Skip to main content
Elsevier - PMC COVID-19 Collection logoLink to Elsevier - PMC COVID-19 Collection
. 2015 Jan 20;16(6):1075–1095. doi: 10.1016/S0195-5616(86)50130-3

Persistent Viral Infection

The Carrier State

R Charles Povey *,**
PMCID: PMC7134487  PMID: 3097907

Abstract

A persistent viral infection is one in which the virus in a replicating or non-replicating form persists in the host beyond the normal recovery and elimination period for that particular viral infection. The clinical significance and mechanisms of persistence, when known, are discussed for the important viral infections of dogs and cats. Particular emphasis is given to feline viral rhinotracheitis, feline calicivirus, canine distemper, and feline leukemia.

Reference

  • 1.Anderson L.J., Kibler R.F., Kaslow R.A. Multiple sclerosis unrelated to dog exposure. Neurology. 1984;34:1149–1154. doi: 10.1212/wnl.34.9.1149. [DOI] [PubMed] [Google Scholar]
  • 2.Appel M.J.G. Pathogenesis of canine distemper. Am. J. Vet. Res. 1969;30:1167–1182. [PubMed] [Google Scholar]
  • 3.Appel M., Pickerill P.H., Menegus M. Current status of canine respiratory disease. Proceedings of the 20th Gaines Symposium; 1970. pp. 15–23. [Google Scholar]
  • 4.Appel M.J.G., Shek W.R., Shesberadaran H. Measles virus and inactivated canine distemper virus induce incomplete immunity to canine distemper. Arch. Virol. 1984;82:73–82. doi: 10.1007/BF01309369. [DOI] [PubMed] [Google Scholar]
  • 5.Baringer J.R., Swoveland P. Recovery of herpes-simplex virus from human trigeminal ganglions. N. Engl. J. Med. 1973;288:648–650. doi: 10.1056/NEJM197303292881303. [DOI] [PubMed] [Google Scholar]
  • 6.Bastian F.O., Rabson A.S., Lee C.L. Herpesvirus hominis: Isolation from human trigeminal ganglion. Science. 1972;178:306–307. doi: 10.1126/science.178.4058.306. [DOI] [PubMed] [Google Scholar]
  • 7.Carmichael L.E. Canine herpesvirus infection in puppies. In: Kirk R.W., editor. Current Veterinary Therapy V. W. B. Saunders Co; Philadelphia: 1977. pp. 1296–1297. [Google Scholar]
  • 8.Carmichael L.E., Binn L.N. New enteric viruses in the dog. Adv. Vet. Sci. Comp. Med. 1981;25:1–37. [PubMed] [Google Scholar]
  • 9.Crandell R.A., Rehkemper J.A., Niemann W.H. Experimental feline viral rhinotracheitis. J. Am. Vet. Med. Assoc. 1961;138:191–196. [PubMed] [Google Scholar]
  • 10.Csiza C.K., Scott F.W. deLahunta, A., et al.: Immune carrier state of feline panleu-kopenia virus-infected cats. Am. J. Vet. Res. 1971;32:419–426. [PubMed] [Google Scholar]
  • 11.Ellis T.M. Feline viral rhinotracheitis virus: Explant and cocultivation studies on tissues collected from persistently infected cats. Res. Vet. Sci. 1982;33:270–274. [PubMed] [Google Scholar]
  • 12.Ellis T.M., Mackenzie J.S., Wilcox G.E. Isolation of feline syncytia-forming virus from oropharyngeal swabs of cats. Aust. Vet. J. 1979;55:202–203. doi: 10.1111/j.1751-0813.1979.tb15288.x. [DOI] [PubMed] [Google Scholar]
  • 13.Engels M., Mayr-Bibrack B., Ruckstuhl B. Seroepizootiology of canine herpes-virus infections in Switzerland and preliminary studies with a vaccine. Zentralb. Veter-inarmed. B. 1980;27:257–267. [PubMed] [Google Scholar]
  • 14.Essex M., Sliski A., Cotter S.M. Immunosurveillance of naturally occurring feline leukemia. Science. 1975;190:790–792. doi: 10.1126/science.173019. [DOI] [PubMed] [Google Scholar]
  • 15.Evermann J.F., Lincoln J.D., McKiernan A.J. Isolation of a paramyxovirus from the cerebrospinal fluid of a dog with posterior paresis. J. Am. Vet. Med. Assoc. 1980;177:1132–1134. [PubMed] [Google Scholar]
  • 16.Fabricant C.G., King J.M., Gaskin J.M. Isolation of a virus from a female cat with urolithiasis. J. Am. Vet. Med. Assoc. 1971;158:200. [PubMed] [Google Scholar]
