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Equine viral arteritis: How serious is the threat to the British horse population?
Br. vel .
f.
(1992) . 148, 1 7 7
GUEST EDITORIAL EQUINE VIRAL ARTERITIS : HOW SERIOUS IS THE THREAT TO THE BRITISH HORSE POPULATION?
Equine viral arteritis (EVA) has assumed increased significance for the horse industries in many countries since the 1984 epidemic in Thoroughbreds in Kentucky (Timoney, 1985) . The occurrence sparked fears that perhaps an andromeda strain of the causal agent, equine arteritis virus (EAV), had emerged that was much more pathogenic than previously isolated strains of the virus . Many were concerned that the international movement of horses would fuel spread of the disease and provide an opportunity for extensive outbreaks of abortion in susceptible populations of mares . These concerns led to the imposition of some of the severest restrictions ever on the movement of horses from North America to certain countries, notably those of the tripartite group of France, Ireland and the United Kingdom . Considerable restrictions still remain in place in relation to EVA, over 7 years since the epidemic in Kentucky . During the interim, there has been no evidence that the disease has become more widespread as a result of that occurrence or that the incidence of EAV-related abortions has increased significantly either in the USA or in other countries . Moreover, it would appear that the vast majority of cases of this infection worldwide continue to be subclinical in nature . Concern has been expressed over the imminent threat that EVA will pose to the British horse population once a free trade market is established within the 12 member states of the European Community in 1992 (Marchant, 1991) . Equine viral arteritis was singled out as an example of a disease not covered by the EC's directives on Animal Health which could be introduced into the United Kingdom for the first time once new rules controlling movement of horses within the Community came into effect . In his review on EAV in this issue, Chirnside reiterates this concern, stating that the risk of importing EVA will increase with the elimination of the mandatory serological testing for EAV infection presently required of all horses imported into the United Kingdom from other member states with the exception of France and Ireland . The current EVA-free status of the British horse population may well be put in jeopardy should unrestricted importation of seropositive horses prevail . In attempting to assess the risks involved, consideration should be given to a number of points that hopefully will help to temper these concerns . It is worth emphasizing at the outset that EVA is not a new disease of the horse, but rather one that probably has afflicted horse populations for many years, long before the condition was aetiologically defined and pathologically characterized in 1953 (Doll et al., 1957) . Pottie (1888) and Clark (1892) provided insightful descriptions of a clinically indistinguishable malady of horses in Scotland just over
1 78
BRITISH VETERINARY JOURNAL . 148, 1
100 years ago . They recognized the contagious nature of the infection and the fact that it could be transmitted venereally by stallions several years after they had clirnically recovered from the disease . Notwithstanding the significant increase in international movement of horses that has taken place in the past 25-30 years, there is no evidence that this has resulted in the introduction of EVA into the British horse population . Prior to the 1984 epidemic in Kentucky, there were no testing requirements and no restrictions on the movement of horses because of this disease . Serological evidence of EAV infection in the British Thoroughbred population was confirmed as far back as 1971 by McCollum & Bryans (1973), who demonstrated a seroprevalence of 2 .3% among 1069 samples tested . In spite of presence of the virus in the native Thoroughbred population, there have been no published reports of any outbreaks of EVA . With the exception of the 1984 epidemic, this is analogous to the situation that has prevailed in respect of the corresponding Thoroughbred population in Kentucky since the late 1960s . Serological surveys conducted during this period (McCollum & Bryans, 1973 ; Timoney & McCollum, unpublished data) have revealed that the seroprevalence of EAV infection in the Thoroughbred breeding population has remained around 2-3% . Moraillon & Moraillon (1978), in an extensive serological survey involving horses from a range of European and African countries, found EAV antibodies in 11 .4% of French Thoroughbreds and 25% of Thoroughbreds from Ireland, both countries with which the United Kingdom has had unrestricted movement of horses with reference to EVA under the tripartite agreement . Initial concerns over the emergence of a more velogenic variant of EAV at the time of the 1984 epidemic of EVA in Kentucky have largely been allayed . None of the in-vivo studies conducted to date has provided any evidence that this was indeed the case . Chirnside reviews the significant advances in our understanding of the epidemiology of EVA and basic biology of the causal virus that have taken place in the past 6-7 years . It is now possible to define more precisely the category of horses that pose the greatest risk of importing additional strains of this virus into the largely susceptible British horse population . It has been shown that the carrier stallion is primarily implicated in the dissemination and perpetuation of EAV (Timoney & McCollum, 1985) . The carrier