Rodent control programmes can integrate Echinococcus multilocularis surveillance by facilitating parasite genotyping: the case of Arvicola terrestris voles screening in France.
Arvicola terrestris
Echinococcus multilocularis
EmsB genotyping
Surveillance
Journal
Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571
Informations de publication
Date de publication:
May 2021
May 2021
Historique:
received:
25
11
2020
accepted:
15
03
2021
pubmed:
21
3
2021
medline:
9
6
2021
entrez:
20
3
2021
Statut:
ppublish
Résumé
The tapeworm Echinococcus multilocularis is the causative agent of alveolar echinococcosis, the most serious parasitic disease for humans in Europe. In Europe, the E. multilocularis lifecycle is based on a prey-predator relationship between the red fox and small rodents. Over the last three decades, the surveillance of E. multilocularis infection in red foxes has led to the description of a wider distribution pattern across Europe. France constitutes the current European western border, but only the north-eastern half of the country is considered endemic. The red fox is the host mainly targeted in E. multilocularis surveillance programmes, but surveys targeting small rodents may be useful for obtaining molecular data, especially when the time-consuming trapping is already carried out in dedicated pest-control programmes. Here, we screened for parasitic lesions in the livers of 1238 Arvicola terrestris voles originating from the historical, but neglected focal area located in central France (Auvergne region) and from Hautes-Alpes, a recently identified endemic department in south-eastern France. This screening identified six voles infected with E. multilocularis in Hautes-Alpes and none in Puy-de-Dôme (Auvergne region) after molecular confirmation. The absence of infected rodents from Puy-de-Dôme can be mainly explained by the generally low prevalence reported in intermediate hosts. The infected Hautes-Alpes samples come all from the same trapping site situated at around 5 km from one of the three fox faecal samples with E. multilocularis DNA collected 15 years prior, thereby confirming the existence and persistence of the E. multilocularis lifecycle in the area. All the rodent E. multilocularis samples from Hautes-Alpes showed the same EmsB microsatellite marker profile. This profile has previously been described in Europe only in the Jura department (central eastern France), located at least 180 km further north. Successive migrations of infected foxes from the historical focal area, including from Jura, to Hautes-Alpes may explain the detection of the parasite in A. terrestris in Hautes-Alpes. Existing trapping efforts in areas where farmers trap A. terrestris for surveillance and pest control can be an effective complement to sampling foxes or fox faeces to obtain E. multilocularis molecular profiles.
Identifiants
pubmed: 33742248
doi: 10.1007/s00436-021-07126-7
pii: 10.1007/s00436-021-07126-7
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1903-1908Références
Beck R, Mihaljevic Z, Brezak R, Bosnic S, Jankovic IL, Deplazes P (2018) First detection of Echinococcus multilocularis in Croatia. Parasitol Res 117(2):617–621. https://doi.org/10.1007/s00436-017-5732-3
doi: 10.1007/s00436-017-5732-3
pubmed: 29280073
Bowles J, Blair D, McManus DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol 54(2):165–173. https://doi.org/10.1016/0166-6851(92)90109-W
doi: 10.1016/0166-6851(92)90109-W
pubmed: 1435857
Combes B, Comte S, Raton V, Raoul F, Boué F, Umhang G, Favier S, Dunoyer C, Woronoff-Rehn N, Giraudoux P (2013) Expansion géographique du parasite Echinococcus multilocularis chez le renard en France. Bull Epidémiol Santé Animale – Alimen 57:16–18
Combes B, Comte S, Raton V, Raoul F, Boué F, Umhang G, Favier S, Dunoyer C, Woronoff N, Giraudoux P (2012) Westward spread of Echinococcus multilocularis in foxes, France, 2005–2010. Emerg Infect Dis 18(12):2059–2062. https://doi.org/10.3201/eid1812.120219
doi: 10.3201/eid1812.120219
pubmed: 23171707
pmcid: 3557902
Eckert J, Conraths FJ, Tackmann K (2000) Echinococcosis: an emerging or re-emerging zoonosis? Int J Parasitol 30(12-13):1283–1294
doi: 10.1016/S0020-7519(00)00130-2
pubmed: 11113255
Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS (2001) WHO/OIE Manual on echinococcosis in humans and animals: a public health problem of global concern. O.I.E. - O.M.S, Paris
Giraudoux P, Pierre D, Takahashi K, Francis R, Jean PQ, Philip C, Dominique V (2002) Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multiscale approaches?
