Open Access

Echinococcus multilocularis in foxes and raccoon dogs: an increasing concern for Baltic countries

  • Guna Bagrade1Email author,
  • Gunita Deksne2,
  • Zanda Ozoliņa2,
  • Samantha Jane Howlett1,
  • Maria Interisano3,
  • Adriano Casulli3, 4 and
  • Edoardo Pozio3
Parasites & Vectors20169:615

https://doi.org/10.1186/s13071-016-1891-9

Received: 6 July 2016

Accepted: 17 November 2016

Published: 29 November 2016

Abstract

Background

In Europe, the life-cycle of Echinococcus multilocularis is predominantly sylvatic, involving red foxes (Vulpes vulpes) as the main definitive hosts and rodents such as muskrats and arvicolids as intermediate hosts. The parasite is the etiological agent of human alveolar echinococcosis, a malignant zoonotic disease caused by the accidental ingestion of eggs shed by definitive hosts in their faeces. The aims of this study were to investigate the prevalence of E. multilocularis in red foxes and raccoon dogs (Nyctereutes procyonoides) and to study the environmental factors favouring the perpetuation of the parasite in Latvia.

Methods

A total of 538 red foxes and 407 raccoon dogs were collected across Latvia from 2010 to 2015. The sedimentation and counting technique was used for collecting E. multilocularis adult worms from fox and raccoon dog intestines. The morphological identification of the parasite was confirmed by molecular analysis.

Results

The prevalence of E. multilocularis was significantly higher in foxes (17.1%; intensity of infection 1–7,050 worms) (P < 0.001) than in raccoon dogs (8.1%; intensity of infection 5–815 worms). In foxes, a significant positive correlation (r (10) = 0.7952, P = 0.001) was found between parasite prevalence and the intensity of infection. A positive relationship (R s = 0.900, n = 5, P = 0.037) between parasite prevalence and precipitation was also observed. In raccoon dogs, a significant negative relationship (F (1,8) = 9.412, P = 0.015) between animal density and parasite prevalence, and a significant positive relationship (F (1,8) = 7.869, P = 0.023) between parasite prevalence and agricultural land cover, were detected.

Conclusions

The results of this study confirm the red fox as the most important definitive host of E. multilocularis and, consequently, as the main target for control programmes in the Baltic countries. Raccoon dogs seem to play a secondary role in the life-cycle of E. multilocularis within the investigated European region.

Keywords

Echinococcus multilocularis Red fox Raccoon dog Prevalence Zoonosis Latvia Baltic countries

Background

Alveolar echinococcosis (AE) is a human disease caused by the metacestode stage of Echinococcus multilocularis and is of considerable public health importance in Europe due to the severity of the disease, which leads to death in untreated patients [1, 2]. According to the Centre for Disease Prevention and Control of Latvia (www.spkc.gov.lv), 146 human cases of echinococcosis were reported in Latvia since 2000. From 1999 to 2010, 14 out of the 100 recorded echinococcosis cases were identified as AE, a figure which represents 13% of all the registered echinococcosis infections in Latvia [3, 4].

In Europe, E. multilocularis is transmitted predominantly through a wildlife cycle involving primarily the red foxes (Vulpes vulpes) as definitive hosts and rodents of the family Arvicolidae as intermediate hosts [5, 6]. Historically, endemic regions for E. multilocularis in Europe consisted of a ‘core’ area comprising regions of southern Germany, eastern France, north-central Switzerland, and western Austria [6, 7]. Since the 1990s, broad epidemiological studies showed the endemic area of the parasite to include regions of 17 European countries [711] and E. multilocularis has been documented in wildlife from Lithuania [12], Estonia [13] and Latvia [14].

The increase in the number of foxes and the colonization of urban and peri-urban areas have been documented for several European countries [15]. Since synanthropic foxes are reservoir hosts of zoonotic pathogens, it is important to understand the factors influencing the transmission of zoonotic parasites including E. multilocularis [16]. In recent years, foxes colonized 33 of 47 Estonian towns [17] and E. multilocularis was detected in 7.1% of urban foxes [18]. In the city of Riga (capital of Latvia), foxes were mainly recorded in forest parks, meadows, private gardens and on Zakusala island with an increase of their number towards the periphery of the city [19]. Consequently, contamination of the environment with fox faeces could be higher in peri-urban areas and, therefore, these areas hypothetically could be more crucial than rural or highly urbanized areas for parasite transmission [15, 20].

According to the hunting regulations in Latvia, red foxes and raccoon dogs can be hunted all year round with no limitations. The population of raccoon dogs in Latvia is stable, whereas the red fox population has decreased in recent years (State Forest Service, unpublished data).

