Westward spread of Echinococcus multilocularis in Foxes, France, 2005-2010.
Subject: Zoonoses
Food contamination
Authors: Combes, Benoit
Comte, Sebastien
Raton, Vincent
Raoul, Francis
Boue, Franck
Umhang, Gerald
Favier, Stephanie
Dunoyer, Charlotte
Woronoff, Natacha
Giraudoux, Patrick
Pub Date: 12/01/2012
Publication: Name: Emerging Infectious Diseases Publisher: U.S. National Center for Infectious Diseases Audience: Academic; Professional Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2012 U.S. National Center for Infectious Diseases ISSN: 1080-6040
Issue: Date: Dec, 2012 Source Volume: 18 Source Issue: 12
Accession Number: 313345663
Full Text: Echinococcus multilocularis is the causative agent of the parasitic zoonosis alveolar echinococcosis. The adult stage of this cestode is found mostly in the digestive tract of the red fox (Vulpes vulpes) (1). Parasite eggs, expelled in feces, are the only external living stage of the parasite life cycle. Once ingested by small mammals, they migrate to the liver and proliferate, forming protoscolices in multivesicular cysts. The life cycle is completed when a definitive host (usually canid) preys on an infected intermediate host (mostly rodent). Epidemiologic studies indicate that humans can be infected by eating raw vegetables contaminated by infected fox or dog feces or by direct contact with an infected fox or dog (2). Despite the low incidence of human alveolar echinococcosis in Europe (0.02-0.18 cases/100,000 inhabitants [3]) the zoonotic potential of the fox tapeworm, in terms of persistence and pathogenicity, poses a major parasitic threat to human health in nontropical regions (4).

Three main trends have been reported in the past decade in Europe. First, E. multilocularis prevalence has increased in foxes within areas to which it is known to be endemic (5), seemingly linked with the increase of fox population densities in Germany and Switzerland (6). Second, the geographic distribution of E. multilocularis in foxes has extended toward southern, northern, and eastern countries where it had not previously been detected; the most recent are northern Italy (7); Svalbard, Norway (8); and Sweden in 2011 (9). Third, the geographic distribution of echinococcosis has extended toward Russia and neighboring countries (10), including the Baltic states.

Until now, the eastern part of the French territory was considered the western limit of the European echinococcosis-endemic area. At the end of the 1990s, E. multilocularis in foxes was reported in only 10 of the 95 French departments (Figure 1). Studies conducted in the neighboring departments (departments 08, 21, 38, 52, 69, and 74) by sedimentation and counting technique (11) did not detect infection in foxes. However, since 1997, new cases of human echinococcosis have been recorded in areas without known infection of local fox populations (departments 01, 03, 07, 08, 12, 21, 23, 31, 35, 61, 44, 59, 61, 76, and 95) (2).

We present the results of a large-scale survey of E. multilocularis infection in foxes in France. Our study was conducted in 42 departments covering an area of 239,178 [km.sup.2] representing almost all of northeastern France.

The Study

During 2005-2010 (time span needed to cover the study area) and during the months more favorable for infection (October-April [3]), foxes were either shot at night or trapped. The sampling size was chosen to collect [approximately equals] 100 foxes from each department. Therefore, a grid of 5 km x 5 km to 10 km x 10 km, depending on the department size, was superimposed over the sampling area, and no more than 1 fox was collected in each square. The geographic district where the sample was taken was then noted, and each fox was randomly allocated geographic coordinates within the commune (a French administrative division of 10-100 [km.sup.2]).

Adult E. multilocularis worms were identified in departmental veterinary laboratories. Staff were trained by the Anses-Nancy laboratory (National Reference Laboratory for echinococcoses); that laboratory also confirmed any unrecognized specimens. For time- and cost-effectiveness during the analysis, we used the segmental and sedimentation counting technique (12).

We used the [chi square] test to compare E. multilocularis prevalence between departments. The distribution of E. multilocularis prevalence in foxes was modeled against geographic coordinates by using a generalized additive model with a logistic link function and a thin plate regression spline on 300 knots (13). Analyses and graphic displays were conducted by using ArcGIS 9.3, R 2.14.0 and the R packages maptools 0.8-10, mgcv 1.7-12, sp. 0.9-91, and splancs 2.01-29.