state can occur in an alarmingly high percentage (30-60%) of infected stallions but not in mares (Timoney & McCollum, 1991) . The virus is localized in certain of the accessory sex glands in the reproductive tract of the stallion whence it is shed constantly in the semen without any evidence of intermittency of virus shedding (Timoney et al., 1987, 1992 ; Neu et al., 1988) . Based on extensive experimental and field data, it would seem prudent in formulating an effective screening programme for EVA, to concentrate on detecting (1) the acutely infected horse that transmits the virus primarily by the respiratory route ; and (2) the chronically infected carrier stallion that is a venereal transmitter of the virus . Apart from stallions, there is little scientific justification in continuing to discriminate against seropositive horses carrying stable antibody titres regardless of their vaccination history against EVA . The potential risk of introducing EAV through the importation of infective fresh or frozen stallion semen must also be recognized . While this is not a problem for the
EQUINE VIRAL ARTERITIS
179
Thoroughbred industry, it could be a cause of significant concern for those breeds in which artificial insemination is permitted . A final point for consideration in assessing the threat that EVA poses to the British horse population relates to the feasibility of vaccination against this disease . An effective modified live virus vaccine against EVA was developed many years ago (Doll et al., 1968) . It stimulated a high level of protective immunity in vaccinated horses that lasted for a period of years (McCollum, 1969, 1986) . This vaccine was produced commercially in early 1985 (ARVAC ® , Fort Dodge Labs), and has been used over the ensuing seven breeding seasons to immunize the Thoroughbred breeding stallion populations in the states of Kentucky and New York . It has been found to be both safe and effective in preventing establishment of the carrier state in a very large and valuable population of stallions . The results of pre-export testing of stallions have confirmed that the vaccine virus does not become established in the reproductive tract and set up a carrier state (Timoney & McCollum, 1991) . While fully mindful and appreciative of the longstanding policy that exists towards the use of modified live virus vaccines in the tripartite countries, this policy may need to be reconsidered with respect to EVA in the light of forthcoming changes in the regulations controlling movement of horses within the EC . Many might question the wisdom of allowing the valuable Thoroughbred stallion population in the United Kingdom to remain at risk of infection with EAV and establishment of the carrier state when a safe and effective vaccine, albeit a modified live virus product, is available . Annual vaccination of the Thoroughbred breeding populations in the states of Kentucky and New York has been an integral and successful component of their respective control programmes against EVA since 1985 (Timoney & McCollum, 1988) . Undoubtedly, forthcoming changes governing animal movement between EC member states will increase the risk of introducing not only EVA but also other infectious diseases into the British horse population . In the case of EVA, however, the threat can be minimized through implementation of a more selective and less restrictive programme of serological and virological testing for EAV infection . Prophylactic vaccination of breeding stallions ought to be considered a necessai v adjunct to any control programme if the risk of EVA becoming endemic in the country is to be avoided . Such measures if adopted internationally, would do a great deal to facilitate movement of horses and re-establish the true significance of EAV as an equine pathogen . P .J . TI ."n(NEY
University of Kentucky, Gluck Equine Research Center, Lexington, KY 40_546-0099, USA
REFERENCES
CHIRNSIDH, E . D . (1992) . Equine arteritis virus : an overview . Br. vet. j. 148, 181-97 .
180
BRITISH VETERINARY JOURNAL, 148, 3
CLARK, 1 . (1892) . Transmission of pink-eye from apparently healthy stallions to mares . f. comp . Path. 5, 261-4 . DOLL, E . R., BRYANS, J . T ., MCCOLLVM, W. H . & CROwE, M . E . W . (1957) . Isolation of a filterable agent causing arteritis of horses and abortion by mares . Its differentiation from the equine abortion (influenza) virus . Cornell Vet. 47, 3-41 . DOLL, E . R., BRYANS, J . T., WILSON, J . C . & MCCOLLUM, W . H . (1968) . Immunization against equine viral arteritis using modified live virus propagated in cell cultures of rabbit kidney. Cornell Vet. 58, 497-524 . MARCHANT, J. (1991) . U . K. Animal production facing up to change . Anim . Pharm. 223, 8 . MCCOLLUM, W . H . (1969) . Development of a modified virus strain and vaccine for equine viral arteritis . J. Am . vet . med. Ass . 155, 318-22 . MCCOLLUM, W. H . (1986) . Responses of horses vaccinated with avirulent modified-live equine arteritis virus propagated in E . Derm (NBL-6) cell line to nasal inoculation with virulent virus . Am. J. vet . Res. 47, 1931-4 . MCCOLLUM, W . H . & BRYANS, J . T . (1973) . Serological identification of infection by equine arteritis virus in horses of several countries . In Proceedings of the Third International Conference on Equine Infectious Diseases, Paris, 1972, pp . 256-62 . Basel: Karger . MORAILLON R . & MORAILLON, A. (1978) . Results of an epidemiological investigation on viral arteritis in France and some other European and African countries . Ann . Rech . Vet. 9, 43-54 . NEU, S . M ., TIMONEY, P . J . & McCoLLuM, W . H . (1988) . Persistent infection of the reproductive tract in stallions experimentally infected with equine arteritis virus . In Proceedings of the Fifth International Conference on Equine Infectious Diseases, Lexington, 1987 pp . 