Summary
An epizootic of feline infectious peritonitis in a captive cheetah population during 1982–1983 served to focus attention on the susceptibility of the cheetah (Acinoyx jubatus) to infectious disease. Subsequent observations based upon seroepidemiological surveys and electron microscopy of fecal material verified that cheetahs were indeed capable of being infected by coronaviruses, which were antigenically related to coronaviruses affecting domestic cats, i.e. feline infectious peritonitis virus/feline enteric coronavirus. Coincident with the apparent increased susceptibility of the cheetah to infectious diseases, were observations that the cheetah was genetically unusual insofar as large amounts of enzyme-encoding loci were monomorphic, and that unrelated cheetahs were capable of accepting allogenic skin grafts. These data provided the basis for a hypothesis that the cheetah, through intensive inbreeding, had become more susceptible to viral infections as a result of genetic homogeneity.
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References
August JR (1984) Feline infectious peritonitis. An immune-mediated coronaviral vasculitis. Vet Clin North Am Small Anim Pract 14(5): 971–984
Aynaud JM, Nguyen TD, Bottreau E, Brun A, Vannier P (1985) Transmissible gastroenteritis (TGE) of swine: survivor selection of TGE virus mutants in stomach juice of adult pigs. J Gen Virol 66: 1911–1917
Bang FB (1978) Genetics of resistance of animals to viruses. I. Introduction and studies in mice. Adv Virus Res 23: 269–348
Barlough JE, Stoddart CA (1988) Feline coronaviral infections. In: Greene CE (ed) Infectious diseases of the dog and cat, 2nd edn. Saunders, Philadelphia (in press)
Barthold SW (1987) Host age and genotypic effects on enterotropic mouse hepatitis virus infection. Lab Anim Sci 37: 36–40
Barthold SW, Smith AL (1987) Response of genetically susceptible and resistant mice to intranasal inoculation with mouse hepatitis virus JHM. Virus Res 7: 225–239
Bland van den Berg P, Botha WS (1977) Feline infectious peritonitis in South Africa. J S Afr Vet Assoc 48: 109–116
Boyle JF, Pedersen NC, Evermann JF, McKeirnan AJ, Ott RL, Black JW (1984) Plaque assay, polypeptide composition and immunochemistry of feline infectious peritonitis virus and feline enteric coronavirus isolates. In: Rottier PJM, van der Zeijst BAM, Spaan WJM, Horzinek MC (eds) Molecular biology and pathogenesis of coronaviruses. Plenum Press, New York, pp 133–147
Boyle JF, Weismiller DG, Holmes KV (1987) Genetic resistance to mouse hepatitis virus correlates with absence of virus-binding activity on target tissues. J Virol 61: 185–189
Briggs MB, Evermann JF, McKeirnan AJ (1986) Feline infectious peritonitis. An update of a captive cheetah population. Fel Pract 16: 13–16
Carman PS, Ernst PB, Rosenthal KL, Clark DA, Befus AD, Bienenstock J (1986) Intraepithelial leukocytes contain a unique subpopulation of NK-like cytotoxic cells active in the defense of gut epithelium to enteric murine coronavirus. J Immunol 163: 1548–1553
Caro TM, Hold ME, Fitzgibbon CD, Bush M, Hawkey CM, Kock RA (1987) Health of adult free-living cheetahs. J Zool (London) 212: 573–584
Chen K-S (1985) Enzymatic and acidic sensitivity profiles of selected virulent and attenuated transmissible gastroenteritis viruses of swine. Am J Vet Res 46: 632–636
Chen K-S, Kahn DE (1985) A double-protease-resistant variant of transmissible gastroenteritis virus and its ability to induce lactogenic immunity. Am J Vet Res 46: 1632–1636
