Group License: 1 User active

Vesicular stomatitis and other vesiculovirus infections

Vesicular stomatitis and other vesiculovirus infections

C J MARÉ AND D G MEAD

GENERAL INTRODUCTION: RHABDOVIRIDAE

Introduction

Vesicular stomatitis (VS) is a viral disease, most often affecting horses, cattle and pigs, characterized by fever, and by vesicular and erosive lesions on the tongue, gums, lips, teats, prepuce and the coronary bands of the feet.18, 19 Infection in dairy herds can result in substantial losses in milk production, and serious weight losses may occur in beef cattle and pigs. In horses, restriction of their use and movement frequently result in disruption of equestrian events. Of particular concern with VS in ruminants and pigs is its close clinical resemblance to foot-and-mouth disease (FMD), one of the world’s most feared livestock diseases. As a result, the diagnosis of VS often results in onerous and economically devastating quarantine measures. Subclinical infection with vesicular stomatitis virus (VSV) is common in livestock,36, 51 and probably in many wildlife species.

Human infection with VSV is frequently seen in persons in close contact with sick animals21, 54 and in laboratory workers.25 The disease in humans is a self-limiting illness characterized by influenza-like symptoms including fever, nausea, chills, vomiting, headaches and muscular pains. Vesicular lesions are rarely seen.39

The early history of VS has been exhaustively reviewed.18, 19 In summary, the first formal report of VSV in the USA was in 1916,47 but historical evidence suggests that VSV has been present in that country for well over 100 years.8, 20, 52

The descriptions of ‘sore tongue’ in cattle, horses, and pigs in the eastern USA in 1801/02, and in 1817 accurately fit modern descriptions of the disease. General G.B. McClellan is credited with the first report of what may have been VS during the Civil War in 1862.18 During that time, over 4 000 horses in the Union Army were incapacitated with what is now believed to have been VS.

Vesicular stomatitis is essentially a disease of the Americas. It has, in the past, been transported to France from the USA via military horses,24 but it did not become established there.

Several South African reports of stomatitis resembling VS4, 32, 49, 55 were not confirmed to be VS by virus isolation, nor were they obviously related to animal importation from the western hemisphere. If they were, in fact, VS, there is no indication that the disease became established in South Africa. There is currently no evidence of the existence of VS outside of the western hemisphere.

Aetiology

Vesicular stomatitis is caused by a group of antigenically related but distinct viruses belonging to the genus Vesiculovirus in the family Rhabdoviridae. 37 This very large family of viruses includes viruses of mammals, birds, fish, insects and plants. Several of the vertebrate and plant rhabdoviruses are transmitted by insects. Two serotypes of vesicular stomatitis virus, VSV-Indiana (VSV-I) and VSV-New Jersey (VSV-NJ), have been associated with vesicular disease among cattle, horses, pigs and humans. There are three serologically distinct types of VSV-I:15 the classical Indiana (type 1), Cocal (type 2), and Alagoas (type 3). Only a single type of VSV-NJ occurs. Vesicular stomatitis virus Indiana was first isolated from a cow in the state of Indiana in 1925,12 while VSV-NJ was isolated from cattle and horses in the state of New Jersey in 1926.13

By far the most frequent cause of VS in the USA has been VSV-NJ, whereas VSV-I, a common cause of VS in Central and South America, was not diagnosed in the USA from 1965 to 1997, when it suddenly reappeared in the southwestern USA. The VS viruses are also known to cause disease in Mexico, Colombia, Venezuela, Panama and Costa Rica.28, 43 The Cocal and Alagoas viruses have not been recognized in North America. Cocal virus was isolated in Trinidad and Brazil in 1964 from rodents, mosquitoes and mites,26, 27 and was first associated with VS in horses during an outbreak that affected horses on more than 50 premises in Argentina in 1963/64.15 Alagoas virus, isolated from mules in Brazil in 1964, has been associated with VS in horses, mules and cattle.15

Epidemiology

The host range of VSV is extremely broad, and the widespread presence of antibodies to the viruses in humans, livestock, pets, and many species of wildlife in endemic areas suggests that most vertebrates may be susceptible to VSV. However, no vertebrate reservoir of the viruses in nature has been identified. Vesicular stomatitis virus has also been shown to replicate in black flies (Simulium spp.),31, 33 sand flies (Lutzomyia spp.),10, 48 the mosquito Aedes aegypti,5 and the leafhopper Peregrinus maidis(Ashri.).29 Thus, it is a virus of both vertebrates and invertebrates.

