- Email: [email protected]
Lentivirus infections in sheep and goats: How big is the burden?
The Veterinary Journal 197 (2013) 521–522
Contents lists available at SciVerse ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Guest Editorial
Lentivirus infections in sheep and goats: How big is the burden?
Maedi visna (MV) in sheep is caused by a lentivirus, one of the family of retroviruses characterised by a long incubation period following infection. Other well-known examples are the human, simian and feline immunodeficiency viruses (HIV, SIV, and FIV, respectively), as well as equine infectious anaemia (EIA) virus. Animal lentiviruses attract great research interest as models for HIV, although the diseases they cause are of great importance in their own right. In addition lentiviruses have potential in gene therapy as they may be used to transfer genetic material into human or animal cells. A spectrum of small ruminant lentiviruses (SRLV) is capable of infecting sheep and goats. While some are adapted to each species, SRLV infections are known to pass from sheep to goats and vice versa. The disease manifestations overlap, but the main clinical signs in sheep are related to interstitial pneumonia (maedi) or meningoencephalomyelitis resulting in ataxia or the dragging of a limb (visna). In goats the classic manifestations are in the joints or brain giving the disease the name caprine arthritis encephalitis (CAE). A chronic mastitis characterised by mononuclear infiltration of the gland and reduced milk yield, is recognised in both species. In the majority of SRLV-infected sheep or goats, however, there are no clinical signs, in contrast to HIV-infected humans. Infection by SRLVs is mainly by inhalation or the ingestion of colostrum and for practical purposes animals are assumed to be infected for life. The provirus is transported to various organs in latently infected monocytes, eluding the host’s immune response. The sequence within the long terminal repeats (LTRs) in the infecting virus influences the response in the target organs, where the monocytes become macrophages and infectious virus is produced. The genetic background of animals also influences the clinical outcome of SRLV infection (Bertoni and Blacklaws, 2010). In this issue of The Veterinary Journal, Dr. Julio Benavides and colleagues from León in Spain describe the losses related to MV in two dairy sheep flocks in the main sheep-producing region of the country (Benavides et al., 2013). These flocks had a high prevalence of ELISA-detectable antibody to MV virus and exhibited mean annual mortalities, ascribed to MV, in adult sheep of 5.3% and 3.3%, respectively. There may however have also been losses related to reduced milk production and lamb growth and loss of lambs (Pekelder et al., 1991; Ploumi et al., 2001). The surveyed farms appear to have financially tolerated these losses, although it would be interesting to calculate the impact the disease had on the gross margins of the enterprises. A further interesting out-
1090-0233/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2013.06.008
come from the Benavides’ study was the fact that, despite similarities between the two flocks, a striking difference was observed in how the disease presented clinically: in one flock the respiratory form was dominant while in the other 70% of animals died or were culled because of neurological signs. Further research will be required to investigate if factors such as viral tissue tropism and/or management conditions contribute to this difference. In the author’s experience of the situation in the UK, clinical cases of MV are typically not seen until the seroprevalence in a flock rises to >50%. For infection to reach this level prolonged close animal contact is required, such as occurs when sheep are housed. Dairy flocks are frequently housed for long periods and pass through a milking parlour twice daily. Some dairy flocks in the UK have gone out of business due to losses directly linked to MV. In contrast, non-milking, commercially-managed flocks are often found to be infected yet do not exhibit clinical signs (Pritchard and Dawson, 1987). Since the introduction of more sensitive ELISA tests that can detect infection at an earlier stage (Saman et al., 1999), it is possible to eliminate SRLV infection from flocks, although given the high cost involved, there needs to be a clearly defined financial benefit (Synge and Ritchie, 2010). In the sheep sector this course of action has been taken by elite pedigree breeders who wish to sell animals accredited as free of infection. Large commercial goat dairies (i.e. those with up to 3000 milking goats) have also eradicated lentiviral infection from their herds. This is costly but the perceived benefits are the elimination of clinical signs of CAE and the ability to sell CAE-accredited stock. There may be economic as well as animal welfare benefits with the elimination of SRLVs from heavily infected flocks in Spain, but the biosecurity measures required to prevent the reintroduction of infection would need to be very robust. This would require complete isolation of the flock from all sheep or goats of unknown SRLV-infection status. Countries with large sheep industries free of MV carry out surveillance to demonstrate this and stringent import controls are in place to keep infection out. CAE has been reported in some of these countries and research on the phylogeny of the viruses identified is given high priority. While the implications and management of MV is low on the list of priorities for many sheep farmers, for flock-owners struggling with the disease, or an owner who suddenly is no longer able to attract high prices because their flock has become infected, this prioritisation rapidly changes. The study by Benavides et al. (2013) has raised the profile of MV in terms of its insidious economic consequences in
522
Guest Editorial / The Veterinary Journal 197 (2013) 521–522
intensively-managed dairy sheep and the information provided should assist those burdened with managing infected flocks. Barti Synge Borthwick Farm, Gorebridge, Midlothian EH23 4QZ, Scotland, UK E-mail address: [email protected]
References Benavides, J., Fuertes, M., García-Pariente, C., Otaola, J., Delgado, L., Javier Giraldez, J., Marín, J.F.G., Ferreras, M.C., Pérez, V., 2013. Impact of maedi-visna in intensively managed dairy sheep. The Veterinary Journal 197, 89–94.
