Abstract
Bovine leukemia virus (BLV) is the causative agent of enzootic bovine leukosis (EBL). Although efficient eradication programs have been successfully implemented in most European countries and Oceania, BLV infection rates are still high worldwide. BLV naturally infects cattle, inducing a persistent infection with diverse clinical outcomes. The virus infects lymphocytes and integrates a DNA intermediate as a provirus into the genome of the cells. Therefore, exposure to biological fluids contaminated with infected lymphocytes potentially spreads the virus. Vertical transmission may occur in utero or during delivery, and about 10% of calves born to BLV-infected dams are already infected at birth. Most frequently, transmission from dams to their offspring occurs through the ingestion of infected colostrum or milk. Therefore, although EBL is not a disease specific to the neonatal period, during this period the calves are at special risk of becoming infected, especially in dairy farms, where they ingest colostrum and/or raw milk either naturally or artificially. Calves infected during the first week of life could play an active role in early propagation of BLV to susceptible animals. This review discusses the main factors that contribute to neonatal BLV infection in dairy herds, as well as different approaches and management practices that could be implemented to reduce the risk of BLV transmission during this period, aiming to decrease BLV infection in dairy herds.
Enzootic bovine leukosis
Enzootic bovine leukosis (EBL), also called bovine lymphosarcoma or bovine leukemia, is an infectious disease naturally occurring in cattle. The viral etiology of this lymphoproliferative disease was first described in 1969, when Miller and colleagues discovered that lymphocytes of cows with persistent lymphocytosis produced viral particles that were visible by electron microscopy after in vitro culture (1). The etiological agent of EBL is bovine leukemia virus (BLV), an oncogenic retrovirus member of the genus Deltaretrovirus (family Retroviridae). This genus also includes the Human T-lymphotropic viruses (HTLV) 1, 2, and 3, and the Simian T-lymphotropic viruses (STLV) 1, 2, and 3 (2). Once BLV infects a cell, it integrates a DNA intermediate as a provirus, both randomly and permanently, into the genome of the host cell. This virus preferentially infects B cells (3). In cattle, the polyclonal expansion of B cells, which is characteristic of animals with persistent lymphocytosis, occurs almost exclusively within the CD5+ IgM+ B cell subset (4, 5) and these B cells are also the primary target for BLV proviral integration (5, 6). However, other cell types like CD4+ T cells, CD8+ T cells, Ī³/Ī“ T cells, monocytes and granulocytes can also be infected by BLV (3, 7ā10). The free virus is rarely detected in vivo, and it is believed that it appears only during the acute stage of infection, before the development of neutralizing antibodies (11).
Infection with deltaretroviruses is characterized by a long incubation period and a variety of clinical outcomes. Almost 70% of BLV-infected animals are asymptomatic carriers of the virus and are referred to as aleukemic. Since these animals do not present clinical and/or hematological manifestations of the disease, they can be identified only by the presence either of specific antibodies or of integrated viral DNA (provirus) (12). Approximately 30% of infected cattle develop a non-malignant proliferation of untransformed B-lymphocytes, termed persistent lymphocytosis, a condition characterized by an increase in the number of peripheral blood circulating B-lymphocytes (above 10,000/mm3) (13). During persistent lymphocytosis, animals may suffer from immunological dysregulation, as evidenced by opportunistic infections (e.g., mastitis) (14ā17). Less than 5% of BLV-infected animals develop malignant B-cell lymphosarcoma, which occurs between 1 and 8 years after infection. This local proliferation of B cells can occur within different organs and tissues like the spleen, liver, heart, abomasum, uterus, lymph nodes, and spinal cord (12, 13, 18, 19). Although clinical signs associated with lymphosarcoma are highly variable, as they depend on the affected organ(s), these tumors may lead to a series of defects that are finally incompatible with the survival of the animals.
Although cattle are the predominant natural hosts for BLV infection, water buffalo, zebu, yak and alpaca can also become naturally infected (20ā23). Although experimental infection has been studied in goats (24), rabbits (25), rats (26, 27), and chickens (28), the most consistent model to study BLV infection seems to be sheep. In this model, the complete onset of the disease occurs in a relatively short period of time (approximately 18 months) and the frequency of leukemia/lymphoma is high (close to 100%) (29, 30).
