Skip to main content
×
×
Home

Transmission ecology of taeniid larval cestodes in rodents in Sweden, a low endemic area for Echinococcus multilocularis

  • ANDREA L. MILLER (a1), GERT E. OLSSON (a2), SOFIA SOLLENBERG (a1), MARION R. WALBURG (a1), MOA SKARIN (a1) and JOHAN HÖGLUND (a1)...
Summary

Although local prevalence of Echinococcus multilocularis may be high, this zoonotic parasite has an overall low prevalence in foxes and rodents in Sweden. To better understand opportunities for E. multilocularis transmission in the Swedish environment, the aim of this study was to investigate other taeniid cestodes and to relate observed patterns to E. multilocularis. Cestode parasites were examined in fox feces and rodents caught in different habitats from four regions of Sweden. Arvicola amphibius and Microtus agrestis were parasitized with Versteria mustelae, Hydatigera taeniaeformis s. l., and E. multilocularis, whereas Myodes glareolus and Apodemus spp. were parasitized with V. mustelae, Taenia polyacantha, H. taeniaeformis s.l., and Mesocestoides spp. Rodents caught in field habitat (Ar. amphibius, Mi. agrestis) were more likely (OR 10, 95% CI 5–19) to be parasitized than rodents caught in forest habitat (My. glareolus, Apodemus spp.). The parasite preference for each rodent species was present regardless of the type of background contamination from fox feces. These results further support the importance of both ecological barriers and individual species susceptibility in parasite transmission, and indicate that future monitoring for E. multilocularis in the Swedish environment should focus in field habitats where Mi. agrestis and Ar. amphibius are abundant.

