, I. and Kapel, C. M. (2005). Experimental alveolar echinococcosis in pigs, lesion development and serological follow up. Veterinary Parasitology 130, 213–222.CrossRefGoogle ScholarPubMed
Eckert, J., Deplazes, P. and Kern, P. (2011). Alveolar echinococcosis (Echinococcus multilocularis) and neotropical forms of echinococcosis (Echinococcus vogeli and Echinococcus oligarthrus). In Oxford Textbook of Zoonoses Biology, Clinical Practice, and Public Health Control, 2nd Edn. (Palmer, S., Soulsby, L., Torgerson, P. R. and Brown, D. W. G.), pp. 669–699. Oxford University Press, UK.Google Scholar
Federer, K., Armua-Fernandez, M. T., Hoby, S., Wenker, C., Deplazes, P. (2015). In vivo viability of Echinococcus multilocularis eggs in a rodent model after different thermo-treatments. Experimental Parasitology 154, 14–19. Epub 2015 Mar 25.CrossRefGoogle Scholar
Gaultier, J. B., Hot, A., Mauservey, C., Dumortier, J., Coppere, B. and Ninet, J. (2009). Granulomatous liver disease as the presenting feature of alveolar echinococcosis in an hepatitis C infected cardiac transplant patient. La Revue de Médecine Interne 30, 812–815. (Article in French).Google Scholar
Geyer, M., Wilpert, J., Wiech, T., Theilacker, C., Stubanus, M., Kramer-Zucker, A., Fischer, K. G., Drognitz, O., Frydrychowicz, A., Kern, W., Walz, G. and Pisarski, P. (2011). Rapidly progressive hepatic alveolar echinococcosis in an ABO-incompatible renal transplant recipient. Transplant Infectious Disease 13, 278–284.CrossRefGoogle Scholar
Gottstein, B. and Hemphill, A. (2008). Echinococcus multilocularis: the parasite-host interplay. Experimental Parasitology 119, 447–452.Google Scholar
Gottstein, B., Deplazes, P. and Aubert, M. (1992). Echinococcus multilocularis: immunological study on the “Em2-positive” laminated layer during in vitro and in vivo post-oncospheral and larval development. Parasitology Research 78, 291–297.CrossRefGoogle Scholar
Gottstein, B., Saucy, F., Deplazes, P., Reichen, J., Demierre, G., Busato, A., Zuercher, C. and Pugin, P. (2001). Is high prevalence of Echinococcus multilocularis in wild and domestic animals associated with disease incidence in humans? Emerging Infectious Diseases 7, 408–412.Google Scholar
Gottstein, B., Wang, J., Boubaker, G., Marinova, I., Spiliotis, M., Müller, N. and Hemphill, A. (2015). Susceptibility versus resistance in alveolar echinococcosis (larval infection with Echinococcus multilocularis). Veterinary Parasitology 213, 103–109.Google Scholar
Gruener, B. C. C., Brunetti, E., Menezes, C. N., Haerter, G., Grobusch, M. P. and Kern, P. (2008). Accelerated larval growth of Echinococcus spp. in the immunodeficient host? (Abstract). The American Journal of Tropical Medicine and Hygiene 6, 118.Google Scholar
Habib, K. S. and El Garhy, M. F. (2002). The pattern of cryptosporidiosis in experimentally immune deficient albino rats. Journal of the Egyptian Society of Parasitology 32, 953–958.Google Scholar
Hofer, S., Gloor, S., Muller, U., Mathis, A., Hegglin, D. and Deplazes, P. (2000). High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology 120, 135–142.Google Scholar
Inceboz, T., Korkmaz, M., Fehmi, Ç. and Üner, A. (2007). The first report in turkey of in vivo cultivation in Rattus norvegicus of Echinococcus multilocularis Human Strain. Türkiye Parazitolojii dergisi 31, 194–196.Google ScholarPubMed
Kamiya, H. (1972). Studies on echinococcosis XXIV: age difference in resistance to infection with Echinococcus multilocularis in AKR strain of mouse. The Japanese Journal of Veterinary Research 20, 69–76.Google Scholar
Kamiya, M., Ooi, H. K., Oku, Y., Okamoto, M., Ohbayashi, M. and Seki, N. (1987). Isolation of Echinococcus multilocularis from the liver of swine in Hokkaido, Japan. The Japanese Journal of Veterinary Research 35, 99–107.Google ScholarPubMed
Kayacan, S. M., Vatansever, S., Temiz, S., Uslu, B., Kayacan, D., Akkaya, V., Erk, O., Saka, B., Karadag, A., Turkmen, K., Yakar, F. and Guler, K. (2008). Alveolar echinococcosis localized in the liver, lung and brain. Chinese Medical Journal 121, 90–92.Google Scholar
Kern, P., Gruener, B. and Wahlers, K. (2011). Diagnosis and course of echinococcocal diseases in the transplant setting. Transplant Infectious Disease 13, 217–221.Google Scholar
Li, T., Zhao, J., Zhang, Y., Pai, Z., Zhang, W., Tuxun, T., Bai, L., Wu, J. and Wen, H. (2011). Suppression of acute rejective response following orthotopic liver transplantation in experimental rats infected with Echinococcus multilocularis . Chinese Medical Journal 124, 2818–2823.Google Scholar
Matsumoto, J., Kouguchi, H., Oku, Y. and Yagi, K. (2010). Primary alveolar echinococcosis: course of larval development and antibody responses in intermediate host rodents with different genetic backgrounds after oral infection with eggs of Echinococcus multilocularis . Parasitology International 53, 435–444.CrossRefGoogle Scholar