BLV infection is widely disseminated throughout the world and is listed by the World Organization for Animal Health (OIE) as a disease of importance to international trade (31). Several countries have established eradication programs and control measures based on ātest and eliminateā and ātest and segregateā approaches, that have been very successful in Western Europe (32ā34), New Zealand (35), and Western Australia (36). However, in several nations of Eastern Europe, including Ukraine, Bulgaria and Croatia, the disease is still present. In addition, high levels of BLV prevalence are still documented in North and South America, and some Middle Eastern and Southeast Asian nations. The updated information on the incidence and distribution of EBL worldwide has been recently reviewed by Polat et al. (37). Argentina, where the disease is endemic, is the South American country with the highest BLV prevalence, with an individual prevalence of 80% in dairy farms of the main productive areas of the country (38).
Different techniques have been developed to diagnose BLV infection. These can be assigned into two main groups: those consisting of antibody-based serological tests and those detecting the proviral genome by PCR. Antibody-based serological tests, which include agar gel immunodiffusion (AGID) and the enzyme linked immunosorbent assay (ELISA), are the most common and reliable way to diagnose BLV infection. AGID is recognized as the official import/export test (31), but is less sensitive than ELISA, which is commonly used for routine diagnosis. Antibody-based serological tests can use different types of antibodies such as antibodies against the viral envelope glycoprotein (gp51) or antibodies against the core polypeptide (p24). Generally, the former has higher titer and appear earlier than the latter. As mentioned above, BLV infection can also be diagnosed by techniques that detect the proviral genome. These techniques include standard PCR, nested PCR or real-time quantitative PCR (qPCR) (39ā43). The advantages of the PCR-based methods are that they allow detecting BLV infection several weeks before it is possible to detect antibodies and that they allow differentiating positive from negative calves in the presence of maternal antibodies.
Transmission
BLV is transmitted mostly through the transfer of infected cells. Biological fluids like blood, colostrum, and milk are potential sources for the transmission of BLV (44ā46), and their infectivity depends on the lymphocyte count of the fluid (46).
Horizontal transmission of BLV occurs mainly associated with iatrogenic procedures, such as dehorning, tattooing, vaccination, castration, and rectal tact (46). The implementation of management practices to minimize exposure of the animals to BLV has proved to reduce overall herd prevalence in some studies (33, 47, 48). However, dairy producers in Argentina that have applied corrective measures to prevent the iatrogenic blood contact have not been able to reduce the BLV prevalence rate in the herd, which suggests that other ways of transmission are playing a key role under natural conditions (49). Transmission by biting insects such as Tabanid flies has also been documented (50), but its relative importance under natural conditions is uncertain. Vertical transmission includes perinatal and postnatal infection. Perinatal infection may occur either in utero or during delivery. In utero infections under field conditions have been demonstrated by testing newborn calves before colostrum feeding, and proved to be between 4 and 18% (51ā55). This natural in utero BLV infection has been found to be independent of the breed (52, 53), dam age, dam parity, and time of BLV infection in the dam (42), but has been associated with maternal lymphocytosis (54, 55), malignant lymphoma (54), and maternal viral loads (52). Experimental infection of cows during pregnancy has also been found to result in seropositive calves at birth, indicating that calves had been infected in utero (56). Recently, Sajiki et al. (57) reported the direct evidence of intrauterine infection in two pregnant dams with a high proviral load (PVL). These authors detected BLV DNA in both of the newborns delivered via cesarean section by nested PCR, and found that the amplified BLV-env gene sequences from the dams and the newborns were completely identical. These authors also detected BLV provirus in placental and cord blood, but not in amniotic fluid, suggesting that placental and cord blood might be routes of vertical BLV transmission. (52) investigated the frequency of perinatal BLV infection in field conditions in Japan and observed that 10 out of 129 (7.7%) calves born from BLV-infected cows were infected in the birth canal, and 14 (10.8%) were infected in utero. In addition, they found no correlation between the rate of birth canal infections and the assistance during parturition or the number of births per dam (52).
Postnatal vertical infection from dams to calves occurs through consumption of infected colostrum or milk. Nowadays, in most dairy farms, calves are fed with colostrum and milk during the first 60 days of life. Colostrum can come directly from their dams or be administered by nipple bottle or oroesophageal tubing. During this period, calves are also fed with bulk-tank milk and balanced feed and then they are moved to pastures occupied exclusively by cattle of similar age and weight. Several authors have described the presence of provirus and infectious virus both in milk and colostrum from most BLV-infected cows and in bulk tank milk (58ā60). Thus, both milk and colostrum are sources of infection to neonatal calves. However, milk and colostrum can also contain BLV specific antibodies (58, 59). Therefore, the potential protective or infective role of colostrum and milk in natural transmission of BLV is still not clear and has been the subject of multiple studies that have suggested contrasting roles.