The aetiological agents of VS, especially VSV-NJ and VSV-I, are among the most thoroughly researched of all animal viruses, and yet, paradoxically, the epidemiology of the disease itself remains an enigma, with major portions of the maintenance and transmission cycles of the viruses remaining unknown. It is clear that contact transmission of VS can occur, but recent evidence suggests that the disease is only mildly contagious. During the 1995 VS epidemics in the southwestern USA stringent quarantine measures were imposed in attempts to limit spread of the disease,7 yet the disease continued to move rapidly northwards apparently unimpeded by these restraints. Epidemiological studies during the 1995 epidemic revealed no correlation between animal movement and spread of the disease.7

The role of insects in the transmission of VS has remained controversial for decades, but recent evidence has led to increasing recognition of the importance of insects, not only as vectors, but as possible reservoirs of the virus. Characteristics of VS which support the contention that insects play a major role in its transmission include the seasonal nature of VS, with sudden appearance in early summer, and disappearance soon after the first killing frosts. The spread of VS along river valleys (as opposed to centrifugal spread) suggests the involvement of insects, as does the fact that the disease is most explosive in areas with irrigation canals and other moving water. The infection rate in stabled animals is much lower than in animals on pasture.53 Spread of the disease along river valleys (usually northward as the summer warmth moves northward) is often characterized by large ‘jumps’ in the absence of evidence of animal movement. This, too, suggests arthropod involvement, and raises the question of whether the disease is in fact moving northward, or whether it is emerging from a hidden reservoir in insects or vertebrate carriers as the weather warms. This strong circumstantial evidence supporting the role of insects in the ecology of VS has been buttressed during the past two decades by extensive experimental evidence that several species of biting flies may be involved in the epidemiology of VS. During epidemics the virus has been isolated from naturally infected black flies, sand flies, and Culicoides midges16, 51, 54 as well as from non-biting flies, including house flies.16

Extensive field studies on the ecology of VSV, combined with laboratory studies, have clearly demonstrated that sand flies are naturally infected with the virus and can transmit the virus to susceptible vertebrates, and that the virus can pass transovarially from generation to generation.9, 10, 48 Isolation of virus from naturally infected male flies (plant feeders, not blood feeders) is either proof that transovarial transmission takes place in nature or that the virus can be acquired from plants. Sentinel pigs, protected from contact with other vertebrates in a VS endemic area, nonetheless seroconverted to VSV, which strongly suggests that arthropods play a role in VSV transmission.44

While sand flies are proven biological vectors of VSV in the small endemic area of Ossabaw Island, Georgia,10 it is doubtful whether they are significant vectors in the rapid spread of VS experienced in major epidemics. Since sand flies have a very limited flight range and are not strong fliers, they are not good candidates for the role of epidemic vectors of VSV.43 The rapid spread of the disease, especially along watercourses, suggests that more aggressive and wideranging flies, such as black flies, which breed in running water, might be the principal vectors during epidemics. Recent laboratory findings in Arizona14, 31, 33 support the hypothesis that black flies can serve as epidemic vectors of VSV. Black flies were infected with VSV by feeding, and the virus replicated in them and was reisolated from the saliva of infected flies. In more recent studies, black flies infected per os with VSV-NJ transmitted it to laboratory mice.34 These experimental findings, together with the evidence that the sand fly is the vector in the natural cycle of VS in endemic areas where transovarial transmission of the virus in sand flies also occurs,9 suggests a central role for insects in the maintenance of this virus in nature.