The aims of the present study were to determine the prevalence of E. multilocularis infection in red foxes and raccoon dogs and to investigate environmental factors associated with the occurrence of the parasite in Latvia.

Methods

Sample collection and parasitological analysis

Animal carcasses were collected from October to January within the Latvian State programme for the Control and Eradication of Rabies. From 2010 to 2014, animals were collected from the entire Latvian territory; whereas in 2014–2015, animals originated from the eastern part of Latvia bordering the Russian Federation and Belarus [21]. A total of 538 and 407 rabies-free red foxes and raccoon dogs, respectively, were included in this study.

For safety reasons, the whole intestine was frozen at −80 °C for 1 week. Adult worms of E. multilocularis were collected by the sedimentation and counting technique using two sieves of 1 mm mesh and 150 μm mesh [22, 23]. Echinococcus multilocularis worms were morphologically identified [24] and preserved in 96% ethanol for further analyses.

Molecular identification

To confirm the morphological identification, 114 worms (82 from red foxes and 32 from raccoon dogs) were tested by molecular analysis according to previously published protocols [25, 26]. Briefly, worms were washed three times in phosphate-buffered saline at pH 7.2 and DNA from individual worms was extracted using the Wizard Magnetic DNA Purification System for Food (Promega, Madison, WI, USA) according to the manufacturer’s instructions. DNA was used as template in a two-step PCR assay. In the first step, DNA from individual worms was amplified using a multiplex-PCR [25] to distinguish E. multilocularis from E. granulosus and from Taenia spp. This multiplex assay was designed to amplify a 395 bp fragment of NADH dehydrogenase subunit 1 (nad1) gene of E. multilocularis and 117 bp and 267 bp of the small subunit of ribosomal RNA (rrnS) gene of E. granulosus and Taenia spp., respectively. All samples were tested in 30 μl amplification reaction mixtures containing primers Cest1, Cest2, Cest3, Cest4 and Cest5 as previously described [25]. In the second step, conventional PCR and sequencing targeting mitochondrial cytochrome c oxidase subunit 1 (cox1) gene were performed on positive amplicons following a previously published protocol [27] with some modifications [26]. This approach was used to confirm species identification. Briefly, the PCR consisted of 38 cycles with a denaturation (30 s at 94 °C), a hybridization (30 s at 55 °C) and an elongation (30 s at 72 °C) step for each cycle. For each PCR reaction, 2 μl of DNA was added to 48 μl of the reaction mixture (GoTaq Master Mix; Promega, Madison, WI, USA), which contained 20 pmol of each primer and 1 unit of Taq polymerase. For the detection of the PCR amplicons, PCR products were separated by capillary electrophoresis (QIAxcel, QIAGEN, Hilden, Germany) using the high resolution kit of the 0 M500 method (QIAGEN, Hilden, Germany). PCR products were purified using a Wizard SV Gel and PCR Clean-Up System (Promega, Madison, WI, USA). Forward and reverse sequencing was carried out on a capillary DNA sequencer ABI PRISM 3100 Genetic Analyzer using the BigDye terminator cycle sequencing kit (Applied Biosystems, Foster City, CA, USA). BLAST algorithm (http://www.ncbi.nlm.nih.gov/BLAST/) was used to compare nucleotide sequences generated in this study with those present on the NCBI database (http://www.ncbi.nlm.nih.gov).

Data analysis

The age group classified as juvenile or adult by the dental wear was known for 377 foxes (75 juveniles, 302 adults) and 263 raccoon dogs (61 juveniles, 202 adults). Since the gender was only determined for very few animals, it was no longer taken into account for the analysis.

The mean annual temperature and mean annual precipitation data were obtained from the Latvian Environment, Geology and Meteorology Centre (www.meteo.lv, on a request). Information on land cover was acquired from the State Forest Service (SFS) (www.vmd.gov.lv, on a request) and Central Statistical Bureau of Latvia (http://www.csp.gov.lv, on a request). The SFS is a surveillance authority inspecting forest management and hunting. It governs a network of local game administrative units and collects annual hunting records (reference period from 1st April to 31st March) from these game units. Animal density was calculated using data of hunted animals per reference period at the scale of game administrative unit territory. Therefore, data on investigated/ infected animals were presented at the same scale.

The prevalence (with 95% confidence interval) of E. multilocularis and the mean intensity of infection were determined. Both Pearson’s and Spearman’s rank correlation tests, Fisher’s exact test, Mann-Whitney U-test and linear regression were used for statistical comparison. Statistical analyses were performed using SPSS Statistics Version 20 [28].

