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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">First identification of <italic>Echinococcus multilocularis</italic> in rodent intermediate hosts in Sweden</title><author><name sortKey="Miller, Andrea L" sort="Miller, Andrea L" uniqKey="Miller A" first="Andrea L." last="Miller">Andrea L. Miller</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Olsson, Gert E" sort="Olsson, Gert E" uniqKey="Olsson G" first="Gert E." last="Olsson">Gert E. Olsson</name><affiliation><nlm:aff id="aff2">Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, 901 83, Sweden</nlm:aff></affiliation></author><author><name sortKey="Walburg, Marion R" sort="Walburg, Marion R" uniqKey="Walburg M" first="Marion R." last="Walburg">Marion R. Walburg</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Sollenberg, Sofia" sort="Sollenberg, Sofia" uniqKey="Sollenberg S" first="Sofia" last="Sollenberg">Sofia Sollenberg</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Skarin, Moa" sort="Skarin, Moa" uniqKey="Skarin M" first="Moa" last="Skarin">Moa Skarin</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Ley, Cecilia" sort="Ley, Cecilia" uniqKey="Ley C" first="Cecilia" last="Ley">Cecilia Ley</name><affiliation><nlm:aff id="aff3">Department of Biomedical Sciences and Veterinary Public Health, Section for Pathology, Swedish University of Agricultural Sciences, Box 7028, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Wahlstrom, Helene" sort="Wahlstrom, Helene" uniqKey="Wahlstrom H" first="Helene" last="Wahlström">Helene Wahlström</name><affiliation><nlm:aff id="aff4">Department of Disease Control and Epidemiology, Zoonosiscenter, National Veterinary Institute, Uppsala, 751 89, Sweden</nlm:aff></affiliation></author><author><name sortKey="Hoglund, Johan" sort="Hoglund, Johan" uniqKey="Hoglund J" first="Johan" last="Höglund">Johan Höglund</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27054089</idno><idno type="pmc">4804384</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4804384</idno><idno type="RBID">PMC:4804384</idno><idno type="doi">10.1016/j.ijppaw.2016.03.001</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000067</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000067</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">First identification of <italic>Echinococcus multilocularis</italic> in rodent intermediate hosts in Sweden</title><author><name sortKey="Miller, Andrea L" sort="Miller, Andrea L" uniqKey="Miller A" first="Andrea L." last="Miller">Andrea L. Miller</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Olsson, Gert E" sort="Olsson, Gert E" uniqKey="Olsson G" first="Gert E." last="Olsson">Gert E. Olsson</name><affiliation><nlm:aff id="aff2">Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, 901 83, Sweden</nlm:aff></affiliation></author><author><name sortKey="Walburg, Marion R" sort="Walburg, Marion R" uniqKey="Walburg M" first="Marion R." last="Walburg">Marion R. Walburg</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Sollenberg, Sofia" sort="Sollenberg, Sofia" uniqKey="Sollenberg S" first="Sofia" last="Sollenberg">Sofia Sollenberg</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Skarin, Moa" sort="Skarin, Moa" uniqKey="Skarin M" first="Moa" last="Skarin">Moa Skarin</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Ley, Cecilia" sort="Ley, Cecilia" uniqKey="Ley C" first="Cecilia" last="Ley">Cecilia Ley</name><affiliation><nlm:aff id="aff3">Department of Biomedical Sciences and Veterinary Public Health, Section for Pathology, Swedish University of Agricultural Sciences, Box 7028, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author><author><name sortKey="Wahlstrom, Helene" sort="Wahlstrom, Helene" uniqKey="Wahlstrom H" first="Helene" last="Wahlström">Helene Wahlström</name><affiliation><nlm:aff id="aff4">Department of Disease Control and Epidemiology, Zoonosiscenter, National Veterinary Institute, Uppsala, 751 89, Sweden</nlm:aff></affiliation></author><author><name sortKey="Hoglund, Johan" sort="Hoglund, Johan" uniqKey="Hoglund J" first="Johan" last="Höglund">Johan Höglund</name><affiliation><nlm:aff id="aff1">Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</nlm:aff></affiliation></author></analytic><series><title level="j">International Journal for Parasitology: Parasites and Wildlife</title><idno type="eISSN">2213-2244</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><italic>Echinococcus multilocularis</italic> is a zoonotic tapeworm with a sylvatic lifecycle and an expanding range in Europe. Monitoring efforts following its first identification in 2011 in Sweden have focused on the parasite's definitive host, the red fox (<italic>Vulpes vulpes</italic>). However, identifying rodent intermediate hosts is important to recognize opportunities for parasite transmission. During 2013–2015, livers from a total of 1566 rodents from four regions in Sweden were examined for <italic>E. multilocularis</italic> metacestode lesions. Species identity of suspect parasite lesions was confirmed by PCR and sequencing. <italic>E. multilocularis</italic> positive lesions >6 mm in diameter were also examined histologically. One <italic>Microtus agrestis</italic> out of 187 (0.5%, 95%CI: 0–2.9%), 8/439 (1.8%, 95%CI: 0.8–3.6%) <italic>Arvicola amphibius</italic>, 0/655 (0%, 95%CI: 0–0.6%) <italic>Myodes glareolus</italic>, and 0/285 (0%, 95%CI: 0–1.3%) <italic>Apodemus</italic> spp. contained <italic>E. multilocularis</italic> metacestode lesions. Presence of protoscoleces was confirmed in the infected <italic>M. agrestis</italic> and in three of eight infected <italic>A. amphibius</italic>. Six of the nine positive rodents were captured from the same field. This is the first report of <italic>E. multilocularis</italic> in intermediate hosts in Sweden. The cluster of positive rodents in one field shows that local parasite prevalence can be high in Sweden despite overall low national prevalence in foxes (<0.1%). The presence of protoscoleces in infected <italic>M. agrestis</italic> and <italic>A. amphibius</italic> indicate these species can serve as competent intermediate hosts in Sweden. However, their relative importance for <italic>E. multilocularis</italic> transmission in the Swedish environment is not yet possible to assess. In contrast, the negative findings in all <italic>M. glareolus</italic> and <italic>Apodemus</italic> spp. suggest that these species are of no importance.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Barabasi, S S" uniqKey="Barabasi S">S.S. Barabási</name></author><author><name sortKey="Marosf I, L" uniqKey="Marosf I L">L. Marosfői</name></author><author><name sortKey="Barabasi, Z S" uniqKey="Barabasi Z">Z.S. Barabási</name></author><author><name sortKey="Cozma, V" uniqKey="Cozma V">V. Cozma</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Burlet, P" uniqKey="Burlet P">P. Burlet</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author><author><name sortKey="Hegglin, D" uniqKey="Hegglin D">D. Hegglin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Dell Arte, G L" uniqKey="Dell Arte G">G.L. Dell'Arte</name></author><author><name sortKey="Laaksonen, T" uniqKey="Laaksonen T">T. Laaksonen</name></author><author><name sortKey="Norrdahl, K" uniqKey="Norrdahl K">K. Norrdahl</name></author><author><name sortKey="Korpim Ki, E" uniqKey="Korpim Ki E">E. Korpimäki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Eckert, J" uniqKey="Eckert J">J. Eckert</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Erlinge, S" uniqKey="Erlinge S">S. Erlinge</name></author><author><name sortKey="Goransson, G" uniqKey="Goransson G">G. Göransson</name></author><author><name sortKey="Hansson, L" uniqKey="Hansson L">L. Hansson</name></author><author><name sortKey="Hogstedt, G" uniqKey="Hogstedt G">G. Högstedt</name></author><author><name sortKey="Liberg, O" uniqKey="Liberg O">O. Liberg</name></author><author><name sortKey="Nilsson, I N" uniqKey="Nilsson I">I.N. Nilsson</name></author><author><name sortKey="Nilsson, T" uniqKey="Nilsson T">T. Nilsson</name></author><author><name sortKey="Von Schantz, T" uniqKey="Von Schantz T">T. von Schantz</name></author><author><name sortKey="Sylven, M" uniqKey="Sylven M">M. Sylvén</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Giraudoux, P" uniqKey="Giraudoux P">P. Giraudoux</name></author><author><name sortKey="Craig, P S" uniqKey="Craig P">P.S. Craig</name></author><author><name sortKey="Delattre, P" uniqKey="Delattre P">P. Delattre</name></author><author><name sortKey="Bao, G" uniqKey="Bao G">G. Bao</name></author><author><name sortKey="Bartholomot, B" uniqKey="Bartholomot B">B. Bartholomot</name></author><author><name sortKey="Harraga, S" uniqKey="Harraga S">S. Harraga</name></author><author><name sortKey="Quere, J P" uniqKey="Quere J">J.-P. Quéré</name></author><author><name sortKey="Raoul, F" uniqKey="Raoul F">F. Raoul</name></author><author><name sortKey="Wang, Y" uniqKey="Wang Y">Y. Wang</name></author><author><name sortKey="Shi, D" uniqKey="Shi D">D. Shi</name></author><author><name sortKey="Vuitton, D A" uniqKey="Vuitton D">D.-A. Vuitton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gottstein, B" uniqKey="Gottstein B">B. Gottstein</name></author><author><name sortKey="Saucy, F" uniqKey="Saucy F">F. Saucy</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author><author><name sortKey="Reichen, J" uniqKey="Reichen J">J. Reichen</name></author><author><name sortKey="Demierre, G" uniqKey="Demierre G">G. Demierre</name></author><author><name sortKey="Busato, A" uniqKey="Busato A">A. Busato</name></author><author><name sortKey="Zuercher, C" uniqKey="Zuercher C">C. Zuercher</name></author><author><name sortKey="Pugin, P" uniqKey="Pugin P">P. Pugin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Guerra, D" uniqKey="Guerra D">D. Guerra</name></author><author><name sortKey="Hegglin, D" uniqKey="Hegglin D">D. Hegglin</name></author><author><name sortKey="Bacciarini, L" uniqKey="Bacciarini L">L. Bacciarini</name></author><author><name sortKey="Schnyder, M" uniqKey="Schnyder M">M. Schnyder</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Guislain, M H" uniqKey="Guislain M">M.-H. Guislain</name></author><author><name sortKey="Raoul, F" uniqKey="Raoul F">F. Raoul</name></author><author><name sortKey="Giraudoux, P" uniqKey="Giraudoux P">P. Giraudoux</name></author><author><name sortKey="Terrier, M E" uniqKey="Terrier M">M.-E. Terrier</name></author><author><name sortKey="Froment, G" uniqKey="Froment G">G. Froment</name></author><author><name sortKey="Ferte, H" uniqKey="Ferte H">H. Ferté</name></author><author><name sortKey="Poulle, M L" uniqKey="Poulle M">M.