Serological surveys for VSV-NJ and VSV-I antibodies in wild animals have revealed silent VS infection in 15 species of wild mammals in Mexico,3 in elk (Cervus elaphus nelsoni) in Colorado,53 in collared peccaries (Tayassu tajacu) in Arizona,11 in white-tailed deer (Odocoileus virginianus) in several USA states,28 and in pronghorn antelope (Antilocapra americana) in Wyoming.50 These antibodies were detected before, during, or after epidemics of VS occurring in livestock. While none of these animal species have been identi- fied as long-term reservoirs of the virus, they serve as useful indicators of VSV activity. In spite of numerous attempts to identify a natural reservoir of the virus, either in vertebrates or invertebrates, none has as yet been found. In the small VS endemic area of Ossabaw Island, Georgia, there is evidence that feral pigs may serve as VSV reservoirs,46 but the possibility that sand flies are the natural reservoir of the virus has not been excluded.

The epidemiology of VSV remains an enigma. It is clearly a virus of invertebrates and vertebrates. Is it possibly also a virus of plants; could they be serving as the silent repository for the virus between epidemics of VS? Much remains to be answered.

Pathogenesis

The virus probably enters the mammalian host via minor oral abrasions when contact transmission occurs, and via insect bites when mechanical or biological arthropod transmission occurs. Initial viral replication occurs in the lower layers of the epidermis, the resulting cellular damage is followed by intercellular oedema, and then by the formation of vesicles which rupture very easily. Subclinical infection is frequent, and there is experimental evidence23 that infection and subsequent excretion of the virus can occur with no detectable clinical signs. This observation is borne out by the widespread presence during epidemics of antibodies in domestic and wild animals showing no clinical signs. Virus excretion is via vesicular fluid, saliva, and nasal discharges.

The presence of IgM antibodies can be demonstrated within four to five days using the competitive ELISA test,2 and both complement fixing (CF) and neutralizing antibodies are detectable by 14 days post-infection.17 The IgM antibodies disappear within two months, the CF antibodies by six months, but the neutralizing antibodies persist for years.

Clinical signs

Vesicular stomatitis is clinically indistinguishable from footand-mouth disease (FMD) in ruminants and pigs.6 Since the latter disease does not affect horses, the appearance of clinical signs in horses during a vesicular disease outbreak in other livestock is a differential diagnostic feature.18

The clinical features of VS during natural outbreaks has been well described.1, 22, 35 After infection, a short incubation period (24 to 72 hours) is followed by a brief febrile period and the appearance of papules and vesicles on the tongue, lips and muzzle, and in the skin of the udder, interdigital spaces and, in some cases, coronary bands. In pigs, vesicles are commonly seen on the snout. The vesicular lesions progress by extension, and it is common for the entire epithelium of the tongue or teat to be sloughed. In some cases, the vesicles may be very transitory, and on first examination the lesions may appear as small erosions. As a result of the mouth lesions, salivation is a common sign in cattle and horses, and the foot lesions may result in lameness, especially in pigs and cattle. In severe cases the hoof may slough. Encephalitis has been described in horses suffering from VS.38 Common complications are secondary bacterial infections, myiasis, and mastitis. Case fatality is low. Since the mouth lesions may result in anorexia, rapid loss of condition and drop in milk production is often seen.

Pathology

The pathology of naturally occurring vesicular stomatitis in horses, cattle and pigs, the species most often clinically affected, has not been well documented since the disease is usually mild and seldom fatal. However, there are good de scriptions of the gross and microscopical lesions of the experimental disease.8, 23, 40, 42 The lesions observed in the above three animal species are very similar. The earliest gross lesions observed are papules and macules which develop within 24 hours, but they often go undetected. Within a day these early lesions are followed by the appearance of vesicles. The vesicles are very fragile and may rupture almost immediately leaving numerous erosions, or, if vesicles are contiguous, large raw areas may appear, especially on the tongue. The erosions are often the first lesions observed since the papules and vesicles are so transitory.

Microscopic lesions include epithelial cell necrosis, intercellular oedema of the Malpighian layer, occasional haemorrhages in the dermis, and perivascular leukocyte in- filtration. Vesicles do not consistently occur in experimental infections23, 42 in which necrosis may be the principal lesion. The characteristics of the lesions which develop after experimental infection varies with different strains of VSV.42

A diagnosis of VS is seldom made on the characteristics of the gross or microscopic pathology since the lesions are so similar to those of other vesicular diseases. Confirmatory serological and virological diagnoses are always required.

