FELINE CORONAVIRUS AND FELINE INFECTIOUS PERITONITIS IN NONDOMESTIC FELID SPECIES

1.4.2021, Translation 8.5.2021
Stout, Alison E., André, Nicole M., and Whittaker, Gary R.
Original article: FELINE CORONAVIRUS AND FELINE INFECTIOUS PERITONITIS IN NONDOMESTIC FELID SPECIES

Abstract

Feline coronavirus (FCoV) is reported worldwide and is known to cause disease in both domestic and non-domesticated feline species. Although FCoV often leads to mild or subclinical disease, a small subset of cats succumb to the deadly systemic disease, feline infectious peritonitis (FIP). The outbreak of FIP in cheetahs (Acinonyx jubatus) in the zoo's collection highlighted the devastating effect of introducing FCoV into a group of animals. In addition to cheetahs, FIP has also been recorded in European wild cats (Felis silvestris), tigers (Panthera tigris), mountain lions (Puma concolor) and lions (Panthera leo). This article provides an overview of reported cases of FIP in non-domesticated cat species and highlights FCoV in non-domesticated cat populations.

Introduction

Infectious diseases pose a significant threat to wildlife conservation.74 Soil fragmentation has the potential to allow higher populations to grow in natural habitats than usual, and urban sprawl may increase the interaction of wild cats with domestic cats.15 Recently, the COVID-19 pandemic also highlighted undelivered felines when the coronavirus SARS-CoV-2 was first detected in a tiger (Panthera tigris) at the Bronx Zoo in New York, NY, with subsequent cases diagnosed in other cats kept in captivity in the same zoo; 122 although the condition of these animals has improved since diagnosis, coronaviruses remain a concern for the health of cats in both domestic and non-domestic environments.

Feline coronavirus infections are currently widespread in the domestic cat population. 17 In most domestic cats, the disease is either asymptomatic or manifests as self-limiting mild diarrhea. 83 However, a small subset of cats experience an "internal mutation" that leads to macrophage tropism46, wherein these cats succumb to a systemic disease known as FIP. 9,60,99 FCoV classified as alpha-coronavirus (species alpha-coronavirus-1) can be divided into two biotypes: benign feline enteric coronavirus or feline infectious peritonitis virus (FIPV).82 Furthermore, the virus can be classified according to serotype as feline coronavirus type I or type II.52 These viral types originally differed based on a different antibody response, but it has recently been proposed that they be considered different genetic strains based on their spike glycoproteins.68 Type II viruses are much less common in natural infections, yet they are more easily isolated and propagated in cell culture systems, and have been characterized in more detail. The type II virus is considered to be derived from double homologous recombination between the native FCoV type and canine coronavirus.46

The viral spike protein is the driving mechanism of cellular tropism and pathogenesis. The FCoV type II receptor is known to be feline aminopeptidase (fAPN), 114 while type I viruses have a different and as yet unknown receptor. 21 Another feature distinguishing between the two virus types is the fusion activation process, the type I virus contains two proteolytic activation points (at sites S1 / S2 and S29), while the type II virus has a single cleavage point S29.52 Although both serotypes are known to cause FIP, many questions remain as to the natural behavior of each and the host's response to infection.

LocationYearSeroprevalenceReferences
South Africa1977–19781.1251
19823.528,45
19890/40and105
1999–2001105/10757
Serengeti / Tanzania19858.258,45
-24/3926
Kenya19854.128,25,45
Namibia1999–200119/3957
1992–199821/7272
2002-20043/88b113
Botswana2008–20112.611
Winston, Oregon (epidemic)Before June 19820/258,45
198335/358,45
198516/168,45
North America198631/908,45
198749/918,45
198942/10226
1990106/16426
199124/3926
England19851.128,25,45
Table 1. FCoV seroprevalence in cheetahs that move freely and in captivity.
a) Paired samples of a total of 40 animals (80 samples).
b) Repeated sampling has taken place

Antibody responses to both type I and type II FCoV have been reported in captive cats in the United States, with reports specifically reporting a response to FCoV type I in cheetahs, African lions (Panthera leo) and Bengal tigers (Panthera tigris tigris). ), and the response against FCoV type II in cheetahs, jaguars (Panthera onca), African lions, Bengal tigers, lynxes (Lynx canadensis), snow leopards (Panthera uncia) and African leopards (Panthera pardus pardus).56 In some cases, type II FCoV is considered to be more transmissible compared to type I virus in domestic cats, 123 although due to the presence of both types of viruses in the study facility, this could not be confirmed. The situation in feral cats is unknown.

Clinically, there are two classic forms of the disease in cats, namely effusion or non-fusion ("wet" or "dry"). The wet form of FIP is characterized by effusion in the abdominal or thoracic cavity, or both, or in the pericardial cavities, and the dry form by the presence of pyogranulomatous lesions. However, the clinical symptoms associated with the FIPV biotype can be quite variable and non-specific. FCoV and FIP remained a major global challenge. Vaccination is not recommended, in part due to concerns about negative outcomes due to exacerbation of antibody-dependent infection in the presence of non-neutralizing antibodies.125 Despite promising initial studies 73,84 and other treatment options still do not have approved antiviral therapies. Prevention is difficult and pre-mortem diagnosis is challenging. Current PCR and serological testing methodologies do not distinguish between pathological forms of the virus and antibody titers are unpredictable. In feline populations, FCoV secretion is often observed in non-FIP positive animals. Likewise, antibody titers only provide evidence of previous exposure and a negative antibody test in domestic cats does not rule out the possibility of FCoV secretion.29 Depending on the antibody assay, sensitivity and specificity may provide variable assistance in the diagnosis of FIP, as found by Felten and Hartmann.28 Immunohistochemistry (IHC) currently remains the gold standard for the diagnosis of FIP.28 Managing the virus can be problematic in the management of captive species, and limited reference ranges for blood analysis, high stress scenarios, and possible new presentations are uncertain.

FIP and FCoV in non-domesticated species

Cheetah (Acinonyx jubatus): In 1979 Horzinek and Osterhaus51 demonstrated a serological response to FCoV in cheetahs for the first time (Table 1). In 1982, it became clear that cheetahs could suffer from the same serious illness as FCoV-infected domestic cats when a FIP outbreak in captive-bred cheetahs at Winston Zoo, Oregon. 27,88 The first individual (8.5 year old female) was recently introduced into the herd and had non-specific symptoms of the disease including lethargy, anorexia, dehydration, fever and jaundice with hematocrit 30%, hyperproteinemia (9.1 g / dl), leukocytosis and azotemia.88 Ascites was present at post-mortem examination, along with fibrinous lesions adjacent to the abdominal organs and fluid in the thoracic cavity.88 Petechization has been reported in several organs.88 In the months that followed between this initial case and other cases of FIP, occasional diarrhea was observed in other cheetahs.27 Pathology of tissue samples from other animals that died of FIP revealed multifocal necrotic lesions affecting the abdominal organs (liver, kidney, pancreas, spleen), lymph nodes, and thyroid gland. Facial erosions and ulcerative glossitis have also been observed.27 Although it is not possible to rule out calicivirus, which also causes these ulcers, there are a number of recent cases with human patients with COVID-19 who have experienced tongue ulcers due to infection.94 Longitudinal serological monitoring following the first case of cheetah FIP showed seroconversion, and by 1983 each cheetah in the park was serologically positive.6,27,45 During this epidemic, almost 60% cheetahs succumbed to FIP.25,45 Early characterization of the cheetah isolate involved inoculation of several cell lines, including feline Crandall-Rees kidney cells (CRFK), Felis catus-4 fetal cells (FCWF-4), and two kidney-derived cheetah cell lines (AjuKid234) or fibroblasts (AjuFib238).24 CRFK cells showed similar properties after inoculation with cheetah isolates compared to the two FCoV type I strains, while FCWF-4 cells were less permissive to the isolate. Across cheetah cell lines, AjuKid234 cell transmissibility was low.24

Other cases of FIP have also been reported in a litter of three caught, approximately 6-month-old wild cheetahs, co-infected with Toxoplasma gondii.119 Clinical pathology data revealed hypochromic anemia, neutrophilia, lymphopenia and eosinopenia with normal total protein but elevated alpha-2 globulin and gamma globulins.119 In addition to fibrinous peritonitis and lesions affecting the abdominal organs, pulmonary edema and gastric blood have also been reported.119 In this report, the authors point to a lack of diet; however, other predisposing factors may include relocation stress and genetic predisposition.119 In a pathological study of 31 dead cheetahs kept in captivity in North America, the FIP was considered the cause of death in two animals.71 Although FIP was undeniably considered a fatal disease in domestic cats, many hypotheses have been considered that have made cheetahs particularly susceptible to FIP, including genetic control of the immune response, especially the homogeneity of the majority histocompatibility complex (MHC). 25,79 Analysis of the cheetah-infected virus showed deletion mutations in gene 7a, although interestingly, genes 7a and 7b were intact in cheetahs with FIP.58 Since the first recorded case of cheetah FIP, the disease remains sporadic despite evidence of exposure. No further devastating losses have been observed since the initial outbreaks of the FIP epidemic in cheetahs, although research continues.