-L. Poulle</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hanosset, R" uniqKey="Hanosset R">R. Hanosset</name></author><author><name sortKey="Saegerman, C" uniqKey="Saegerman C">C. Saegerman</name></author><author><name sortKey="Adant, S" uniqKey="Adant S">S. Adant</name></author><author><name sortKey="Massart, L" uniqKey="Massart L">L. Massart</name></author><author><name sortKey="Losson, B" uniqKey="Losson B">B. Losson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hansen, F" uniqKey="Hansen F">F. Hansen</name></author><author><name sortKey="Jeltsch, F" uniqKey="Jeltsch F">F. Jeltsch</name></author><author><name sortKey="Tackmann, K" uniqKey="Tackmann K">K. Tackmann</name></author><author><name sortKey="Staubach, C" uniqKey="Staubach C">C. Staubach</name></author><author><name sortKey="Thulke, H H" uniqKey="Thulke H">H.H. Thulke</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hansson, L" uniqKey="Hansson L">L. Hansson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hofer, S" uniqKey="Hofer S">S. Hofer</name></author><author><name sortKey="Gloor, S" uniqKey="Gloor S">S. Gloor</name></author><author><name sortKey="Muller, U" uniqKey="Muller U">U. Müller</name></author><author><name sortKey="Mathis, A" uniqKey="Mathis A">A. Mathis</name></author><author><name sortKey="Hegglin, D" uniqKey="Hegglin D">D. Hegglin</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Houin, R" uniqKey="Houin R">R. Houin</name></author><author><name sortKey="Deniau, M" uniqKey="Deniau M">M. Deniau</name></author><author><name sortKey="Liance, M" uniqKey="Liance M">M. Liance</name></author><author><name sortKey="Puel, F" uniqKey="Puel F">F. Puel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Liccioli, S" uniqKey="Liccioli S">S. Liccioli</name></author><author><name sortKey="Duignan, P J" uniqKey="Duignan P">P.J. Duignan</name></author><author><name sortKey="Lejeune, M" uniqKey="Lejeune M">M. Lejeune</name></author><author><name sortKey="Deunk, J" uniqKey="Deunk J">J. Deunk</name></author><author><name sortKey="Majid, S" uniqKey="Majid S">S. Majid</name></author><author><name sortKey="Massolo, A" uniqKey="Massolo A">A. Massolo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lindstrom, E" uniqKey="Lindstrom E">E. Lindström</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Myllym Ki, A" uniqKey="Myllym Ki A">A. Myllymäki</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Myllym Ki, A" uniqKey="Myllym Ki A">A. Myllymäki</name></author><author><name sortKey="Paasikallio, A" uniqKey="Paasikallio A">A. Paasikallio</name></author><author><name sortKey="Pankakoski, E" uniqKey="Pankakoski E">E. Pankakoski</name></author><author><name sortKey="Kanervo, V" uniqKey="Kanervo V">V. Kanervo</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Piras, P" uniqKey="Piras P">P. Piras</name></author><author><name sortKey="Marcolini, F" uniqKey="Marcolini F">F. Marcolini</name></author><author><name sortKey="Claude, J" uniqKey="Claude J">J. Claude</name></author><author><name sortKey="Ventura, J" uniqKey="Ventura J">J. Ventura</name></author><author><name sortKey="Kotsakis, T" uniqKey="Kotsakis T">T. Kotsakis</name></author><author><name sortKey="Cubo, J" uniqKey="Cubo J">J. Cubo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Raoul, F" uniqKey="Raoul F">F. Raoul</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author><author><name sortKey="Rieffel, D" uniqKey="Rieffel D">D. Rieffel</name></author><author><name sortKey="Lambert, J C" uniqKey="Lambert J">J.-C. Lambert</name></author><author><name sortKey="Giraudoux, P" uniqKey="Giraudoux P">P. Giraudoux</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Reperant, L A" uniqKey="Reperant L">L.A. Reperant</name></author><author><name sortKey="Hegglin, D" uniqKey="Hegglin D">D. Hegglin</name></author><author><name sortKey="Tanner, I" uniqKey="Tanner I">I. Tanner</name></author><author><name sortKey="Fischer, C" uniqKey="Fischer C">C. Fischer</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Romig, T" uniqKey="Romig T">T. Romig</name></author><author><name sortKey="Dinkel, A" uniqKey="Dinkel A">A. Dinkel</name></author><author><name sortKey="Mackenstedt, U" uniqKey="Mackenstedt U">U. Mackenstedt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stieger, C" uniqKey="Stieger C">C. Stieger</name></author><author><name sortKey="Hegglin, D" uniqKey="Hegglin D">D. Hegglin</name></author><author><name sortKey="Schwarzenbach, G" uniqKey="Schwarzenbach G">G. Schwarzenbach</name></author><author><name sortKey="Mathis, A" uniqKey="Mathis A">A. Mathis</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Torgerson, P R" uniqKey="Torgerson P">P.R. Torgerson</name></author><author><name sortKey="Keller, K" uniqKey="Keller K">K. Keller</name></author><author><name sortKey="Magnotta, M" uniqKey="Magnotta M">M. Magnotta</name></author><author><name sortKey="Ragland, N" uniqKey="Ragland N">N. Ragland</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Torgerson, P R" uniqKey="Torgerson P">P.R. Torgerson</name></author><author><name sortKey="Schweiger, A" uniqKey="Schweiger A">A. Schweiger</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author><author><name sortKey="Pohar, M" uniqKey="Pohar M">M. Pohar</name></author><author><name sortKey="Reichen, J" uniqKey="Reichen J">J. Reichen</name></author><author><name sortKey="Ammann, R W" uniqKey="Ammann R">R.W. Ammann</name></author><author><name sortKey="Tarr, P E" uniqKey="Tarr P">P.E. Tarr</name></author><author><name sortKey="Halkik, N" uniqKey="Halkik N">N. Halkik</name></author><author><name sortKey="Mullhaupt, B" uniqKey="Mullhaupt B">B. Müllhaupt</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Trachsel, D" uniqKey="Trachsel D">D. Trachsel</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author><author><name sortKey="Mathis, A" uniqKey="Mathis A">A. Mathis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Von Schantz, T" uniqKey="Von Schantz T">T. von Schantz</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Veit, P" uniqKey="Veit P">P. Veit</name></author><author><name sortKey="Bilger, B" uniqKey="Bilger B">B. Bilger</name></author><author><name sortKey="Schad, V" uniqKey="Schad V">V. Schad</name></author><author><name sortKey="Sch Fer, J" uniqKey="Sch Fer J">J. Schäfer</name></author><author><name sortKey="Frank, W" uniqKey="Frank W">W. Frank</name></author><author><name sortKey="Lucius, R" uniqKey="Lucius R">R. Lucius</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Viel, J F" uniqKey="Viel J">J.-F. Viel</name></author><author><name sortKey="Giraudoux, P" uniqKey="Giraudoux P">P. Giraudoux</name></author><author><name sortKey="Abrial, V" uniqKey="Abrial V">V. Abrial</name></author><author><name sortKey="Bresson Hadni, S" uniqKey="Bresson Hadni S">S. Bresson-Hadni</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wahlstrom, H" uniqKey="Wahlstrom H">H. Wahlstrom</name></author><author><name sortKey="Lindberg, A" uniqKey="Lindberg A">A. Lindberg</name></author><author><name sortKey="Lindh, J" uniqKey="Lindh J">J. Lindh</name></author><author><name sortKey="Wallensten, A" uniqKey="Wallensten A">A. Wallensten</name></author><author><name sortKey="Lindqvist, R" uniqKey="Lindqvist R">R. Lindqvist</name></author><author><name sortKey="Plym Forshell, L" uniqKey="Plym Forshell L">L. Plym-Forshell</name></author><author><name sortKey="Osterman Lind, E" uniqKey="Osterman Lind E">E. Osterman Lind</name></author><author><name sortKey="Agren, E O" uniqKey="Agren E">E.O. Agren</name></author><author><name sortKey="Widgren, S" uniqKey="Widgren S">S. Widgren</name></author><author><name sortKey="Carlsson, U" uniqKey="Carlsson U">U. Carlsson</name></author><author><name sortKey="Christensson, D" uniqKey="Christensson D">D. Christensson</name></author><author><name sortKey="Cedersmyg, M" uniqKey="Cedersmyg M">M. Cedersmyg</name></author><author><name sortKey="Lindstrom, E" uniqKey="Lindstrom E">E. Lindström</name></author><author><name sortKey="Olsson, G E" uniqKey="Olsson G">G.E. Olsson</name></author><author><name sortKey="Hornfeldt, B" uniqKey="Hornfeldt B">B. Hörnfeldt</name></author><author><name sortKey="Barragan, A" uniqKey="Barragan A">A. Barragan</name></author><author><name sortKey="Davelid, C" uniqKey="Davelid C">C. Davelid</name></author><author><name sortKey="Hjertqvist, M" uniqKey="Hjertqvist M">M. Hjertqvist</name></author><author><name sortKey="Elvander, M" uniqKey="Elvander M">M. Elvander</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wilson, D E" uniqKey="Wilson D">D.E. Wilson</name></author><author><name sortKey="Reeder, D M" uniqKey="Reeder D">D.M. Reeder</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Woolsey, I D" uniqKey="Woolsey I">I.D. Woolsey</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Woolsey, I D" uniqKey="Woolsey I">I.D. Woolsey</name></author><author><name sortKey="Bune, N E T" uniqKey="Bune N">N.E.T. Bune</name></author><author><name sortKey="Jensen, P M" uniqKey="Jensen P">P.M. Jensen</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author><author><name sortKey="Kapel, C M O" uniqKey="Kapel C">C.M.O. Kapel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Woolsey, I D" uniqKey="Woolsey I">I.D. Woolsey</name></author><author><name sortKey="Jensen, P M" uniqKey="Jensen P">P.M. Jensen</name></author><author><name sortKey="Deplazes, P" uniqKey="Deplazes P">P. Deplazes</name></author><author><name sortKey="Kapel, C M O" uniqKey="Kapel C">C.M.O. Kapel</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Parasitol Parasites Wildl</journal-id><journal-id journal-id-type="iso-abbrev">Int J Parasitol Parasites Wildl</journal-id><journal-title-group><journal-title>International Journal for Parasitology: Parasites and Wildlife</journal-title></journal-title-group><issn pub-type="epub">2213-2244</issn><publisher><publisher-name>Elsevier</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27054089</article-id><article-id pub-id-type="pmc">4804384</article-id><article-id pub-id-type="publisher-id">S2213-2244(16)30008-6</article-id><article-id pub-id-type="doi">10.1016/j.ijppaw.2016.03.001</article-id><article-categories><subj-group subj-group-type="heading"><subject>Regular article</subject></subj-group></article-categories><title-group><article-title>First identification of <italic>Echinococcus multilocularis</italic> in rodent intermediate hosts in Sweden</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Miller</surname><given-names>Andrea L.</given-names></name><email>andrea.miller@slu.se</email><xref rid="aff1" ref-type="aff">a</xref><xref rid="cor1" ref-type="corresp">∗</xref></contrib><contrib contrib-type="author"><name><surname>Olsson</surname><given-names>Gert E.</given-names></name><xref rid="aff2" ref-type="aff">b</xref></contrib><contrib contrib-type="author"><name><surname>Walburg</surname><given-names>Marion R.</given-names></name><xref rid="aff1" ref-type="aff">a</xref></contrib><contrib contrib-type="author"><name><surname>Sollenberg</surname><given-names>Sofia</given-names></name><xref rid="aff1" ref-type="aff">a</xref></contrib><contrib contrib-type="author"><name><surname>Skarin</surname><given-names>Moa</given-names></name><xref rid="aff1" ref-type="aff">a</xref></contrib><contrib contrib-type="author"><name><surname>Ley</surname><given-names>Cecilia</given-names></name><xref rid="aff3" ref-type="aff">c</xref></contrib><contrib contrib-type="author"><name><surname>Wahlström</surname><given-names>Helene</given-names></name><xref rid="aff4" ref-type="aff">d</xref></contrib><contrib contrib-type="author"><name><surname>Höglund</surname><given-names>Johan</given-names></name><xref rid="aff1" ref-type="aff">a</xref></contrib></contrib-group><aff id="aff1"><label>a</label>Department of Biomedical Sciences and Veterinary Public Health, Section for Parasitology, Swedish University of Agricultural Sciences, Box 7036, Uppsala, 750 07, Sweden</aff><aff id="aff2"><label>b</label>Department of Wildlife, Fish and Environmental Studies, Swedish University of Agricultural Sciences, Umeå, 901 83, Sweden</aff><aff id="aff3"><label>c</label>Department of Biomedical Sciences and Veterinary Public Health, Section for Pathology, Swedish University of Agricultural Sciences, Box 7028, Uppsala, 750 07, Sweden</aff><aff id="aff4"><label>d</label>Department of Disease Control and Epidemiology, Zoonosiscenter, National Veterinary Institute, Uppsala, 751 89, Sweden</aff><author-notes><corresp id="cor1"><label>∗</label>Corresponding author. <email>andrea.miller@slu.se</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>08</day><month>3</month><year>2016</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="collection"><month>4</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>08</day><month>3</month><year>2016</year></pub-date><volume>5</volume><issue>1</issue><fpage>56</fpage><lpage>63</lpage><history><date date-type="received"><day>29</day><month>1</month><year>2016</year></date><date date-type="rev-recd"><day>4</day><month>3</month><year>2016</year></date><date date-type="accepted"><day>5</day><month>3</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 The Authors</copyright-statement><copyright-year>2016</copyright-year><license license-type="CC BY-NC-ND" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/"><license-p>This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).