Echinococcus multilocularis and other cestodes in red foxes (Vulpes vulpes) of northeast Italy, 2012-2018

Abstract

Background: Echinococcus multilocularis is a small tapeworm affecting wild and domestic carnivores and voles in a typical prey-predator life cycle. In Italy, there has been a focus of E. multilocularis since 1997 in the northern Italian Alps, later confirmed in red foxes collected from 2001 to 2005. In this study, we report the results of seven years of monitoring on E. multilocularis and other cestodes in foxes and describe the changes that occurred over time and among areas (eco-regions) showing different environmental and ecological features on a large scale.

Methods: Eggs of cestodes were isolated from feces of 2872 foxes with a sedimentation/filtration technique. The cestode species was determined through multiplex PCR, targeting and sequencing ND1 and 12S genes. Analyses were aimed to highlight variations among different eco-regions and trends in prevalence across the study years.

Results: Out of 2872 foxes, 217 (7.55%) samples resulted positive for cestode eggs at coproscopy, with differences of prevalence according to year, sampling area and age class. Eight species of cestodes were identified, with Taenia crassiceps (2.65%), Taenia polyacantha (1.98%) and E. multilocularis (1.04%) as the most represented. The other species, Mesocestoides litteratus, Taenia krabbei, T. serialis, T. taeniaeformis and Dipylidium caninum, accounted for < 1% altogether. Echinococcus multilocularis was identified in foxes from two out of six eco-regions, in 30 fecal samples, accounting for 1.04% within the cestode positives at coproscopy. All E. multilocularis isolates came from Bolzano province. Prevalence of cestodes, both collectively and for each of the three most represented species (T. crassiceps, T. polyacantha and E. multilocularis), varied based on the sampling year, and for E. multilocularis an apparent increasing trend across the last few years was evidenced.

Conclusions: Our study confirms the presence of a focus of E. multilocularis in red foxes of northeast Italy. Although this focus seems still spatially limited, given its persistence and apparent increasing prevalence through the years, we recommend research to be conducted in the future on the ecological factors that, on a smaller scale, allow this zoonotic species to persist. On the same scale, we recommend a health education campaign to inform on the measures to prevent this zoonosis, targeted at people living in the area, especially hunters, dog owners, forestry workers and other potentially exposed categories.

Keywords: Alveolar echinococcosis; Cestode; Echinococcus multilocularis; Northeast Italy; Vulpes vulpes.

Fig. 1

Distribution of cestode-positive and E. multilocularis-positive foxes (whole sample) according to province and ecoregions in the northeast of Italy

Fig. 2

Overall cestode prevalence (%) by bimester

Fig. 3

E. multilocularis (E. m.), T. crassiceps (T. c.) and T. polyacantha (T. p.) overall prevalence (%) by bimester

Fig. 4

Joined E. multilocularis (E. m.), T. crassiceps (T. c.) and T. polyacantha (T. p.) prevalence (%) in ecoregions 1A2b and 1A2c by bimester

Fig. 5

Cestodes (Cest.), E. multilocularis (E. m.), T. crassiceps (T. c.) and T. polyacantha (T. p.) overall prevalence (%) in the study area by year

Fig. 6

Cestodes (Cest.), E. multilocularis (E. m.), T. crassiceps (T. c.) and T. polyacantha (T. p.) overall prevalence (%) in ecoregion 1A2b and 1A2c by year