SARS-Coronavirus (CoV)-2 and cats

edited 2 August, 2020

These guidelines were drafted by Margaret J. Hosie, Katrin Hartmann, Regina Hofmann-Lehmann, Diane D. Addie, Uwe Truyen, Herman Egberink, Séverine Tasker, Tadeusz Frymus, Maria Grazia Pennisi, Karin Möstl et al.

 

Introduction

 

The coronavirus (CoV) that causes coronavirus disease 2019 (COVID-19) was first isolated in December 2019, in Wuhan City, Hubei province, China. The new virus is closely related to the severe acute respiratory syndrome coronavirus (SARS-CoV) that caused a disease outbreak in 2003, and has been named SARS coronavirus 2 (SARS-CoV-2). SARS-CoV-2 is a member of the genus Betacoronavirus, family Coronaviridae, order Nidovirales (Table 1). It is a new strain that has not previously been identified in humans or animals. SARS-CoV-2 did not emerge from any companion animal CoV; neither is it related to the commonly occurring feline coronavirus (FCoV) associated with feline infectious peritonitis. SARS-CoV-2 infection has spread to many countries worldwide, leading to the declaration of a pandemic by the World Health Organisation on 11 March 2020 (WHO, 2020).

 

Table 1 Classification of coronaviruses (CoVs)

 

Other human coronaviruses

 

To date, seven human coronaviruses (HCoVs) have been identified (Corman et al., 2018; Cui et al., 2019), as shown in Table 1. All can cause respiratory illnesses in humans, ranging in severity from asymptomatic infection or a mild, common cold to pneumonia and bronchiolitis.

 

In the last two decades there have been two major human disease outbreaks associated with coronaviruses: SARS (Drosten et al., 2003) and middle eastern respiratory syndrome (MERS) (Zaki et al., 2012). Both the SARS and MERS viruses evolved from viruses circulating in bats, the natural reservoir host of many CoV (Li et al., 2005; Ithete et al., 2013). Viruses with highly similar genetic sequences to SARS-CoV-2 have been isolated from bats, which indicates that, similar to previous CoV outbreaks, bats are a potential source of the new CoV. It is currently not clear whether transmission of SARS-CoV-2 occurred directly from bats to humans, or whether transmission occurred indirectly, via an intermediate host.

 

Three of these seven human coronaviruses (agents of MERS, SARS and COVID-19) can cause severe illnesses and death, although some infections in some individuals can be mild, or asymptomatic. The other four common human coronaviruses typically cause only mild respiratory illnesses in healthy human adults. However, they contribute to a third of common cold infections and can cause life-threatening illnesses in immunocompromised people.

 

Host range of SARS-CoV-2

 

The host range of a virus depends on several factors. The first step of viral infection occurs when the virus particle binds to a susceptible host cell via specific interactions between the receptor binding site on a viral protein and the virus receptor molecules on the host cell, a key determinant of the host range and tissue tropism of a virus.

 

Both SARS-CoV and SARS-CoV-2 utilise the angiotensin-converting enzyme 2 (ACE-2) molecule, a single-pass type I membrane protein, as the virus receptor for infection. ACE-2 is highly expressed in the lungs, arteries, heart, kidney and intestines; it is an important protein involved in blood pressure regulation. In addition to ACE-2, neuropilin-1 facilitates SARS-CoV-2 cell entry and provides a possible pathway into the central nervous system.

 

The viral receptor binding site lies in a domain on the spike protein (S), a glycoprotein that protrudes from the surface of the virus. The S protein and the viral receptor binding site have been well studied for SARS-CoV, and recently extensive sequence analysis studies and functional tests have been performed with SARS-CoV-2. The sequence of human SARS-CoV-2 is similar to that of CoVs circulating in bats (Zhou et al., 2020) that gave rise to SARS in 2002. Related viruses have been found in Malayan pangolins (Lam et al., 2020; Zhang et al., 2020a), indicating these imported animals might be intermediate hosts, although this has yet to be proven.

 

Three short regions of the ACE-2 molecule (3-11 amino acids long) have been identified that are involved in virus binding, and a comparative analysis of the sequences from different mammals, including humans, apes macaques, horse, swine, goat, sheep, bovine, cat, dog, rat, mouse, ferret, bat and civet, revealed some differences (Li et al., 2020). The sequences were identical for all apes, monkeys and humans, but differences were found in residues that are considered important for virus binding in other species. For cats and dogs, one residue in ACE-2 that is critical for virus binding was different and, most interestingly, the bat and civet sequences contained two critical residues that differed from the human sequence. Although differences in the ACE-2 sequences from different animals have been identified, the impact of these single amino acid changes on receptor binding and the susceptibility of other species to infection is not yet known. However, the high overall sequence identity could explain the relatively broad host range of SARS coronaviruses.

 

SARS-CoV infections in cats

 

SARS was first detected in 2002 and originated in a seafood market in Guangdong, China (Drosten et al., 2003; Ksiazek et al., 2003; Peiris et al., 2003). The causative agent, SARS-CoV, spread from China around the world (Guan et al., 2003; Lee et al., 2003; WHO, 2003b), but the outbreak was contained after approximately 9 months following strict infection control measures (Guan et al., 2003). The epidemic resulted in 8,096 reported human cases and 774 deaths in 27 countries (WHO, 2003b).

 

SARS-CoV has been shown to infect a wide range of species under experimental conditions, including masked palm civets (Wu et al., 2005), monkeys (Fouchier et al., 2003; Glass et al., 2004; McAuliffe et al., 2004; Subbarao et al., 2004; Wentworth et al., 2004; Roberts et al., 2005a; Miyoshi-Akiyama et al., 2011), mice (Liang et al., 2005; Roberts et al., 2005b; Zhao et al., 2007; Zaki et al., 2012), pigs, chickens (ProMED, 2020a), guinea pigs (Mohd et al., 2016), and Golden Syrian Hamsters (Cui et al., 2019; Donnelly et al., 2019). The prevalence of SARS-CoV infection in masked palm civets (Paguma larvata) that were raised for human consumption was high (Wang et al., 2005; Sun et al., 2020), and the animals developed neutralizing antibodies. Masked palm civets were considered to be transient accidental hosts (Kuiken et al., 2003; Chen et al., 2005), and were also confirmed as occasional direct sources of human infections (Qin et al., 2005; Shi and Hu, 2008; Sun et al., 2020).

