Table 2.
Summary of data extracted from English and Chinese language primary literature reporting surveillance for Echinococcus multilocularis in wild and/or domestic canids (2008–2018).
| Authors, year (language) |
Host | Location | Study design | Sampling method | Sample size | Prevalence % (95% CI) |
Detection method(s) | Case definition | Seq/submissiona |
|---|---|---|---|---|---|---|---|---|---|
| Hanosset et al. 2008 (English) |
Red foxes | Wallonoia, Southern Belgium | Cross-sectional | Convenience | 990 | 24.55 (22.38–27.87) |
(i) Intestines: mucosal scraping (ii) Cestode morphology |
Morphology +ve | NA |
| Dyachenko et al. 2008 (English) |
Dogs | Austria Denmark Germany France Italy Luxembourg Netherlands |
Cross-sectional | Convenience | Austria: 812 Denmark: 517 Germany: 17894 France: 980 Italy: 249 Luxembourg: 165 Netherlands: 734 |
Germany: 0.24 (0.17–0.32) Other countries: 0 |
(i) Feces: ZnCl2/NaCl flotation (ii) Nested PCR (12S) |
Microscopy and PCR +ve | Not sequenced |
| Bagrade et al. 2008 (English) |
Red foxes | Latvia | Cross-sectional | Convenience | 45 | 35.60 | (i) Intestinal examination (ii) Cestode morphology (iii) PCR (CO1, ND1, rrnS, ATP6, actII) (iv) Sequencing |
NR | Sequenced |
| Guislain et al. 2008 (English) |
Foxes | French Ardennes region, France | Cross-sectional | Convenience | 149 | 53 (45.4–60.6) |
(i) Intestines: SCTb (ii) Cestode morphology (iii) Fragment size analyses (EmsB microsatellite target) |
NR | Not sequenced |
| Ziadinov et al. 2008 (English) |
Dogs (no puppies, pregnant bitches) | At-Bashy, Naryn province, Kyrgyzstan | Cross-sectional | Cluster | 466 | 11 | (i) Arecoline purgation (ii) Cestode morphology (iii) Fecal: ZnCl2 sieving/flotation (v) Multiplex PCR |
Morphology or PCR +ve | Not sequenced |
| Bourecka et al. 2008 (English) |
Red foxes | Małopolskie voivodship, Poland | Cross-sectional | Convenience | 214 | 20.1 (14.72–25.46) |
(i) Intestines: ISTc (ii) Cestode morphology |
Morphology +ve | NA |
| Antolova et al. 2009 (English) |
Dogs (not dewormed in 4 mos) | Presov and Kosice regions, Slovakia | Cross-sectional | NR | 289 | 2.8 | (i) Feces-Sheather's sucrose flotation (ii) Copro-antigen ELISAd (iii) Nested copro-PCR (12S) |
PCR +ve | Not sequenced |
| Takumi et al. 2008 (English) |
Foxes | Groningen & Limburg Provinces, The Netherlands | Cross-sectional | Convenience | 1996–1997: 39 2003: 195 |
1996–1997: 7.7 2003: 11.7 |
(i) Intestines: IST (ii) PCR |
NR | Not sequenced |
| Malczewski et al. 2008 (English) |
Red foxes | Northeast & Southeast Poland | NR | NR | 1514 | 23.8 (21.63–25.92) |
(i) Intestines: IST (ii) Cestode morphology |
Morphology +ve | NA |
| Robardet et al. 2008 (English) |
Red foxes | Nancy, France | Cross-sectional | Convenience | 127 | 30 | (i) Intestines: SCT (ii) Cestode morphology |
Morphology +ve | NA |
| Nonaka et al. 2009 (English) |
Dogs | Hokkaido, Honshu, Kyushu, Japan | Cross-sectional | Convenience | Hokkaido: 4768 Honshu/Kyushu: 348 |
