Feline infectious upper
WALTHAM
FOCUS®
VOL 9 NO 3
1999
respiratory tract disease
Alan D. Radford BSc, BVSc, PhD, MRCVS
Lynne M. Sommerville BVMS, MRCVS
University of Liverpool, UK
INTRODUCTION
Feline infectious upper respiratory tract disease is caused by a
number of pathogens. It results in severe acute clinical signs in
individuals and groups of cats (Figure 1) and chronic disease in
individuals (Figure 2). This article considers the etiological agents
known to be primary pathogens in feline upper respiratory tract
disease (URTD), their clinical signs, diagnosis, and treatment.
ETIOLOGY
The major causes of feline infectious URTD are feline calicivirus
and feline herpesvirus. More recently, a primary role has also been
demonstrated for Bordetella bronchiseptica. Chlamydia psittaci is
Alan Radford graduated from Liverpool University in 1993. After
one year at University College Dublin as the Small Animal primarily a conjunctival pathogen but may also induce mild URTD.
Medicine House Surgeon, he returned to Liverpool to do a PhD There are several reports implicating Mycoplasma felis in URTD
entitled ‘Studies on feline calicivirus with particular reference to and Haemophilus felis has also been isolated from cats with rhinitis and
persistence’. He is currently a Research Associate at Liverpool, conjunctivitis (1, 2). Reovirus infection in cats has been experimentally
and his main interests are small animal virology, particularly associated with mild conjunctivitis, but may also cause mild respiratory
feline calicivirus. signs. Pasteurella spp., Staphylococcus spp., streptococcal species, and
Lynne Sommerville graduated from Glasgow University in 1996.
coliforms are also isolated from the respiratory tract of cats but their
After working in small animal practice in Warwickshire, she is
now studying for a PhD at Liverpool University entitled ‘Studies role in disease is uncertain and most likely secondary.
on feline calicivirus with particular reference to potential
improvements in vaccination strategies’.
KEY POINTS
● The major causes of feline upper respiratory
infection are feline calicivirus and feline
herpesvirus.
● Recently a primary role has been demonstrated for
Bordetella bronchiseptica, which may be of
particular concern in rescue catteries.
Figure 1 A pair of kittens showing typical signs of upper respiratory
● Treatment of active disease is largely dependent on tract disease. The clinical presentation of such cats may suggest which
nursing, supportive care, and control of secondary pathogen is involved, but is not usually diagnostic.
bacterial infection. Active steps to control cat-to-cat
transmission may be important in catteries.
Figure 2
● Vaccination and cattery management strategies are Chronic nasal
important in the control of feline upper respiratory discharge in an
disease. FHV-positive cat.
18
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1999
Figure 3 Ulceration of the dorsal margin of the tongue in a case of FCV. Figure 4 Electron micrograph of a herpesvirus showing the viral
Such ulceration is suggestive of FCV, but may also be seen in FHV. envelope.
Feline calicivirus (FCV) Feline herpesvirus-1 (FHV)
FCV was first isolated from the spleens of cats in the 1950s. FCV is FHV was first isolated in 1957 and initially named feline
one of the major causes of feline URTD. The majority of FCV isolates rhinotracheitis virus. Clinical signs of FHV tend to be more uniform
examined are different from each other and may be distinguished both and severe than FCV, particularly in young cats. Initially, following
serologically (3–5) and genetically (6, 7). Despite this, sufficient an incubation period of approximately 2–6 days, cats become
similarities exist between isolates such that FCVs are currently depressed, inappetant, pyrexic, and often develop marked sneezing.
considered to belong to a single serotype (8) and a single genotype (7). Ptyalism may occur but is not consistent. Conjunctivitis with serous
Typically, FCV is associated with a relatively mild syndrome (becoming mucopurulent) ocular and nasal discharges may follow.
characterized by ocular and nasal discharge, oral ulceration Severely affected cats cough and develop dyspnea (9). FHV may be
(particularly on the dorsal margin of the tongue; Figure 3) and an important cause of morbidity, particularly in young animals in
pyrexia. Cats may also become anorexic, and develop sneezing and breeding colonies, and severely affected kittens may die.