</license-p></license></permissions><abstract><p><italic>Echinococcus multilocularis</italic> is a zoonotic tapeworm with a sylvatic lifecycle and an expanding range in Europe. Monitoring efforts following its first identification in 2011 in Sweden have focused on the parasite's definitive host, the red fox (<italic>Vulpes vulpes</italic>). However, identifying rodent intermediate hosts is important to recognize opportunities for parasite transmission. During 2013–2015, livers from a total of 1566 rodents from four regions in Sweden were examined for <italic>E. multilocularis</italic> metacestode lesions. Species identity of suspect parasite lesions was confirmed by PCR and sequencing. <italic>E. multilocularis</italic> positive lesions >6 mm in diameter were also examined histologically. One <italic>Microtus agrestis</italic> out of 187 (0.5%, 95%CI: 0–2.9%), 8/439 (1.8%, 95%CI: 0.8–3.6%) <italic>Arvicola amphibius</italic>, 0/655 (0%, 95%CI: 0–0.6%) <italic>Myodes glareolus</italic>, and 0/285 (0%, 95%CI: 0–1.3%) <italic>Apodemus</italic> spp. contained <italic>E. multilocularis</italic> metacestode lesions. Presence of protoscoleces was confirmed in the infected <italic>M. agrestis</italic> and in three of eight infected <italic>A. amphibius</italic>. Six of the nine positive rodents were captured from the same field. This is the first report of <italic>E. multilocularis</italic> in intermediate hosts in Sweden. The cluster of positive rodents in one field shows that local parasite prevalence can be high in Sweden despite overall low national prevalence in foxes (<0.1%). The presence of protoscoleces in infected <italic>M. agrestis</italic> and <italic>A. amphibius</italic> indicate these species can serve as competent intermediate hosts in Sweden. However, their relative importance for <italic>E. multilocularis</italic> transmission in the Swedish environment is not yet possible to assess. In contrast, the negative findings in all <italic>M. glareolus</italic> and <italic>Apodemus</italic> spp. suggest that these species are of no importance.</p></abstract><abstract abstract-type="graphical"><title>Graphical abstract</title><fig id="undfig1" position="anchor"><graphic xlink:href="fx1"></graphic></fig></abstract><abstract abstract-type="author-highlights"><title>Highlights</title><p><list list-type="simple"><list-item id="u0010"><label>•</label><p>Overall prevalence of <italic>Echinococcus multilocularis</italic> in rodents is low in Sweden.</p></list-item><list-item id="u0015"><label>•</label><p>The distribution of infected rodents was focalized.</p></list-item><list-item id="u0020"><label>•</label><p>Absence of competent intermediate hosts may limit parasite occurrence.</p></list-item><list-item id="u0025"><label>•</label><p><italic>Arvicola amphibius</italic> and <italic>Microtus agrestis</italic> are confirmed intermediate hosts in Sweden.</p></list-item></list></p></abstract><kwd-group><title>Keywords</title><kwd><italic>Echinococcus multilocularis</italic></kwd><kwd><italic>Arvicola amphibius</italic></kwd><kwd><italic>Microtus agrestis</italic></kwd><kwd>Intermediate host</kwd><kwd>Sweden</kwd><kwd>Rodent</kwd></kwd-group></article-meta></front><body><sec id="sec1"><label>1</label><title>Introduction</title><p><italic>Echinococcus multilocularis</italic> is a tapeworm with a sylvatic lifecycle between canids and rodents. In humans, <italic>E. multilocularis</italic> causes alveolar echinococcosis, which is a highly fatal disease without treatment (<xref rid="bib26" ref-type="bibr">Torgerson et al., 2008</xref>). The known geographic range of <italic>E. multilocularis</italic> has been expanding from its high endemic areas in central Europe in recent decades, and it is now considered an emerging disease throughout Europe (<xref rid="bib23" ref-type="bibr">Romig et al., 2006</xref>, <xref rid="bib25" ref-type="bibr">Torgerson et al., 2010</xref>). To better understand risk for human exposure, there is an increased need for understanding of the transmission dynamics of this parasite in the wild. This is particularly true in areas, such as Sweden, where the parasite has only recently been detected in red foxes (<italic>Vulpes vulpes</italic>) (<xref rid="bib19" ref-type="bibr">Osterman Lind et al., 2011</xref>).</p><p>Although host species vary throughout the parasite's range globally, suitable intermediate hosts in Europe are rodent species mainly within the subfamily <italic>Arvicolinae</italic> (<xref rid="bib4" ref-type="bibr">Eckert and Deplazes, 2004</xref>). The importance of a particular rodent species as an intermediate host for <italic>E. multilocularis</italic> transmission is dependent on such physiological and ecological factors as species susceptibility, species abundance, and predator preferences (<xref rid="bib6" ref-type="bibr">Giraudoux et al., 2003</xref>). In central Europe, the common vole (<italic>Microtus arvalis</italic>) and the water vole (<italic>Arvicola terrestris</italic>) are considered the most important intermediate hosts with the bank vole (<italic>Myodes glareolus</italic>) of lesser importance (<xref rid="bib24" ref-type="bibr">Stieger et al., 2002</xref>, <xref rid="bib23" ref-type="bibr">Romig et al., 2006</xref>). In high endemic areas in Switzerland, prevalence in <italic>A. terrestris</italic> has been reported up to 39% (11/28 voles examined) and 23% (12/52 voles examined) in <italic>M. arvalis</italic> (<xref rid="bib7" ref-type="bibr">Gottstein et al., 2001</xref>). Both <italic>M. arvalis</italic> and <italic>A. terrestris</italic> are important prey items of the red fox, the most common definitive host for <italic>E. multilocularis</italic> in central Europe. During cyclic peaks of <italic>A. terrestris</italic> in France, the red fox may feed almost exclusively on this species (<xref rid="bib30" ref-type="bibr">Viel et al., 1999</xref>). Although a generalist predator, some studies have also shown that the red fox prefers to feed on <italic>Microtus</italic> spp. even in areas of low <italic>Microtus</italic> spp. densities (<xref rid="bib9" ref-type="bibr">Guislain et al., 2008</xref>, <xref rid="bib21" ref-type="bibr">Raoul et al., 2010</xref>). In contrast to <italic>M. arvalis</italic> and <italic>A. terrestris</italic>, <italic>M. glareolus</italic> is not heavily preyed upon by foxes (<xref rid="bib3" ref-type="bibr">Dell'Arte et al., 2007</xref>, <xref rid="bib21" ref-type="bibr">Raoul et al., 2010</xref>) and prevalence of <italic>E. multilocularis</italic> in <italic>M. glareolus</italic> is usually low even in high endemic areas (<xref rid="bib24" ref-type="bibr">Stieger et al., 2002</xref>, <xref rid="bib10" ref-type="bibr">Hanosset et al., 2008</xref>).</p><p><italic>E. multilocularis</italic> was first identified in Sweden in a red fox shot December 2010 in the municipality of Uddevalla (<xref rid="bib19" ref-type="bibr">Osterman Lind et al., 2011</xref>) (<xref rid="fig1" ref-type="fig">Fig. 1</xref>). Increased nationwide monitoring during 2011 identified three infected areas in Sweden, and prevalence in foxes on a country level was estimated to be approximately 0.1% (<xref rid="bib31" ref-type="bibr">Wahlstrom et al., 2012</xref>) (<xref rid="fig1" ref-type="fig">Fig. 1</xref>). This low prevalence has remained and is intriguing as in large parts of Sweden conditions for the existence of the parasite are considered to be favorable. These conditions include presence of the red fox and a cool, moist environment ideal for survival of tapeworm eggs (<xref rid="bib29" ref-type="bibr">Veit et al., 1995</xref>, <xref rid="bib4" ref-type="bibr">Eckert and Deplazes, 2004</xref>). Nevertheless, the absence of Europe's most important intermediate hosts could be a limiting factor for the presence of the parasite in the Swedish environment. The common vole (<italic>M. arvalis</italic>) does not exist in Sweden (<xref rid="bib32" ref-type="bibr">Wilson and Reeder, 2005</xref>). Furthermore, <italic>A. terrestris</italic> has recently been recognized as two species, <italic>Arvicola scherman</italic> and <italic>Arvicola amphibius</italic> (<xref rid="bib32" ref-type="bibr">Wilson and Reeder, 2005</xref>). Of the two, only <italic>A. amphibius</italic> exists in Sweden (<xref rid="bib32" ref-type="bibr">Wilson and Reeder, 2005</xref>). In the absence of <italic>M. arvalis</italic> and <italic>A. scherman</italic>, the intermediate hosts most likely to maintain the <italic>E. multilocularis</italic> lifecycle in Sweden are <italic>A. amphibius</italic>, <italic>Microtus agrestis</italic> and <italic>M. glareolus</italic> (<xref rid="bib31" ref-type="bibr">Wahlstrom et al., 2012</xref>).</p><p>Thus far, there have been no reports of <italic>E. multilocularis</italic> in intermediate hosts in Sweden. Monitoring of rodents around Uddevalla where the parasite was first detected red foxes, included examination of 236 rodents (mostly <italic>A. amphibius</italic>) with no positive findings (<xref rid="bib31" ref-type="bibr">Wahlstrom et al., 2012</xref>). The purpose of this paper is to describe the first findings of <italic>E. multilocularis</italic> in rodents in Sweden and to discuss their importance for transmission of the parasite in the Swedish ecosystem.</p></sec><sec id="sec2"><label>2</label><title>Methods</title><sec id="sec2.1"><label>2.1</label><title>Field methods</title><p>During 2013–2015, rodents were collected from four regions in Sweden (<xref rid="fig1" ref-type="fig">Fig. 1</xref>). Two regions within the municipalities of Uddevalla and Katrineholm were sites where <italic>E. multilocularis</italic> had been identified through national surveillance in foxes in 2011 (<xref rid="bib31" ref-type="bibr">Wahlstrom et al., 2012</xref>). Two additional regions within the municipalities of Vetlanda/Växjö and Gnesta/Nyköping were part of a National Environmental and Wildlife Monitoring and Assessment program (FoMA, <ext-link ext-link-type="uri" xlink:href="http://www.slu.se/en/environment" id="intref0010">http://www.slu.se/en/environment</ext-link>) where seasonal rodent trapping had been occurring since 2012 and where the <italic>E. multilocularis</italic> status in foxes was unknown.