Though the does and cows were not observed in physical contact, feed and water sources as well as lounging areas were shared between species. Of the nine live fawns born, all three singlet fawns were born PI virus positive, antibody negative , and all twin fawns cleared the infection and were born virus negative and seropositive Passler and Walz, Another North American cervid known to have the potential for persistent infection is mule deer Odocoileus hemionus. Thus, in a routine survey of tissues from hunter-harvested deer in Colorado for chronic wasting disease, BVDV was added to the testing protocol.
The animal showed no signs of illness, though the virus was identified in both the submitted ear and lymph node, and these findings are suggestive of persistent infection. The source of infection in this case was unknown, but is assumed to be spillover from cattle Duncan et al. Two of these seroconverted on subsequent sampling dates, but one young female remained viremic over time and was determined to be persistently affected. The PI animal eventually lost condition and died following an episode of febrile illness Vilcek et al.
Presumably domestic cattle served as the primary viral source. There are multiple reports of PI domestic species including new world camelids. Two PI crias were identified on a Pennsylvania breeding farm. Both presented for stunting and immunosuppression. The first affected cria was determined to be PI following repeated virus isolation in the absence of seroconversion. Euthanasia was elected to protect the breeding herd.
The second cria was euthanized after initial virus isolation at 6 weeks of age. On the same day, blood was submitted from the 15 adults on the property. A second report in alpacas chronicled a farm in eastern Ontario, Canada, where a chronically ill cria was evaluated at necropsy.
Upon reviewing the herd records, it was discovered that the cria's dam had traveled to four different breeding farms during her pregnancy, two of which had experienced numerous abortions and stillbirths. The Ontario herd experienced vague herd illness following the birth of the PI cria, characterized by anorexia, lethargy, and several abortions all of which were positive for BVDV. Out of 20 animals tested, 17 were positive for antibody to both BVDV strains. Only one of these crias was positive, euthanasia was elected.
The euthanized cria was positive for virus at necropsy using IHC Carman et al. Bovine viral diarrhea virus infection has also been reported in domestic sheep.
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The lambs that were born alive were positive for BVDV at birth and were negative for antibody after maternal antibody waned, which confirms PI status. Of the ewes infected at 65—70 days gestation, the death loss was Ewes infected with BVDV at — days of gestation gave birth to healthy virus negative, antibody positive lambs Scherer et al. Domestic swine can also become PI. Of the 13 pigs in the litter, seven died within 2—4 weeks of birth. Three of the remaining six were euthanized due to wasting and deep ulcers of the jaw and extremities.
Three of the remaining pigs survived until slaughter, including one PI boar, one seropositive boar, and one intersex pig. The PI boar remained viremic and immunotolerant until slaughter at 26 weeks of age. The viremic boar shed the virus in oropharyngeal fluid, urine, and semen and was leukopenic from 3 months onward Terpstra and Wensvoort, Since persistent infection can occur in domestic swine, feral swine can potentially become sources for disease transmission. The trace back identified 10 PI animals in two generations all of which could be traced back to a single PI female.
All other animals in contact with these PI mousedeer were found to be antibody positive and virus negative. The PI mousedeer was asymptomatic throughout the testing, but was viremic over multiple testing dates without evidence of seroconversion Uttenthal et al. This is the first report of the existence of mature PI animals, other than cattle, that were able to reproduce and produce PI offspring. Domestic goats can be infected with BVDV with reproductive disease as the most common disease manifestation.
PI cattle are considered the main source of infection, as this occurs under natural and experimental conditions.
Persistent bovine viral diarrhea virus (BVDV) infection in cattle herds
Another similar study with pregnant goats exposed to PI heifers with BVDV-2a resulted in abortion and stillbirth but not PI kids suggesting that the development of PI kids is relatively rare Broaddus et al. There is also evidence for BVDV infection in wild goats. Mountain goats in Nevada experienced an all age bacterial bronchopneumonia die off during the winter of — and three sampled mountain goats from this outbreak were seropositive for BVDV-1 and BVDV-2 on virus neutralization.
