What would be the impact on the rabies risk of reducing the waiting period before dogs are imported? A modelling study based on the European Union legislation.

AIMS: Lyssavirus rabies (RABV) is responsible for a major zoonotic infection that is almost always lethal once clinical signs appear. Rabies can be (re)introduced into rabies-free areas through transboundary dog movements, thus compromising animal and human health. A number of measures have been implemented to prevent this happening, one of which is the waiting period (WP) after anti-rabies vaccination and serological testing. This WP ensures that antibodies assessed through the serological test are due to the vaccine, not to infection. Indeed, if antibodies are due to RABV infection, the dog should display clinical signs within this WP and would not therefore be imported. METHODS AND RESULTS: Within a framework of quantitative risk assessment, we used modelling approaches to evaluate the impact of this WP and its duration on the risk of introducing rabies via the importation of dogs into the European Union. Two types of models were used, a classical stochastic scenario tree model and an individual-based model, both parameterised using scientific literature or data specifically applicable to the EU. Results showed that, assuming perfect compliance, the current 3-month waiting period was associated with a median annual number of 0.04 infected dogs imported into the EU. When the WP was reduced, the risk increased. For example, for a 1-month WP, the median annual number of infected dogs imported was 0.17 or 0.15 depending on the model, which corresponds to a four-fold increase. CONCLUSION: This in silico study, particularly suitable for evaluating rare events such as rabies infections in rabies-free areas, provided results that can directly inform policymakers in order to adapt regulations linked to rabies and animal movements.

Quantitative risk assessment of rabies being introduced into mainland France through worldwide noncommercial dog and cat movements.

France has been rabies-free among nonflying mammals since 2001. Despite this status, the rabies virus has been introduced several times through noncommercial pet movements, posing a threat of infection by this 100%-lethal zoonosis among local animal and human populations. To quantify the risk of rabies being introduced through worldwide noncommercial dog and cat movements, we performed a quantitative risk assessment using stochastic scenario tree modeling. The mean annual probability of at least one rabies introduction incident was 0.35 (median: 0.24, 90% prediction interval (PI) [0.04; 0.98]) and the mean annual number of rabies-infected pets introduced through pet movements was 0.96 (median: 0.27, 90% PI [0.04; 3.88]). These results highlight a nonnegligible, even high risk due to the associated consequences of such events. In alternative scenario testing, preventive anti-rabies vaccination proved to be an effective measure since removing the vaccination requirement led to a > 15-fold increase in risk. The serological testing requirement had less of an effect (approximately two-fold increase when removed) and the posttest waiting period to ensure that antibodies were not linked to an infection had a negligible effect. Any change in pet owner compliance, especially regarding vaccination, could have a major impact on the risk. This study also shows that reinforced border control staff training could be more effective in reducing risk than more frequent checks. These results provide quantitative data for assessing the probability of the rabies virus entering France, and could help policymakers decrease this risk in rabies-free areas.

Management practices of dog and cat owners in France (pet traveling, animal contact rates and medical monitoring): Impacts on the introduction and the spread of directly transmitted infectious pet diseases.

A number of owner practices among the pet dog and cat population can influence the dynamics of directly transmitted infectious dog and cat diseases, including zoonotic ones. To better depict these management practices, which include pet traveling, contact rates with other companion animals and their medical monitoring (which herein includes prevention aspects), we surveyed 2,122 dog- and/or cat-owning French households through an anonymous online questionnaire. Trips with dogs within the European Union (EU) were frequent, while cats travelled less frequently within the EU and both cats and dogs travelled less frequently outside the EU. Recurrent illegal trips with dogs and cats (non-compliant with regulatory measures) were observed in a context of non-systematic pet border controls. We found that a large proportion of dogs are taken for walks in metropolitan France, with frequent intraspecific contacts (1.4 contacts/day on average), but only a minority (1.4%) of dogs were allowed to roam freely. On the other hand, 59.7% of cat owners allowed their cats to roam freely. We classified pet owners according to different profiles, some of which may be considered 'at risk' for directly transmitted infectious pet diseases. Indeed, one dog owner profile and one cat owner profile depict 'spreaders' of pet diseases (high connectivity with other individuals, little medical monitoring but no traveling) and another dog owner profile describes a potential 'introducer' and 'spreader' of pet diseases (foreign travel, high connectivity with other individuals, and intermediate medical monitoring). While these 'at risk' profiles represent only a minority of French pet owners, they should be better characterized to reinforce targeted prevention designed to minimize the risk of (re)introduction and (re)emergence of directly transmitted infectious dog and cat diseases in France, especially when considering zoonoses with a significant potential impact, such as rabies.