</p><p>Trapping occurred during 2013–2015 over a period of 4–6 weeks in both the spring (April–June) and autumn (September–October) seasons. Due to logistical constraint and to focus trapping in an area with high numbers of positives, only the FoMA sites (Vetlanda/Växjö and Gnesta/Nyköping) were trapped spring 2015. Although every effort was made to use the same trap sites each season, environmental changes (e.g. plowing or forestry practices) sometimes necessitated dropping or moving a site for trapping. Fieldwork was performed with ethical permits from the Swedish Environmental Protection Agency (NV-02939-11) and the Swedish Board of Agriculture (A-135-12).</p><sec id="sec2.1.1"><label>2.1.1</label><title>Snap trapping</title><p>Small rodent trapping was performed within an approximately 20 × 20 km square region. Snap trapping design was based on the small quadrat method described in <xref rid="bib18" ref-type="bibr">Myllymäki et al. (1971)</xref>. Briefly, a snap trap site consisted of two to four 15 × 15 m small quadrats placed at least 50 m apart from each other. At the corner of each small quadrat a marking stick was placed and three snap traps (Etutuote Ky, Vaasa, Finland) were laid in the best microhabitat as possible within an approximately 1 m<sup>2</sup> area. Traps were baited with hempseed sandwiched between two pieces of beeswax.</p><p>The study regions of Uddevalla and Katrineholm were divided into 10–11 4 × 4 km areas that encompassed both forest and field habitats. These areas were designed to simulate a fox territorial home range (<xref rid="bib28" ref-type="bibr">von Schantz, 1981</xref>) with the idea that rodents captured within these areas would be a reflection of prey availability for one fox. Each 4 × 4 km area contained one to two snap trap sites. In contrast, snap trap sites in the Växjö and Gnesta/Nyköping study regions were set at points previously designated by the wildlife monitoring (FoMA) design. In all study regions, every attempt was made to set snap trap sites along ecotone borders with the purpose to maximize catches of the bank vole (<italic>M. glareolus</italic>), the field vole (<italic>M. agrestis</italic>), the wood mouse (<italic>Apodemus sylvaticus</italic>) and the yellow-necked mouse (<italic>Apodemus flavicollis)</italic> (Mouse species are hereafter referred to as <italic>Apodemus</italic> spp.). Although <italic>Apodemus</italic> spp. were collected both years, only those from 2014 were examined due to the low likelihood for <italic>Apodemus</italic> spp. to contain <italic>E. multilocularis</italic> lesions (<xref rid="bib24" ref-type="bibr">Stieger et al., 2002</xref>) and logistical constraint. All snap traps were kept open for two nights and checked daily. To increase catches, in autumn 2013, some snap trap sites were kept open up to seven nights.</p></sec><sec id="sec2.1.2"><label>2.1.2</label><title>Topcat trapping</title><p>Water vole (<italic>A. amphibius</italic>) fields were defined as fields that contained water vole signs (i.e. tunnels and tumuli). If possible, at least one water vole field was located near the snap trap sites described in Section <xref rid="sec2.1.1" ref-type="sec">2.1.1</xref>. <italic>A. amphibius</italic> in all study areas were captured using topcat traps (Andermatt Biocontrol AG, Grossdietwil, Switzerland). These traps may also capture burrowing <italic>M. agrestis</italic>. Topcat traps were kept open a minimum of 2 h but not more than 30 h.</p></sec></sec><sec id="sec2.2"><label>2.2</label><title>Laboratory methods</title><sec id="sec2.2.1"><label>2.2.1</label><title>Dissection methods and parasite lesion identification</title><p>Rodent specimens were frozen in the field at −20 °C. At dissection information collected included species identification, weight, morphometric measurements, and breeding status. Rodents missing a liver (due to scavenging in the field) were excluded from the analysis. Upon dissection, each rodent liver was examined macroscopically for suspect parasite lesions. In most cases, the lesion was taken in its entirety. However, if parasite lesions >6 mm in diameter were present, only small pieces (weighing up to 10 mg) of the lesions were collected. If the liver contained more than three parasite lesions of similar morphology, only three were excised. From all collected lesions, DNA was extracted using the QIAamp<sup>®</sup> DNA mini kit (Qiagen, Sollentuna, Sweden). Parasite species were then identified using PCR with primers specific for <italic>E. multilocularis</italic>, <italic>Echinococcus granulosus</italic>, and <italic>Taenia</italic> spp. targeting the mitochondrial gene of 12S rRNA (<xref rid="bib24" ref-type="bibr">Stieger et al., 2002</xref>) or the NADH dehydrogenase subunit 1 (<xref rid="bib27" ref-type="bibr">Trachsel et al., 2007</xref>). All negative results from the multiplex PCR (<xref rid="bib27" ref-type="bibr">Trachsel et al., 2007</xref>) were tested using a PCR specific for <italic>E. multilocularis</italic> (<xref rid="bib24" ref-type="bibr">Stieger et al., 2002</xref>). Observed bands from either PCR method were purified using the Illustra ExoProStar 1-step kit (VWR International, Stockholm, Sweden) or, in cases where two bands were present, with the QIAquick<sup>®</sup> Gel Extraction Kit (Qiagen, Sollentuna, Sweden) and sent for sequencing (Macrogen, Amsterdam, The Netherlands). Sequence results were analyzed using the software CLC Main Workbench (CLC Bio, v5.6.1) and submitted for nucleotide BLAST search through the NCBI database. Sequences with ≥95% quality cover and identity were considered to be positive for <italic>E. multilocularis</italic>. Percentages of rodents positive for <italic>E. multilocularis</italic> are presented with 95% confidence intervals (95% CI) based on binomial exact calculations performed in R (i386, v 3.2.2).</p></sec><sec id="sec2.2.2"><label>2.2.2</label><title>Protoscolex identification and preparation of histologic sections</title><p>Protoscoleces were identified in parasite lesions >6 mm in diameter by examining fluid from freshly cut parasite vesicles by light microscopy, by histologic examination of tissue sections, or by a combination of both methods. For histology, pieces of thawed <italic>E. multilocularis</italic> parasite lesions >6 mm in diameter were fixed in 10% formalin, routinely processed and embedded in paraffin. Four μm thick sections were cut and stained with hematoxylin and eosin (H&E) and periodic acid-Schiff (PAS).</p></sec></sec></sec><sec id="sec3"><label>3</label><title>Results</title><sec id="sec3.1"><label>3.1</label><title>Field and laboratory results</title><p>Over the five trapping seasons in 2013–2015, 1702 rodents were collected. Of these, 1566 were examined for <italic>E. multilocularis</italic> (<xref rid="tbl1" ref-type="table">Table 1</xref>). One of 187 (0.5%, 95%CI 0–2.9%) <italic>M. agrestis</italic> and 8/439 (1.8%, 95% CI 0.8–3.6%) <italic>A. amphibius</italic> were positive for <italic>E. multilocularis</italic> (<xref rid="tbl1" ref-type="table">Table 1</xref>, <xref rid="tbl2" ref-type="table">Table 2</xref>). All 655 <italic>M. glareolus</italic> (0%, 95%CI 0–0.6%) and 285 <italic>Apodemus</italic> spp. (0%, 95%CI 0–1.3%) were negative (<xref rid="tbl1" ref-type="table">Table 1</xref>, <xref rid="tbl2" ref-type="table">Table 2</xref>).</p><p>Most (6/9) positive voles (five <italic>A. amphibius</italic>, one <italic>M. agrestis</italic>) were captured in the Gnesta/Nyköping region during the spring seasons of 2013–2015 (<xref rid="tbl2" ref-type="table">Table 2</xref>). These six positive voles were caught within the same water vole field. During 2013–2014 the proportion of voles positive for <italic>E. multilocularis</italic> in this field was 3/10 (30%, 95%CI 6.7–65.2%) for <italic>A. amphibius</italic> and 1/17 (5.9%, 0.1–28.7%) for <italic>M. agrestis</italic>. In 2015, the proportion of <italic>A. amphibius</italic> positive for <italic>E. multilocularis</italic> collected in this field was 2/43 (4.7%, 0.6–15.8%) and for <italic>M. agrestis</italic> 0/1 (0%, 95%CI 0–97.5%).</p></sec><sec id="sec3.2"><label>3.2</label><title>Macroscopic and histologic parasite description of metacestode lesions</title><p>Three of the nine positive rodent livers (three <italic>A. amphibius</italic>) contained metacestode lesions of ≤3 mm in diameter. The six remaining positive rodents contained livers with one or multiple metacestode lesions that in some cases invaded half of the normal liver tissue (<xref rid="fig2" ref-type="fig">Fig. 2</xref>). Four of these six rodent livers (one <italic>M. agrestis</italic>, three <italic>A. amphibius</italic>) contained protoscoleces. The protoscoleces were present in soft, fluid filled vesicles (<xref rid="fig2" ref-type="fig">Fig. 2</xref>, A and C). Of the remaining two positive rodent livers, one <italic>A. amphibius</italic> liver contained multiple hard metacestode lesions with no fluid and no protoscoleces (<xref rid="fig2" ref-type="fig">Fig. 2</xref>, B). One <italic>A. amphibius</italic> liver contained two metacestode lesions ≤6 mm in diameter, and one metacestode lesion >6 mm in diameter with no fluid and with no protoscoleces (<xref rid="fig2" ref-type="fig">Fig. 2</xref>, D).</p><p>In liver sections from four rodents (one <italic>M. agrestis</italic>, three <italic>A. amphibius</italic>) large cyst-like vesicles outlined by an eosinophilic homogenous to laminated PAS-positive wall were present (<xref rid="fig3" ref-type="fig">Fig. 3</xref>, A–D). Multifocal remnants of a germinative epithelium were detected along vesicle walls in some sections. Basophilic ovals, consistent with calcareous corpuscles, and varying numbers of protoscoleces were detected within vesicular lumina in sections from all four animals. Protoscoleces were sometimes grouped in brood capsules with individual protoscoleces measuring approximately 80–180 μm in cross section (<xref rid="fig3" ref-type="fig">Fig. 3</xref>, B). Rostrellar hooks were often identified (<xref rid="fig3" ref-type="fig">Fig. 3</xref>, E). Lesions were surrounded by a fibrous capsule and varying amount of inflammatory cells, including granulocytes, lymphocytes, plasma cells, macrophages and multinucleated giant cells.</p><p>Smaller vesicular lesions with empty lumina were seen in sections from the remaining two water voles and in some sections from the voles with protoscolex-containing vesicles. These smaller lesions were typically surrounded by a severe granulocytic inflammatory reaction, fibrosis and areas of necrosis (<xref rid="fig3" ref-type="fig">Fig. 3</xref>, F).</p></sec></sec><sec id="sec4"><label>4</label><title>Discussion</title><p>These findings are the first records of <italic>E. multilocularis</italic> in rodent intermediate hosts in Sweden. Importantly, nearly all (6/9) positive rodents were captured in one field from an area previously unknown to have the parasite. The morphologic and histologic observations described here are consistent with descriptions of <italic>E. multilocularis</italic> lesions in rodent species from previous studies (<xref rid="bib14" ref-type="bibr">Houin et al., 1982</xref>, <xref rid="bib1" ref-type="bibr">Barabási et al., 2011</xref>, <xref rid="bib15" ref-type="bibr">Liccioli et al., 2013</xref>). The identification of protoscoleces in <italic>M. agrestis</italic> (1/1) and <italic>A. amphibius</italic> (3/8) show that these rodent species are competent intermediate hosts for <italic>E. multilocularis</italic> in Sweden.