• 1.

    Rémond M, Sheldrick P, Lebreton F, et al. Gene organization in the UL region and inverted repeats of the canine herpesvirus genome. J Gen Virol 1996;77:3748.

    • Search Google Scholar
    • Export Citation
  • 2.

    Manning A, Buchan A, Skinner GR, et al. The immunological relationship between canine herpesvirus and four other herpesviruses. J Gen Virol 1988;69:16011608.

    • Search Google Scholar
    • Export Citation
  • 3.

    Tyack SG, Studdert MJ, Johnson MA. Nucleotide sequence of canine herpesvirus homologues of herpes simplex virus type 1 US2, US3, glycoproteins I and E, US8.5 and US9 genes. DNA Seq 1997;7:365368.

    • Search Google Scholar
    • Export Citation
  • 4.

    Carmichael LE, Squire RA, Krook L. Clinical and pathological features of a fatal viral disease of newborn pups. Am J Vet Res 1965;26:803814.

    • Search Google Scholar
    • Export Citation
  • 5.

    Hill H, Maré CJ. Genital disease in dogs caused by canine herpesvirus. Am J Vet Res 1974;35:669672.

  • 6.

    Karpas A, Garcia FG, Calvo F, et al. Experimental production of canine tracheobronchitis (kennel cough) with canine herpesvirus isolated from naturally infected dogs. Am J Vet Res 1968;29:12511257.

    • Search Google Scholar
    • Export Citation
  • 7.

    Burr PD, Campbell ME, Nicolson L, et al. Detection of canine herpesvirus 1 in a wide range of tissues using polymerase chain reaction. Vet Microbiol 1996;53:227237.

    • Search Google Scholar
    • Export Citation
  • 8.

    Miyoshi M, Ishii Y, Takiguchi M, et al. Detection of canine herpesvirus DNA in the ganglionic neurons and lymph node lymphocytes of latently infected dogs. J Vet Med Sci 1999;61:375379.

    • Search Google Scholar
    • Export Citation
  • 9.

    Poste G, King N. Isolation of a herpesvirus from the canine genital tract: association with infertility, abortion and stillbirths. Vet Rec 1971;88:229233.

    • Search Google Scholar
    • Export Citation
  • 10.

    Okuda Y, Hashimoto A, Yamaguchi T, et al. Repeated canine herpesvirus (CHV) reactivation in dogs by an immunosuppressive drug. Cornell Vet 1993;83:291302.

    • Search Google Scholar
    • Export Citation
  • 11.

    Ledbetter EC, Riis RC, Kern TJ, et al. Corneal ulceration associated with naturally occurring canine herpesvirus-1 infection in two adult dogs. J Am Vet Med Assoc 2006;229:376384.

    • Search Google Scholar
    • Export Citation
  • 12.

    Reading MJ, Field HJ. A serological study of canine herpesvirus-1 infection in the English dog population. Arch Virol 1998;143:14771488.

    • Search Google Scholar
    • Export Citation
  • 13.

    Carmichael LE. Herpesvirus canis: aspects of pathogenesis and immune response. J Am Vet Med Assoc 1970;156:17141721.

  • 14.

    Gallardo E. Primary herpes simplex keratitis: clinical and experimental study. Arch Ophthalmol 1943;30:217220.

  • 15.

    Jones BR, Al-Hussaini MK. Therapeutic considerations in ocular vaccinia. Trans Ophthalmol Soc U K 1963;83:613631.

  • 16.

    Pusterla N, Wilson WD, Conrad PA, et al. Cytokine gene signatures in neural tissue of horses with equine protozoal myeloencephalitis or equine herpes type 1 myeloencephalopathy. Vet Rec 2006;159:341346.

    • Search Google Scholar
    • Export Citation
  • 17.

    Lacheretz A, Cognard S. Epidemiology and serological diagnosis of canine herpesvirus infection [in French]. Rev Méd Vét 1998;149:853856.

    • Search Google Scholar
    • Export Citation
  • 18.

    Ronsse V, Verstegen J, Onclin K, et al. Risk factors and reproductive disorders associated with canine herpesvirus-1 (CHV-1). Theriogenology 2004;61:619636.

    • Search Google Scholar
    • Export Citation
  • 19.

    Remeijer L, Maertzodorf J, Buitenwerf J, et al. Corneal herpes simplex virus type 1 superinfection in patients with recrudescent herpetic keratitis. Invest Ophthalmol Vis Sci 2002;43:358363.

    • Search Google Scholar
    • Export Citation
  • 20.

    Darougar S, Wishart MS, Viswalingam ND. Epidemiology and clinical features of primary herpes simplex virus ocular infection. Br J Ophthalmol 1985;69:26.

    • Search Google Scholar
    • Export Citation
  • 21.