The protective role of colostrum has been reported by different groups. Van der Maaten et al., for example, performed an experimental study with newborn calves to which they gave 106 to 109 BLV-infected lymphocytes in either colostrum free of BLV specific antibodies or colostrum from BLV-infected cows. Their results revealed that BLV antibody-containing colostrum protected calves from infection (61). Lassauzet et al. found similar results in a 3-year prospective study in a dairy herd where calves were housed in individual hutches. They observed that the number of calves that had not received BLV colostral antibodies and had become infected was significantly higher than that of calves that had received BLV colostral antibodies (62). Similarly, Nagy and colleagues reported that the incidence of BLV infection was higher in colostrum-deprived calves and suggested that the administration of BLV-positive colostrum reduces the risk of infection compared with colostrum deprivation (63).
The infectivity of colostrum and milk has been experimentally demonstrated in sheep inoculated or oral administered with these secretions, and subsequently examined for the development of infection (64, 65). Milk-borne transmission has also been reported in calves born to BLV-negative dams that had been fed milk from BLV-infected cows (66), as well as in calves fed on colostrum and milk from their BLV-positive dams since birth and then reared in complete or partial isolation from infected cattle (45). Another study performed in dairy herds showed that almost all new BLV infections occurred in calves born to uninfected dams. However, when feeding with bulk milk was stopped and calves began to be fed only milk from BLV-free cows, no new infections occurred in the following 2.5 years (67).
Different studies performed by our group in dairy herds of Argentina have revealed that the presence of provirus in colostrum is significantly correlated with the blood PVL (60, 68). Our studies have also shown that the colostrum of individual cows shows different provirus/antibody profiles, and that consumption of colostrum with infected cells and a poor content of antibodies could play a critical role in BLV propagation during young age (59, 60). In addition, when analyzing the relationship between the level of BLV antibodies and the PVL in blood and milk of lactating cows under natural conditions, we found a negative correlation, suggesting that the consumption of raw milk containing provirus or free virus particles and low levels of antibodies could favor BLV transmission to calves (58). All these findings suggest that the feeding management of young calves could greatly influence the risk of milk-borne transmission.
Importance of BLV infection during the neonatal period
Although EBL is not considered an infectious disease causing abortions or neonatal mortality, special attention should be given to neonatal calves in dairy herds, especially in those with high prevalence of BLV infection. Epidemiological studies carried out by our group in dairy herds in Argentina have shown that calves infected during the first week of life play an active role in early BLV propagation to non-infective calves, since their PVL increases during the first 12 months and remains high for years (68). Since high levels of BLV infection are associated with higher probability of transmission (69), the presence of animals with high PVL is epidemiologically dangerous. This could be a reason for the high incidence observed in Argentinean dairy herds before first parturition, when approximately half of pregnant heifers are already infected, and between 20 and 44% of them have high PVL (60, 70). Culling the animals with high PVL might be a strategy for reducing overall incidence in the herds, but this would be economically feasible only in herds with low prevalence of high PVL cows.
Peak rates tend to occur in the interval in which heifers are being bred, calving, and entering the milking herd, a time of intensive human intervention, closer physical contact and exposure to older cows with higher BLV infection rates (46, 49). However, it has also been reported that BLV infection can occur during the first 2 years of life, when young animals are still not in contact with adult cows. At this stage, the only potential sources of virus are their own mothers, bulk tank milk, and calves that were born infected (8ā11% in dairy herds of Argentina) (60, 70).
Preventive strategies to reduce perinatal transmission
Considering all the above, it is clear that management strategies focused on reducing BLV transmission during the perinatal period could be of great help to diminish the prevalence of infection in dairy herds. Different strategies should be implemented at specific times from parturition.
Preventive strategies during parturition
As previously mentioned, the frequency of in utero transmission is significantly correlated with the maternal viral load. Therefore, selecting breeding cows according to their viral loads could reduce the number of intrauterine infections. In addition, considering that BLV can also be transmitted through the birth canal, cesarean section in dams with high PVL should be aseptically conducted to minimize the risk of BLV transmission to newborn calves.
Ideally, heifers should be separated from adult cows with high rates of infection before the calving process and newborn calves should be removed from their dams at birth and placed in a clean dry area to be fed good-quality colostrum during their first 12 h of life. Additionally, calves born infected should be identified as soon as possible and segregated from the herd. Some of these management practices are included in control programmes based on ātest and segregate,ā and have been useful to decrease prevalence or even achieve eradication of the disease (33, 47, 71).