</p><p>Although prevalence in <italic>M. glareolus</italic> has been reported as high as 10.3% (6/58) (<xref rid="bib22" ref-type="bibr">Reperant et al., 2009</xref>), prevalence in central Europe has generally been low with reports by <xref rid="bib10" ref-type="bibr">Hanosset et al. (2008)</xref> of 4.3% (1/23) and by <xref rid="bib24" ref-type="bibr">Stieger et al. (2002)</xref> of 2.4% (2/83). Experimentally, <italic>M. glareolus</italic> has also shown a limited capacity for infection with <5% animals developing cysts two months after inoculation (<xref rid="bib33" ref-type="bibr">Woolsey, 2015</xref>). Reports of infected wild <italic>Apodemus</italic> spp. are very few and are often limited to single reports, such as the infection of one <italic>Apodemus agrarius</italic> in Romania (<xref rid="bib1" ref-type="bibr">Barabási et al., 2011</xref>). Even in a high endemic area of Switzerland, the prevalence of <italic>E. multilocularis</italic> in <italic>Apodemus</italic> spp. was 0% (0/154) (<xref rid="bib24" ref-type="bibr">Stieger et al., 2002</xref>). In a low endemic area, such as Sweden, the probability to find infected <italic>M. glareolus</italic> and <italic>Apodemus</italic> spp. would likely be low. Therefore, the negative findings in all of the <italic>M. glareolus</italic> and <italic>Apodemus</italic> spp. in this study were not unexpected.</p><p>The significance of <italic>M. glareolus</italic> and <italic>Apodemus</italic> spp. to the transmission of <italic>E. multilocularis</italic> depends not only on susceptibility to infection but also rates of fox predation. According to a fox fecal analysis performed in central Sweden, fox predation on <italic>M. glareolus</italic> was almost half that of <italic>M. agrestis</italic> (<xref rid="bib16" ref-type="bibr">Lindström, 1982</xref>). In addition, the presence of <italic>Apodemus</italic> spp. in a fox fecal analysis in southern Sweden was negligible (<xref rid="bib5" ref-type="bibr">Erlinge et al., 1983</xref>). This, together with our negative findings in these species, suggest that <italic>M. glareolus</italic> and <italic>Apodemus</italic> spp. are of no importance for <italic>E. multilocularis</italic> transmission in the Swedish environment.</p><p>The majority of our positive findings were identified in the water vole, <italic>A. amphibius</italic>. Due to reclassification of species within the <italic>Arvicola</italic> genus, many studies on <italic>E. multilocularis</italic> report all examined water voles as <italic>A. terrestris</italic>. However, <italic>A. terrestris</italic> has been separated into two species, <italic>A. scherman</italic> and <italic>A. amphibius</italic> (<xref rid="bib32" ref-type="bibr">Wilson and Reeder, 2005</xref>). <italic>A. scherman</italic> is mainly a fossorial vole with a range limited to central Europe (<xref rid="bib32" ref-type="bibr">Wilson and Reeder, 2005</xref>, <xref rid="bib20" ref-type="bibr">Piras et al., 2012</xref>). Investigations in France suggest that population peaks of the fossorial form (<italic>A. scherman</italic>) induce prey specialization by foxes and thereby increase the prevalence of the parasite in the fox (<xref rid="bib30" ref-type="bibr">Viel et al., 1999</xref>, <xref rid="bib6" ref-type="bibr">Giraudoux et al., 2003</xref>). In contrast, <italic>A. amphibius</italic> is a semi-aquatic vole with a much wider distribution which also includes Sweden (<xref rid="bib32" ref-type="bibr">Wilson and Reeder, 2005</xref>, <xref rid="bib20" ref-type="bibr">Piras et al., 2012</xref>). It is unclear if the same prey specialization occurs with <italic>A. amphibius</italic>, a vole of differing ecology (<xref rid="bib20" ref-type="bibr">Piras et al., 2012</xref>).</p><p>Although prevalence in <italic>Arvicola</italic> spp. has been reported as high as 41–79% in localized areas of Europe (<xref rid="bib2" ref-type="bibr">Burlet et al., 2011</xref>), the potential infectivity of these water voles may be much lower. In a study by <xref rid="bib13" ref-type="bibr">Hofer et al. (2000)</xref> only 2/19 <italic>Arvicola</italic> spp. positive for <italic>E. multilocularis</italic> had protoscoleces (i.e. were infectious to the definitive host). Similar figures were reported by <xref rid="bib22" ref-type="bibr">Reperant et al. (2009)</xref> where 2/31 positive <italic>Arvicola</italic> spp. contained protoscoleces, and <xref rid="bib24" ref-type="bibr">Stieger et al. (2002)</xref> where 26/81 positive <italic>Arvicola</italic> spp. contained protoscoleces. Although the age of the rodent and size of the metacestode lesions may explain some of this variation, it is likely that many of these rodents contained non-infectious metacestode lesions. <xref rid="bib2" ref-type="bibr">Burlet et al. (2011)</xref> demonstrated that <italic>Arvicola</italic> spp. in Switzerland were unlikely to have <italic>E. multilocularis</italic> lesions containing mature protoscoleces until the rodents were at least three months of age. Furthermore, only metacestode lesions >3 mm in diameter contained protoscoleces (<xref rid="bib2" ref-type="bibr">Burlet et al., 2011</xref>). In our study, 3/8 positive <italic>A. amphibius</italic> contained infectious metacestode lesions. Of the five rodents with non-infectious metacestode lesions, two met the age and lesion size limitations outlined by <xref rid="bib2" ref-type="bibr">Burlet et al. (2011)</xref>. It is possible that sampling method may have affected outcome in one of these two rodents, as two lesions ≤6 mm in diameter were taken for PCR (<xref rid="fig2" ref-type="fig">Fig. 2</xref>, D). Our findings, particularly with respect to those in Switzerland, suggest a lesser importance for <italic>A. amphibius</italic> in the transmission of <italic>E. multilocularis</italic> in Sweden. To better address this question, there is a need for a laboratory study to investigate the growth and development of <italic>E</italic>. <italic>multilocularis</italic> metacestode lesions in <italic>Arvicola</italic> spp. In addition, the extent to which Swedish foxes prey on <italic>A. amphibius</italic> needs to be determined.</p><p>While few studies of rodent intermediate hosts differentiate between <italic>Microtus</italic> spp., in those that do, <italic>M. arvalis</italic> seems to be more common. For instance, <xref rid="bib10" ref-type="bibr">Hanosset et al. (2008)</xref> reports a capture of 914 <italic>M. arvalis</italic> and only 39 <italic>M. agrestis</italic>. These results may reflect interspecific competition in areas where both species coexist, and where it is known that <italic>M. arvalis</italic> outcompete <italic>M. agrestis</italic> for grassland/open field habitats (<xref rid="bib17" ref-type="bibr">Myllymäki, 1977</xref>). These habitats can be associated with high levels of fox fecal egg contamination if infected foxes are attracted to prey on abundant grassland rodents (<xref rid="bib30" ref-type="bibr">Viel et al., 1999</xref>, <xref rid="bib6" ref-type="bibr">Giraudoux et al., 2003</xref>). Because <italic>M. arvalis</italic> does not exist in Sweden, <italic>M agrestis</italic> inhabits the open fields and grassland habitat in southern Sweden where <italic>E. multilocularis</italic> is found (<xref rid="bib12" ref-type="bibr">Hansson, 1971</xref>, <xref rid="bib31" ref-type="bibr">Wahlstrom et al., 2012</xref>). Our findings show that <italic>M. agrestis</italic> can contribute to parasite transmission. It is possible that <italic>M. agrestis</italic> could fulfill the role that <italic>M. arvalis</italic> has as a major intermediate host in central Europe. However, we can make no conclusion about this with only one positive finding.</p><p>Recent laboratory studies (<xref rid="bib34" ref-type="bibr">Woolsey et al., 2015a</xref>, <xref rid="bib35" ref-type="bibr">Woolsey et al., 2015b</xref>) have demonstrated susceptibility of both <italic>M. agrestis</italic> and <italic>M. arvalis</italic> to <italic>E. multilocularis</italic>. Following infection with parasite eggs, metacestode development differed with <italic>M. arvalis</italic> creating larger and more numerous metacestode lesions than <italic>M. agrestis</italic> at the same age time point (<xref rid="bib35" ref-type="bibr">Woolsey et al., 2015b</xref>). Although protoscolex production was not examined in <italic>M. agrestis</italic>, <xref rid="bib35" ref-type="bibr">Woolsey et al. (2015b)</xref> speculates that the smaller metacestode lesion size (as compared to <italic>M. arvalis</italic>) would reduce the potential for protoscolex production and limit the transmission potential of <italic>M. agrestis</italic>. Such a limitation could be of massive importance in environments such as in Sweden where <italic>M. arvalis</italic> is absent. Indeed, at one of the southernmost border of the <italic>E. multilocularis</italic> range in the Ticino canton of Switzerland, <xref rid="bib8" ref-type="bibr">Guerra et al. (2014)</xref> observed an overlap between the presence of <italic>M. arvalis</italic> and <italic>E. multilocularis</italic>. These authors noted that the occurrence of <italic>E. multilocularis</italic> infected foxes was limited to the range of <italic>M. arvalis</italic>—despite the presence of other <italic>Microtus</italic> spp. (albeit not <italic>M. agrestis</italic>).</p><p>The presence of 6/9 positive rodents in the same field further demonstrates the heterogeneous spatial distribution of <italic>E. multilocularis</italic> (<xref rid="bib11" ref-type="bibr">Hansen et al., 2004</xref>) and the potential for prevalence in rodent populations in small areas to be quite high (<xref rid="bib7" ref-type="bibr">Gottstein et al., 2001</xref>, <xref rid="bib2" ref-type="bibr">Burlet et al., 2011</xref>). The local prevalence of 30% (95%CI 6.7–65.2%) found in <italic>A. amphibius</italic> reflects an area with an aggregation of <italic>E. multilocularis</italic> eggs from fox feces during 2013–2014 that may also reflect a particular risk for human exposure (Miller et al., unpublished). Although the sample size for 2013–2014 was low (n = 10), repeated sampling in 2015 (n = 43, <italic>A. amphibius</italic>) demonstrated the continued presence of <italic>E. multilocularis</italic> in this field (4.7%, 95%CI 0.6–15.8%). While the fox prevalence in Sweden is presumed to be very low (≤1%) on a nationwide level, these findings indicate that local contamination of <italic>E. multilocularis</italic> eggs in the Swedish environment will vary.</p></sec><sec id="sec5"><label>5</label><title>Conclusions</title><p>Our findings of infected <italic>A. amphibius</italic> and <italic>M. agrestis</italic> with protoscoleces show that these rodents can act as suitable intermediate hosts for <italic>E. multilocularis</italic> in Sweden. The identification of these intermediate hosts increases the knowledge about the lifecycle of the parasite in Sweden and thereby the possibilities in the future to predict areas where a higher prevalence of <italic>E. multilocularis</italic> could be expected.</p></sec></body><back><ref-list><title>References</title><ref id="bib1"><element-citation publication-type="journal" id="sref1"><person-group person-group-type="author"><name><surname>Barabási</surname><given-names>S.S.</given-names></name><name><surname>Marosfői</surname><given-names>L.</given-names></name><name><surname>Barabási</surname><given-names>Z.S.</given-names></name><name><surname>Cozma</surname><given-names>V.</given-names></name></person-group><article-title>Natural alveolar echinococcosis with <italic>Echinococcus multilocularis</italic> in wild rodents</article-title><source>Sci. Parasitol.