Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-27T10:11:28.878Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  09 March 2017

ANDREA L. MILLER ,
GERT E. OLSSON ,
SOFIA SOLLENBERG ,
MARION R. WALBURG ,
MOA SKARIN  and
JOHAN HÖGLUND
ANDREA L. MILLER*
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden
GERT E. OLSSON
Affiliation:
Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, 901 83, Sweden
SOFIA SOLLENBERG
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden
MARION R. WALBURG
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden
MOA SKARIN
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden
JOHAN HÖGLUND
Affiliation:
Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden
*
*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
Get access Rights & Permissions [Opens in a new window]

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.

Keywords

Rodentfoxparasitetransmission ecologyhabitatMicrotus agrestisArvicola amphibiusEchinococcus multilocularisVersteria mustelaeHydatigera taeniaeformis
Type
Research Article
Information
Parasitology , Volume 144 , Issue 8 , July 2017 , pp. 1041 - 1051
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Acock, A. C. and Stavig, G. R. (1979). A measure of association for nonparametric statistics. Social Forces 57, 1381–1386.Google Scholar
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, 112–117. http://doi:10.1017/S0022149X13000680 CrossRefGoogle ScholarPubMed
Bates, D., Mächler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48. http://doi:10.18637/jss.v067.i01 Google Scholar
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 CrossRefGoogle ScholarPubMed
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, 239–247. http://dx.doi.org/10.1016/j.pt.2012.03.004 Google Scholar
Deplazes, P., Eckert, J., Mathis, A., Samson-Himmelstjerna, G. V. and Zahner, H. (2016). Parasitology in Veterinary Medicine. Wageningen Academic Publishers, Wageningen, The Netherlands.CrossRefGoogle Scholar
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 Google Scholar
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. 698–716. Oxford University Press, New York, NY.Google Scholar
Eckert, J. and Deplazes, P. (2004). Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clinical Microbiology Reviews 17, 107–135. http://doi:10.1128/CMR.17.1.107-135.2004 CrossRefGoogle ScholarPubMed
Erlinge, S. (1975). Feeding habits of the weasel Mustela nivalis in relation to prey abundance. Oikos 26, 378–384.Google Scholar
Erlinge, S. (1981). Food preference, optimal diet and reproductive output in stoats Mustela erminea in Sweden. Oikos 36, 303–315.CrossRefGoogle Scholar
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, 597–603. http://dx.doi.org/10.2307/1381799 Google Scholar
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 Google Scholar
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, 100–109.Google Scholar
Giesecke, J. (2002). Modern Infectious Disease Epidemiology, 2nd edn. Arnold, London, UK.Google Scholar
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. 251–266. IOS Press, Amsterdam, Netherlands.Google Scholar
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.), S121–S131. http://dx.doi.org/10.1017/S0031182003003512 Google Scholar
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, 407–412. http://dx.doi.org/10.1016/j.pt.2015.06.001 Google Scholar
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, 299–308. http://dx.doi.org/10.1051/parasite/2007144299 CrossRefGoogle Scholar
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. 267–285 . IOS Press, Amsterdam, Netherlands.Google Scholar
Haukisalmi, V. and Henttonen, H. (1993). Population dynamics of Taenia polyacantha metacestodes in the bank vole Clethrionomys glareolus . Annales Zoologici Fennici 30, 81–84.Google Scholar
Haukisalmi, V., Henttonen, H. and Tenora, F. (1988). Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology 57, 807–825.CrossRefGoogle Scholar
Henttonen, H. (1987). The impact of spacing behavior in microtine rodents on the dynamics of least weasels Mustela nivalis: a hypothesis. Oikos 50, 366–370.CrossRefGoogle Scholar
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, 840–842.Google Scholar
Jędrzejewska, B. and Jędrzejewski, W. (1990). Antipredatory behaviour of bank voles and prey choice of weasels--enclosure experiments. Annales Zoologici Fennici 27, 321–328.Google Scholar
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. 213–226. Birkhäuser Basel, Basel, Switzerland.Google Scholar
Katoh, K. and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780. http://mafft.cbrc.jp/alignment/software Google Scholar
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264. http://doi:10.1111/j.0141-9838.2004.00710.x Google Scholar
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, 361–374. http://dx.doi.org/10.1016/j.ijpara.2016.01.009 CrossRefGoogle ScholarPubMed
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, 155–160.Google Scholar
Lenth, R. V. (2016). Least-squares means: the R package (lsmeans). Journal of Statistical Software 69, 1–33. doi:10.18637/jss.v069.i01 Google Scholar
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, 424–432.Google Scholar
Maddison, W. P. and Maddison, D. R. (2016). Mesquite: a modular system for evolutionary analysis. Version 3.10. http://mesquiteproject.org Google Scholar
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 CrossRefGoogle ScholarPubMed
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, 56–63. http://dx.doi.org/10.1016/j.ijppaw.2016.03.001 Google Scholar
Myllymäki, A. (1977). Demographic mechanisms in the fluctuating populations of the field vole Microtus agrestis . Oikos 29, 468–493.Google Scholar
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, 177–185.Google Scholar
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, 427–437.Google Scholar
National Veterinary Institute (SVA). (2016). The red fox tapeworm as a zoonosis (in Swedish). http://www.sva.se/djurhalsa/zoonoser/ravens-dvargbandmask Google Scholar
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 Google Scholar
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, 157–158.Google Scholar
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, 129–139.Google Scholar
Raoul, F., Hegglin, D. and Giraudoux, P. (2015). Trophic ecology, behaviour and host population dynamics in Echinococcus multilocularis transmission. Veterinary Parasitology 213, 162–171. http://dx.doi.org/10.1016/j.vetpar.2015.07.034 CrossRefGoogle ScholarPubMed
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, 263–277.CrossRefGoogle ScholarPubMed
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, 334–348.CrossRefGoogle ScholarPubMed
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, 329–337. https://doi.org/10.1017/S0031182008005428 Google Scholar
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, 145–154. http://dx.doi.org/10.1016/j.ijpara.2010.08.007 Google Scholar
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, 1693–1700. https://doi.org/10.1017/S0031182013001352 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. https://doi.org/10.1017/S0031182002001749 Google Scholar
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, 176–181.Google Scholar
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, 72–77. http://dx.doi.org/10.1016/j.jhep.2008.03.023 Google Scholar
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, 911–920. https://doi.org/10.1017/S0031182007002235 Google Scholar
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, 79–86. https://doi.org/10.1017/S0031182000081075 Google Scholar
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 Google Scholar
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, 172–181. http://dx.doi.org/10.1016/j.vetpar.2015.07.037 Google Scholar
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, 1703–1709. http://dx.doi.org/10.1007/s00436-015-4355-9 Google Scholar
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, 571–575. http://dx.doi.org/10.1016/j.parint.2015.08.006.Google Scholar
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, 158–163. http://dx.doi.org/10.1016/j.ijppaw.2016.05.004 Google Scholar
Wiger, R. (1977). Some pathological effects of endoparasites on rodents with special reference to the population ecology of microtines. Oikos 29, 598–606.Google Scholar
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 Google Scholar
Supplementary material: File

Miller supplementary material

Tables S1-S2

Download Miller supplementary material(File)
File 16.7 KB
Supplementary material: File

Miller supplementary material

Tables S1-S2

Download Miller supplementary material(File)
File 31.6 KB
Supplementary material: File

Miller supplementary material

Table

Download Miller supplementary material(File)
File 12.6 KB