Bertoni, G., Blacklaws, B., 2010. Small ruminant lentiviruses and cross species transmission. In: Desport, M. (Ed.), Lentiviruses and Macrophages: Molecular and Cellular Interactions. Caister Academic Press, Norfolk, UK. Pekelder, J.J., Houwers, D.J., Elving, L., 1991. Effect of maedi-visna virus-infection on lamb growth. Veterinary Record 129, 368. Ploumi, K., Christodoulou, V., Vainas, E., Lymberopoulos, A., Xioufis, A., Giouzeljiannis, A., Paschaleri, E., Dewi, I.A., 2001. Effect of maedi-visna virus infection on milk production in dairy sheep in Greece. Veterinary Record 149, 526–527. Pritchard, G.C., Dawson, M., 1987. Maedi-visna virus infection in commercial flocks of sheep in East Anglia. Veterinary record 120, 208–209. Saman, E., Van Eynde, G., Lujan, L., Extramiana, B., Harkiss, G., Tolari, F., Gonzalez, L., Amorena, B., Watt, N., Badiola, J., 1999. A new sensitive serological assay for detection of lentivirus infections in small ruminants. Clinical and Diagnostic Laboratory Immunology 6, 734–740. Synge, B.A., Ritchie, C.M., 2010. Elimination of small ruminant lentivirus infection from sheep flocks and goat herds aided by health schemes in Great Britain. Veterinary Record 167, 739–743.
Contents lists available at SciVerse ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Guest Editorial
Lentivirus infections in sheep and goats: How big is the burden?
Maedi visna (MV) in sheep is caused by a lentivirus, one of the family of retroviruses characterised by a long incubation period following infection. Other well-known examples are the human, simian and feline immunodeficiency viruses (HIV, SIV, and FIV, respectively), as well as equine infectious anaemia (EIA) virus. Animal lentiviruses attract great research interest as models for HIV, although the diseases they cause are of great importance in their own right. In addition lentiviruses have potential in gene therapy as they may be used to transfer genetic material into human or animal cells. A spectrum of small ruminant lentiviruses (SRLV) is capable of infecting sheep and goats. While some are adapted to each species, SRLV infections are known to pass from sheep to goats and vice versa. The disease manifestations overlap, but the main clinical signs in sheep are related to interstitial pneumonia (maedi) or meningoencephalomyelitis resulting in ataxia or the dragging of a limb (visna). In goats the classic manifestations are in the joints or brain giving the disease the name caprine arthritis encephalitis (CAE). A chronic mastitis characterised by mononuclear infiltration of the gland and reduced milk yield, is recognised in both species. In the majority of SRLV-infected sheep or goats, however, there are no clinical signs, in contrast to HIV-infected humans. Infection by SRLVs is mainly by inhalation or the ingestion of colostrum and for practical purposes animals are assumed to be infected for life. The provirus is transported to various organs in latently infected monocytes, eluding the host’s immune response. The sequence within the long terminal repeats (LTRs) in the infecting virus influences the response in the target organs, where the monocytes become macrophages and infectious virus is produced. The genetic background of animals also influences the clinical outcome of SRLV infection (Bertoni and Blacklaws, 2010). In this issue of The Veterinary Journal, Dr. Julio Benavides and colleagues from León in Spain describe the losses related to MV in two dairy sheep flocks in the main sheep-producing region of the country (Benavides et al., 2013). These flocks had a high prevalence of ELISA-detectable antibody to MV virus and exhibited mean annual mortalities, ascribed to MV, in adult sheep of 5.3% and 3.3%, respectively. There may however have also been losses related to reduced milk production and lamb growth and loss of lambs (Pekelder et al., 1991; Ploumi et al., 2001). The surveyed farms appear to have financially tolerated these losses, although it would be interesting to calculate the impact the disease had on the gross margins of the enterprises. A further interesting out-
1090-0233/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2013.06.008