Copyright
Corresponding author
*Corresponding author: Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden. Email: andreavet15@gmail.com
References
Hide All
Acock, A. C. and Stavig, G. R. (1979). A measure of association for nonparametric statistics. Social Forces 57, 13811386.
Al-Sabi, M. N. S., Jensen, P. M., Christensen, M. U. and Kapel, C. M. O. (2013). Morphological and molecular analyses of larval taeniid species in small mammals from contrasting habitats in Denmark. Journal of Helminthology 89, 112117. http://doi:10.1017/S0022149X13000680
Bates, D., Mächler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148. http://doi:10.18637/jss.v067.i01
Burlet, P., Deplazes, P. and Hegglin, D. (2011). Age, season and spatio-temporal factors affecting the prevalence of Echinococcus multilocularis and Taenia taeniaeformis in Arvicola terrestris . Parasites & Vectors 4, 6. http://www.parasitesandvectors.com/content/4/1/6
Davidson, R. K., Romig, T., Jenkins, E., Tryland, M. and Robertson, L. J. (2012). The impact of globalisation on the distribution of Echinococcus multilocularis . Trends in Parasitology 28, 239247. http://dx.doi.org/10.1016/j.pt.2012.03.004
Deplazes, P., Eckert, J., Mathis, A., Samson-Himmelstjerna, G. V. and Zahner, H. (2016). Parasitology in Veterinary Medicine. Wageningen Academic Publishers, Wageningen, The Netherlands.
Dorai-Raj, S. (2014). Binom: binomial confidence intervals for several parameterizations, R package version 1.1–1 [Online]. http://CRAN.R-project.org/package=binom
Eckert, J. (1998). Alveolar echinococcosis (Echinococcus multilocularis) and other forms of echinococcosis (Echinococcus vogeli and Echinococcus oligarthrus). In Zoonoses: Biology, Clinical Practice, and Public Health Control (ed. Palmer, S. R., Soulsby, L., Simpson, D. I. H.), pp. 698716. Oxford University Press, New York, NY.
Eckert, J. and Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107135. http://doi:10.1128/CMR.17.1.107-135.2004
Erlinge, S. (1975). Feeding habits of the weasel Mustela nivalis in relation to prey abundance. Oikos 26, 378384.
Erlinge, S. (1981). Food preference, optimal diet and reproductive output in stoats Mustela erminea in Sweden. Oikos 36, 303315.
Erlinge, S., Hoogenboom, I., Agrell, J., Nelson, J. and Sandell, M. (1990). Density-related home-range size and overlap in adult field voles (Microtus agrestis) in southern Sweden. Journal of Mammalogy 71, 597603. http://dx.doi.org/10.2307/1381799
Fox, J. and Weisberg, S. (2011). A (R) Companion to Applied Regression, 2nd Edn. [Online]. Sage, Thousand Oaks, California. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
Fujita, O., Oku, Y., Okamoto, M., Sato, H., Ooi, H. K., Kamiya, M. and Rausch, R. L. (1991). Early development of larval Taenia polyacantha in experimental intermediate hosts. Journal of the Helminthological Society of Washington 58, 100109.
Giesecke, J. (2002). Modern Infectious Disease Epidemiology, 2nd edn. Arnold, London, UK.
Giraudoux, P., Delattre, P., Takahashi, K., Raoul, F., Quéré, J.-P., Craig, P. and Vuitton, D. A. (2002). Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multi-scale approaches? In Cestode Zoonoses: Echinococcus and Cysticercosis: An Emergent and Global Problem (ed. Craig, P. and Pawlowski, Z.), pp. 251266. IOS Press, Amsterdam, Netherlands.
Giraudoux, P., Craig, P. S., Delattre, P., Bao, G., Bartholomot, B., Harraga, S., Quéré, J.-P., Raoul, F., Wang, Y., Shi, D. and Vuitton, D. A. (2003). Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127 (Suppl.), S121S131. http://dx.doi.org/10.1017/S0031182003003512
Gottstein, B., Stojkovic, M., Vuitton, D. A., Millon, L., Marcinkute, A., and Deplazes, P. (2015). Threat of alveolar echinococcosis to public health—a challenge for Europe. Trends in Parasitology 31, 407412. http://dx.doi.org/10.1016/j.pt.2015.06.001
Guislain, M. H., Raoul, F., Poulle, M. L. and Giraudoux, P. (2007). Fox faeces and vole distribution on a local range: ecological data in a parasitological perspective for Echinococcus multilocularis . Parasite 14, 299308. http://dx.doi.org/10.1051/parasite/2007144299
Hansson, L. (2002). Rodent dynamics, population regulation and predation in changeable landscapes: importance for Echinococcus transmission. In Cestode Zoonoses: Echinococcus and Cysticercosis: An Emergent and Global Problem (ed. Craig, P. and Pawlowski, Z.), pp. 267285 . IOS Press, Amsterdam, Netherlands.
Haukisalmi, V. and Henttonen, H. (1993). Population dynamics of Taenia polyacantha metacestodes in the bank vole Clethrionomys glareolus . Annales Zoologici Fennici 30, 8184.
Haukisalmi, V., Henttonen, H. and Tenora, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807825.
Henttonen, H. (1987). The impact of spacing behavior in microtine rodents on the dynamics of least weasels Mustela nivalis: a hypothesis. Oikos 50, 366370.