Results

Echinococcus multilocularis was significantly more prevalent in red foxes (17.1%; P < 0.001) (parasite intensity of 1–7,050 worms) than in raccoon dogs (8.1%) (parasite intensity of 1–815 worms) (Table 1). There was a significant positive correlation (r (10) = 0.7952, P = 0.001) between parasite prevalence and intensity of infection for foxes; however, no such correlation was detected for raccoon dogs. The proportion between investigated and hunted animals in the whole territory was about 1% (Additional file 1: Table S1).
Table 1

Prevalence and intensity of Echinococcus multilocularis worms in red foxes and raccoon dogs in Latvia from 2010 to 2015

Year

Red foxes

Raccoon dogs

No. of infected/tested animals

Prevalence (%) (95% CI)

Mean intensity (95% CI)

Intensity range

No. of infected/tested animals

Prevalence (%) (95% CI)

Mean intensity (95% CI)

Intensity range

2010/2011

42/177

23.7 (17.5–30.0)

307.8 (0–636.8)

1–7,050

5/98

5.1 (0.7–9.5)

184.2 (0–493.3)

19–815

2011/2012

18/113

15.9 (9.2–22.7)

172.8 (45.1–300.5)

1–902

8/96

8.3 (2.8–13.7)

34.8 (8–61.5)

6–123

2012/2013

12/58

20.7 (10.3–31.1)

54.7 (0–157.5)

5–317

3/56

5.4 (0–11.3)

28.7 (5.5–51.9)

8–49

2013/2014

5/76

6.6 (1.0–12.2)

117.8 (0–250.8)

2–371

1/56

1.8 (0–5.3)

72

72

2014/2015a

15/114

13.1 (6.9–19.4)

1,020.2 (0–2132.8)

1–6,748

16/101

15.8 (8.7–23.0)

152.6 (5.5–51.9)

1–810

Total

92/538

17.1 (13.9–20.3)

375.1 118–632.2

1–7,050

33/407

8.1 (5.5–10.8)

115.1 (44.8–185.4)

1–815

aIn 2014/2015 material was collected only in eastern Latvia (border territory with Russian Federation and Belarus)

Infected foxes were found to occur across the whole territory of Latvia (Fig. 1, Additional file 1: Table S1). Prevalence did not change significantly between the eastern and western part of Latvia. Infected raccoon dogs were found in all game administrative units except one (Fig. 2, Additional file 1: Table S1). There was no significant correlation between the total number of harvested animals and the infection rate for both species by game administrative units. The linear regression between raccoon dog density and E. multilocularis prevalence showed a significant negative relationship (F (1,8) = 9.412, P = 0.015) (Fig. 3). The same tendency was observed for foxes although it was not statistically significant (F (1,8) = 2.115, P = 0.133) (Fig. 3).
Fig. 1

Echinococcus multilocularis prevalence in foxes of Latvia from 2010 to 2015. Game administrative units: DK, Dienvidkurzeme; ZK, Ziemeļkurzeme; ZE, Zemgale; RR, Rīgas reģionālā; SE, Sēlija; DL, Dienvidlatgale; AL, Austrumlatgale; ZA, Ziemeļaustrumu; CV, Centrālvidzeme; ZV, Ziemeļvidzeme. Numbers indicate positive/tested (%) animals per game administrative unit

Fig. 2

Echinococcus multilocularis prevalence in raccoon dogs of Latvia from 2010 to 2015. Game administrative units: DK, Dienvidkurzeme; ZK, Ziemeļkurzeme; ZE, Zemgale; RR, Rīgas reģionālā; SE, Sēlija; DL, Dienvidlatgale; AL, Austrumlatgale; ZA, Ziemeļaustrumu; CV, Centrālvidzeme; ZV, Ziemeļvidzeme. Numbers indicate positive/tested (%) animals per game administrative unit

Fig. 3

Correlation between the Echinococcus multilocularis prevalence and the animal population density for foxes (a) and raccoon dogs (b)

There was no statistically significant difference between the age of host species and parasite prevalence (Fisher’s exact test), or between the age and parasite intensity (Mann-Whitney U-test).

A temporal fluctuation of E. multilocularis prevalence was observed for both species in the study period (Table 1). In foxes, there was a positive relationship (R s = 0.900, n = 5, P = 0.037) between E. multilocularis prevalence and precipitation and a negative but non-significant relationship (R s = -8.66, n = 5, P = 0.058) between the prevalence and the environmental temperature (Fig. 4). No apparent relationship was observed between prevalence and environmental temperature (R s = 0.296, n = 5, P = 0.628) or prevalence and precipitation (R s = 0.154, n = 5, P = 0.805) for raccoon dogs (Fig. 4).
Fig. 4

Relationship between climate factors and Echinococcus multilocularis prevalence in foxes (a) and raccoon dogs (b)

