Comp Immunol Microbiol Infect Dis. 1981; 4(2): 175–189.
Language: English | French
Antibody-mediated enhancement of disease in feline infectious peritonitis: Comparisons with dengue hemorrhagic fever☆
Rôle des anticorps dans l'aggravation de la péritonite infectieux feline (comparaisons avec une fiévre hémorragique, la dengue)
Department of Microbiology and the Cornell Feline Health Center, N.Y.S. College of Veterinary Medicine, Cornell University, Ithaca, NY 14853, U.S.A.
†Present address: Syntex Research, 2375 Charleston Rd., Mountain View, CA 94043, U.S.A.
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Abstract
Non-immune kittens passively immunized with feline serum containing high-titered antibodies reactive with feline infectious peritonitis virus (FIPV) developed a more rapid disease after FIPV challenge than did kittens pretreated with FIPV antibody-negative serum. Antibody-sensitized, FIPV challenged—kittens developed earlier clinical signs (including pyrexia, icterus, and thrombocytopenia) and died more rapidly than did non-sensitized, FIPV-challenged kittens. Mean survival time in sensitized kittens was significantly (P < 0.05) reduced compared to non-sensitized kittens (mean ± SEM, 10.0 ± 0.6 days vs. 28.8 ± 8.3 days, respectively). Lesions induced included fibrinous peritonitis, disseminated pyogranulomatous inflammation and necrotizing phlebitis and periphlebitis. FIPV antigen, immunoglobulin G, complement (C3) and fibrinogen were demonstrated in lesions by immunofluorescence microscopy.
The pathogenesis of dengue hemorrhagic fever (DHF) in persons bears striking resemblance to that of FIP in experimental kittens. In both FIP and DHF, non-neutralizing antibody may promote acute disease by enhancement of virus infection in mononuclear phagocytes or by formation of immune complexes, activation of complement and secondary vascular disturbances.
Keywords: (FIP), Feline infectious peritonitis; (DHF), dengue hemorrhagic fever; immunopathology; immunofluorescence; passive immunity
Résumé
Des chatons passivement immunisés par du sérum felin contenant un titre élevé en anticorps reagissant avec le virus de la péritonite infectieux feline ont développé une maladie plus rapide après injection virale (experimentale) que ceux ayant reçu un sérum dépourvu de ces anticorps. Les chatons sensibiliés par les anticorps et infectés par la virus (PIF) développent les symptômes plus rapidement (notamment de la fièvre, ictère et une thrombocytopenie) et meurent plus vite que les non-sensibilisés. La duré de survie moyenne chez les chatons sensilisés est reduite significativement (P < 0.05) par rapport à celle des non sensibilisés (mean ± SEM, 10.0 ± 0.6 jours vs. 28.8 ± jours respectivement). Les lesions observées comprennent une péritonite fibrineuse, une inflammation pyogranulomateuse dissenimée, et une phlebite et periphlebite nécrosante. L'antigène du FIPV, les immunologlobulines G, le fragment C3 du complément et le fibrinogène ont été revélés dans les lesions par immunofluorescence.
La pathogèneie de la fièvre hémorragique dengue (DHF) chez l'homme montre une ressemblance étonnante avec celles de la PIF experimentale chez les chatons. Dans les deux cas, les anticorps non neuralisants peuvent permettre une maladie plus forte par l'augmentation de l'infection par le virus des cellules phagocytaires, monouclées, par activation du complément et par des pertubations vasculaires secondaires.
Mots-clé: Péritonite infectieuse feline, la fièvre hémorragique dengue, immunopathologie, immunofluorescence, immunité passive
Footnotes
☆This study was performed in partial fulfillment by the senior author for a PhD thesis at Cornell University. Support for the study was obtained from private contributions to the Cornell Feline Health Center and a grant from Pitman-Moore, Inc., Washington Crossing, New Jersey.
References
1.
Horzinek M.C., Osterhaus A.D.M.E. Feline infectious peritonitis: a coronavirus disease of cats. J. Small Anim. Pract. 1978;19:623–630. [PubMed] [Google Scholar]2.