 

Domestic cats can be infected experimentally with SARS-CoV and develop active infection, shedding, and pulmonary changes very similar to those seen in fatal human cases (Martina et al., 2003). In an experimental study, SARS-CoV was inoculated intratracheally in cats, with 106 median tissue culture infectious dose units (TCID50), which was obtained from a human patient who had died from SARS, and then passaged 4 times in vitro. Nasal, pharyngeal, and rectal swabs were collected from the cats on different days post-infection, but no clinical signs were observed following experimental infection. Virus could be isolated from pharyngeal swabs taken on days 2 to 8 post-infection and from nasal swabs taken on days 4 and 6 post-infection, but SARS-CoV was not detected in rectal swabs. Four cats were euthanised and necropsied at four days post infection, and SARS-CoV could be isolated from the trachea and lungs, confirming infection of the lower respiratory tract. However, quantification of the viral RNA in lung homogenates revealed only low amounts. All of the SARS-CoV-infected cats that were not euthanised developed neutralising antibodies (titres 40 to 320) by day 28 post-infection. Two uninfected cats that were housed together with SARS-CoV-infected cats tested positive for SARS-CoV by RT-PCR, with viral loads gradually increasing from two days post-infection onwards, peaking at days 6 to 8 post-infection. Two in-contact cats showed no clinical signs but developed antibodies by day 28 (Martina et al., 2003). In another study, in which cats were experimentally infected with 106 TCID50 SARS-CoV intratracheally, pulmonary lesions were also described (van den Brand et al., 2008). Histologically, SARS-CoV was detected in cells expressing the ACE-2 receptor, and the cats had developed diffuse alveolar damage and many pathological changes also seen in human SARS patients (van den Brand et al., 2008). One difference was that the cats developed also tracheo-bronchoadenitis, which has not been reported in humans (van den Brand et al., 2008; 2014). The data from the two studies demonstrated that domestic cats are susceptible to experimental infection with SARS-CoV, that the virus could be transmitted to other cats and that clinical signs and pathology were similar to those in humans (Martina et al., 2003; van den Brand et al., 2008).

 

Natural infection in field cats was also described during the first SARS outbreak, when domestic cats tested SARS-CoV-positive by RT-PCR (Kuiken et al., 2003; Rowe et al., 2004; Wang et al., 2005; Shi and Hu, 2008; He et al., 2013). In addition, domestic cats living in an apartment block in Hong Kong where 100 people contracted SARS-CoV infection, also tested RT-PCR-positive. However, final proof of direct transmission from humans to cats was lacking (Martina et al., 2003; WHO, 2003a; Lawler et al., 2006). Oropharyngeal and rectal swabs were collected from cats from a multiple cat household and from two dogs in this apartment block over 14 days, after their owners were diagnosed with SARS; eight cats and one of the dogs tested RT-PCR-positive. Spontaneous infection of cats from another three multiple pet households was demonstrated by RT-PCR of oropharyngeal and rectal swabs collected over a 14-day period (WHO, 2003a). SARS-CoV was also isolated from the cats, with the sequenced virus being indistinguishable from the human isolates (WHO, 2003a). Antibody testing using serum neutralisation assays confirmed SARS-CoV infection in one RT-PCR-positive cat from one household and in 4/5 cats (including three RT-PCR-positive cats) from another household. The cats were isolated and kept in household groups in single cages and in separate rooms while in isolation. There was limited evidence of spread in the isolation cages (five cats in close direct contact with these cats remained uninfected) (Martina et al., 2003; WHO, 2003a; Lawler et al., 2006). SARS-CoV was also detected in the bodies of cockroaches and in rodent droppings collected in this apartment block. Droppings and throat swabs of rats also tested RT-PCR-positive, but the rats showed no signs of disease (Legislative Council Select Committee, 2004). Cats might have been infected by feeding on cockroaches or rodents.

 

Evidence of human-to-domestic animal transmission of SARS-CoV-2

 

At the time of writing (2 August, 2020), there have been several sporadic reports of domestic animals from COVID-19 households that tested positive for SARS-CoV-2 and were presumed to be infected from their owners (Table 2). In addition, farmed mink have been reported to be infected on 27 mink farms in the Netherlands (as of 2 August, ProMED 2020q). COVID-19 symptoms were present in individuals working on the farms before clinical signs were observed in mink, and infection was confirmed in one hospitalised person (Oreshkova et al., 2020). It was suggested that the widespread infection amongst the mink followed the introduction of the virus by humans and subsequent transmission between the mink.

 

Evidence of mink-to-cat transmission

 

At the first mink farm found to be infected with SARS-CoV-2, antibodies against the virus were detected in three out of eleven farm cats, but no virus was isolated (ProMED, 2020j). Later, farm cats living on all four infected farms were sampled and seven of 24 cats tested antibody-positive; one cat tested positive for SARS-CoV-2 RNA.

 

Evidence of mink-to-human transmission of SARS-CoV-2

 

It was reported recently that two cases of mink-to-human transmission occurred on two different mink farms. These findings were based on phylogenetic analysis of sequences of the viruses in the infected mink and humans (Oreshkova et al., 2020) and are consistent with possible exposure of farm workers to virus in the environment that had been excreted by the infected mink. Subsequently it was decided to cull all mink in the affected farms (ProMED, 2020f, k).

