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

Abstract

The 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.

FIG 1

Spatial distribution of Coxiella burnetii seroprevalence in Iberian red deer and presence of C. burnetii DNA in spleen samples. Each dot represents a surveyed red deer population. The current geographic distribution of the red deer in the Iberian Peninsula is shown in pale orange (54, 55). The number of sera analyzed per population is shown. A red asterisk next to the sampling size indicates red deer farms. The map of Spain has been divided into the bioregions established in the current Spanish wildlife disease surveillance program (27). Por, Portugal.

FIG 2

Relationships between the seroprevalence of C. burnetii in the population and explanatory factors identified through risk factor modeling for each of the modeled data sets (overall deer populations [OD], unmanaged populations [UD], managed populations [MD], and farmed populations [FD]).