Hokkaido: 0.86 Honshu/Kyusho: 0.86 |
(i) Feces: Sieving/flotation (ii) Copro-antigen ELISA (iii) PCR (CO1, 12S, U1 snRNA) |
NR | Sequenced |
| Bružinskaitė et al. 2009 (English) |
Dogs (in AE +ve villages) | Lithuania | Cross-sectional | Convenience | 240 | 0.8% (0.1–3) |
(i) Feces: McMaster method (ii) ZnCl2 sieving/flotation (iii) Multiplex PCR |
NR | Not sequenced |
| Nonaka et al. 2009 (English) |
Silver foxes, red foxes, raccoon dogs, Dogs | Hokkaido, Japan | Cross-sectional | NR | Foxes: 209 Raccoon dogs: 3 Dogs: 3 |
Foxes: 12.9 Raccoon dogs: 0 Dogs: 0 |
(i) Feces: Sucrose flotation (ii) Copro-antigen ELISA (iii) PCR (CO1) |
PCR +ve | Not sequenced |
| Hurnikova et al. 2009 (English) |
Red foxes, Raccoon dogs | Tatra National Park, Slovakia | Cross-sectional | Convenience | Red foxes: 328 Raccoon dogs: 2 |
Red foxes: 42.7 Raccoon dogs: 50 |
(i) Intestines: SCT (ii) Cestode morphology |
Morphology +ve | NA |
| Bagrade et al. 2009 (English) |
Wolves | Latvia | NR | NR | 34 | 5.9 | (i) Intestinal examination (ii) Cestode morphology |
Morphology +ve | NA |
| Barabasi et al. 2010 (English) |
Red foxes | Romania | Cross-sectional | Convenience | 561 | 4.8 (3.2–6.9) |
(i) Intestines: Sedimentation & mucosal scraping (ii) Cestode morphology (iii) Multiplex PCR (iv) Sequencing |
NR | Sequenced |
| Casulli et al. 2010 (English) |
Red foxes | Hungary | Cross-sectional | NR | 840 | 10.7 (9.7–11.7) |
(i) Intestines: SCT (ii) Cestode morphology (iii) Fluorescent PCR & fragment size analyses (EmsB microsatellite target) |
NR | Not sequenced |
| Stien et al. 2010 (English) |
Arctic foxes | Svalbard Islands, Norway | Cross-sectional | Convenience | 353 | 8.5 (6–11.9) |
(i) Intestines: IST (ii) Cestode morphology |
Morphology +ve | NA |
| Wang et al. 2010 (English) |
Dogs | Shiqu County, Ganzi Tibetan Autonomous Prefecture, China | NR | Clustered, non-random | 228 | 14.80 | (i) Arecoline purgation (ii) Cestode morphology (iii) Copro-PCR (12S) |
Copro-PCR +ve | Not sequenced |
| Ziadinov et al. 2010 (English) |
Red foxes | Naryn Oblast, Kyrgyzstan | Cross-sectional | Convenience | 151 | 63.6 (55.4–71.3) |
(i) Intestines – SCT (ii) Cestode morphology |
Morphology +ve | NA |
| Siko et al. 2011 (English) |
Red foxes | Romania | Cross-sectional | Convenience | 561 | 4.8 (3.2–6.9) | (i) Intestines: SCT and/or mucosal scraping (ii) Cestode morphology (iii) Multiplex PCR (iv) Sequencing |
NR | Sequenced |
| Beiromvand et al. 2011 (English) |
Dogs, foxes, wolves | Chenaran,Razavi Khorasan Province, Iran | Cross-sectional | Convenience | Dogs: 77 Foxes: 3 Wolf: 1 |
Dogs: 6.5 (2.8–14.3) Foxes & wolf: 100 (78.5–100) |
Dogs: (i) Fecal ZnCl2 sieving/flotation (ii) Multiplex PCR Foxes & wolf: (i) Intestines: IST or SCT (iii) Cestode morphology |
NR | Sequenced and submitted |
| Karamon et al. 2011 (English) |
Red foxes | Świętokrzyskie & Lubelskie Provinces, Poland | Cross-sectional | NR | 353 | 13.6 | Intestines: SCT | SCT +ve | NA |
| Umhang et al. 2011 (English) |