149-54 . Lexington : University Press of Kentucky . POTTIE, A . (1888) . The propagation of influenza from stallions to mares. J. comp. Path . 1, 37-8 . TIMONEY, P . J . (1985) . Clinical, virological and epidemiological features of the 1984 outbreak of equine viral arteritis in the Thoroughbred population in Kentucky, U .S .A. In Proceedings of the Grayson Foundation International Conference of Thoroughbred Breeders Organizations, Drumoland Castle, Ireland, 1984, pp . 24-48 . TIMONEY, P . J . & MCCOLLUM, W. H . (1985) . The epidemiology of equine arteritis virus . Proc. Am . Ass. Equine Practnr pp . 545-51 . TIMONEY, P. J . & McCOL.t.uM, W . H . (1988) . Equine viral arteritis : epidemiology and control . J Equine vet. Sci. 8, 54-9 . TIMONEY, P . J. & MCCOLLUM, W . H . (1991) . Equine viral arteritis : current clinical and economic significance . Proc. Am . Ass. Equine Practnr pp . 403-9 . TIMONEY, P. J ., MCCOLLUM, W. H ., MURPHY, T . W ., ROBERTS, A . W ., WILLARD, A . W . & CARSWELL, J . G . (1987) . The carrier state in equine arteritis virus infection in the stallion with specific emphasis on the venereal mode of transmission . f Reprod . Fert. Suppl. 35, 95-102 . TIMONEY, P . J ., McCOLLuM, W . H . & MURPHY, T . W . (1992) . A longitudinal study of equine arteritis virus infection in Standardbred stallions with special reference to occurrence of the carrier state . In Proceedings of the Sixth International Conference on Equine Infectious Diseases, Cambridge, 1991 . Newmarket: R & W Publications, in press .
f.
(1992) . 148, 1 7 7
GUEST EDITORIAL EQUINE VIRAL ARTERITIS : HOW SERIOUS IS THE THREAT TO THE BRITISH HORSE POPULATION?
Equine viral arteritis (EVA) has assumed increased significance for the horse industries in many countries since the 1984 epidemic in Thoroughbreds in Kentucky (Timoney, 1985) . The occurrence sparked fears that perhaps an andromeda strain of the causal agent, equine arteritis virus (EAV), had emerged that was much more pathogenic than previously isolated strains of the virus . Many were concerned that the international movement of horses would fuel spread of the disease and provide an opportunity for extensive outbreaks of abortion in susceptible populations of mares . These concerns led to the imposition of some of the severest restrictions ever on the movement of horses from North America to certain countries, notably those of the tripartite group of France, Ireland and the United Kingdom . Considerable restrictions still remain in place in relation to EVA, over 7 years since the epidemic in Kentucky . During the interim, there has been no evidence that the disease has become more widespread as a result of that occurrence or that the incidence of EAV-related abortions has increased significantly either in the USA or in other countries . Moreover, it would appear that the vast majority of cases of this infection worldwide continue to be subclinical in nature . Concern has been expressed over the imminent threat that EVA will pose to the British horse population once a free trade market is established within the 12 member states of the European Community in 1992 (Marchant, 1991) . Equine viral arteritis was singled out as an example of a disease not covered by the EC's directives on Animal Health which could be introduced into the United Kingdom for the first time once new rules controlling movement of horses within the Community came into effect . In his review on EAV in this issue, Chirnside reiterates this concern, stating that the risk of importing EVA will increase with the elimination of the mandatory serological testing for EAV infection presently required of all horses imported into the United Kingdom from other member states with the exception of France and Ireland . The current EVA-free status of the British horse population may well be put in jeopardy should unrestricted importation of seropositive horses prevail . In attempting to assess the risks involved, consideration should be given to a number of points that hopefully will help to temper these concerns . It is worth emphasizing at the outset that EVA is not a new disease of the horse, but rather one that probably has afflicted horse populations for many years, long before the condition was aetiologically defined and pathologically characterized in 1953 (Doll et al., 1957) . Pottie (1888) and Clark (1892) provided insightful descriptions of a clinically indistinguishable malady of horses in Scotland just over
1 78
BRITISH VETERINARY JOURNAL . 148, 1
100 years ago . They recognized the contagious nature of the infection and the fact that it could be transmitted venereally by stallions several years after they had clirnically recovered from the disease . Notwithstanding the significant increase in international movement of horses that has taken place in the past 25-30 years, there is no evidence that this has resulted in the introduction of EVA into the British horse population . Prior to the 1984 epidemic in Kentucky, there were no testing requirements and no restrictions on the movement of horses because of this disease . Serological evidence of EAV infection in the British Thoroughbred population was confirmed as far back as 1971 by McCollum & Bryans (1973), who demonstrated a seroprevalence of 2 .3% among 1069 samples tested . In spite of presence of the virus in the native Thoroughbred population, there have been no