conjunctivitis (9). Less frequently, FHV may induce pneumonia or keratitis (with
Despite this typical pattern of disease, FCV can induce a wide associated complications including descemetocele formation).
spectrum of clinical signs from inapparent infections to fatal Rarely, skin ulceration and neurological signs have also been seen in
pneumonia in kittens (10, 11). However, early experiments using FHV-infected cats (23). As in FCV, FHV may also induce tongue
aerosolized virus to challenge naive kittens may have artefactually ulcers but not as frequently. Abortion, most probably secondary to
induced more severe forms of disease, and fatalities in the field are general debilitation and pyrexia, has been reported in pregnant
probably rare (11, 12). Indeed, it has been demonstrated that fomite queens (24). Damage to turbinates by FHV in acute disease may
transmission and not aerosol transmission of virus is most likely predispose animals to chronic rhinosinusitis in later life,
responsible for the infection of naive cats (13). characterized by a chronic, often purulent, nasal discharge and
Some isolates of FCV induce a well-characterized acute febrile sneezing.
lameness syndrome which has also been reported following the use FHV (Figure 4) belongs to the alphaherpesvirus group of the
of some live, attenuated vaccines (see below) (4, 14). There is also a Herpesviridae. It is therefore related to varicella zoster virus and
strong association between FCV isolation and chronic stomatitis in Herpes simplex virus type 1 (HSV-1), the cause of chicken pox and
the field (15–17). However, attempts to reproduce this condition cold sores in humans respectively. FHV contains a large, double-
experimentally have failed (18, 19), and it is likely that other factors, stranded DNA genome that codes for many proteins, some of which
particularly concurrent infection with feline immunodeficiency virus, are essential to the virus, while others are nonessential. The latter
are involved (16, 20). encode proteins that may be associated with virulence and, as such,
FCV has also been isolated from cats with many other patterns have been targeted for deletion to generate attenuated viruses
of disease including sudden death in kittens, ulceration of the skin, suitable for use in novel vaccines (e.g., thymidine kinase). The large
jaundice, and abortion. However, as FCV is able to induce a non- size of the genome also makes it possible to engineer FHVs
apparent persistent infection (see below), it is possible that some of containing genes from other viruses, such as the FCV capsid gene, in
these disease associations represent concurrent infection with FCV. an attempt to generate novel dual vaccines. However, to date,
FCV is a small nonenveloped RNA virus, belonging to the family protection from such experimental vaccines has only proved
Caliciviridae, which includes other important pathogens of man (e.g., marginal (22).
Norwalk virus) and animals (e.g., rabbit hemorrhagic disease virus).
The name comes from the distinct appearance of most caliciviruses Bordetella bronchiseptica
by electron microscopy when the surface of the virus capsid appears Bordetellae are gram-negative, strictly aerobic coccobacilli
to be covered in cup-like depressions (calyx meaning cup or chalice). (Figure 5). Until recently, the role of B. bronchiseptica in feline
The virus capsid contains a single major capsid protein, and it is respiratory disease was uncertain and it was largely considered to be
believed that this protein contains the major determinants a secondary pathogen. However, following both its isolation from
responsible for virus neutralisation by antibodies. As such, it has several natural cases of URTD (25, 26) and the demonstration of
been targeted experimentally in attempts to generate novel subunit disease following experimental challenge of specific pathogen-free
vaccines, either alone (21) or in combination with feline herpesvirus cats (27, 28), a primary role for B. bronchiseptica in some cases of
(22). Such subunit vaccines would contain only a small, non- feline URTD is now accepted. Clinical signs are relatively mild and
infectious, immunogenic fragment of FCV as opposed to whole, live include pyrexia, sneezing, nasal discharge, lymphadenopathy, and
virus, in theory making them safer than live, attenuated FCV occasional coughing (27, 28). A recent field survey has suggested B.
vaccines (see below). bronchiseptica may be particularly important in URTD in rescue 19
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WALTHAM
FOCUS® Table 1
VOL 9 NO 3
1999 A guide to the typical clinical signs associated with
infection with FHV, FCV, B. bronchiseptica and
C. psittaci
Clinical signs FHV FCV B. bronchiseptica C. psittaci
Depression +++ + + +
Sneezing +++ + + +
Ptyalism ++ – – –
Conjunctivitis ++ + – +++
Figure 5 Scanning electron micrograph of B. bronchiseptica (arrow) Ocular discharge +++ + – +++
adherent to cilia of the respiratory epithelium. Nasal discharge +++ + + +
Oral ulceration + +++ – –
catteries, with isolation rates of up to 19.5% (29).
