Influenza virus infection in cats

 

Edited November 2020

 

These guidelines were published in J Feline Med Surg 2009; 11: 615-618 (Thiry et al., 2009). This completely new version was authored by Tadeusz Frymus.

 

Introduction

 

Influenza is a highly contagious, acute infection, usually of the upper respiratory tract, found worldwide in many vertebrate hosts (Krammer et al., 2018). Feline respiratory disease seems to be rare and usually self-limiting, but secondary bacterial infections may lead to complications, and can be associated with fatalities. Very rarely, highly pathogenic influenza virus strains may induce in cats a severe, generalized viral disease with high fatality rate (Thiry et al., 2007).

 

Virus

 

The virus is a member of Orthomyxoviridae family. Four types (A, B, C and D) of this agent are known. Influenza virus type A (IAV) is the most important one inducing worldwide mass disease in humans and a broad spectrum of animals including birds, horses, pigs, mink, ferrets, bats and marine mammals. Additionally, dogs and cats may be affected.

 

The IAV types are further classified as subtypes based on the antigenicity of the two viral surface proteins, haemagglutinin (H) and neuraminidase (N). There are at least 16 H and 9 N antigens (Krammer et al., 2018), and their different combinations result in 144 IAV subtypes (e.g. H1N1, H3N8, H5N2 etc.).

 

Influenza viruses are genetically highly variable, therefore rapidly changing their antigens, virulence, and ability to replicate in novel host species (Wille and Holmes, 2019). Two mechanisms are responsible for this: genetic drift and genetic shift. Genetic drift results from mutations in the genes encoding N or H producing a new antigenic variant of a given subtype. If replication of such a variant is less effectively inhibited by the host immunity that eliminated the infection caused by the original strain, the mutated virus may infect again the same population. In contrast, antigenic shift is a sudden emergence of a new subtype resulting from exchange (reassortment) of RNA fragments between 2 or more IAV subtypes replicating at the same time in a host (Wille and Holmes, 2019). Well recognized “mixing vessel” hosts for human IAVs are pigs and birds, but recent data suggest that also dogs and cats might potentially play such a role (Chen et al., 2018; Zhao S et al., 2020). Such new subtypes, that share pathogenic properties with their parental lineages and have a mixture of the surface antigens of the original strains, may be highly dangerous. As the target host population is often immunologically naïve to the new subtype, epidemics, or even pandemics, in different animal species and humans have been the outcome in the past (Krammer et al., 2018). Due to further selection pressure (genetic drift) a new subtype may evolve into multiple antigenic variants, grouped in sublineages or clades (He et al., 2019). All these genetic variability mechanisms are responsible for the permanent circulation of IAVs in avian and mammalian populations.

 

Influenza viruses are quickly inactivated by UV-light, detergents and disinfectants. However, in water IAV remains infectious for weeks to months depending on pH, salinity, and temperature (Irwin et al., 2011, Keeler et al., 2012).

 

Circulation of IAVs

 

Among 144 possible IAV subtypes the vast majority have been found in waterfowl (especially ducks, geese, and swans), their natural host (Sonnberg et al., 2013). Birds, often subclinically infected, may shed IAVs also with faeces, and their seasonal migrations are crucial for the circulation of IAVs in the world (Fig. 1). In ice (e.g. of northern lakes) the virus may overwinter, which enables re-emergence of influenza in the next season.

 

Fig. 1. Emergence of influenza A virus from aquatic wild bird reservoirs (after Krammer et al., 2018).

 

Generally, IAVs isolated from a given species are able to replicate effectively in this host. Thus, the terms “human strains”, “avian strains”, “equine strains” etc. are commonly used. However, their high genetic variability facilitates adaptation to other host species, inducing “novel” influenza outbreaks in it. Examples for this are well documented epidemics of human influenza that emerged from pigs (Krammer et al., 2018), or canine outbreaks induced by equine H3N8 IAV (Crawford et al., 2005; Crawford et al., 2011), and especially several influenza epidemics in different mammals that were generated by avian viruses, like the canine and feline outbreaks caused by H3N2 or H7N2 IAVs (Song et al., 2008; Newbury et al., 2017).