Iwaki, T., Abe, N., Shibahara, T., Oku, Y. and Kamiya, M. (1996). Developmental study of Taenia mustelae in the intermediate and definitive hosts, with a note on the life cycle of T. mustelae in Hokkaido, Japan. The Journal of Parasitology 82, 840842.
Jędrzejewska, B. and Jędrzejewski, W. (1990). Antipredatory behaviour of bank voles and prey choice of weasels--enclosure experiments. Annales Zoologici Fennici 27, 321328.
Jeppsson, B. (1990). Effects of density and resources on the social system of water voles. In Social Systems and Population Cycles in Voles (ed. Tamarin, R. H., Ostfeld, R. S., Pugh, S. R. and Bujalska, G.), pp. 213226. Birkhäuser Basel, Basel, Switzerland.
Katoh, K. and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772780. http://mafft.cbrc.jp/alignment/software
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247264. http://doi:10.1111/j.0141-9838.2004.00710.x
Lavikainen, A., Iwaki, T., Haukisalmi, V., Konyaev, S. V., Casiraghi, M., Dokuchaev, N. E., Galimberti, A., Halajian, A., Henttonen, H., Ichikawa-Seki, M., Itagaki, T., Krivopalov, A. V., Meri, S., Morand, S., Näreaho, A., Olsson, G. E., Ribas, A., Terefe, Y. & Nakao, M. (2016). Reappraisal of Hydatigera taeniaeformis (Batsch, 1786) (Cestoda: Taeniidae) sensu lato with description of Hydatigera kamiyai n. sp. International Journal for Parasitology 46, 361374. http://dx.doi.org/10.1016/j.ijpara.2016.01.009
Le Pesteur, M. H., Giraudoux, P., Delattre, P., Damange, J. P. and Quéré, J. P. (1992). Spatiotemporal distribution of four species of cestodes in a landscape of mid-altitude mountains (Jura, France). Annales de Parasitologie Humaine et Comparée (Paris) 67, 155160.
Lenth, R. V. (2016). Least-squares means: the R package (lsmeans). Journal of Statistical Software 69, 133. doi:10.18637/jss.v069.i01
Liberg, O. (1984). Food habits and prey impact by feral and house-based domestic cats in a rural area in southern Sweden. Journal of Mammalogy 65, 424432.
Maddison, W. P. and Maddison, D. R. (2016). Mesquite: a modular system for evolutionary analysis. Version 3.10. http://mesquiteproject.org
Miller, A. L., Olsson, G. E., Sollenberg, S., Skarin, M., Wahlström, H. and Höglund, J. (2016 a). Support for targeted sampling of red fox (Vulpes vulpes) feces in Sweden: a method to improve the probability of finding Echinococcus multilocularis . Parasites & Vectors 9, 613. http://doi10.1186/s13071-016-1897-3
Miller, A. L., Olsson, G. E., Walburg, M. R., Sollenberg, S., Skarin, M., Ley, C., Wahlström, H. and Höglund, J. (2016 b). First identification of Echinococcus multilocularis in rodent intermediate hosts in Sweden. International Journal of Parasitology: Parasites and Wildlife 5, 5663. http://dx.doi.org/10.1016/j.ijppaw.2016.03.001
Myllymäki, A. (1977). Demographic mechanisms in the fluctuating populations of the field vole Microtus agrestis . Oikos 29, 468493.
Myllymäki, A., Paasikallio, A., Pankakoski, E. and Kanervo, V. (1971). Removal experiments on small quadrats as a means of rapid assessment of the abundance of small mammals. Annales Zoologici Fennici 8, 177185.
Nakao, M., Lavikainen, A., Iwaki, T., Haukisalmi, V., Konyaev, S., Oku, Y., Okamoto, M. and Ito, A. (2013). Molecular phylogeny of the genus Taenia (Cestoda: Taeniidae): proposals for the resurrection of Hydatigera Lamarck, 1816 and the creation of a new genus Versteria . International Journal for Parasitology 43, 427437.
National Veterinary Institute (SVA). (2016). The red fox tapeworm as a zoonosis (in Swedish). http://www.sva.se/djurhalsa/zoonoser/ravens-dvargbandmask
Osterman Lind, E., Juremalm, M., Christensson, D., Widgren, S., Hallgren, G., Ågren, E. O., Uhlhorn, H., Lindberg, A., Cedersmyg, M. and Wahlström, H. (2011). First detection of Echinococcus multilocularis in Sweden, February to March 2011. Euro Surveillance 16, 19836. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19836
Pétavy, A.-F., Tenora, F. and Deblock, S. (2003). Co-occurrence of metacestodes of Echinococcus multilocularis and Taenia taeniaeformis (Cestoda) in Arvicola terrestris (Rodentia) in France. Folia Parasitologica 50, 157158.
Raoul, F., Deplazes, P., Rieffel, D., Lambert, J.-C. & Giraudoux, P. (2010). Predator dietary response to prey density variation and consequences for cestode transmission. Oecologia 164, 129139.
Raoul, F., Hegglin, D. and Giraudoux, P. (2015). Trophic ecology, behaviour and host population dynamics in Echinococcus multilocularis transmission. Veterinary Parasitology 213, 162171. http://dx.doi.org/10.1016/j.vetpar.2015.07.034
Rausch, R. L. and Fay, F. H. (1988 a). Postoncospheral development and cycle of Taenia polyacantha Leuckart, 1856 (Cestoda: Taeniidae). First part. Annales de Parasitologie Humaine et Comparée (Paris) 63, 263277.
