Concurrent oral shedding of feline calicivirus and herpesvirus 1 in cats with chronic gingivostomatitis

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Concurrent oral shedding of feline calicivirus and herpesvirus 1 in cats with chronic gingivostomatitis

  1. 1. Oral Microbiology Immunology 2003: 18: 131±134Printed in Denmark. All rights reserved Short communicationConcurrent oral shedding of feline M. J. LommerÃ, F. J. M. Verstraete Department of Surgical and Radiological Sciences, School of Veterinary Medicine,calicivirus and feline herpesvirus University of California, Davis, CA, USA Ã Current af®liation: Aggie Animal Dental Service, San Francisco, CA, USA1 in cats with chronicgingivostomatitisLommer MJ, Verstraete FJM. Concurrent oral shedding of feline calicivirus and felineherpesvirus 1 in cats with chronic gingivostomatitis.Oral Microbiol Immunol 2003: 18: 131±134. ß Blackwell Munksgaard, 2003.Oral mucosal salivary samples were collected from 25 cats with chronic Key words: cats; feline calicivirus; felinegingivostomatitis and 24 cats with periodontal disease. Viral culture and isolation of herpesvirus 1; stomatitisfeline calicivirus and feline herpesvirus 1 were performed. Eighty-eight per cent of catswith chronic gingivostomatitis were shedding both viruses, compared to 21% of cats F J. M. Verstraete, Department of Surgical .without chronic oral in¯ammatory disease. Cats with chronic gingivostomatitis are and Radiological Sciences, School of Veterinary Medicine, University of California,signi®cantly more likely to concurrently shed both feline calicivirus and feline Davis, CA 95616, USAherpesvirus 1 than are cats with classical periodontal disease. Accepted for publication June 25, 2002In¯ammatory conditions affecting the oral (FORL) may be present (5). Histopatholo- this study was to determine the prevalencemucosa and gingiva of cats are commonly gic examination of affected tissues typi- of concurrent feline herpesvirus and calici-seen in veterinary practice. `Feline stoma- cally reveals in®ltrates of lymphocytes and virus infection in cats with chronic stomatitistitis consists of a number of syndromes plasma cells (5, 12), giving this complex compared to that in cats with routine period-with the common presenting clinical sym- the name `lymphocytic-plasmacytic gingi- ontal disease.ptom being severe in¯ammation of the vitis-stomatitis (LPGS). The initiating Oral mucosal salivary samples weregingiva and oral mucosa. These cases pre- cause is usually not identi®ed, and may collected from feline patients presentedsent a diagnostic and therapeutic challenge differ from case to case. It has been noted to the Veterinary Medical Teaching Hos-to veterinarians. Clinical signs include ha- that oral tissue in¯ammatory responses may pitals Dentistry and Oral Surgery Servicelitosis, ptyalism, dysphagia, pawing at the be similar despite different etiologies, and at the University of California, Davis be-mouth, poor grooming, and weight loss. that secondary infection by oral microbes tween April 1997 and October 1999.Oral examination may reveal proliferative often leads to a super®cial suppurative Twenty-four cats presented for periodontaland/or ulcerative in¯ammation of the phar- process overlying the more chronic in®l- treatment of mild to moderate periodontalynx, the mucosa lateral to the palatoglossal trate (22), making determination of the disease (11), and 25 cats presented forfolds, gingiva, buccal or palatal mucosa, or initiating cause dif®cult. The underlying treatment of chronic gingivostomatitistongue. The area lateral to the palatoglos- pathophysiologic process leading to feline were included in the study. All cats under-sal folds is commonly referred to as the gingivitis-stomatitishasnotbeen elucidated. went a complete oral examination includ-`fauces and in¯ammation in this area as Affected cats may be actively shedding ing periodontal probing and full-mouth`faucitis; however, the fauces is in fact the feline calicivirus, feline immunode®ciency radiographs. Cats in the periodontal dis-area surrounding the tonsils, or the lateral virus, and/or feline leukemia virus in saliva ease group only had mild to moderatewalls of the pharynx, caudomedial to the (21, 22, 25, 26, 34, 38, 41). While the role plaque and calculus accumulation, mildpalatoglossal folds (1). The term `caudal of calicivirus in the pathogenesis of chronic to moderate gingivitis, and/or mild to mod-stomatitis will therefore be used, instead stomatitis has been investigated (14, 26, 34, erate increased probing depths without anyof `faucitis, to denote in¯ammation in 35, 38), feline herpesvirus has not been ex- other in¯ammatory lesions in the rest ofthis area. Concomitant periodontal disease amined in conjunction with feline calicivirus the oral cavity. Cats in the chronic gingi-and feline odontoclastic resorption lesions as a possible etiologic factor. The purpose of vostomatitis group were presented with a
