Echinococcus multilocularis infection in the field vole (Microtus agrestis): an ecological model for studies on transmission dynamics
We propose a model involving the oral inoculation of Echinococcus multilocularis eggs in a vole species and examine the infection dynamics in a dose-response experiment. Defined doses, 100 (n = 8), 500 (n = 5) and 1000 (n = 5) of E. multilocularis eggs were used to inoculate Microtus agrestis. Four female C57BL/6j mice were inoculated with 1000 eggs as positive controls. The groups inoculated with 100 and 500 eggs exhibited significantly higher lesion numbers, and relatively smaller lesion size was observed in the 1000 dose group. Undetectable abortive lesions may be responsible for some form of resource limitation early in the infection, resulting in lower lesion counts and size in the 1000 dose group. The C57BL/6j mice exhibited significantly fewer lesions than M. agrestis. The feasibility of measuring corticosterone (which has been shown to downregulate Th1 cytokines) in rodent hair and tumour necrosis factor (TNF) production in spleen cells was demonstrated by a positive correlation between corticosterone levels and higher lesion counts and TNF production in C57BL/6j, respectively. These results suggest that M. agrestis is more prone to a Th2 immune response than C57BL/6j, which is associated with E. multilocularis susceptibility and may explain why the parasite develops more slowly in murine models. This is the first data to suggest that M. agrestis is capable of supporting E. multilocularis transmission and thus may be suited as a model to describe the infection dynamics in an intermediate host that affects transmission under natural conditions.
KeywordsEchinococcus multilocularis Microtus agrestis TNF Corticosterone
The authors would like to thank Otso Huitu and Heikki Henttonen at METLA (Finnish Forest Research Institute, Finland) for providing the voles for this study. This study was conducted under the framework of the project “Echinococcus multilocularis in Rodents (EMIRO)” funded by EMIDA, Era-Net under the EU-FP7.
Conflict of interest
The authors declare no conflict of interest.
- Amiot F, Voung P, Defontaines M, Pater C, Dautry F, Liance M (1999) Secondary alveolar echinococcosis in lymphotoxi-α and tumor necrosis factor-α deficient mice: exacerbation of Echinococcus multilocularis larval growh is associated with cellular changes in the periparasitic granuloma. Parasite Immunol 21:475–483CrossRefPubMedGoogle Scholar
- Eckert J, Deplazes P, Kern P (2011) Alveolar echinococcosis (Echinococcus multilocularis).Google Scholar
- Liance M, Bresson-Hadni S, Meyer JP, Houin R, Vuitton DA (1990) Cellular immunity in experimental Echinococcus multilocularis infection I. Sequential and comparative study of specific in vivo delayed-type hypersensitivity against E. multilocularis antigens in resistant and sensitive mice. Clin Exp Immunol 82:373–377CrossRefPubMedCentralPubMedGoogle Scholar
- Ohbayashi M (1960) Studies on echinococcosis X: histological observations on experimental cases of multilocular echinococcosis. Jpn J Vet Res 8:134–160Google Scholar
- Ohbayashi M, Rausch RL, Fay FH (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. Leukart, 1863 in the intermediate host. Japanese Journal of Veterinary Research 19 (supplement):1–53Google Scholar
- Russell WMW, Burch RL, Hume CW (1959) The principles of humane experimental technique. Methuen, United KingdomGoogle Scholar
- Stieger C, Hegglin D, Schwarzenback G, Mathis A, Deplazes P (2002) Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitilogy 124:631–640Google Scholar
- Swantek JL, Cobb MH, Geppert TD (1997) Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) is required for lipopolysaccharide stimulation of tumor necrosis factor alpha (TNF-alpha) translation: glucocorticoids inhibit TNF-alpha translation by blocking JNK/SAPK. Mol Cell Biol 17:6247–6282Google Scholar