Date Published: April 12, 2019
Publisher: Public Library of Science
Author(s): Andreas König, Thomas Romig, Ernst Holzhofer, Michael Lierz.
Effective preventive strategies are available to control Echinococcus multilocularis in foxes in order to reduce the human infection risk. Reduction of E. multilocularis prevalence in foxes was achieved in various studies by distributing praziquantel-containing bait by hand or by aircraft in either rural or settlement areas. Here, an integrated approach is described from southern Germany (district of Starnberg). Baseline data were obtained in winter 2002/03, when the prevalence rate in the project area was 51%. Between December 2005 and December 2011, air distribution of bait in agricultural and recreational areas was combined with distribution by hand in towns and villages, in order to cover the entire fox population, with a bait density of 50 pieces / km2 (baiting area: 213 km2). In addition, a control area without anthelmintic treatment was selected. Prevalence was reduced in the baiting area to 1% by March 2007. Subsequently, from 2007 to the end of 2011, prevalence rates remained at a low level with 2.4% (2007), 2.4% (2008), 2.6% (2009), 1.2% (2010) and 0.0% (2011). In the un-baited control area the prevalence rates remained high, ranging from 19.6% to 35.1% with an average of 27.3%. During the 6 years of anthelmintic treatment, differences between baiting and control areas were highly significant (P<0.001). In the suburban and urban parts of the study area prevalence could be reduced to less than 1%, i.e. to a level below the limit of detection, which was maintained even after the measures had been discontinued. The applicability and effectiveness of anthelmintic baiting was therefore confirmed even for a heavily settled and fragmented landscape, which posed challenges for practical application of the control measures. The cost of the project ranged between € 1.70 and € 2.00 per inhabitant of the baiting area per year.
Echinococcus multilocularis is a zoonotic cestode of foxes and other canids, whose metacestode utilises rodents and other small mammals as intermediate hosts. Accidental infection of humans leads to alveolar echinococcosis (AE), which is potentially fatal due to the progressing occupation of space by the metacestode, analogous to a malignant tumour . E. multilocularis and AE are widely distributed across temperate and cold regions of the northern hemisphere; in Europe, the parasite is present in most regions except southern Europe, the British Isles and most parts of Scandinavia . There was a drastic emergence of this parasite in central Europe and elsewhere at the end of the 20th century, in conjunction with a several-fold increase in fox populations , a marked tendency of foxes to establish populations within human settlements, including cities, and an increased parasite transmission within human settlements [4, 5, 6, 7, 8, 9,10]. The publicly perceived increase in the human infection risk prompted various studies on the feasibility of controlling the parasite through the anthelmintic treatment of foxes with baits, using a variety of different bait types, baiting schedules (frequency, bait density), landscapes (rural, urban) and area sizes [11, 12, 13]. Consistent outcomes of the various approaches were (a) the effectiveness in decreasing E. multilocularis prevalence in foxes in different environments, in different regions and with very different sizes of study areas (<10 to >4500 km2) , (b) the need for long-term application of the methods and (c) the failure to completely eliminate parasite transmission during baiting periods ranging from 9 months to 6 years [12, 14]. Persistence at low level was explained by small study areas (facilitating immigration of non-treated foxes), exclusive reliance on bait distribution by aircraft, which allows transmission to persist in and around villages and towns, inadequate bait densities in relation to rising fox populations, and short application periods.
The study area and methods are to a large degree identical to those described for the initial phase of the project . In the following we present an abbreviated version, highlighting differences to the previous approach.
The change of prevalence over time is shown in Table 1. Immediately prior to the baiting period, prevalence was 37.5% (baiting area) and 39.0% (control area). During the baiting phase, the prevalence in the baiting areas was rapidly reduced to 5.0% during 2006, and continued to decrease towards 0.0% in 2011. Importantly, prevalence did not rise after the increase in the length of intervals between bait distributions from 1 to 2.5 months after 2009. After baiting was stopped in December 2011, however, prevalence increased to 10.7% in the following year, although positive foxes were found on the edges of the baiting area (Fig 2).
In this study we confirmed the effectiveness of anthelmintic praziquantel treatment of foxes in a mixed urban-rural area of southern Germany. Prevalence could be rapidly reduced in the initial phase of the baiting period, and after 6 years of the treatment programme, the infection rate was close to 0% (CI 0%-4%). This is in accordance with simulations carried out by previous authors , which, starting with an initial prevalence of 55%, calculated a prevalence of 1% after 5 years of treatment. In the suburban / urban areas the prevalence rate of E. multilocularis could be sustained at 0% one year after treatment. In contrast to a previous simulation , however, the lack of infected animals could be sustained over the 6 year period. This result suggests that, provided a treatment area can be demarcated in accordance with the principles of wildlife biology, an elimination of E. multilocularis in foxes is possible even in larger areas. Possibly, by implementing measures only on the edges of the area, re-intruduction of the parasite from outside could be prevented.