Collins JK, Riegel CA, Olson JD, Fountain A (1987) Shedding of eneteric coronavirus in adult cattle. Am J Vet Res 48: 361–365
Crouch CF, Bielfeldt Ohmann H, Watts TC, Babiuk LA (1985) Chronic shedding of bovine enteric coronavirus antigen-antibody complexes by clinically normal cows. J Gen Virol 1489–1500
Daughaday CC, Brandt WE, McCown JM, Russell PK (1981) Evidence for two mechanisms of dengue virus infection of adherent human monocytes: trypsin-sensitive virus receptors and trypsin-resistant immune complex receptors. Infect Immun 32: 469–473
De Groot FJ, Maduro J, Lenstra JA, Horzinck MC, van der Zeijst BAM, Spaan WJ (1987) cDNA cloning and sequence analysis of the gene encoding the peplomer protein of feline infectious peritonitis virus. J Gen Virol 68: 2639–2646
De Groot RJ, Ter Haar RJ, Horzinek MC, van der Zeijst BAM (1987) Intracellular RNAs of the feline infectious peritonitis coronavirus strain 79–1146. J Gen Virol 68: 995–1002
Dindzans JV, Skamene E, Levy GA (1986) Susceptibility/resistance to mouse hepatitis virus strain 3 and macrophage procoagulant activity are genetically linked and controlled by two non-H-2-linked genes. J Immunol 137: 2355–2360
Dubois-Dalcq M, Holmes KV, Rentiar B (1984) Assembly ofCoronaviridae. In: Dubois-Dalcq M, Holmes KV, Rentiar B, Kingsbury DW (eds) Assembly of enveloped RNA viruses. Springer, Wien New York, pp 100–119
Dupuy JM, Levy-Leblond E, Le Prévost C (1975) Immunopathology of mouse hepatitis virus type 3 infection. II. Effect of immunosuppression in resistance mice. J Immunol 114: 226–230
Emancipator SN, Lamm ME (1986) Pathways of tissue injury initiated by humoral immune mechanisms. Lab Invest 54: 475–478
Esa AH, Reissig M (1985) Influences of nutrition on immunity and susceptibility to mouse hepatitis virus type 2. Immunology 55: 539–545
Evermann JF, Baumgartner L, Ott RL, Davis EV, McKeirnan AJ (1981) Characterization of a feline infectious peritonitis virus isolate. Vet Pathol 18: 256–265
Evermann JF, Burns G, Roelke ME, McKeirnan AJ, Greenlee A, Ward AC, Pfeifer M (1984) Diagnostic features of an epizootic of feline infectous peritonitis in captive cheetahs. Am Assoc Vet Lab Diag Proc 26: 365–382
Evermann JF, Heeney JL, McKeirnan AJ, O'Brien SJ (1988) Comparative features of a coronavirus isolated from a cheetah with feline infectious peritonitis. Virus Res, submitted for publication
Evermann JF, McKeirnan AJ, Eugster AK, Solozano RF, Collins JK, Black JW, Kim JS (1988) Update on canine coronavirus infections and interactions with other enteric pathogens of the dog. Comp Anim Pract 2: 15–23
Evermann JF, Roelke ME, Briggs MB (1986) Clinical and diagnostic features of feline coronavirus infections of cheetahs. Fel Pract 26: 21–30
Feldmann BM, Jortner BS (1964) Clinicopathologic conference [Feline systemic proliferative and exudative vasculitis]. J Am Vet Med Assoc 144: 1409–1420
Fiscus SA, Rivoire BL, Teramoto YA (1987) Epitope-specific antibody responses to virulent and avirulent feline infectious peritonitis virus isolates. J Clin Microbiol 25: 1529–1534
Fiscus SA, Teramoto YA (1987) Functional differences in the peplomer glycoproteins of feline coronavirus isolates. J Virol 61: 2655–2657
Fiscus SA, Teramoto YA, Mildbrand MM, Knisley CV, Winston SE, Pedersen NC (1985) Competitive enzyme immunoassay for the rapid detection of antibodies to feline infectious peritonitis virus polypeptides. J Clin Microbiol 22: 395–401
