Infection of red foxes with Echinococcus multilocularis in western Switzerland

Abstract

In the Jura mountains, Plateau and Alps of western Switzerland important variations in the prevalence of Echinococcus multilocularis infection in red foxes were observed between geographical areas from 1990 to 1995. The Jura mountains and the Plateau had higher mean prevalence levels than the Alps with 30.6, 32.4 and 18.8%, respectively. The highest rate was recorded in the Plateau in the canton of Fribourg with a prevalence of 52.3%. The prevalence of E. multilocularis infection in foxes in the alpine canton of Valais was the lowest (7.1%). Juvenile foxes were found to be more susceptible to E. multilocularis than adults. Adult foxes were less heavily infected in summer and autumn, while the prevalence in juveniles (less than 1 year old) increased between the spring and winter, when they are more than 6 months old. The retrospective data relate to the beginning of the 1990s, since when a drastic prevalence increase of E. multilocularis infection in foxes has occurred in several regions of Europe. Nevertheless, the study is a major contribution to the epidemiological situation of E. multilocularis in central Europe, in that it contains valuable information on spatial distribution and seasonal differences in different age groups of foxes.

Full text

Infection of red foxes with Echinococcus
multilocularis in western Switzerland
M. Brossard*, C. Andreutti and M. Siegenthale r
Institute of Zoology, 11 Rue Emile Argand, CH-2007 Neucha
ˆ
tel,
Switzerland
Abstract
In the Jura mountains, Plateau and Alps of western Switzerland important
variations in the prevalence of Echinococcus multilocularis infection in red foxes
were observed between geographical areas from 1990 to 1995. The Jura
mountains and the Plateau had higher mean prevalence levels than the Alps
with 30.6, 32.4 and 18.8%, respectively. The highest rate was recorded in the
Plateau in the canton of Fribourg with a prevalence of 52.3%. The prevalence of
E. multilocularis infection in foxes in the alpine canton of Valais was the lowest
(7.1%). Juvenile foxes were found to be more susceptible to E. multilocularis than
adults. Adult foxes were less heavily infected in summer and autumn, while the
prevalence in juveniles (less than 1 year old) increased between the spring and
winter, when they are more than 6 months old. The retrospective data relate
to the beginning of the 1990s, since when a drastic prevalence increase of
E. multilocularis infection in foxes has occurred in several regions of Europe.
Nevertheless, the study is a major contribution to the epidemiological situation
of E. multilocularis in central Europe, in that it contains valuable information on
spatial distribution and seasonal differences in different age groups of foxes.
Introduction
Human alveolar echinococcosis has a widespread
distribution in the northern hemisphere including
Switzerland (Gottstein et al., 1987) and other parts of
central Europe (Eckert, 1996). In the vicinity of Switzer-
land, alveolar echinococcosis has been observed in
Austria (Auer & Aspock, 1991), northern Italy (Casulli
et al., 2005), Germany (Daugschies, 1995) and France
(Massif Central, Savoie and Franche-Comte
´
) (Petavy et al.,
1991). The incidence of human alveolar echinococcosis is
low in the European endemic area with 0.02–1.4 new
cases per year for 100,000 inhabitants (Eckert, 1996). The
causative agent of human alveolar echinococcosis is the
larval stage of Echinococcus multilocularis (Leuckart)
(Cestoda: Cyclophyllidea: Taeniidae). Humans are an
aberrant intermediate host, with the disease causing liver
pathology. Natural intermediate hosts are wild rodents.
The water vole Arvicola terrestris and the common vole
Microtus arvalis have been found to be infected in
Switzerland (Gottstein et al., 1996). The red fox Vulpes
vulpes is the most important final host, with between 1
and 50% of animals infected (Auer & Aspock, 1991).
Domestic dogs and cats rarely harbour the adult parasite
(mostly , 1%) in Europe, but dogs are frequently
infected in other endemic areas such as China (Budke &
Campos-Ponce, 2005). Because the parasite is a severe
human pathogen, it is important to evaluate and to
characterize the infection of red foxes in Switzerland. In
the eastern part of the country, between 5 and 50% of
foxes were reported to be infected with E. multilocularis
(Ewald et al., 1992).