  • 17.Fekadu M., Shaddock J.H., Baer G.M. Excretion of rabies virus in the saliva of dogs. J. Infect. Dis. 1982;145:715–719. doi: 10.1093/infdis/145.2.715. [DOI] [PubMed] [Google Scholar]
  • 18.Francis D.P., Essex M., Cotter S. Feline leukemia virus infections: The significance of chronic viremia. Leukemia Res. 1979;3:435–441. doi: 10.1016/0145-2126(79)90040-7. [DOI] [PubMed] [Google Scholar]
  • 19.Friedman R.M., Ramseur J.M. Mechanisms of persistent infections by cytopathic viruses in tissue culture. Arch. Virol. 1979;60:83–103. doi: 10.1007/BF01348025. [DOI] [PubMed] [Google Scholar]
  • 20.Galloway D.A., Fenoglio C.M., McDougall J.K. Limited transcription of herpes simplex virus genome when latent in human sensory ganglia. J. Virol. 1982;41:686–691. doi: 10.1128/jvi.41.2.686-691.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Gaskell R.M., Povey R.C. Re-excretion of feline viral rhinotracheitis virus following corticosteroid treatment. Vet. Rec. 1973;93:204–205. doi: 10.1136/vr.93.7.204. [DOI] [PubMed] [Google Scholar]
  • 22.Gaskell R.M., Povey R.C. Experimental induction of feline viral rhinotracheitis virus re-excretion in FVR-recovered cats. Vet. Rec. 1977;100:128–133. doi: 10.1136/vr.100.7.128. [DOI] [PubMed] [Google Scholar]
  • 23.Gaskell R.M., Povey R.C. The dose response of cats to experimental infection with feline viral rhinotracheitis virus. J. Comp. Pathol. 1979;89:179–191. doi: 10.1016/0021-9975(79)90057-4. [DOI] [PubMed] [Google Scholar]
  • 24.Goodpasture E.W. Herpetic infection, with special reference to involvement of the nervous system. Medicine. 1929;8:223–243. doi: 10.1097/00005792-199303000-00006. [DOI] [PubMed] [Google Scholar]
  • 25.Haase A.T., Ventura P., Gibbs C.J. Measles virus nucleotide sequences: detection by hybridization in situ. Science. 1981;212:672–675. doi: 10.1126/science.7221554. [DOI] [PubMed] [Google Scholar]
  • 26.Hackett A.J., Manning J.S. Comments on feline syncytia-forming virus. J. Am. Vet. Med. Assoc. 1971;158:948–954. [PubMed] [Google Scholar]
  • 27.Hardy W.D., Jr., Hirshaut Y., Hess P.W. Detection of the feline leukemia virus and other mammalian oncornaviruses by immunofluorescence. Bibl. Haematologica. 1973;39:778–799. doi: 10.1159/000427906. [DOI] [PubMed] [Google Scholar]
  • 28.Hardy W.D., Jr., Hess P.W., MacEwan E.G. Biology of feline leukemia virus in the natural environment. Cancer Res. 1976;36:582–588. [PubMed] [Google Scholar]
  • 29.Hardy W.D., Jr., McClelland A.J., Zuckerman E. Prevention of the contagious spread of feline leukemia virus and the development of leukemia in pet cats. Nature (Lond.) 1976;263:326–328. doi: 10.1038/263326a0. [DOI] [PubMed] [Google Scholar]
  • 30.Hardy W.D., Jr., McClelland A.J., Zuckerman E. Development of virus non-producer lymphosarcomas in pet cats exposed to FeLV. Nature (Lond.) 1980;288:90–92. doi: 10.1038/288090a0. [DOI] [PubMed] [Google Scholar]
  • 31.Hashimoto A., Hirai L., Fukushi H. The vaginal lesions of a bitch with a history of canine herpesvirus infection. Jpn. J. Vet. Sci. 1983;45:123–126. doi: 10.1292/jvms1939.45.123. [DOI] [PubMed] [Google Scholar]
  • 32.Hoover E.A., Olsen R.G., Hardy W.D., Jr. Feline leukemia virus infection: Age-related variation in response of cats to experimental infection. J. Natl. Cancer Inst. 1976;57:365–369. doi: 10.1093/jnci/57.2.365. [DOI] [PubMed] [Google Scholar]
  • 33.Hoover E.A., Olsen R.G., Mathes L.E. Relationship between feline leukemia virus antigen expression in blood and bone marrow and viral infectivity in blood, bone marrow and saliva of cats. Cancer Res. 1977;37:3707–3710. [PubMed] [Google Scholar]