Foxes | France | Cross-sectional | NR | 358 | 32.7 | Reference: SCT Index: SSCTe |
SCT +ve | NA |
| Miterpakova et al. 2011 (English) | Red foxes | Slovakia | Cross-sectional | Stratified cluster | 4761 | 30.3 | Intestines: SCT | SCT +ve | NA |
| Umhang et al. 2012 (English) |
Dogs | Meuse and Haute-Saone, France | Cross-sectional | Convenience | Meuse: 493 Haute-saone: 367 |
Meuse: <1 Haute-saone: <0.75 |
(i) Fecal ZnCl2 sieving/flotation (ii) PCR (ND1) |
PCR +ve | Not sequenced |
| Catalano et al. 2012 (English) |
Coyotes | Alberta, Canada | Cross-sectional | Convenience | 91 | 25.30 | (i) Intestinal sieving (ii) Cestode morphology (iii) Multiplex PCR |
Morphology and PCR +ve | Not sequenced |
| Jiang et al. 2012a (English) |
Tibetan foxes, Red foxes | Shiqu County, China | Cross-sectional | Convenience | 184 | 35 | Reference: RFLP-PCR Index: (i) Nested multiplex copro-PCR (CO1) (ii) Sequencing |
NR | Sequenced and submitted |
| Compte et al. 2012 (English) |
Foxes | France | Cross-sectional | Stratified | 3307 | 17 (16–19) |
Intestines: SSCT | SSCT +ve | NA |
| Jiang et al. 2012b (Chinese) |
Tibetan foxes | Yunbo Gou, Shiqu County, Sichuan Province, China | Cross-sectional | Cluster | 120 | 19 | Nested duplex copro-PCR | PCR +ve | Sequenced and submitted |
| Takahashi et al. 2013 (English) |
Foxes | Nemuro peninsula, Hokkaido, Japan | Cross-sectional | Simple random | Bait zone: 411 Control zone: 163 |
Pre-baitf (1994–1999): Bait: 49.4 (43.7–55) Control: 70.5 (60.2–79.2) Post-bait: (2003–2006): Bait: 15.8 (7.9–28.4) Control: 65 (40.9–83.7) |
(i) Intestines: mucosal scraping (ii) Cestode morphology |
Morphology +ve | NA |
| Tolnai et al. 2013 (English) |
Red foxes | Hungary | Cross-sectional | Random | 2008: 840 2012: 772 |
2008: 10.7 (9.7–11.7) 2012: 7.9 (6.9–8.9) |
(i) Intestines: SCT (ii) Cestode morphology (iii) Microsatellite analysis (iv) PCR (12S) |
Morphology +ve | Not sequenced |
| Gesy et al. 2013 (English) |
Red foxes, coyotes | Quesnel, Canada | Cross-sectional | Convenience | Red foxes: 6 Coyotes: 27 |
Coyotes: 71 Foxes: 17 |
(i) Intestines: SFCTg (ii) Cestode morphology (iii) PCR (ND1, ND2, COB, CO1) (iv) Sequencing |
Morphology and PCR +ve | Sequenced |
| Mobedi et al. 2013 (English) |
Dogs, red foxes | Moghan Plain, Iran | Cross-sectional | NR | Dogs: 59 Red foxes: 84 |
Dogs: 0 Red foxes: 0 |
(i) Copro-antigen ELISA (ii) Nested copro-PCR (12S) |
NR | Not sequenced |
| Moss et al. 2013 (English) |
Dogs | Shiqu and Yajiang counties, China | Cohort | NR | 592 | 11.20 | (i) Copro-antigen ELISA (ii) Copro-PCR (ND1) |
NR | Not sequenced |
| Li et al. 2013 (English) |
Tibetan sand foxes and red foxes | Qinghai, China | Cross-sectional | Convenience | Intestines: 36 Feces: 70 |
Intestines: 3 Feces: 1.4 |
(i) Intestinal examination (ii) Feces-Sucrose flotation (iii) PCR (CO1) (iv) Sequencing |
NR | Sequenced |
| Comte et al. 2013 (English) |
Foxes | Annemasse & Pontarlier, France | Cross-sectional | Purposive | Annemasse: 700 Pontarlier: 700 |
