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Control of caprine arthritis–encephalitis virus infection in three Norwegian goat herds
Small Ruminant Research 28 Ž1998. 109–114
Control of caprine arthritis–encephalitis virus infection in three Norwegian goat herds K. Nord a
a,)
˚ Orten , T. Løken a , A.
b
Department of Large Animal Clinical Sciences, Norwegian College of Veterinary Medicine, P.O. Box 8146 Dep., Oslo N-0033, Norway b District Veterinary Office, VoldaÕegen 2, Ørsta N-6150, Norway Accepted 22 May 1997
Abstract A control programme for caprine arthritis–encephalitis virus ŽCAEV. infection was established in three Norwegian goat herds comprising between 60 and 90 dairy goats. Prior to the start of the programme, herd prevalences of animals with antibodies against CAEV were 57.1%, 11.5% and 71.1%, respectively. The kids were removed from the infected herds at birth, avoiding any contact with the dam, and fed cow’s colostrum and milk. They were tested for antibodies against CAEV twice a year. Seronegative groups were gradually established within each herd. When housed indoors, the seronegative groups were kept segregated from the seropositive groups by compact pen fences. At pastures, the degree of segregation varied. Altogether 56 out of 245 goats which were raised according to the scheme tested positively or indeterminately in an ELISA for antibodies against CAEV. Positive and indeterminate animals were culled. Two years after establishing the control programme, the herd with the highest initial prevalence and in which infected and seronegative goats grazed on common pastures, had a higher seroconversion rate than the other herds. q 1998 Published by Elsevier Science B.V. Keywords: Caprine arthritis–encephalitis virus; CAE; Antibodies; ELISA; Control
1. Introduction Caprine arthritis–encephalitis ŽCAE. is a significant lentiviral disease of goats in intensive dairy goat farming based on European breeds ŽDawson, 1987.. In Norway, a survey of the prevalence of antibodies against CAEV revealed about 90% of goat herds to be positive ŽNord et al., to be published.. CAE is characterised by a long incubation period, protracted clinical course and persistent infection ŽMacDiarmid, 1984.. The disease is commonly associated with )
61.
Corresponding author. Tel.: q47-22-96-55; fax: q47-22-47-
arthritis, encephalitis, pneumonia, mastitis andror chronic wasting ŽAdams et al., 1983; Dawson, 1987; Robinson and Ellis, 1986; Woodard et al., 1982; Zink and Narayan, 1989; Zwahlen et al., 1983.. The majority of CAEV infected goats are, however, subclinical carriers. Natural secretions and excretions such as milk, saliva, urine and faeces may contaminate feed and drink. The infection spreads readily in dairy goat herds in which kids are often raised on pooled unpasteurised goat’s milk. Transfer of virus may occur during licking and milking ŽAdams et al., 1983; East et al., 1993.. Although the importance of other routes of transmission is a subject of discussion, horizontal transmission has been registered as a
00921-4488r98r$19.00 q 1998 Published by Elsevier Science B.V. All rights reserved. PII S 0 9 2 1 - 4 4 8 8 Ž 9 7 . 0 0 0 7 9 - 5
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K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
result of close contact, even at pasture ŽAdams et al., 1983; Rowe et al., 1992b.. Virus may be transferred from dam to caesarean-derived kids, but whether this occurs during birth or intrauterinely is not known ŽAdams et al., 1983.. Antibody-negative females seroconverted after mating with antibody-positive males ŽRowe et al., 1992b.. CAEV might be transferred with semen via infected leucocytes. Infection by artificial insemination has not yet been demonstrated. Lentiviruses are more resistant than most other viruses to UV-light and irradiation ŽFenner et al., 1987., but are sensitive to drying, heating and sunshine ŽNarayan et al., 1982.. Specific control programmes have been reported to successfully reduce the number of infected animals, inter al. in Switzerland, France, U.S.A., Australia and New Zealand ŽAdams et al., 1983; Ellis, 1988; Ellis et al., 1983; MacDiarmid, 1984; MacKenzie et al., 1987; Rowe et al., 1992a,b.. The object of this study was to establish a control programme, the implementation of which would be feasible for Norwegian goat farmers, realising that a very strict segregation procedure using separate housing systems and different pastures for infected and seronegative groups, would be rather difficult to practice in the majority of Norwegian goat herds.