A negative but non-significant relationship was found between E. multilocularis prevalence in foxes and the amount of forest or agricultural land within each game administrative unit (R 2 = 0.120, F (1,8) = 0.100, P = 0.759 and R 2 = 0.015, F (1,8) = 0.898, P = 0.371, respectively). In raccoon dogs, there was no significant relationship between prevalence and forest cover (R 2 = 0.064, F (1,8) = 0.605, P = 0.459), but a statistically significant positive relationship (R 2 = 0.495, F (1,8) = 7.869, P = 0.023) was detected between prevalence and agricultural land (Fig. 5).
Fig. 5

Relationship between land cover and Echinococcus multilocularis prevalence in foxes (a) and raccoon dogs (b) within each game administrative unit

Echinococcus multilocularis worms were successfully identified in 69 isolates (82.1%). Out of the 15 (17.9%) isolates, which did not show any molecular amplification for E. multilocularis, 10 showed a positive reaction for Taeniidae. In three of these animals, E. multilocularis and Taenia sp. worms were morphologically identified.

Discussion

The prevalence and distribution of E. multilocularis in foxes in Latvia has been investigated since 2003. In the study of Bagrade et al. [14], 16 out of 45 tested animals (35.6%) were infected, and most of the positive foxes originated from western Latvia. Poļakova [29] detected E. multilocularis in 19.1% (n = 42) of foxes collected from only three game administrative units of Latvia. The results of the present study show no significant difference of E. multilocularis prevalence between the eastern and western part of the country. The highest prevalence of E. multilocularis in foxes was detected in three game administrative units, two of which were in the eastern part (DL and AL, Fig. 1) and one in the western part (SE) of Latvia. However, the high prevalence in SE could have been influenced by the small sample size. The 17.1% prevalence of E. multilocularis found in foxes in the present study is lower than in Estonia (29.4%) and significantly lower than in Lithuania (58.7%; P < 0.001). However, the sample size in the studies from Estonia and Lithuania was lower than in the present study, 17 and 269, respectively [13, 30, 31].

Previous studies on E. multilocularis in the raccoon dog population of Latvia showed a prevalence ranging from 5.3% (n = 19, from different regions of the country; [32]) to 14.3% (n = 42, from three game administrative units; [29]). During the current study, E. multilocularis was not detected in raccoon dogs hunted in one game administrative unit (ZV, Fig. 2, Additional file 1: Table S1), although this parasite had been previously reported in this territory [29].

In other European countries (Estonia, Lithuania, Poland and western part of Germany), E. multilocularis prevalence in raccoon dogs ranged from 1.6 to 8.2% [31, 3335]. The present data are in agreement with previous studies and confirm the susceptibility of the raccoon dog to E. multilocularis infection, although its role as a final host of the life-cycle may be of less importance than that of the red fox. The susceptibility of the raccoon dog to E. multilocularis infection has been also confirmed by experimental infections [36]. The feeding behaviour of the raccoon dog may partially explain the lower prevalence and worm intensity detected in this host species. In Denmark, where E. multilocularis was detected in foxes, none of the raccoon dogs examined (n = 99) were infected with E. multilocularis. These data highlight the importance of the feeding behaviour; in fact, amphibian-transmitted parasite species were more prevalent in raccoon dogs than in foxes, in which rodent-transmitted parasites prevailed [37]. In Estonia, a difference between the raccoon dog diet and the fox diet was observed in the cold period of the year, revealing anthropogenic plants and carrions as the most important food sources for raccoon dogs, while foxes consumed significantly more arvicolid rodents [38].

According to Hegglin et al. [39], some raccoon dog behavioural traits could affect the parasite cycle. The use of latrines renders the raccoon dog epidemiologically less important compared to red foxes for transmission and perpetuation of E. multilocularis life-cycle. Moreover, the raccoon dog, as well as other wild canids such as the golden jackal (Canis aureus) and the wolf (Canis lupus), can act as definitive hosts, but there is no evidence that they can maintain the life-cycle of the parasite in the absence of the red fox [40]. Meanwhile, studies from western Germany [34] and Estonia [35] indicate an increasing importance of the raccoon dog as a definitive host, particularly because they are becoming widespread and have well-established populations, and share the same areas with foxes.

In recent years, several biotic and abiotic factors (e.g., landscape change composition and use, fox urbanization, wildlife introduction, changing human behavioural attitudes toward foxes, climate change, and host-parasite population dynamics) were suggested as explanations behind the increasing risk of E. multilocularis transmission [41]. These factors and their interactions change across regions and even between different ecosystems of the same area [16, 42].

