SARS-Coronavirus (CoV)-2 and cats

edited 23 April, 2020 (1)

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). 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)

HostAlphaBetaGammaDelta
HumanHuman CoV-229E,
Human CoV-NL63
Human CoV OC43,
Human CoV- HKU1
Bat origin (outbreaks in humans)SARS-CoV-2,
SARS-CoV,
Middle East Respiratory Syndrome-related CoV
FelidsFeline CoV
CaninesCanine enteric CoVCanine respiratory CoV
PorcinesPorcine epidemic diarrhoea,
Porcine respiratory CoV,
Transmissible gastroenteritis virus
Porcine haemagglutinating encephalomyelitis virusPorcine CoV HKU15
RuminantsBovine CoV,
Antelope CoV,
Giraffe CoV
EquidsEquine CoV
BatVarious bat CoVsThree bat CoVs
AvianTurkey CoV,
Infectious bronchitis virus
Nine avian CoVs
RodentsMurine CoV, Rat CoV
VariousHedgehog CoV HKU31,
Pangolin CoV
Beluga whale CoV-SW1

 

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.

 

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 ACE2 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 ACE2 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 and 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 on Vero 118 cells 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 4 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 2 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 ACE2 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 2 dogs in this apartment block over 14 days, after their owners were diagnosed with SARS; 8 cats and 1 of the dogs tested RT-PCR-positive. Spontaneous infection of cats from another 3 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 1 RT-PCR-positive cat from one household and in 4/5 cats (including 3 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 (5 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 (23 April, 2020), there have been a few isolated reports of domestic animals that tested positive for SARS-CoV-2 and were presumed to be infected from their owners who had symptoms of COVID-19. 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 has conducted tests on dogs and cats from households with confirmed human COVID-19 cases or persons in close contact with confirmed patients. At the time of writing (23 April, 2020), 2 of 30 dogs and one of 17 cats that had been placed in quarantine in Hong Kong have tested RT-PCR-positive for SARS-CoV-2 RNA (WSAVA 2020); antibodies were also detected in both of the dogs (ProMED, 2020d). In addition, one cat (also with an owner with COVID-19) tested positive in Belgium, as well as two cats in New York (ProMED- COVID-19 update (113) USA (NY) cats).

 

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 3 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 third animal to test positive, also 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 has not shown any signs of disease.

 

Recently, a cat living in Belgium with its owner, who was confined in isolation 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 (23 April, 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 cats in New York (ProMED, 2020e). The owner of one cat tested positive for COVID-19, but the second cat came from a household in which there were no confirmed cases of COVID-19. Both cats displayed respiratory signs. 

 

Prevalence of SARS-CoV-2 infection in domestic animals

 

The commercial diagnostic laboratory IDEXX conducted a survey on more than 4,000 canine, feline and equine samples collected from USA and South Korea, but did not detect any positive pet samples (www.idexx.com/en/veterinary/reference-laboratories/idexx-sars-cov-2-covid-19-realpcr-test/, EVAg, 2020; IDEXX, 2020) using a real-time RT-PCR test to detect SARS-CoV-2 that was based on a unique alignment to the published viral sequences from the human outbreak.

 

The patient samples included swabs (mostly deep pharyngeal and conjunctival swabs) and faeces and had been submitted from 14 February to 12 March, 2020, from across the United States and South Korea. The specimens had been submitted for testing for agents causing canine, feline or equine respiratory disease, or feline, canine or equine diarrhoea. Specimens were also tested in parallel with three assays from the Center of Disease Control and Prevention (CDC). No positive results were detected in any specimens (www.idexx.com/en/veterinary/reference-laboratories/idexx-sars-cov-2-covid-19-realpcr-test/). 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.

 

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 2 Malayan tigers, 2 Amur tigers (Pantheratigris altaica), and 3 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 3 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.

 

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. 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 can be transmitted from cats to humans.

 

Stability of coronaviruses

 

Coronaviruses 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, coronaviruses appear to be more stable in dry conditions compared to many other enveloped viruses, remaining infectious for longer periods of time on surfaces; this is why they are used frequently to test chemical disinfectants. 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 9 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, coronaviruses 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 generally not recommended that cats are tested for SARS-CoV-2 infection as tests and reagents are being prioritised for human testing and the CDC has developed recommendations to help identify situations that may warrant SARS-CoV-2 testing in animals. Testing for SARS-CoV-2 in pets is available in the US (https://www.idexx.com/en/veterinary/reference-laboratories/idexx-realpcr-tests/idexx-sars-cov-2-covid-19-realpcr-test/), as long as public health and animal health officials agree to proceed with testing (CDC, 2020). In households where people have COVID-19 symptoms or test positive for SARS-CoV-2, cats are at risk of infection. In such cases strict hygiene measures should be followed to prevent human-to-cat transmission.

 

Testing of cats can be performed in some countries in special situations, such as in COVID-19 households, but, elsewhere, testing is reserved for hospitalised human patients and healthcare workers. RT-PCR tests are used to detect viral RNA in swabs and ELISA tests can be used 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 pet cats and dogs should be avoided in households where people are infected with SARS-CoV-2 or have symptoms of COVID-19. If any owner with COVID-19 must continue to care for their pet while ill, they should maintain basic hygiene measures, which include 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 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 we have 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, 2020).

 

ABCD emphasises that there is currently no evidence that cats can 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.

 

 

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