  2. 2. 132 Lommer & Verstraetehistory of dysphagia, weight loss, or signs Table 1. Results of viral isolationof oral pain, and were found to have pro-liferative or ulcerative in¯ammation of the Stomatitis Periodontal disease 95% confidence (n ˆ 25) (n ˆ 24) intervalpharynx, the mucosa lateral to the palato-glossal folds, the buccal or palatal mucosa, FHV positive à à FCV positive 22 5 (0.4056, 0.8115)and/or tongue, in addition to the severegingivitis typical of the disease. Cats po- FHV positivesitive for either feline leukemia virus or FCV negative 1 1 (À0.1608, 0.1624)feline immunode®ciency virus were ex- FHV negativecluded. Immediately following anesthetic FCV positive 2 1 (À0.1325, 0.2114)induction and prior to performance of any FHV negative 0 17 à (À0.9486, À0.5658) Ãdental procedures, a sterile cotton-tipped FCV negativeviral culture swab was rolled several times Ãover the gingiva, buccal and caudal oral Statistically significant.mucosa, then placed in viral culture med-ium. Samples were inoculated on Crandell- odontoclastic resorption lesions were pre- chronic caudal stomatitis or generalizedReese feline kidney (CRFK) cells (ATCC sent in 59.1% of the stomatitis cats and in stomatitis. However, there is evidence thatCCL-94; American Type Culture Collec- 45.8% of the control cats. Two of the the virus is present in cats with chronic oraltion, Rockville, MD) and incubated at stomatitis cats were edentulous, and data disease: shedding of feline calicivirus has378C in 5% CO2. Observation for cyto- on FORL were unavailable for one addi- been demonstrated in 50±92% of cats withpathic effect was performed twice weekly. tional stomatitis cat, so FORL statistics chronic in¯ammation of the gingiva andNegative cytopathic effect after three pas- were computed based on n ˆ 22 for the oral mucosa (14, 35). The site of persis-sages (approximately 10 days) constituted stomatitis cats. There was no statistically tence has been found to be the tonsil anda negative diagnosis. Observation of posi- signi®cant difference between the two adjacent mucosa (4, 37). In the currenttive cytopathic effect resulted in a positive groups with regard to breed status or pre- study, 96% of cats with chronic gingivos-diagnosis, and was followed by serum-virus sence of FORL. tomatitis were shedding calicivirus. It wasneutralization, also on CRFK cells, with Because viral shedding may be in¯u- initially thought that different strains ofantisera against feline calicivirus (ATCC enced by steroid administration (20, 21, calicivirus may result in varying clinicalVR-956 AS; American Type Culture Col- 39), and gingivostomatitis is often treated syndromes: when a large sample of felinelection) and feline herpesvirus 1 (Animal with corticosteroids, the medical history of calicivirus-shedding cats was divided intoResource Services, University of Califor- each cat in the study was reviewed. Of the groups according to clinical signs (asymp-nia, Davis, CA). Twice-weekly observa- 27 cats for whom results of viral isolation tomatic shedders, cats with acute oral andtion for cytopathic effect was performed to of both herpesvirus 1 and calicivirus were respiratory disease, and cats with chroniccon®rm isolation of either or both viruses. positive, 13 (48.1%) had received either stomatitis), virus neutralization assays re- Cats were also classi®ed according to injectable or oral corticosteroids in the vealed that isolates from chronic stomatitisbreed, and the presence of FORL was 6 weeks prior to viral culture. Cats who cats differed from the other clinical groupsnoted. Statistical analysis was performed tested positive for both viruses were not (3). However, this is more likely to be theusing 95% con®dence intervals (a Wilson more likely to have received steroids than result of antigenic variation of the virusprocedure without correction for continu- not to have received steroids within the within the host during persistent infectionity) to compare viral isolation ®ndings, 6 weeks prior to testing (Fisher exact prob- (15, 23). It is currently believed that spe-breed status, and presence of FORL be- ability test, P ˆ 1.085). ci®c biotypes for distinct disease manifes-tween the two groups. Feline calicivirus is a common upper tations are unlikely, but that the antigenic Of 25 cats with chronic gingivostoma- respiratory pathogen, and has been impli- variation occurs related to the presence oftitis, 22 (88%) were actively shedding both cated in the pathogenesis of chronic oral hypervariable regions of the capsid pro-feline