Gosselin SJ, Loudy DL, Tarr MJ, Balistreri WF, Setchell KDR, Johnston JO, Kramer LW, Dresser BL (1988) Veno-occlusive disease of the liver in captive cheetah. Vet Pathol 25: 48–57
Gould EA, Buckley A, Groeger BK, Cane PA, Doenhoff M (1987) Immune enhancement of yellow fever virus neurovirulence for mice: studies of mechanisms involved. J Gen Virol 68: 3105–3112
Haelterman EO (1972) On the pathogenesis of transmissible gastroenteritis of swine. J Am Vet Med Assoc 160: 534–540
Haywood AM (1986) Patterns of persistent viral infections. N Engl J Med 315: 939–948
Heeney JL, Evermann JF, McKeirnan AJ, O'Brien SJ (1988) Prevalence and implications of coronavirus infections in captive and free-ranging cheetah populations. J Virol, submitted for publication
Holmes KV, Boyle JF, Williams RK, Stephensen CB, Robbins SG, Bauer EC, Duchala CS, Frana MF, Weismiller D, Compton S, McGowan J, Sturman LS (1987) Processing of coronavirus proteins and assembly of virions. In: Briton, MA, Rueckert RR (eds) Positive strand RNA viruses. Alan Liss, New York, pp 339–349
Holzworth JK (1963) Some important disorders of cats. Cornell Vet 53: 157–160
Horzinek MC, Ederveen J, Egberink H, Jacobse-Geels HEL, Niewold T, Prins J (1986) Virion polypeptide specificity of immune complexes and antibodies in cats inoculated with feline infectious peritonitis virus. Am J Vet Res 47: 754–761
Horzinek M, Lulz H, Pedersen NC (1982) Antigenic relationships among homologous structural polypeptides of porcine, feline and canine coronaviruses. Infect Immun 37: 1148–1155
Horzinek MC, Osterhaus ADME (1979) Feline infectious peritonitis: a worldwide serosurvey. Am J Vet Res 40: 1487–1492
Horzinek MC, Osterhaus ADME (1979) The virology and pathogenesis of feline infectious peritonitis. Arch Virol 59: 1–15
Hoshino Y, Scott FW (1980) Coronavirus-like particles on the feces of normal cats. Arch Virol 63: 147–152
Jacobs L, de Groot R, van der Zeijst BAM, Horzinek MC, Spaan W (1987) The nucleotide sequence of the peplomer gene of porcine transmissible gastroenteritis virus (TGEV): comparison with the sequence of the peplomer protein of feline infectious peritonitis virus (FIPV). Virus Res 8: 363–371
Jacobse-Geels HEL, Daha MR, Horzinek MC (1982) Antibody, immune complexes and complement activity fluctuations in kittens with experimentally induced feline infectious peritonitis. Am J Vet Res 43: 666–670
Jacobse-Geels H, Horzinek MC (1983) Expression of feline infectious peritonitis coronavirus antigens on the surface of feline macrophage-like cells. J Gen Virol 64: 1985–1866
Jimenez G, Correa I, Melgosa MP, Bullida MJ, Enjvanes L (1986) Critical epitopes in transmissible gastroenteritis virus neutralization. J Virol 60: 131–139
Keenan KP, Jervis HR, Marchwicki RH, Binn LN (1976) Intestinal infection of neonatal dogs with canine coronavirus 1–71: studies by virologic, histologic, histochemical, and immunofluorescent techniques. Am J Vet Res 37: 247–256
Lai MMC, Baric RC, Makino S, Keck JG, Egbert J, Leibowitz JL, Stohlman SA (1985) Recombination between nonsegmented RNA genomes of murine coronaviruses. J Virol 56: 449–456
LePrévost C, Levy-Lebland E, Virelizier JL, Dupuy JM (1975) Immunopathology of mouse hepatitis virus type 3 infection. I. Role of humoral and cell-mediated immunity in resistance mechanisms. J Immunol 114: 221–225
LePrévost C, Virelizier JL, Dupuy JM (1975) Immunopathology of mouse hepatitis virus type 3 infection. III. Clinical and virologic observation of a persistent viral infection. J Immunol 115: 640–643