The aim of the present study is to define the preva-
lence of E. multilocularis in red foxes in the cantons of
Soleure, Berne, Jura, Neucha
ˆ
tel, Fribourg, Vaud and
Valais (western Switzerland), and to study differences in
prevalence between the Jura mountains (mean altitude of
700 m), the Plateau (mean altitude of 600 m) and the
Alpine areas of these cantons (mean altitude of 1700 m).
Variations of prevalence and intensity of infection with
age and gender of the fox, in addition to seasonal patterns
of infection, are described.
*Author for correspondence
Fax: (41) 32 718 30 01
E-mail: michel.brossard@unine.ch
Published in Journal of Helminthology 81, 369-376, 2007
which should be used for any reference to this work
1

Material and methods
Between October 1990 and May 1995, 3793 red foxes
originating from the cantons of Jura, Berne, Soleure,
Neucha
ˆ
tel, Vaud, Fribourg and Valais were examined for
E. multilocularis infection. Most of them (n ¼ 3020) were
supplied by the Swiss Centre for Rabies, Bern. The
remainder were provided by the Institute Galli-Valerio,
Lausanne (n ¼ 707) or the Institute of Zoology of the
University of Neucha
ˆ
tel (n ¼ 66). The small intestine of
each fox was carefully examined for E. multilocularis as
described by Ewald et al. (1992). The small intestine (or
the whole fox as necessary) was deep frozen at 2 808C for
at least one week to kill the eggs. Diagnosis was achieved
by microscopic examination at a 12 £ magnification of 15
samples of mucosa which were cut off with microscope
slides and prepared in thin layers in Petri dishes. The total
length of strobila (1.2– 4.5 mm), the form of uterus (sac-
like), the position of the genital pore (anterior to middle)
and the number of proglottids (2–6) were used as criteria
for identification (Thompson, 1986).
The intensity of infection was defined as the number
of E. multilocularis adults in each infected fox according
to Margolis et al. (1982). Practically, positive foxes were
classified into three classes, namely 1, less than 100
E. multilocularis adult worms; 2, from 100 to 1000 worms;
and 3, over 1000 worms.
The age, sex and location where foxes were collected
were recorded. Fox age, supplied by the Swiss Centre for
Rabies, was estimated by X-ray examination of the teeth
to measure the relative breadth of the canine cavity
(Kappeler, 1985). Foxes were categorized into two age
groups, i.e. juveniles, less than one year old, and adults,
more than one year old.
Statistical analysis
Calculation of 95% confidence intervals (CI) of preva-
lence was performed as described by Newcomb (2004).
Pearson’s
x
2
test was used to compare the intensity and
the prevalence of E. multilocularis infection between
geographical areas of western Switzerland, between male
and female foxes and to investigate the effect of season on
the prevalence of infection in juvenile and adult foxes.
Differences were considered significant at P , 0.05.
Results
Prevalence of E. multilocularis in red foxes
A total of 3793 red foxes were collected between October
1990 and May 1995 in the Jura mountains (Soleure,
Jura, Berne, Neucha
ˆ
tel and Vaud), the Plateau (Berne,
Fribourg and Vaud) and the Alps (Berne, Fribourg, Vaud
and Valais) of western Switzerland (table 1 and fig. 1).
Echinococcus multilocularis adults were found in the
intestine of 1142 foxes (30.1%) from all areas. The highest
prevalence occurred in the Plateau in the canton of
Fribourg (52.3%) and the lowest prevalence was recorded
in Valais (7.1%).
Important variations in prevalence values were obser-
ved inside and between geographical areas. The preva-
lence of E. multilocularis in foxes varies between different
parts of the Jura mountains. The highest prevalence rates
were observed in the north-eastern part (Jura, Berne and
Soleure) with 40.5 and 32.7%, respectively and the lowest
rates were seen in the south-western part of the region
(Neucha
ˆ
tel and Vaud) with 23.9 and 13.7%, respectively
(P , 0.01 to P , 0.001). The north-eastern part of the Jura
mountains is considered later in the study as a high
endemic area and the south-western part of the area as a
low endemic area.