 

On the other hand, variability allows not only the emergence of new viral strains, but also the disappearance of established ones, like H7N7 equine IAV that has not been isolated from horses since 1979 (Webster, 1993), or H3N8 canine influenza virus (CIV) that circulated continuously among dogs in USA for 15 years but since 2016 has been very rarely found (Wille and Holmes, 2019).

 

Pathogenesis of influenza

 

Most IAV strains induce acute upper respiratory tract infections that are either self-limiting or subclinical (Krammer et al., 2018). Though secondary bacterial infections or other complications may result from IAV infection, these agents are called “low pathogenic strains”. In humans, horses, pigs, dogs and some other mammalian species they replicate only in the upper respiratory tract inducing the common “seasonal” flu. After an incubation period of 1 to a few days, inflammation of the bronchial epithelium leads to necrotic lesions, exudate, and lung hyperemia. Most cases recover after 1 to 3 weeks but in some bacterial complications may result in pneumonia; this occurs especially in poor conditions, during stress, in the very young as well as the old. The fatality rate is <1% in most infections (Wasik et al., 2019). Such a natural feline disease has been very rarely seen (Song et al., 2011; Fiorentini et al., 2011; Jeoung et al., 2013). Experimental infection of cats with low pathogenic IAVs hardly ever induced disease, but subclinical replication usually occurred for a few days (Hinshaw et al., 1981; Paniker and Nair, 1970; Romváry et al., 1975).

 

In contrast, appearing mostly in birds, highly pathogenic strains of IAVs are able to replicate not only in the respiratory tract, but also in the gastrointestinal tract, muscles, heart, brain and other organs resulting in acute, systemic disease that can be associated with a high fatality rate. They often induce sudden, mass mortality of chicken, turkeys and other fowl, but in wild birds subclinical infections are common as well. In mammals, such influenza is very rare. However, in 1918-1920 the worldwide human “Spanish flu” pandemic, with an estimated 20-40 millions of deaths, was caused by a highly pathogenic IAV (H1N1).

 

Also, in cats the highly pathogenic avian H5N1 IAV may induce severe generalized disease after an incubation period of 1-2 days (Kuiken et al., 2004). Virus shedding via the respiratory tract and with faeces starts by day 3 post infection and persists 4 days or longer (Rimmelzwaan et al., 2006). After oral, and possibly also respiratory infection, replication starts most probably in the gastrointestinal and/or upper respiratory tracts, and then in the lungs, resulting in foci of alveolar damage (van Riel et al., 2006). The virus eventually reaches the liver, heart, brain, renal glomeruli, adrenal cortex and sometimes the spleen, pancreas, and large intestine (Rimmelzwaan et al., 2006; Songserm et al., 2006; Yingst et al., 2006). In some cats non-suppurative encephalitis and ganglio-neuritis of the intestinal plexus nervosus were observed (Keawcharoen et al., 2004; Rimmelzwaan et al., 2006). Multifocal haemorrhages and necroses in different organs and bronchointerstitial pneumonia are responsible for acute mortality (Reperant et al., 2012).

 

Epidemiology of IAV infections in cats

 

For a long time, it was believed that cats were resistant to influenza. Now it is clear, that cats, dogs, ferrets and other carnivores are involved in the worldwide circulation of IAVs (Wasik et al., 2019).

 

Low pathogenic strains

 

Early experiments revealed that cats are susceptible to some IAVs isolated from humans, birds and seals which induced usually only subclinical infections or mild fever (Paniker and Nair, 1970; Romváry et al., 1975; Hinshaw et al., 1981).