Following the outbreak of FIP in Oregon, FCoV monitoring revealed a common antibody response to the virus (Table 1). Initial tests have shown that faecal excretion and antibody titers are often inconsistent.45 In a study of farmed and wild South African cheetahs, an overall seroprevalence of 57% (169/298) was observed compared to 36% (66/182) in those who secreted the viral antigen, as assessed by nested reverse transcription polymerase chain reaction (RT / nCR). .57 In 49 animals that shed viral antigen, 46 showed an antibody response against FCoV type I, 45 showed an antibody response against FCoV type II, and three showed no antibody response.57 Whether this high seroprevalence against both type I and II FCoV was caused by a number of circulating viruses, cross-reactivity, or other factors remains unknown, but this finding is unique. In South African cheetahs that were observed longitudinally (n¼48), almost a fifth (n¼10) excreted antigen at more than one time point, even after a negative test after a positive test.57 In serological research, Munson et al. in Namibia72 were more seropositive males, with 5/14 (36%) juvenile males showing seroprevalence compared to 0/8 juvenile females and 13/37 (35%) adult males compared to 3/13 (23%) adult females.

Lifestyle and risk factors for wild and captive species may vary depending on the disease. In a study among captive cheetahs in the United States, three of the 22 healthy cheetahs shed viral antigen (RT / nPCR) (Table 2).55 Of the three viral antigen shedding animals, one animal was positive for anti-FCoV type I antibodies and the other two were seronegative.55 In another 19 animals, the antibody response was determined in 15 animals, of which 10 showed no antibodies, four animals were seropositive against type I virus and one animal was seropositive against both type I and type II viruses.55 However, in another study on 10 cheetahs that did not shed the virus, the antibodies were common against type II virus (5/10) compared to type I (4/10) or both (1/10). Discrepancies in the response of specific antibodies may be due to changes in management strategies, seasonal fluctuations, or differences in sample handling. In addition, the differences between the antibody response and faecal excretion pose a challenge to the actual disease state of the animal, both in captive cheetahs and in wild cheetahs. To provide guidance on the testing strategy, faecal samples were collected from 25 cheetahs in captivity in the United States for 30 days.38 Of these faecal samples, viral antigen was found in 13% (4/31 samples) fecal samples from one animal to 93% (26/28 samples) samples from one animal.38

Common nameGenus speciesAntigen frequencyReferences
European wild catFelis silvestris5/1544
African wild catFelis lybica0/257
Black-footed catFelis nigripes0/157
American cougarPuma concolor0/2037
Jaguarundi catPuma yagouaroundi0/1637
  0/143
CheetahAcinonyx jubatus22/9045
  66/18257
  3/2255
Bengal catPrionailurus bengalensis3/3412
Spanish lynxLynx pardinus0/2567
  0/6865
LynxLynx lynx0/2102
OcelotLeopardus pardalis0/843
  0/2137
  0/1and62
MargayLeopardus wiedii0/1443
  0/737
Pampas catLeopardus colocolo0/2237
Small-spotted catLeopardus [Oncifelis] geoffroyi0/143
  0/637
Ocelot treeLeopardus tigrinus0/2437
  0/2043
Rys caracalCaracal caracal0/257
African lionPanthera leo0/157
American JaguarPanthera onca0/6137
Spotted leopardPanthera pardus0/257
Table 2. Detection of FCoV antigen in non-domesticated cats.
(a) part of the diagnostic test

The role of persistent cheetah infections in the development of ulcerative colitis and other long-term consequences remains relatively unclear and represents a potential area for study.96,112 In 1993 Munson71 described in two dead cheetahs with lesions characteristic of FIP also pathological changes in the villi of the small intestine in one animal (FIP did not consider the cause of death in even one cheetah). In a sample of nine cheetahs with necrotizing colitis and diarrhea that ruled out FCoV, six animals showed antibodies only to FCoV type I, two animals showed antibodies to both type I and type II, and one animal was not positive for antibodies of any serotype.56 Furthermore, FCoV was diagnosed in cheetah pups showing acute hind limb paresis, but no apparent relationship to serology was demonstrated, and antibody titers varied from animal to animal during testing.120,121 Feline leukoencephalomyelopathy (LFL) in large cats has been identified in many cheetahs and two other feline species in the United States. The disease is characterized by progressive vision loss, disorientation and difficulty eating.7 In the process of understanding the etiology of LFL, 14 animals were tested immunohistochemically for FCoV, but no animals in this small subgroup showed positive.7

European wild cat (Felis silvestris): In 1993, Watt and colleagues124 reported an outbreak of FIP in European feral cats in a closed colony that had existed for almost 14 years and affected only males. Numerous clinical signs have been reported, along with multisystem organ involvement, including liver, kidney, intestine, brain, lung, heart, and lymphatic tissue.124 Respiratory symptoms were noted in two cats.124 It has not been established how cats became infected and it is considered unlikely that a stray cat could introduce the virus. Whether the source of the contamination could have been the nurse or the nurses at the zoo was not further investigated. It was also not determined whether there was long-term shedding of the virus. Interestingly, a previous study by McOrist et al.64 was unable to identify European feral kittens as serologically positive for FCoV exposure by indirect immunofluorescence assay (IFA) performed on plasma and directed against the Wellcome virus strain (Table 3). Most recently, however, Heddergott et al.44 reported 47.1% (16/34) seroprevalence in a sample of 34 European wild cats in Luxembourg and found that increasing age was a predictor of antibody status. Of the 16 seropositive cats, 75% were seropositive for at least one other common feline viral infection (feline leukemia virus, feline parvovirus, feline calicivirus, or feline herpesvirus).44 Paradoxically, another group of European feral cats was seronegative in Portugal (0/26), although a third (5/15) of faecal samples were positive for viral antigen (Tables 2, 3).19 Differences in sampling and processing may explain some inconsistencies; Possible additional differences include interactions with domestic and other felines and the nature of FCoV infections.

LocationYearSeroprevalenceReferences
European wild cat (Felis silvestris), Scotland1987–19890/2364
1992–19973/4914
France1996–19972/5161
Luxembourg2001–201616/3444
Portugal1992–20070/2619
American Puma (Puma concolor), USA1978–19914/21 (IFA) vs 0/32 (KELA)97a
1987–199016/5881
1990–200425 / 180b4
2005-20080/977
1990–200874/48033
BrazilUnknown3/5103
1998–20040/1830
Canada1996–20010/1589
African lion (Panthera leo), Botswana2003-20050/2191
1992–200016 / 146b1
2008–20110/1411
2012–20140/1363
Namibia1991–20015/2231
1999–200116/9857
South Africa1987–19900/32106
1992–200043/3121
Tanzania1984–1991177 / 311c47
Uganda1997–19990/1418
Zimbabwe1990–19980/411
Germany19890 / 1d116
Table 3. Seroprevalence in non - domesticated cat species by country and year.
a) Felis concolor coryi.
b) Estimate from the bar graph presented in the study.
c) Repeated sampling.
d) Part of the diagnostic examination.
IFA uno immunofluorescence test; KELA ¼ Kinetic enzyme-linked immunosorbent assay.

