Brucella melitensis in France: Persistence in Wildlife and Probable Spillover from Alpine Ibex to Domestic Animals

Abstract

Bovine brucellosis is a major zoonosis, mainly caused by Brucella abortus, more rarely by Brucella melitensis. France has been bovine brucellosis officially-free since 2005 with no cases reported in domestic/wild ruminants since 2003. In 2012, bovine and autochthonous human cases due to B. melitensis biovar 3 (Bmel3) occurred in the French Alps. Epidemiological investigations implemented in wild and domestic ruminants evidenced a high seroprevalence (>45%) in Alpine ibex (Capra ibex); no cases were disclosed in other domestic or wild ruminants, except for one isolated case in a chamois (Rupicapra rupicapra). These results raised the question of a possible persistence/emergence of Brucella in wildlife. The purpose of this study was to assess genetic relationships among the Bmel3 strains historically isolated in humans, domestic and wild ruminants in Southeastern France, over two decades, by the MLVA-panel2B assay, and to propose a possible explanation for the origin of the recent bovine and human infections. Indeed, this genotyping strategy proved to be efficient for this microepidemiological investigation using an interpretation cut-off established for a fine-scale setting. The isolates, from the 2012 domestic/human outbreak harbored an identical genotype, confirming a recent and direct contamination from cattle to human. Interestingly, they clustered not only with isolates from wildlife in 2012, but also with local historical domestic isolates, in particular with the 1999 last bovine case in the same massif. Altogether, our results suggest that the recent bovine outbreak could have originated from the Alpine ibex population. This is the first report of a B. melitensis spillover from wildlife to domestic ruminants and the sustainability of the infection in Alpine ibex. However, this wild population, reintroduced in the 1970s in an almost closed massif, might be considered as a semi-domestic free-ranging herd. Anthropogenic factors could therefore account with the high observed intra-species prevalence.

The European Union One Health 2018 Zoonoses Report

“…France, bovine brucellosis officially free since 2005 with no cases reported in domestic/wild ruminants since 2003, reported isolations of B. melitensis from wild mountain goats (Alpine ibex or Capra ibex). Previously, Mick et al (2014) reported on the risk of transmission to livestock and spill over of B. melitensis from wildlife to domestic ruminants and the sustainability of infection in Alpine ibex in a well-delineated mountain area in the French Alps. To get insight into brucellosis in dogs in Europe, the database in Germany of a veterinary diagnostic laboratory which received samples from dogs for B. canis testing from 20 European countries, was investigated (2011-2016) (Buhmann et al, 2019).…”

The quest for a true One Health perspective of brucellosis

“…can spill over into livestock and humans. In France, B. melitensis has been isolated from an Alpine ibex (Capra ibex) and has probably spilled over to cattle and from cattle to humans (110). In Argentina, B. suis has been isolated in armadillos (Chaetophractus villosus), but spillover from armadillos to livestock and humans has not yet been reported (111).…”

Epidemiology of Brucellosis and Genetic Diversity of Brucella abortus in Kazakhstan

“…Molecular characterization of circulating strains of Brucella is critical for elimination of repeated outbreaks, tracking infection spread, and informing selection of anti-brucellosis strategies [15, 16]. Multiple-Locus Variable-number tandem-repeat Analysis (MLVA) is a well-suited technique for genotyping of Brucella [17–19].…”