 

Additionally, canine influenza virus (CIV) may occasionally be transmitted to cats. The first outbreak of severe influenza in dogs occurred in 2002 in English foxhounds and was caused by equine H3N8 IAV (Daly et al., 2008). Serological studies revealed that this agent, adapted to dogs as CIV, was circulating among racing greyhounds in the USA from the early 2000s (Anderson et al., 2012). After an outbreak in Florida, this virus spread to other breeds and regions of the USA, especially to shelters (Crawford et al., 2005; Payungporn et al., 2008). Another cross-species transmission of the H3N8 virus to dogs was documented during an epidemic of equine influenza in Australia 2007 (Kirkland et al., 2010; Crawford et al., 2011). Natural equine H3N8 IAV has not been found in cats so far, but after experimental infection cats developed disease, shed virus, and transmitted the infection to other cats by contact (Su et al., 2014).

 

In South Korea and China around 2004-2005 a H3N2 CIV emerged in dogs, most probably of avian origin, and became enzootic there (Song et al., 2008; Zhu et al., 2015). Since 2015, this agent has been repeatedly introduced to the USA and Canada by dogs rescued from Asian meat production farms resulting in several outbreaks (Voorhees et al., 2017; Wasik et al., 2019). Cross-species transmission of this virus is possible as after experimental inoculations ferrets, guinea pigs and also cats have been infected (Kim et al., 2013). Furthermore, natural feline outbreaks with fever, tachypnea, sneezing, coughing, dyspnea and lethargy were noted in 2 shelters (Song et al., 2011; Jeoung et al., 2013). In one of them morbidity was 100% and mortality 40%. Though cats can be infected via direct dog-to-cat or cat-to-cat transfer, this virus obviously replicates less efficiently in cats than in dogs, as natural feline outbreaks seem to be very rare. They were largely confined to shelters, and the virus does not appear to undergo pro­longed transmission in household cats (Voorhees et al., 2017).

 

In 2016-2017, an avian H7N2 IAV infected cats in a New York shelter, and quickly spread to other shelters in New York and Pennsylvania, likely by the movement of cats between the shelters (Newbury et al., 2017; Blachere et al., 2018). The virus was easily transmitted between cats, but not among dogs, chickens, or rabbits housed in the same facilities (Lee et al., 2017). In total about 500 cats were found infected and most experienced mild respiratory ill­ness (Hatta et al., 2018). One el­derly cat with underlying conditions developed severe pneumonia and was eu­thanized. Also, a veterinarian and a shelter worker, both having multiple direct cat exposures without using personal protective equipment, became infected and showed mild, transient respiratory disease (Belser et al., 2017, Poirot et al., 2019).

 

Experimental inoculations confirmed that cats were susceptible to the human H3N2 virus that induced the “Hong-Kong” influenza pandemic in 1968 (Paniker and Nair, 1970). Furthermore, several studies indicated that in 2009 cats (and dogs) could be worldwide infected during the next human influenza pandemic, probably by direct transmission from their owners (Löhr et al., 2010; Sponseller et al., 2010; Ali et al., 2011; Campagnolo et al., 2011; Lin et al., 2012; Zhao FR et al., 2014; Zhao S et al., 2020). In Italy, this virus caused an outbreak of respiratory and gastrointestinal disease in a colony of 90 cats, resulting in 25 deaths (Fiorentini et al., 2011). Cat-to-cat transmission was suspected (van den Brand et al., 2010; Fiorentini et al., 2011).

 

There are also reports of occasional influenza cases in cats caused by other strains of IAVs (Cao et al., 2017; Wasik et al., 2019; Borland et al., 2020). A recent study confirmed that presence of antibodies to IAVs of both avian and human origin is not uncommon in European shelter cats (Zhao S et al., 2020). Antibodies against H1, H3, H5, H7 and H9 were found in their sera.