</source><volume>12</volume><year>2011</year><fpage>11</fpage><lpage>21</lpage></element-citation></ref><ref id="bib2"><element-citation publication-type="journal" id="sref2"><person-group person-group-type="author"><name><surname>Burlet</surname><given-names>P.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name><name><surname>Hegglin</surname><given-names>D.</given-names></name></person-group><article-title>Age, season and spatio-temporal factors affecting the prevalence of <italic>Echinococcus multilocularis</italic> and <italic>Taenia taeniaeformis</italic> in <italic>Arvicola terrestris</italic></article-title><source>Parasit. Vectors</source><volume>4</volume><year>2011</year><fpage>6</fpage><pub-id pub-id-type="pmid">21247427</pub-id></element-citation></ref><ref id="bib3"><element-citation publication-type="journal" id="sref3"><person-group person-group-type="author"><name><surname>Dell'Arte</surname><given-names>G.L.</given-names></name><name><surname>Laaksonen</surname><given-names>T.</given-names></name><name><surname>Norrdahl</surname><given-names>K.</given-names></name><name><surname>Korpimäki</surname><given-names>E.</given-names></name></person-group><article-title>Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey</article-title><source>Acta Oecol.</source><volume>31</volume><year>2007</year><fpage>276</fpage><lpage>281</lpage></element-citation></ref><ref id="bib4"><element-citation publication-type="journal" id="sref4"><person-group person-group-type="author"><name><surname>Eckert</surname><given-names>J.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name></person-group><article-title>Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern</article-title><source>Clin. Microbiol. Rev.</source><volume>17</volume><year>2004</year><fpage>107</fpage><lpage>135</lpage><pub-id pub-id-type="pmid">14726458</pub-id></element-citation></ref><ref id="bib5"><element-citation publication-type="journal" id="sref5"><person-group person-group-type="author"><name><surname>Erlinge</surname><given-names>S.</given-names></name><name><surname>Göransson</surname><given-names>G.</given-names></name><name><surname>Hansson</surname><given-names>L.</given-names></name><name><surname>Högstedt</surname><given-names>G.</given-names></name><name><surname>Liberg</surname><given-names>O.</given-names></name><name><surname>Nilsson</surname><given-names>I.N.</given-names></name><name><surname>Nilsson</surname><given-names>T.</given-names></name><name><surname>von Schantz</surname><given-names>T.</given-names></name><name><surname>Sylvén</surname><given-names>M.</given-names></name></person-group><article-title>Predation as a regulating factor on small rodent populations in southern Sweden</article-title><source>Oikos</source><volume>40</volume><year>1983</year><fpage>36</fpage><lpage>52</lpage></element-citation></ref><ref id="bib6"><element-citation publication-type="journal" id="sref6"><person-group person-group-type="author"><name><surname>Giraudoux</surname><given-names>P.</given-names></name><name><surname>Craig</surname><given-names>P.S.</given-names></name><name><surname>Delattre</surname><given-names>P.</given-names></name><name><surname>Bao</surname><given-names>G.</given-names></name><name><surname>Bartholomot</surname><given-names>B.</given-names></name><name><surname>Harraga</surname><given-names>S.</given-names></name><name><surname>Quéré</surname><given-names>J.-P.</given-names></name><name><surname>Raoul</surname><given-names>F.</given-names></name><name><surname>Wang</surname><given-names>Y.</given-names></name><name><surname>Shi</surname><given-names>D.</given-names></name><name><surname>Vuitton</surname><given-names>D.-A.</given-names></name></person-group><article-title>Interactions between landscape changes and host communities can regulate <italic>Echinococcus multilocularis</italic> transmission</article-title><source>Parasitology</source><volume>127</volume><year>2003</year><fpage>S121</fpage><lpage>S131</lpage><pub-id pub-id-type="pmid">15027609</pub-id></element-citation></ref><ref id="bib7"><element-citation publication-type="journal" id="sref7"><person-group person-group-type="author"><name><surname>Gottstein</surname><given-names>B.</given-names></name><name><surname>Saucy</surname><given-names>F.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name><name><surname>Reichen</surname><given-names>J.</given-names></name><name><surname>Demierre</surname><given-names>G.</given-names></name><name><surname>Busato</surname><given-names>A.</given-names></name><name><surname>Zuercher</surname><given-names>C.</given-names></name><name><surname>Pugin</surname><given-names>P.</given-names></name></person-group><article-title>Is high prevalence of <italic>Echinococcus multilocularis</italic> in wild and domestic animals associated with disease incidence in humans?</article-title><source>Emerg. Infect. Dis.</source><volume>7</volume><year>2001</year><fpage>408</fpage><lpage>412</lpage><pub-id pub-id-type="pmid">11384517</pub-id></element-citation></ref><ref id="bib8"><element-citation publication-type="journal" id="sref8"><person-group person-group-type="author"><name><surname>Guerra</surname><given-names>D.</given-names></name><name><surname>Hegglin</surname><given-names>D.</given-names></name><name><surname>Bacciarini</surname><given-names>L.</given-names></name><name><surname>Schnyder</surname><given-names>M.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name></person-group><article-title>Stability of the southern European border of <italic>Echinococcus multilocularis</italic> in the Alps: evidence that <italic>Microtus arvalis</italic> is a limiting factor</article-title><source>Parasitology</source><volume>141</volume><year>2014</year><fpage>1593</fpage><lpage>1602</lpage></element-citation></ref><ref id="bib9"><element-citation publication-type="journal" id="sref9"><person-group person-group-type="author"><name><surname>Guislain</surname><given-names>M.-H.</given-names></name><name><surname>Raoul</surname><given-names>F.</given-names></name><name><surname>Giraudoux</surname><given-names>P.</given-names></name><name><surname>Terrier</surname><given-names>M.-E.</given-names></name><name><surname>Froment</surname><given-names>G.</given-names></name><name><surname>Ferté</surname><given-names>H.</given-names></name><name><surname>Poulle</surname><given-names>M.-L.</given-names></name></person-group><article-title>Ecological and biological factors involved in the transmission of <italic>Echinococcus multilocularis</italic> in the French Ardennes</article-title><source>J. Helminthol.</source><volume>82</volume><year>2008</year><fpage>143</fpage><lpage>151</lpage><pub-id pub-id-type="pmid">18394209</pub-id></element-citation></ref><ref id="bib10"><element-citation publication-type="journal" id="sref10"><person-group person-group-type="author"><name><surname>Hanosset</surname><given-names>R.</given-names></name><name><surname>Saegerman</surname><given-names>C.</given-names></name><name><surname>Adant</surname><given-names>S.</given-names></name><name><surname>Massart</surname><given-names>L.</given-names></name><name><surname>Losson</surname><given-names>B.</given-names></name></person-group><article-title><italic>Echinococcus multilocularis</italic> in Belgium: prevalence in red foxes (<italic>Vulpes vulpes</italic>) and in different species of potential intermediate hosts</article-title><source>Vet. Parasitol.</source><volume>151</volume><year>2008</year><fpage>212</fpage><lpage>217</lpage><pub-id pub-id-type="pmid">18164551</pub-id></element-citation></ref><ref id="bib11"><element-citation publication-type="journal" id="sref11"><person-group person-group-type="author"><name><surname>Hansen</surname><given-names>F.</given-names></name><name><surname>Jeltsch</surname><given-names>F.</given-names></name><name><surname>Tackmann</surname><given-names>K.</given-names></name><name><surname>Staubach</surname><given-names>C.</given-names></name><name><surname>Thulke</surname><given-names>H.H.</given-names></name></person-group><article-title>Processes leading to a spatial aggregation of <italic>Echinococcus multilocularis</italic> in its natural intermediate host <italic>Microtus arvalis</italic></article-title><source>Int. J. Parasitol.</source><volume>34</volume><year>2004</year><fpage>37</fpage><lpage>44</lpage><pub-id pub-id-type="pmid">14711588</pub-id></element-citation></ref><ref id="bib12"><element-citation publication-type="journal" id="sref12"><person-group person-group-type="author"><name><surname>Hansson</surname><given-names>L.</given-names></name></person-group><article-title>Habitat, food and population dynamics of the field vole <italic>Microtus agrestis</italic> (L.) in south Sweden</article-title><source>Viltrevy</source><volume>8</volume><year>1971</year><fpage>267</fpage><lpage>378</lpage></element-citation></ref><ref id="bib13"><element-citation publication-type="journal" id="sref13"><person-group person-group-type="author"><name><surname>Hofer</surname><given-names>S.</given-names></name><name><surname>Gloor</surname><given-names>S.</given-names></name><name><surname>Müller</surname><given-names>U.</given-names></name><name><surname>Mathis</surname><given-names>A.</given-names></name><name><surname>Hegglin</surname><given-names>D.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name></person-group><article-title>High prevalence of Echinococcus multilocularis in urban red foxes (<italic>Vulpes vulpes</italic>) and voles (<italic>Arvicola terrestris</italic>) in the city of Zürich</article-title><source>Switz. Parasitol.</source><volume>120</volume><year>2000</year><fpage>135</fpage><lpage>142</lpage></element-citation></ref><ref id="bib14"><element-citation publication-type="journal" id="sref14"><person-group person-group-type="author"><name><surname>Houin</surname><given-names>R.</given-names></name><name><surname>Deniau</surname><given-names>M.</given-names></name><name><surname>Liance</surname><given-names>M.</given-names></name><name><surname>Puel</surname><given-names>F.</given-names></name></person-group><article-title><italic>Arvicola terrestris</italic> an intermediate host of <italic>Echinococcus multilocularis</italic> in France: epidemiological consequences</article-title><source>Int. J. Parasitol.</source><volume>12</volume><year>1982</year><fpage>593</fpage><lpage>600</lpage><pub-id pub-id-type="pmid">6761290</pub-id></element-citation></ref><ref id="bib15"><element-citation publication-type="journal" id="sref15"><person-group person-group-type="author"><name><surname>Liccioli</surname><given-names>S.</given-names></name><name><surname>Duignan</surname><given-names>P.J.</given-names></name><name><surname>Lejeune</surname><given-names>M.</given-names></name><name><surname>Deunk</surname><given-names>J.</given-names></name><name><surname>Majid</surname><given-names>S.</given-names></name><name><surname>Massolo</surname><given-names>A.</given-names></name></person-group><article-title>A new intermediate host for <italic>Echinococcus multilocularis</italic>: the southern red-backed vole (<italic>Myodes gapperi</italic>) in urban landscape in Calgary, Canada</article-title><source>Parasitol. Int.</source><volume>62</volume><year>2013</year><fpage>355</fpage><lpage>357</lpage><pub-id pub-id-type="pmid">23608104</pub-id></element-citation></ref><ref id="bib16"><element-citation publication-type="book" id="sref16"><person-group person-group-type="author"><name><surname>Lindström</surname><given-names>E.