  • 34.Horta-Barbosa L., Fuccillo D.A., Sewer J.L. Subacute sclerosing panencephalitis: Isolation of measles virus from a brain biopsy. Nature (Lond.) 1969;221:974–981. doi: 10.1038/221974a0. [DOI] [PubMed] [Google Scholar]
  • 35.Imagawa D.T., Howard E.B., Van Pelt L.F. Isolation of canine distemper virus from dogs with chronic neurological diseases. Proc. Soc. Exp. Biol. Med. 1980;164:355–362. doi: 10.3181/00379727-164-40877. [DOI] [PubMed] [Google Scholar]
  • 36.Johnson R.H., Thomas R.G. Feline viral rhinotracheitis in Britain. Vet. Rec. 1966;79:188–191. [Google Scholar]
  • 37.Johnson R.P., Povey R. C: Feline calicivirus infection in kittens borne by cats persistently infected with the virus. Res. Vet. Sci. 1984;37:114–119. [PubMed] [Google Scholar]
  • 38.Jones F.R., Yoshida L.H., Ladiges W.C. Treatment of feline leukemia and reversal of FeLV by ex vivo removal of IgG: A preliminary report. Cancer. 1980;46:675–684. doi: 10.1002/1097-0142(19800815)46:4<675::aid-cncr2820460408>3.0.co;2-x. [DOI] [PubMed] [Google Scholar]
  • 39.Jordan M.C., Mar V.L. Spontaneous activation of latent cytomegalovirus from murine spleen explants. Role of lymphocytes and macrophages in release and replication of virus. J. Clin. Invest. 1982;70:762–768. doi: 10.1172/JCI110672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Keenan K.P., Jervis H.R., Marchwicki R.H. Intestinal infection of neonatal dogs with canine coronavirus 1–71: Studies by virologic, histologic, histochemical and immunofluorescent techniques. Am. J. Vet. Res. 1976;37:247–256. [PubMed] [Google Scholar]
  • 41.Kobilinsky L., Hardy W.D., Jr., Ellis R. Activation of feline complement by feline leukemia virus. Fed. Proc. 1979;38:1089–1096. doi: 10.1128/iai.29.1.165-170.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Laliberte L. 1982. The epidemiology of coronavirus infections in cats with special reference to feline infectious peritonitis. M.Sc Thesis, University of Guelph. [Google Scholar]
  • 43.Lincoln S.D., Gorham J.R., Ott R.L. Etiologic studies of old dog encephalitis. 1. Demonstration of canine distemper viral antigen in the brain in two cases. Vet. Pathol. 1971;8:1–8. doi: 10.1177/030098587100800101. [DOI] [PubMed] [Google Scholar]
  • Low R.J., Colby E.D., Covington H.J. Report on the isolation of an agent from cell cultures of kidneys from domestic cats. Vet. Rec. 1971;88:557–559. doi: 10.1136/vr.88.21.557. [DOI] [PubMed] [Google Scholar]
  • 44.Lundgren D.L., Clapper W.E. Neutralization of canine herpesvirus by dog and human serums: A survey. Am. J. Vet. Res. 1969;30:479–482. [PubMed] [Google Scholar]
  • 45.Lutz H., Pedersen N., Higgins J. Humoral immune reactivity to feline leukemia virus and associated antigens in cats naturally infected with feline leukemia virus. Cancer Res. 1980;40:3642–3651. [PubMed] [Google Scholar]
  • 46.Madewell B.L., Jarrett O. Recovery of feline leukaemia virus from non-viraemic cats. Vet. Rec. 1983;112:339–342. doi: 10.1136/vr.112.15.339. [DOI] [PubMed] [Google Scholar]
  • 47.Mathes L.E., Olsen R.G. Feline Leukemia. CRC Press; Boca Raton: 1981. Immunobiology of feline leukemia virus disease; pp. 77–88. [Google Scholar]
  • 48.Morgan C.M., Rapp F. Measles virus and its associated diseases. Bact. Rev. 1977;41:636–666. doi: 10.1128/br.41.3.636-666.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Payne F.E., Baublis J.V., Itabashi H.H. Isolation of measles virus from cell cultures of brain from a patient with subacute sclerosing panencephalitis. N. Engl. J. Med. 1969;281:585–589. doi: 10.1056/NEJM196909112811103. [DOI] [PubMed] [Google Scholar]
  • 50.Pedersen N.C. Feline infectious peritonitis and feline enteric coronavirus infections. Part 1. Feline enteric coronaviruses. Feline Pract. 1983;13(4):13–19. [Google Scholar]
