Discussion
According to this expert elicitation of knowledge, forty-six drivers of COVID-19 emergence in carnivore domestic pets (cats, dogs and ferrets) were ranked and aggregated into four homogenous groups. The first group of drivers categorised in the “very high importance” node, will be further discussed and it includes in decreasing order: availability and quality of diagnostic tools, human density close to pets, ability of preventive/control measures to stop the disease from entering the country or spreading (except for treatment, vaccination and reservoir(s) control), current species specificity of the disease causing agent and current knowledge on the pathogen. The sensitivity analysis indicated a limited effect of the experts involved in the elicitation, which shows that there is an acceptable robustness of the elicitation.
Considering as the highest driver of emergence of COVID-19 in pets, the availability and quality of diagnostic tools of COVID-19 infection in pets seemed to be critical (driver: D3-4). Currently, diagnostic tests are only available in specialized laboratories, e.g. polymerase chain reaction assay (PCR), virus neutralisation assay (VNT), microsphere immunoassay (MIT), enzyme-linked immunosorbent assay (ELISA) (e.g. Zhang et al., 2020; Sailleau et al., 2020). Indeed, the capacity to confirm a suspected case is very limited. Some of these laboratories are also often prioritise to diagnose human cases of COVID-19, and not animal cases. The PCR assay allows the specific detection of SARS-Cov-2 RNA and helps finding the source of infection (e.g. phylogenetic tree). Addition of serological assays would allow differentiating between environmental contamination (PCR positive and serological test negative) and (transient) infection (PCR positive or negative depending of the stage of infection but serological test positive) in pets. Another aspect is the usefulness to collect and share the different information on pets at national and international levels to be able to assess properly the true status of pets in the transmission of the COVID-19, based on evidence, and to guide both risk management and risk communication under the One Health approach. This is particularly important to avoid any inadequate behaviour of owners like panic abandonment of household pets. Recently, the OIE published guidelines for pet sampling (based on epidemiological contexts, e.g. close contact with a suspected or confirmed SARS-CoV-2-infected patient, or animal exposed to a known high-risk environment, and clinical presentation, e.g. clinical signs suggestive of SARS-Cov-2 infection), testing (based on validated tests, suitable for its intended use, which is essential when testing different species due to possible variation in sensitivity and specificity), and reporting of SARS-Cov-2 in animals (OIE, 2020). In addition, according to the Terrestrial Animal Health Code, the notification of COVID-19 cases in animals should be reported to the OIE as an emerging disease through the World Animal Health Information System (WAHIS).
The second most important driver was the human density close to pets (driver: D4-5). Indeed, humans have a strong effect on the introduction and spread of COVID-19 in pets. In Europe, at least 80 million households own at least one pet and the number of cats and dogs accounts for 103,828,000 and 85,184,000 heads, respectively. Around 25% of owners have at least one cat and 25%, one pet (FEDIAF, 2019). This percentage is not homogeneous and large disparities exists depending of the region for a same country. As an example, this percentage is higher in the Southern part (around 33% - more rural part) than in the Northern part (around 25%) of Belgium. No data on households with ferret are available at national level despite its important experimental susceptibility regarding the SARA-Cov-2. However, more studies are needed to assess properly the human density close to pets in Europe, in particular species by species.
The third most important driver was the ability of preventive/control measures to stop the disease from entering the country or spreading (containment of the pandemic), except for treatment, vaccination and reservoir(s) control (driver: D3-1). Most experts mentioned the current lack of sanitary certification, incomplete traceability of animals, ineffective disinfection measures, incomplete restriction of contacts between pets and wild animals and ineffective biosecurity measures. The main present interest of this driver is that the more human infection will be limited, the more risks of pet infections by humans will be reduced. Moreover reporting of all confirmed COVID-19 infections of pets should be mandatory. Additionally, several initiatives need to be emphasised to improve the situation like the OIE guidelines for sampling, testing and reporting of SARS-Cov-2 in animals (OIE, 2020) and several pet management recommendations given by national (e.g. Académie Nationale de Médecine, 2020) or international (e.g. American Veterinary Medical Association. 2020) expert committees. More evidence-base information and protocols should be stimulated and shared.
The fourth most important driver was the current species specificity of the disease-causing agent (driver: D1-2). The number of pet species susceptible to SARS-Cov-2 is not yet completely elucidated (OIE, 2020) but according to field studies, animals such as cats, dogs, ferrets, tigers, minks and small rodents have been identified as susceptible (e.g. Zhang et al., 2020; Almendros, 2020; Almendros & Gascoigne, 2020; American Veterinary Medical Association. 2020; van der Poel W., 2020).
In addition, experimental infections indicate a particular susceptibility of bats, cats and ferrets (Sit et al., 2020; Young-Il et al., 2020; Beer et al., 2020). The species specificity is related to the aptitude of the coronavirus to interact with the host receptor (Li, 2012). The receptor recognition mechanism of the SARS-Cov-2 regulates, in great part, its infectivity, pathogenesis and host range (Shang et al., 2020). SARS-CoV-2, SARS-CoV and RaTG13 (a bat coronavirus that is closely related to SARS-CoV-2) recognize the same receptor angiotensin-converting enzyme 2 (ACE2) in humans (Li et al., 2003; Li et al., 2005; Shang et al., 2020). However, some specific structural characteristics of the receptor-binding domain (RBD) of SARS-Cov-2 spike protein increase its ACE2-binding affinity (Shang et al., 2020). Differences among the three cited viruses in ACE2 recognition could contribute to explain their differential potentials for animal-to-human transmission, which appears more limited for SARS-CoV-2 & SARS-CoV1 than for MERS-CoV, but also for human-to-human transmission (conversely more reduced for MERS-CoV than for SARS-CoV-2 & SARS-CoV1), and eventually for human-to-animal transmission, which is supposed to occur for SARS-CoV2 only. With the exception of few works (Xu et al., 2009; Bao et al., 2020), more studies are needed to investigate the ACE2 receptor in various animal species. In addition, other unknown important factors conditioning animal-to-human and/or human-to-animal could deserve to be characterized (McNamara et al., 2020).
The fifth most important driver was the current knowledge on the pathogen (driver: D1-1). Scientific knowledge on the SARS-Cov2 is limited so far because it is still under characterization, even if it belongs to a well-known and studied family of pathogens. The pathogen includes multiple variants that are not characterised yet. A recent study on SARS-CoV-2 sequences (N = 95), from the first 3 months of the pandemic, reveals a beginning of diversification and phylogenetic clustering due to base substitutions and deletions in the genomes. This preliminary result should permit tracing of source infection but such variability could induce differences in virulence or antigenicity, with possible consequence in virulence (implication on population immunity) or antigenicity (implication on the diagnostic) (Kaden, 2020). This variability could also contribute to a change in species barriers, which could contribute to variants more adapted to pets and potentially to retransmission to humans (or to reduced zoonotic potential for these variants). More global studies are needed with good sharing of information to ensure progress in tracing of source infection and the development of accurate vaccines and diagnostic assays.
The methodology that was develop in this paper should be extended to a wide number of other diseases of pets, starting from cats and dogs, the two main species in households (FEDIAF, 2019). In addition, this expert elicitation of knowledge should be refined in the future (some months) when more evidence data will be available. In this case, addition of an uncertainty rate should be recommended during elicitation.