    Romanowski EG, Bartels SP, Gordon YJ. Comparative antiviral efficacies of cidofovir, trifluridine, and acyclovir in the HSV-1 rabbit keratitis model. Invest Ophthalmol Vis Sci 1999;40:378384.

    • Search Google Scholar
    • Export Citation
  • 22.

    Schang LM, Jones C. Analysis of bovine herpesvirus 1 transcripts during primary infection of trigeminal ganglia of cattle. J Virol 1997;71:67866795.

    • Search Google Scholar
    • Export Citation
  • 23.

    Nasisse MP, Guy JS, Davidson MG, et al. Experimental ocular herpesvirus infection in the cat. Sites of virus replication, clinical features and effects of corticosteroid administration. Invest Ophthalmol Vis Sci 1989;30:17581768.

    • Search Google Scholar
    • Export Citation
  • 24.

    Haid C, Kaps S, Gönczi E, et al. Pretreatment with feline interferon omega and the course of subsequent infection with feline herpesvirus in cats. Vet Ophthalmol 2007;10:278284.

    • Search Google Scholar
    • Export Citation
  • 25.

    Brandt CR. The role of viral and host genes in corneal infection with herpes simplex virus type 1. Exp Eye Res 2005;80:607621.

  • 26.

    Chodosh J, Banks MC, Stroop WC. Rose bengal inhibits herpes simplex virus replication in vero and human corneal epithelial cells in vitro. Invest Ophthalmol Vis Sci 1992;33:25202527.

    • Search Google Scholar
    • Export Citation
  • 27.

    Brooks SE, Kaza V, Nakamura T, et al. Photoinactivation of herpes simplex virus by rose bengal and fluorescein. In vitro and in vivo study. Cornea 1994;13:4350.

    • Search Google Scholar
    • Export Citation
  • 28.

    Regnier A, Toutain PL, Alvinerie M, et al. Adrenocortical function and plasma biochemical values in dogs after subconjunctival treatment with methylprednisolone acetate. Res Vet Sci 1982;32:306310.

    • Search Google Scholar
    • Export Citation
  • 29.

    Martin CL. Effect of topical vitamin A, antibiotic, mineral oil, and subconjunctival corticosteroid on corneal epithelial wound healing in the dog. J Am Vet Med Assoc 1971;159:13921399.

    • Search Google Scholar
    • Export Citation
  • 30.

    Zamansky GB, Lee BP, Chang RK, et al. Quantitation of herpes simplex virus in rabbit corneal epithelium. Invest Ophthalmol Vis Sci 1985;26:873876.

    • Search Google Scholar
    • Export Citation
  • 31.

    Cooper JA Jr, Daniels CA, Trofatter EF Jr. The effect of prednisolone on antibody-dependent cell-mediated cytotoxicity and the growth of type 1 herpes simplex virus in human cells. Invest Ophthalmol Vis Sci 1978;17:381385.

    • Search Google Scholar
    • Export Citation
  • 32.

    Stiles J, Pogranichniy R. Detection of virulent feline herpesvirus-1 in the corneas of clinically normal cats. J Feline Med Surg 2008;10:154159.

    • Search Google Scholar
    • Export Citation
  • 33.

    Kaufman HE, Varnell ED, Centifanto YM, et al. Effect of herpes simplex virus genome on the response of infection to corticosteroids. Am J Ophthalmol 1985;100:114118.

    • Search Google Scholar
    • Export Citation
  • 34.

    Remeijer L, Osterhaus A, Verjans G. Human herpes simplex virus keratitis: the pathogenesis revisited. Ocul Immunol Inflamm 2004;12:255285.

    • Search Google Scholar
    • Export Citation
  • 35.

    Wishart MS, Darougar S, Viswalingam ND. Recurrent herpes simplex virus ocular infection: epidemiological and clinical features. Br J Ophthalmol 1987;71:669672.

    • Search Google Scholar
    • Export Citation
  • 36.

    Wright NG, Cornwell HJC. The susceptibility of six-week old puppies to canine herpes virus. J Small Anim Pract 1970;10:669674.

  • 37.

    Tullo AB, Shimeld C, Blyth WA, et al. Spread of virus and distribution of latent infection following ocular herpes simplex in the non-immune and immune mouse. J Gen Virol 1982;63:95101.

    • Search Google Scholar
    • Export Citation
  • 38.

    Appel MJ, Menegus M, Parsonson IM, et al. Pathogenesis of canine herpesvirus in specific-pathogen-free dogs: 5- to 12-week old pups. Am J Vet Res 1969;30:20672073.

    • Search Google Scholar
    • Export Citation
  • 39.

    Reubel GH, Pekin J, Venables D, et al. Experimental infection of European red foxes (Vulpes vulpes) with canine herpesvirus. Vet Microbiol 2001;83:217233.

    • Search Google Scholar
    • Export Citation
  • 40.