  • 51.Pedersen N.C., Boyle J.F., Floyd K. An enteric coronavirus of cats and its relation to feline infectious peritonitis. Am. J. Vet. Res. 1981;42:368–377. [PubMed] [Google Scholar]
  • 52.Pedersen N.C., Pool R.R., O’Brien T. Feline chronic progressive polyarthritis. Am. J. Vet. Res. 1980;41:522–535. [PubMed] [Google Scholar]
  • 53.Plummer G. Isolation of herpesviruses from trigeminal ganglia of man, monkeys and cats. J. Infect. Dis. 1973;128:345–348. doi: 10.1093/infdis/128.3.345. [DOI] [PubMed] [Google Scholar]
  • 54.Plummer G., Hollingsworth D.C., Phuangsab A. Chronic infections by herpes simplex viruses and by the horse and cat herpesviruses. Infect. Immun. 1970;1:351–355. doi: 10.1128/iai.1.4.351-355.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Poppensiek G.C., Baker J.A. Persistence of virus in urine as a factor in spread of infectious hepatitis in dogs. Proc. Soc. Exp. Biol. Med. 1951;77:279–281. doi: 10.3181/00379727-77-18749. [DOI] [PubMed] [Google Scholar]
  • 56.Post J.E., Warren L. Reactivation of latent feline leukemia virus. Developments in Cancer Research (Feline Leukemia Virus) 1980;4:151–158. [Google Scholar]
  • 57.Poste G.H., King N. Isolation of a herpesvirus from the canine genital tract: Association with infertility, abortion and stillbirths. Vet. Res. 1971;88:229–233. doi: 10.1136/vr.88.9.229. [DOI] [PubMed] [Google Scholar]
  • 58.Povey R.C., Johnson R.H. Further observations on feline viral rhinotracheitis. Vet. Rec. 1967;81:686–689. [Google Scholar]
  • 59.Povey R.C., Johnson R.H. Observations on the epidemiology and control of feline viral respiratory disease. J. Small Anim. Pract. 1970;11:485–494. doi: 10.1111/j.1748-5827.1970.tb05599.x. [DOI] [PubMed] [Google Scholar]
  • 60.Povey R.C., Wardley R.C., Jessen H. Feline picornavirus infection. The in vivo carrier state. Vet Rec. 1973;92:224–229. doi: 10.1136/vr.92.9.224. [DOI] [PubMed] [Google Scholar]
  • 61.Puga A., Rosenthal J.D., Openshaw H. Herpes simplex virus DNA and mRNA sequences in acutely and chronically infected trigeminal ganglia of mice. Virology. 1978;89:102–111. doi: 10.1016/0042-6822(78)90044-2. [DOI] [PubMed] [Google Scholar]
  • 62.Riggs J.L., Oshiro L.S., Taylor D.O.N. Syncytium-forming agent isolated from domestic cats. Nature (Lond.) 1969;222:1190–1191. doi: 10.1038/2221190a0. [DOI] [PubMed] [Google Scholar]
  • 63.Rojko J.L., Hoover E.A., Finn B.L. Determinants of susceptibility and resistance to feline leukemia virus infection. II. Susceptibility of feline lymphocytes to productive feline leukemia infection. J. Natl. Cancer Inst. 1981;67:899–910. [PubMed] [Google Scholar]
  • 64.Rojko J.L., Hoover E.A., Quackenbush S.L. Reactivation of latent feline leukaemia virus infection. Nature (Lond.) 1982;298:385–388. doi: 10.1038/298385a0. [DOI] [PubMed] [Google Scholar]
  • 65.Rojko J.L., Olsen R.G. The immunobiology of the feline leukemia virus. Vet. Immunol. Immunopathol. 1984;6:107–165. doi: 10.1016/0165-2427(84)90050-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 66.Saxinger C., Essex M., Hardy W.D. Detection of antigen related to feline leukemia virus in the sera of “virus-negative” cats. Developments in Cancer Research (Feline Leukemia Virus) 1980;4:489–496. [Google Scholar]
  • 67.Scriba M. Persistence of herpes simplex virus infection in ganglia and peripheral tissues of guinea pigs. Med. Microbiol. Immunol. 1981;169:91–96. doi: 10.1007/BF02171776. [DOI] [PubMed] [Google Scholar]
  • 68.Shapshak P., Graves M.C., Imagawa D.T. Polypeptides of canine distemper virus strains derived from dogs with chronic neurological disease. Virology. 1982;122:158–170. doi: 10.1016/0042-6822(82)90385-3. [DOI] [PubMed] [Google Scholar]