In , one mountain goat kid from the same area also died of bronchopneumonia with suppurative mural enteritis and suppurative serositis suggesting secondary septicemia. Necrotizing mesenteric lymphadenitis prompted testing for BVDV infection. To the authors' knowledge, mountain goats are the only wild goat species with definitive evidence of persistent pestivirus infection.
Two captive mountain goats from a zoological collection in Idaho were proven to be infected with BVDV While one goat had evidence of systemic BVDV-2 infection by IHC, virus isolation, and PCR with sequencing, the histological lesions indicated that suppurative enteritis with bacterial septicemia was a major factor in the cause of death.
Longitudinal evidence of prolonged BVDV infection was not possible in this goat, but persistent infection was considered probable due to prolonged seronegativity and widespread virus distribution without associated necrosis. The second goat from the same premises had suppurative bronchopneumonia and suppurative hepatitis indicating bacterial septicemia was again the likely cause of death.
This second goat had repeated longitudinal evidence of BVDV-2 infection by virus isolation and PCR with sequencing yet was seronegative over time providing definitive proof of persistent infection Nelson et al. The epidemiology and spectrum of disease syndromes due to bovine viral diarrhea infection in mountain goats is currently not well understood. Serosurvey of the Idaho zoological collection cohorts including domestic sheep, domestic goats, mule deer, and whitetail deer in the same pen suggested there may have been transmission between these wild caught mountain goats and the other ruminants, but the origin of this virus was not determined Nelson et al.
Evidence of BVDV infection in domestic cattle and free-living bighorn sheep, mountain goats, and mule deer sharing the same range in Nevada demonstrated interspecies transmission in wild settings Wolff et al. Since pestivirus infection causes immunosuppression with increased susceptibility to bacterial infection, BVDV likely played this indirect role in these mountain goats with septicemia. BVDV infection in mountain goats likely affects reproductive rates as seen in domestic goats and may cause diarrhea as seen in Korean goats Kim et al.
The difficulty of access and limited numbers of these high mountain dwellers will limit further investigations into the incidence, epidemiology, and full characterization of natural disease. Control and prevention of BVDV is based on three elements: elimination of PI animals, biosecurity, and early detection. Many Scandinavian countries are considered BVDV-free following widespread eradication programs in the s based on these elements Stahl and Alenius, The methods used to eradicate the disease included identification of positive herds, implementation of quarantine protocols, elimination through rigorous test and cull strategies, and prevention of BVDV introduction into non-infected herds.
Considering that PI animals provide a significant source for virus transmission, the key factor in BVDV control is identification and elimination of PIs. The Swedish eradication program identified PIs by performing serology on virus positive herds to find seronegative animals. Once seronegative animals were detected, virus isolation was performed. If an animal was found to be seronegative and virus positive, it was declared a PI and was eliminated from the herd Stahl and Alenius, Once BVDV is eliminated from the herd, rigorous biosecurity programs should be established to prevent re-introduction of the virus.
All incoming animals, including purchased calves, replacement heifers, cows, and bulls, should be tested using one of the methods described above. Three week quarantine practices should also be implemented before introducing newly acquired animals into a disease free herd Walz et al. Semen and embryos being used in breeding programs should also be considered as a source for herd infection and only be acquired from BVDV-free sources.
Vaccination may have a role in preventing disease, but efficacy in field conditions is not well documented and practicality is likely limited. Vaccination in domestic livestock is recommended in cases where the risk of re-introduction is high, but should always be used in conjunction with other control methods Stahl and Alenius, When a vaccination program is considered, it is important to remember that antibodies associated with vaccination may complicate diagnosis of PI animals.
The goal of vaccination is to limit transmission and severity of clinical disease in affected animals, rather than true prevention of BVDV infection. Vaccine use is commonly targeted to prevent the development of PI offspring Walz et al. In a study, seroprevalence of BVDV in cattle was compared to that of white-tailed deer in the state of New York Kirchgessner et al. Seroprevalence in cattle herds was found to closely mirror seroprevalence in hunter-harvested white-tailed deer. This may also be true of the other species discussed in this paper.