Horzinek M.C., Osterhaus A.D.M.E. The virology and pathogenesis of feline infectious peritonitis—brief review. Arch. Virol. 1979;59:1–15. [PMC free article] [PubMed] [Google Scholar]3.
Weiss R.C., Scott F.W. Feline Infectious Peritonitis. In: Kirk R.W., editor. Vol. 11. W.B. Saunders; Philadelphia: 1980. pp. 1288–1292. (Current Veterinary Therapy). [Google Scholar]4.
Weiss R.C. Feline infectious peritonitis—an update. Mod. Vet. Pract. 1978;59:832–836. [PubMed] [Google Scholar]5.
Pedersen N.C. Serologic studies of naturally occurring feline infectious peritonitis. Am. J. vet. Res. 1976;37:1449–1453. [PubMed] [Google Scholar]6.
Pedersen N.C. Feline infectious peritonitis. Proceedings, American Animal Hospital Association; South Bend, Ind.; 1978. pp. 142–146. [Google Scholar]7.
Wolfe L.G., Griesemer R.A. Feline infectious peritonitis. Vet. Path. 1966;3:225–270. [PubMed] [Google Scholar]8.
Montali R.J., Strandberg J.D. Extraperitoneal lesions in feline infectious peritonitis. Vet. Path. 1972;9:109–121. [PubMed] [Google Scholar]9.
Tuch K., Witte K.H., Wüller H. Festellung der felinen infektiosen peritonitis (FIP) bei hauskatzen und leoparden in deutschland. Zentbl. VetMed. B. 1974;21:426–441. [PubMed] [Google Scholar]10.
Hayashi T., Goto N., Takahashi R., Fujiwara K. Systemic vascular lesions in feline infectious peritonitis. Jap. J. Vet. Sci. 1977;39:365–377. [PubMed] [Google Scholar]11.
Hayashi T., Utsumi F., Takahashi R., Fujiwara K. Pathology of non-effusive type feline infectious peritonitis and experimental transmission. Jap. J. vet. Sci. 1980;42:197–210. [PubMed] [Google Scholar]12.
Weiss R.C., Dodds W.J., Scott F.W. Disseminated intravascular coagulation in experimentally induced feline infectious peritonitis. Am. J. vet. Res. 1980;40:663–671. [PubMed] [Google Scholar]13.
Pedersen N.C., Boyle J.F. Immunologic phenomena in the effusive form of feline infectious peritonitis. Am. J. vet. Res. 1980;41:868–876. [PubMed] [Google Scholar]14.
Weiss R.C., Scott F.W. Pathogenesis of feline infectious peritonitis: nature and development of viremia. Am. J. vet. Res. 1981;42:382–390. [PubMed] [Google Scholar]15.
Pedersen N.C. Feline infectious peritonitis: something old, something new. Fel. Pract. 1976;6:42–51. [Google Scholar]16.
Weiss R.C., Scott F.W. Laboratory diagnosis of feline infectious peritonitis. Fel. Pract. 1980;10:16–22. [Google Scholar]17.
Jacobse-Geels H.E.L., Daha M.R., Horzinek M.C. Isolation and characterization of feline C3 and evidence for the immune complex pathogenesis of feline infectious peritonitis. J. Immunol. 1980;125:1606–1610. [PubMed] [Google Scholar]18.
Halstead S.B., Nimmannitya S., Yamarat S., Russell P.K. Hemorrhagic fever in Thailand: recent knowledge regarding etiology. Jap. J. med. Sci. Biol. 1967;20:96–103. [PubMed] [Google Scholar]19.
Halstead S.B. Observations related to pathogenesis of dengue hemorrhagic fever. VI. hypothesis and discussion. Yale J. biol. Med. 1970;42:350–362. [PMC free article] [PubMed] [Google Scholar]20.
Russell P.K. Immunopathologic mechanisms in the dengue shock syndrome. In: Amos B., editor. Progress in Immunology I. Academic Press; New York: 1971. pp. 831–838. [Google Scholar]21.
Bokisch V.A., Top F.H., Russell P.K., Dixon F.J., Müller-Eberhard H.J. The potential pathogenic role of complement in dengue hemorrhagic shock syndrome. N. Engl. J. med. 1973;289:996–1000. [PubMed] [Google Scholar]22.