 

Table 2 Reported SARS-CoV-2 RT-PCR positive animals (adapted from AVMA, 2020a)

[1]Also, three antibody-positive cats were recently suspected to have been infected with SARS-CoV-2 from infected mink (OIE, 2020c; ProMED, 2020m). [2]ProMED 2020h; [3]ProMED 2020e; [4]ProMED 2020n; [5]ProMED 2020o; [6]Sit et al., 2020; [7]ProMED 2020q; [8]ProMed 2020i; [9]Promed2020g; [&]Unpublished data (RHL/AK); [10] OIE 2020d

 

In Hong Kong, dogs and cats from households with infected people have been quarantined by the Hong Kong Agriculture, Fisheries and Conservation Department (AFCD) (Cheng, 2020). The AFCD (2020) conducted tests on dogs and cats from households with confirmed human COVID-19 cases or persons in close contact with confirmed patients. Two of 15 dogs (Sit et al., 2020) and one of 17 cats (WSAVA, 2020) from confirmed COVID-19 households that had been placed in quarantine in Hong Kong have tested RT-PCR-positive for SARS-CoV-2 RNA; antibodies were also detected in both of the dogs (ProMED, 2020d), and the viral sequences from the dogs were identical to those in the respective human contacts. In addition, one cat (also with an owner with COVID-19) tested positive in Belgium, two cats in France (ProMED, 2020g), one cat in Germany (ProMED, 2020h), one cat in Spain (Ruiz-Arondo et al., 2020), as well as two cats in New York (ProMED, 2020p).

 

The first suspected case of human-to-animal transmission of SARS-CoV-2 was a 17-year-old Pomeranian dog, which was quarantined in Hong Kong; this dog repeatedly tested RT-PCR-positive for SARS-CoV-2 at low levels, in swabs from the oral and nasal cavities (ProMED, 2020a, b). The dog remained RT-PCR-positive for 12 days after its removal from the household of its owner who had COVID-19. Sequencing showed high identity between the virus in the dog and its owner, suggesting spread from the human to the dog (ProMED, 2020c). Virus isolation from the dog was negative, indicating that no live virus was retrieved, which was consistent with the low amount of virus genetic material detected in the samples. The dog tested RT-PCR-positive for 12 days before testing negative, when it was sent home. The dog also developed antibodies, indicating that active virus replication had occurred, leading to the development of an immune response (ProMED, 2020d). The dog died three days after returning home without displaying any clinical signs of COVID-19. Since no post-mortem examination was conducted, it is not known whether the virus had induced any pathological changes; the cause of death was not determined, but the dog had comorbidities (ProMED, 2020c).

 

A second dog, a 2-year-old German Shepherd dog, owned by a COVID-19 patient from Hong Kong, repeatedly tested SARS-CoV-2 RT-PCR-positive in oral and nasal swabs. This dog did not show any clinical signs but seroconverted and virus isolation was successful. However, there was no virus transmission between this dog and a second dog in the household (WSAVA, 2020).

 

The first cat that tested positive in Hong Kong was a domestic short-haired cat that was quarantined when the owner was confirmed with COVID-19. Swabs collected from the oral and nasal cavities and the rectum tested positive for SARS-CoV-2 RNA. The cat did not show any signs of disease.

 

A cat living in Belgium with its owner, who was self-isolating after testing positive for SARS-CoV-2, developed clinical signs one week after the owner’s return from Italy. The cat’s clinical signs (anorexia, diarrhoea, vomiting, cough and shallow breathing) were compatible with a CoV infection (respiratory and/or digestive) and the cat tested positive for the SARS-CoV-2 RNA in successive samples of faeces and vomitus. Positive RT-PCR results were confirmed by sequencing. Nine days after the onset of clinical signs, the cat’s condition improved (Giet and Desmecht, 2020, unpublished). The test results were consistent with a high number of viral RNA genomic copies (D. Desmecht, personal communication), indicative of infection following human-to-cat transmission. However, the detection of SARS-CoV-2 RNA in the contents of the stomach and faeces of the cat should be interpreted with caution, since SARS-CoV-2 from the patient and the environment could have entered the gastrointestinal tract. At the time of writing (24 June, 2020), the results of antibody testing are not known, which would confirm whether or not a productive infection had occurred in this cat.

 

Two cases of SARS-CoV-2 infection were confirmed in US cats in New York by the CDC and the U.S. Department of Agriculture (USDA). These were the first reported companion animals with SARS-CoV-2 infection in the United States, originated from separate households and were epidemiologically linked to suspected or confirmed human COVID-19 cases in their respective households (MMWR, 2020).

 

Prevalence of SARS-CoV-2 infection in domestic animals

 

The commercial diagnostic laboratory IDEXX conducted a survey on canine, feline and equine swabs (mostly deep pharyngeal and conjunctival swabs) and faeces that had been submitted from 14 February to 12 March 2020, from across the United States and South Korea. No positive results were detected in any specimens (unpublished). However, it is possible that samples collected later in the pandemic, or from households in which COVID-19 had be identified, might show evidence of SARS-CoV-2 infections in dogs and cats.

 

Zhang et al. (2020b) reported, in a preprint on 1 April, 2020 (not yet peer-reviewed), that cats become infected with SARS-CoV-2 following natural exposure to infected people, with 15 of 102 (14.7%) cat sera collected following the outbreak in Wuhan testing positive for antibodies that recognised the receptor binding domain of SARS-CoV-2 by ELISA. The results of this study imply that cat populations could become infected in any region affected by the COVID-19 pandemic. The authors noted that sera from three cats known to be owned by COVID-19 patients, and therefore presumed to have close contact, demonstrated higher neutralising antibody titres compared to sera collected from either hospitalised or stray cats. Although the mechanism of transmission to stray cats is not fully understood, stray cats could have become infected via SARS-CoV-2 contamination of their environment, from COVID-19 patients who fed the cats, or even as a result of cat-to-cat transmission.

 

A study conducted in a veterinary community of 20 students, two of whom tested positive for COVID-19, while eleven of the remaining 18 displayed symptoms of COVID-19, demonstrated that none of the nine cats and none of the twelve cats living in the community tested positive by RT-PCR and none of the cats or dogs developed antibodies (Temman et al., 2020), suggesting that human-to-domestic animal transmission is variable, and is likely minimised where good hygiene is practised.