Pre-baitf (2006) Annemasse: 13.3 Pontarlier: 10.9 Post-bait (2007–2009) Annemasse: 2.2 Pontarlier: 7.1 |
Copro-antigen ELISA | ELISA +ve | NA |
| Schurer et al. 2014 (English) |
Wolves | Saskatchewan (SK), Manitoba (MB), Northwest Territories (NT) | Cross-sectional | Convenience | SK: 17 MB: 3 NT: 73 |
SK: 23.5 MB: 67 NT: 8.2 |
(i) Intestines: SFCT (ii) Cestode morphology (iii) PCR (CO1, ND1) (iv) Sequencing |
PCR +ve | Sequenced and submitted |
| Umhang et al. 2014 (English) |
Dogs | Annemasse and Pontarlier, France | Cross-sectional | NR | 817 | 0.5 (0.1–1.3) | (i) Fecal sieving/flotation (ii) Multiplex PCR (iii) Sequencing |
PCR +ve | Sequenced |
| Isaksson et al. 2014 (English) |
Red foxes | Eastern Switzerland and Sweden | Cross-sectional | NR | Switzerland: 177 Sweden: 2158 |
NA | Reference: Intestines: SCT Index: Fecal Magnetic Capture RT-PCR |
SCT +ve | Not sequenced |
| Denzin et al. 2014 (English) |
Red foxes | Saxony-Anhalt, Germany | Cross-sectional | NR | 1998–2005: 1882 2006–2010: 2307 |
1998–2005: 13.6 (11.6–15.6) 2006–2010: 23.4 (21.2–25.7) |
(i) Intestinal Smear Technique (ii) Cestode morphology |
‘Smear’ +ve | NA |
| Maas et al. 2014 (English) |
Red foxes, Dogs (>6 mos, not dewormed in 1 mo) | South Limburg, Maastricht, The Netherlands | Cross-sectional | Convenience | Red foxes: 37 Dogs: 142 |
Red foxes: 59 (43–74) Dogs: 0 |
Red foxes: (i) IST (ii) Nested PCR Dogs: Copro-qPCR |
Red foxes: IST or PCR +ve Dogs: qPCR +ve |
Not sequenced |
| Liccioli et al. 2014 (English) |
Coyotes | Calgary, Canada | Cross-sectional | Convenience | 385 | 21.42 | (i) Fecal ZnCl2 sieving/flotation (ii) PCR |
PCR +ve | Not sequenced |
| Karamon et al. 2014 (English) |
Red foxes | Poland | Cross-sectional | Convenience | 1546 | 16.5 (14.7–18.4) | Intestines: SCT | SCT +ve | NA |
| Gesy et al. 2014 (English) |
Arctic foxes Red foxes Coyotes | Canada | Cross-sectional | Convenience | Arctic foxes: 404 Red foxes: 6 Coyotes: 48 |
Arctic foxes: 0.74 Red foxes: 17 Coyotes: 58 |
(i) Fecal Sucrose Flotation (ii) Intestines: SFCT (iii) Simplex/multiplex PCR (iv) Sequencing |
NR | Sequenced and submitted |
| Ma et al. 2014 (Chinese) |
Red foxes | Zhaosu basin, China | Cross-sectional | Stratified cluster | 6 | 50 | (i) Intestinal examination (ii) Cestode morphology |
Morphology +ve | Not sequenced |
| Karamon et al. 2015 (English) |
Red foxes | Śląskie, Opalskie, Lubelskie, Podkarpackie, Poland | Cross-sectional | Convenience | 500 | Śląskie: 11.7 (6.7–19.4) Opalskie: 3.9 (1.6–8.4) Podkarpackie: 54.6 (46.7–62.3) Lubelskie: 18.9 (12.0–28.3) Overall: 23.6 |
Intestines: SCT | SCT +ve | NA |
| Melotti et al. 2015 (English) |
Coyotes, red foxes, grey foxes | Michigan, USA | Cross-sectional | Convenience | Coyotes: 223 Grey foxes: 45 Red foxes: 34 |
Coyotes: 0.4 Red foxes: 0 Grey foxes: 0 |
All canids: (i) Intestines: SCT (ii) Multiplex PCR (iii) Sequencing |
NR | Sequenced |
| Villeneuve et al. 2015 (English) |
