Temporal dynamics of antibody level against Lyme disease bacteria in roe deer: Tale of a sentinel?

Abstract

Changes in the risk of exposure to infectious disease agents can be tracked through variations in antibody prevalence in vertebrate host populations. However, information on the temporal dynamics of the immune status of individuals is critical. If antibody levels persist a long time after exposure to an infectious agent, they could enable the efficient detection of the past circulation of the agent; if they persist only a short time, they could provide snap shots of recent exposure of sampled hosts. Here, we explored the temporal dynamics of seropositivity against Lyme disease agent Borrelia burgdorferi sensu lato (Bbsl) in individuals of a widespread medium-sized mammal species, the roe deer (Capreolus capreolus), in France. Using a modified commercially available immunoassay we tested 1554 blood samples obtained in two wild deer populations monitored from 2010 to 2020. Using multi-event capture-mark-recapture models, we estimated yearly population-, age-, and sex-specific rates of seroconversion and seroreversion after accounting for imperfect detection. The yearly seroconversion rates indicated a higher level of exposure in early (2010-2013) than in late years (2014-2019) to infected tick bites in both populations, without any detectable influence of sex or age. The relatively high rates of seroreversion indicated a short-term persistence of antibody levels against Bbsl in roe deer. This was confirmed by the analysis of samples collected on a set of captive individuals that were resampled several times a few weeks apart. Our findings show the potential usefulness of deer as a sentinel for tracking the risk of exposure to Lyme disease Bbsl, although further investigation on the details of the antibody response to Bbsl in this incompetent host would be useful. Our study also highlights the value of combining long-term capture-mark-recapture sampling and short-time analyses of serological data for wildlife populations exposed to infectious agents of relevance to wildlife epidemiology and human health.

Keywords: Borrelia burdorgferi sensu lato; Capreolus capreolus; Ixodes ricinus; capture–mark–recapture; disease ecology; serology; tick‐borne disease.

FIGURE 1

Location of the study sites in France. Trois‐Fontaines (TF) and Chizé (CH) are sites where a long‐term capture–mark–recapture of roe deer has been conducted and blood samples were available each year between 2010 and 2020. Gardouch (GA) is the site where four roe deer individuals in enclosures could be sampled repeatedly over a series of months.

FIGURE 2

Distribution of optical density (OD) measures at 450 nm of the modified anti‐Bbsl ELISA in roe deer sampled at TF and CH. The distribution is bimodal, with low values corresponding to seronegative sera samples and high values to seropositive sera samples. The histogram presents the normalized counts of individuals, and the curves correspond to the probability density function of two fitted normal distributions. The dotted line represents the threshold of seropositivity, defined as the mean value of the negative distribution plus 2 times its standard deviation: 1.146 for TF and for CH.

FIGURE 3

Change in roe deer seroprevalence against Bbsl between 2010 and 2020 for individuals of TF (a) and CH (b). The error bars in black represent the standard error of the mean.

FIGURE 4

Annual survival and transition rates estimated from the CMR analyses conducted in both sites from the best model. Based on a previous demographic work, the sex effect was not considered on the survival for juvenile individuals (i.e. ψ = a2) (Gaillard et al., 1997). In the other age classes, survival is represented in dark grey for females and in light grey for males in TF (a) and CH (b). The seroconversion and seroreversion rates were estimated from the best model including the time on the annual serological rates of change (c). Error bars for each bar plot represent the standard errors.

FIGURE 5

Dynamics of antibody levels against Bbsl were assessed via repeated sampling of four individuals in the experimental platform of GA from October 2020 to July 2021. OD values are represented by orange points (individual 1), blue points (individual 2), green points (individual 3), yellow points (individual 4). The red full line represents the seropositivity threshold (OD = 1.146).