Preventive strategies when feeding calves with colostrum and milk
Colostrum is the main source of nutrients and maternal immunoglobulins for the newborn calf. The timely feeding of high-quality and adequate volumes of uncontaminated colostrum is a key factor, essential to the health and survival of neonatal dairy calves (72). Since the incidence of BLV infection in dairy herds is usually high, natural suckling from dams should be avoided and replaced by artificial feeding with either a high-quality colostrum bank or colostrum replacer. The high-quality colostrum bank could be obtained as pooled colostrum from BLV-negative dams. However, in dairy herds with high rates of infection, this would be almost impossible to conceive. In this case, a colostrum bank should be created from dams with high levels of BLV-specific antibodies (59). Alternatively, the colostrum bank could be pre-treated to render it non-infectious. Kanno et al. reported that a useful means of inactivating the infectivity of BLV is by freezing the colostrum. Thus, these authors used frozen-thawed or untreated colostrum from a BLV-infected cow, and then isolated the leukocytes from these colostra to use them to inoculate sheep. The sheep inoculated intraperitoneally with the leukocytes from the frozen-thawed colostrum remained BLV-negative until 9 weeks after inoculation, whereas the sheep inoculated with the cells of the untreated colostrum became infected with BLV at 3 weeks after inoculation (73). However, a disadvantage of using frozen colostrum is that it requires large amounts of refrigerated storage space and considerable time for thawing and warming prior to feeding.
Currently there are several commercially available colostrum supplements or replacers made from dried bovine colostrum. Colostrum may be dried by means of different methods such as freeze-drying, microwave vacuum evaporation, and spray-drying. Comparison of these methods has shown that spray-drying is the most cost-effective and allows obtaining a dried colostrum in which immunoglobulin quantity and function are preserved (74). Moreover, our group has recently reported that the experimental spray-drying process is effective in inactivating infectious BLV in colostrum. In that study, we inoculated susceptible lambs with treated (spry-dried) or untreated colostrum spiked with BLV-infected cells and found that lambs that had received the untreated colostrum showed evidence of infection 60 days post-inoculation (75).
Pasteurization of milk is another feasible strategy to ensure the inactivation of BLV without significantly altering the concentration of immunoglobulins or their physiological activities (75ā77). It has been reported that sheep inoculated with milk experimentally contaminated with BLV and treated by a simulated high-temperature short-time (HT ST) pasteurization procedure do not become infected or develop tumors (75, 77). In addition, HT ST pasteurization has the additional benefit of helping to limit the spread of Johne's disease and other pathogens (78). All these findings suggest that performing pre-treatments to both colostrum and bulk tank milk before they are administered to calves might help to prevent early BLV infection.
Preventive strategies in raising calves
In most dairy herds, raising calves are generally fed with bulk tank milk (with approximately 10ā15% of their body weight daily), for 60 days. Considering a dairy herd with high prevalence of BLV infection, calves might be receiving a constant supply of virus during that period. Supplementation of the milk with BLV-specific antibodies able to neutralize the virus prior to intake, which would complement the neutralizing capacity provided by natural antibodies already present, could be an interesting approach. In this regard, a promising and practical strategy that has been explored since the early 1990s is the supplementation of the milk diet of calves with specific antibodies from egg yolk (IgY) (79ā81). This IgY is deposited in egg yolk in large quantities, making chickens an ideal source of specific polyclonal antibodies (82). The supplementation of newborn calves' diets with egg yolk powder enriched in specific IgY antibodies has been successfully used in preventive and therapeutic treatments against bovine rotavirus diarrhea (79, 80, 83, 84). Thus, our group is currently evaluating the use of specific IgY antibodies as a milk supplement to achieve passive protection of newborn calves against BLV in field conditions. For this purpose, non-infected newborn calves (tested negative for BLV by nested PCR) are being fed with non-pasteurized bulk tank milk, supplemented with egg powder enriched with BLV-specific IgY during their first 60 days of life. This study would help to know the real risk of milk-borne transmission and the potential use of IgY technology to prevent this route of infection.
Final conclusions
The greatest advance in dairy health in the last years has been the shift to disease prevention, rather than treatment (85). In Argentina and many other countries worldwide, BLV infection is endemic, with high prevalence in dairy farms. Thus, several control measures should be implemented to control the dissemination of the disease until a treatment or vaccine become available. Experimental evidence has indicated that BLV infection can easily propagate during the perinatal period when young animals are still not in contact with infected adult cows. Therefore, different approaches should be simultaneously implemented to effectively interrupt BLV transmission to calves and finally have herds with decreased levels of BLV infection.