Keratitis + – – –
Chlamydia psittaci Pneumonia (+) + – +/–
Chlamydia are highly specialized, obligate intracellular bacteria. Limping – + – –
C. psittaci was first isolated in 1942, when it was considered the +++ = marked. + = mild. (+) = rare but has been reported. +/– =
subclinical.
major cause of respiratory disease of cats and called feline
pneumonitis. Disease is primarily associated with conjunctivitis and
a serous ocular discharge (30). Occasionally, mild sneezing with a
nasal discharge may occur; systemic signs of depression and A recent in vitro study found the majority of feline
lameness have also been reported (31). However, as C. psittaci is B. bronchiseptica isolates were sensitive to oxytetracycline,
primarily a conjunctival pathogen, it will not be considered in any doxycycline, and enrofloxacin, and resistant to trimethoprim and
detail in this paper. Interestingly, while it is primarily a host-specific ampicillin (34).
pathogen, there are occasional, rare case reports of apparent human The recommended treatment of feline chlamydiosis is both
infection (32), raising the possibility that, under some topical oxytetracycline and systemic oxytetracycline or doxycycline.
circumstances, C. psittaci may be zoonotic. In young kittens it is advisable to warn owners of the possibility of
tetracycline-associated tooth discoloration.
In cases of FHV-associated chronic rhinosinusitis, treatment is
DIAGNOSIS aimed at controlling infection during clinical episodes of disease. It
It is important to achieve a definitive diagnosis in cases of URTD, is recommended that antibiotic therapy should reflect the results of
as acutely infected diseased animals and clinically normal, carrier culture and sensitivity. However, in the absence of such information,
animals may be infectious to contact susceptibles. Relevant history broad-spectrum antibiosis should be instigated. In all cases,
includes that of vaccination for protection and the potential for treatment should continue for three to six weeks. The use of
vaccine reactions (see below). Clinical signs are rarely diagnostic mucolytics, such as bromhexine, may ease the clinical signs.
(Figure 1) but may suggest one agent over another (Table 1). However, in many cases, clinical resolution remains incomplete
Definitive diagnosis is usually by isolation. Plain swabs, usually and/or temporary. In severe cases, surgical management of chronic
taken from the oropharynx, should be placed in virus transport rhinitis may be considered to remove diseased turbinates, promote
medium for FCV and FHV isolation and charcoal Amies’ transport sinus drainage, and allow topical antibiosis. However, such
medium for B. bronchiseptica isolation. The significance of positive treatment regimes are poorly tolerated in the cat, not often curative,
virus isolations to current disease needs to be interpreted in the light and should not be undertaken lightly.
of frequent FCV and FHV carriers (see below). Where no virus is
isolated, particularly for FHV, the intermittent nature of virus EPIDEMIOLOGY
shedding in carrier cats must be taken into account before animals
are considered ‘virus-free’. Feline calicivirus and feline herpesvirus
Diagnosis of feline chlamydiosis is usually by serology or Both FCV and FHV are considered highly successful pathogens.
detection of the organism in conjunctival swabs. Recently, a Indeed, most domestic cats have antibodies to both viruses and the
technique based on the polymerase chain reaction has been prevalence of infected individuals in the cat population in countries
developed to detect chlamydia DNA, and has been shown to be more such as the UK has remained surprisingly high (especially for FCV)
sensitive than isolation (33). Such techniques may become more despite the widespread use of vaccines. This success has been
widely available in the future. attributed to the ability of these viruses to pass from acutely infected
cats to those which are susceptible, to survive (albeit for a relatively
short duration) outside their host, and, perhaps most importantly, to
TREATMENT persist in clinically normal animals that have recovered from acute
Treatment of viral URTD in cats is largely dependent on good disease.