Diagnosis

Since VS is clinically indistinguishable from other vesicular diseases of livestock it is imperative that the diagnosis be confirmed by laboratory methods. In the early stages of the disease the virus is readily isolated from vesicle fluids or epithelium, saliva, and from nasal, pharyngeal or tonsillar swabs.23, 53 A wide variety of mammalian cell cultures are susceptible to the virus, but the most commonly used are Vero cells, in which cytopathic effects can be present within 24 to 48 hours. Confirmation of VSV is usually by serumvirus neutralization (SVN), ELISA, or immunofluorescence.7, 36 Demonstration of the presence of VSV by polymerase chain reaction41 is now a useful diagnostic tool, as is the demonstration of VS antigens by immunohistochemical techniques.45

The standard tests used for serological confirmation of the presence of VS antibodies, namely the CF and SVN tests, are being supplanted by the very sensitive, competitive ELISA test.2, 36 The IgG antibodies (detected by SVN or ELISA), which appear following infection, persist for years,17 but the IgM antibodies (detected by CF or ELISA), which appear very soon after infection, decline within two months. The presence of IgM antibodies is thus a useful indicator of recent VSV infection.

Differential diagnosis

In cattle and pigs, the most important disease resembling VS is FMD, and it is essential that the appropriate laboratory diagnostic tests, as described above, be quickly performed to exclude this possibility. Less likely to be confused with VS in cattle are mucosal disease, bovine virus diarrhoea, malignant catarrhal fever, bluetongue, epizootic haemorrhagic disease of deer, and mycotic stomatitis.

In pigs, VS is clinically indistinguishable from FMD, swine vesicular disease (SVD), and vesicular exanthema of swine (VES). Since horses are not susceptible to any of these, outbreaks of vesicular disease are most likely to be VS, except where horsepox causing contagious pustular stomatitis occurs. Laboratory confirmation in all cases of vesicular disease of livestock is essential.

Control

Since the epidemiology of VS is so poorly understood, it is difficult to recommend effective control methods. The clear evidence that stabling of animals, especially at night, results in a lower prevalence of the disease suggests that this is a useful control method, especially for horses. Insect control is advisable and apparently effective during outbreaks. Restriction of animal movement to control the spread of the disease has had limited success. In the 1995 USA epidemics, which originated in New Mexico, VS spread rapidly north and west into neighbouring states in spite of stringent quarantine measures. The disease often appeared in new areas despite the fact that there was no evidence of animal movements. Vaccination has not been an effective control method for VS.

Experimental live-virus30 and killed-virus vaccines7 have been used during epidemics of VSV-NJ, but controlled evaluations of their efficacy are lacking.