World Health Organization Pathogenetic mechanisms in dengue hemorrhagic fever: report of an international collaborative study. Bull. Wld. Hlth. Org. 1973;48:117–133. [PMC free article] [PubMed] [Google Scholar]23.
Halstead S.B., O'Rourke E.J. Dengue viruses and mononuclear phagocytes. II. Identity of blood and tissue leukocytes supporting in vitro infection. J. exp. Med. 1977;146:218–229. [PMC free article] [PubMed] [Google Scholar]24.
Scott R.M., Nisalak A., Cheamudon U., Seridhoranakul S., Nimmannitya S. Isolation of dengue viruses from peripheral blood leukocytes of patients with hemorrhagic fever. J. infect. Dis. 1980;141:1–6. [PubMed] [Google Scholar]25.
Theofilpoulos A.N., Wilson C.B., Dixon F.J. The raji cell radioimmune assay for detecting immune complexes in human sera. J. Clin. Invest. 1976;57:169–182. [PMC free article] [PubMed] [Google Scholar]26.
Rvangjirachuporn W., Boonpuvknavig S., Nimmannitya S. Circulating immune complexes in serum from patients with dengue hemorrhagic fever. Clin. exp. Immun. 1979;36:46–53. [PMC free article] [PubMed] [Google Scholar]27.
Russell P.K., Intavivat A., Kanchanapilant S. Antidengue immunoglobulins and serum β-1c globulin levels in dengue shock syndrome. J. Immunol. 1969;102:412–420. [PubMed] [Google Scholar]28.
Boonpucknavig S., Boonpucknavig V., Bhamarapravati N., Nimmannitya S. Immunofluorescence study of skin rash in patients with dengue hemorrhagic fever. Arch. Pathol. Lab. Med. 1979;103:463–466. [PubMed] [Google Scholar]29.
Srichaikul T., Nimmannitya S., Artchararit N., Siriasawakul T., Sungpeuk P. Fibrinogen metabolism and disseminated intravascular coagulation in dengue hemorrhagic fever. Am. J. trop. Med. Hyg. 1977;26:525–532. [PubMed] [Google Scholar]30.
Malloy H.T., Evelyn K.A. The determination of bilirubin with the photoelectric colorimeter. J. biol. Chem. 1937;118:481–490. [Google Scholar]31.
Osterhaus A.D.M.E., Horzinek M.C., Reynolds D.J. Seroepidemiology of feline infectious peritonitis virus infections using transmissible gastroenteritis virus as antigen. Zentbl. VetMed B. 1977;24:835–841. [PMC free article] [PubMed] [Google Scholar]32.
Kronvall G., Frommel D. Definition of staphylococcal protein A reactivity for human immunoglobulin G fragments. Immunochemistry. 1970;7:124–127. [PubMed] [Google Scholar]33.
Roitt I. Vol. 2. Blackwell Scientific; Oxford: 1974. pp. 129–158. (Essential Immunology). [Google Scholar]34.
Halstead S.B. In vivo enhancement of dengue virus infection in rhesus monkeys by passively transferred antibody. J. infect. Dis. 1979;140:527–533. [PubMed] [Google Scholar]35.
Halstead S.B., O'Rourke E.J. Antibody-enhanced dengue virus infection in primate leukocytes. Nature, Lond. 1977;265:739–741. [PubMed] [Google Scholar]37.
Halstead S.B., O'Rourke E.J. Dengue viruses and mononuclear phagocytes. I. Infection enhancement by non-neutralizing antibody. J. exp. Med. 1977;146:201–217. [PMC free article] [PubMed] [Google Scholar]38.
Weiss R.C., Scott F.W. Pathogenesis of feline infectious peritonitis: pathology and immunofluorescence. Am. J. vet. Res. 1981 in press. [PubMed] [Google Scholar]39.
Porter D.D., Larsen A.E. Aleutian Disease of Mink. In: Melnick J.L., Hatchin J., editors. Progress in Medical Virology (Slow Virus Disease) S. Karger; Basel: 1974. pp. 32–47. [PubMed] [Google Scholar]