A total of 3,307 foxes were collected (Table 1). Eighty-five could not be assigned a commune code and were not kept for further analysis, except to compute E. multilocularis prevalence in departments. The mean number of foxes collected by department was 84.95 ([+ or -] SD 25.76), which represents a mean of 1.56 foxes per 100 km2 ([+ or -] SD 0.57). For 4 departments, (36, 61, 67, and 69), full sampling could not be completed because of technical and/or administrative reasons. Urban areas, such as departments 93, 95, and 91, also were undersampled because of human population density and high urbanization, all factors preventing easy fox sampling.


We confirmed E. multilocularis in foxes in 35 departments (Figure 2). The prevalence varied widely among departments, from 0 (95% CI 0-5%) to 54% (95% CI 42%-64%) (Table 1) but was locally higher in some areas (Figure 2). The mean prevalence in the entire studied area was 17% (n = 3,307; 95% CI 16%-19%). The prevalence in the historically echinococcosis-endemic area was 41% (n = 789; 95% CI 37%-44%) and represented >55% of all infected foxes and <21% of the total area studied. Furthermore, in comparing our results with those of earlier similar studies during the same season with the same technique, we detected a significant increase of E. multilocularis prevalence in foxes over time in most of these departments (Table 2).


Our study confirms the presence of E. multilocularis in areas where it is known to be endemic and indicates its presence in 25 additional departments. However, we cannot discard the possibility that E. multilocularis was present but remained undetected during the 1980s-1990s. That E. multilocularis could have remained undetected if it were not already at a very low prevalence in general is doubtful. Isolated human cases recorded in the early 2000s outside areas to which it is known to be endemic corroborate this possibility (3). The same uncertainty applies in other parts of Europe (14). Taken as a whole, these findings indicate that the transmission intensity of E. multilocularis through fox populations in the occidental part of the European focus area is likely to have increased during the late 1990s and led to a much higher average prevalence than previously reported. Furthermore, infected foxes close to large-scale conurbations, such as Paris and its large suburban surrounding departments (93, 91, and 77) (Figure 1) amounting to 11,728,240 inhabitants, may create new conditions for human exposure similar to those already described in other highly urbanized cities, such as in Switzerland, Germany, and eastern France (Nancy), but on a much larger scale.

We believe that the public needs to be proactively informed and protected, including through awareness initiatives among urban residents and, in specific areas (15), more direct action toward the parasite may be considered. Monitoring the possible further extension of the parasite westward and southward and the evolution of prevalence in foxes in the historically and the newly echinococcosisendemic areas also are essential.


We thank the wildlife and game associations for the fox sampling and the departmental veterinary laboratories for the analyses of fox intestines.

Dr Combes is head of the Entente for the Control of Zoonoses, Nancy, France. His research interests include epidemiologic surveillance and control of zoonoses.

DOI: 10.3201/eid1812.120219

Author affiliations: Entente for the Control of Zoonoses, Nancy, France (B. Combes, S. Comte, V. Raton, S. Favier); University of Franche-Comte/National Center for Scientific Research, Besancon, France (F. Raoul, P. Giraudoux); Institut Universitaire de France, Paris, France (P. Giraudoux); French Agency for Food, Environmental and Occupational Health and Safety, Nancy (F. Boue, G. Umhang); National Game Federation, Issy-lesMoulineaux, France (C. Dunoyer); and Departmental Veterinary Laboratories Manager Association, Besancon (N. Woronoff)


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Benott Combes, [1] Sebastien Comte, Vincent Raton, Francis Raoul, Franck Boue, Gerald Umhang, Stephanie Favier, Charlotte Dunoyer, Natacha Woronoff, and Patrick Giraudoux [1]

[1] These authors contributed equally to this article.

Address for correspondence: Patrick Giraudoux, Chrono-environment, University of Franche-Comte, place Leclerc, 25030 Besancon Cedex, France; email: patrick.giraudoux@univ-fcomte.fr
Table 1. Fox prevalence by department, France,

Department              Total no.
no., name               no., name

01-Ain                      98
02-Aisne                    89
08-Ardennes                 91
10-Aube                     99
14-Calvados                 96
15-Cantal *                 97
18-Cher                     74
21-Cote d'Or                72
25-Doubs *                 113
27-Eure                     93
28-Eure et Loire            42
36-Indre                    52
38-Isere                    89
39-Jura *                  102
41-Loire et Cher            86
42-Loire                    97
45-Loiret                  100
50-Manche                   81
51-Marne                   103
52-Haute Marne              94
54-Meurthe                  84
et Moselle *
55-Meuse *                 104
57-Moselle *               103
58-Nievre                  110
59-Nord                     96
60-Oise                     87
61-Orne                     55
62-Pas de Calais            90
67-Bas Rhin *               7
69-Rhone                    48
70-Haute Saone *            81
71-Saone et Loire           79
73-Savoie                   75
74-Haute Savoie *           73
77-Seine et Marne           55
80-Somme                    89
88-Vosges                   90
89-Yonne                    97
90-Territoire               25
de Belfort *
91-Essonne ([dagger])       41
93-Seine                    6
Saint Denis ([dagger])
95-Val d'Oiset              44
Historical                 789
endemic area
Total                      3307