nursing and control of secondary bacterial infections for which the Transmission from acutely infected cats relies upon the
use of a broad-spectrum antibiotic is recommended. In severely presence of sufficient numbers of susceptible individuals. It probably
affected animals, fluid therapy and nutritional support may be occurs by direct contact although indirect spread may also occur via
necessary. There are no specific antiviral treatments available for contaminated feeding bowls, cages, utensils, and personnel. Both
FCV or FHV apart from those that have been used to treat FHV- viruses are shed into the oropharynx and are present in ocular and
associated corneal ulcers (e.g., idoxuridine, trifluoridine), and none nasal discharges. FCV is also shed in urine and feces although the
20 is currently licensed in the UK for use in cats. significance of this is unclear. Aerosol transmission is not
considered to be important, as cats are thought to have an CONTROL WALTHAM
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insufficient tidal volume for efficient aerosol production to occur VOL 9 NO 3
(13). However, the viruses may occasionally be spread in There are two main strategies used in the control of feline 1999
macrodroplets when infected cats sneeze. infectious URTD – namely, vaccination and careful husbandry.
Probably less successful as a means of transmission is the FHV and FCV vaccination
persistence of virus in the environment. FHV is relatively labile, and
remains infectious only for about 18 hours in damp conditions and Three types of vaccine against FHV and FCV are currently
12 hours in dry conditions. In contrast, FCV can persist for up to one available: live, attenuated systemic vaccines; live, attenuated
week outside the host. It is also more resistant to disinfectants than intranasal vaccines, and inactivated, adjuvant systemic vaccines.
FHV, as it does not possess a detergent-susceptible envelope. Live, attenuated systemic vaccines are most widely used.
Crucial to the epidemiology of viral URTD, and common to both Their main disadvantage (as with most live vaccines) is that they
FHV and FCV, is the ability of these viruses to persist in clinically may induce disease if vaccine virus inadvertently gains access to the
normal, recovered individuals (or carriers). However, the natural route of infection. This may occur if the vaccine is
mechanisms of each carrier state are quite different. aerosolized during administration or if some leaks back onto the skin
In most, and possibly all cats infected with FHV, the virus surface and is licked by a cat. There is also evidence to suggest that
develops a specialized carrier phase known as latency, during which even in correctly vaccinated cats, vaccine virus may generalize and
the virus switches off its replication and ‘hides’ within the host, be shed from the oropharynx (39, 40). However, the significance of
mainly in neuronal cells of the trigeminal ganglion. At this stage, no this in the field is uncertain.
virus is shed from the latently infected cat and most carrier cats will The advantage of live, intranasal vaccines is that the immunity
appear clinically normal. Intermittently, often following periods of they induce is rapid (partial protection as early as two days post-
stress such as kittening and transport or the use of glucocorticoids, vaccination) and at the site through which natural infection is
virus replication is switched back on (reactivation). In such cats, acquired. Such immunity is also less subject to interference by
virus shedding is again detectable after a lag period of about seven MDAs. Where owners are concerned about injection site reactions
days following the stress, and continues for approximately two (for example sarcomas), intranasal vaccines also offer a sensible
weeks. During reactivation, mild respiratory signs may be observed alternative to parenterally administered vaccines. However, mild
(recrudescence). Cats persistently infected with FHV remain so for URTD at the time of vaccination may occur. Their use is particularly
life. indicated where the rapid induction of immunity is deemed
Unlike FHV, feline calicivirus is shed more or less continuously important – for example, in the presence of epidemic or endemic
into the oropharynx of carriers, so that these animals represent a colony disease (see below). Live, intranasal vaccines are not
constant hazard to susceptible individuals. Duration of the carrier currently available in some countries.
state is variable but usually not lifelong. An infective animal half-life Inactivated vaccines are most useful in catteries considered
has been described such that during a 75-day period, approximately free of respiratory pathogens. Some are also licensed for use in
half a given number of carriers appear to clear the virus. pregnant animals (this is not usually the case with live vaccines).