Overall, the prevalence of infection in foxes from the
Jura mountains (30.6%) did not differ from that of
the Plateau (32.4%) (P . 0.05) but differed from that of the
Alps (18.8%, P , 0.001). The prevalence of E. multi-
locularis in the canton of Valais (7.1%) was lower than that
observed in other areas of the Alps (P , 0.01 to P , 0.001)
and in all areas of the Jura mountains and the Plateau
(P , 0.05 to P , 0.001).
In western Switzerland, infected foxes were observed
between the altitude of 300 and 1900 m with the highest
prevalence being found between 600 and 1000 m (results
not shown).
Prevalence and intensity of E. multilocularis infection,
relative to fox age and gender
The age of 3016 foxes was estimated by X-ray
examination. The prevalence of E. multilocularis was
significantly higher in juveniles (34.1%) than in adults
(27.6%) (table 2, P , 0.001). The intensity of infection was
Table 1. Prevalence of Echinococcus multilocularis in red foxes in
western Switzerland (1990–1995).
Area
Number
of red foxes
Number
of positive
foxes
Prevalence
(CI) %
Jura mountains
JU þ BE 1198 485 40.5 (37.7–43.3) a
SO 211 69 32.7 (26.7–39.3) a
NE 863 206 23.9 (21.1–26.8) a
VD 379 52 13.7 (10.6–17.6) a
Total 2651 812 30.6 (28.9–32.4)
Plateau
BE 108 24 22.2 (15.4–30.9) b
VD 597 195 32.7 (29.0–36.5) b
FR 86 45 52.3 (41.9–62.6) b,c
Total 791 264 32.4 (30.2–36.7)
Alps
BE 31 7 22.6 (11.4–39.8)
VD 211 50 23.7 (18.5–29.9)
FR 10 2 20.0 (5.7–51.0)
VS 99 7 7.1 (3.4–13.9) d
Total 351 66 18.8 (15.0–23.2) e
Overall total 3793 1142 30.1 (28.7–31.6)
a, P , 0.05–P , 0.001 between all areas of the Jura mountains; b,
P , 0.05–P , 0.001 between all areas of the Plateau; c, P , 0.05–
P , 0.001 between the Plateau of Fribourg and all areas of the
Jura mountains, the Plateau and the Alps; d, P , 0.01–P , 0.001
between the canton of Valais, the areas of the Jura mountains, the
Plateau and the Alps of Berne and Vaud; e, P , 0.001 between the
Alps and the Plateau or the Jura mountains.
CI, confidence interval; JU, Jura; BE, Berne; SO, Soleure; NE,
Neucha
ˆ
tel; VD, Vaud; FR, Fribourg; VS, Valais.
2

also higher in juveniles where 22.9% of positive
individuals were highly infected (class 3) compared to
only 8.9% found in adult (P , 0.001, table 2). Furthermore,
71.1% of adult foxes harboured a lower number of
parasites (class 1) than juveniles (51.4%, P , 0.001). In the
high endemic area of the Jura mountains the infection
intensity was also higher in juveniles (6–12 months old)
than in adult foxes during October 1991 to March 1992 and
October 1992 to March 1993, (fig. 2A, P , 0.001 and
P , 0.01). In the low endemic area the infection intensity of
juvenile foxes was only statistically higher from October
1991 to March 1992 (fig. 2B, P , 0.01).
The gender of 3008 foxes was determined, making a
total of 1293 females and 1715 males (table 3). No
statistical differences were observed between prevalences
in female and male foxes (30.2 and 30.9% respectively).
Similarly, there was no difference in the intensity of
infection of foxes with E. multilocularis, relative to gender.
Seasonal variations in E. multilocularis infections in juvenile
and adult foxes
Data on the prevalence of E. multilocularis in juvenile
and adult foxes originating from the Jura mountains
(n ¼ 2212) were collected during three consecutive years,
from October 1990 to December 1993. In a first step,
results have been grouped and analysed together on a
seasonal basis, with juvenile and adult foxes analysed
separately (tables 4 and 5).
