For the study European countries were chosen with considerable difference in the dynamics of the fox populations, the epidemiology of E. multilocularis and the information on AE provided to the public. After a first evaluation we selected the Czech Republic (CZ), France (FR), Germany (DE) and Switzerland (CH). Country-specific details are given below.
Czech Republic
The Czech Republic is classified as rabies free since 2004 [
18]. It is believed that fox populations have experienced a pronounced increase during the last decade [
19]. Urban foxes are reported from cities such as Prague and Pilsen (Martinek, pers. comm.). However, public awareness of urban foxes is minimal because of their low abundance.
Up to date only one human case of AE has been recorded [
20]. The patient lived in West Bohemia. In this area prevalences of up to 63% have been found in foxes [
19]. Pavlasek detected
E. multilocularis in foxes from North, Central and Southern Bohemia [
21] and unpublished records of infected foxes are reported from the eastern part of Czech Republic [
21,
22].
The presence of E. multilocularis was communicated to the Czech public for the first time in spring 1999 by a popular television broadcast. The contribution was prepared as shocking reportage (Martinek, pers. comm.). Subsequently many articles with inaccurate information were published. In response a TV production was broadcast by the state TV with cooperation of the Academy of Sciences of Czech Republic. This program (1999) was the only information provided on a national level before the public survey of this study started.
France
Rabies was eliminated in France in 1998 [
23]. Correspondingly a significant increase of fox density indices has been reported [
13]. Urban foxes are present in several cities in France, but the actual national status has not been systematically documented [
24,
25].
In France 212 cases of human AE were diagnosed between 1981 and 2000 [
26]. Most cases were concentrated in Eastern France (Franche Comté, Lorraine and Haute Savoie). Some cases were also clustered in the Department of Auvergne [
26,
27]. This distribution corresponds with the distribution of
E. multilocularis–infected foxes [
28].
Public information on E. multilocularis has been carried out mainly at a regional level in areas where the parasite has long been known. At a national level an information leaflet was issued by the French Ministry of Health. However, this leaflet was distributed only after our public inquiry in autumn 2004 (Raoul, pers. comm.).
Germany
There still exists a residual rabies focus in the border triangle of Hessen, Baden-Wuerttemberg and Rhineland Palatinate [
29]. However, the decline of rabies seems to parallel increasing fox populations [
13]. There exists no systematic survey on urban foxes in Germany, but they seem to be present in many cities: for example in Berlin [
30], Kassel (Hesse, U. Hohmann, pers. Comm.), Munich [
31] and Stuttgart [
32].
A total of 102 human cases of AE were recorded between 1981 and 2000 [
26]. Most cases are clustered in the southern federal states Baden-Wuerttemberg and Bavaria [
26]. Today this parasite has been confirmed in all regions of Germany [
33]. However, high prevalences exceeding 30% are mainly reported from fox populations of the south of the country [
33]. In northern Germany areas of high endemicity appear to be interspersed focally in low endemicity regions [
34,
35].
E. multilocularis received regular public attention through numerous articles and broadcasts during the past two decades. However, there has been no information campaign on a national level. In federal states with high prevalences of E. multilocularis the public is officially informed with leaflets and newspaper articles.
Switzerland
Switzerland was declared rabies free in 1999 [
36]. The Swiss hunting statistics gives evidence for a strong increase of the Swiss fox population from the mid 1980ies to the mid 1990ies (Swiss Federal Office for Environment). Urban foxes have been recorded in all Swiss cities [[
14] and unpublished data]. In Zurich, the largest Swiss city, fox density was estimated to be 9.8–11.2 adult foxes per km
2 [
37].
Between 1952 and 2005 a total of 494 cases of human AE have been recorded with patients originating from all parts of Switzerland [
17]. However, there exist huge differences in the prevalences of
E. multilocularis in foxes, with high rates in northern cantons and low rates in cantons within and south of the Alps.
Information on the fox tapeworm was intensively carried out in the 1980s. With regard to prevention the information is concentrated on berries, fruits and vegetables contaminated by EM eggs, gardening and handling foxes. In the German part of Switzerland, an extensive information campaign (INFOX) started in 1997 [
38].