herpesvirus and feline calicivirus in disease (26). It has been suggested that tein, which is typical for the Caliciviridaesaliva. One cat was shedding only herpes- calicivirus infection is responsible for the family (8, 23). A speci®c tissue af®nity forvirus, and two cats were shedding only development of in¯ammation in the caudal different strains could also not be demon-calicivirus. None of these 25 cats was aspect of the oral cavity: 100% of a small strated (36). The antigenic variation is alsonegative for both viruses. sample of cats with caudal stomatitis were likely to be responsible for the differences Of 24 cats with periodontal disease, ®ve shedding calicivirus, compared with 61% between feline calicivirus isolates from(21%) were actively shedding both feline of cats with oral disease and 19% of ran- different geographical origins (13, 16).herpesvirus 1 and feline calicivirus in saliva. domly selected cats. Several different strains The second virus investigated in thisSeventeen (71%) were negative for both were identi®ed in these cases. Speci®c- study, feline herpesvirus 1, is most com-viruses; one cat was positive for herpes- pathogen-free cats inoculated with any of monly associated with rhinotracheitis invirus only, and one cat was positive for four calicivirus strains isolated from clin- cats. It has also been linked with manycalicivirus only. Cats with stomatitis were ical cases developed acute caudal stoma- other clinical syndromes, includingsigni®cantly more likely than cats with titis (26). chronic conjunctivitis and keratitis, phar-periodontal disease to be positive for both Although it is recognized that feline yngitis, ulcerative glossitis and palatitis,viruses, and signi®cantly less likely to be calicivirus can cause acute caudal stoma- facial dermatitis, abortion, and neonatalnegative for both viruses (Table 1). titis and glossitis, its role in chronic oral mortality (9, 19, 21, 22, 31). Immunization Of the stomatitis cats, six (24.0%) were in¯ammation has not been elucidated. does not prevent acute or latent infectionpurebred; six of the periodontal disease None of the inoculated speci®c-patho- with feline herpesvirus, or virus shedding,group (25.0%) were also purebred. Feline gen-free cats in the above study developed but clinical signs may be less severe in
  3. 3. Calicivirus and herpesvirus in cats 133vaccinated cats (21, 28). During acute out stomatitis and are `predisposed by Acknowledgmentsstages of illness, the virus may be easily LP(G)S to occur (40). If the in¯ammatory The authors wish to thank Dr N. C. Ped-isolated from conjunctival, oropharyngeal, process leading to chronic gingivostoma- ersen for his contributions to this project.or nasal swabs of symptomatic animals titis were also implicated in the develop-(22). Isolation of feline herpesvirus is more ment of FORL, one would expect a higherdif®cult following resolution of clinical prevalence of FORL in cats with stomatitis Referencessigns. Once recovered, cats may become compared to those with routine periodontal 1. Bezuidenhout AJ. Oral anatomy. In: Slatterlatent carriers, as the virus persists in cra- disease. In this study, the prevalence of DH, ed. Textbook of small animal surgery,nial tissues, including trigeminal ganglia, resorptive lesions was not signi®cantly 3rd edn. Philadelphia: W. B. Saunders,optic nerves, olfactory bulbs, and corneas different between the two groups. 2003, 2630±2637.(20, 27, 39). Shedding may recur during The results of this study indicate that 2. Contreras A, Slots J. Herpesviruses inperiods of stress or following corticoster- concomitant infection with both feline her- human periodontal disease. J Periodont Res 2000: 35: 3±16.oid administration (20, 21, 39). Recently pesvirus and feline calicivirus is more 3. Dawson S, McArdle F, Bennett M et al.developed polymerase chain reaction (PCR) common in cats with chronic gingivosto- Typing of feline calicivirus isolates fromassays for feline herpesvirus 1 have greater matitis than in cats with routine period- different clinical groups by virus neutralisa-sensitivity than viral culture for detecting ontal disease. It should be noted that these tion tests. Vet Rec 1993: 133: 13±17.the virus in vaccinated cats (32, 33), and ®ndings are not an indication of a causal 4. Dick CP, Johnson RP, Yamashiro S. Sites of persistence of feline calicivirus. Res Vet Scimay prove useful in future investigations relationship. Shedding of the viruses in 1989: 47: 367±373.into the role of feline herpesvirus 1 in the these cats may be in¯uenced by corticos- 5. Diehl K, Rosychuk RA. Feline gingivitis-development of oral in¯ammatory dis- teroid administration or the stress of stomatitis-pharyngitis. Vet Clin North Ameases. chronic disease. An underlying immune Small Anim Pract 1993: 23: 139±153. While the role of herpesvirus in feline defect, the potential cause of the oral in- 6. Dilley DC, Siegel MA, Budnick S. Diagno- sing and treating common oral pathologies.chronic oral in¯ammation has not been ¯ammation, might also result in coincident Pediatr Clin North Am 1991: 38: 1227±investigated, herpetic gingivostomatitis is viral shedding. 