References

  1. ACREE, J.A., 1964. Colorado epizootic of vesicular stomatitis: Observations on its effects, transmission and response to therapy. Proceedings of the American Association of Equine Practitioners, 10, 289–299.
  2. AFSHAR, A., 1993. Development of a competitive enzyme-linked immunosorbent assay for detection of bovine, ovine, porcine, and equine antibodies to vesicular stomatitis virus. Journal of Clinical Microbiology, 31, 1860–1865.
  3. AGUIRRE, A.A., MCLEAN, R.G., COOK, R.S. & QUAN, T.J., 1992. Serologic survey for selected arboviruses and other potential pathogens in wildlife from Mexico. Journal of Wildlife Diseases, 28, 435–442.
  4. BEKKER, J.G., DE KOCK, F.V.D.W. & QUINLAN, J.B., 1934. The occurrence and identification of bluetongue in cattle — the so-called pseudo foot-and-mouth disease in South Africa. Onderstepoort Journal of Veterinary Science and Animal Industry, 2, 395–507.
  5. BERGOLD, G.H., SUAREZ, O.M. & MUNZ, K., 1968. Multiplication in and transmission by Aedes aegypti of vesicular stomatitis virus. Journal of Invertebrate Pathology,11, 406–412.
  6. BRANDLY, C.A., HANSON, R.P & CHOW, T.L., 1951. Vesicular stomatitis with particular reference to the 1949 Wisconsin epizootic. Proceedings of the 88th Annual Meeting of the American Veterinary Medical Association, pp. 61–69.
  7. BRIDGES, V.E., MCCLUSKEY, B.J., SALMAN, M.D., HURD, H.S. & DICK, J., 1997. Review of the 1995 vesicular stomatitis outbreak in the western United States. Journal of the American Veterinary Medical Association, 211, 556–560.
  8. CHOW, T.L. & MCNUTT, S.H., 1953. Pathological changes of experimental vesicular stomatitis of swine. American Journal of Veterinary Research, 14, 420–424.
  9. COMER, J.A., KAVANAUGH, D.M., STALLKNECHT, D.E. & CORN, J.L., 1994. Population dynamics of Lutzomyia shannoni (Diptera: Psychodidae) in relation to the epizootiology of vesicular stomatitis virus on Ossabaw Island, Georgia. Journal of Medical Entomology, 31, 850–854.
  10. COMER, J.A., TESH, R.B., MODI, G.B., CORN, J.L., & NETTLES, V.F., 1990. Vesicular stomatitis virus, New Jersey serotype: replication in and transmission by Lutzomyia shannoni (Diptera: Psychodidae). American Journal of Tropical Medicine and Hygiene, 42, 483–490.
  11. CORN, J.L., LEE, R.M., ERICKSON, G.A. & MURPHY, C.D., 1987. Serologic survey for evidence of exposure to vesicular stomatitis virus, pseudorabies virus, brucellosis and leptospirosis in collared peccaries from Arizona. Journal of Wildlife Diseases, 23, 551–557.
  12. COTTON, W.E., 1926. The causal agent of vesicular stomatitis proved to be a filter-passing virus. Journal of the American Veterinary Medical Association, 70, 168–171.
  13. COTTON, W.E., 1927. Vesicular Stomatitis, Veterinary Medicine, 22, 169–175.
  14. CUPP, E. W., MARÉ, C.J., CUPP, M.S. & RAMBERG, F.B., 1992. Biological transmission of vesicular stomatitis virus (New Jersey) by Simulium vittatum (Diptera: Simuliidae). Journal of Medical Entomology, 29, 137–140.
  15. FEDERER, K.E., BURROWS, R. & BROOKSBY, J.B., 1967. Vesicular stomatitis virus — The relationship between some strains of the Indiana serotype. Research in Veterinary Science, 8, 103–117.
  16. FRANCY, D.B., MOORE, C.G., SMITH, G.C., JAKOB, W.L., TAYLOR, S.A. & CALISHER, C.H., 1988. Epizootic vesicular stomatitis in Colorado, 1982: Isolation of virus from insects collected along the northern Colorado Rocky Mountain front range. Journal of Medical Entomology, 24, 343–347.
  17. GELETA, J.N. & HOLBROOK, A.A., 1961. Vesicular stomatitis — patterns of complement fixing and serum-neutralizing antibody in serum of convalescent cattle and horses. American Journal of Veterinary Research, 22, 713–719.
  18. HANSON, R.P., 1952. The natural history of vesicular stomatitis virus. Bacteriological Reviews, 16, 179–204