published reports of any outbreaks of EVA . With the exception of the 1984 epidemic, this is analogous to the situation that has prevailed in respect of the corresponding Thoroughbred population in Kentucky since the late 1960s . Serological surveys conducted during this period (McCollum & Bryans, 1973 ; Timoney & McCollum, unpublished data) have revealed that the seroprevalence of EAV infection in the Thoroughbred breeding population has remained around 2-3% . Moraillon & Moraillon (1978), in an extensive serological survey involving horses from a range of European and African countries, found EAV antibodies in 11 .4% of French Thoroughbreds and 25% of Thoroughbreds from Ireland, both countries with which the United Kingdom has had unrestricted movement of horses with reference to EVA under the tripartite agreement . Initial concerns over the emergence of a more velogenic variant of EAV at the time of the 1984 epidemic of EVA in Kentucky have largely been allayed . None of the in-vivo studies conducted to date has provided any evidence that this was indeed the case . Chirnside reviews the significant advances in our understanding of the epidemiology of EVA and basic biology of the causal virus that have taken place in the past 6-7 years . It is now possible to define more precisely the category of horses that pose the greatest risk of importing additional strains of this virus into the largely susceptible British horse population . It has been shown that the carrier stallion is primarily implicated in the dissemination and perpetuation of EAV (Timoney & McCollum, 1985) . The carrier state can occur in an alarmingly high percentage (30-60%) of infected stallions but not in mares (Timoney & McCollum, 1991) . The virus is localized in certain of the accessory sex glands in the reproductive tract of the stallion whence it is shed constantly in the semen without any evidence of intermittency of virus shedding (Timoney et al., 1987, 1992 ; Neu et al., 1988) . Based on extensive experimental and field data, it would seem prudent in formulating an effective screening programme for EVA, to concentrate on detecting (1) the acutely infected horse that transmits the virus primarily by the respiratory route ; and (2) the chronically infected carrier stallion that is a venereal transmitter of the virus . Apart from stallions, there is little scientific justification in continuing to discriminate against seropositive horses carrying stable antibody titres regardless of their vaccination history against EVA . The potential risk of introducing EAV through the importation of infective fresh or frozen stallion semen must also be recognized . While this is not a problem for the
EQUINE VIRAL ARTERITIS
179
Thoroughbred industry, it could be a cause of significant concern for those breeds in which artificial insemination is permitted . A final point for consideration in assessing the threat that EVA poses to the British horse population relates to the feasibility of vaccination against this disease . An effective modified live virus vaccine against EVA was developed many years ago (Doll et al., 1968) . It stimulated a high level of protective immunity in vaccinated horses that lasted for a period of years (McCollum, 1969, 1986) . This vaccine was produced commercially in early 1985 (ARVAC ® , Fort Dodge Labs), and has been used over the ensuing seven breeding seasons to immunize the Thoroughbred breeding stallion populations in the states of Kentucky and New York . It has been found to be both safe and effective in preventing establishment of the carrier state in a very large and valuable population of stallions . The results of pre-export testing of stallions have confirmed that the vaccine virus does not become established in the reproductive tract and set up a carrier state (Timoney & McCollum, 1991) . While fully mindful and appreciative of the longstanding policy that exists towards the use of modified live virus vaccines in the tripartite countries, this policy may need to be reconsidered with respect to EVA in the light of forthcoming changes in the regulations controlling movement of horses within the EC . Many might question the wisdom of allowing the valuable Thoroughbred stallion population in the United Kingdom to remain at risk of infection with EAV and establishment of the carrier state when a safe and effective vaccine, albeit a modified live virus product, is available . Annual vaccination of the Thoroughbred breeding populations in the states of Kentucky and New York has been an integral and successful component of their respective control programmes against EVA since 1985 (Timoney & McCollum, 1988) . Undoubtedly, forthcoming changes governing animal movement between EC member states will increase the risk of introducing not only EVA but also other infectious diseases into the British horse population . In the case of EVA, however, the threat can be minimized through implementation of a more selective and less restrictive programme of serological and virological testing for EAV infection . Prophylactic vaccination of breeding stallions ought to be considered a necessai v adjunct to any control programme if the risk of EVA becoming endemic in the country is to be avoided . Such measures if adopted internationally, would do a great deal to facilitate movement of horses and re-establish the true significance of EAV as an equine pathogen . P .J . TI ."n(NEY
University of Kentucky, Gluck Equine Research Center, Lexington, KY 40_546-0099, USA
REFERENCES
CHIRNSIDH, E . D . (1992) . Equine arteritis virus : an overview . Br. vet. j. 148, 181-97 .