The results of this study show a statistically significant negative relationship between raccoon dog density and E. multilocularis prevalence (Fig. 3). This finding may be influenced by the use of latrines, which increase the probability that rodents acquire the infection only in restricted areas, irrespective of the raccoon dog density. In contrast, in eastern France, a positive correlation was found between fox density and E. multilocularis prevalence; indeed, a decreased prevalence was associated with a reduction in fox numbers [43]. According to Karamon et al. [44], an increasing animal population is not always an absolute factor determining a higher prevalence of the parasite.

This study demonstrated a correlation between E. multilocularis prevalence and worm intensity in foxes, i.e., the increased prevalence was associated with an increased worm burden. Several studies revealed that the distribution of E. multilocularis biomass was highly aggregated; therefore, a few highly infected foxes are responsible for most of the environmental egg contamination [15, 45, 46].

No statistically significant age-dependent difference between E. multilocularis prevalence or intensity of infection in either foxes or raccoon dogs was detected. However, the age was known only for a small number of animals in our study.

In Latvia, a strong west-east gradient characterizes both the continental climate and the distribution of precipitation, and a south-north configuration of uplands and lowlands plays an important role in climate differentiation when moving away from the sea to the inland [47]. Comparing the fluctuation of E. multilocularis prevalence with climate factors in Latvia, results showed a slight tendency towards an increase in E. multilocularis prevalence in the fox population in the years characterised by lower temperatures and higher precipitation (Fig. 4). Interestingly, when the parasite prevalence in the fox population was increasing, the opposite tendency was observed in the raccoon dog population and vice versa. The only exception was during 2013/2014 period, when a dramatic decrease in E. multilocularis prevalence was observed in both host species. The temporal fluctuation of E. multilocularis prevalence in raccoon dogs could be related to sampling bias (more animals sampled from a single clan) influenced by animal behavioural traits (use of latrines). The effect of climate on the prevalence and burden of E. multilocularis was shown in a long-term study in Slovakia, where the highest parasite prevalence in foxes was detected in the years with a lower mean annual air temperature and a higher mean annual rainfall [4850]. Mean annual temperature and annual precipitations were also noted as the major determinants of the spatial distribution of E. multilocularis in Hungary [51]. However, studies in Poland did not show a strict correlation between the annual rainfall and the parasite prevalence [44].

In the present study, the comparison between parasite prevalence in foxes and raccoon dogs with land cover (forest and agricultural land) showed a statistically significant difference only for the raccoon dog and agricultural land (Fig. 5). In Poland, a weak negative correlation was detected between E. multilocularis prevalence in foxes and agricultural land, and a positive correlation between E. multilocularis prevalence in foxes and forest cover [44].

Echinococcus multilocularis has been recorded in wolves from Latvia in 2003 [52]. In the Ziemeļkurzeme game administrative unit, one of the areas with the highest parasite prevalence in the fox population, E. multilocularis was detected in all three canid species (fox, raccoon dog and wolf). This might suggest that environmental conditions within this area favour the E. multilocularis life-cycle.

Conclusions

The significant difference in the prevalence of E. multilocularis between foxes and raccoon dogs, found in this study, is in agreement with other studies carried out within the Baltic region [31]. The significant correlation between parasite prevalence and the intensity of infection in foxes recorded here provides strong evidence to the role of the red fox in the contamination of the environment with E. multilocularis eggs. However, the importance of the raccoon dog as a definitive host, as suggested by other studies [34, 35], should not be underestimated in the presence of a stable fox population and a high E. multilocularis prevalence.

Abbreviations

AE: 

Alveolar echinococcosis

cox1: 

Cytochrome c oxidase subunit 1

nad1: 

NADH dehydrogenase subunit 1

rrnS: 

Small subunit of ribosomal RNA

SFS: 

State Forest Service

Declarations

Acknowledgements

We would like to thank the hunters for their cooperation and positive attitude toward studying sylvatic carnivore parasites. We would like also to express our gratitude to Mārtiņš Lūkins for helping us create the maps. We also thank personnel of the World Health Organization Collaborating Centre for epidemiology, detection and control of cystic and alveolar echinococcosis, Rome, Italy for their scientific support.

Funding

This research received in part funding from the European Community's Seventh Framework Programme under the grant agreement 602051, project HERACLES: Human cystic Echinococcosis ReseArch in CentraL and Eastern Societies; http://www.heracles-fp7.eu/. The funding body had no involvement in the conseption, preparation and writing of the manuscript.

Molecular identification of the parasites was in part funded by the DG SANTE of the European Commission.

Availability of data and material

The datasets supporting the conclusions of this article are included within the article and its additional file.