2. Materials and methods 2.1. Animals and herd management The three goat herds in the study, A, B and C, located in Sunnmøre County in the western region of Norway, comprised approximately 60, 90 and 80 milking goats, respectively, of the Norwegian goat breed. The number of milking goats in herd B fell from 90 to 75 during the first year of the study. Females were mostly bred naturally to males belonging to a breeding cooperative comprising 17 herds, all of which were positive for CAEV-antibodies. Some of the males originated from other counties, and most of them were mated with several females in at least three different herds. The main kidding season was April to May in herd A and January to February in herds B and C. The feeding of kids on pooled, unpasteurised goat’s milk had been practiced over the past two or three decades.
2.2. Rearing procedures and herd management in the control programme Housing systems were washed, using high pressure hoses, before installing the negative animals. Kids were removed from the dams in the infected group at the time of birth, avoiding any contact, including sucking and licking. All kids were raised on cow’s colostrum and cow’s sour milk or sour milk replacers in addition to silage, concentrates and hay. The kids were kept in the same room as their positive herdmates ŽB and C., or in a neighbouring room with an open connection ŽA., in groups of 20 to 30 separated by compact pen fences four to five feet high. During summer, the seronegative group of herd A was kept on a separate pasture. The seronegative groups of herds B and C were allowed to mix with the infected groups at pasture, but when housed indoors they were again kept in separate pens. Breeding males, originating from seronegative groups, were antibody-negative. Semen for artificial insemination originated mostly from untested animals. In herds A and C, offspring of goats in the seronegative groups were born naturally and allowed to suck colostrum, while all kids in herd B were removed from their dams at birth. Seronegative goats were milked before the seropositive ones. Milking equipment was washed and disinfected using routine procedures Ž0.15% sulphonamidic acid and 4.1% chloride.. Adults were defined as animals above six months of age. Animals testing positively or indeterminately were culled, although on one occasion, when many results were indeterminate, culling was postponed until confirmatory retesting was carried out two or three months later. The offspring or dams of animals with positive or indeterminate results, who had sucked or nursed, were likewise culled.
2.3. Clinicopathological examinations Goats in the seronegative groups showing signs indicative of CAE, as observed by the owner, were examined clinically including a general assessment of condition and gait, inspection and palpation of joints and udder, and auscultation of the chest. Such goats were autopsied routinely.
K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
2.4. Serological testing The ELISA employed for all samples was based on the recombinantly synthesised core proteins p17 and p28 ŽRimstad et al., 1994.. Before the control programme was introduced, all goats in herds A and C were examined, but only 26 randomly selected animals in herd B. During the control programme, all kids were likewise tested for antibodies against CAEV before their 14th day of life, except those in herd B in the first year, when only seven out of 33 were tested. Furthermore, all goats in the negative groups were similarly tested every six months.
3. Results 3.1. Clinicopathological findings No signs of CAE were observed in the groups being established according to the control scheme, apart from one yearling in herd C. This female, which tested antibody-negative in late pregnancy, developed signs including head tilt and circling and was euthanised. On necropsy, non-suppurative demyelinating encephalomyelitis was found. The lesions of the central nervous system were considered indicative of CAE. 3.2. Serological findings Prior to introduction of the control programme, the herd prevalences of antibody-positive animals in herds A, B and C were 57.1%, 11.5% and 71.1%, respectively.
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During the control programme, of 207 kids tested before 14 days of age, 205 were negative and only two had indeterminate results ŽTable 1.. The latter were delivered naturally by dams found to be seronegative in late gestation, and had been nursed and suckled. Of the 209 six-month olds, 12 were antibodypositive, while nine had indeterminate results ŽTable 1.. At the age of 12 months, two animals tested antibody-positive while four had indeterminate results out of a total of 98. Pregnant females were mostly in the last trimester of gestation. However, about a month after parturition, on retesting two former seronegative females in herd A whose newborn kids had indeterminate results, one was positive and one had an indeterminate result. Of 80 goats tested at the age of 18 months, six out of seven found to be positive and nine out of 14 found to have indeterminate results belonged to herd C. Four six-month old and 14 18-month old females with indeterminate results were negative on retesting two months later. They were kept in the negative groups, some being in their last trimester of gestation. Of their 15 newborn kids, which were mothered, six were antibody-positive. When adult females were retested, a further two months after delivery, altogether nine proved to be positive. Seven of these adults and all kids belonged to herd C. 4. Discussion The most practical, virus-free source of immunoglobulins for newborn kids was considered to be
Table 1 Number of goats with ELISA-antibodies against CAEV in three goat herds before and after implementation of a control programme Age
Before control ) 12 months After control - 14 days 6 months 12 months 18 months a
No. of goats positive Ž p . q indeterminate Ž i .rtotal examined Ž†. ŽŽ p q i .r† %. Herd Aa
Herd B b
Herd C b
Total
36; 9r63 Ž71.4. 0; 2r72 Ž2.8. 4; 2r63 Ž9.5. 1; 1r22 Ž9.0. 0; 3r20 Ž15.0.