Statements
Author contributions
VR and IA conceived the idea of the review. All authors wrote sections of the manuscript. The submitted version of the manuscript was read, edited, and approved by all authors.
Funding
This work was supported by grants PICT-2013-029 from Agencia Nacional de PromociĆ³n CientĆfica y TecnolĆ³gica, Argentina and PNSA 115054 from INTA.
Conflict of interest
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. The handling Editor declared a shared affiliation with the authors.
References
1.
MillerJMillerLOlsonCGilletteK. Virus-like particles in phytohemagglutinin-stimulated lymphocyte cultures with reference to bovine lymphosarcoma. J Natl Cancer Inst. (1969) 43:1297ā305.
2.
ICTV. International Committee on Taxonomy of Viruses (ICTV). Available online at: https://talk.ictvonline.org/taxonomy
3.
SchwartzIBensaidAPolackBPerrinBBerthelemyMLevyD. In vivo leukocyte tropism of bovine leukemia virus in sheep and cattle. J Virol. (1994) 68:4589ā96.
4.
DepelchinALetessonJJLostrie-TrussartNMammerickxMPortetelleDBurnyA. Bovine leukemia virus (BLV)-infected B-cells express a marker similar to the CD5 T cell marker. Immunol Lett. (1989) 20:69ā76. 10.1016/0165-2478(89)90071-0
5.
MeiromRMossSBrennerJ. Bovine leukemia virus-gp5 1 antigen expression is associated with CDS and IgM markers on infected lymphocytes. Vet Immunol Immunopathol. (1997) 59:113ā9. 10.1016/S0165-2427(97)00056-1
6.
PaneiCJTakeshimaSOmoriTNunoyaTDavisWCIshizakiHet al. Estimation of bovine leukemia virus (BLV) proviral load harbored by lymphocyte subpopulations in BLV-infected cattle at the subclinical stage of enzootic bovine leucosis using BLV-CoCoMo-qPCR. BMC Vet Res. (2013) 9:95. 10.1186/1746-6148-9-95
7.
WilliamsDLBartaOAmborskiGF. Molecular studies of T-lymphocytes from cattle infected with bovine leukemia virus. Vet Immunol Immunopathol. (1988) 19:307ā23. 10.1016/0165-2427(88)90117-1
8.
StottMLThurmondMCDunnSJOsburnBIStottJL. Integrated bovine leukosis proviral DNA in T helper and T cytotoxic/suppressor lymphocytes. J Gen Virol. (1991) 72(Pt 2):307ā15.
9.
MirskyMLOlmsteadCADaYLewinHA. The prevalence of proviral bovine leukemia virus in peripheral blood mononuclear cells at two subclinical stages of infection. J Virol. (1996) 70:2178ā83.
10.
PaneiCTassaraFPĆ©rez AguirreburualdeMEcheverrĆaMGalosiCTorresAet al. Seroprevalencia de infecciĆ³n por el virus de leucosis bovina durante 2015 en rodeos de crĆa de la Zona Deprimida del RĆo Salado, provincia de Buenos Aires. Analecta Vet. (2017) 37:65ā68. 10.24215/15142590e005
11.
GuptaPKashmiriSVFerrerJF. Transcriptional control of the bovine leukemia virus genome: role and characterization of a non-immunoglobulin plasma protein from bovine leukemia virus-infected cattle. J Virol. (1984) 50:267ā70.
12.
KettmannRBurnyACallenbautIDroogmansLMammerickxMWillemsLet al. (ed). The Bovine Leukemia virus. In: LevyJ., editors. The Retroviridae, New York, NY: Plenum Press. p. 39ā81.
13.
FerrerJ. Bovine lymphosarcoma. Adv Vet Sci Comp Med. (1980) 24:1ā68.
14.
EmanuelsonUScherlingKPetterssonH. Relationships between herd bovine leukemia virus infection status and reproduction, disease incidence, and productivity in Swedish dairy herds. Prev Vet Med Elsevier Sci Publ BV (1992) 12:12ā131.
15.
SandevNKolevaMBinevRIlievaD. Influence of enzootic bovine leukosis virus upon the incidence of subclinical mastitis in cows at a different stage of infection. Vet Arh. (2004) 74:411ā6.
16.
FrieMCCoussensPM. Bovine leukemia virus: a major silent threat to proper immune responses in cattle. Vet Immunol Immunopathol. (2015) 163:103ā14. 10.1016/j.vetimm.2014.11.014
17.