180
BRITISH VETERINARY JOURNAL, 148, 3
CLARK, 1 . (1892) . Transmission of pink-eye from apparently healthy stallions to mares . f. comp . Path. 5, 261-4 . DOLL, E . R., BRYANS, J . T ., MCCOLLVM, W. H . & CROwE, M . E . W . (1957) . Isolation of a filterable agent causing arteritis of horses and abortion by mares . Its differentiation from the equine abortion (influenza) virus . Cornell Vet. 47, 3-41 . DOLL, E . R., BRYANS, J . T., WILSON, J . C . & MCCOLLUM, W . H . (1968) . Immunization against equine viral arteritis using modified live virus propagated in cell cultures of rabbit kidney. Cornell Vet. 58, 497-524 . MARCHANT, J. (1991) . U . K. Animal production facing up to change . Anim . Pharm. 223, 8 . MCCOLLUM, W . H . (1969) . Development of a modified virus strain and vaccine for equine viral arteritis . J. Am . vet . med. Ass . 155, 318-22 . MCCOLLUM, W. H . (1986) . Responses of horses vaccinated with avirulent modified-live equine arteritis virus propagated in E . Derm (NBL-6) cell line to nasal inoculation with virulent virus . Am. J. vet . Res. 47, 1931-4 . MCCOLLUM, W . H . & BRYANS, J . T . (1973) . Serological identification of infection by equine arteritis virus in horses of several countries . In Proceedings of the Third International Conference on Equine Infectious Diseases, Paris, 1972, pp . 256-62 . Basel: Karger . MORAILLON R . & MORAILLON, A. (1978) . Results of an epidemiological investigation on viral arteritis in France and some other European and African countries . Ann . Rech . Vet. 9, 43-54 . NEU, S . M ., TIMONEY, P . J . & McCoLLuM, W . H . (1988) . Persistent infection of the reproductive tract in stallions experimentally infected with equine arteritis virus . In Proceedings of the Fifth International Conference on Equine Infectious Diseases, Lexington, 1987 pp . 149-54 . Lexington : University Press of Kentucky . POTTIE, A . (1888) . The propagation of influenza from stallions to mares. J. comp. Path . 1, 37-8 . TIMONEY, P . J . (1985) . Clinical, virological and epidemiological features of the 1984 outbreak of equine viral arteritis in the Thoroughbred population in Kentucky, U .S .A. In Proceedings of the Grayson Foundation International Conference of Thoroughbred Breeders Organizations, Drumoland Castle, Ireland, 1984, pp . 24-48 . TIMONEY, P . J . & MCCOLLUM, W. H . (1985) . The epidemiology of equine arteritis virus . Proc. Am . Ass. Equine Practnr pp . 545-51 . TIMONEY, P. J . & McCOL.t.uM, W . H . (1988) . Equine viral arteritis : epidemiology and control . J Equine vet. Sci. 8, 54-9 . TIMONEY, P . J. & MCCOLLUM, W . H . (1991) . Equine viral arteritis : current clinical and economic significance . Proc. Am . Ass. Equine Practnr pp . 403-9 . TIMONEY, P. J ., MCCOLLUM, W. H ., MURPHY, T . W ., ROBERTS, A . W ., WILLARD, A . W . & CARSWELL, J . G . (1987) . The carrier state in equine arteritis virus infection in the stallion with specific emphasis on the venereal mode of transmission . f Reprod . Fert. Suppl. 35, 95-102 . TIMONEY, P . J ., McCOLLuM, W . H . & MURPHY, T . W . (1992) . A longitudinal study of equine arteritis virus infection in Standardbred stallions with special reference to occurrence of the carrier state . In Proceedings of the Sixth International Conference on Equine Infectious Diseases, Cambridge, 1991 . Newmarket: R & W Publications, in press .