 

Highly pathogenic strain H5N1

 

In Asia, a highly pathogenic strain H5N1 emerged in 1996 which caused a huge epidemic of “avian flu” with high mortality in poultry at the beginning of the 21st century. Hundreds of millions of poultry were destroyed (World Organization for Animal Health, 2020). Sporadically mammals were affected, including over 860 humans with a fatality rate of more than 50% (World Health Organization, 2020). Severe cases in domestic cats were also noted (Kuiken et al., 2004; Thiry et al., 2007) as well as in wild felids (Keawcharoen et al., 2004) that were fed, or had other contact with, infected chickens. In one outbreak in wild felids, tiger-to-tiger transmission was suspected (Thanawongnuwech et al., 2005). As this epidemic reached Europe and Africa, incidental feline cases also were seen there (Thiry et al., 2007) as well as subclinical infections (Leschnik et al., 2007). Usually these were connected to infected wild birds or poultry. Nevertheless, even in areas in which birds are infected with H5N1 virus, cats are rarely positive by serology or PCR (Marschall et al., 2008; Zhao FR et al., 2015). Experimental infections have confirmed that the H5N1 strain may induce a severe, fatal disease in domestic cats, and can spread via cat-to-cat contact (Kuiken et al., 2004; Rimmelzwaan et al., 2006; Vahlenkamp et al., 2008). The virus was excreted not only via the respiratory tract but also via faeces.

 

In summary, the data presented above clearly show that domestic cats are susceptible to natural IAV infections from other species. They result most likely from close contact with infected humans or animals, especially birds. Serologic surveys suggest low to moderate rates of seroconversion to low pathogenic seasonal human or animal strains, and sporadic seroconversions to highly pathogenic avian strains. However, IAVs seem to spread inefficiently among feline populations probably due to social organization that limits the direct cat-to-cat contact required for viral transmission. So far, feline influenza epidemics have not been seen, but only rare outbreaks in dense populations like shelters. Therefore, cats are not considered a reservoir of influenza. In contrast to humans, horses, pigs, bats, dogs and some other mammalian species, adaptation of IAVs to feline hosts has not yet occurred.

 

Clinical signs

 

Low pathogenic IAVs usually only induce a subclinical infection or mild, self-limiting upper respiratory tract disease with sneezing as well nasal and/or ocular discharge in cats. Very rarely, in shelters or other crowded colonies, secondary bacterial infections may lead to pneumonia manifested by a rise in body temperature, tachypnea, dyspnea, coughing, lethargy, and fatalities (Fiorentini et al., 2011; Song et al., 2011; Jeoung et al., 2013; Hatta et al., 2018).

 

Though subclinical infection is also possible, highly pathogenic H5N1 avian strain induces in cats usually severe clinical signs including high fever from day 1 post infection, and by day 2 lethargy, protrusion of the nictitating membranes, conjunctivitis, dyspnea and high fatality rate. If diffuse haemorrhagic lesions occur, some cats show serosanguinuous nasal discharge and icterus. Convulsions, ataxia or other neurological signs, as well as gastrointestinal symptoms, can also be seen (Kuiken et al., 2004; Thanawongnuwech et al., 2005; Rimmelzwaan et al., 2006; Songserm et al., 2006; Vahlenkamp et al., 2008).

 

Pathological lesions

 

In cats that died due to low pathogenic IAV infection (H1N1/2009 human pandemic strain), histological examination revealed bronchointerstitial pneumonia, epithelial bronchiolar hyperplasia and alveolar necrosis (Fiorentini et al., 2011; Knight et al., 2016).

 

The necropsy of cats infected by the H5N1 highly pathogenic virus showed multifocal pulmonary lesions and petechial haemorrhages in the lungs, heart, thymus, stomach, intestine, tonsils, mandibular and retropharyngeal lymph nodes and liver, as well as a haemorrhagic pancreatitis (Keawcharoen et al., 2004; Yingst et al., 2006). Microscopically, these were inflammatory and necrotic lesions.