</given-names></name></person-group><chapter-title>Population Ecology of the Red Fox (<italic>Vulpes Vuples</italic> L.) in Relation to Food Supply</chapter-title><comment>PhD Thesis</comment><year>1982</year><publisher-name>Department of Zoology, University of Stockholm</publisher-name><publisher-loc>Stockholm, Sweden</publisher-loc><fpage>154</fpage></element-citation></ref><ref id="bib17"><element-citation publication-type="journal" id="sref17"><person-group person-group-type="author"><name><surname>Myllymäki</surname><given-names>A.</given-names></name></person-group><article-title>Interactions between the field vole <italic>Microtus agrestis</italic> and its microtine competitors in Central-Scandinavian populations</article-title><source>Oikos</source><volume>29</volume><year>1977</year><fpage>570</fpage><lpage>580</lpage></element-citation></ref><ref id="bib18"><element-citation publication-type="journal" id="sref18"><person-group person-group-type="author"><name><surname>Myllymäki</surname><given-names>A.</given-names></name><name><surname>Paasikallio</surname><given-names>A.</given-names></name><name><surname>Pankakoski</surname><given-names>E.</given-names></name><name><surname>Kanervo</surname><given-names>V.</given-names></name></person-group><article-title>Removal experiments on small quadrats as a means of rapid assessment of the abundance of small mammals</article-title><source>Ann. Zool. Fenn.</source><volume>8</volume><year>1971</year><fpage>177</fpage><lpage>185</lpage></element-citation></ref><ref id="bib19"><mixed-citation publication-type="other" id="oref1">Osterman Lind, E., Juremalm, M., Christensson, D., Widgren, S., Hallgren, G., Ågren, E.O., Uhlhorn, H., Lindberg, A., Cedersmyg, M., Wahlström, H., First detection of <italic>Echinococcus multilocularis</italic> in Sweden, February to March 2011. Euro Surveill. 16 pii19836, available online. <ext-link ext-link-type="uri" xlink:href="http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19836" id="intref0020">http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19836</ext-link></mixed-citation></ref><ref id="bib20"><element-citation publication-type="journal" id="sref20"><person-group person-group-type="author"><name><surname>Piras</surname><given-names>P.</given-names></name><name><surname>Marcolini</surname><given-names>F.</given-names></name><name><surname>Claude</surname><given-names>J.</given-names></name><name><surname>Ventura</surname><given-names>J.</given-names></name><name><surname>Kotsakis</surname><given-names>T.</given-names></name><name><surname>Cubo</surname><given-names>J.</given-names></name></person-group><article-title>Ecological and functional correlates of molar shape variation in European populations of <italic>Arvicola</italic> (Arvicolinae, Rodentia)</article-title><source>Zool. Anz.</source><volume>251</volume><year>2012</year><fpage>335</fpage><lpage>343</lpage></element-citation></ref><ref id="bib21"><element-citation publication-type="journal" id="sref21"><person-group person-group-type="author"><name><surname>Raoul</surname><given-names>F.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name><name><surname>Rieffel</surname><given-names>D.</given-names></name><name><surname>Lambert</surname><given-names>J.-C.</given-names></name><name><surname>Giraudoux</surname><given-names>P.</given-names></name></person-group><article-title>Predator dietary response to prey density variation and consequences for cestode transmission</article-title><source>Oecologia</source><volume>164</volume><year>2010</year><fpage>129</fpage><lpage>139</lpage><pub-id pub-id-type="pmid">20461413</pub-id></element-citation></ref><ref id="bib22"><element-citation publication-type="journal" id="sref22"><person-group person-group-type="author"><name><surname>Reperant</surname><given-names>L.A.</given-names></name><name><surname>Hegglin</surname><given-names>D.</given-names></name><name><surname>Tanner</surname><given-names>I.</given-names></name><name><surname>Fischer</surname><given-names>C.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name></person-group><article-title>Rodents as shared indicators for zoonotic parasites of carnivores in urban environments</article-title><source>Parasitology</source><volume>136</volume><year>2009</year><fpage>329</fpage><lpage>337</lpage><pub-id pub-id-type="pmid">19154652</pub-id></element-citation></ref><ref id="bib23"><element-citation publication-type="journal" id="sref23"><person-group person-group-type="author"><name><surname>Romig</surname><given-names>T.</given-names></name><name><surname>Dinkel</surname><given-names>A.</given-names></name><name><surname>Mackenstedt</surname><given-names>U.</given-names></name></person-group><article-title>The present situation of echinococcosis in Europe</article-title><source>Parasitol. Int.</source><volume>55</volume><year>2006</year><fpage>S187</fpage><lpage>S191</lpage><pub-id pub-id-type="pmid">16352465</pub-id></element-citation></ref><ref id="bib24"><element-citation publication-type="journal" id="sref24"><person-group person-group-type="author"><name><surname>Stieger</surname><given-names>C.</given-names></name><name><surname>Hegglin</surname><given-names>D.</given-names></name><name><surname>Schwarzenbach</surname><given-names>G.</given-names></name><name><surname>Mathis</surname><given-names>A.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name></person-group><article-title>Spatial and temporal aspects of urban transmission of <italic>Echinococcus multilocularis</italic></article-title><source>Parasitology</source><volume>124</volume><year>2002</year><fpage>631</fpage><lpage>640</lpage><pub-id pub-id-type="pmid">12118719</pub-id></element-citation></ref><ref id="bib25"><element-citation publication-type="journal" id="sref25"><person-group person-group-type="author"><name><surname>Torgerson</surname><given-names>P.R.</given-names></name><name><surname>Keller</surname><given-names>K.</given-names></name><name><surname>Magnotta</surname><given-names>M.</given-names></name><name><surname>Ragland</surname><given-names>N.</given-names></name></person-group><article-title>The global burden of alveolar echinococcosis</article-title><source>PLoS Negl. Trop. Dis.</source><volume>4</volume><year>2010</year><fpage>e722</fpage><pub-id pub-id-type="pmid">20582310</pub-id></element-citation></ref><ref id="bib26"><element-citation publication-type="journal" id="sref26"><person-group person-group-type="author"><name><surname>Torgerson</surname><given-names>P.R.</given-names></name><name><surname>Schweiger</surname><given-names>A.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name><name><surname>Pohar</surname><given-names>M.</given-names></name><name><surname>Reichen</surname><given-names>J.</given-names></name><name><surname>Ammann</surname><given-names>R.W.</given-names></name><name><surname>Tarr</surname><given-names>P.E.</given-names></name><name><surname>Halkik</surname><given-names>N.</given-names></name><name><surname>Müllhaupt</surname><given-names>B.</given-names></name></person-group><article-title>Alveolar echinococcosis: from a deadly disease to a well-controlled infection. Relative survival and economic analysis in Switzerland over the last 35 years</article-title><source>J. Hepatol.</source><volume>49</volume><year>2008</year><fpage>72</fpage><lpage>77</lpage><pub-id pub-id-type="pmid">18485517</pub-id></element-citation></ref><ref id="bib27"><element-citation publication-type="journal" id="sref27"><person-group person-group-type="author"><name><surname>Trachsel</surname><given-names>D.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name><name><surname>Mathis</surname><given-names>A.</given-names></name></person-group><article-title>Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA</article-title><source>Parasitology</source><volume>134</volume><year>2007</year><fpage>911</fpage><lpage>920</lpage><pub-id pub-id-type="pmid">17288631</pub-id></element-citation></ref><ref id="bib28"><element-citation publication-type="journal" id="sref28"><person-group person-group-type="author"><name><surname>von Schantz</surname><given-names>T.</given-names></name></person-group><article-title>Female cooperation, male competition, and dispersal in the red fox <italic>Vulpes vulpes</italic></article-title><source>Oikos</source><volume>37</volume><year>1981</year><fpage>63</fpage><lpage>68</lpage></element-citation></ref><ref id="bib29"><element-citation publication-type="journal" id="sref29"><person-group person-group-type="author"><name><surname>Veit</surname><given-names>P.</given-names></name><name><surname>Bilger</surname><given-names>B.</given-names></name><name><surname>Schad</surname><given-names>V.</given-names></name><name><surname>Schäfer</surname><given-names>J.</given-names></name><name><surname>Frank</surname><given-names>W.</given-names></name><name><surname>Lucius</surname><given-names>R.</given-names></name></person-group><article-title>Influence of environmental factors on the infectivity of <italic>Echinococcus multilocularis</italic> eggs</article-title><source>Parasitology</source><volume>110</volume><issue>Pt 1</issue><year>1995</year><fpage>79</fpage><lpage>86</lpage><pub-id pub-id-type="pmid">7845716</pub-id></element-citation></ref><ref id="bib30"><element-citation publication-type="journal" id="sref30"><person-group person-group-type="author"><name><surname>Viel</surname><given-names>J.-F.</given-names></name><name><surname>Giraudoux</surname><given-names>P.</given-names></name><name><surname>Abrial</surname><given-names>V.</given-names></name><name><surname>Bresson-Hadni</surname><given-names>S.</given-names></name></person-group><article-title>Water vole (<italic>Arvicola terrestris scherman</italic>) density as risk factor for human alveolar echinococcosis</article-title><source>Am. J. Trop. Med. Hyg.</source><volume>61</volume><year>1999</year><fpage>559</fpage><lpage>565</lpage><pub-id pub-id-type="pmid">10548289</pub-id></element-citation></ref><ref id="bib31"><element-citation publication-type="journal" id="sref31"><person-group person-group-type="author"><name><surname>Wahlstrom</surname><given-names>H.</given-names></name><name><surname>Lindberg</surname><given-names>A.</given-names></name><name><surname>Lindh</surname><given-names>J.</given-names></name><name><surname>Wallensten</surname><given-names>A.</given-names></name><name><surname>Lindqvist</surname><given-names>R.</given-names></name><name><surname>Plym-Forshell</surname><given-names>L.</given-names></name><name><surname>Osterman Lind</surname><given-names>E.</given-names></name><name><surname>Agren</surname><given-names>E.O.</given-names></name><name><surname>Widgren</surname><given-names>S.</given-names></name><name><surname>Carlsson</surname><given-names>U.</given-names></name><name><surname>Christensson</surname><given-names>D.</given-names></name><name><surname>Cedersmyg</surname><given-names>M.</given-names></name><name><surname>Lindström</surname><given-names>E.</given-names></name><name><surname>Olsson</surname><given-names>G.E.</given-names></name><name><surname>Hörnfeldt</surname><given-names>B.</given-names></name><name><surname>Barragan</surname><given-names>A.</given-names></name><name><surname>Davelid</surname><given-names>C.</given-names></name><name><surname>Hjertqvist</surname><given-names>M.</given-names></name><name><surname>Elvander</surname><given-names>M.