Host and Environmental Factors Modulate the Exposure of Free-Ranging and Farmed Red Deer (Cervus elaphus) to Coxiella burnetii

Abstract

fThe control of multihost pathogens, such as Coxiella burnetii, should rely on accurate information about the roles played by the main hosts. We aimed to determine the involvement of the red deer (Cervus elaphus) in the ecology of C. burnetii. We predicted that red deer populations from broad geographic areas within a European context would be exposed to C. burnetii, and therefore, we hypothesized that a series of factors would modulate the exposure of red deer to C. burnetii. To test this hypothesis, we designed a retrospective survey of 47 Iberian red deer populations from which 1,751 serum samples and 489 spleen samples were collected. Sera were analyzed by enzyme-linked immunosorbent assays (ELISA) in order to estimate exposure to C. burnetii, and spleen samples were analyzed by PCR in order to estimate the prevalence of systemic infections. Thereafter, we gathered 23 variables-within environmental, host, and management factors-potentially modulating the risk of exposure of deer to C. burnetii, and we performed multivariate statistical analyses to identify the main risk factors. Twenty-three populations were seropositive (48.9%), and C. burnetii DNA in the spleen was detected in 50% of the populations analyzed. The statistical analyses reflect the complexity of C. burnetii ecology and suggest that although red deer may maintain the circulation of C. burnetii without third species, the most frequent scenario probably includes other wild and domestic host species. These findings, taken together with previous evidence of C. burnetii shedding by naturally infected red deer, point at this wild ungulate as a true reservoir for C. burnetii and an important node in the life cycle of C. burnetii, at least in the Iberian Peninsula.C oxiella burnetii is a Gram-negative intracellular bacterium that causes Q fever, a disease that affects both humans and animals. Whereas the epidemiological status of C. burnetii in European domestic ruminants is well known (1), information for wildlife is mostly local and scattered (2, 3). Although the majority of human Q fever outbreaks are linked to the transmission of C. burnetii from domestic ruminants (4, 5), the ability of C. burnetii to infect wild hosts (3, 6) and its high environmental resistance (1) make wildlife species potential reservoirs of C. burnetii. Based on this hypothesis, wildlife could maintain C. burnetii and transmit it to wildlife (7), domestic animals (8), or humans (9). It is therefore of paramount relevance (i) to identify those potential wild reservoir species that could, through direct and indirect interactions, transmit C. burnetii to target species (domestic animals and humans) and (ii) to determine which environmental factors are the main drivers of C. burnetii within the most relevant wild reservoirs. Efficient prevention of C. burnetii transmission at the wildlifedomestic-animal-human interface can be approached only once the main reservoirs have been identified and the driving risk factors are known (10).Several wild ruminant species are present and wel...

Diverse tick-borne microorganisms identified in free-living ungulates in Slovakia

“…However, the role of free-living ungulates in the epidemiology of C. burnetii may differ between ecosystems and geographic areas [56]. …”

Coxiella burnetii Genotypes in Iberian Wildlife

“…This finding, in addition to the wide geographic distribution of exposure to C. burnetii of Iberian red deer and wild rabbit populations [12,13], suggests that wildlife, red deer, and European wild rabbit in particular may be important wild sources of C. burnetii for humans. An additional interesting finding was the low similarity of MLVA genotypes from livestock and wildlife, even considering those from close geographic locations described in this study (Table 3); only genotypes from a Japanese cow and a Portuguese goat clustered with red deer and rabbit genotypes.…”

“…In order to prevent and detect sample cross-contamination, negative controls (Nuclease free water; Promega, Madison, WI, USA) were included every 10 samples during the DNA extraction procedure. All samples were tested by a qPCR targeting the IS1111a insertion element of C. burnetii as described previously [13,21].…”

“…In the European context, C. burnetii genotypes that circulate among domestic ruminants and humans in Hungary, Poland, Portugal, Spain, and the Netherlands have been genotyped [4][5][6][7][8][9][10]. In contrast, information regarding the relevance of wild hosts in the ecology of C. burnetii is scarce [11][12][13][14], and consequently, genotypes circulating in wildlife have been rarely identified [6,15]. Interestingly, the origin of several human Q fever cases remains unclarified [16] and human-wildlife interaction has been suggested as a risk factor for human infection with C. burnetii [17].…”

Genotypes of Coxiella burnetii in wildlife: disentangling the molecular epidemiology of a multi‐host pathogen

“…Q fever is a zoonotic infectious disease caused by Coxiella burnetii , a gram‐negative bacterium with high environmental resistance (Maurin and Raoult, ). Domestic ruminants, pets and wild mammals are natural reservoirs of C. burnetii (Maurin and Raoult, ; González‐Barrio et al ., ). Transmission to humans occurs mainly at the livestock‐human interface through aerosols (Maurin and Raoult, ).…”