Shelter dogs (not dewormed in 5 mos) | Canada | Cross-sectional | Quota | 1086 | 0 | (i) Fecal sucrose flotation (ii) Multiplex PCR |
PCR +ve | Not sequenced |
| Laurimaa et al. 2015 (English) |
Raccoon dogs | Estonia | Cross-sectional | Convenience | 249 | 1.6 (0.4–4.1) |
(i) Intestines: SCT (ii) Cestode morphology (iii) PCR (Ile/Lys) (iv) Sequencing |
NR | Sequenced and submitted |
| Laurimaa et al. 2016 (English) |
Red foxes | Estonia | Cross-sectional | Convenience | 111 | 31.5 (22.7–40.3) |
(i) Intestines: SCT (ii) Cestode morphology |
Morphology +ve | NA |
| Bagrade et al. 2016 (English) |
Red foxes, racoon dogs | Latvia | Cross-sectional | NR | Red foxes: 538 Racoon dogs: 407 |
Red foxes: 17.1 (13.9–20.3) Racoon dogs: 8.1 (5.5–10.8) |
All canids: (i) Intestines: SCT (ii) Cestode morphology (iii) Multiplex PCR (iv) PCR (CO1) (v) Sequencing |
NR | Sequenced |
| Miller et al. 2016 (English) |
Red fox | Katrineholm, Uddevalla, Gnesta/Nyköping, Vetlanda/Växjö, Sweden | Cross-sectional | Purposive | 714 | 5.7 (4.2–7.7) | (i) Fecal sieving/flotation (ii) Multiplex PCR (iii) Sequencing |
PCR and sequence +ve | Sequenced and submitted |
| Umhang et al. 2016 (English) |
Wild: foxes Captive: red foxes, Alaskan tundra wolves, Eurasian wolves |
Moselle, France | Wild: cross-sectional Captive: cohort |
Purposive | Captive: Foxes:3 Alaskan wolves: 35 Eurasian wolves: 75 Wild foxes: Feces (in/out park): 142 Intestines: 5 |
Captive: Eurasian wolves: 1.3 Red fox: 0 Alaskan wolves: 0 Wild foxes: Outside park: 20.6 (13.1–30) Inside park: 17.8 (8–32.1) Intestines: 60 |
Feces: (i) Sieving/flotation (ii) Multiplex PCR (iii) Sequencing Intestines: (i) SSCT (ii) EmsB microsatellite analysis |
NR | Sequenced |
| Comte et al., 2017 (English) |
Foxes | Nancy, France | Cross-sectional | Systematic | 445 | 57% | Intestines: SSCT | SSCT +ve | NA |
| Frey et al. 2017 (English) |
Dogs (clinical AE cases, presumed uninfected, negative controls) | Switzerland | Diagnostic investigation | Presumed uninfected - random; Clinical AE and negative controls - NR | 75 | NA | Reference: Abdominal ultrasound Index (Serology): (i) ELISA (EmVF, Em2-antigen, rEm18, rEm95) (ii) In-house Western Blot (iii) Anti-Echinococcus EUROLINE-Western Blot (IgG, rEm18, rEm95, rEgAgB) |
Ultrasound +ve | NA |
| Schuster & Shimalov 2017 (English) |
Raccoon dogs, red foxes | Uckermark district, Brandenburg state, Germany | Cross-sectional | Convenience | Raccoon dogs: 101 Red foxes: 144 |
Raccoon dogs: 0.99 Red Foxes: 1.39 |
(i) Intestines: Sedimentation Technique (ii) Cestode morphology |
Morphology +ve | NA |
| Maksimov et al. 2017 (English) |
Foxes | NR | NR | NR | 120 | NA | Reference: intestines: IST Index 1: (i) ZR Faecal DNA MiniPrep™ (ii) FastDNA® SPIN Kit for Soil (iii) QIAamp® Fast DNA Stool MiniKit (iv) NucleoSpin®Soil Index 2: (i) PCR (rrnS), (ii) iQS-qPCR (rrnL) (iii) QT-qPCR (rrnL) |
NR | Not sequenced |
| Poulle et al. 2017 (English) |
Dogs, red foxes | Ardennes, France | Cross-sectional | Convenience | Dogs: 18 Red foxes: 69 |
