Designing a Syndromic Bovine Mortality Surveillance System: Lessons Learned From the 1-Year Test of the French OMAR Alert Tool.

Between May 2018 and 2019, a syndromic bovine mortality surveillance system (OMAR) was tested in 10 volunteer French départements (French intermediate-level administrative unit) to assess its performance in real conditions, as well as the human and financial resources needed to ensure normal functioning. The system is based on the automated weekly analysis of the number of cattle deaths reported by renderers in the Fallen Stock Data Interchange Database established in January 2011. In our system, every Thursday, the number of deaths is grouped by ISO week and small surveillance areas and then analyzed using traditional time-series analysis steps (cleaning, prediction, signal detection). For each of the five detection algorithms implemented (i.e., the exponentially weighted moving average chart, cumulative sum chart, Shewhart chart, Holt-Winters, and historical limits algorithms), seven detection limits are applied, giving a signal score from 1 (low excess mortality) to 7 (high excess mortality). The severity of excess mortality (alarm) is then classified into four categories, from very low to very high, by combining the signal scores, the relative excess mortality, and the persistence of the signal(s) over the previous 4 weeks. Detailed and interactive weekly reports and a short online questionnaire help pilot départements and the OMAR central coordination cell assess the performance of the system. During the 1-year test, the system showed highly variable sensitivity among départements. This variability was partly due not only to the demographic distribution of cattle (very few signals in low-density areas) but also to the renderer's delay in reporting to the Fallen Stock Data Interchange Database (on average, only 40% of the number of real deaths had been transmitted within week, with huge variations among départements). As a result, in the pilot départements, very few alarms required on-farm investigation and excess mortality often involved a small number of farms already known to have health or welfare problems. Despite its perfectibility, the system nevertheless proved useful in the daily work of animal health professionals for collective and individual surveillance. The test is still ongoing for a second year in nine départements to evaluate the effectiveness of the improvements agreed upon at the final meeting.

Was the French clinical surveillance system of bovine brucellosis influenced by the occurrence and surveillance of other abortive diseases?

The bovine brucellosis clinical surveillance system implemented in France aims to detect early any case of bovine brucellosis, a disease of which the country has been declared free since 2005. It relies on the mandatory notification of every bovine abortion. Following the spread of the Schmallenberg virus (SBV) in France in 2012 and 2013, and the implementation in 2012 of a clinical surveillance programme of Q fever based on abortion notifications in ten pilot départements, our objective was to study whether these two events influenced the brucellosis clinical surveillance system. The proportion of notifying farmers was analyzed over each semester from June 1, 2009 to June 30, 2013 according to the size and production type of herds, SBV status of départements and the implementation of the Q fever surveillance. Our analysis showed a slight increase in the proportion of notifying farmers as départements became infected by SBV, and after the implementation of Q fever surveillance (during the first semester of 2013). These variations might be explained by an increase in abortion occurrence (congenital deformities in newborns, due to SBV) and/or by an increase in farmers' and veterinarians' awareness (due to the spread of SBV and the implementation of the Q fever surveillance). These results highlight the difficulties in interpreting variations in the proportion of notifying farmers as a consequence of an increase in abortion occurrence. As bovine abortion surveillance can play an important role in the early warning for several diseases, there is a need to explore other ways to monitor abortions in cattle, such as syndromic surveillance using the dates of artificial insemination or calving data.

Spread and impact of the Schmallenberg virus epidemic in France in 2012-2013.

BACKGROUND: The Schmallenberg virus (SBV) emerged in Europe in 2011 and caused a widespread epidemic in ruminants.In France, SBV emergence was monitored through a national multi-stakeholder surveillance and investigation system. Based on the monitoring data collected from January 2012 to August 2013, we describe the spread of SBV in France during two seasons of dissemination (vector seasons 2011 and 2012) and we provide a large-scale assessment of the impact of this new disease in ruminants. RESULTS: SBV impact in infected herds was primarily due to the birth of stillborns or deformed foetuses and neonates. Congenital SBV morbidity level was on average moderate, although higher in sheep than in other ruminant species. On average, 8% of lambs, 3% of calves and 2% of kids born in SBV-infected herds showed typical congenital SBV deformities. In addition, in infected herds, farmers reported retrospectively a lower prolificacy during the vector season, suggesting a potential impact of acute SBV infection during mating and early stages of gestation. CONCLUSIONS: Due to the lack of available control and prevention measures, SBV spread quickly in the naive ruminant population. France continues to monitor for SBV, and updated information is made available online on a regular basis [http://www.plateforme-esa.fr/]. Outbreaks of congenital SBV are expected to occur sporadically from now on, but further epidemics may also occur if immunity at population level declines.

Assessment of vaccination by a phase I Coxiella burnetii-inactivated vaccine in goat herds in clinical Q fever situation.