3; 11r26 Ž53.9. 0; 0r36 Ž0. 2; 2r59 Ž6.8. 0; 1r31 Ž3.2. 1; 2r24 Ž12.5.
91; 10r128 Ž78.9. 0; 0r99 Ž0. 6; 5r87 Ž12.6. 1; 2r45 Ž6.7. 6; 9r36 Ž41.7.
130; 30r217 Ž73.7. 0; 2r207 Ž0.9. 12; 9r209 Ž10.1. 2; 4r98 Ž6.1. 7; 14r80 Ž26.3.
The seronegative group was kept segregated from the infected one. All animals in each herd mingled at pasture.
b
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K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
cow’s colostrum. No signs of disease associated with lack of passive immunity were recorded in 229 kids fed cow’s colostrum ŽNord, to be published.. However, in the second year of the control programme, an increased occurrence of respiratory disease in the kids and yearlings was experienced in herd C. This may have been due to deprivation of maternal goat antibodies increasing the susceptibility of kids to respiratory infection. The increased burden of infective respiratory organisms in the environment probably also influenced the development of disease. Some cows produce colostrum containing antibodies against kids’ erythrocytes, inducing haemolysis ŽWinter and Clarkson, 1992.. As the risk of the presence of such antibodies is greater in pooled cow’s milk, the kids were fed colostrum originating from one cow at a time. No signs of disease associated with the bovine colostrum were registered. Although the detection of CAEV antibodies in goats is considered to be diagnostic for the infection ŽCutlip et al., 1988., delayed seroconversion has been well documented ŽAdams et al., 1983; East et al., 1993; Ellis et al., 1983; McGuire et al., 1990; Rimstad et al., 1993.. In the control programme with twice yearly testing, a newly infected goat would be in contact with susceptible herdmates from one to six months before it is detected and removed, possibly in addition to the time from exposure to seroconversion. Virus-positive, undetected or antibody-negative animals represent a hazard as a continuous source of infection in any control programme based on serological testing. This was demonstrated by the testnegative goat in herd C with clinical and pathological findings consistent with CAE, and by some of the results at serological retesting. On retesting animals with indeterminate ELISA results, about 50% proved to be antibody-positive Ždata not shown.. Indeterminate results might be caused by low production of antibodies regardless of stage of infection, a terminal stage of illness with excess antigen, or by unspecific reactions ŽRimstad et al., 1994.. As such animals represent a potential risk of infection, they were culled. However, because of the relatively large proportion of 18-month old animals showing indeterminate results, on that occasion, all animals with indeterminate results were retested before culling. The differences between herd seroconversion rates
seemed to increase with the age of the animals. About 18 months after introducing the control programme, the percentage of goats with positive or indeterminate results for the first time was more than twice as high in herd C compared to herds A and B. New infections have a cumulative effect, as antibody production is lifelong. In addition, the probability of triggering antibody production in a CAEV-positive animal generally increases with time ŽEast et al., 1987; Randall et al., 1992; Rowe et al., 1992a. ŽNord et al., to be published.. The CAEV does not stay infective for any amount of time outside the host, but may survive for some time protected in cells, i.e., in faeces and milk ŽFenner et al., 1987; Narayan et al., 1982.. Mechanical cleaning of the premises was considered sufficient to eliminate the virus. In herds B and C, seronegative and infected groups were allowed to mingle on common pasture, as fencing would have been difficult. Risk of virus transmission on pasture increases with degree of contact, length of time ŽAdams et al., 1983; Rowe et al., 1992b., and with the prevalence of infected animals. Thus, mixing uninfected goats with a herd with 71% seropositive animals, as in herd C, was more risky than mixing them with a herd with 12% seropositives Žherd B.. The risk of transmission by close contact was probably also greater on herd C’s relatively confined pasture than on herd B’s open mountain pasture. On the other hand, transmission in herd B during the grazing season might well be more pronounced than would be anticipated from the low seroprevalence, as a somewhat larger prevalence of virus-positive animals in the original herd is indicated by the large rate of indeterminate results ŽTable 1.. Herd A, in which the groups were kept segregated both indoors and on pasture, should be at lower risk as regards transmission than the others. However, inadequate supervision of kidding might have caused a greater risk of transmission of virus early in life. In addition, the total space available per animal, both indoors and at pasture, was smallest in herd A. Transmission of the virus from dam to kids either intrauterine or during parturition cannot be ruled out in any of the herds. At birth, kids are negative for antibodies against CAEV, and antibody production is negligible before one to three months of age ŽBulgin, 1990.. Thus, any