American Puma (Puma concolor): A case of FIP has been reported in a young male American cougar, moving freely in California, who, in addition to enlarged lymph nodes, also had lesions in the small and large intestine, heart, lungs and brain. Interestingly, the kidneys appeared histologically normal, but viral RNA was evident.108 This case report is unique in demonstrating FIP in a free-moving animal, especially in a species that often lives alone. The risk of further cases of FIP in free-ranging bombs remains unknown and other pathogens, such as the zoonotic disease Yersinia pseudotuberculosis, have been reported in bombs with pyogranulomatous liver lesions and peritonitis.3

According to serological research in California bombs, seroprevalence appears to fluctuate during the 18 years during which samples were taken.33 In 1992, only three samples were taken, but one animal was positive, while in the next 3 years no animal was positive (n ¼46). By 1996, seroprevalence began to rise and peaked in 2000–2001, and after another period of decline, the highest seroprevalence reached almost 50% (n ¼ 29).33 Longitudinal data provided by Foley et al.33 are important because previous years do not predict future seroprevalence. An additional study in the Rocky Mountains demonstrates a high degree of correlation between antibody levels in females and their pups, even when the pups were 4 months of age or older at the time of sampling.4 In addition, statistical modeling suggests that increasing age and population location are risk factors for FCoV exposure.4 Other seroprevalences have been reported in the United States (Table 3).

Tiger (Panthera tigris): FIP was reported in an 8-year-old male tiger in captivity in Romania, which initially showed non-specific clinical signs.49 The postmortem examination corresponded to FIP and revealed uveitis, abdominal discharge and, in addition to pericarditis, serous fluid in the pericardial space.49 Macrophage staining for FIP was consistent with the diagnosis, with infected macrophages being identified in the lung and other tissues.49 Amyloid deposits have also been reported.49 There was an increase in serum amyloid A in cats with FIP, potentially similar to human patients with SARS-CoV-2,39,69 Interestingly, amyloidosis is often observed in black-legged cats (Felis nigripes); thus, there may be other host factors that lead to the presence of amyloid plaques in the tiger.111 Finally, in a tiger with FIP, liquefied necrosis was detected in the spleen, although this may not be specific for FIP infection.49

In addition to the described case of FIP in tigers, one case of peritonitis in tigers was recorded in a survey of Italian zoos between 2004 and 2015; however, whether it was related to FCoV infection has not been established and is unlikely.101 A compilation of mortality data on captive-bred tigers in India identified peritonitis in addition to enteritis, gastritis, gastroenteritis, hepatitis and gastric ulcers.107 Although no viral etiology has been reported, gastrointestinal diseases have been one of the most common causes of mortality, even during the monsoon season.107

In Siberian or Amur tigers (Panthera tigris altaica), 43% animals (n-44) were positive for the presence of FCoV antibodies (Table 4).42 Neither sex nor age was associated with seroprevalence, although longitudinal monitoring led to three other tigers becoming seropositive.42 In one case report of a Siberian tiger that succumbed to a morbillivirus infection, IFA demonstrated the presence of anti-FCoV antibodies, although this was unlikely to have contributed to the animal's death.90 In the case report of an captured Amur tiger, which was originally presented with anorexia and lethargy, the IFA was negative for FCoV; further diagnosis revealed bacterial pyothorax.104 Virus shedding was observed in another Siberian tiger considered clinically healthy, but no antibody response.56

Of the three Bengal tigers housed in the same institution, two showed antibody responses to both type I and type II FCoV, and the third showed anti-type II antibodies, although none of these animals secreted viral antigen.56

Lion (Panthera leo): In 1970, Colby reported two cases of FIP in lions.13 Although this initial report did not provide any clinical details, the ocular form of FIP in a 15-year-old captive lion was recently described and confirmed to be blind.75 The patient's clinical pathology, including anisocytosis and hypochromasia, was non-specific for FIP, although PCV (HCT) was lower than normal (31%) and total plasma protein was higher than normal (7.8 g / dl), values commonly found in domestic Histopathology revealed bilateral panuveitis and retinal detachment along with an infiltrate of lymphocytes, plasma cells and several macrophages.75 In the anterior chamber, the exudate was characterized as eosinophilic and proteinaceous, and lesions were found in the brain.75

In free-ranging lions in East Africa, 57% serum samples were evaluated as evidence of an antibody response by IFA (Table 3). 47 FCoV secretion was previously observed in the captive African lion, but without an antibody response.56 Similarly, two other lions in different institutions did not actively secrete the virus, but showed antibody responses.56,57 Interestingly, one of these lions showed a low-level antibody response to both type I and type II FCoV.56. In the case of a series of lions with encephalitis, one lion was tested for antibodies to FCoV, but appeared negative.116 In the "inbred" study of lions compared to the "outbred" population, the relationship between kinship status and FCoV antibodies was not statistically significant.115 A longitudinal study of lions in the Serengeti showed a high degree of seroprevalence variability each year, especially in younger animals.80 In addition, these data revealed possible effects on fertility and a possible link between the spread of the virus and higher population densities.80 The second longitudinal study showed a high degree of seroprevalence; in most age groups more than 50% animals demonstrated seroprevalence and a trend of increasing seroprevalence with increasing age, with a few exceptions34 (additional data from the study). In addition, FCoV seroprevalence may predict the occurrence of calicivirus or feline immunodeficiency virus (FIV).34

Common nameGenus speciesSeroprevalenceReferences
Desert catFelis margarita0/151
ManulOtocolobus manul0/376
  0/6and59
Amur catPrionailurus bengalensis euptilura0/151
  0/241
Iriomote catPrionailurus bengalensis iriomotensis14/1770
Flat-faced catPrionailurus planiceps0/151
JaguarundiPuma yagouaroundi0/131
  0/1103
OcelotLeopardus pardalis1/1103
  1/130
  0/1031
  0/1235
MargayLeopardus wiedii0/151
  4/4103
Pampas catLeopardus colocolo1/1103
Pampas catLeopardus geoffroyi0/931
  1/40118
Ocelot treeLeopardus tigrinus0/230
Rys caracalCaracal2/257
  3/3113
ServalLeptailurus serval0/251
JaguarPanthera onca3/4103
Spotted leopardPanthera pardus0/151
  1/257
  0/7113
  0/411
Sumatrian tigerPanthera tigris sondaica0/151
Ussuri TigerPanthera tigris altaica19/4442
Snow leopardPanthera uncia0/2b32
Table 4. Seroprevalence in other non-domesticated cat species.
(a) Immunodeficient animals from the Zoo. b) Part of a diagnostic run that involved two paired samples.

Serval (Leptailurus serval): Juan-Salle´sa et al.54 report two FIP cases in a group of four coexisting servers. Case 1, a two-year-old male, stopped entering the indoor area where the animals were routinely fed. It was not determined whether the cause was neurological behavioral changes or anorexia. Case 2 was an 8-year-old female with a melengesterol acetate implant, with non-specific clinical signs and mild abdominal distension.54 Exploratory laparotomy revealed abdominal effusion and FIP-like lesions, and clinical pathology demonstrated leukocytosis and anemia. Although no extensive lesions were reported in Case 1, histology revealed fibrinopurulent ventriculitis; accumulation of neutrophils, fibrin and macrophages in the brain; and severe leptomeningitis. Focal pyogranulomatous lesions were present in the kidneys.54 In case 2, in addition to pyogranulomatous necrotizing splenitis, pyogranulomatous lesions were also present in the mesentery, liver and gallbladder.54

Feature: VanRensburg and Silkstone119 mention personal communication about FIP that has affected at least one red lynx. Of the 25 red lynx in the Golden Gate National Recreation Area near San Francisco, California, the only urban red lynx was serologically positive for FCoV (Table 5).95 FCoV secretion was reported in two captive red lynx in the US Zoo, despite the absence of an antibody response.56 Similarly, in the second US zoological collection, one healthy feature in captivity secreted FCoV in the absence of an antibody response, while the other trait did not secrete virus but showed a low-level antibody response against FCoV type II.56