Gottstein B, Stojkovic M, Vuitton DA, Millon L, Marcinkute A, Deplazes P (2015) Threat of alveolar echinococcosis to public health – a challenge for Europe. Trends Parasitol 31(9):407–412. https://doi.org/10.1016/j.pt.2015.06.001
doi: 10.1016/j.pt.2015.06.001
pubmed: 26115902
Guerra D, Hegglin D, Bacciarini L, Schnyder M, Deplazes P (2014) Stability of the southern European border of Echinococcus multilocularis in the Alps: evidence that Microtus arvalis is a limiting factor. Parasitology 141(12):1593–1602. https://doi.org/10.1017/S0031182014000730
doi: 10.1017/S0031182014000730
Isaksson M, Hagstrom A, Armua-Fernandez M, Wahlstrom H, Agren E, Miller A, Holmberg A, Lukacs M, Casulli A, Deplazes P, Juremalm M (2014) A semi-automated magnetic capture probe based DNA extraction and real-time PCR method applied in the Swedish surveillance of Echinococcus multilocularis in red fox (Vulpes vulpes) faecal samples. Parasit Vectors 7(1):583. https://doi.org/10.1186/s13071-014-0583-6
doi: 10.1186/s13071-014-0583-6
pubmed: 25522844
pmcid: 4282741
Knapp J, Bart JM, Glowatzki ML, Ito A, Gerard S, Maillard S, Piarroux R, Gottstein B (2007) Assessment of use of microsatellite polymorphism analysis for improving spatial distribution tracking of Echinococcus multilocularis. J Clin Microbiol 45(9):2943–2950. https://doi.org/10.1128/JCM.02107-06
doi: 10.1128/JCM.02107-06
pubmed: 17634311
pmcid: 2045259
Knapp J, Damy S, Brillaud J, Tissot JD, Navion J, Melior R, Afonso E, Hormaz V, Gottstein B, Umhang G, Casulli A, Dadeau F, Millon L, Raoul F (2017) EWET: data collection and interface for the genetic analysis of Echinococcus multilocularis based on EmsB microsatellite. PLoS One 12(10):e0183849. https://doi.org/10.1371/journal.pone.0183849
doi: 10.1371/journal.pone.0183849
pubmed: 28972978
pmcid: 5626424
Knapp J, Staebler S, Bart JM, Stien A, Yoccoz NG, Drogemuller C, Gottstein B, Deplazes P (2012) Echinococcus multilocularis in Svalbard, Norway: microsatellite genotyping to investigate the origin of a highly focal contamination. Infect Genet Evol 12(6):1270–1274. https://doi.org/10.1016/j.meegid.2012.03.008
doi: 10.1016/j.meegid.2012.03.008
pubmed: 22465539
Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam
Massolo A, Valli D, Wassermann M, Cavallero S, D'Amelio S, Meriggi A, Torretta E, Serafini M, Casulli A, Zambon L, Boni CB, Ori M, Romig T, Macchioni F (2018) Unexpected Echinococcus multilocularis infections in shepherd dogs and wolves in south-western Italian Alps: a new endemic area? Int J Parasitol 7(3):309–316. https://doi.org/10.1016/j.ijppaw.2018.08.001
doi: 10.1016/j.ijppaw.2018.08.001
Oksanen A, Siles-Lucas M, Karamon J, Possenti A, Conraths FJ, Romig T, Wysocki P, Mannocci A, Mipatrini D, La Torre G, Boufana B, Casulli A (2016) The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: a systematic review and meta-analysis. Parasit Vectors 9(1):1–23. https://doi.org/10.1186/s13071-016-1746-4
doi: 10.1186/s13071-016-1746-4
Petavy AF, Deblock S (1983) Connaissance du foyer auvergnat d'échinococcose alvéolaire. Ann Parasitol Hum Comp 58(5):439–453
doi: 10.1051/parasite/1983585439
pubmed: 6362536
R Development Core Team (2005) R: A language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna
Romig T (2009) Echinococcus multilocularis in Europe—state of the art. Vet Res Commun 33(Suppl 1):31–34. https://doi.org/10.1007/s11259-009-9244-1