K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
antibodies present in neonates probably derive from colostrum, with transfer of virus likely at the same time. The females in the seronegative groups were found to be negative during late gestation. Nevertheless, eight of their newborn kids proved seropositive. Serolevels of antibodies against CAEV have been reported to fall around parturition, while antibody levels in milk increase. The passage of antibodies to the colostrum might explain such a depletion of serum antibodies ŽEllis, 1985; Smith and Cutlip, 1988.. On retesting two months after parturition, all the dams of these kids were positive. Six had tested indeterminately once before, prior to mating. The use of other test routines, such as testing the females earlier in pregnancy, might have led to earlier detection of antibodies. On the other hand, seroconversion induced by the stress of late pregnancy and parturition should not be ruled out. The testing for maternal antibodies in all kids early in life allows carriers of CAEV to be identified and culled at an early stage. It seems that total segregation of seronegative and seropositive groups, even at pasture, is of vital importance for the establishment of herds free from CAEV infection. Before final conclusions are drawn regarding the possibility of reducing CAEV prevalence in a herd with less strict segregation, further investigations are needed. Even with a strict control scheme, considerable reduction in the prevalence of virus-positive animals rather than complete eradication is probably the most realistic aim for the first two or three years. To be declared free of the infection, a previously infected herd should test negatively on at least three or four occasions at intervals of six to twelve months ŽEllis, 1988; Halgaard, 1988..
Acknowledgements We are grateful to the herd owners for allowing us to use their dairy goat herds in this study and for their help and continued interest. Thanks are due also to Dr. G. Gunnes, Department of Pathology, Norwegian College of Veterinary Medicine, for pathological examinations. We are indebted to Dr. E. Skjerve, Norwegian College of Veterinary Medicine for valuable advice, constructive criticism and correction of the manuscript.
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References Adams, D.S., Klevjer, A.P., Carlson, J.L., McGuire, T.C., Gorham, J.R., 1983. Transmission and control of caprine arthritis–encephalitis virus. Am. J. Vet. Res. 44, 1670–1675. Bulgin, M.S., 1990. Ovine progressive pneumonia, caprine arthritis–encephalitis, and related lentiviral diseases of sheep and goats. Vet. Clin. North Am. Food Anim. Pract. 6, 691–704. Cutlip, R.C., Lehmkuhl, H.D., Schmerr, M.J., Brogden, K.A., 1988. Ovine progressive pneumonia Žmaedi–visna. in sheep. Vet. Microbiol. 17, 237–250. Dawson, M., 1987. Caprine arthritis-encephalitis. In Pract., Farm Pract., 8–11. East, N.E., Rowe, J.D., Madewell, B.R., Floyd, K., 1987. Serologic prevalence of caprine arthritis–encephalitis virus in California goat dairies. J. Am. Vet. Med. Assoc. 190, 182–186. East, N.E., Rowe, J.D., Dahlberg, J.E., Theilen, G.H., Pedersen, N.C., 1993. Modes of transmission of caprine arthritis–encephalitis virus infection. Small Rumin. Res. 10, 251–262. Ellis, T.M., 1985. ‘Big knee’ virus of goats. West. Aust. Dept. Agric. Farm. 60 Ž85., 91–95. Ellis, T., 1988. Control of caprine arthritis–encephalitis in goats. J. Agric. West. Aust. 29, 91–95. Ellis, T., Robinson, W., Wilcox, G., 1983. Effect of colostrum deprivation of goat kids on the natural transmission of caprine retrovirus. Aust. Vet. J. 60, 326–329. Fenner, F., Bachmann, P.A., Gibbs, E.P.J., Murphy, F.A., Studdert, M.J., White, D.O., 1987. Veterinary Virology. Academic Press, London, 660 pp. Halgaard, C., 1988. Det frivillige maedi–visna kontrolprogram. ŽVoluntary maedirvisna control programme.. Dan. Vet. Tidsskr. 71, 198–202. MacDiarmid, S.C., 1984. Scheme to accredit flocks free from caprine arthritis encephalitis infection. N. Z. Vet. J. 32, 165– 166. MacKenzie, R.W., Oliver, R.E., Rooney, J.P., Kagei, H., 1987. A successful attempt to raise goat kids free of infection with caprine arthritis encephalitis virus in an endemically infected goat herd. N. Z. Vet. J. 35, 184–186. McGuire, T.C., O’Rourke, K.I., Knowles, D.P., Cheevers, W.P., 1990. Caprine arthritis encephalitis lentivirus transmission and disease. Curr. Top. Microbiol. Immunol. 