The Spanish lynx (Lynx pardinus) was once considered one of the most endangered wild carnivores, and as such, the risks of FCoV infection could be devastating. In one study of 22 Spanish traits evaluated by competitive enzyme-linked immunosorbent assay (ELISA) and 25 animals evaluated by IFA or rapid immunochromography, no animals showed signs of exposure or active FCoV infection.67. However, further studies have shown a seroprevalence of approximately 26%, with no apparent relationship between FCoV and FeLV.65 In a single sample of the Spanish lynx, 19/74 were positive for FCoV IFA exposure, although 0/68 animals shed virus in the faeces, as assessed by RT-PCR.65 In two other lynx features for which the cause of death could not be determined, neither animal was found to be IHC positive for FCoV, despite pancreatitis and fibrinous serositis in one of these animals.102 The effect of FCoV on the development of other disease pathologies, including membrane glomerulonephritis and lymphoid cell depletion, has also been investigated, but no study has shown an apparent link to disease development.53,86

Kind ofLocationYearSeroprevalenceReferences
Spanish Lynx (Lynx pardinus)Spain1989–20000/3798
  2003-200719/7465
  2004-20060/2267
Lynx lynxNetherlands1977–19780/151
 Sweden1993–19990/102100
Canadian Lynx (Lynx canadensis)North America1993–200112/2155
 Canada20000/589and
Red Lynx (Lynx rufus)USA1992–19951/2595
  Unknown0/1b87
Table 5. FCoV seroprevalence by lynx species species.
(a) Listed as a feature. b) Part of diagnostic processing.

Leopard (Panthera pardus): FIP has also been reported in leopards in Germany.117 No exclusion of FCoV was observed in three African leopards at two US zoos, but all three were serologically positive for type II FCoV.56 Of the other two African leopards in South Africa, only one animal was seropositive and none shed the virus (Tables 2, 4).57

Bengal wild cat (Prionailurus bengalensis): Between 2005 and 2006, 35 of a total of 1,453 rectal swab specimens obtained from Asian leopard cats in wildlife markets were positive for the new coronavirus, which found that the spike protein was phylogenetically similar to the spike protein of other alpha-coraviruses.16 However, this virus showed a phylogenetic relationship outside the group, suggesting that it separated at the beginning of the coronavirus evolutionary history, or probably represented an unidentified group of coronaviruses. Recent analysis suggests that the spike protein is related to a newly identified genus of deltacoronavirus.110 According to previously published results of an RT seminested PCR assay targeting viral polymerase, 8.8% (3/34) wild Bengal cats were positive for pancoronavirus, with a close phylogenetic relationship to FCoV.12 In Iriomote cats, subspecies (Prionailurus bengalensis iriomotensis), most animals (14/17) tested by ELISA against canine coronaviruses showed the presence of antibody (Tables 2, 4).70

Clouded Leopard (Neofelis nebulosa): In a survey of the causes of mortality of non-domesticated carnivores at Nandankanan Biological Park in Bhubaneswar, Orissa, India, peritonitis was thought to be the cause of death in one clouded leopard; 92 however, FCoV has not been studied.

Snow Leopard (Panthera uncia): FCoV secretion was observed in a healthy captive snow leopard, although no antibody response was evident.56 In contrast, virus excretion was not observed in two snow leopards at different institutions, but were positive for antibodies to FCoV type II. 56 In the case report of a 6-week-old captured bred male snow leopard with neurological disease, including cerebellar degeneration and encephalomyelopathy, FCoV was investigated as a potential cause, but was not identified.109

Ocelot (Leopardus pardalis): Philoni et al.30 reported one seropositive, caught, apparently healthy Amazonian ocelot, which was also serologically positive for feline herpesvirus1, feline calicivirus, feline parvovirus and Bartonella henselae. This single observation may have been an anomaly and the result of other underlying medical conditions. Interestingly, however, the anti-B. henselae antibody response was associated with the anti-FCoV antibody in domestic cats.40 It is not known whether a similar association exists for ocelots or other cats. Natural FCoV circulation in isolated ocelots nevertheless appears to be rare (Tables 2, 4).31,35

Swamp cat (Felis chaus): In a survey of non-domesticated feline carnivores in Nandankanan Biological Park, peritonitis was thought to be the cause of death in one jungle cat; 92 however, FCoV has not been studied.

American Jaguar (Panthera onca): FIP was considered a differential diagnosis in a case report of a newborn jaguar with respiratory difficulties that progressed to ascites.36 However, the confirmatory diagnosis did not take place and the pup recovered after extensive treatment.36 In two apparently healthy jaguars in captivity, FCoV secretion was observed; in addition, one of these animals showed an antibody response to FCoV type II. (Tables 2, 4)56

Caracal caracal: Four caracals showed an antibody response, although none animal excreted FCoV (Tables 2, 4).56,57

Discussion

In addition to other infectious diseases, feline coronavirus challenges the effort to preserve non-domesticated felines.74 Credible FIP records exist for seven non-domesticated species of felines and 15 species have shown seroprevalence. However, antigen release is observed relatively rarely. Screening and diagnostic testing are challenging and it is still difficult to determine the source of FCoV infection. In the cases reported by Watt et al.124 and Juan-Salle et al., 54 it was considered unlikely that the stray cat would be the source of the infection. Whether the virus was constantly circulating in these animals, or whether the virus was introduced in any other way, remains unknown. This leads to the need to always be vigilant with regard to biosecurity, especially in the case of endangered animals. The use of faeces to identify FCoV creates a strategy for easy sampling of both wild and captive animals; however, PCR from fecal contents may be inhibited.20 In addition, treacherous onset in some cases of FIP often requires an investigation of the potential or exposure to FCoV infection. The spectrum of clinical manifestations, in addition to the "standard clinical picture", also includes dermatological lesions, 10,93 myocarditis 22 and upper respiratory tract diseases.2

Reports of FIP outbreaks in non-domestic cats have shown that males are likely to be at higher risk than females, similar to those observed in domestic cats. FIP has only been found in European wild male cats, and through individual reports we know of FIP in mountain lion, lion and tiger, which only affected males. 49,75,108, 124 In domestic cats, males are also over-represented in FIP cases.78 In addition, in humans, SARSCoV-2 infection led to more serious consequences in men compared to women.66

While shelters and kennels are the optimal place for FCoV to spread, FCoV circulation in free-moving species can be improved by the solitary lifestyle of some of these species. The virus survives in the environment for a relatively short time, so that the transmission takes place mainly through direct or indirect interactions within the species or with other felines. In some cases, domestic cats can be a source of prey for larger non-domesticated felines. It is not known whether an infection could occur in this way, but it could be the cause of certain antibody responses or antigen secretion in the feces. Habitat changes, including fragmentation and habitat expansion, may, in addition to exposing domestic cats, lead to increased interactions within the same species in the wild.

Although antibody testing is useful for detecting previous exposure, even in non-domesticated species, a seronegative assay does not always indicate the absence of virus shedding.38,56 This discrepancy poses a challenge to understanding the true levels of FCoV circulating in feral cat populations. Several testing strategies have demonstrated the ability to detect virus shedding with a high degree of reliability, including the feasible possibility of obtaining five samples in a row.38 Taking into account critically endangered species, individuals must be adequately tested before being introduced to individuals of the same species, together with stress minimization, unnecessary anesthesia, etc. Sequential testing of faecal samples has been performed in captive animals, and similar strategies may be useful for understanding the presence or absence of FCoV in wild animal populations.

Acknowledgments: The authors greatly appreciate the members of the Whittaker Lab and the Cheetah Conservation Fund for their helpful discussion in preparing this manuscript. Jobs Dr. Stouta is supported by the National Institutes of Health comparative medicine training program (T32OD011000). The work in the author's laboratory (GRW) is partly funded by the Cornell Feline Health Center and the Winn Feline Foundation.