doi: 10.1007/s11259-009-9244-1
pubmed: 19578966
Romig T, Dinkel A, Mackenstedt U (2006) The present situation of echinococcosis in Europe. Parasitol Int 55(Suppl):S187–S191. https://doi.org/10.1016/j.parint.2005.11.028
doi: 10.1016/j.parint.2005.11.028
pubmed: 16352465
Shimodaira H (2002) An approximately unbiased test of phylogenetic tree selection. Syst Biol 51(3):492–508. https://doi.org/10.1080/10635150290069913
doi: 10.1080/10635150290069913
pubmed: 12079646
Shimodaira H (2004) Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. Ann Stat 32(6):2616–2641
doi: 10.1214/009053604000000823
Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22(12):1540–1542. https://doi.org/10.1093/bioinformatics/btl117
doi: 10.1093/bioinformatics/btl117
pubmed: 16595560
Umhang G, Comte S, Hormaz V, Boucher JM, Raton V, Favier S, Raoul F, Giraudoux P, Combes B, Boue F (2016) Retrospective analyses of fox feces by real-time PCR to identify new endemic areas of Echinococcus multilocularis in France. Parasitol Res 115(11):4437–4441. https://doi.org/10.1007/s00436-016-5220-1
doi: 10.1007/s00436-016-5220-1
pubmed: 27517858
Umhang G, Karamon J, Hormaz V, Knapp J, Cencek T, Boué F (2017) A step forward in the understanding of the presence and expansion of Echinococcus multilocularis in Eastern Europe using microsatellite EmsB genotyping in Poland. Infect Genet Evol 54:176–182. https://doi.org/10.1016/j.meegid.2017.07.004
doi: 10.1016/j.meegid.2017.07.004
pubmed: 28688974
Umhang G, Knapp J, Hormaz V, Raoul F, Boue F (2014) Using the genetics of Echinococcus multilocularis to trace the history of expansion from an endemic area. Infect Genet Evol 22:142–149. https://doi.org/10.1016/j.meegid.2014.01.018
doi: 10.1016/j.meegid.2014.01.018
pubmed: 24468327
Umhang G, Richomme C, Boucher JM, Guedon G, Boue F (2013) Nutrias and muskrats as bioindicators for the presence of Echinococcus multilocularis in new endemic areas. Vet Parasitol 197(1-2):283–287. https://doi.org/10.1016/j.vetpar.2013.05.003
doi: 10.1016/j.vetpar.2013.05.003
pubmed: 23725822
Vuitton DA, Demonmerot F, Knapp J, Richou C, Grenouillet F, Chauchet A, Vuitton L, Bresson-Hadni S, Millon L (2015) Clinical epidemiology of human AE in Europe. Vet Parasitol 213(3–4):110–120. https://doi.org/10.1016/j.vetpar.2015.07.036
doi: 10.1016/j.vetpar.2015.07.036
pubmed: 26346900
Vuitton DA, McManus DP, Rogan MT, Romig T, Gottstein B, Naidich A, Tuxun T, Wen H, Menezes da Silva A, Echinococcosis TWAO, Vuitton DA, McManus DP, Romig T, Rogan MR, Gottstein B, Menezes da Silva A, Wen H, Naidich A, Tuxun T, Avcioglu A, Boufana B, Budke C, Casulli A, Güven E, Hillenbrand A, Jalousian F, Jemli MH, Knapp J, Laatamna A, Lahmar S, Naidich A, Rogan MT, Sadjjadi SM, Schmidberger J, Amri M, Bellanger A-P, Benazzouz S, Brehm K, Hillenbrand A, Jalousian F, Kachani M, Labsi M, Masala G, Menezes da Silva A, Sadjjadi Seyed M, Soufli I, Touil-Boukoffa C, Wang J, Zeyhle E, Aji T, Akhan O, Bresson-Hadni S, Dziri C, Gräter T, Grüner B, Haïf A, Hillenbrand A, Koch S, Rogan MT, Tamarozzi F, Tuxun T, Giraudoux P, Torgerson P, Vizcaychipi K, Xiao N, Altintas N, Lin R, Millon L, Zhang W, Achour K, Fan H, Junghanss T, Mantion GA (2020) International consensus on terminology to be used in the field of echinococcoses. Parasite 27:41. https://doi.org/10.1051/parasite/2020024
doi: 10.1051/parasite/2020024
pubmed: 32500855
pmcid: 7273836