160, 61–75. Narayan, O., Wolinsky, J.S., Clements, J.S., Strandberg, J.D., Griffin, D.E., Cork, L.C., 1982. Slow virus replication: the role of macrophages in the persistence and expression of visna viruses of sheep and goats. J. Gen. Virol. 59, 345–356. Randall, C., Cutlip, D.V.M., Howard, D., Lehmkuhl, P., Jerome, M., Sacks, P., Amy, L., Weaver, M.S., 1992. Prevalence of antibody to caprine arthritis–encephalitis virus in goats in the United States. J. Am. Vet. Med. Assoc. 200, 802–805. Rimstad, E., East, N.E., Torten, M., Higgins, J., Derock, E., Pedersen, N.C., 1993. Delayed seroconversion following naturally acquired caprine arthritis–encephalitis virus infection in goats. Am. J. Vet. Res. 54, 1858–1862. Rimstad, E., East, N., Derock, E., Higgins, J., Pedersen, N.C., 1994. Detection of antibodies to caprine arthritis–encephalitis
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virus using recombinant GAG proteins. Arch. Virol. 134, 345–356. Robinson, W.F., Ellis, T.M., 1986. Caprine arthritis–encephalitis virus infection: from recognition to eradication. Aust. Vet. J. 63, 237–241. Rowe, J.D., East, N.E., Franti, C.E., Thurmond, M.C., Pedersen, N.C., Theilen, G.H., 1992a. Risk factors associated with the incidence of seroconversion to caprine arthritis–encephalitis virus in goats on California dairies. Am. J. Vet. Res. 53, 2396–2403. Rowe, J.D., East, N.E., Thurmond, M.C., Franti, C.E., Pedersen, N.C., 1992b. Cohort study of natural transmission and two methods for control of caprine arthritis–encephalitis virus infection in goats on a California dairy. Am. J. Vet. Res. 53, 2386–2395. Smith, M.C., Cutlip, R., 1988. Effects of infection with caprine
arthritis–encephalitis virus on milk production in goats. J. Am. Vet. Med. Assoc. 193, 63–67. Winter, A., Clarkson, M., 1992. Anaemia in lambs and kids caused by feeding cow colostrum. In Pract., November 1992, 283–286. Woodard, J.C., Gaskin, J.M., Poulos, P.W., MacKay, R.J., Burridge, M.J., 1982. Caprine arthritis–encephalitis: clinicopathologic study. Am. J. Vet. Res. 43, 2085–2096. Zink, M.C., Narayan, O., 1989. Lentivirus-induced interferon inhibits maturation and proliferation of monocytes and restricts the replication of caprine arthritis–encephalitis virus. J. Virol. 63, 2578–2584. Zwahlen, R., Aeschbacher, M., Balcer, T., 1983. Lentivirusinfectionen bei ziegen mit carpitis und interstitieller mastitis. ŽLentivirus infections in goats with carpitis and interstitial mastitis.. Schweiz. Arch. Tierheilk 125, 281–299.
Control of caprine arthritis–encephalitis virus infection in three Norwegian goat herds K. Nord a
a,)
˚ Orten , T. Løken a , A.
b
Department of Large Animal Clinical Sciences, Norwegian College of Veterinary Medicine, P.O. Box 8146 Dep., Oslo N-0033, Norway b District Veterinary Office, VoldaÕegen 2, Ørsta N-6150, Norway Accepted 22 May 1997
Abstract A control programme for caprine arthritis–encephalitis virus ŽCAEV. infection was established in three Norwegian goat herds comprising between 60 and 90 dairy goats. Prior to the start of the programme, herd prevalences of animals with antibodies against CAEV were 57.1%, 11.5% and 71.1%, respectively. The kids were removed from the infected herds at birth, avoiding any contact with the dam, and fed cow’s colostrum and milk. They were tested for antibodies against CAEV twice a year. Seronegative groups were gradually established within each herd. When housed indoors, the seronegative groups were kept segregated from the seropositive groups by compact pen fences. At pastures, the degree of segregation varied. Altogether 56 out of 245 goats which were raised according to the scheme tested positively or indeterminately in an ELISA for antibodies against CAEV. Positive and indeterminate animals were culled. Two years after establishing the control programme, the herd with the highest initial prevalence and in which infected and seronegative goats grazed on common pastures, had a higher seroconversion rate than the other herds. q 1998 Published by Elsevier Science B.V. Keywords: Caprine arthritis–encephalitis virus; CAE; Antibodies; ELISA; Control
1. Introduction Caprine arthritis–encephalitis ŽCAE. is a significant lentiviral disease of goats in intensive dairy goat farming based on European breeds ŽDawson, 1987.. In Norway, a survey of the prevalence of antibodies against CAEV revealed about 90% of goat herds to be positive ŽNord et al., to be published.. CAE is characterised by a long incubation period, protracted clinical course and persistent infection ŽMacDiarmid, 1984.. The disease is commonly associated with )
61.