BlagitzMGSouzaFNBatistaCFAzevedoLFFSanchezEMRDinizSAet al. Immunological implications of bovine leukemia virus infection. Res Vet Sci. (2017) 114:109ā16. 10.1016/j.rvsc.2017.03.012
18.
BurnyACleuterYKettmannRMammerickxMMarbaixGPortetelleDet al. Bovine leukaemia: facts and hypotheses derived from the study of an infectious cancer. Vet Microbiol Elsevier Sci Publ BV (1988) 17:197ā218.
19.
KettmannRCleuterYMammerickxMMeunier-RotivalMBernardiGBurnyAet al. Genomic integration of bovine leukemia provirus: comparison of persistent lymphocytosis with lymph node tumor form of enzootic. Proc Natl Acad Sci USA. (1980) 77:2577ā81. 10.1073/pnas.77.5.2577
20.
LeeLCScarrattWKBuehringGCSaundersGK. Bovine leukemia virus infection in a juvenile alpaca with multicentric lymphoma. Can Vet J. (2012) 53:283ā6.
21.
MeasSSetoJSugimotoCBakhshMRiazMSatoTet al. Infection of Bovine immunodeficiency virus and bovine leukemia virus in water buffalo and cattle populations in Pakistan. J Vet Med Sci. (2000) 62:329ā31. 10.1292/jvms.62.329
22.
MolnĆ”rEMolnĆ”rLGuedesVTde LimaES. Naturally occurring bovine leukosis virus in water buffalo (Bubalus bubalis) in Brazil. Vet Rec. (2000) 146:705ā6. 10.1136/vr.146.24.705
23.
MaJGZhengWBZhouDHQinSYYinMYZhuXQet al. First report of Bovine leukemia virus infection in Yaks (Bos mutus) in China. Biomed Res Int. (2016) 2016:9170167. 10.1155/2016/9170167
24.
OlsonCKajaRBurnyAKettmannR. Goat lymphosarcoma from bovine leukemia virus. J Natl Cancer Inst. (1981) 67:671ā5.
25.
WyattCRWingettDWhiteJSBuckCDKnowlesDReevesRet al. Persistent infection of rabbits with bovine leukemia virus associated with development of immune dysfunction. J Virol. (1989) 63:4498ā506.
26.
AltanerovaVPortetelleDKettmannRAltanerC. Infection of rats with bovine leukaemia virus: establishment of a virus-producing rat cell line. J Gen Virol. (1989) 70:1929ā32. 10.1099/0022-1317-70-7-1929
27.
Boris-LawrieKAltanerovaVAltanerCKucerovaLTeminHM. In vivo study of genetically simplified bovine leukemia virus derivatives that lack tax and rex. J Virol. (1997) 71:1514ā20.
28.
AltanerovaVBanJKettmannRAltanerC. Induction of leukemia in chicken by bovine leukemia virus due to insertional mutagenesis. Arch fĆ¼r Geschwulstforsch (1990) 60:89ā96.
29.
DjilaliSParodiAL. The BLV-induced leukemia-lymphosarcoma complex in sheep. Vet Immunol Immunopathol. (1989) 22:233ā44. 10.1016/0165-2427(89)90010-X
30.
DjilaliSParodiALLevyDCockerellGL. Development of leukemia and lymphosarcoma induced by bovine leukemia virus in sheep: a hematopathological study. Leukemia (1987) 1:777ā81.
31.
Enzootic Bovine Leukosis. In: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, Paris: OIE, 729ā38.
32.
NuotioLRusanenHSihvonenLNeuvonenE. Eradication of enzootic bovine leukosis from Finland. Prev Vet Med. (2003) 59:43ā9. 10.1016/S0167-5877(03)00057-6
33.
AcaiteJTamosiunasVLukauskasKMiliusJPieskusJ. The eradication experience of enzootic bovine leukosis from Lithuania. Prev Vet Med. (2007) 82:83ā9. 10.1016/j.prevetmed.2007.05.010
34.
KnapenKKerkhofsPMammerickxM. Eradication of enzootic bovine leukosis in Belgium: results of the mass detection on the national cattle population in 1989, 1990 and 1991. Ann Med Vet. (1993) 137:197ā201.
35.
ChethanondU-S. The Epidemiology of Enzootic Bovine Leukosis in Dairy Cattle in New Zealand (1999). Available online at: https://mro.massey.ac.nz/bitstream/handle/10179/5391/01_front.pdf?sequence=1&isAllowed=y
36.