 

Evidence of human-to-non-domestic cat transmission of SARS-CoV-2

 

SARS-CoV-2 infection of a non-domestic cat was first reported by the OIE on 4 April, 2020 (OIE, 2020a). Nasal and oropharyngeal swabs and tracheal wash samples collected from a 4-year-old female Malayan tiger (Panthera tigris jacksoni) with respiratory signs tested positive for SARS-CoV-2 RNA. The tiger was kept in the Wildlife Conservation Society's (WCS) Bronx Zoo, where two Malayan tigers, two Amur tigers (Pantheratigris altaica), and three African lions (Panthera leo) had developed respiratory signs over the course of a week and showed clinical improvement following supportive treatment. On 15 April 2020, one of the three lions was confirmed positive for SARS-CoV-2 (OIE, 2020b). As there had been no new animal introductions for several years, it was presumed that SARS-CoV-2 was transmitted to the tiger from a SARS-CoV-2-infected keeper who was either asymptomatic or pre-symptomatic at the time of exposure. Subsequently all of the tigers and lions in the group tested positive when faecal samples were examined (ProMED, 2020i).

 

Experimental infection of cats with SARS-CoV-2

 

It has been shown that cats, ferrets and Golden Syrian hamsters can be infected experimentally with SARS-CoV-2 (Shi et al., 2020; Chan et al., 2020; Richard et al., 2020). Shi et al. (2020) demonstrated that cats, ferrets, and (to a lesser extent) dogs were susceptible to infection, but not pigs, chickens or ducks. When 8-month-old domestic cats were infected intranasally with 105 PFU of SARS-CoV-2 isolated from a human patient, viral RNA was detected in the upper respiratory tract, small intestine and faeces; infectious virus was found only in the upper respiratory tract, but not from the tissues tested. When the same high dose of virus was used to infect 10-14-week-old kittens, viral RNA and infectious virus was detected in the upper respiratory tract, lung, small intestine and nasal washes, and histopathological changes were observed in the lungs, suggesting that SARS-CoV-2 replicates more efficiently in younger cats. One of three 10-14-week-old kittens died on day 3 after virus exposure. Three infected 10-14-week-old kittens and three infected 8-month-old domestic cats were housed individually in cages adjacent to uninfected cats. Subsequently, two animals that were in cages adjacent to experimentally infected cats became infected and developed antibodies; the exposed cats that became infected were one 10-14-week-old kitten and one 8-month-old domestic cat. However, as the exposed cats were in cages adjacent to the infected cats within an isolator, it was not clear whether the mode of transmission was via respiratory droplets or faeces, as the exposed cats might have also been exposed to virus in the faeces of the infected cats.

 

In another experimental study, three cats were inoculated with SARS-CoV-2 on day 0 and then cohoused, in pairs, with uninfected cats starting one day after inoculation (Halfmann et al., 2020).  The inoculated cats shed infectious virus in nasal swabs from day 1 to 3, until day 6 and the in-contact cats started shedding virus from day 3 to day 5. No virus was detected in rectal swabs and none of the cats displayed clinical signs, although all cats developed antibodies confirming infection.

 

These experimental studies showed that cats are susceptible to SARS-CoV-2 infection (Bosco-Lauth et al., 2020); however, the findings suggested that cats were unlikely to develop clinical disease under these experimental conditions. In addition, these studies demonstrated that cats develop a robust neutralising antibody response that prevented cats from being re-infected following a second viral challenge. Further studies will be required to determine how easily SARS-CoV-2 can be transmitted between cats. At present, there is no evidence that SARS-CoV-2 is transmitted from cats to humans.

 

Stability of coronaviruses

 

CoV are enveloped viruses and once the envelope is damaged or destroyed, the virus is no longer infectious, which is why handwashing for at least 20 seconds with soap and water can prevent transmission of SARS-CoV-2. However, CoV appear to be more stable in dry conditions compared to many other enveloped viruses, remaining infectious for longer periods of time on surfaces. In addition, extraneous proteins in blood or faeces can protect viruses from inactivation, prolonging viral infectivity (Scott, 1988).

 

The stability of coronaviruses is variable on surfaces, with the SARS-CoV, a beta-coronavirus being slightly more stable than the alpha-coronavirus human coronavirus HCoV-229E (Rabenau et al., 2005a). A recent study compared the stability of SARS-CoV and SARS-CoV-2 in aerosols and on surfaces and found virtually identical results (van Doremalen et al., 2020), with both viruses remaining infectious on dry surfaces for up to 72 hours.

 

The nature of the surfaces, however, is crucial, and SARS-CoV-2 remains infectious for longer on plastic and stainless-steel compared to cardboard or copper surfaces (24-72 hours versus 8-24 hours, respectively) (van Doremalen et al., 2020)). For SARS, MERS and other human CoV, persistence was tested on different types of inanimate surfaces (summarized in Kampf et al., 2020): at room temperature persistence of several days was documented on metal, wood, paper, glass and plastic with a maximum of nine days on plastic in one study (Rabenau et al., 2005a). SARS-CoV and SARS-CoV-2 remained viable and infectious in aerosols for hours and on different surfaces for days; these results indicate that aerosol as well as fomite transmission of these viruses can be expected (van Doremalen et al., 2020).

 

As with all other known enveloped viruses, CoV are highly susceptible to common chemical disinfectants and are readily inactivated by e.g., alcohols, household bleach, benzalkonium, aldehydes, and others (Rabenau et al., 2005b; Kampf et al., 2020). Differences have been observed between cat litters concerning inactivation of the alpha-coronavirus FCoV. One study revealed that some cat litters, particularly those based on bentonite, can bind and might inactivate CoV shed in faeces and could help to reduce the FCoV load within infected households (Addie et al., 2020).

 

It is possible that cats could act as fomites when living in households with COVID-19 owners, although no studies have been published documenting the survival of SARS-CoV-2 on fur. Cats themselves should not be disinfected under any circumstances, only inanimate materials, as toxicity and burns can result from the inappropriate use of disinfectants that could be ingested during self-grooming.

 

Diagnosis

 

At present, it is recommended that cats should be tested for SARS-CoV-2 infection only following consultation with the appropriate public health authority, since recommendations are different between countries. Testing is available in several European countries, using RT-PC to detect viral RNA in swabs and ELISA tests to detect antibodies in serum or plasma. Virus isolation from swabs is restricted to specialist laboratories with containment level 3 facilities, as the isolation of SARS-CoV-2 poses a risk to laboratory staff.