References

  1. Alexander KA, McNutt JW, Briggs MB, StandersPE, Funston P, Hemson G, Keet D, van Vuuren M. Multi-host pathogens and carnivore management in southern Africa. Comp Immunol Microbiol Infect Dis. 2010; 33 (3): 249–265.
  2. Andre´ NM, Miller AD, Whittaker GR. Feline infectious peritonitis virus-associated rhinitis in a cat. J Feline Med Surg Open Rep. 2020; 6 (1): 1–6.
  3. Bernard JM, Newkirk KM, McRee AE, Whittemore JC, Ramsay EC. Hepatic lesions in 90 captive nondomestic felids presented for autopsy. Vet Pathol. 2015; 52 (2): 369–376.
  4. Biek R, Ruth TK, Murphy KM, Anderson CR, Johnson M, DeSimone R, Gray R, Hornocker MG, Gillin CM, Poss M. Factors associated with pathogen seroprevalence and infection in rocky mountain cougars. J Wildl Dis. 2006; 42 (3): 606–615.
  5. Biek R, Zarnke RL, Gillin C, Wild M, Squires JR, Poss M. Serological survey for viral and bacterial infections in western populations of Canada lynx (Lynx canadensis). J Wildl Dis. 2002; 38 (4): 840–845.
  6. Briggs MB, Evermann JF, McKeirnan AJ. Felineinfectious peritonitis: an update of a captive cheetah population. Feline Pract. 1986; 16 (2): 13–16.
  7. Brower AI, Munson L, Radcliffe RW, Citino SB, Lackey LB, Van Winkle TJ, Stalis I, Terio KA, Summers BA, de Lahunta A. Leukoencephalomyelopathyof mature captive cheetahs and other large felids: a novel neurodegenerative disease that came and went? Vet Pathol. 2014; 51 (5): 1013–1021.
  8. Brown EW, Olmsted RA, Martenson JS, O'BrienSJ. Exposure to FIV and FIPV in wild and captive cheetahs. Zoo Biol. 1993; 12 (1): 135-142.
  9. Brown MA, Troyer JL, Pecon-Slattery J, RoelkeME, O'Brien SJ. Genetics and pathogenesis of feline infectious peritonitis virus. Emerg Infect Dis. 2009; 15 (9): 1445–1452.
  10. Cannon MJ, Silkstone MA, Kipar AM. Cutaneous lesions associated with coronavirus-induced vasculitis in a cat with feline infectious peritonitis and concurrent feline immunodeficiency virus infection. J Feline Med Surg. 2005; 7 (4): 233–236.
  11. Chaber AL, Cozzi G, Broekhuis F, Hartley R, JW McNutt. Serosurvey for selected viral pathogens among sympatric species of the African large predator guild in northern Botswana. J Wildl Dis. 2017; 53 (1): 170–175.
  12. Chen CC, Chang AM, Chen WJ, Chang PJ, Lai YC, Lee HH. Molecular survey for selected viral pathogens in wild leopard cats (Prionailurus bengalensis) in Taiwan with an emphasis on the spatial and temporal dynamics of carnivore protoparvovirus 1. BioRxiv [Internet]. 2020.02.21.960492; doi: https: // doi. org / 10.1101 / 2020.02.21.960492
  13. Colby ED. Feline infectious peritonitis. Vet MedSmall Anim Clin. 1970; 65 (8): 783–786.
  14. Daniels MJ, Golder MC, Jarrett O, MacDonaldDW. Feline viruses in wildcats from Scotland. J Wildl Dis. 1999; 35 (1): 121–124.
  15. Daszak P, Cunningham A, Hyatt A. Emerginginfectious diseases of wildlife — threats to biodiversity and human health. Science. 2000; 287 (5452): 443-449.
  16. Dong BQ, Liu W, Fan XH, Vijaykrishna D, TangXC, Gao F, Li LF, Li GJ, Zhang JX, Yang LQ, Poon LLM, Zhang SY, Peiris JSM, Smith GJD, Chen H, Guan Y. Detection of a novel and highly divergent coronavirus from Asian leopard Cats and Chinese ferret badgers in southern China. J Virol. 2007; 81 (13): 6920–6926.
  17. Drechsler Y, Alcaraz A, Bossong FJ, CollissonEW, Diniz PPVP. Feline coronavirus in multicat environments. Vet Clin North Am Small Anim Pract. 2011; 41 (6): 1133–1169.
  18. Driciru M, Siefert L, Prager KC, Dubovi E, Sande R, Princee F, Friday T, Munson L. A serosurvey of viral infections in lions (Panthera leo), from Queen Elizabeth National Park, Uganda. J Wildl Dis. 2006; 42 (3): 667–671.
  19. Duarte A, Fernandes M, Santos N, Tavares L.
    Virological survey in free-ranging wildcats (Felis silvestris) and feral domestic cats in Portugal. Vet Microbiol. 2012; 158 (3-4): 400-404.
  20. Dye C, Helps CR, Siddell SG. Evaluation of realtime RT-PCR for the quantification of FCoV shedding in the faeces of domestic cats. J Feline Med Surg. 2008; 10 (2-3): 167-174.
  21. Dye C, Temperton N, Siddell SG. Type I felinecoronavirus spike glycoprotein fails to recognize aminopeptidase N as a functional receptor on feline cell lines. J Gen Virol. 2007; 88 (Pt 6): 1753–1760.
  22. Ernandes MA, Cantoni AM, Armando F, Corradi A, Ressel L, Tamborini A. Feline coronavirusassociated myocarditis in a domestic longhair cat. JFMS Open Rep. 2019; 5 (2): 1–5.
  23. Evermann JF, Burns G, Roelke ME, McKeirnanAJ, Greenlee A, Ward AC, Pfeifer ML. Diagnostic features of an epizootic of feline infectious peritonitis in captive cheetahs. In: Proc Am Assoc Vet Lab Diagn; 1983. 26: 365–382.
  24. Evermann JF, Heeney JL, McKeirnan AJ, O'Brien SJ. Comparative features of a coronavirus isolated from a cheetah with feline infectious peritonitis. Virus Res. 1989; 13 (1): 15-27.
  25. Evermann JF, Heeney JL, Roelke ME,
    McKeirnan AJ, O'Brien SJ. Biological and pathological consequences of feline infectious peritonitis virus infection in the cheetah. Arch Virol. 1988; 102 (3-4): 155-171.
  26. Evermann JF, Laurenson MK, McKeirnan AJ, Caro TM. Infectious disease surveillance in captive and free-living cheetahs: an integral part of the species survival plan. Zoo Biol. 1993; 12 (1): 125-133.
  27. Evermann JF, Roelke ME, Briggs MB. Felinecoronavirus infections of cheetahs: clinical and diagnostic features. Feline Pract. 1986; 16 (3): 21-28.
  28. Felten S, Hartmann K. Diagnosis of felineinfectious peritonitis: a review of the current literature. Viruses. 2019; 11 (11): 1068.
  29. Felten S, Klein-Richers U, Hofmann-LehmannR, Bergmann M, Unterer S, Leutenegger CM, Hartmann K. Correlation of feline coronavirus shedding in feces with coronavirus antibody titer. Pathogens. 2020; 9 (8): 598.
  30. Filoni C, Cata˜o-Dias JL, Bay G, Durigon EL, Jorge RSP, Lutz H, Hofmann-Lehmann R. First evidence of feline herpesvirus, calicivirus, parvovirus, and Ehrlichia exposure in Brazilian Free-ranging felids. J Wildl Dis. 2006; 42 (2): 470–477.
  31. Fiorello CV, Noss AJ, Deem SL, Maffei L, Dubovi EJ. Serosurvey of small carnivores in the Bolivian Chaco. J Wildl Dis. 2007; 43 (3): 551–557.
  32. Fix AS, Riordan DP, Hill HT, Gill MA, EvansMB. Feline panleukopenia virus and subsequent canine distemper virus infection in two snow leopards (Panthera uncia). J Zoo Wildl Med. 1989; 20 (3): 273–281.
  33. Foley JE, Swift P, Fleer KA, Torres S, GirardYA, Johnson CK. Risk factors for exposure to feline pathogens in California mountain lions (Puma concolor). J Wildl Dis. 2013; 49 (2): 279–293.