  19. HANSON, R.P., 1968. Discussion of the natural history of vesicular stomatitis. American Journal of Epidemiology, 87, 264–266
  20. HANSON, R.P. & BRANDLY, C.A., 1957. Epizootiology of vesicular stomatitis. American Journal of Public Health, 47, 205–209.
  21. HANSON, R.P., RASMUSSEN, A.F., BRANDLEY, C.A. & BROWN, J.W., 1950. Human infection with the virus of vesicular stomatitis. Journal of Laboratory and Clinical Medicine, 36, 754–758.
  22. HEINY, E., 1945. Vesicular stomatitis in cattle and horses in Colorado. North American Veterinarian, 26, 726–730.
  23. HOWERTH, E.W., STALLKNECHT, D.E., DORMINY, M., PISELL, T. & CLARKE, G.R., 1997. Experimental vesicular stomatitis in swine: Effects of route of inoculation and steroid treatment. Journal of Veterinary Diagnostic Investigation, 9, 136–142
  24. JACOULET, M., 1915. Au sujet d’une stomatite érosive de nature indéterminée (chez le cheval). Bulletin de la Société Centrale de Médicin Veterinaire,68, 576–578.
  25. JOHNSON, K.M., VOGEL, J.E. & PERALTA, P.H., 1966. Clinical and serological response to laboratory acquired human infection by Indiana type vesicular stomatitis virus (VSV). American Journal of Tropical Medicine and Hygiene, 15, 244–246.
  26. JONKERS, R.H., SHOPE, R.H., AITKEN, T.H.G. & SPENCE, L., 1964. Cocal virus: A new agent in Trinidad related to vesicular stomatitis virus, type Indiana. American Journal of Veterinary Research, 25, 236–242.
  27. JONKERS, R.H., SPENCE, L. & AITKEN, T.H.G., 1965. Cocal virus epizootology in Bush Bush Forest and the Nariva Swamp, Trinidad. American Journal of Veterinary Research, 26, 758–763.
  28. KARSTAD, L. & HANSON, R.P., 1957. Vesicular stomatitis in deer. American Journal of Veterinary Research, 18, 162–166.
  29. LASTRA, J.R. & ESPARZA, J., 1976. Multiplication of vesicular stomatitis virus in the leafhopper Peregrinus maidis (Ashm.), a vector of a plant rhabdovirus. Journal of General Virology, 32, 139–142.
  30. LAUERMAN, L.H. & HANSON, R.P., 1963. Field trial of live virus vaccination procedures for prevention of vesicular stomatitis in dairy cattle. III. Evaluation of emergency vaccination in Georgia. Proceedings of the U.S. Animal Health Association, 67, 473–482.
  31. MARÉ, C.J., CUPP, E.W. & CUPP, M.S., 1991. Vesicular stomatitis virus (New Jersey) infection and replication in black flies (Simulium vittatum). Proceedings, US Animal Health Association, 95, 179–188.
  32. MASON, J.H. & NEITZ, W.O., 1940. Erosive stomatitis of cattle. Onderstepoort Journal of Veterinary Science and Animal Industry, 15, 159–173.
  33. MEAD, D.G., MARÉ, C.J. & CUPP, E.W., 1997. Vector competence of select black fly species for vesicular stomatitis virus (New Jersey serotype). American Journal of Tropical Medicine and Hygiene, 57, 42–48.
  34. MEAD, D.G., MARÉ, C.J. & RAMBERG, F.B., 1999. Bite transmission of vesicular stomatitis virus (New Jersey serotype) to laboratory mice by Simulium vittatum (Diptera: Simliidae). Journal of Medical Entomology, 36, 11–14.
  35. MEYER, N.L., MOULTON, W.M., JENNEY, E.W. & RODGERS, R.J., 1960. Outbreaks of vesicular stomatitis in Oklahoma and Texas. Proceedings, U.S. Livestock Sanitary Association, 64th Meeting, pp. 324–332.
  36. MUMFORD, E.L., MCCLUSKEY, B.J., TRAUB-DARGATZ, J.L., SCHMITT, B.J., & SALMAN, M.D., 1998. Serologic evaluation of vesicular stomatitis virus exposure in horses and cattle in 1996. Journal of the American Veterinary Medical Association, 213, 1265–1269.
  37. MURPHY, F.A., FAUQUET, C.M., BISHOP, D.H.L., GHABRIAL, S.A., JARVIS, A.W., MARTINELLI, G.P., MAYO, M.A. & SUMMERS, M.D., 1994. Virus taxonomy. The classification and nomenclature of viruses. Sixth report of the International Committee on Taxonomy of Viruses. Wien, New York: Springer-Verlag,