Department              Prevalence, %
no., name               (95% CI)

01-Ain                  20 (13-30)
02-Aisne                20 (13-30)
08-Ardennes             36 (27-47)
10-Aube                 12 (7-21)
14-Calvados             14 (8-22)
15-Cantal *              9 (5-17)
18-Cher                  1 (0-8)
21-Cote d'Or            21 (12-32)
25-Doubs *              53 (44-62)
27-Eure                  0 (0-5)
28-Eure et Loire         0 (0-10)
36-Indre                 0 (0-9)
38-Isere                 1 (0-7)
39-Jura *               52 (42-62)
41-Loire et Cher         2 (0-9)
42-Loire                 1 (0-6)
45-Loiret                0 (0-5)
50-Manche               15 (8-25)
51-Marne                19 (13-29)
52-Haute Marne          14 (8-23)
54-Meurthe              54 (42-64)
et Moselle *
55-Meuse *              41 (32-51)
57-Moselle *            34 (25-44)
58-Nievre                1 (0-6)
59-Nord                 20 (13-29)
60-Oise                  7 (3-15)
61-Orne                  4 (1-14)
62-Pas de Calais         0 (0-5)
67-Bas Rhin *           29 (5-70)
69-Rhone                 8 (3-21)
70-Haute Saone *        36 (26-47)
71-Saone et Loire        9 (4-18)
73-Savoie               11 (5-20)
74-Haute Savoie *       49 (38-61)
77-Seine et Marne       29 (18-43)
80-Somme                 8 (3-16)
88-Vosges               24 (16-35)
89-Yonne                 0 (0-5)
90-Territoire           32 (16-54)
de Belfort *
91-Essonne ([dagger])    7 (2-21)
93-Seine                17 (1-64)
Saint Denis ([dagger])
95-Val d'Oiset           0 (0-10)
Historical              41 (35-41)
endemic area
Total                   17 (16-19)

Department              Density of collected
no., name               foxes, no./100 [km.sup.2]

01-Ain                     1.7
02-Aisne                   1.22
08-Ardennes                1.85
10-Aube                    1.68
14-Calvados                1.73
15-Cantal *                1.68
18-Cher                    1.55
21-Cote d'Or               0.85
25-Doubs *                 2.21
27-Eure                    1.66
28-Eure et Loire           0.97
36-Indre                   1.03
38-Isere                   1.2
39-Jura *                  2.02
41-Loire et Cher           1.47
42-Loire                   2.06
45-Loiret                  1.53
50-Manche                  1.35
51-Marne                   1.26
52-Haute Marne             1.51
54-Meurthe                 1.8
et Moselle *
55-Meuse *                 1.67
57-Moselle *               1.65
58-Nievre                  1.74
59-Nord                    1.74
60-Oise                    1.53
61-Orne                    0.93
62-Pas de Calais           1.34
67-Bas Rhin *              0.44
69-Rhone                   1.69
70-Haute Saone *           1.54
71-Saone et Loire          1.13
73-Savoie                  1.26
74-Haute Savoie *          1.76
77-Seine et Marne           1
80-Somme                   1.68
88-Vosges                  1.7
89-Yonne                   1.75
90-Territoire              4.09
de Belfort *
91-Essonne ([dagger])      2.37
93-Seine                   2.53
Saint Denis ([dagger])
95-Val d'Oiset             3.59
Historical                 1.56
endemic area
Total                      1.38

* Department belonging to the historically echinococcosis-endemic

([dagger]) Department of the Paris capital conurbation (Figure 1).

Table 2. Changes in fox prevalence over time, France

Department   Total no. foxes collected

            1984-1987    2006-2010
54/57          153          187
39             146          102
25              37          116
67             192          21

Department       Prevalence, %

            1984-1987    2006-2010
54/57           28          43
39              18          52
25              46          52
67              4           19


            p value *
54/57          0.05
39            0.0002
25             0.85
67             0.04

* p value of the [chi square] comparing the 2 periods.
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