Makino S, Keck JG, Stohlman SA, Lai MMC (1986) High-frequency RNA recombination of murine coronaviruses. J Virol 57: 729–737
Makino S, Shieh C-K, Keck JG, Lai MMC (1988) Defective-interfering particles of murine coronavirus: mechanism of synthesis of defective viral RNAs. Virol 163: 104–111
Marker L, O'Brien SJ (1988) Captive breeding of the cheetah (Acinonyx jubatus) in North American zoos (1871–1986). Zoo Biol, in press
Martin ML (1985) Canine coronavirus enteritis and a recent outbreak following modified live virus vaccination. Compend Cont Educ Pract Vet 7: 1012–1017
McKeirnan AJ, Evermann JF, Davis EV, Ott RL (1987) Comparative properties of feline coronaviruses in vitro. Canad J Vet Res 51: 212–216
McKeirnan AJ, Evermann JF, Hargis A, Miller LM, Ott RL (1981) Isolation of feline coronaviruses from two cats with diverse disease manifestations. Fel Pract 11: 16–20
McNulty MS, Bryson DG, Allan GM, Logan EF (1984) Coronavirus infection of the bovine respiratory tract. Vet Microbiol 9: 425–434
Nguyen TD, Bottreau E, Bernard S, Lantier I, Aynaud JM (1986) Neutralizing secretory IgA and IgG do not inhibit attachment of transmissible gastroenteritis virus. J Gen Virol 67: 939–943
O'Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol, in press
O'Brien SJ, Roelke ME, Marker L, Newman A, Winkler CA, Meltzer D, Colly L, Evermann JF, Bush M, Wildt DE (1985) Genetic basis for species vulnerability in the cheetah. Science 227: 1428–1434
O'Brien SJ, Wildt DE, Goldman D, Merril CR, Bush M (1983) The cheetah is depauperate in genetic variation. Science 221: 459–462
Pang T (1983) Delayed-type hypersensitivity: probable role in the pathogenesis of dengue hemorrhagic fever/dengue shock syndrome. Rev Infect Dis 5: 346–352
Pedersen NC (1987) Coronavirus disease (coronavirus enteritis, feline infectious peritonitis). In: Holzworth J (ed) Diseases of the cat. WB Saunders, Philadelphia, pp 193–214
Pedersen NC, Boyle JF, Floyd K (1981) Infection studies in kittens using feline infectious peritonitis virus propagated in cell culture. Am J Vet Res 42: 363–367
Pedersen NC, Boyle JF, Floyd K, Fudge A, Barker J (1981) An enteric coronavirus infection of cats and relationship to feline infectious peritonitis. Am J Vet Res 42: 368–377
Pedersen NC, Evermann JF, McKeirnan AJ, Ott RL (1984) Pathogenicity studies of feline coronavirus isolates 79–1146 and 79–1683. Am J Vet Res 45: 2580–2585
Pedersen NC, Floyd K (1985) Experimental studies with three new strains of feline infectious peritonitis virus: FIPV-UCD 2, FIPV-UCD 3 and FIPV-UCD 4. Compend Cont Educ Pract Vet 7: 1001–1011
Pernikoff DS, Sundberg JP, Miller RE, Boever WJ, Scherba G (1986) Eosinophilic ulcers in association with herpetic dermatitis in sibling cheetahs. Proc Am Zool Assoc 1985, 145 (Abstr)
Pfeifer ML, Evermann JF, Roelke ME, Gallina AM, Ott RL, McKeirnan AJ (1983) Feline infectious peritonitis in a captive cheetah. J Am Vet Med Assoc 183: 1317–1319
Porterfield JS (1986) Antibody-dependent enhancement of viral infectivity. Adv Virus Res 31: 335–356
Quesenberry KE (1984) Infectious disease of nondomestic cats. Vet Clin North Am Small Anim Pract 14: 1089–1106
Saif LJ, Redman DR, Moorhead PD, Theil KW (1986) Experimentally induced coronavirus infections in calves: viral replication in the respiratory and intestinal tracts. Am J Vet Res 47: 1426–1432