Benefit-Risk Assessment of the French Surveillance Protocol of Apparently Healthy Biting Dogs and Cats for Human Rabies Prevention.

In France, apparently healthy dogs and cats that bite humans must undergo an observation period of 15 days with three veterinary visits to ascertain that they remain healthy, indicating that no zoonotic transmission of rabies virus occurred via salivary presymptomatic excretion. This surveillance protocol is mandatory for all pets that have bitten humans, despite France's rabies-free status in non-flying mammals (i.e., a very low rabies risk). In this context, we aimed to perform a benefit-risk assessment of the existing regulatory surveillance protocol of apparently healthy biting animals, as well as alternative surveillance protocols. A scenario-tree modelling approach was used to consider the possible successions of events between a dog or cat bite and a human death attributed to either rabies or to lethal harm associated with the surveillance protocol (e.g., lethal traffic accidents when traveling to veterinary clinics or anti-rabies centers). The results demonstrated that the current French surveillance protocol was not beneficial, as more deaths were generated (traffic accidents) than avoided (by prompt post-exposure prophylaxis administration). We showed here that less stringent risk-based surveillance could prove more appropriate in a French context. The results in this study could allow policy-makers to update and optimize rabies management legislation.

Evaluation of the Worldwide Occurrence of Rabies in Dogs and Cats Using a Simple and Homogenous Framework for Quantitative Risk Assessments of Rabies Reintroduction in Disease-Free Areas through Pet Movements.

Dog and cat rabies cases imported from rabies enzootic countries represent a major threat for areas that have acquired rabies-free status and quantitative risk analyses (QRAs) are developed in order to assess this risk of rabies reintroduction through dog and cat movements. Herein we describe a framework to evaluate dog and cat rabies incidence levels in exporting countries along with the associated uncertainty for such QRAs. For enzootic dog rabies areas (EDRAs), we extended and adapted a previously published method to specify the relationship between dog rabies vaccination coverage and canine rabies incidence; the relationship between dog and cat rabies incidences; and then to predict annual dog and cat rabies incidences. In non-enzootic dog rabies areas (nEDRAs), we provided annual incidence based on declared dog and cat rabies cases. For EDRAs, we predicted an annual incidence potentially greater than 1.5% in dogs and about ten times lower in cats with a high burden in Africa and Asia but much lower in Latin America. In nEDRAs, the occurrence of rabies was lower and of similar magnitude in dogs and cats. However, wildlife could still potentially infect dogs and cats through spillover events. This framework can directly be incorporated in QRAs of rabies reintroduction.

Investigation of field intradermal tuberculosis test practices performed by veterinarians in France and factors that influence testing.

Bovine tuberculosis infection remains at a low but persistent level in French cattle herds and requires for its surveillance the use of tests with limited sensitivity and specificity. It thus appears essential to understand the reality of the field situation, to identify parameters which could affect how veterinarians perform these tests and how it can affect the sensitivity of the bovine tuberculosis surveillance system. We surveyed rural veterinarians (n = 1084), major stakeholders of the bovine tuberculosis surveillance system, after judgement (non-random) sampling to investigate their skin-test practices and their perception of the surveillance and control programs for this disease. The response rate was 19.4% (210/1084). The responses highlighted that veterinarians were aware of the importance of the fight against bovine tuberculosis and were resilient to the challenges and issues faced during fieldwork. However, we identified several areas of noncompliance with regulatory recommendations, particularly regarding the choice of injection site, verifying the quality of the injection, the method of test reading, and the reporting of non-negative test results. Multivariate analysis showed that veterinarians who had worked for fewer years in large-animal practice had better skin-test procedures. A higher proportion of performed comparative tests and a more positive perception of surveillance and control programs by veterinarians were associated with better skin-test practices. The areas of noncompliance identified in this study could be detrimental to the sensitivity of bovine tuberculosis surveillance but our results suggest that improving the information provided to veterinarians and increasing their awareness are feasible solutions to improve the surveillance efficacy.