Nine hundred and eighty juvenile foxes were examined
during their first year of life (table 4). In Switzerland, foxes
are born at the beginning of spring. In April and May, 2 of
Fig. 1. Prevalence values of Echinococcus multilocularis in red foxes in the Jura mountains, the Plateau and the Alps in western Switzerland
(1990–1995).
Table 2. Prevalence (%) and intensity of infection of Echinococcus multilocularis in juvenile or adult red foxes in western
Switzerland (1990–1995).
Degree of infection
Number
of infected foxes
Number
of analysed foxesAge 1 2 3
Juveniles 244 (51.4%) a 122 (25.7%) b 109 (22.9%) a 475 (34.1%) a CI: 31.6–36.7% 1392
Adults 318 (71.1%) 89 (19.9%) 40 (8.9%) 447 (27.6%) CI: 25.4–29.8% 1621
Total 562 (61%) 211 (22.9%) 149 (16.2%) 922 3016
Degree 1 ¼ ,100 worms; 2 ¼ 100–1000 worms; 3 ¼ . 1000 worms; a, P , 0.001; b, P , 0.05 between juveniles and adults.
3

23 young animals were infected but by the beginning of the
summer, when foxes were three to four months old, the
prevalence had increased to 15.0% (P . 0.05), then to
24.0% by August–September (P , 0.05). In the autumn
(October–November), a sudden and significant increase
to 42.0% (P , 0.001) was observed followed by a
stabilization of prevalence (44.7%) in winter (December–
January) (P . 0.05), then a decrease in February and
March to reach 8.7% in April–May (P , 0.01).
In total, 1232 adult foxes were examined (table 5).
Statistical differences in prevalences were observed
between two periods, i.e. a decrease from 30.7% in
April–May to 14.8% in August–September (P , 0.01)
then a progressive increase from 14.8% to 31.8% in
February–March (P , 0.001).
In a second step, results of 1990 to 1993 have been
analysed on a seasonal and annual basis for the high and
low endemic areas in the Jura mountains, with juvenile
and adult foxes analysed separately.
The prevalence of E. multilocularis infection in young
foxes generally increased from spring to winter (April–
March) (fig. 3). This tendency was more pronounced in
the area of low endemicity. The prevalence of infection in
adult foxes of the two areas diminished from spring
(April–June) to summer (July–September) and increased
again in autumn and winter (from October to March)
(fig. 4).
The prevalence of infection in juvenile foxes from the
south-western area of the Jura mountains was generally
lower than the prevalence in the north-eastern area
during 1990 to 1993. The differences are statistically
significant for five periods (fig. 3). The prevalence in adult
foxes from the south-western area was also often lower
than the prevalence from the north-eastern area. The
differences are statistically significant for four periods
(fig. 4). Although not significant, the prevalence in
juvenile foxes increased in the low endemic area in spring
1993 (April–June) and in autumn 1993 (October–
December). The same tendency was observed in autumn
1992 and winter 1993 for adult foxes (figs 3 and 4). The last
results could indicate an epidemiological modification in
a zone that was slightly infected.
Discussion
Echinococcus multilocularis is widespread in the north-
ern hemisphere (North America, north and central Asia
and central Europe). In central Europe, infected red foxes
(V. vulpes) have been reported in Belgium, Luxembourg,
France (Massif Central, Savoie and eastern parts),
Switzerland, Lichtenstein, Austria, Germany, in northern
parts of Poland and in Italy (Eckert, 1996; Deplazes, 2006).
Following the success of rabies vaccination (Aubert,
1995), foxes seem to be more abundant and now
commonly inhabit urban areas (Stieger et al., 2002). This
presents an increased risk of infection to a large human
population. The prevalence rates of E. multilocularis in fox
populations are highly variable regionally and range
between , 1 and . 50%. In the southern (canton of Tessin)
Fig. 2. Intensity of infection of Echinococcus multilocularis in foxes
from high (A) and low (B) endemic areas of the Jura mountains,
Switzerland, in juvenile and adult foxes during 1990 to 1993. a,
P , 0.001; b, P , 0.01: significant differences between juvenile
and adult foxes between October–March. Number of foxes
in each class is indicated.
degree 1, , 100 worms; degree 2,
100–1000 worms;
degree 3, . 1000 worms.