RyanD. Eradication of Enzootic Bovine Leucosis in National Dairy Herd (2013). Available online at: http://www.flockandherd.net.au/cattle/reader/ebl-eradication-national-dairy-herd.html
37.
PolatMTakeshimaS-NAidaY. Epidemiology and genetic diversity of bovine leukemia virus. Virol J. (2017) 14:209. 10.1186/s12985-017-0876-4
38.
GutiĆ©rrezGCarignanoHAlvarezIMartĆnezCPortaNPolitzkiRet al. Bovine leukemia virus p24 antibodies reflect blood proviral load. BMC Vet Res. (2012) 8:187. 10.1186/1746-6148-8-187
39.
NaifHMBrandonRBDanielRCWLavinMF. Bovine leukaemia proviral DNA detection in cattle using the polymerase chain reaction. Vet Microbiol. (1990) 25:117ā29. 10.1016/0378-1135(90)90071-3
40.
NaifHMDanielRCCougleWGLavinMF. Early detection of bovine leukemia virus by using an enzyme-linked assay for polymerase chain reaction-amplified proviral DNA in experimentally infected cattle. J Clin Microbiol. (1992) 30:675ā9.
41.
KlintevallKBallagi-PordĆ”nyANƤslundKBelĆ”kS. Bovine leukaemia virus: rapid detection of proviral DNA by nested PCR in blood and organs of experimentally infected calves. Vet Microbiol. (1994) 42:191ā204. 10.1016/0378-1135(94)90018-3
42.
BrymPRuÅÄAKaminskiS. Evaluation of reference genes for qRT-PCR gene expression studies in whole blood samples from healthy and leukemia-virus infected cattle. Vet Immunol Immunopathol. (2013) 153:302ā7. 10.1016/j.vetimm.2013.03.004
43.
JimbaMTakeshimaS-NMurakamiHKoharaJKobayashiNMatsuhashiTet al. BLV-CoCoMo-qPCR: a useful tool for evaluating bovine leukemia virus infection status. BMC Vet Res. (2012) 8:167. 10.1186/1746-6148-8-167
44.
EvermannJFDiGiacomoRFFerrerJFParishSM. Transmission of bovine leukosis virus by blood inoculation. Am J Vet Res. (1986) 47:1885ā7.
45.
FerrerJFPiperCE. Role of colostrum and milk in the natural transmission of the bovine leukemia virus. Cancer Res. (1981) 41:4906ā9.
46.
HopkinsSGDiGiacomoRF. Natural transmission of bovine leukemia virus in dairy and beef cattle. Vet Clin North Am Food Anim Pract. (1997) 13:107ā28. 10.1016/S0749-0720(15)30367-4
47.
SprecherDJPelzerKDLessardP. Possible effect of altered management practices on seroprevalence of bovine leukemia virus in heifers of a dairy herd with history of high prevalence of infection. J Am Vet Med Assoc. (1991) 199:584ā8.
48.
RuppannerRBehymerDEPaulSMillerJMTheilenGH. A strategy for control of bovine leukemia virus infection: test and corrective management. Can Vet J. (1983) 24:192ā5.
49.
GutierrezGAlvarezIPolitzkiRLomoMRondelliFFondevilaNTronoK. Natural progression of Bovine Leukemia Virus infection in Argentinean dairy cattle. Vet Microbiol. (2011) 151:255ā63. 10.1016/j.vetmic.2011.03.035
50.
OhshimaKOkadaKNumakunaiSYoneyamaYSatoSTakahashiK. Evidence on horizontal transmission of bovine leukemia virus due to blood-sucking tabanid flies. Japanese. J Vet Sci. (1981) 43:79ā81. 10.1292/jvms1939.43.79
51.
PiperCEFerrerJFMarshakRR. Postnatal and prenatal transmission of the bovine leukemia virus under natural conditions. J Natl Cancer Inst. (1979) 62:165ā8.
52.
MekataHSekiguchiSKonnaiSKirinoYHonkawaKNonakaNet al. Evaluation of the natural perinatal transmission of bovine leukaemia virus. Vet Rec. (2014) 176:1ā4. 10.1136/vr.102464
53.
ThurmondMCCarterRLPuhrDMBurridgeMJMillerJMSchmerrMJVan der MaatenMJ. An epidemiological study of natural in utero infection with bovine leukemia virus. Can J Comp Med. (1983) 47:316ā9.
54.
LassauzetMLThurmondMCJohnsonWOStevensFPicansoJP. Factors associated with transmission of bovine leukemia virus by contact in cows on a California dairy. Am J Epidemiol. (1991) 133:164ā76. 10.1093/oxfordjournals.aje.a115855
55.