A study was carried out to assess the efficacy of vaccination, using a phase I Coxiella burnetii-inactivated vaccine (Coxevac®; CEVA), within three goat herds experiencing Q fever abortions waves. The stratification of the population (n = 905) was based on parity and on infection status related to both serological and qPCR vaginal shedding results. Control (n = 443) and vaccinated (n = 462) groups were established in each farm. Vaccination was administered to does before mating and to kids after active immunity acquisition (at least 3­4 months old). The vaccine effectiveness was analyzed at subsequent farrowing on both clinical incidence and vaginal shedding at the delivery day. Among the 231 animals considered as susceptible, that is, seronegative nonshedders, about 90% were infected whatever the group, showing that vaccination did not prevent infection under high infection exposure. Fortunately, vaccination induced an overall decrease in shedding levels. A significant average difference between groups was estimated to 1.16 log(10) bacteria per swab for primiparous and even higher (1.81 log(10)) for initially susceptible ones. Thus, in a clinical context, vaccination should be implemented first in renewal animals. Indeed, young animals are those which best respond to vaccination by significantly reducing C. burnetii burden and, conversely, which excrete bacteria most massively if not vaccinated.

Coxiella burnetii vaginal shedding and antibody responses in dairy goat herds in a context of clinical Q fever outbreaks.

This study, carried out in three goat herds, was aimed at describing individual responses to Q fever infection in an abortive context, focusing on both antibody and shedding levels. Seroprevalence of Coxiella burnetii (Cb) infection and vaginal shedding of 1083 goats were investigated using ELISA and realtime qPCR assays, respectively. At the end of the outbreaks, a seroprevalence of 45.0% was found, and vaginal shedding appeared massive with levels above 10(4) Cb per swab in 42.3% of the whole population and above 10(6) Cb per swab for 90.9% of aborted goats. Susceptible animals (i.e. seronegative nonshedders) were unfrequent (31.2%), most of them being kids (94.7%). Seronegative females were predominant among nonshedders and conversely seropositive ones, predominant among high shedders (above 10(6) Cb per swab). Nevertheless, at least 43.3% of seronegative goats shed bacteria confirming the need of interpreting serology on a herd scale. The subsequent farrowing period was characterized by a significant reduction in the number of clinical cases. Females that had already aborted were more often involved than others. Shedding quantities remained high, particularly for primiparous does, mainly when facing infection for the first time. Thus, Q fever control must be based on both preventive measures directed to the preherd and environmental precautions.

Coxiella burnetii shedding routes and antibody response after outbreaks of Q fever-induced abortion in dairy goat herds.

Q fever is a zoonosis caused by Coxiella burnetii, a bacterium largely carried by ruminants and shed into milk, vaginal mucus, and feces. The main potential hazard to humans and animals is due to shedding of bacteria that can then persist in the environment and be aerosolized. The purpose of this study was to evaluate shedding after an outbreak of Q fever abortion in goat herds and to assess the relationship with the occurrence of abortions and antibody responses. Aborting and nonaborting goats were monitored by PCR for C. burnetii shedding 15 and 30 days after the abortion episodes. PCR analysis of all samples showed that 70% (n = 50) of the aborting and 53% (n = 70) of the nonaborting goats were positive. C. burnetii was shed into vaginal mucus, feces, and milk of 44%, 21%, and 38%, respectively, of goats that aborted and 27%, 20%, and 31%, respectively, of goats that delivered normally. Statistical comparison of these shedding results did not reveal any difference between these two groups. PCR results obtained for the vaginal and fecal routes were concordant in 81% of cases, whereas those for milk correlated with only 49% of cases with either vaginal or fecal shedding status. Serological analysis, using enzyme-linked immunosorbent assay (ELISA), indirect immunofluorescence assay (IFA), and complement fixation tests, showed that at least 24% of the seronegative goats shed bacteria. Positive vaginal and fecal shedding, unlike positive milk shedding, was observed more often in animals that were weakly positive or negative by ELISA or IFA. Two opposite shedding trends were thus apparent for the milk and vaginal-fecal routes. Moreover, this study showed that a nonnegligible proportion of seronegative animals that delivered normally could excrete C. burnetii.

Comparative diagnostic potential of three serological tests for abortive Q fever in goat herds.

Performances of an ELISA, an immunofluorescence assay (IFA) and a complement fixation test (CFT) were assessed for detecting antibodies against Coxiella burnetii after Q fever abortions in naturally infected goats. The goal of the study was to provide information useful for veterinary serodiagnosis in regard to categories of goats either experiencing Q fever abortion or not, blood sampling times and recommended cut-offs. The study was conducted on eight goat herds with evidence of C. burnetii abortions. In each herd, at least 5 goats that had aborted and 10 goats prior to parturition or at term were monitored 15, 30 and 60 days (D15, D30, D60) after the onset of Q fever abortion. The overall CFT results distribution did not differ between the two groups of goats and showed poor agreement with the ELISA results. In contrast, the ELISA and IFA results revealed comparable significant differences, but overall the ELISA test was slightly more sensitive than the IFA test. Seroprevalence, according to ELISA and IFA respectively, was higher in the aborting (88% and 82%) than in the non-aborting group (60% and 50%). High levels of serum antibodies were detected in goats post-abortion with an average of 114 %OD using ELISA and a log10(titer) of 2.4 using IFA. Strongly positive ELISA (%OD>80) and positive IFA results (log10(titers)>1.9) were significantly associated with abortion. Sampling on D15 gave the best association with ORs of 10 for ELISA and 6 for IFA. The practical interest of these results is discussed.