Rausch, R. L. and Fay, F. H. (1988 b). Postoncospheral development and cycle of Taenia polyacantha Leuckart, 1856 (Cestoda: Taeniidae). Second part. Annales de Parasitologie Humaine et Comparée (Paris) 63, 334348.
Reperant, L. A., Hegglin, D., Tanner, I., Fischer, C. and Deplazes, P. (2009). Rodents as shared indicators for zoonotic parasites of carnivores in urban environments. Parasitology 136, 329337. https://doi.org/10.1017/S0031182008005428
Robardet, E., Giraudoux, P., Caillot, C., Augot, D., Boue, F. and Barrat, J. (2011). Fox defecation behaviour in relation to spatial distribution of voles in an urbanised area: an increasing risk of transmission of Echinococcus multilocularis? International Journal for Parasitology 41, 145154. http://dx.doi.org/10.1016/j.ijpara.2010.08.007
Said-Ali, Z., Grenouillet, F., Knapp, J., Bresson-Hadni, S., Vuitton, D. A., Raoul, F., Richou, C., Millon, L., Giraudoux, P. and the FrancEchino Network. (2013). Detecting nested clusters of human alveolar echinococcosis. Parasitology 140, 16931700. https://doi.org/10.1017/S0031182013001352
Stieger, C., Hegglin, D., Schwarzenbach, G., Mathis, A. and Deplazes, P. (2002). Spatial and temporal aspects of urban transmission of Echinococcus multilocularis . Parasitology 124, 631640. https://doi.org/10.1017/S0031182002001749
Tenora, F., Wiger, R. & Baruš, V. (1979). Seasonal and annual variations in the prevalence of helminths in a cyclic population of Clethrionomys glareolus . Holarctic Ecology 2, 176181.
Torgerson, P. R., Schweiger, A., Deplazes, P., Pohar, M., Reichen, J., Ammann, R. W., Tarr, P. E., Halkik, N. and Müllhaupt, B. (2008). Alveolar echinococcosis: from a deadly disease to a well-controlled infection. Relative survival and economic analysis in Switzerland over the last 35 years. Journal of Hepatology 49, 7277. http://dx.doi.org/10.1016/j.jhep.2008.03.023
Trachsel, D., Deplazes, P. and Mathis, A. (2007). Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology 134, 911920. https://doi.org/10.1017/S0031182007002235
Veit, P., Bilger, B., Schad, V., Schäfer, J., Frank, W. and Lucius, R. (1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 7986. https://doi.org/10.1017/S0031182000081075
Wahlström, H., Lindberg, A., Lindh, J., Wallensten, A., Lindqvist, R., Plym-Forshell, L., Osterman Lind, E., Ågren, E. O., Widgren, S., Carlsson, U., Christensson, D., Cedersmyg, M., Lindström, E., Olsson, G. E., Hörnfeldt, B., Barragan, A., Davelid, C., Hjertqvist, M. and Elvander, M. (2012). Investigations and actions taken during 2011 due to the first finding of Echinococcus multilocularis in Sweden. Euro Surveillance 17, 20215. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20215
Wahlström, H., Enemark, H. L., Davidson, R. K. and Oksanen, A. (2015). Present status, actions taken and future considerations due to the findings of E. multilocularis in two Scandinavian countries. Veterinary Parasitology 213, 172181. http://dx.doi.org/10.1016/j.vetpar.2015.07.037
Woolsey, I. D., Bune, N. E. T., Jensen, P. M., Deplazes, P. and Kapel, C. M. O. (2015 a). Echinococcus multilocularis infection in the field vole (Microtus agrestis): an ecological model for studies on transmission dynamics. Parasitology Research 114, 17031709. http://dx.doi.org/10.1007/s00436-015-4355-9
Woolsey, I. D., Jensen, P. M., Deplazes, P. and Kapel, C. M. O. (2015 b). Establishment and development of Echinococcus multilocularis metacestodes in the common vole (Microtus arvalis) after oral inoculation with parasite eggs. Parasitology International 64, 571575. http://dx.doi.org/10.1016/j.parint.2015.08.006.
Woolsey, I. D., Jensen, P. M., Deplazes, P. and Kapel, C. M. O. (2016). Peroral Echinococcus multilocularis inoculation in Myodes glareolus, Mesocricetus auratus and Mus musculus (CD-1 IGS and C57BL/6j). International Journal for Parasitology: Parasites and Wildlife 5, 158163. http://dx.doi.org/10.1016/j.ijppaw.2016.05.004
Wiger, R. (1977). Some pathological effects of endoparasites on rodents with special reference to the population ecology of microtines. Oikos 29, 598606.
Wilson, D. E. and Reeder, D. M. (2005). Mammal species of the world: a taxonomic and geographic reference, 3rd Edn. Johns Hopkins University Press, Baltimore, Maryland. Online Database from Smithsonian National Museum of Natural History. http://vertebrates.si.edu/msw/mswCFApp/msw/index.cfm
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
WORD
Supplementary materials

Miller supplementary material
Tables S1-S2

 Word (17 KB)
17 KB
EXCEL
Supplementary materials

Miller supplementary material
Table

 Excel (13 KB)
13 KB
WORD
Supplementary materials

Miller supplementary material
Tables S1-S2

 Word (32 KB)
32 KB

Metrics

Altmetric attention score