Table 3. Prevalence (%) and intensity of infection of Echinococcus multilocularis in female or male red foxes in western
Switzerland (1990–1995).
Degree of infection
Number
of infected foxes
Number
of analysed foxesSex 1 2 3
Female 228 (58.3%) 98 (25.1%) 65 (16.6%) 391 (30.2%) CI: 27.8–32.8% 1293
Male 333 (62.8%) 113 (21.3%) 84 (15.8%) 530 (30.9%) CI: 28.7–33.2% 1715
Total 561 211 149 921 3008
Degree 1 ¼ ,100 worms; 2 ¼ 100–1000 worms, 3 ¼ . 1000 worms; P . 0.05.
4

and eastern parts of Switzerland 2 and 50% of foxes are
infected, respectively (Deplazes et al., 1992). In the present
work we studied the E. multilocularis infection of red
foxes in the western part of Switzerland between 1990
and 1995 (cantons of Soleure, Berne, Jura, Neucha
ˆ
tel,
Fribourg, Vaud and Valais). Infected foxes were observed
in all cantons studied and at altitudes from 300 to 1900 m,
with the highest prevalence recorded between 600 and
1000 m. Human alveolar echinococcosis was specially
mentioned in northern Switzerland (Gottstein et al., 1987).
Nevertheless, foxes were also infected south of the Jura
mountains on the Swiss Plateau (32.4%) and in the Alps
(18.8%). In the isolated alpine canton of Valais, 7.1% of
foxes were still infected. In the canton of Geneva, the
prevalence decreased from the rural and residential areas
(52 and 49% respectively) to urban areas (prevalence of
31%) (Fischer et al., 2005). In several regions of Europe, a
drastic prevalence increase has occurred since the early
1990s (Vuitton et al., 2003). This might account for the
differences between the low rates given for western Vaud
(13.7%), and the high rates cited for neighbouring Geneva
obtained a decade later (Fischer et al., 2005). As shown in
the present study, the prevalence of infection in foxes of
the south-western area of the Jura mountains increased
from 1990 to 1993 and became comparable with that of
the high endemic area of the north-eastern part (figs 3 and
4). In southern Germany, a long-term increase in the
prevalence of E. multilocularis in foxes was reported, with
a more widespread distribution than previously thought
(Lucius & Bilger, 1995). Despite high prevalences in foxes,
alveolar echinococcosis in humans is relatively rare. In
Switzerland, a relatively stable annual morbidity rate of
0.18 cases per 100,000 inhabitants was recorded in recent
decades, with high annual incidence rates occurring more
regionally, as observed in the Swiss canton of Jura (0.74/
100,000) (Gottstein et al., 1987, Ammann et al., 1999, Kern
et al., 2003). From 1990 to 1993 we studied the infection of
foxes from the Jura mountains, which constitute an area
adjacent to the endemic Doubs department in France
(Bresson-Hadni et al., 1994). The prevalence of the
infection decreases from 40.5% in the canton of Jura
and Berne (north-eastern area of the Jura mountains) to
13.7% in the north of the canton of Vaud (south-western
area of the Jura mountains). A decrease in prevalence is
spatially regular and could be explained by region
differences in density of arvicolid species and prevalence
of E. multilocularis metacestodes in the intermediate host.
On the other hand the geology (altitudes), vegetation and
the climate are all similar in the Jura range.
The only free living stage of E. multilocularis is the egg
which survives better under cold than warm tempera-
tures (Veit et al., 1995). These authors performed an
interesting experiment in south-western Germany.
Echinococcus multilocularis eggs were sealed into bags
of nylon mesh and exposed there to the natural climate
during various seasons. The maximal survival time was
240 days from autumn to spring but only 78 days in
summer. Accordingly, the prevalence of E. multilocularis
Table 4. The prevalence (%) of Echinococcus multilocularis in juvenile foxes in
western Switzerland during 1990 to 1995.