come from the Benavides’ study was the fact that, despite similarities between the two flocks, a striking difference was observed in how the disease presented clinically: in one flock the respiratory form was dominant while in the other 70% of animals died or were culled because of neurological signs. Further research will be required to investigate if factors such as viral tissue tropism and/or management conditions contribute to this difference. In the author’s experience of the situation in the UK, clinical cases of MV are typically not seen until the seroprevalence in a flock rises to >50%. For infection to reach this level prolonged close animal contact is required, such as occurs when sheep are housed. Dairy flocks are frequently housed for long periods and pass through a milking parlour twice daily. Some dairy flocks in the UK have gone out of business due to losses directly linked to MV. In contrast, non-milking, commercially-managed flocks are often found to be infected yet do not exhibit clinical signs (Pritchard and Dawson, 1987). Since the introduction of more sensitive ELISA tests that can detect infection at an earlier stage (Saman et al., 1999), it is possible to eliminate SRLV infection from flocks, although given the high cost involved, there needs to be a clearly defined financial benefit (Synge and Ritchie, 2010). In the sheep sector this course of action has been taken by elite pedigree breeders who wish to sell animals accredited as free of infection. Large commercial goat dairies (i.e. those with up to 3000 milking goats) have also eradicated lentiviral infection from their herds. This is costly but the perceived benefits are the elimination of clinical signs of CAE and the ability to sell CAE-accredited stock. There may be economic as well as animal welfare benefits with the elimination of SRLVs from heavily infected flocks in Spain, but the biosecurity measures required to prevent the reintroduction of infection would need to be very robust. This would require complete isolation of the flock from all sheep or goats of unknown SRLV-infection status. Countries with large sheep industries free of MV carry out surveillance to demonstrate this and stringent import controls are in place to keep infection out. CAE has been reported in some of these countries and research on the phylogeny of the viruses identified is given high priority. While the implications and management of MV is low on the list of priorities for many sheep farmers, for flock-owners struggling with the disease, or an owner who suddenly is no longer able to attract high prices because their flock has become infected, this prioritisation rapidly changes. The study by Benavides et al. (2013) has raised the profile of MV in terms of its insidious economic consequences in
522
Guest Editorial / The Veterinary Journal 197 (2013) 521–522
intensively-managed dairy sheep and the information provided should assist those burdened with managing infected flocks. Barti Synge Borthwick Farm, Gorebridge, Midlothian EH23 4QZ, Scotland, UK E-mail address: [email protected]
References Benavides, J., Fuertes, M., García-Pariente, C., Otaola, J., Delgado, L., Javier Giraldez, J., Marín, J.F.G., Ferreras, M.C., Pérez, V., 2013. Impact of maedi-visna in intensively managed dairy sheep. The Veterinary Journal 197, 89–94.
Bertoni, G., Blacklaws, B., 2010. Small ruminant lentiviruses and cross species transmission. In: Desport, M. (Ed.), Lentiviruses and Macrophages: Molecular and Cellular Interactions. Caister Academic Press, Norfolk, UK. Pekelder, J.J., Houwers, D.J., Elving, L., 1991. Effect of maedi-visna virus-infection on lamb growth. Veterinary Record 129, 368. Ploumi, K., Christodoulou, V., Vainas, E., Lymberopoulos, A., Xioufis, A., Giouzeljiannis, A., Paschaleri, E., Dewi, I.A., 2001. Effect of maedi-visna virus infection on milk production in dairy sheep in Greece. Veterinary Record 149, 526–527. Pritchard, G.C., Dawson, M., 1987. Maedi-visna virus infection in commercial flocks of sheep in East Anglia. Veterinary record 120, 208–209. Saman, E., Van Eynde, G., Lujan, L., Extramiana, B., Harkiss, G., Tolari, F., Gonzalez, L., Amorena, B., Watt, N., Badiola, J., 1999. A new sensitive serological assay for detection of lentivirus infections in small ruminants. Clinical and Diagnostic Laboratory Immunology 6, 734–740. Synge, B.A., Ritchie, C.M., 2010. Elimination of small ruminant lentivirus infection from sheep flocks and goat herds aided by health schemes in Great Britain. Veterinary Record 167, 739–743.