Inquiry
We undertook a public survey by telephone. The interviews were conducted in the framework of an omnibus by ISO certified (ISO 9001:2000) marketing companies (Synovate GmbH, Wiesbaden, Germany: Czech Republic, France, Germany; IHA-GfK AG, Hergiswil, Switzerland: Switzerland). An Omnibus is a multipurpose survey, where several clients share the same questionnaire. It is a cost-effective method, since all fixed costs are shared. Omnibuses are carried out as nationwide studies.
The interviews were held between March 29 and May 28, 2004. In Czech Republic, France and Germany, an automated dialling system was used to randomly select listed and unlisted telephone numbers (RDD). In Switzerland, where most numbers are listed (92% in 2004 [
39]), the random sample was based on listed numbers only and interviews were conducted in German and French according to the prevailing mother tongue of the region. The single Swiss Canton where the majority is of Italian mother tongue (Ticino) was not considered in the survey. Cell phones were not included in all countries.
The interviews were carried out according to the "Random-Quota" method, i.e. regions and community size were randomly selected and age and sex were chosen according to a representative quota. Up to 5 attempts were made to contact each number. For each country, a population sample of ≥ 500 women and men between 15 and 74 years was interviewed. The data was weighted according to "quota" and standardized on a sample size of 500 persons.
In 2004, there were 3.6 Mio main telephone lines in the Czech Republic (population: 10.2 Mio, proportion: 35%), 33.9 Mio in France (60.6 Mio, 56%), 54.3 Mio in Germany (82.4 Mio, 66%) and 5.4 Mio in Switzerland (7.5 Mio, 72%). The omnibus surveys from Synovate GmbH go through to someone in a mean percentage of 83.1% and a mean percentage of 14.1% of the persons are willing to give an interview. The rest of the called persons either do not fit the quota or they refuse to participate. The response rates are not significantly different between the three countries. The corresponding percentages for Switzerland, where only listed numbers where called, are roughly 70% (successful contacts) and 35% (effective interviews).
The survey consisted of five questions (Table
1). The first question asked about the attitude towards urban foxes. Then people were asked about their knowledge of EM (question 2). People who had heard about EM were asked a further three questions concerning their perception of information received (question 3), their risk perception (question 4) and their knowledge about possible countermeasures against an infection with AE (question 5). The questionnaire was translated into Czech, French and German by national experts in helminthology who were familiar with the common terms concerning this zoonosis (see Additional file
1) and the five questions were always asked in the same order for each interview.
Table 1
Questionnaire of the representative telephone inquiry conducted in Czech Republic, France, Germany and Switzerland (March – May 2004).
Do you think, it is all right that there live foxes in urban areas? | Very good | 1 |
Do you think, it is ... | Rather good | 2 |
(Enter a single response) | Rather bad | 3 |
| Very bad | 4 |
| Don't know | 5 |
Question 2:
| | |
Have you ever heard about the fox tapeworm? | Yes | 1 |
| No | 2 |
Question A3:
| | |
Do you think you received reasonable information on the fox tapeworm? | Yes | 1 |
| No | 2 |
| Don't know | 3 |
Question A4:
| | |
Do you think the fox tapeworm is a health risk to you? | A high risk... | 1 |
Do you think it is ..... | A small risk | 2 |
(Enter a single response) | No risk | 3 |
| Don't know | 4 |
Question A5:
| | |
Do you know how you are able to protect yourself against the fox tapeworm? | To treat foxes | 1 |
(Read and randomise list. Enter multiple responses.) | To de-worm cats and dogs regularly | 1 |
| To pick and eat no wild berries | 1 |
| To wash food before eating | 1 |
| To cook food before eating | 1 |
| To avoid contact with fox excrement | 1 |
| Don't know | 9 |
Each questionnaire contained data about age and sex of the interviewees, household size, size of the community and region where they lived. In Czech Republic eight, in France nine, in Germany sixteen and in Switzerland four regions were differentiated. For each country separately, the regions were classified into areas with relative low, middle or high infection pressure (Variable STATE EM, see Table
2). The classification was done by parasitologists who have a detailed knowledge of published but also unpublished epidemiological studies on
E. multilocularis of their country (Karel Martinek, University of West Bohemia, Czech Republik; Francis Raoul, University of Franche-Comté, France; Thomas Romig, Germany; Peter Deplazes, Switzerland).