Months
Number
of foxes
Number of
positive foxes
Prevalence
(CI) %
April–May 23 2 8.7 (1.5–29.5) a
June–July 147 22 15.0 (9.8–22.0) b,c
August–September 104 25 24.0 (16.4 –33.6) c,d
October–November 231 97 42.0 (35.6 –48.6) a,b,d
December–January 266 119 44.7 (38.7–51.0) a,b
February–March 209 79 37.8 (31.3–44.8) a,b
Total 980 344 35.1 (32.1–38.2)
CI, confidence interval. a, P , 0.01; b, P , 0.001; c, P , 0.05; d, P , 0.01:
significant differences between the monthly periods.
Table 5. The prevalence (%) of Echinococcus multilocularis in adult foxes in
western Switzerland during 1990 to 1995.
Months
Number
of foxes
Number of
positive foxes
Prevalence
(CI) %
April–May 114 35 30.7 (22.6–40.1) a,b
June–July 314 64 20.4 (16.1–25.3) a
August–September 122 18 14.8 (9.2–22.6) b,c,d,e
October–November 175 44 25.1 (19.4–32.4) c
December–January 262 79 30.2 (24.7–36.2) d
February–March 245 78 31.8 (26.1–38.1) e
Total 1232 318 25.8 (23.4–28.4)
CI, confidence interval. a, P , 0.05; b, P , 0.01; c, P , 0.05; d, P , 0.01; e,
P , 0.001: significant differences between the monthly periods.
5

in adult foxes of western Switzerland was less pro-
nounced during the second half of summer than in
autumn and winter. The seasonal vole population
densities, and the seasonal size of the fox population,
with the resulting differences in egg production could
also influence the seasonal prevalence of infection. Small
mammals (Insectivora and Rodentia) are the intermedi-
ate hosts of E. multilocularis. In central Europe, the
common vole M. arvalis and the water vole A. terrestris
are important in transmission. As shown in the Doubs
department (France), human alveolar echinococcosis is
strongly influenced by the densities of arvicolid species
(Viel et al., 1999). In Switzerland, water and common
voles also seem to be important intermediate hosts
(Gottstein et al., 1996, 2001). In a small area of the
Plateau in canton of Fribourg E. multilocularis metaces-
tode was found in 10–39% of an A. terrestris population
and in 10–23% of an M. arvalis population during six
seasons of investigation (1993–1998). A high prevalence
ranging between 47% and 56% was consistently
determined in the fox population of that area during
1993 and 1994, respectively.
Fig. 3. The prevalence (%) of Echinococcus multilocularis in juvenile foxes during 1990 to 1993 in a high ( ) or low ( ) endemic area in the
Jura mountains, Switzerland. Number of foxes in each class is indicated. *P , 0.05, **P , 0.01, ***P , 0.001: significant differences
between high and low endemic areas.
Fig. 4. The prevalence (%) of Echinococcus multilocularis in adult foxes during 1990 to 1993 in a high ( ) or low ( ) endemic area in the Jura
mountains, Switzerland. Number of foxes in each class is indicated. *P , 0.05, **P , 0.01: significant differences between high and low
endemice areas.
6

Young foxes (less than 1 year old) were more frequently
and more intensely infected by E. multilocularis than in
older animals. In the high endemic area of the Jura
mountains, prevalence and intensity of infection were
lower in adult than in juvenile foxes. This may be due to
parasite-induced host immunity to reinfection. This
phenomenom was also observed in other studies (Hofer
et al., 2004) and was also seen in dogs infected with
E. granulosus (Torgerson et al., 2004).
In brief, the prevalence of E. multilocularis in foxes of the
Jura mountains and the Plateau was higher than that
recorded in foxes in the Alps, with important variations
inside each geographical area. Between 1990 and 1995, the
highest rate was recorded in the Plateau in the canton of
Fribourg with a prevalence of 52.3%. Moreover, the
prevalence of E. multilocularis infection in foxes in the
alpine canton of Valais was the lowest (7.1%). Young foxes
were more often and more intensively infected than the
adults.
Acknowledgements
The authors thank the Swiss Centre for Rabies, the
Galli-Valerio Institute in Lausanne for providing intes-
tines of red foxes, the Swiss Federal Office for Public
Health and Wildlife Protection Service of Cantor Vaud for
their financial support, and Dr P. Torgesson for critically
reviewing the manuscript.
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