  • 69.Shen D.T., Gorham J.R. Viruria in dogs infected with canine distemper. Vet. Med. Small Anim. Clin. 1981;76:1175–1177. [PubMed] [Google Scholar]
  • 70.Shroyer E.L., Shalaby M.R. Isolation of feline syncytia-forming virus from oropharyngeal swab samples and buffy coat cells. Am. J. Vet. Res. 1978;39:555–560. [PubMed] [Google Scholar]
  • 71.Snyder H.W., Jones F.R., Day N.K. Isolation and characterization of circulating feline leukemia virus-immune complexes from plasma of persistently-infected pet cats removed by ex vivo immunosorption. J. Immunol. 1982;124:2726–2730. [PubMed] [Google Scholar]
  • 72.Spertzel R.O., Huxsoll D.L., McConnell S.J. Recovery and characterization of a herpes-like virus from dog kidney cell cultures. Proc Soc. Exp. Biol. Med. 1965;120:651–655. doi: 10.3181/00379727-120-30615. [DOI] [PubMed] [Google Scholar]
  • 73.Stevens J.G., Cook M.L. Latent herpes simplex virus in spinal ganglia of mice. Science. 1971;173:843–845. doi: 10.1126/science.173.3999.843. [DOI] [PubMed] [Google Scholar]
  • 74.Stewart S.E., David-Ferreira J., Lovelace E. Herpes-like virus isolated from neonatal and fetal dogs. Science. 1965;148:1341–1343. doi: 10.1126/science.148.3675.1341. [DOI] [PubMed] [Google Scholar]
  • 75.Stoddart C.A., Barlough J.E., Scott F.W. Experimental studies of a coronavirus and coronavirus-like agent in a barrier-maintained feline breeding colony. Arch. Virol. 1984;79:85–94. doi: 10.1007/BF01314306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Summers B.A., Greisen H.A., Appel M.J.G. Dog virus persist in the uvea in multiple sclerosis, as in canine distemper encephalomyelitis. Lancet (August 13. 1983:372–375. doi: 10.1016/s0140-6736(83)90346-x. [DOI] [PubMed] [Google Scholar]
  • 77.Summers B.A., Greisen H.A., Appel M.J.G. Canine distemper encephalomyelitis: Variation with virus strain. J. Comp. Pathol. 1984;94:65–75. doi: 10.1016/0021-9975(84)90009-4. [DOI] [PubMed] [Google Scholar]
  • 78.Tobler L.H., Imagawa D.T. Mechanism of persistence with canine distemper virus difference between a laboratory strain and an isolate from a dog with chronic neurological disease. Intervirology. 1984;21:77–86. doi: 10.1159/000149505. [DOI] [PubMed] [Google Scholar]
  • 79.Tsai S.C., Summers B.A., Appel M.J.G. Interferon in cerebrospinal fluid. A marker for viral persistence in canine distemper encephalitis. Arch. Virol. 1982;72:257–265. doi: 10.1007/BF01315222. [DOI] [PubMed] [Google Scholar]
  • 80.Van der Veen J., Lambriex M. Relationship of adenovirus to lymphocytes in naturally infected human tonsils and adenoids. Infect. Immun. 1973;7:604–609. doi: 10.1128/iai.7.4.604-609.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 81.Wardley R.C. Studies on feline caliciviruses with particular reference to persistent infections. University of Bristol; 1974. Ph.D. Thesis. [Google Scholar]
  • 82.Wardley R.C. Feline calicivirus carrier state. A study of the host/virus relationship. Arch. Virol. 1976;52:243–249. doi: 10.1007/BF01348021. [DOI] [PubMed] [Google Scholar]
  • 83.Wardley R.C., Povey R.C. The clinical disease and patterns of excretion associated with three different strains of feline caliciviruses. Res. Vet. Sci. 1977;23:7–14. [PubMed] [Google Scholar]
  • 84.Wardley R.C., Gaskell R.M., Povey R. C: Feline respiratory viruses: Their prevalence in clinically healthy cats. J. Small Anim. Pract. 1974;15:579–586. doi: 10.1111/j.1748-5827.1974.tb06538.x. [DOI] [PubMed] [Google Scholar]
  • 85.Wright N.G. Canine adenovirus: Its role in renal and ocular disease: A review. J. Small Anim. Pract. 1976;17:25–33. doi: 10.1111/j.1748-5827.1976.tb06543.x. [DOI] [PubMed] [Google Scholar]

Articles from The Veterinary Clinics of North America. Small Animal Practice are provided here courtesy of Elsevier

RESOURCES