Nono, J. K., Lutz, M. B. and Brehm, K. (2014). EmTIP, a T-cell immunomodulatory protein secreted by the tapeworm Echinococcus multilocularis is important for early metacestode development. PLoS Neglected Tropical Diseases 8, e2632.Google Scholar
Obayashi, M., Rausch, R. L. and Fay, F. H. (1971). On the ecology and distribution of Echinococcus spp. (Cestoda: Taeniidae), and characteristics of their development in the intermediate host. II. Comparative studies on the development of larval E. multilocularis Leuckart, 1863, in the intermediate host. Japanese Journal of Veterinary Research 19, 1–53.Google Scholar
Okamoto, M., Fujita, O., Arikawa, J., Kurosawa, T., Oku, Y. and Kamiya, M. (1992). Natural Echinococcus multilocularis Infection in a Norway Rat, Rattus norvegicus, in Southern Hokkaido, Japan. International Journal for Parasitology 22, 681–684.Google Scholar
Playford, M. C., Ooi, H. K., Ito, M., Kamiya, M. (1993). Lymphocyte engraftment conveys immunity and alters parasite development in scid mice infected with Echinococcus multilocularis . Parasitology Research 79, 261–268.Google Scholar
Rausch, R. L. (1995). Life cycle patterns and geographic distribution of Echinococcus species. In Echinococcus and Hydatid Disease (Thompson, R. C. A., Lymbery, A. J.), CAB International, Wallingford, UK.Google Scholar
Rehmann, P., Grone, A., Lawrenz, A., Pagan, O., Gottstein, B. and Bacciarini, L. N. (2003). Echinococcus multilocularis in two lowland gorillas (Gorilla g. gorilla). Journal of Comparative Pathology 129, 85–88.Google Scholar
Reynolds, C. W., Timonen, T. T., Holden, H. T., Hansen, C. T. and Herberman, R. B. (1982). Natural killer cell activity in the rat. Analysis of effector cell morphology and effects of interferon on natural killer cell function in the athymic (nude) rat. European Journal of Immunology 12, 577–582.Google Scholar
Romig, T., Kratzer, W., Kimmig, P., Frosch, M., Gaus, W., Flegel, W. A., Gottstein, B., Lucius, R., Beckh, K. and Kern, P. (1999). An epidemiologic survey of human alveolar echinococcosis in southwestern Germany. Römerstein Study Group. The American Journal of Tropical Medicine and Hygiene 61, 566–573.Google Scholar
Stieger, C., Hegglin, D., Schwarzenbach, G., Mathis, A. and Deplazes, P. (2002). Spatial and temporal aspects of urban transmission of Echinococcus multilocularis . Parasitology 124, 631–640.Google Scholar
Thompson, R. C. A. (1995): Biology and systematics of Echinococcus multilocularis . In Echinococcus and Hydatid Disease (Thompson, R. C. A., Lymbery, A. J.), CAB International, Wallingford, UK.Google Scholar
Umhang, G., Lahoreau, J., Nicolier, A. and Boué, F. (2013). Echinococcus multilocularis infection of a ring-tailed lemur (Lemur catta) and a nutria (Myocastor coypus) in a French zoo. Parasitology International 62, 561–563.Google Scholar
Vuitton, D. A. (2003). The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Tropica 85, 119–132.Google Scholar
Vuitton, D. A., Demonmerot, F., Knapp, J., Richou, C., Grenouillet, F., Chauchet, A., Vuitton, L., Bresson-Hadni, S. and Millon, L. (2015). Clinical epidemiology of human AE in Europe. Veterinary Parasitology 213, 110–120.Google Scholar
Webster, G. A. and Cameron, T. W. M. (1961). Observation on experimental infections with Echinococcus in rodents. Canadian Journal of Zoology 39, 877–891.Google Scholar
Weiner, S. M., Krenn, V., Koelbel, C., Hoffmann, H. G., Hinkeldey, K. and Ockert, D. (2011). Echinococcus multilocularis infection and TNF inhibitor treatment in a patient with rheumatoid arthritis. Rheumatology International 31, 1399–1400.Google Scholar
Wessels, J. A. M., Huizinga, T. W. J. and Guchelaar, H. J. (2008). Recent insights in the pharmacological actions of methotrexate in the treatment of rheumatoid arthritis. Rheumatology (Oxford) 47, 249–255.Google Scholar
Woolsey, I. D., Bune, N. E., Jensen, P. M., Deplazes, P. and Kapel, C. M. (2015 a). Echinococcus multilocularis infection in the field vole (Microtus agrestis): an ecological model for studies on transmission dynamics. Parasitology Research 114, 1703–1709.Google Scholar
Woolsey, I. D., Jensen, P. M., Deplazes, P. and Kapel, C. M. (2015 b). Establishment and development of Echinococcus multilocularis metacestodes in the common vole (Microtus arvalis) after oral inoculation with parasite eggs. Parasitology International 64, 571–575.Google Scholar
Yamashita, M., Imagawa, T., Nakaya, K., Sako, Y., Okamoto, Y., Tsuka, T., Osaki, T., Okamoto, M. and Ito, A. (2013). Echinococcus multilocularis: single hepatic lesion experimentally established without metastasis in rats. Experimental Parasitology 135, 320–324.Google Scholar
Zen, M., Canova, M., Campana, C., Bettio, S., Nalotto, L., Rampudda, M., Ramonda, R., Iaccarino, L. and Doria, A. (2011). The kaleidoscope of glucorticoid effects on immune system. Autoimmunity Reviews 10, 305–310.CrossRefGoogle ScholarPubMed