Authors’ contributions

GB generated and analysed parasitological data and wrote the manuscript; GD coordinated the collection of foxes and raccoon dogs, generated parasitological data and contributed to the manuscript; ZO generated parasitological data and contributed to the manuscript; SJH carried out the statistical analyses and contributed to the manuscript; MI generated molecular data; AC analysed molecular data and contributed to the manuscript; EP critically revised the manuscript. All authors read and approved the final version of the manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Latvian State Forest Research Institute “Silava”
(2)
Institute of Food Safety, Animal Health and Environment “BIOR”
(3)
Istituto Superiore di Sanità
(4)
WHO Collaborating Centre for the epidemiology, detection and control of cystic and alveolar echinococcosis, ISS

References

  1. Pawlowski ZS, Eckert J, Vuitton DA, Ammann RW, Kern P, Craig PS, et al. Echinococcosis in humans: clinical aspects, diagnosis and treatment. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, editors. WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. Paris: World Health Organization; 2001. p. 20–71.Google Scholar
  2. Kern P. Report of the WHO Informal Working Group on cystic and alveolar echinococcosis surveillance, prevention and control, with the participation of the Food and Agriculture Organization of the United Nations and the World Organisation for Animal Health. Geneva: World Health Organization; 2011. p. 1–3.Google Scholar
  3. Keiss J, Sondore V, Cernusenko A, Viksna L, Rozentale B. Current trends in echinococcosis in Latvia. The 17th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID) & 25th International Congress of Chemotherapy (ICC), Conference Proceedings. 2007. p. 122–3.Google Scholar
  4. Laivacuma S, Vīksne L. Case analyzes of alveolar echinococossis. Riga Stradins University Scientific Conference 2014, Abstracts. 2014. p. 184.Google Scholar
  5. Thompson RCA, McManus DP. Aetiology: parasites and life-cycles. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, editors. WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. Paris: World Health Organization; 2001. p. 1–19.Google Scholar
  6. Romig T. Spread of Echinococcus multilocularis in Europe? In: Craig P, Pawlowski Z, editors. Cestode zoonoses: echinococcosis and cysticercosis. An emergent and global problem. Amsterdam: Ios Press; 2002. p. 65–80.Google Scholar
  7. Romig T, Dinkel A, Mackensted U. The present situation of echinococcosis in Europe. Parasitol Int. 2006;55:187–91.View ArticleGoogle Scholar
  8. Eckert J, Schantz PM, Gasser RB, Torgerson PR, Bessonov AS, Movsessian SO, et al. Geographic distribution and prevalence. In: Eckert J, Gemmell MA, Meslin FX, Pawlowski ZS, editors. WHO/OIE Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern. Paris: World Health Organization; 2001. p. 100–42.Google Scholar
  9. Sikó SB, Deplazes P, Cozma V, Pop S, Tivadar C, Bogolin I, Popescu R. Echinococcus multilocularis confirmed in Romania. Sci Parasitol. 2010;11(2):89–96.Google Scholar
  10. Osterman Lind E, Juremalm M, Christensson D, Widgren S, Hallgren G, Agren EO, et al. First detection of Echinococcus multilocularis in Sweden, February to March 2011. Euro Surveill. 2011;16(14):19836.PubMedGoogle Scholar
  11. Davidson RK, Romig T, Jenkins E, Tryland M, Robertson LJ. The impact of globalisation on the distribution of Echinococcus multilocularis. Trends Parasitol. 2012;28(6):239–47.View ArticlePubMedGoogle Scholar
  12. Mažeika V, Paulauskas A, Balčiauskas L. New data on the helminth fauna of rodents of Lithuania. Acta Zool Litu. 2003;13:41–7.View ArticleGoogle Scholar
  13. Moks E, Saarma U, Valdmann H. Echinococcus multilocularis in Estonia. Emerg Infect Dis. 2005;11:1973–4.View ArticlePubMed CentralPubMedGoogle Scholar
  14. Bagrade G, Šnábel V, Romig T, Ozoliņš J, Hüttner M, Miterpáková M, et al. Echinococcus multilocularis is a frequent parasite of red foxes (Vulpes vulpes) in Latvia. Helminthologia. 2008;45(4):157–61.View ArticleGoogle Scholar