Corresponding author. Tel.: q47-22-96-55; fax: q47-22-47-
arthritis, encephalitis, pneumonia, mastitis andror chronic wasting ŽAdams et al., 1983; Dawson, 1987; Robinson and Ellis, 1986; Woodard et al., 1982; Zink and Narayan, 1989; Zwahlen et al., 1983.. The majority of CAEV infected goats are, however, subclinical carriers. Natural secretions and excretions such as milk, saliva, urine and faeces may contaminate feed and drink. The infection spreads readily in dairy goat herds in which kids are often raised on pooled unpasteurised goat’s milk. Transfer of virus may occur during licking and milking ŽAdams et al., 1983; East et al., 1993.. Although the importance of other routes of transmission is a subject of discussion, horizontal transmission has been registered as a
00921-4488r98r$19.00 q 1998 Published by Elsevier Science B.V. All rights reserved. PII S 0 9 2 1 - 4 4 8 8 Ž 9 7 . 0 0 0 7 9 - 5
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K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
result of close contact, even at pasture ŽAdams et al., 1983; Rowe et al., 1992b.. Virus may be transferred from dam to caesarean-derived kids, but whether this occurs during birth or intrauterinely is not known ŽAdams et al., 1983.. Antibody-negative females seroconverted after mating with antibody-positive males ŽRowe et al., 1992b.. CAEV might be transferred with semen via infected leucocytes. Infection by artificial insemination has not yet been demonstrated. Lentiviruses are more resistant than most other viruses to UV-light and irradiation ŽFenner et al., 1987., but are sensitive to drying, heating and sunshine ŽNarayan et al., 1982.. Specific control programmes have been reported to successfully reduce the number of infected animals, inter al. in Switzerland, France, U.S.A., Australia and New Zealand ŽAdams et al., 1983; Ellis, 1988; Ellis et al., 1983; MacDiarmid, 1984; MacKenzie et al., 1987; Rowe et al., 1992a,b.. The object of this study was to establish a control programme, the implementation of which would be feasible for Norwegian goat farmers, realising that a very strict segregation procedure using separate housing systems and different pastures for infected and seronegative groups, would be rather difficult to practice in the majority of Norwegian goat herds.
2. Materials and methods 2.1. Animals and herd management The three goat herds in the study, A, B and C, located in Sunnmøre County in the western region of Norway, comprised approximately 60, 90 and 80 milking goats, respectively, of the Norwegian goat breed. The number of milking goats in herd B fell from 90 to 75 during the first year of the study. Females were mostly bred naturally to males belonging to a breeding cooperative comprising 17 herds, all of which were positive for CAEV-antibodies. Some of the males originated from other counties, and most of them were mated with several females in at least three different herds. The main kidding season was April to May in herd A and January to February in herds B and C. The feeding of kids on pooled, unpasteurised goat’s milk had been practiced over the past two or three decades.
2.2. Rearing procedures and herd management in the control programme Housing systems were washed, using high pressure hoses, before installing the negative animals. Kids were removed from the dams in the infected group at the time of birth, avoiding any contact, including sucking and licking. All kids were raised on cow’s colostrum and cow’s sour milk or sour milk replacers in addition to silage, concentrates and hay. The kids were kept in the same room as their positive herdmates ŽB and C., or in a neighbouring room with an open connection ŽA., in groups of 20 to 30 separated by compact pen fences four to five feet high. During summer, the seronegative group of herd A was kept on a separate pasture. The seronegative groups of herds B and C were allowed to mix with the infected groups at pasture, but when housed indoors they were again kept in separate pens. Breeding males, originating from seronegative groups, were antibody-negative. Semen for artificial insemination originated mostly from untested animals. In herds A and C, offspring of goats in the seronegative groups were born naturally and allowed to suck colostrum, while all kids in herd B were removed from their dams at birth. Seronegative goats were milked before the seropositive ones. Milking equipment was washed and disinfected using routine procedures Ž0.15% sulphonamidic acid and 4.1% chloride.. Adults were defined as animals above six months of age. Animals testing positively or indeterminately were culled, although on one occasion, when many results were indeterminate, culling was postponed until confirmatory retesting was carried out two or three months later. The offspring or dams of animals with positive or indeterminate results, who had sucked or nursed, were likewise culled.