 

Conclusion

 

Given the potential for infected owners to transmit virus to their pets, and the possibility that cats could act as fomites, close contact with cats (and dogs) should be avoided in households where people are infected with SARS-CoV-2 or have symptoms of COVID-19. If an owner with COVID-19 must continue to care for their pet while ill, they should maintain basic hygiene measures, which include handling animals only when wearing masks, washing their hands with soap and water for at least 20 seconds before and after being near or handling their animals, their food, or their supplies, as well as avoiding kissing their pets or sharing food or towels or the bed with them.

 

In light of recent reports of SARS-CoV-2 infections in some cats living in households with SARS-CoV-2 infected people, as well as the tiger that was presumed to be infected by its zookeeper, it is prudent to keep cats from SARS-CoV-2-infected households indoors, until there is a better understanding of how efficiently the virus is transmitted from humans to cats, whether cats can transmit virus to other cats under natural conditions, and whether virus could be transmitted from cats to humans. Any cat from a COVID-19 household should not be taken into another household. The American Veterinary Medical Association (AVMA) has developed detailed protocols that could be implemented to protect staff when they are exposed to high risk situations, such as when entering an infected person’s home or coming into proximity with a sick person. AVMA recommends that procedures should be consistent with the most up-to-date guidance from the relevant public health authorities (AVMA, 2020b).

 

ABCD emphasises that there is currently no evidence that cats transmit SARS-CoV-2 to humans. This guideline will continue to be updated regularly as new data become available. Pet owners should always maintain good hygiene practices and under no circumstances should cats be abandoned.

 

Acknowledgement

 

ABCD Europe gratefully acknowledges the support of Boehringer Ingelheim (the founding sponsor of the ABCD) and Virbac.

 

 

References

 

Addie D, Houe L, Maitland K, Passantino G, Decaro N (2020): Effect of cat litters on feline coronavirus infection of cell culture and cats. J Feline Med Surg 22(4), 350–357.

 

AFCD Press release (2020): https://www.news.gov.hk/eng/2020/03/20200331/20200331_220128_110.html; accessed 5 April, 2020.

 

AVMA (2020a): https://www.avma.org/resources-tools/animal-health-and-welfare/covid-19/depth-summary-reports-naturally-acquired-sars-cov-2-infections-domestic-animals-and-farmed-or?fbclid=IwAR3FHl3wpZuy7aT0THY1cVUf_SsisvT5jMZljtunGsd73-PX82hNBdi94-A

 

AVMA (2020b): https://www.avma.org/resources-tools/animal-health-and-welfare/covid-19/interim-recommendations-intake-companion-animals-households-humans-COVID-19-are-present" https://www.avma.org/resources-tools/animal-health-and-welfare/covid-19/interim-recommendations-intake-companion-animals-households-humans-COVID-19-are-present

 

Bosco-Lauth AM, Hartwig AE, Porter SM, Gordy PW, Nehring M, Byas AD, VandeWoude S, Ragan IK, Maison RM, Bowen RA (2020): Pathogenesis, transmission and response to re-exposure of SARS-1 CoV-2 in domestic cats. bioRxiv preprint doi: https://doi.org/10.1101/2020.05.28.120998

 

CDC (2020a): CDC 2019-Novel Coronavirus (2019-nCoV) real-time RT-PCR diagnostic panel instructions for use. Ed. Centers for Disease Control and Prevention, Division of Viral Diseases [online], www.fda.gov/media/134922/download. Updated March 15, 2020.

 

CDC (2020b): Research use only real-time RT-PCR protocol for identification of 2019-nCoV. Ed. Centers for Disease Control and Prevention, Division of Viral Diseases [online], www.cdc.gov/coronavirus/2019-ncov/lab/rt-pcr-detection-instructions.html. Updated March 14, 2020.

 

CDC (2020c): https://www.cdc.gov/coronavirus/2019-ncov/php/animal-testing.html#" https://www.cdc.gov/coronavirus/2019-ncov/php/animal-testing.html#

 

Chan JF, et al (2020):  https://www.ncbi.nlm.nih.gov/pubmed/32215622

 

Chen W, Yan M, Yang L, Ding B, He B, Wang Y, Liu X, Liu C, Zhu H, You B, Huang S, Zhang J, Mu F, Xiang Z, Feng X, Wen J, Fang J, Yu J, Yang H, Wang J (2005): SARS-associated coronavirus transmitted from human to pig. Emerg Infect Dis 11, 446-448.

 

Cheng L (2020): Coronavirus: Hong Kong’s infected dogs were asymptomatic and close contacts of confirmed patients, expert says. Ed. South China Morning Post [online], https://www.scmp.com/news/hong-kong/health-environment/article/3076480/ coronavirus-hong-kongs-infected-dogs-were.

 

Corman VM, Muth D, Niemeyer D, Drosten Ch (2018): Chapter Eight - Hosts and Sources of Endemic Human Coronaviruses. Advances Virus Res 100, 163-188. https://doi.org/10.1016/bs.aivir.2018.01.001].

 

Cui J, Li F, Shi ZL (2019): Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol 17, 181-192.

 

Donnelly CA, Malik MR, Elkholy A, Cauchemez S, Van Kerkhove MD (2019): Worldwide reduction in MERS Cases and Deaths since 2016. Emerg Infect Dis 25, 1758-1760.

 

Drosten C, Gunther S, Preiser W, van der Werf S, Brodt HR, Becker S, Rabenau H, Panning M, Kolesnikova L, Fouchier RA, Berger A, Burguiere AM, Cinatl J, Eickmann M, Escriou N, Grywna K, Kramme S, Manuguerra JC, Muller S, Rickerts V, Sturmer M, Vieth S, Klenk HD, Osterhaus AD, Schmitz H, Doerr HW (2003): Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348, 1967-1976.

 

Fouchier RA, Kuiken T, Schutten M, van Amerongen G, van Doornum GJ, van den Hoogen BG, Peiris M, Lim W, Stohr K, Osterhaus AD (2003): Aetiology: Koch's postulates fulfilled for SARS virus. Nature 423, 240.