  34. Fountain-Jones NM, Packer C, Jacquot M, Blanchet FG, Terio K, Craft ME. Endemic infection can shape exposure to novel pathogens: pathogen cooccurrence networks in the Serengeti lions. Ecol Lett. 2019; 22 (6): 904–913.
  35. Franklin SP, Kays RW, Moreno R, TerWee JA, Troyer JL, VandeWoude S. Ocelots on Barro Colorado Island are infected with feline immunodeficiency virus but not other common feline and canine viruses. J Wildl Dis. 2008; 44 (3): 760–765.
  36. Fransen DR. Feline infectious peritonitis in an infantile jaguar. In: Proc Am Assoc Zoo Vet; 1974. 261– 264.
  37. Furtado MM, Taniwaki SA, de Barros IN, Branda˜o PE, Cata˜o-Dias JL, Cavalcanti S, Cullen L, Filoni C, Almeida Ja´como AT de, Jorge RSP, Silva NDS, Silveira L, Ferreira Neto JS . Molecular detection of viral agents in free-ranging and captive neotropical felids in Brazil. J Vet Diagn Invest. 2017; 29 (5): 660– 668.
  38. Gaffney PM, Kennedy M, Terio K, Gardner I, Lothamer C, Coleman K, Munson L. Detection of feline coronavirus in cheetah (Acinonyx jubatus) feces by reverse transcription-nested polymerase chain reaction in cheetahs with variable frequency of viral shedding. J Zoo Wildl Med. 2012; 43 (4): 776–786.
  39. Giordano A, Spagnolo V, Colombo A, PaltrinieriS. Changes in some acute phase protein and immunoglobulin concentrations in cats affected by feline infectious peritonitis or exposed to feline coronavirus infection. Vet J. 2004; 167 (1): 38–44.
  40. Glaus T, Hofmann-Lehmann R, Greene C, Glaus B, Wolfensberger C, Lutz H. Seroprevalence of Bartonella henselae infection and correlation with disease status in cats in Switzerland. J Clin Microbiol. 1997; 35 (11): 2883–2885.
  41. Goncharuk MS, Kerley LL, Naidenko SV, Rozhnov VV. Prevalence of seropositivity to pathogens in small carnivores in adjacent areas of Lazovskii Reserve. Biol Bull Russ Acad Sci. 2012; 39 (8): 708–713.
  42. Goodrich JM, Quigley KS, Lewis JCM, AstafievAA, Slabi EV, Miquelle DG, Smirnov EN, Kerley LL, Armstrong DL, Quigley HB, Hornocker MG. Serosurvey of free-ranging Amur tigers in the Russian Far East. J Wildl Dis. 2012; 48 (1): 186–189.
  43. Guimaraes AMS, Branda˜o PE, Moraes W de, Cubas ZS, Santos LC, Villarreal LYB, Robes RR, Coelho FM, Resende M, Santos RCF, Oliveira RC, Yamaguti M, Marques LM, Neto RL, Buzinhani M, Marques R , Messick JB, Biondo AW, Timenetsky J. Survey of feline leukemia virus and feline coronaviruses in captive neotropical wild felids from southern Brazil. J Zoo Wildl Med. 2009; 40 (2): 360–364.
  44. Heddergott M, Steeb S, Osten-Sacken N, Steinbach P, Schneider S, Pir JP, Mu¨ller F, Pigneur LM, Frantz AC. Serological survey of feline viral pathogens in free-living European wildcats (Felis s. Silvestris) from Luxembourg. Arch Virol. 2018; 163 (11): 3131–3134.
  45. Heeney JL, Evermann JF, McKeirnan AJ, Marker-Kraus L, Roelke ME, Bush M, Wildt DE, Meltzer DG, Colly L, Lukas J. Prevalence and implications of feline coronavirus infections of captive and freeranging cheetahs (Acinonyx jubatus). J Virol. 1990; 64 (5): 1964–1972.
  46. Herrewegh AAPM, Smeenk I, Horzinek MC, Rottier PJM, Groot RJ de. Feline coronavirus type II strains 79-1683 and 79-1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J Virol. Ame Soc Microbiol J. 1998; 72 (5): 4508–4514.
  47. Hofmann-Lehmann R, Fehr D, Grob M, ElgizoliM, Packer C, Martenson JS, O'Brien SJ, Lutz H.
    Prevalence of antibodies to feline parvovirus, calicivirus, herpesvirus, coronavirus, and immunodeficiency virus and of feline leukemia virus antigen and the interrelationship of these viral infections in freeranging lions in east Africa. Clin Diagn Lab Immunol. 1996; 3 (5): 554–562.
  48. Holzworth J. Some important disorders of cats.Cornell Vet. 1963; 53: 157–160.
  49. Horhogea C, Lazar M. Immunohistochemicalmethods to diagnose atraumatic spleen rupture in feline infectious peritonitis of tiger (Panthera tigris). Rev Chim Buchar. 2017; 68 (5): 1055.
  50. Horzinek MC, Osterhaus AD. The virology andpathogenesis of feline infectious peritonitis. Brief review. Arch Virol. 1979; 59 (1-2): 1-15.
  51. Horzinek MC, Osterhaus ADME. Feline infectious peritonitis: a worldwide serosurvey. Am J Vet Res. 1979; 40 (10): 1487–1492.
  52. Jaimes JA, Millet JK, Stout AE, Andre´ NM, Whittaker GR. A tale of two viruses: the distinct spike glycoproteins of feline coronaviruses. Viruses. 2020; 12 (1): 83.
  53. Jime´nez A, Sa´nchez B, Pe´rez Alenza D, Garcı´a P, Lo´pez JV, Rodriguez A, Mun˜oz A, Martı´nez F, Vargas A, Pen˜a L. Membranous glomerulonephritis in the Iberian lynx (Lynx pardinus). Vet Immunol Immunopathol. 2008; 121 (1–2): 34–43.
  54. Juan-Salle´s C, Domingo M, Herra´ez P, Ferna´ndez A, Segale´s J, Ferna´ndez J. Feline infectious peritonitis in servals (Felis serval). Vet Rec. 1998; 143 (19): 535–536.
  55. Kennedy M, Citino S, Dolorico T, McNabb AH, Moffat AS, Kania S. Detection of feline coronavirus infection in captive cheetahs (Acinonyx jubatus) by polymerase chain reaction. J Zoo Wildl Med. 2001;
    32 (1): 25-30.
  56. Kennedy M, Citino S, McNabb AH, Moffatt AS, Gertz K, Kania S. Detection of feline coronavirus in captive Felidae in the USA. J Vet Diagn Invest. 2002; 14 (6): 520–522.
  57. Kennedy M, Kania S, Stylianides E, BertschingerH, Keet D, van Vuuren M. Detection of feline coronavirus infection in southern African nondomestic felids. J Wildl Dis. 2003; 39 (3): 529-535.
  58. Kennedy MA, Moore E, Wilkes RP, Citino SB, Kania SA. Analysis of genetic mutations in the 7a7b open reading frame of coronavirus of cheetahs (Acinonyx jubatus). Am J Vet Res. 2006; 67 (4): 627–632.
  59. Ketz-Riley CJ, Ritchey JW, Hoover JP, JohnsonCM, Barrie MT. Immunodeficiency associated with multiple concurrent infections in captive Pallas' cats (Otocolobus manul). J Zoo Wildl Med. 2003; 34 (3): 239-245.
  60. Kipar A, Meli ML. Feline infectious peritonitis:
    still an enigma? Vet Pathol. 2014; 51 (2): 505–526.
  61. Leutenegger CM, Hofmann-Lehmann R, RiolsC, Liberek M, Worel G, Lups P, Fehr D, Hartmann M, Weilenmann P, Lutz H. Viral infections in free-living populations of the European wildcat. J Wildl Dis. 1999; 35 (4): 678–686.
  62. Masot AJ, Gil M, Risco D, Jime´nez OM, Nu´nez˜ JI, Redondo E. Pseudorabies virus infection (Aujeszky's disease) in an Iberian lynx (Lynx pardinus) in Spain: a case report. BMC Vet Res. 2016; 13 (1): 6.
  63. McDermid KR, Snyman A, Verreynne FJ, Carroll JP, Penzhorn BL, Yabsley MJ. Surveillance for viral and parasitic pathogens in a vulnerable African lion (Panthera leo) population in the Northern Tuli Game Reserve, Botswana. J Wildl Dis. 2017; 53 (1): 54–61.