2.3. Clinicopathological examinations Goats in the seronegative groups showing signs indicative of CAE, as observed by the owner, were examined clinically including a general assessment of condition and gait, inspection and palpation of joints and udder, and auscultation of the chest. Such goats were autopsied routinely.
K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
2.4. Serological testing The ELISA employed for all samples was based on the recombinantly synthesised core proteins p17 and p28 ŽRimstad et al., 1994.. Before the control programme was introduced, all goats in herds A and C were examined, but only 26 randomly selected animals in herd B. During the control programme, all kids were likewise tested for antibodies against CAEV before their 14th day of life, except those in herd B in the first year, when only seven out of 33 were tested. Furthermore, all goats in the negative groups were similarly tested every six months.
3. Results 3.1. Clinicopathological findings No signs of CAE were observed in the groups being established according to the control scheme, apart from one yearling in herd C. This female, which tested antibody-negative in late pregnancy, developed signs including head tilt and circling and was euthanised. On necropsy, non-suppurative demyelinating encephalomyelitis was found. The lesions of the central nervous system were considered indicative of CAE. 3.2. Serological findings Prior to introduction of the control programme, the herd prevalences of antibody-positive animals in herds A, B and C were 57.1%, 11.5% and 71.1%, respectively.
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During the control programme, of 207 kids tested before 14 days of age, 205 were negative and only two had indeterminate results ŽTable 1.. The latter were delivered naturally by dams found to be seronegative in late gestation, and had been nursed and suckled. Of the 209 six-month olds, 12 were antibodypositive, while nine had indeterminate results ŽTable 1.. At the age of 12 months, two animals tested antibody-positive while four had indeterminate results out of a total of 98. Pregnant females were mostly in the last trimester of gestation. However, about a month after parturition, on retesting two former seronegative females in herd A whose newborn kids had indeterminate results, one was positive and one had an indeterminate result. Of 80 goats tested at the age of 18 months, six out of seven found to be positive and nine out of 14 found to have indeterminate results belonged to herd C. Four six-month old and 14 18-month old females with indeterminate results were negative on retesting two months later. They were kept in the negative groups, some being in their last trimester of gestation. Of their 15 newborn kids, which were mothered, six were antibody-positive. When adult females were retested, a further two months after delivery, altogether nine proved to be positive. Seven of these adults and all kids belonged to herd C. 4. Discussion The most practical, virus-free source of immunoglobulins for newborn kids was considered to be
Table 1 Number of goats with ELISA-antibodies against CAEV in three goat herds before and after implementation of a control programme Age
Before control ) 12 months After control - 14 days 6 months 12 months 18 months a
No. of goats positive Ž p . q indeterminate Ž i .rtotal examined Ž†. ŽŽ p q i .r† %. Herd Aa
Herd B b
Herd C b
Total
36; 9r63 Ž71.4. 0; 2r72 Ž2.8. 4; 2r63 Ž9.5. 1; 1r22 Ž9.0. 0; 3r20 Ž15.0.
3; 11r26 Ž53.9. 0; 0r36 Ž0. 2; 2r59 Ž6.8. 0; 1r31 Ž3.2. 1; 2r24 Ž12.5.
91; 10r128 Ž78.9. 0; 0r99 Ž0. 6; 5r87 Ž12.6. 1; 2r45 Ž6.7. 6; 9r36 Ž41.7.
130; 30r217 Ž73.7. 0; 2r207 Ž0.9. 12; 9r209 Ž10.1. 2; 4r98 Ž6.1. 7; 14r80 Ž26.3.
The seronegative group was kept segregated from the infected one. All animals in each herd mingled at pasture.