  15. Deplazes P, Hegglin D, Gloor S, Romig T. Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends Parasitol. 2004;20:77–84.View ArticlePubMedGoogle Scholar
  16. Mackenstedt U, Jenkins D, Romig T. The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. Int J Parasitol Parasites Wildl. 2015;4:71–9.View ArticlePubMed CentralPubMedGoogle Scholar
  17. Plumer L, Davison J, Saarma U. Rapid urbanization of red foxes in Estonia: distribution, behaviour, attacks on domestic animals, and health-risks related to zoonotic diseases. PLoS One. 2014;9(12):e115124.View ArticlePubMed CentralPubMedGoogle Scholar
  18. Laurimaa L, Davison J, Plumer L, Süld K, Oja R, Moks E, et al. Noninvasive detection of Echinococcus multilocularis tapeworm in urban area, Estonia. Emerg Infect Dis. 2015;21(1):163–4.View ArticlePubMed CentralPubMedGoogle Scholar
  19. Zorenko T, Leontyeva T. Species diversity and distribution of mammals in Riga. Acta Zool Litu. 2003;13(1):78–86.View ArticleGoogle Scholar
  20. Liccioli S, Giraudoux P, Deplazes P, Massolo A. Wilderness in the ‘city’ revisited: different urbes shape transmission of Echinococcus multilocularis by altering predator and prey communities. Trends Parasitol. 2015;31(7):297–305.View ArticlePubMedGoogle Scholar
  21. State Monitoring plan of animal infectious diseases (in Latvian). Food and Veterinary Service. Riga: Ministry of Agriculture; 2014. p. 43.Google Scholar
  22. Miterpáková M, Hurníková Z, Antolová D, Dubinský P. Endoparasites of red fox (Vulpes vulpes) in the Slovak Republic with the emphasis on zoonotic species Echinococcus multilocularis and Trichinella spp. Helminthologia. 2009;46(2):73–9.View ArticleGoogle Scholar
  23. Gesy K, Pawlik M, Kapronczai L, Wagner B, Elkin B, Schwantje H, Jenkins E. An improved method for the extraction and quantification of adult Echinococcus from wildlife definitive hosts. Parasitol Res. 2013;112:2075–8.View ArticlePubMedGoogle Scholar
  24. Rausch RL. Family Taeniidae. In: Khalil LF, Jones A, Bray RA, editors. Keys to the cestode parasites of vertebrates. Wallingford: CAB International; 1994. p. 665–72.Google Scholar
  25. Trachsel D, Deplazes P, Mathis A. Identification of taeniid eggs in the faeces from carnivores based on multiplex PCR using targets in mitochondrial DNA. Parasitology. 2007;134(6):911–20.View ArticlePubMedGoogle Scholar
  26. Casulli A, Interisano M, Sreter T, Chitimia L, Kirkova Z, La Rosa G, Pozio E. Genetic variability of Echinococcus granulosus sensu stricto in Europe inferred by mitochondrial DNA sequences. Infect Genet Evol. 2012;12(2):377–83.View ArticlePubMedGoogle Scholar
  27. Bowles J, Blair D, McManus DP. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol Biochem Parasitol. 1992;54(2):165–73.View ArticlePubMedGoogle Scholar
  28. IBM Corp. IBM SPSS Statistics for Window, Version 20.0. Armonk: IBM Corp; 2011.Google Scholar
  29. Poļakova A. Fox (Vulpes vulpes) and raccoon dog (Nyctereutes procyonoides) helminth fauna in Latvia. MSc degree thesis (in Latvian). Jelgava: Latvia University of Agriculture; 2009. p. 81.Google Scholar
  30. Sarkūnas M, Bružinskaitė R, Marcinkutė A, Strupas K, Sokolovas V, Mathis A, Deplazes P. Emerging alveolar echinococcosis (AE) in humans and high prevalence of Echinococcus multilocularis in foxes and raccoon dogs in Lithuania. Acta Vet Scan. 2010;52 Suppl 1:S11.View ArticleGoogle Scholar
  31. Bružinskaitė-Schmidhalter R, Šarkūnas M, Malakauskas A, Mathis A, Torgerson P, Deplazes P. Helminths of red foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in Lithuania. Parasitology. 2012;139:120–7.View ArticlePubMedGoogle Scholar
  32. Bagrade G. Helminth fauna of wild felids and canids in Latvia. PhD thesis (in Latvian with summary in English). Riga: University of Latvia; 2008. p. 128.Google Scholar
  33. Machnicka-Rowińska B, Rocki B, Dziemian E. Kołodziej-Sobocińska M Raccoon dog (Nyctereutes procyonoides) - the new host of Echinococcus multilocularis in Poland. Wiad Parazytol. 2002;48(1):65–8.Google Scholar
  34. Schwarz S, Sutor A, Staubach C, Mattis R, Tackmann K, Conraths FJ. Estimated prevalence of Echinococcus multilocularis in raccoon dogs Nyctereutes procyonoides in northern Brandenburg, Germany. Curr Zool. 2011;57:655–61.View ArticleGoogle Scholar