 

Glass WG, Subbarao K, Murphy B, Murphy PM (2004): Mechanisms of host defense following severe acute respiratory syndrome-coronavirus (SARS-CoV) pulmonary infection of mice. J Immunol 173, 4030-4039.

 

Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX, Cheung CL, Luo SW, Li PH, Zhang LJ, Guan YJ, Butt KM, Wong KL, Chan KW, Lim W, Shortridge KF, Yuen KY, Peiris JS, Poon LL (2003): Isolation and characterization of viruses related to the SARS coronavirus from animals in Southern China. Science 302, 276-278.

 

Halfmann PJ, Hatta M, Chiba S, et al (2020): Transmission of SARS-CoV-2 in Domestic Cats. N Engl J Med 10.1056/NEJMc2013400. doi:10.1056/NEJMc2013400.

 

He WP, Li BA, Zhao J, Cheng Y (2013): Safety of convalescent sera for the treatment of viral severe acute respiratory syndrome: an experimental model in rhesus macaque. Chin Med J (Engl) 126, 3790-3792.

 

Ithete N, Stoffberg S, Corman V, Cottontail VM, Richards L, Schoeman M, et al (2013): Close Relative of Human Middle East Respiratory Syndrome Coronavirus in Bat, South Africa. Emerg Infect Dis 19(10),1697-1699. https://dx.doi.org/10.3201/eid1910.130946

 

Kampf G, Todt D, Pfaender S, Steinman E (2020): Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents. J Hosp Infect 104, 246-251.

 

Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc JW, Bellini WJ, Anderson LJ, Group SW (2003): A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Vet Med 348, 1953-1966.

 

Kuiken T, Fouchier RA, Schutten M, Rimmelzwaan GF, van Amerongen G, van Riel D, Laman JD, de Jong T, van Doornum G, Lim W, Ling AE, Chan PK, Tam JS, Zambon MC, Gopal R, Drosten C, van der Werf S, Escriou N, Manuguerra JC, Stohr K, Peiris JS, Osterhaus AD (2003): Newly discovered coronavirus as the primary cause of severe acute respiratory syndrome. Lancet 362, 263-270.

 

Lam TT, Shum MH, Zhu HC, Tong YG, Ni XB, Liao YS, Wei W, Cheung WY, Li WJ, Li LF, Leung GM, Holmes EC, Hu YL, Guan Y (2020): Identifying SARS-CoV-2 related coronaviruses in Malayan pangolins. Nature Mar 26. doi: 10.1038/s41586-020-2169-0. [Epub ahead of print], PMID: 32218527

 

Lawler JV, Endy TP, Hensley LE, Garrison A, Fritz EA, Lesar M, Baric RS, Kulesh DA, Norwood DA, Wasieloski LP, Ulrich MP, Slezak TR, Vitalis E, Huggins JW, Jahrling PB, Paragas J (2006): Cynomolgus macaque as an animal model for severe acute respiratory syndrome. PLoS Med 3, e149.

 

Lee N, Hui D, Wu A, Chan P, Cameron P, Joynt GM, Ahuja A, Yung MY, Leung CB, To KF, Lui SF, Szeto CC, Chung S, Sung JJ (2003): A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med 348, 1986-1994.

 

Legislative Council Select Committee, L.C.S. (2004): Chapter 8 Outbreak at the Amoy Gardens. In: Report of the Select Committee to inquire into the handling of the Severe Acute Respiratory Syndrome outbreak by the Government and the Hospital Authority July 2004. Ed. Legislative Council of the Hong Kong special administrative region of the people´s republic of China [online], https://www.who.int/csr/sars/en/ WHOconsensus.pdf, pp. 122-148.

 

Li R, Qiao S, Zhang G (2020): Analysis of angiotensin-converting enzyme 2 (ACE2) from different species sheds some light on cross-species receptor usage of a novel coronavirus 2019-nCoV. J Infect 80(4), 469-496. doi: 10.1016/j.jinf.2020.02.013. Epub 2020 Feb 21. No abstract available.  PMID: 32092392.

 

Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF (2005): Bats are natural reservoirs of SARS-like coronaviruses. Science 310(5748), 676-679.

 

Liang L, He C, Lei M, Li S, Hao Y, Zhu H, Duan Q (2005): Pathology of guinea pigs experimentally infected with a novel reovirus and coronavirus isolated from SARS patients. DNA Cell Biol 24, 485-490.

 

Martina BE, Haagmans BL, Kuiken T, Fouchie, RA, Rimmelzwaan GF, Van Amerongen G, Peiris JS, Lim W, Osterhaus AD (2003): Virology: SARS virus infection of cats and ferrets. Nature 425, 915.

 

McAuliffe J, Vogel L, Roberts A, Fahle G, Fischer S, Shieh WJ, Butler E, Zaki S, St Claire M, Murphy B, Subbarao K (2004): Replication of SARS coronavirus administered into the respiratory tract of African Green, rhesus and cynomolgus monkeys. Virology 330, 8-15.

 

Miyoshi-Akiyama T, Ishida I, Fukushi M, Yamaguchi K, Matsuoka Y, Ishihara T, Tsukahara M, Hatakeyama S, Itoh N, Morisawa A, Yoshinaka Y, Yamamoto N, Lianfeng Z, Chuan Q, Kirikae T, Sasazuki T (2011): Fully human monoclonal antibody directed to proteolytic cleavage site in severe acute respiratory syndrome (SARS) coronavirus S protein neutralizes the virus in a rhesus macaque SARS model. J Infect Dis 203, 1574-1581.

 

MMWR - Morbidity and Mortality Weekly Report of the Centre for Disease Control (2020), Vol 69, June 8, 2020.

 

Mohd HA, Al-Tawfiq JA, Memish ZA (2016): Middle East Respiratory Syndrome Coronavirus (MERS-CoV) origin and animal reservoir. Virol J 13, 87.

 

OIE (2020a) : https://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?page_refer=MapFullEventReport&reportid=33885

 

OIE (2020b): https://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?reportid=34054

 

OIE (2020c): Questions and Answers on the 2019 Coronavirus Disease (COVID-19).  (www.oie.int/en/scientific-expertise/specific-information-and-recommendations/questions-and-answers-on-2019novel-coronavirus), 2020.