b
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K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
cow’s colostrum. No signs of disease associated with lack of passive immunity were recorded in 229 kids fed cow’s colostrum ŽNord, to be published.. However, in the second year of the control programme, an increased occurrence of respiratory disease in the kids and yearlings was experienced in herd C. This may have been due to deprivation of maternal goat antibodies increasing the susceptibility of kids to respiratory infection. The increased burden of infective respiratory organisms in the environment probably also influenced the development of disease. Some cows produce colostrum containing antibodies against kids’ erythrocytes, inducing haemolysis ŽWinter and Clarkson, 1992.. As the risk of the presence of such antibodies is greater in pooled cow’s milk, the kids were fed colostrum originating from one cow at a time. No signs of disease associated with the bovine colostrum were registered. Although the detection of CAEV antibodies in goats is considered to be diagnostic for the infection ŽCutlip et al., 1988., delayed seroconversion has been well documented ŽAdams et al., 1983; East et al., 1993; Ellis et al., 1983; McGuire et al., 1990; Rimstad et al., 1993.. In the control programme with twice yearly testing, a newly infected goat would be in contact with susceptible herdmates from one to six months before it is detected and removed, possibly in addition to the time from exposure to seroconversion. Virus-positive, undetected or antibody-negative animals represent a hazard as a continuous source of infection in any control programme based on serological testing. This was demonstrated by the testnegative goat in herd C with clinical and pathological findings consistent with CAE, and by some of the results at serological retesting. On retesting animals with indeterminate ELISA results, about 50% proved to be antibody-positive Ždata not shown.. Indeterminate results might be caused by low production of antibodies regardless of stage of infection, a terminal stage of illness with excess antigen, or by unspecific reactions ŽRimstad et al., 1994.. As such animals represent a potential risk of infection, they were culled. However, because of the relatively large proportion of 18-month old animals showing indeterminate results, on that occasion, all animals with indeterminate results were retested before culling. The differences between herd seroconversion rates
seemed to increase with the age of the animals. About 18 months after introducing the control programme, the percentage of goats with positive or indeterminate results for the first time was more than twice as high in herd C compared to herds A and B. New infections have a cumulative effect, as antibody production is lifelong. In addition, the probability of triggering antibody production in a CAEV-positive animal generally increases with time ŽEast et al., 1987; Randall et al., 1992; Rowe et al., 1992a. ŽNord et al., to be published.. The CAEV does not stay infective for any amount of time outside the host, but may survive for some time protected in cells, i.e., in faeces and milk ŽFenner et al., 1987; Narayan et al., 1982.. Mechanical cleaning of the premises was considered sufficient to eliminate the virus. In herds B and C, seronegative and infected groups were allowed to mingle on common pasture, as fencing would have been difficult. Risk of virus transmission on pasture increases with degree of contact, length of time ŽAdams et al., 1983; Rowe et al., 1992b., and with the prevalence of infected animals. Thus, mixing uninfected goats with a herd with 71% seropositive animals, as in herd C, was more risky than mixing them with a herd with 12% seropositives Žherd B.. The risk of transmission by close contact was probably also greater on herd C’s relatively confined pasture than on herd B’s open mountain pasture. On the other hand, transmission in herd B during the grazing season might well be more pronounced than would be anticipated from the low seroprevalence, as a somewhat larger prevalence of virus-positive animals in the original herd is indicated by the large rate of indeterminate results ŽTable 1.. Herd A, in which the groups were kept segregated both indoors and on pasture, should be at lower risk as regards transmission than the others. However, inadequate supervision of kidding might have caused a greater risk of transmission of virus early in life. In addition, the total space available per animal, both indoors and at pasture, was smallest in herd A. Transmission of the virus from dam to kids either intrauterine or during parturition cannot be ruled out in any of the herds. At birth, kids are negative for antibodies against CAEV, and antibody production is negligible before one to three months of age ŽBulgin, 1990.. Thus, any
K. Nord et al.r Small Ruminant Research 28 (1998) 109–114
antibodies present in neonates probably derive from colostrum, with transfer of virus likely at the same time. The females in the seronegative groups were found to be negative during late gestation. Nevertheless, eight of their newborn kids proved seropositive. Serolevels of antibodies against CAEV have been reported to fall around parturition, while antibody levels in milk increase. The passage of antibodies to the colostrum might explain such a depletion of serum antibodies ŽEllis, 1985; Smith and Cutlip, 1988.. On retesting two months after parturition, all the dams of these kids were positive. Six had tested indeterminately once before, prior to mating. The use of other test routines, such as testing the females earlier in pregnancy, might have led to earlier detection of antibodies. On the other hand, seroconversion induced by the stress of late pregnancy and parturition should not be ruled out. The testing for maternal antibodies in all kids early in life allows carriers of CAEV to be identified and culled at an early stage. It seems that total segregation of seronegative and seropositive groups, even at pasture, is of vital importance for the establishment of herds free from CAEV infection. Before final conclusions are drawn regarding the possibility of reducing CAEV prevalence in a herd with less strict segregation, further investigations are needed. Even with a strict control scheme, considerable reduction in the prevalence of virus-positive animals rather than complete eradication is probably the most realistic aim for the first two or three years. To be declared free of the infection, a previously infected herd should test negatively on at least three or four occasions at intervals of six to twelve months ŽEllis, 1988; Halgaard, 1988..
Acknowledgements We are grateful to the herd owners for allowing us to use their dairy goat herds in this study and for their help and continued interest. Thanks are due also to Dr. G. Gunnes, Department of Pathology, Norwegian College of Veterinary Medicine, for pathological examinations. We are indebted to Dr. E. Skjerve, Norwegian College of Veterinary Medicine for valuable advice, constructive criticism and correction of the manuscript.
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