1264.well recognized in humans. Exposure to An immune basis for feline gingivitis- 7. Eversole LR. Immunopathogenesis of oralherpes simplex I is widespread among stomatitis complex is supported by the lichen planus and recurrent aphthous sto-humans, but only 1% of those infected hyperglobulinemia commonly identi®ed matitis. Semin Cutan Med Surg 1997: 16:will develop primary herpetic gingivosto- in affected cats (12), and increased levels 284±294. 8. Geissler K, Schneider K, Platzer G, Truyenmatitis (6). The disease is characterized of messenger RNA for interleukins (in- B, Kaaden OR, Truyen U. Genetic andby swollen gingiva and vesicles or ulcers cluding IL-2, IL-4, IL-5, IL-6, IL-10 and antigenic heterogeneity among feline cali-on the oral mucosa, lips, and facial skin IL-12) and interferon-g detected in cats civirus isolates from distinct disease mani-(17). with stomatitis compared with normal cats festations. Virus Res 1997: 48: 193±206. Herpesviruses have recently been impli- (10). 9. Hargis AM, Ginn PE. Feline herpesvirus 1- associated facial and nasal dermatitis andcated as an underlying cause for period- It has been postulated that plasma cell stomatitis in domestic cats. Vet Clin Northontitis in humans (2, 29). Herpesvirus gingivitis and mucositis in humans may Am Small Anim Pract 1999: 29: 1281±infections generally involve a mild or represent a hypersensitivity reaction (30), a 1290.asymptomatic primary phase followed by failure to regulate the immune response. 10. Harley R, Helps CR, Harbour DA, Gruf-an asymptomatic latent phase interrupted Like feline LPGS, recurrent aphthous sto- fydd-Jones TJ, Day MJ. Cytokine mRNA expression in lesions in cats with chronicsporadically by periods of exacerbation, matitis and oral lichen planus in humans gingivostomatitis. Clin Diagn Lab Immunolwhere virus shedding may occur. In peri- are characterized by increased lymphocyte 1999: 6: 471±478.odontal disease, herpesviruses may cause in®ltration into oral mucosa (7, 24). This 11. Holmstrom SE, Frost P, Eisner ER. Veteri-release of tissue-destructive cytokines, occurs through the interaction of several nary dental techniques ± for the small ani-overgrowth of pathogenic periodontal bac- cell-surface adhesion molecules, whose mal practitioner, 2nd edn. Philadelphia: W.teria, and initiation of cytotoxic or immu- expression on endothelial cells may be B. Saunders, 1998. 12. Johnessee JS, Hurvitz AI. Feline plasma cellnopathogenic events (29). It is therefore induced by pro-in¯ammatory mediators gingivitis-pharyngitis. J Am Anim Hospimportant to study the concomitant occur- such as lipopolysaccharide, tumor necrosis Assoc 1983: 19: 179±181.rence of viruses in a disease process like factor, and IL-1 (18). These adhesion mo- 13. Knowles JO, Dawson S, Gaskell RM, Gas-chronic stomatitis. lecules bind to activated lymphocytes, kell CJ, Harvey CE. Neutralisation patterns In spite of widespread immunization of resulting in adherence of lymphocytes to among recent British and North American feline calicivirus isolates from different cli-domestic cats against feline herpesvirus 1, vascular walls. Transendothelial migra- nical origins. Vet Rec 1990: 127: 125±127.feline viral rhinotracheitis and herpetic tion of the lymphocytes follows, leading 14. Knowles JO, Gaskell RM, Gaskell CJ,ocular disease remain problematic, parti- to lymphocytic in®ltration of adjacent Harvey CE, Lutz H. Prevalence of felinecularly in multiple cat households and tissues. calicivirus, feline leukaemia virus andcatteries. Feline LPGS is also reported to In summary, in®ltration of lymphocytes antibodies to FIV in cats with chronic stomatitis. Vet Rec 1989: 124: 336±338.be more prevalent in cattery situations, is a common feature of human oral in¯am- 15. Kreutz LC, Johnson RP, Seal BS. Phenoty-which may lead to the impression that matory conditions and feline gingivosto- pic and genotypic variation of feline cali-purebred cats are predisposed (5). This matitis. In the feline oral cavity, infection civirus during persistent infection of cats.study did not ®nd evidence to support such with feline herpesvirus and calicivirus, Vet Microbiol 1998: 59: 229±236.an impression; however, large-scale inves- combined with bacterial plaque, may act 16. Lauritzen A, Jarrett O, Sabara M. 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