Distribution of alveolar echinococcosis according to environmental and geographical factors in Germany, 1992-2018

Highlights

• Distribution of alveolar echinococcosis according to environmental factors in Germany was analyzed.

• There was a heterogeneous distribution of alveolar echinococcosis in Germany.

• In regions with higher altitudes (505-672 m) most cases of disease were recorded.

• The most cases we found in regions with a moderate temperature (6,0-7,9°C).

• In regions with higher precipitation rates (701-1000 mm) most cases were recorded.

Abstract

Alveolar echinococcosis (AE) is a rare zoonotic disease caused by the larval stage of Echinococcus multilocularis. Despite its low world-wide prevalence, this disease shows differences in the regional distribution of cases. In the present cohort study, we analyse the distribution of AE according to environmental and geographical factors in Germany. We identified the place of residence of 591 cases of AE from the national database for AE, and georeferenced these localities in the Universal Transverse Mercator coordinate system. Data on elevation, air temperature, precipitation height and land cover were mapped out and correlated with the distribution of cases of disease during the period 1992-2018. Moran's I statistic was used for spatial autocorrelation. Differences in frequency distribution between elevation, air temperature, precipitation height and landscape feature classes were analysed with the Kruskal-Wallis test. With the multiple linear regression analysis, we determined the influences and interactions of geographical and climatic factors on the number of AE cases. The results showed a heterogeneous distribution of AE cases with a higher concentration in southern Germany than in the rest of Germany (I = 0.225517, Z = 35.8182 and p < 0.001). There was a statistically significant difference in frequency distribution between precipitation height, air temperature, elevation and landscape feature classes and AE cases in Germany (p < 0.0001). In regions with higher elevations (505-672 m), moderate average air temperatures (6.0-7.9°C) and higher precipitation rates (701-1000 mm) most AE cases were recorded. It seems, that regions with higher precipitation rates, higher elevations and moderate average air temperatures have a higher infection burden and infection conditions. It is therefore extremely important to generate greater awareness of the disease in these regions, with the aim of recognising potential cases of AE as early as possible and introducing the appropriate therapeutic measures.

Introduction

Alveolar echinococcosis (AE) is a rare zoonosis caused by the larval stage of Echinococcus multilocularis (Eckert et al., 2001; Moro and Schantz, 2009). The life cycle of E. multilocularis involves two hosts, with a crucial interaction between them (Eckert and Deplazes, 2004). The most common and most important definitive host in Europe is the red fox (Vulpes vulpes) (Eckert and Deplazes, 2004). The natural intermediate hosts of E. multilocularis are mainly rodents of the vole family, which are the foxes’ main prey (Eckert and Deplazes, 2004). Domestic dogs and cats may also be infected with this parasite and thus become definitive hosts (Eckert and Deplazes, 2004). Humans are not involved in the E. multilocularis life cycle but can become dead-end intermediate hosts through the inadvertent ingestion of infectious tapeworm eggs (Eckert and Deplazes, 2004; Kern et al., 2004). Infection with the parasite can cause AE in humans, initially manifesting almost exclusively in the liver (Brunetti et al., 2010; Eckert et al., 2001). Human AE resembles a malignant tumour in its appearance and destructive behaviour. Left untreated, it may cause serious illness with a fatal outcome (Eckert et al., 2001).

AE occurs predominantly in temperate to cold climate zones of the northern hemisphere and is found particularly across central Europe, a large part of north and central Asia, and in some parts of North America (Baumann et al., 2019; Deplazes et al., 2017; Kern et al., 2003). The main ‚historical’ endemic areas in Europe include Northern Switzerland, Western Austria, Eastern France and Southern Germany (Baumann et al., 2019; Deplazes et al., 2017; Kern et al., 2003; Romig, 2003). Estimates put the prevalence of human AE in these regions between 2 and 40 cases per 100,000 inhabitants (Eckert et al., 2001; Romig et al., 1999). For the past decades, in Europe an increasing spread of E. multilocularis from the old known endemic areas to non-endemic areas has been observed (Baumann et al., 2019; Deplazes et al., 2017; Eckert et al., 2000; Romig, 2003). A recent study determined the current high-risk areas in the Federal Republic of Germany especially in Bavaria and Baden-Württemberg and the distribution of AE cases (Schmidberger et al., 2018).

Several studies have already demonstrated a relationship between potential risk factors (e.g. dog and cat ownership, have a kitchen garden, occupation: farmer, haymaking in meadows not adjacent to water, went to forests for vocational reasons, chewed grass and hunting / handling foxes) and an increased risk of contracting the infection (Conraths et al., 2017; Kern et al., 2004; Piarroux et al., 2013). Behavioural, occupational and lifestyle factors associated with disease risk play a role in the prevalence of human AE but do not provide a sufficient explanation for the heterogeneous distribution of cases in Germany. The prevailing climatic conditions and the topographical differences in Germany suggest that elevation, climate and landscape features may also affect the risk of AE and the heterogeneous distribution of AE cases. Recent studies from China and France have already demonstrated an influence of these factors on disease risk (Cadavid Restrepo et al., 2018a; Cadavid Restrepo et al., 2018b; Giraudoux et al., 2013; Piarroux et al., 2015). There was a clear increase in the risk of contracting AE in the more elevated regions of France with very cold winters and higher annual precipitation rates (Piarroux et al., 2015). In China, too, an increase in elevation and precipitation rate seemed to be associated with a greater risk of disease, as well as a decrease in the average temperature (Cadavid Restrepo et al., 2018a; Cadavid Restrepo et al., 2018b; Giraudoux et al., 2013). Landscape features as well as climate factors therefore seem to play a substantial role in the occurrence of human AE and its geographical distribution. However, it has to be mentioned that these geographical factors do not directly represent an increased risk for human AE, but rather potentially have an influence on the life cycle of E. multilocularis (particularly on the predator-prey interaction) and thus on the risk of transmission of E. multilocularis to humans. No studies have yet been carried out in Germany to confirm such a relationship, although it is known that there is a higher prevalence of human AE in the Swabian Alb, the Alpine foothills and the Bavarian Alps (Schmidberger et al., 2018). As these more elevated regions are characterised by lower temperatures and higher precipitation rates, it cannot be ruled out that geographical factors have an effect on the risk of AE in Germany (Dietrich and Wagner, 2015).

The main aim of our study was to analyse and evaluate the frequency distribution of AE according to environmental and geographical factors (elevation, climate and landscape features) in order to gain a better understanding of risk-areas and influencing factors in Germany.