    Mainka C, Fuss B, Geiger H, et al. Characterization of viremia at different stages of varicella-zoster virus infection. J Med Virol 1998;56:9198.

    • Search Google Scholar
    • Export Citation
  • 41.

    Naraqi S, Jackson GG, Jonasson OM. Viremia with herpes simplex type 1 in adults. Four nonfatal cases, one with features of chicken pox. Ann Intern Med 1976;85:165169.

    • Search Google Scholar
    • Export Citation
  • 42.

    Craig CP, Nahmias AJ. Different patterns of neurologic involvement with herpes simplex virus types 1 and 2: isolation of herpes simplex virus type 2 from buffy coat of two adults with meningitis. J Infect Dis 1973;127:365372.

    • Search Google Scholar
    • Export Citation
  • 43.

    Rinaldo CR Jr, Richter BS, Black PH, et al. Persistent infection of human lymphoid and myeloid cell lines with herpes simplex virus. Infect Immun 1979;25:521525.

    • Search Google Scholar
    • Export Citation
  • 44.

    Chesters PM, Allsop R, Purewal A, et al. Detection of latency-associated transcripts of equid herpesvirus 1 in equine leukocytes but not in trigeminal ganglia. J Virol 1997;71:34373443.

    • Search Google Scholar
    • Export Citation
  • 45.

    Mweene AS, Okazaki K, Kida H. Detection of viral genome in non-neural tissues of cattle experimentally infected with bovine herpesvirus 1. Jpn J Vet Res 1996;44:165174.

    • Search Google Scholar
    • Export Citation
  • 46.

    Westermeyer HD, Thomasy SM, Kado-Fong H, et al. Assessment of viremia associated with experimental primary feline herpesvirus infection or presumed hereptic recrudescence in cats. Am J Vet Res 2009;70:99104.

    • Search Google Scholar
    • Export Citation
  • 47.

    Falcon MG, Jones BR. Herpes simplex keratitis: animal models to guide the selection and optimal delivery of antiviral chemotherapy. J Antimicrob Chemother 1977;3 (suppl A):8389.

    • Search Google Scholar
    • Export Citation
  • 48.

    Kaye SB, Shimeld C, Grinfeld E, et al. Non-traumatic acquisition of herpes simplex virus infection through the eye. Br J Ophthalmol 1992;76:412418.

    • Search Google Scholar
    • Export Citation
  • 49.

    Richards CM, Shimeld C, Williams NA, et al. Induction of mucosal immunity against herpes simplex virus type 1 in the mouse protects against ocular infection and establishment of latency. J Infect Dis 1998;177:14511457.

    • Search Google Scholar
    • Export Citation
  • 50.

    Lund EM, Armstrong PJ, Kirk CA, et al. Health status and population characteristics of dogs and cats examined at private veterinary practices in the United States. J Am Vet Med Assoc 1999;214:13361341.

    • Search Google Scholar
    • Export Citation

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Experimental primary ocular canine herpesvirus-1 infection in adult dogs

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  • 1 Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.
  • | 2 Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.
  • | 3 Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.
  • | 4 Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California, Davis, CA 95616.
  • | 5 Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

Abstract

Objective—To characterize clinical ocular disease, viral shedding, and serologic response associated with primary canine herpesvirus-1 (CHV-1) ocular infection in naïve adult dogs.

Animals—12 specific pathogen-free adult Beagles.

Procedures—Dogs were topically inoculated in the right eye with CHV-1 (infection group; n = 8) or virus-free medium (control group; 4). Dogs were inoculated with or without corneal microtrephination and subconjunctivally administered corticosteroids. Conjunctiva, buffy coat, and serum samples for real-time PCR assay, virus isolation, and serum neutralization (SN) antibody titers were collected until postinfection day (PID) 224, and general physical and ophthalmologic examinations were performed.

Results—Dogs in the infection group developed bilateral, mild to moderate conjunctivitis that reached maximal intensity on PIDs 7 to 10. Ocular viral shedding was detected in all dogs in the infection group between PIDs 3 and 10. Infected dogs developed CHV-1 SN antibody titers, beginning at PID 7 and peaking on PID 21. All buffy coat PCR assay results were negative. Corneal microtrephination and subconjunctival corticosteroid administration did not significantly affect clinical disease or viral shedding. Following recovery from primary infection, dogs remained clinically normal, did not shed virus, and had slowly decreasing SN antibody titers. Dogs in the control group did not develop conjunctivitis, shed virus, or develop CHV-1 SN antibody titers.

Conclusions and Clinical Relevance—Primary ocular infection of adult dogs with CHV-1 was associated with self-limiting conjunctivitis and ocular viral shedding, which was evident in the absence of clinically detectable keratitis or systemic disease. Features of this infection resembled herpes simplex virus primary ocular infection in humans.

Contributor Notes

Address correspondence to Dr. Ledbetter.