  64. McOrist S, Boid R, Jones TW, Easterbee N, Hubbard AL, Jarrett O. Some viral and protozool diseases in the European wildcat (Felis silvestris). J Wildl Dis. 1991; 27 (4): 693-696.
  65. Meli ML, Cattori V, Martínez F, Lo´pez G, Vargas A, Simo´n MA, Zorrilla I, Mun˜oz A, Palomares F, Lo´pez-Bao JV, Pastor J, Tandon R, Willi B , Hofmann-Lehmann R, Lutz H. Feline leukemia virus and other pathogens as important threats to the survival of the critically endangered Iberian lynx (Lynx pardinus). PLOS ONE. 2009; 4 (3): e4744.
  66. Meng Y, Wu P, Lu W, Liu K, Ma K, Huang L, Cai J, Zhang H, Qin Y, Sun H, Ding W, Gui L, Wu P.
    Sex-specific clinical characteristics and prognosis of coronavirus disease-19 infection in Wuhan, China: a retrospective study of 168 severe patients. PLOS Pathog. 2020; 16 (4): e1008520.
  67. Milla´n J, Candela MG, Palomares F, Cubero MJ, Rodrı´guez A, Barral M, de la Fuente J, Almerı´a S, Leo´n-Vizcaı´no L. Disease threats to the endangered Iberian lynx (Lynx pardinus). Vet J. 2009; 182 (1): 114– 124.
  68. Millet JK, Whittaker GR. Host cell proteases: critical determinants of coronavirus tropism and pathogenesis. Virus Res. 2015; 202 (2015): 120-134.
  69. Mo XN, Su ZQ, Lei CL, Chen DF, Peng H, Chen RC, Sang L, Wu HK, Li SY. Serum amyloid A is a predictor for prognosis of COVID-19. Respirology. 2020; 25 (7): 764–765.
  70. Mochizuki M, Akuzawa M, Nagatomo H. Serological survey of the Iriomote cat (Felis iriomotensis) in Japan. J Wildl Dis. 1990; 26 (2): 236-245.
  71. Munson L. Diseases of captive cheetahs (Acinonyx jubatus): results of the cheetah research council pathology survey, 1989–1992. Zoo Biol. 1993; 12 (1): 105–124.
  72. Munson L, Marker L, Dubovi E, Spencer JA,
    Evermann JF, O'Brien SJ. Serosurveyof viral infections in free-ranging Namibian cheetahs (Acinonyx jubatus). J Wildl Dis. 2004; 40 (1): 23–31.
  73. Murphy BG, Perron M, Bauer K, Park Y, Eckstrand C, Liepnieks M, Pedersen NC. The nucleoside analog GS-441524 strongly inhibits feline infectious peritonitis (FIP) virus in tissue culture and experimental cat infection studies. Vet Microbiol. 2018; 219 (2018): 226–233.
  74. Murray DL, Kapke CA, Evermann JF, FullerTK. Infectious disease and the conservation of freeranging large carnivores. Anim Conserv. 1999; 2 (4): 241–254.
  75. Mwase M, Shimada K, Mumba C, Yabe J,
    Squarre D, Madarame H. Positive immunolabelling for feline infectious peritonitis in an African lion (Panthera leo) with bilateral panuveitis. J Comp Pathol. 2015; 152 (2-3): 265-268.
  76. Naidenko SV, Pavlova EV, Kirilyuk VE. Detection of seasonal weight loss and a serologic survey of potential pathogens in wild Pallas' cats (Felis [Otocolobus] manul) of the Daurian steppe, Russia. J Wildl Dis. 2014; 50 (2): 188–194.
  77. Nicholson KL, Noon TH, Krausman PR. Serosurvey of mountain lions in southern Arizona. Wildl Soc Bull. 2012; 36 (3): 615–620.
  78. Norris JM, Bosward KL, White JD, Baral RM, Catt MJ, Malik R. Clinicopathological findings associated with feline infectious peritonitis in Sydney, Australia: 42 cases (1990–2002). Aust Vet J. 2005; 83 (11): 666–673.
  79. O'Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colly L, Evermann JF, Bush M, Wildt DE. Genetic basis for species vulnerability in the cheetah. Science. 1985; 227 (4693): 1428–1434.
  80. Packer C, Altizer S, Appel M, Brown E, Martenson J, O'Brien SJ, Roelke-Parker M, HofmannLehmann R, Lutz H. Viruses of the Serengeti: patterns of infection and mortality in African lions. J Anim Ecol. 1999; 68 (6): 1161–1178.
  81. Paul-Murphy J, Work T, Hunter D, McFie E, Fjelline D. Serologic survey and serum biochemical reference ranges of the free-ranging mountain lion (Felis concolor) in California. J Wildl Dis. 1994; 30 (2): 205-215.
  82. Pedersen NC. A review of feline infectiousperitonitis virus infection: 1963–2008. J Feline Med Surg. 2009; 11 (4): 225–258.
  83. Pedersen NC, Allen CE, Lyons LE. Pathogenesisof feline enteric coronavirus infection. J Feline Med Surg. 2008; 10 (6): 529–541.
  84. Pedersen NC, Perron M, Bannasch M, Montgomery E, Murakami E, Liepnieks M, Liu H. Efficacy and safety of the nucleoside analog GS-441524 for the treatment of cats with naturally occurring feline infectious peritonitis. J Feline Med Surg. 2019; 21 (4): 271–281.
  85. Pedersen NC, Sato R, Foley JE, Poland AM.Common virus infection in cats, before and after being placed in shelters, with emphasis on feline enteric coronavirus. J Feline Med Surg. 2004; 6 (2): 83–88.
  86. Pen˜a L, Garcia P, Jime´nez MA´, Benito A, Alenza MDP, Sa´nchez B. Histopathological and immunohistochemical findings in lymphoid tissues of the endangered Iberian lynx (Lynx pardinus). Comp Immunol Microbiol Infect Dis. 2006; 29 (2): 114-126.
  87. Persky ME, Jafarey YS, Christoff SE, MaddoxDD, Stowell SA, NortonTM. Tick paralysis in a freeranging bobcat (Lynx rufus). J Am Vet Med Assoc.
    2020; 256 (3): 362-364.
  88. Pfeifer ML, Evermann JF, Roelke ME, GallinaAM, Ott RL, McKeirnan AJ. Feline infectious peritonitis in a captive cheetah. J Am Vet Med Assoc. 1983; 183 (11): 1317–1319.
  89. Philippa JDW, Leighton FA, Daoust PY, NielsenO, Pagliarulo M, Schwantje H, Shury T, Van Herwijnen R, Martina BEE, Kuiken T, Van de Bildt MWG, Osterhaus ADME. Antibodies to selected pathogens in free-ranging terrestrial carnivores and marine mammals in Canada. Vet Rec. 2004; 155 (5): 135–140.
  90. Quigley KS, Evermann JF, Leathers CW, Armstrong DL, Goodrich J, Duncan NM, Miquelle DG. Morbillivirus infection in a wild Siberian tiger in the Russian Far East. J Wildl Dis. 2010; 46 (4): 1252–1256.
  91. Ramsauer S, Bay G, Meli M, Hofmann-Lehmann R, Lutz H. Seroprevalence of selected infectious agents in a free-ranging, low-density lion population in the Central Kalahari Game Reserves in Botswana. Clin Vaccine Immunol. 2007; 14 (6): 808–810.
  92. Rao AT, Acharjyo LN. Etiopathology of mortality in Indian lesser cats at Nandankanan Biological Park. Indian Vet J. 1994; 71 (6): 550–553.
  93. Redford T, Al-Dissi AN. Feline infectious peritonitis in a cat presented because of papular skin lesions. Can Vet J. 2019; 60 (2): 183–185.
  94. Riad A, Kassem I, Hockova B, Badrah M, Klugar M. Tongue ulcers associated with SARS-CoV2 infection: a case series. Oral Dis. 2020. doi: 10.1111 / odi.13635
  95. Riley SPD, Foley J, Chomel B. Exposure tofeline and canine pathogens in bobcats and gray foxes in urban and rural zones of a national park in
    California. J Wildl Dis. 2004; 40 (1): 11-22.