 

OIE (2020d): https://www.oie.int/wahis_2/public/wahid.php/Reviewreport/Review?page_refer=MapFullEventReport&reportid=35182

 

Oreshkova N,  Molenaar RJ,  Vreman S,  Harders F, Munnink BBO, Hakze R, Gerhards N, Tolsma P, Bouwstra R, Sikkema R, Tacken M,  de Rooij MMT,  Weesendorp E,  Engelsma M,  Bruschke C, Smit LAM, Koopmans M, van der Poel WHM, Stegeman A (2020): SARS-CoV2 infection in farmed mink, Netherlands, April 2020. bioRxiv 2020.05.18.101493; doi: https://doi.org/10.1101/2020.05.18.101493

 

Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, Nicholls J, Yee WK, Yan WW, Cheung MT, Cheng VC, Chan KH, Tsang DN, Yung RW, Ng TK, Yuen KY, Group Ss (2003): Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361, 1319-1325.

 

ProMED (2020a): COVID-19 update (22): Companion animals, dog susp, RFI, 2020. Ed. International Society for Infectious Diseases [online], https://promedmail.org/ promed-post/?id=7036661.

 

ProMED (2020b): COVID-19 update (30): China (Hong Kong) dog, susp, serology pending, 2020. Ed. International Society for Infectious Diseases [online], https://prom edmail.org/promed-post/?id=7057595.

 

ProMED (2020c): COVID-19 update (37): China (Hong Kong) animals, dog, prelim. serology negative, 2020. Ed. International Society for Infectious Diseases [online], http://www.promedmail.org.

 

ProMED (2020d): COVID-19 update (56): China (Hong Kong) animal, dog,  final serology positive, 2020. Ed. International Society for Infectious Diseases [online], https://www.tephinet.org/promed-outbreak-alerts.

 

ProMED (2020e): COVID-19 update (123) USA (NY) cats

 

ProMED (2020f): COVID-19 update (215): Netherlands (NB) animal, mink-to-human, epidem, control

 

Promed (2020g): COVID-19 update (149): France (IF) animal, cat, owned https://promedmail.org/promed-post/?id=7289409

 

ProMED (2020h): COVID-19 update (181): GERMANY (BAVARIA), FRANCE (NOUVELLE-AQUITAINE), CAT, OIE ANIMAL CASE DEFINITION.  (https://promedmail.org/promed-post/?id=20200513.7332909), 2020.

 

Promed (2020i):COVID-19 update (143): USA (NY) animal, zoo, tiger, lion, tests, https://promedmail.org/promed-post/?id=7284183

 

ProMED (2020j): COVID-19 update (189): Netherlands (NB) animal, farmed mink, research, cat, dog. https://promedmail.org/promed-post/?id=20200517.7344274

 

ProMED (2020k): COVID-19 update (251): Netherlands (NB, LI) animal, farmed mink, spread, culling

 

ProMED (2020m): COVID-19 update (198): Netherlands (NB) farmed mink, animal-to-human infect susp.  (https://promedmail.org/promed-post/?id=20200520.7359976), 2020.

 

ProMED (2020n): CORONAVIRUS DISEASE 2019 UPDATE (166): CHINA (HONG KONG) ANIMAL, CAT, OIE, RESOLVED.  (https://promedmail.org/promed-post/?id=20200508.7314521), 2020.

 

ProMED (2020o): CORONAVIRUS DISEASE 2019 UPDATE (58): BELGIUM, ANIMAL, CAT, CLINICAL CASE, REQUEST FOR INFORMATION.  (https://promedmail.org/), 2020.

 

ProMED (2020p): COVID-19 update (113): USA (NY) animal, cat, susp, RFI

 

ProMED (2020q): COVID-19 update (340): animal, China, envir monitoring, Netherlands (NB), mink

 

Qin C, Wang J, Wei Q, She M, Marasco WA, Jiang H, Tu X, Zhu H, Ren L, Gao H, Guo L, Huang L, Yang R, Cong Z, Guo L, Wang Y, Liu Y, Sun Y, Duan S, Qu J, Chen L, Tong W, Ruan L, Liu P, Zhang H, Zhang J, Zhang H, Liu D, Liu Q, Hong T, He W (2005): An animal model of SARS produced by infection of macaca mulatta with SARS coronavirus. J Pathol 206, 251-259.

 

Rabenau HF, Cinatl J, Morgenstern B, Bauer G, Preiser W, Doerr HW (2005a): Stability and inactivation of SARS coronavirus. Med Microbiol Immunol 194(1-2):1-6. PMID:15118911.

 

Rabenau HF, Kampf G, Cinatl J, Doerr HW (2005b): Efficacy of various disinfectants against SARS coronavirus. J Hosp Infect 61(2), 107-11, PMID: 15923059.

 

Richard et al (2020): https://www.biorxiv.org/content/10.1101/2020.04.16.044503v1

 

Roberts A, Paddock C, Vogel L, Butler E, Zaki S, Subbarao K (2005a): Aged BALB/c mice as a model for increased severity of severe acute respiratory syndrome in elderly humans. J Virol 79, 5833-5838.

 

Roberts A, Vogel L, Guarner J, Hayes N, Murphy B, Zaki S, Subbarao K (2005b): Severe acute respiratory syndrome coronavirus infection of golden Syrian hamsters. J Virol 79, 503-511.

 

Rowe T, Gao G, Hogan RJ, Crystal RG, Voss TG, Grant RL, Bell P, Kobinger GP, Wivel NA, Wilson JM (2004): Macaque model for severe acute respiratory syndrome. J Virol 78, 11401-11404.

 

Ruiz Arondo et al (2020): Detection of SARS-CoV-2 in pets living with COVID-19 owners diagnosed during the COVID-19 lockdown in Spain: A case of an asymptomatic cat with SARS-CoV-2 in Europe. medRxiv preprint doi: https://doi.org/10.1101/2020.05.14.20101444

 

Scott FW (1988): Update on FIP.  Proc Kal Kan Symp 12, 43-47.