</given-names></name></person-group><article-title>Investigations and actions taken during 2011 due to the first finding of <italic>Echinococcus multilocularis</italic> in Sweden</article-title><source>Eurosurveillance</source><volume>17</volume><year>2012</year><comment>pii=20215, available online</comment><ext-link ext-link-type="uri" xlink:href="http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20215" id="intref0025">http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20215</ext-link></element-citation></ref><ref id="bib32"><element-citation publication-type="book" id="sref32"><person-group person-group-type="editor"><name><surname>Wilson</surname><given-names>D.E.</given-names></name><name><surname>Reeder</surname><given-names>D.M.</given-names></name></person-group><source>Mammal Species of the World: a Taxonomic and Geographic Reference</source><edition>third ed.</edition><year>2005</year><publisher-name>Johns Hopkins University Press</publisher-name><publisher-loc>Baltimore, Maryland</publisher-loc><fpage>2142</fpage><comment>Online database from Smithsonian National Museum of Natural History</comment><ext-link ext-link-type="uri" xlink:href="http://vertebrates.si.edu/msw/mswCFApp/msw/index.cfm" id="intref0030">http://vertebrates.si.edu/msw/mswCFApp/msw/index.cfm</ext-link><comment>Accessed Jan. 26, 2016</comment></element-citation></ref><ref id="bib33"><element-citation publication-type="book" id="sref33"><person-group person-group-type="author"><name><surname>Woolsey</surname><given-names>I.D.</given-names></name></person-group><chapter-title>Experimental <italic>Echinococcus multilocularis</italic> Infection in Intermedate Hosts</chapter-title><comment>PhD Thesis</comment><year>2015</year><publisher-name>Faculty of Science, University of Copenhagen</publisher-name><publisher-loc>Copenhagen, Denmark</publisher-loc><fpage>118</fpage></element-citation></ref><ref id="bib34"><element-citation publication-type="journal" id="sref34"><person-group person-group-type="author"><name><surname>Woolsey</surname><given-names>I.D.</given-names></name><name><surname>Bune</surname><given-names>N.E.T.</given-names></name><name><surname>Jensen</surname><given-names>P.M.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name><name><surname>Kapel</surname><given-names>C.M.O.</given-names></name></person-group><article-title><italic>Echinococcus multilocularis</italic> infection in the field vole (<italic>Microtus agrestis</italic>): an ecological model for studies on transmission dynamics</article-title><source>Parasitol. Res.</source><volume>114</volume><year>2015</year><fpage>1703</fpage><lpage>1709</lpage><pub-id pub-id-type="pmid">25663069</pub-id></element-citation></ref><ref id="bib35"><element-citation publication-type="journal" id="sref35"><person-group person-group-type="author"><name><surname>Woolsey</surname><given-names>I.D.</given-names></name><name><surname>Jensen</surname><given-names>P.M.</given-names></name><name><surname>Deplazes</surname><given-names>P.</given-names></name><name><surname>Kapel</surname><given-names>C.M.O.</given-names></name></person-group><article-title>Establishment and development of <italic>Echinococcus multilocularis</italic> metacestodes in the common vole (<italic>Microtus arvalis</italic>) after oral inoculation with parasite eggs</article-title><source>Parasitol. Int.</source><volume>64</volume><year>2015</year><fpage>571</fpage><lpage>575</lpage><pub-id pub-id-type="pmid">26279253</pub-id></element-citation></ref></ref-list><ack id="ack0010"><title>Acknowledgments</title><p>This work is funded through an <funding-source id="gs1">EU Formas grant (EMIDA-ERA NET)</funding-source> for a project entitled “Echinococcus Multilocularis in ROdents (EMIRO)” (221-2011-2212). The samples from Vetlanda/Växjö and Gnesta/Nyköping were mainly collected within the National Environmental and Wildlife Monitoring and Assessment program (FoMA, <ext-link ext-link-type="uri" xlink:href="http://www.slu.se/en/environment" id="intref0015">http://www.slu.se/en/environment</ext-link>). The authors thank Miloš Anděra for providing the rodent pictures used in the graphical abstract. We also thank the local landowners that put their land at our disposal and the students that helped complete fieldwork.</p></ack></back><floats-group><fig id="fig1"><label>Fig. 1</label><caption><p>Study areas and positive findings of <italic>E. multilocularis</italic> in southern Sweden at the beginning of the study, 2013. Boxes show study areas and stars indicate where positive foxes/fox fecal samples had been found. Circles encompass the study areas where rodents positive for <italic>E. multilocularis</italic> were captured. The lines are county boundaries. (CRS: WGS 84, QGIS 2.12.3).</p></caption><graphic xlink:href="gr1"></graphic></fig><fig id="fig2"><label>Fig. 2</label><caption><p>Macroscopic photos of rodent livers containing <italic>Echinococcus multilocularis</italic> metacestode lesions. The ruler in each picture is in millimeters. (A) Liver from <italic>Microtus agrestis</italic> with one lesion that contained protoscoleces. (B) Liver from <italic>Arvicola amphibius</italic> with multiple lesions that did not contain protoscoleces. (C) Liver from <italic>Arvicola amphibius</italic> with multiple lesions that did contain protoscoleces. (D) Liver from <italic>Arvicola amphibius</italic>. Arrow points to the only lesion examined for protoscoleces, which were absent.</p></caption><graphic xlink:href="gr2"></graphic></fig><fig id="fig3"><label>Fig. 3</label><caption><p>Photomicrographs of liver sections. Sections in A, C, and E are stained with hematoxylin and eosin (H&E) and sections in B, D, and F are stained with periodic acid-Schiff (PAS). (A) Section from <italic>Arvicola amphibius</italic> with multiple fluid filled parasite vesicles outlined by an eosinophilic wall (black arrow) containing large numbers of protoscoleces (arrow head). (B) Section from <italic>Arvicola amphibius</italic> with fluid filled parasite vesicles outlined by PAS-positive laminar layer (arrows). Protoscoleces are organized in places into brood capsules (lining wall indicated by arrow heads). (C) Fluid-filled parasite vesicle with protoscoleces (arrow heads) in a <italic>Microtus agrestis</italic>. (D) Fluid filled parasite vesicle outlined by a PAS-positive laminar layer (arrows) in a <italic>Microtus agrestis</italic>. Protoscoleces are seen within the vesicle. (E) Protoscolex with rostrellar hooks (arrow). (F) Numerous empty variably sized parasite vesicles outlined by a PAS-positive laminar layer (arrows), multifocally surrounded by dense inflammatory infiltrates (asteriks). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)</p></caption><graphic xlink:href="gr3"></graphic></fig><table-wrap id="tbl1" position="float"><label>Table 1</label><caption><p>Results of 1566 rodents captured in four different regions in Sweden during 2013–2015 and examined for <italic>Echinococcus multilocularis</italic>. Number of examined rodents (<italic>n</italic>), number of positive rodents (N), percent positive (%), and 95% confidence interval (95 CI) are given for each region and for each species.</p></caption><table frame="hsides" rules="groups"><thead><tr><th></th><th colspan="3">Uddevalla<hr></hr></th><th colspan="3">Katrineholm<hr></hr></th><th colspan="3">Gnesta/Nyköping<hr></hr></th><th colspan="3">Vetlanda/Växjö<hr></hr></th></tr><tr><th><italic>n</italic></th><th>N</th><th>% (95 CI)</th><th><italic>n</italic></th><th>N</th><th>% (95 CI)</th><th><italic>n</italic></th><th>N</th><th>% (95 CI)</th><th><italic>n</italic></th><th>N</th><th>% (95 CI)</th></tr></thead><tbody><tr><td><italic>Arvicola amphibius</italic></td><td align="char">147</td><td align="char">0</td><td align="char">0 (≤2.5)</td><td align="char">159</td><td align="char">3</td><td align="char">1.9 (0.4–5.4)</td><td align="char">131</td><td align="char">5</td><td align="char">3.8 (1.3–8.7)</td><td align="char">2</td><td align="char">0</td><td align="char">0 (≤84.2)</td></tr><tr><td><italic>Microtus agrestis</italic></td><td align="char">60</td><td align="char">0</td><td align="char">0 (≤6.0)</td><td align="char">73</td><td align="char">0</td><td align="char">0 (≤5.0)</td><td align="char">44</td><td align="char">1</td><td align="char">2.3 (0.1–12.0)</td><td align="char">10</td><td align="char">0</td><td align="char">0 (≤30.8)</td></tr><tr><td><italic>Myodes glareolus</italic></td><td align="char">205</td><td align="char">0</td><td align="char">0 (≤1.8)</td><td align="char">166</td><td align="char">0</td><td align="char">0 (≤2.2)</td><td align="char">124</td><td align="char">0</td><td align="char">0 (≤2.9)</td><td align="char">160</td><td align="char">0</td><td align="char">0 (≤2.3)</td></tr><tr><td><italic>Apodemus</italic> spp.</td><td align="char">78</td><td align="char">0</td><td align="char">0 (≤4.6)</td><td align="char">84</td><td align="char">0</td><td align="char">0 (≤4.3)</td><td align="char">36</td><td align="char">0</td><td align="char">0 (≤9.7)</td><td align="char">87</td><td align="char">0</td><td align="char">0 (≤4.2)</td></tr><tr><td>TOTAL</td><td align="char">490</td><td align="char">0</td><td></td><td align="char">482</td><td align="char">3</td><td></td><td align="char">335</td><td align="char">6</td><td></td><td align="char">259</td><td align="char">0</td><td></td></tr></tbody></table></table-wrap><table-wrap id="tbl2" position="float"><label>Table 2</label><caption><p>Individual description of rodents confirmed <italic>Echinococcus multilocularis</italic> positive in Sweden from 2013 to 2015.</p></caption><table frame="hsides" rules="groups"><thead><tr><th></th><th>Functional group</th><th>Breeding status<xref rid="tbl2fna" ref-type="table-fn">a</xref></th><th>Sex<xref rid="tbl2fnb" ref-type="table-fn">b</xref></th><th>Season<xref rid="tbl2fnc" ref-type="table-fn">c</xref></th><th>Region</th><th>Protoscoleces identified</th></tr></thead><tbody><tr><td colspan="7"><italic>Microtus agrestis</italic></td></tr><tr><td></td><td>Adult</td><td>B</td><td>F</td><td>S 2014</td><td>Gnesta/Nyköping</td><td>Yes</td></tr><tr><td colspan="7"><italic>Arvicola amphibius</italic></td></tr><tr><td></td><td>Adult</td><td>B</td><td>F</td><td>S 2013</td><td>Gnesta/Nyköping</td><td>No</td></tr><tr><td></td><td>Subadult</td><td>NB</td><td>M</td><td>A 2013</td><td>Katrineholm</td><td>No</td></tr><tr><td></td><td>Adult</td><td>B</td><td>F</td><td>S 2014</td><td>Gnesta/Nyköping</td><td>Yes</td></tr><tr><td></td><td>Adult</td><td>B</td><td>F</td><td>S 2014</td><td>Gnesta/Nyköping</td><td>No</td></tr><tr><td></td><td>Adult</td><td>ND<xref rid="tbl2fnd" ref-type="table-fn">d</xref></td><td>F</td><td>S 2015</td><td>Gnesta/Nyköping</td><td>Yes</td></tr><tr><td></td><td>Adult</td><td>B</td><td>M</td><td>S 2015</td><td>Gnesta/Nyköping</td><td>Yes</td></tr><tr><td></td><td>Subadult</td><td>ND<xref rid="tbl2fnd" ref-type="table-fn">d</xref></td><td>M</td><td>A 2013</td><td>Katrineholm</td><td>No</td></tr><tr><td></td><td>Subadult</td><td>NB</td><td>F</td><td>A 2013</td><td>Katrineholm</td><td>No</td></tr></tbody></table><table-wrap-foot><fn id="tbl2fna"><label>a</label><p id="ntpara0010">(B) breeding, (NB) non-breeding (ND) not determined.</p></fn></table-wrap-foot><table-wrap-foot><fn id="tbl2fnb"><label>b</label><p id="ntpara0015">(F) female, (M) male.</p></fn></table-wrap-foot><table-wrap-foot><fn id="tbl2fnc"><label>c</label><p id="ntpara0020">(S) spring, (A) autumn.</p></fn></table-wrap-foot><table-wrap-foot><fn id="tbl2fnd"><label>d</label><p id="ntpara0025">Rodent breeding status was not clearly categorizable.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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