  96. Robert N, Walzer C. Pathological disorders incaptive cheetahs. In: Vargas A, Breitenmoser-Wu¨rsten C, Breitenmoser U (eds.). Iberian Lynx ex situ conservation: an interdisciplinary approach]. Madrid (Spain): Biodiversity Fundation / IUCN Cat Specialist Group; 2009. p. 265–272.
  97. Roelke M, Forrester D, Jacobson E, Kollias G, Scott F, Barr M, Evermann J, Pirtle E. Seroprevalence of infectious disease agents in free-ranging Florida panthers (Felis concolor coryi). J Wildl Dis. 1993; 29 (1): 36-49.
  98. Roelke ME, Johnson WE, Milla´n J, Palomares F, Revilla E, Rodrí´guez A, Calzada J, Ferreras P, Leo´nVizcaı´no L, Delibes M, O'Brien SJ. Exposure to disease agents in the endangered Iberian lynx (Lynx pardinus). Eur J Wildl Res. 2008; 54 (2): 171–178.
  99. Rottier PJM, Nakamura K, Schellen P, VoldersH, Haijema BJ. Acquisition of macrophage tropism during the pathogenesis of feline infectious peritonitis is determined by mutations in the feline coronavirus spike protein. J Virol. 2005; 79 (22): 14122–14130.
  100. Ryser-Degiorgis M, Hofmann-Lehmann R, Leutenegger CM, Segerstad CH, Morner T, Mattsson R, Lutz H. Epizootiologic investigations of selected infectious disease agents in free-ranging Eurasian lynx from Sweden. J Wildl Dis. 2005; 41 (1): 58–66.
  101. Scaglione FE, Biolatti C, Pregel P, Berio E, Cannizzo FT, Biolatti B, Bollo E. A survey on zoo mortality over a 12-year period in Italy. PeerJ. 2019; 7: e6198.
  102. Schmidt-Posthaus H, Breitenmoser-Wu¨rsten C, Posthaus H, Bacciarini L, Breitenmoser U. Causes of mortality in reintroduced Eurasian lynx in Switzerland. J Wildl Dis. 2002; 38 (1): 84–92.
  103. Schmitt AC, Reischak D, Clavac CL, MonforteCHL, Couto FT, Almeida ABPF, Santos DGG, Souza L, Alves C, Vecchi K. life and knowledge of the Pantanal matogrossense region. [Feline leukemia and feline peritonitis virus infection in captive and wildcats from Mato Grosso swamp region]. Acta Sci Vet. 2003; 31 (3): 185-188.
  104. Schrader GM, Whiteside DP, Slater OM, BlackSR. Conservative management of pyothorax in an Amur tiger (Panthera tigris altaica). J Zoo Wildl Med. 2012; 43 (2): 425–429.
  105. Spencer JA. Lack of antibodies to coronaviruses in a captive cheetah (Acinonyx jubatus) population. JS Afr Vet Assoc. 1991; 62 (2): 124–125.
  106. Spencer JA. Survey of antibodies to felineviruses in free-ranging lions. South Afr J Wildl Res, 1991; 21 (2): 59–61.
  107. Srivastav A, Chakrabarty B. Seasonal distribution of deaths of tigers (Panthera tigris) in Indian zoos. Zoos Print J. 2002; 17 (3): 741–743.
  108. Stephenson N, Swift P, Moeller RB, Worth SJ, Foley J. Feline infectious peritonitis in a mountain lion (Puma concolor), California, USA. J Wildl Dis. 2013; 49 (2): 408–412.
  109. Stidworthy MF, Lewis JCM, Penderis J, PalmerAC. Progressive encephalomyelopathy and cerebellar degeneration in a captive-bred snow leopard (Uncia uncia). Vet Rec. 2008; 162 (16): 522–524.
  110. Stout AE, Andre´ NM, Jaimes JA, Millet JK, Whittaker GR. Coronaviruses in cats and other companion animals: where does SARS-CoV-2 / COVID-19 fit? Vet Microbiol. 2020; 247: 108777. doi: 10.1016 / j. vetmic.2020.108777
  111. Terio KA, O'Brien T, Lamberski N, FamulaTR, Munson L. Amyloidosis in black-footed cats (Felis nigripes). Vet Pathol. 2008; 45 (3): 393–400.
  112. Terio KA, Walzer ME, Schmidt-Kuntzel A, Marker L, Citino S. Diseases impacting captive and free-ranging cheetahs. In: Marker L, Boast, LK, Schmidt-Kuntzel A. Cheetahs: biology and conservation. Biodiversity of the world: conservation from genes to landscapes. Cambridge (MA): Academic Press; 2018. p. 349–364.
  113. Thalwitzer S, Wachter B, Robert N, Wibbelt G, Mu¨ller T, Lonzer J, Meli ML, Bay G, Hofer H, Lutz H. Seroprevalences to viral pathogens in free-ranging and captive cheetahs (Acinonyx jubatus) on Namibian farmland . Clin Vaccine Immunol. 2010; 17 (2): 232–238.
  114. 114. Tresnan DB, Levis R, Holmes KV. Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J Virol. 1996; 70 (12): 8669-8674.
  115. Trinkel M, Cooper D, Packer C, Slotow R.
    Inbreeding depression increases susceptibility to bovine tuberculosis in lions: an experimental test using an inbred-outbred contrast through translocation. J Wildl Dis. 2011; 47 (3): 494–500.
  116. Truyen U, Stockhofe-Zurwieden N, KaadenOR, Pohlenz J. A case report: encephalitis in lions. Pathological and virological findings. Dtsch Tierarztl Wochenschr. 1990; 97 (2): 89-91.
  117. Tuch K, Witte KH, Wu¨ller H. Feststellung der Felinen Infektio¨sen Peritonitis (FIP) bei Hauskatzen und Leoparden v Deutschland [Determination of feline infectious peritonitis (FIP) in domestic cats and leopards in Germany]. J Vet Med B Infect Dis Vet
    Public Health. 1974; 21 (6): 426–441.
  118. Uhart MM, Rago MV, Marull CA, Ferreyra Hdel V, Pereira JA. Exposure to selected pathogens in Geoffroy's cats and domestic carnivores from central Argentina. J Wildl Dis. 2012; 48 (4): 899–909.
  119. Van Rensburg IB, Silkstone MA. Concomitantfeline infectious peritonitis and toxoplasmosis in a cheetah (Acinonyx jubatus). JS Afr Vet Assoc. 1984; 55 (4): 205–207.
  120. Walzer C, Ku¨bber-Heiss A, Gelbmann W, Suchy A, Weissenblo¨ck H. Acute hind limb paresis in Cheetah (Acinonyx jubatus) cubs. In: Proc Eur Assoc Zoo Wildl Vet; 1998. p. 267–274.
  121. Walzer C, Url A, Robert N, Ku¨bber-Heiss A, Nowotny N, Schmidt P. Idiopathic acute onset myelopathy in cheetah (Acinonyx jubatus) cubs. J Zoo Wildl Med. 2003; 34 (1): 36–46.
  122. Wang L, Mitchell PK, Calle PP, Bartlett SL, McAloose D, Killian ML, Yuan F, Fang Y, Goodman LB, Fredrickson R, Elvinger F, Terio K, Franzen K, Stuber T, Diel DG, Torchetti MK. Complete genome sequence of SARS-CoV-2 in a tiger from a US zoological collection. Microbiol Resour Announc. 2020; 9 (22): e00468-20.
  123. Wang Y, Su B, Hsieh L, Chueh L. An outbreacof feline infectious peritonitis in a Taiwanese shelter: molecular and epidemiological evidence for horizontal transmission of a novel type II feline coronavirus. Vet Res. 2013; 44 (1): 57.
  124. Watt NJ, MacIntyre NJ, McOrist S. An extended outbreak of infectious peritonitis in a closed colony of European wildcats (Felis silvestris). J Comp Pathol. 1993; 108 (1): 73–79.
  125. Weiss RC, Scott FW. Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp Immunol Microbiol Infect Dis. 1981; 4 (2): 175-189.
  126. Zook BC, King NW, Robison RL, McCombs
    HL. Ultrastructural evidence for the viral etiology of feline infectious peritonitis. Pathol Vet. 1968; 5 (1): 91-95.

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