  35. Laurimaa L, Süld K, Moks E, Valdmann H, Umhang G, Knapp J, Saarma U. First report of the zoonotic tapeworm Echinococcus multilocularis in raccoon dogs in Estonia, and comparisons with other countries in Europe. Vet Parasitol. 2015;212:200–5.View ArticlePubMedGoogle Scholar
  36. Thomson RCA, Kapel CMO, Hobbs RP, Deplazes P. Comparative development of Echinococcus multilocularis in its definitive hosts. Parasitology. 2006;132(Pt 5):709–16.Google Scholar
  37. Al-Sabi MNS, Chriel M, Jensen TH, Enemark HL. Endoparasites of the raccoon dog (Nyctereutes procyonoides) and the red fox (Vulpes vulpes) in Denmark 2009–2012 - A comparative study. Int J Parasitol Parasites Wildl. 2013;2:144–51.Google Scholar
  38. Süld K, Valdman H, Laurimaa L, Soe E, Davison J, Saarma U. An invasive vector of zoonotic disease sustained by anthropogenic resources: the raccoon dog in northern Europe. PLoS One. 2014;9(5):e96358.View ArticlePubMed CentralPubMedGoogle Scholar
  39. Hegglin D, Bontadina F, Deplazes P. Human-wildlife interactions and zoonotic transmission of Echinococcus multilocularis. Trends Parasitol. 2015;31(5):167–73.Google Scholar
  40. EFSA AHAW Panel (EFSA Panel on Animal Health and Welfare). Scientific opinion on Echinococcus multilocularis infection in animals. EFSA J. 2015;13(12):4373. 129 pp.View ArticleGoogle Scholar
  41. Casulli A, Possenti A, La Torre G, Boue F, Busani L, Colamensta V, et al. Echinococcus multilocularis infection in animals (GP/EFSA/AHAW/2012/01). EFSA supporting publication. EN-882. 2015. p. 168.Google Scholar
  42. Otero-Abad B, Torgerson PR. A systematic review of the epidemiology of echinococcosis in domestic and wild animals. PLoS Negl Trop Dis. 2013;7(6):e2249.View ArticlePubMed CentralPubMedGoogle Scholar
  43. Raoul F, Michelat D, Ordinaire M, Décoté Y, Aubert M, Delattre P, et al. Echinococcus multilocularis: secondary poisoning of fox population during a vole outbreak reduces environmental contamination in a high endemicity area. Int J Parasitol. 2003;33:945–54.View ArticlePubMedGoogle Scholar
  44. Karamon J, Kochanowski M, Sroka J, Cencek T, Różycki M, Chmurzyńska E, Bilska-Zając E. The prevalence of Echinococcus multilocularis in red foxes in Poland - current results (2009–2013). Parasitol Res. 2014;113:317–22.View ArticlePubMedGoogle Scholar
  45. Hofer S, Gloor S, Muller U, Mathis A, Hegglin D, Deplazes P. High prevalence of Echinococcus multilocularis in urban red foxes (Vulpes vulpes) and voles (Arvicola terrestris) in the city of Zurich, Switzerland. Parasitology. 2000;120:135–42.View ArticlePubMedGoogle Scholar
  46. Fischer C, Reperant LA, Weber JM, Hegglin D, Deplazes P. Echinococcus multlocularis infections of rural, residential and urban foxes (Vulpes vulpes) in the canton of Geneva, Switzerland. Parasite. 2005;12:339–46.View ArticlePubMedGoogle Scholar
  47. Laiviņš M, Melecis V. Bio-geographical interpretation of climate data in Latvia: multidimensional analysis. Acta Uni Lat. 2003;654:7–22.Google Scholar
  48. Miterpáková M, Dubinský P, Reiterová K, Stanko M. Climate and environmental factors influencing Echinococcus multilocularis occurrence in the Slovak Republic. Ann Agr Environ Med. 2006;13:235–42.Google Scholar
  49. Miterpáková M, Dubinský P. Fox tapeworm (Echinococcus multilocularis) in Slovakia – summarizing the long-term monitoring. Helminthologia. 2011;48(3):155–61.View ArticleGoogle Scholar
  50. Antolova D, Miterpakova M, Radoňak J, Hudačkova D, Szilagyiova M, Zače M. Alveolar echinococcosis in a highly endemic area of northern Slovakia between 2000 and 2013. Euro Surveill. 2014;19(34):20882.View ArticlePubMedGoogle Scholar
  51. Tolnai Z, Széll Z, Sréter T. Environmental determinants of the spatial distribution of Echinococcus multilocularis in Hungary. Vet Parasitol. 2013;198:292–7.View ArticlePubMedGoogle Scholar
  52. Bagrade G, Kirjušina M, Vismanis K, Ozoliņš J. Helminth parasites of the wolf Canis lupus from Latvia. J Helminthol. 2009;83:63–8.View ArticlePubMedGoogle Scholar

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