Setchell KDR, Gosselin SJ, Welsh MB, Johnston JO, Balistreri WF, Kramer LW, Dresser BL, Tarr MJ (1987) Dietary estrogen—a probable cause of infertility and liver disease in captive cheetahs. Gastroenterology 93: 225–233
Shockley LJ, Kapke PA, Lapps W, Brian DA, Potgieter LND, Woods R (1987) Diagnosis of porcine and bovine enteric coronavirus infections using cloned cDNA probes. J Clin Microbiol 25: 1591–1596
Smith DB, Inglis SC (1987) The mutation rate and variability of eukaryotic viruses: an analytical review. J Gen Virol 68: 2729–2740
Sprino PJ, Ristic M (1982) Intestinal, pulmonary, and serum antibody responses of feeder pigs exposed to transmissible gastroenteritis virus by the oral and the oralintranasal routes of inoculation. Am J Vet Res 43: 255–261
Steinhauer DA, Holland JJ (1987) Rapid evolution of RNA viruses. Ann Rev Microbiol 41: 409–433
Stoddart CA, Barlough JE, Scott FW (1984) Experimental studies of a coronavirus and coronavirus-like agent in a barrier-maintained feine breeding colony. Arch Virol 79: 85–94
Sturman LS, Ricard CS, Holmes KV (1985) Proteolytic cleavage of the E 2 glycoprotein of murine coronavirus: activation of cell-fusing activity of virions by trypsin and separation of two different 90 K cleavage fragments. J Virol 56: 904–911
Takenouchi T, Ami Y, Hayashi T, Fujiwara K (1985) Role of T cells in feline infectious peritonitis virus infection of suckling mice. Jpn J Vet Sci 47: 465–468
Toth TE (1982) Trypsin-enhanced replication of neonatal calf diarrhea coronavirus in bovine embryonic lung cells. Am J Vet Res 43: 967–972
Tupper GT, Evermann JF, Russell RG, Thouless ME (1987) Antigenic and biological diversity of feline coronaviruses: feline infectious peritonitis and feline enteritis virus. Arch Virol 96: 29–38
Ward JM (1970) Morphogenesis of a virus in cats with experimental feline infectiuos peritonitis. Virology 41: 191–194
Weiss RC, Scott FW (1981) Antibody-mediated enhancement of disease in feline infectious peritonitis: comparisons with dengue hemorrhagic fever. Comp Immunol Microbiol Infect Dis 4: 175–189
Weiss RC, Scott FW (1981) Pathogenesis of feline infectious peritonitis: nature and development of viremia. Am J Vet Res 42: 382–390
Wellink J, van Kammen A (1988) Proteases involved in the processing of viral polyproteins. Arch Virol 98: 1–26
Whitaker-Dowling P, Youngner JS (1987) Viral interference-dominance of mutant viruses over wild-type viruses in mixed infections. Microbiol Rev 51: 179–191
Wolfe LG, Griesemer RA (1971) Feline infectious peritonitis: review of gross and histopathologic lesions. J Am Vet Med Assoc 158: 987–993
Woods RD, Cheville NF, Gallagher JE (1981) Lesions in the small intestine of newborn pigs inoculated with porcine, feline and canine coronaviruses. Am J Vet Res 42: 1163–1169
Worley M (1987) Feline coronavirus. In: Appel MJ (ed) Virus infections of carnivores. Elsevier, New York, pp 431–436
Yuhki N, O'Brien SJ (1988) Genetic variation of major histocompatibility complex class I genes in various species: the lack of polymorphism in the African cheetah. Immunogenetics, in preparation
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Evermann, J.F., Heeney, J.L., Roelke, M.E. et al. Biological and pathological consequences of feline infectious peritonitis virus infection in the cheetah. Archives of Virology 102, 155–171 (1988). https://doi.org/10.1007/BF01310822
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DOI: https://doi.org/10.1007/BF01310822