 

Diagnosis

 

In cats showing signs of acute upper respiratory tract inflammation, influenza should be considered if feline herpesvirus and calicivirus have been excluded as etiological agents. Risk factors include being in a shelter and close contact with humans or animals suffering from influenza. This applies especially when severe acute respiratory disease is seen in a cat having outdoor access during an outbreak of highly pathogenic avian influenza infection in poultry and/or aquatic wild birds in the region (Thiry et al., 2007).

 

IAVs can be isolated in tissue culture or embryonated eggs from nasal or oropharyngeal swabs, or at post-mortem examination from pulmonary tissue (and, in the case of highly pathogenic strains, also from rectal swabs or fecal samples, affected organs, intestinal content and pleural fluid).

 

Viral RNA can be detected in nasal swabs by reverse-transcriptase PCR during the first 4 days of infection; other tissue specimens can also be used.

 

In subclinical cases, serology (haemagglutination inhibition test or microneutralization assay) may be useful for the detection of antibodies. A four-fold serum titre increase within 14 days indicates recent influenza virus infection. A comparison of serological assays during a screening of IAV antibodies in cats has been published recently (Zhao S et al., 2020).

 

For dogs and some other animal species, commercial point-of-care tests are offered for the quick detection of IAV in nasal swabs. They have not been validated for cats so far.

 

Control

 

In the case of an influenza outbreak in a cattery, routine isolation and quarantine procedures should be followed to prevent spread, as cat-to-cat transmission may occur. The upper respiratory tract disease is usually mild and self-limiting. In rare, complicated cases symptomatic medication, combined with control of secondary bacterial infections, should be implemented as well as other procedures used in cats suffering from other acute viral upper respiratory diseases. In humans, oseltamivir is commonly used for the treatment or prevention of IAV infections. This antiviral drug has been applied in healthy tigers at risk of highly pathogenic H5N1 virus infection, but evidence of protection was not obtained (Thanawongnuwech et al., 2005).

 

Though it was shown that a heterologous (H5N6) avian influenza virus vaccine can protect cats against lethal challenge with the H5N1 strain (Vahlenkamp et al., 2008), no commercial vaccines for cats are available at present. The only prophylaxis in cats is prevention of any contact with poultry or wild birds infected by H5N1 or other highly pathogenic IAVs. The European Commission has therefore recommended to keep cats indoors in areas where outbreaks of H5N1 virus infections are recorded in poultry or wild birds (Anonymous, 2006; Council of the European Union, 2006).

 

Recently, it has been shown that a commercial inactivated H3N2 canine influenza virus vaccine was well tolerated and induced seroconversion in cats (Velineni et al., 2020). Even if this vaccine was to be licensed for cats, its usage in Europe is not recommended as canine H3N2 virus has not been found in Europe so far and, even in regions with canine outbreaks, infections in cats are very rare.

 

Zoonotic risk

 

Cats are not considered a reservoir of IAVs. Up to now, cats infected by both low as well highly pathogenic IAVs appear to be dead-end hosts (Harder and Vahlenkamp, 2010). Only two cases of cat-to-human transmission of a low pathogenic avian H7N2 IAV has been documented so far (Belser et al., 2017, Poirot et al., 2019, Borland et al., 2020). They occurred in a shelter after prolonged and unprotected exposure of a veterinarian and a worker to ill cats and their respiratory secretions, which indicates that the risk for cat to-human transmission is low (Lee et al., 2017). Rather, infected humans may be the source of feline infections with seasonal IAVs.

 

Though cats are sensitive to the highly pathogenic H5N1 avian IAV that caused over 860 human cases worldwide, not one human case was derived from cats. Nevertheless, if highly pathogenic IAV strains are found or suspected in a cat, the risk of transmission to humans should be reduced by wearing gloves, a mask and goggles, minimizing all unnecessary contact, and carrying out disinfection (Thiry et al., 2007).

 

Acknowledgement

 

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

 

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