  38. RADELEFF, R.D., 1949. Clinical encephalitis occurring during an outbreak of vesicular stomatitis in horses. Veterinary Medicine, 44, 494–496.
  39. REIF, J.S., WEBB, P.A., MONATH, T.P., EMERSON, J.K., POLAND, J.D., KEMP, G.E. & CHOLAS, G., 1987. Epizootic vesicular stomatitis in Colorado, 1989: Infection in occupational risk groups. American Journal of Tropical Medicine and Hygiene, 36, 177–182.
  40. RIBELIN, W.E., 1958. The cytopathogenesis of vesicular stomatitis infection in cattle. American Journal of Veterinary Research, 19, 66–73.
  41. RODRIGUEZ, L.L., LETCHWORTH, G.L., SPIROPOULOU, C.F. & NICHOL, S.T., 1993. Rapid detection of vesicular stomatitis virus New Jersey serotype in clinical samples by using polymerase chain reaction. Journal of Clinical Microbiology, 31, 2016–2020
  42. SEIBOLD, H.R. & SHARP, J.B., 1960. A revised concept of the pathological changes of the tongue in cattle with vesicular stomatitis. American Journal of Veterinary Research, 21, 35–51.
  43. SELLERS, R.F. & MAAROUF, A.R., 1990. Trajectory analysis of winds and vesicular stomatitis in North America. Epidemiology and Infection, 104, 313–328.
  44. STALLKNECHT, D.E., FLETCHER, W.O., ERICKSON, G.A. & NETTLES, V.F., 1987. Antibodies to vesicular stomatitis New Jersey type virus in wild and domestic sentinel swine. American Journal of Epidemiology, 125, 1058–1065.
  45. STALLKNECHT, D.E., HOWERTH, E.W. & REEVES, C.L., 1999. Potential for contact and mechanical vector transmission of vesicular stomatitis virus New Jersey. American Journal of Veterinary Research, 60, 43–48.
  46. STALLKNECHT, D.E., KAVANAUGH, D.M., CORN, J.L., EERNISSE, K.A., COMER, J.A. & NETTLES, V.F., 1993. Feral swine as a potential amplifying host for vesicular stomatitis virus New Jersey serotype on Ossabaw Island, Georgia. Journal of Wildlife Diseases, 29, 337–383.
  47. TEIDEBOLD, T.C., MATHER, C.S. & MERRILLAT, L.A. 1916. Gangrenous glossitis of horses. Report of the 20th Annual Meeting, U.S. Livestock Sanitary Association, pp 29–42.
  48. TESH, R.B., CHANIOTIS, B.N. & JOHNSON, K.M., 1972. Vesicular stomatitis virus (Indiana serotype): Transovarial transmission by phlebotomine sand flies. Science, 175, 1477–1479.
  49. THEILER, A., 1901. Eine contagiose Stomatitis der Pferd in Süd-Afrika. Deutsche Tierärztliche Wochenschrift, 9, 131–132.
  50. THORNE, E.T., WILLIAMS, E.S., ADRIAN, W.J. & GILLIN, C.N., 1983. Vesicular stomatitis in pronghorn antelope: Serologic survey and artificial infection. Proceedings of the U.S. Animal Health Association, 87, 638– 642
  51. WALTON, T.E., WEBB, P.A., KRAMER, W.L., SMITH, G.C., DAVIS, T., HOLBROOK, F.R., MOORE, C.G., SCHIEFER, T.J., JONES, R.H. & JANNEY, G.C., 1987. Epizootic vesicular stomatitis in Colorado, 1982: Epidemiologic and entomologic studies. American Journal of Tropical Medicine and Hygiene, 36, 166–176.
  52. WEBB, P.A. & HOLBROOK, F.R., 1989. ‘Vesicular Stomatitis’. In: MONATH, T.P. (ed.). The Arboviruses: Epidemiology and Ecology. Boca Raton, Florida: CRC Press. pp 1–29.
  53. WEBB, P.A., MCLEAN, R.G., SMITH, G.C., ELLENBERGER, J.H., FRANCY, D.B., WALTON, T.E. & MONATH, T.P., 1987. Epizootic vesicular stomatitis in Colorado, 1982: Some observations on the possible role of wildlife populations in an enzootic maintenance cycle. Journal of Wildlife Diseases, 23, 192–198.
  54. WEBB, P.A., MONATH, T.P., REIF, J.S., SMITH, G.C., KEMP, G.E., LAZUICK, J.S. & WALTON, T.E., 1987. Epizootic vesicular stomatitis in Colorado, 1982: Epidemiologic studies along the northern Colorado Front Range. American Journal of Tropical Medicine and Hygiene,36, 183–188.
  55. WHEELER, W.J., VILJOEN, J.H.B. & ROBINSON, E.M., 1945. An outbreak of severe stomatitis in cattle. Journal of the South African Veterinary Medical Association,16, 20–25.