The mechanism of the FCV carrier state is still uncertain. A long-standing concern in FCV vaccinology is the difficulty of
However, there is some evidence that, as for other RNA viruses, FCV producing a vaccine that protects against all the different isolates of
is able to evolve rapidly within its host (35–37). Such evolution FCV. Most FCV vaccines contain a single isolate chosen because
promotes the generation of viral variants that escape neutralization immunity to this virus neutralizes a high proportion of field isolates.
by the host’s immune response and these variants are thought to However, the widespread use of such vaccines may select for existing
continue the persistent infection. FCVs not neutralized by the vaccine. There is some recent evidence
While preexisting immunity may prevent clinical disease on virus to suggest this may be beginning to occur (5, 6), and it will therefore
challenge, with either FHV or FCV, it may not prevent infection of the be important to assess the efficacy of such vaccines continuously
individual. Indeed, such animals may develop persistent infections, against field strains of FCV.
and be sources of infection to naive cats, without ever having shown Most vaccination schedules are based on first vaccinating
clinical disease. This is true whether immunity is acquired naturally kittens at nine weeks, when MDA has declined sufficiently in the
through maternally-derived antibodies (MDA) or artificially following majority of animals to levels that do not interfere with vaccination. A
vaccination. second vaccine is given three weeks later, followed by annual
boosters.
Bordetella bronchiseptica In some cases, if MDA levels are low, kittens may develop URTD
The epidemiology of B. bronchiseptica is less defined than that before vaccination is complete. In such cases, vaccination of queens
of the viruses. As in FHV and FCV, B. bronchiseptica is frequently with a live vaccine before mating or a licensed, inactivated vaccine
isolated from clinically normal animals. The bacteria are shed into during pregnancy, may extend the duration of MDA in her kittens
the nasal cavity and oropharynx for up to 19 weeks postinfection. In and bridge this apparent immunity gap. Another approach is to try
addition, as in FHV, parturition may promote shedding. In general early vaccination of kittens with a live, intranasal vaccine, as these
however, young kittens appear to be protected from disease by MDA are not affected by MDA (see above).
and do not succumb to infection even if the queen is shedding B. bronchiseptica
bacteria (28).
Results of a recent field survey have suggested that, as with dogs Vaccines against feline bordetellosis are still relatively new. A
in kennels, B. bronchiseptica is most likely to be associated with fimbrial antigen-based vaccine has recently been developed but is
disease in larger cat colonies, especially rescue colonies (29). There only marketed in some European countries. An intranasal vaccine
is also some intriguing evidence to suggest that B. bronchiseptica has been developed for use in the USA (Intervet, personal
may pass between dogs and cats, although the relevance of this is communication). Such vaccines will be particularly indicated for use
uncertain (38). in colonies where disease has been shown to have a
B. bronchiseptica component.
21
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WALTHAM and FCV could also be tried. Such vaccines are less susceptible than
FOCUS® HUSBANDRY AND MANAGEMENT
VOL 9 NO 3 parenteral vaccines to interference by MDA, and may reduce the risk
1999 Control measures adopted to prevent respiratory disease of disease in young kittens (see above). Vaccination may be started
introduction or spread within cat housing depend upon the situation in kittens just prior to the age at which disease is seen in the colony.
and purpose for which the animals are kept. Brief outlines of control However, these vaccines are not available in all countries and, where
strategies recommended in boarding catteries, breeding catteries, they are available, they are not generally licensed for use in kittens
stray cat homes, and households are described below. More details younger than 12 weeks old. Kittens vaccinated at under 12 weeks
can be found elsewhere (9). should receive subsequent vaccinations at three-weekly intervals,
In households where a small numbers of cats are kept as pets, with a final vaccine at 12 weeks of age.
respiratory disease can usually be controlled by regular vaccination Further protection of the kittens may be merited by early
of all cats. When an owner intends to leave the home for a short weaning at four to five weeks of age if it is suspected that the queen
period of time – for example, to go on vacation – cats may be best is an FHV carrier. Ultimately, queens implicated in postnatal
kept at home by a friend or neighbor, rather than being boarded in infection of kittens may be removed from the colony or neutered.