In many of the reports white tail deer, alpaca , the PI animals had known exposure to BVDV positive herds during their gestation. Reduced contact between cattle and wildlife can be achieved with non-lethal methods such as high or electrified fencing, livestock protection dogs, enclosing stored feedstuffs, reduction of wasted feed, and elimination of baiting and winter feeding practices Van Campen and Rhyan, ; VerCauteren et al. Producers with multiple domestic species on the same premises should be aware of the potential for disease spread among their animals. Even if the species are not in direct contact, these PI animals increase the potential for BVDV spread through environmental contamination or use of shared equipment.
Biosecurity measures should be implemented for control of disease on mixed-species farms, including decontamination of shared equipment, separation of shared feed or water sources, and reduction of disease spread by personnel tending to multiple species change clothes, footbaths, hand washing between species.
Care should be taken to isolate animals returning from mixed-species exhibitions fairs, rodeos, shows upon their return to the breeding herd. Though it is an uncommon disease of wildlife, BVDV should be viewed as a threat to the health of wildlife populations and measures should be considered to reduce transmission of the disease within the ecosystem.
For mountain goats, remote high mountain habitat has likely historically minimized BVDV transmission, though as this habitat is increasingly encroached upon by domestic livestock grazing and human development, opportunities for disease transmission are likely increasing over time. Since multiple wildlife species have been shown to be capable of persistent and transient infection, interactions with other wild species such as deer and bighorn sheep also increase the opportunity for disease transmission.
Assuming mountain goats are affected similar to domestic goats, BVDV infection likely causes significant reductions in the reproductive rate which could pose additional challenges for this wild species. Increased surveillance is an important factor in the control and understanding of BVDV infection in wildlife. Implementation of BVDV testing on hunter-harvested samples may be a good way to track disease progression within an ecosystem. It would be a sensitive, specific, and inexpensive way to monitor disease prevalence. PCR could also be performed on pooled samples, as is commonly preferred for diagnosis in cattle herds.
Vaccination may eventually become an important consideration for control of BVDV in areas with high disease prevalence in wildlife species. The implications of BVDV in zoological collections are similar to those in the domestic livestock industry. Increased biosecurity practices should be implemented to prevent fomite transmission of the disease between species. Quarantine and testing of new arrivals is also an important consideration for disease control captive collections.
Disease transmission should be a consideration when mixed species exhibits are being planned and the animals should be tested accordingly. Bovine viral diarrhea virus is a disease with significant economic and health implications for positive herds. It causes economic losses to producers through loss of production, increased susceptibility to infection, and reproductive insufficiency. Considerable effort has gone into control and eradication of the disease through identification and elimination of PI cattle, but because wildlife and non-bovid have the potential for persistent infection, they must also be considered as an integral part of any eradication effort.
Additionally, increased monitoring is an essential part of disease control and identification of new host species. Surveillance for BVDV in wild animal populations is increasing in areas with high seroprevalence and will likely continue to improve. Cattle producers, wildlife conservationists, and zoological staff members all need to consider the role of nonstandard BVDV hosts when attempting to control or eliminate the disease within a population.
DN is the first author and had the greatest contribution to the research, editing, and writing of this paper.
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JD is the second author and significantly contributed to the research and writing of this paper. PW is the third author and significantly contributed to the research and writing of this paper. JE is the final author and mentored and editing this paper with some primary writing contribution. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Ames, T. Goyal and J.
Bachofen, C. Persistent infections after natural transmission of bovine viral diarrhoea virus from cattle to goats and among goats. BMC Vet. Belknap, E.
Bovine viral diarrhea virus in New World camelids. Botner, A. Virus survival in slurry: analysis of the stability of foot-and-mouth disease, classical swine fever, bovine viral diarrhoea and swine influenza viruses. Broaddus, C. Transmission of bovine viral diarrhea virus to adult goats from persistently infected cattle. Brownlie, J. Bovine viral diarrhea virus—strategic decisions for diagnosis and control. Pract 22, — Carman, S.
Bovine Viral Diarrhea Virus: Diagnosis, Management, and Control. India ,Ed. :1
Bovine viral diarrhea virus in alpaca: abortion and persistent infection. Chamorro, M. Evaluation of transmission of bovine viral diarrhea virus BVDV between persistently infected and naive cattle by the horn fly Haematobia irritans. DeFilippis, V. Hurst New York: Academic Press , — CrossRef Full Text. Duncan, C.
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