Table 2
Regional classification in low, middle and high endemic areas for E. multilocularis (variable STATE EM) based on the expertise of epidemiologists of Czech Republic (CZ), France (FR), Germany (DE) and Switzerland (CH).
CZ* | Central Bohemia (Central Bohemia), East Bohemia (East Bohemia, Region Pardubice, Moravian Highlands (northern part)), North Moravia (Region Olomouc, Maravian – Silesian), Prague (Prague)
| low (N = 287) |
| North Bohemia (North-West Bohemia, Giant Mountains – Liberec), South Bohemia (South Bohemia, Moravian Highland (western part)), South Moravia (Southern Moravia, Region Zlin, Moravian Highlands (eastern part))
| middle (N = 213) |
| West Bohemia (Pilsen Region, Spas of the Western Bohemia)
| high (N = 41) |
FR | Mediterranean Area (Languedoc Roussillon, Provence-Alpes Côte-d'Azur), Nord (Nord Pas-de-Calais), Paris Area (Ile de France), South West (Aquitaire, Midi-Pyrénées, Limousin), West (Bretagne, Pays-de-la-Loire, Poitou-Charentes), West Paris Basin (Haute-Normandie, Basse Normandie, Centre)
| low (N = 356) |
| East Paris Basin (Picardie, Champagne-Ardennes, Bourgogne)
| middle (N = 40) |
| East (Lorraine, Alsac, Franche-Comté), Rhône Alps (Rhône-Alpes, Auvergne)
| high (N = 104) |
DE | Berlin, Brandenburg, Bremen, Hamburg, Mecklenburg-Vorpommern, Sachsen, Sachsen-Anhalt, Schleswig-Holstein | low (N = 125) |
| Niedersachsen, Nordrhein-Westfalen, Rheinland-Pfalz, Saarland, Thueringen | middle (N = 202) |
| Baden-Wuerttemberg, Bayern, Hessen | high (N = 173) |
CH † | Highlands of Switzerland (Appenzell-Ausserrhoden, Appenzell- Innerrhoden, Graubuenden, Luzern, Nidwalden, Obwalden, St. Gallen, Uri, Zug, eastern part of Valais, highlands of Bern and Schwyz) | middle (N = 121) |
| Western Switzerland (cantons Gêneve, Jura, Neuchâtel, Vaud and western part of the cantons Fribourg and Valais), Mid-Western | high (N = 379) |
| Switzerland (cantons Baselland, Baselstadt, Solothurn, western part of canton Aargau and lowlands of canton Bern) | |
| Mid-Eastern Switzerland (cantons Schaffhausen, Schwyz, Turgau, Zuerich, eastern part of canton Aargau and northern part of canton Schwyz) | |
Data analysis
In order to reach the quota of age and sex occurring in the population the data of the questionnaires were weighted with factors between 0.20 and 3.48 (median = 1). The result of the analysis with square-root transformed data did not differ substantially compared to original data. Therefore we used untransformed data. A logistic regression model selection procedure (stepwise backward method using log-likelihood statistic) was used to identify factors affecting knowledge about the fox tapeworm (levels of response variable: 0/1, question 2) with the following variables (levels): COUNTRY, AGE (< 25, 25–44 and > 44 years), SEX, HOUSEHOLD (1–2 persons, > 2 persons, answer refused), COMMUNITY (< 5'000 inhabitants, 5'000 – 90'000 in Czech Republic and 5'000 – 50'000 in the other countries, > 90'000 in Czech Republic and > 50'000 in the other countries), STATE EM (low, middle and high endemic areas for EM, see Table
2) and ATTITUDE (attitude towards urban foxes, five levels, see question 1 in Table
1). In order to recognize country-specific effects of the other independent variables, all two way interactions with the variable COUNTRY were added to the initial model. The same procedure was applied to identify factors affecting their perception of information received (levels of response variable: 0/1, question 3). χ
2 randomizations were done with Actus2 [
40]. Exact binomial 95% confidence intervals (CI) for means of binomial variables were calculated with unweighted data according to the method of Clopper and Pearson [
41]. All other calculations were carried out with the statistical software packages SPSS 10 [
42].