catteries. This reduces both the risk of exposure to respiratory Respiratory tract disease in cats is as important now as it was
pathogens and of FHV stress-induced reactivation or recrudescence. before the onset of widespread vaccination. An understanding of the
If boarding outside the home is essential, it is wise to suggest that complex epidemiology of the primary pathogens responsible is
cats are vaccinated within six months of boarding. essential if veterinarians are to control these diseases. Recent
Measures for the control of respiratory diseases should be advances in biotechnology have confirmed that current vaccination
incorporated into the design and management of boarding schedules are unlikely to eliminate these pathogens. They have
accommodation for cats. Unless cats are from the same household, opened up exciting new vaccine technologies that should keep us
they should be housed singly in pens with solid partitions, and, if employed for many interesting years to come.
possible, not share the same airspace. The cats should be fed in a set
order every day, completely attending to one cat before moving on to
the next. Food bowls and litter trays should be easily accessible so VACCINE FAILURES
that it is not necessary to enter the pen in order to clean or refill Vaccine failures are defined as clinical disease in vaccinated
them. Bowls, utensils, and litter trays should be cleaned with a animals. Depending on when disease is observed relative to
suitable disinfectant (e.g., 0.175% solution of sodium hypochlorite – vaccination, such failures have been divided into vaccine reactions
domestic bleach (42) or an appropriate veterinary disinfectant used (disease within 21 days postvaccination) and vaccine breakdowns
according to the manufacturer’s instructions). One set of equipment (disease after 21 days postvaccination) (4).
may be soaked in the disinfectant while a second set is in use. Vaccine reactions most frequently occur following the nine-
Rubber boots should be worn by personnel working in the cattery, week kitten vaccine and most likely represent field virus causing
and a foot bath containing disinfectant should be placed at the door. disease before vaccine-induced immunity is complete. Occasionally,
A further recommended measure is to assign a pair of rubber gloves however, vaccine virus is implicated in vaccine reactions (4, 41).
to each pen; these should only be used when cleaning that pen and While this is worrying, it is not surprising that live vaccines may
disinfected or disposed of between consecutive residents of the same themselves occasionally cause disease, especially if inadvertently
pen. Pens should be thoroughly disinfected after each use (42), and given by the incorrect route (see above).
preferably remain empty for two days before a new resident is Vaccine breakdowns represent disease in animals that should
introduced. Good ventilation will help to ensure the accommodation be protected; they are less common than reactions. Many factors
is not damp and therefore reduce the survival time of pathogens in have been implicated in their origin, including immunosuppression,
the environment. levels of MDA interfering with primary vaccination, and the dose of
Any cats showing clinical signs of respiratory disease should be infection received by the cat. In the latter case, a large virus
immediately isolated and attended to by a veterinary surgeon. Such challenge may overwhelm the acquired immune response, resulting
cats should be fed and attended to last by cattery personnel. in clinical disease. Since both FCV and FHV may be shed from
Stray cat homes should follow the same guidelines as for clinically normal animals during persistent infection (see above),
boarding catteries. Since vaccination status cannot be guaranteed, a virus isolated from vaccine breakdowns may not be the cause of
quarantine period is necessary. Where cat population turnovers are URTD and other pathogens such as C. psittaci or B. bronchiseptica
high, the use of live, intranasal vaccination on admission may also be should be considered.
necessary. The rapid onset of immunity induced by such vaccines Feline calicivirus vaccine failures can be monitored by typing the
means that this quarantine period may be as short as one or two isolates involved, using serological typing (4), and, more recently,
days. sequence-based typing (41). These methods can distinguish vaccine
In breeding colonies, cats are at risk from respiratory disease virus from field viruses and determine whether a vaccine failure is
pathogens through contact with stud animals, the introduction of likely to be caused by vaccine virus or a field virus. Such techniques
new breeding stock, and, to a lesser extent, from cats attending are relatively expensive and are probably only available at specialist
shows. If possible, stud cats should only be used from respiratory diagnostic laboratories or academic institutions. FHVs are so similar
disease-free colonies, and a three-week quarantine period is that their differentiation for typing purposes is currently not
recommended prior to the introduction of any new breeding stock generally possible.
into the main colony. During this time, cats should be screened at
least twice by oropharyngeal swabs.
Another control measure that may be implemented (usually in
the presence of significant disease) is the isolation of pregnant
queens three weeks before term. This allows FHV, reactivated from
latency as a result of the change of housing, time to cease before the
kittens are born. However, the stress of lactation is also likely to
22 cause reactivation. Early vaccination of kittens with intranasal FHV
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