 

Shi J, Wen Z, Zhong G, Yang H, Wang Ch, Huang B, Liu R, He X, Shuai L, Sun Z, Zhao Y, Liu P, Liang L, Cui P, Wang J, Zhang X, Guan Y, Tan W, Wu G, Chen H, Bu Z (2020): Susceptibility of ferrets, cats, dogs, and other domesticated animals to SARS–coronavirus 2. Science 10.1126/science.abb7015.

 

Shi Z, Hu Z (2008): A review of studies on animal reservoirs of the SARS coronavirus. Virus Res 133, 74-87.

 

Sit THC, Brackman CJ, Ip SM, Tam KWS, Law PYT, To EMW, Yu VYT, Sims LD, Tsang DNC, Chu DKW, Perera RAPM, Poon LLM, Peiris M (2020): Infection of dogs with SARS-CoV-2. Nature. 2020 May 14. doi: 10.1038/s41586-020-2334-5. Online ahead of print.

 

Subbarao K, McAuliffe J, Vogel L, Fahle G, Fischer S, Tatti K, Packard M, Shieh WJ, Zaki S, Murphy B (2004): Prior infection and passive transfer of neutralizing antibody prevent replication of severe acute respiratory syndrome coronavirus in the respiratory tract of mice. J Virol 78, 3572-3577.

 

Sun Z, Thilakavathy K, Kumar SS, He G, Liu SV (2020): Potential Factors Influencing Repeated SARS Outbreaks in China. Int J Environ Res Public Health 17. pii: E1633. doi: 10.3390/ijerph17051633.

 

Temman S, Barbarino A, Maso D, Belhillil S, Enouf V, Huo C, Jaraud A, Chevallier L, Backovic M, Pérot P, Verwaerde P, Tiret L, van der Werf S, Eloit M (2020): Absence of SARS-CoV-2 infection in cats and dogs in close contact with a cluster of COVID-19 patients in a veterinary campus. BioRxiv preprint doi: https://doi.org/10.1101/2020.04.07.029090

 

Van den Brand JM, Haagmans BL, Leijten L, van Riel D, Martina BE, Osterhaus AD, Kuiken T (2008): Pathology of experimental SARS coronavirus infection in cats and ferrets. Vet Pathol 45, 551-562.

 

Van den Brand JM, Haagmans BL, van Riel D, Osterhaus AD, Kuiken T (2014): The pathology and pathogenesis of experimental severe acute respiratory syndrome and influenza in animal models. J Comp Pathol 151, 83-112.

 

Van Doremalen N, Bushmaker T, Morris DH, Holbrook MG, Gamble A, Williamson BN, Tamin A, Harcourt JL, Thornburg NJ, Gerber SI, Lloyd-Smith JO, de Wit E, Munster VJ (2020): Aerosol and Surface Stability of SARS-CoV-2 as Compared with SARS-CoV-1. N Engl J Med Mar 17. doi: 10.1056/NEJMc2004973. [Epub ahead of print] No abstract available. PMID: 32182409.

 

Wang M, Yan M, Xu H, Liang W, Kan B, Zheng B, Chen H, Zheng H, Xu Y, Zhang E, Wang H, Ye J, Li G, Li M, Cui Z, Liu YF, Guo RT, Liu XN, Zhan LH, Zhou DH, Zhao A, Hai R, Yu D, Guan Y, Xu J (2005): SARS-CoV infection in a restaurant from palm civet. Emerg Infect Dis 11, 1860-1865.

 

Wentworth DE, Gillim-Ross L, Espina N, Bernard KA (2004): Mice susceptible to SARS coronavirus. Emerg Infect Dis 10, 1293-1296.

 

WHO (2003a): Consensus document on the epidemiology of severe acute respiratory sondrome (SARS). Ed. World Health Organization: Department of Communicable Diseases Surveillance and Response [online], https://www.who.int/csr/sars /en/WHOconsen sus.pdf.

 

WHO (2003b): Summary of probable SARS cases with onset of illness from from 1 November 2002 to 31 July 2003, Ed. World Health Organization [online], www.who.int/csr/ sars/country /table 2004_04_21/en.

 

WHO (2020): WHO Director-General’s opening remarks at the media briefing on COVID-19-11 March 2020. https://www.who.int/dg/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19---11-march-2020

 

WSAVA (2020): Webinar: COVID-19 and companion animals - what we know today, 17. April 2020.

 

Wu D, Tu C, Xin C, Xuan H, Meng Q, Liu Y, Yu Y, Guan Y, Jiang Y, Yin X, Crameri G, Wang M, Li C, Liu S, Liao M, Feng L, Xiang H, Sun J, Chen J, Sun Y, Gu S, Liu N, Fu D, Eaton BT, Wang LF, Kong X (2005): Civets Are Equally Susceptible to Experimental Infection by Two Different Severe Acute Respiratory Syndrome Coronavirus Isolates. J Virol 79(4), 2620–2625. doi: 10.1128/JVI.79.4.2620-2625.2005

 

Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA (2012): Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367, 1814-1820.

 

Zhang Q, Zhang H, Huang K, Yang Y, Hui X, Gao J, He X, Li C, Gong W, Zhang Y, Peng C, Gao X, Chen H, Zou Z, Shi Z, Jin M (2020b): SARS-CoV-2 neutralizing serum antibodies in cats: a serological investigation. BioRxiv preprint doi: https://doi.org/10.1101/2020.04.01.021196.

 

Zhang T, Wu Q, Zhang Z (2020a): Probable Pangolin Origin of SARS-CoV-2 Associated with the COVID-19 Outbreak. Curr Biol Mar 13. pii: S0960-9822(20)30360-2. doi: 10.1016/j.cub.2020.03.022.

 

Zhao G, Ni B, Jiang H, Luo D, Pacal M, Zhou L, Zhang L, Xing L, Zhang L, Jia Z, Lin Z, Wang L, Li J, Liang Y, Shi X, Zhao T, Zhou L, Wu Y, Wang X (2007): Inhibition of severe acute respiratory syndrome-associated coronavirus infection by equine neutralizing antibody in golden Syrian hamsters. Viral Immunol 20, 197-205.

 

Zhou P, Yang X, Wang X et al (2020): A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579, 270–273.