Dogs: 11.1 (1.4–34.7) Red foxes: 34.8 (23.5–47.6) |
Copro-qPCR (rrnL) | qPCR +ve | Not sequenced |
| Kohansal et al. 2017 (English) |
Stray dogs | Zanjan Province, Iran | Cross-sectional | NR | 450 | 0 | (i) Fecal Formalin ethyl acetate concentration test (ii) ZnCl2 sieving/flotation (iii) Multiplex PCR |
PCR +ve | Not sequenced |
| Hermosilla et al. 2017 (English) |
Wolves | Gorski Kotar region, Croatia | Cross-sectional | NR | 400 | 0 | (i) Fecal Sodium acetate formalin test (ii) Nested PCR (12S) (iii) Sequencing |
NR | Sequenced and submitted |
| Otero-Abad et al. 2017 (English) |
Red foxes | Switzerland | Cross-sectional | Convenience | 300 | 59.5 (43.1–66.4) | Reference: Intestines – SCT Index (i): Polyclonal copro-antigen ELISA Index (ii): Monoclonal copro-antigen ELISA Index (iii): Multiplex PCR |
SCT +ve | Not sequenced |
| Schurer et al. 2018 (English) |
Wolves, coyotes, red foxes, Arctic foxes | Quebec Canada (QC), Maine USA (ME) | Cross-sectional | Convenience | QC: 284 ME: 23 |
QC: 0 ME: 0 |
All canids: (i) Intestines: SFCT (ii) Simplex/multiplex PCR (CO1, ND1) (iii) Sequencing |
NR | Sequenced and submitted |
| Petersen et al. 2018 (English) |
Red foxes, Raccoon dogs | Denmark | Cross-sectional | Convenience | Red foxes: 1073 Raccoon dogs: 272 |
Red foxes: 1.8 Raccoon dogs: 0.7 |
Intestines: (i) SCT (ii) Cestode morphology Feces: Magnetic Capture RT- PCR |
Morphology or PCR + ve | Sequenced and submitted |
| Massolo et al. 2018 (English) |
Wolves, dogs | Parco Regionale delle Alpi Liguri, Italy | Cross-sectional | Convenience | Dogs: 32 Wolves: 120 |
Dogs: 12.5 Wolves: 4.2 |
All canids: (i) Feces - ZnCl2 sieving/flotation (ii) PCR (ND1, COB) (iii) Sequencing |
PCR +ve | Sequenced |
| Gurler et al. 2018 (English) |
Red foxes | Central Anatolia and Thrace, Turkey | Cross-sectional | Random | 405 | 1.90 | (i) Fecal flotation (ii) Multiplex PCR |
PCR +ve | Not sequenced |
| Beiromvand et al. 2018 (English) |
Domestic dogs | Ahvaz County, Khuzestan Province, Iran | Cross-sectional | Simple random | 167 | 0 | (i) ZnCl2 sieving/flotation (ii) Multiplex PCR |
NR | Sequenced |
| Knapp et al. 2018 (English) |
Red foxes, Dogs | Franche-Comté and Ile-de-France, France | Cross-sectional | Systematic | Red foxes: 590 Dogs: 1858 |
Red foxes: 27.9 (23.8–32.4) Dogs: 1.1 (0.4–3.0) |
(i) Copro-qPCR (rrnL) (ii) Sequencing |
Sequence +ve | Sequenced |
| Liu et al. 2018 (English) |
Dog | Xiji County, Ningxia Hui Autonomous Region, China | Cross-sectional | Convenience | 750 | 14.1 | (i) Multiplex copro-PCR (ND5) | Copro-PCR +ve | Not sequenced |
NR - not reported; NA - not applicable.
a
E. multilocularis PCR products sequenced and submitted to GenBank.
b
SCT - Sedimentation and Counting Technique.
c
IST - Intestinal Scraping Technique.
d
Enzyme-linked Immunosorbent Assay.
e
SSCT - Segmental Sedimentation and Counting Technique.
f
Praziquantel-based baits.
g
SFCT - Sedimentation, Filtration, and Counting Technique.