AgrestiAPontiWRocchiMMeneveriRMarozziACavalleriDet al. Use of polymerase chain reaction to diagnose bovine leukemia virus infection in calves at birth. Am J Vet Res. (1993) 54:373ā8.
56.
Van der MaatenMJMillerJMSchmerrMJ. In utero transmission of bovine leukemia virus. Am J Vet Res. (1981) 42:1052ā4.
57.
SajikiYKonnaiSNishimoriAOkagawaTMaekawaNGotoSet al. Intrauterine infection with bovine leukemia virus in pregnant dam with high viral load. J Vet Med Sci. (2017) 79:2036ā9. 10.1292/jvms.17-0391
58.
JaworskiJPPortaNGGutierrezGPolitzkiRPĆlvarezIGalarzaRet al. Short communication: relationship between the level of bovine leukemia virus antibody and provirus in blood and milk of cows from a naturally infected herd. J Dairy Sci. (2016) 99:5629ā34. 10.3168/jds.2015-10813
59.
GutiĆ©rrezGLomonacoMAlvarezIFernandezFTronoK. Characterization of colostrum from dams of BLV endemic dairy herds. Vet Microbiol. (2015) 177:366ā9. 10.1016/j.vetmic.2015.03.001
60.
LomonacoMAlvarezIMartĆnezCPortaNMerliniRCarignanoHet al. Epidemiological features of BLV natural infection. Retrovirology (2014) 11:P45. 10.1186/1742-4690-11-S1-P45
61.
Van Der MaatenMJMillerJMSchmerrMJ. Effect of colostral antibody on bovine leukemia virus infection of neonatal calves. Am J Vet Res. (1981) 42:1498ā500.
62.
LassauzetMLJohnsonWOThurmondMCStevensF. Protection of colostral antibodies against bovine leukemia virus infection in calves on a California dairy. Can J Vet Res. (1989) 53:424ā30.
63.
NagyDWTylerJWKleiboekerSB. Decreased periparturient transmission of bovine leukosis virus in colostrum-fed calves. J Vet Intern Med. (2007) 21:1104ā7. 10.1111/j.1939-1676.2007.tb03071.x
64.
MillerJMVan Der MaatenMJ. Infectivity tests of secretions and excretions from cattle infected with bovine leukemia virus. J Natl Cancer Inst. (1979) 62:425ā8.
65.
FerrerJFKenyonSJGuptaP. Milk of dairy cows frequently contains a leukemogenic virus. Science (1981) 213:1014ā6. 10.1126/science.6267692
66.
RomeroCHCruzGERALDOBRoweCA. Transmission of Bovine Leukaemia Virus in milk. Trop Anim Health Prod. (1981) 15:215ā8. 10.1007/BF02242060
67.
DimmockCKChungYSMacKenzieAR. Factors affecting the natural transmission of bovine leukaemia virus infection in Queensland dairy herds. Aust Vet J. (1991) 68:230ā3. 10.1111/j.1751-0813.1991.tb03213.x
68.
GutiƩrrezGAlvarezIMerliniRRondelliFTronoK. Dynamics of perinatal bovine leukemia virus infection. BMC Vet Res. (2014) 10:82. 10.1186/1746-6148-10-82
69.
MammerickxMPortetelleDde ClercqKBurnyA. Experimental transmission of enzootic bovine leukosis to cattle, sheep and goats: infectious doses of blood and incubation period of the disease. Leuk Res. (1987) 11:353ā8. 10.1016/0145-2126(87)90180-9
70.
MerliniRGutiĆ©rrezGAlvarezIJaworskiJPCarignanoHPoliMWillemsLTronoK. Bovine leukemia virus becomes established in dairy herds before the first lactation. Arch Virol. (2016) 161:3215ā7. 10.1007/s00705-016-2973-x
71.
SuhGHLeeJCLeeCYHurTYSonDSAhnBSet al. Establishment of a bovine leukemia virus-free dairy herd in Korea. J Vet Sci. (2005) 6:227ā30. Available online at: http://www.vetsci.org/journal/view.html?volume=6&number=3&spage=227
72.
WeaverDMTylerJWVanMetreDCHostetlerDEBarringtonGM. Passive transfer of colostral immunoglobulins in calves. J Vet Intern Med. (2000) 14:569ā77. 10.1111/j.1939-1676.2000.tb02278.x
73.
KannoTIshiharaRHatamaSOueYEdamatsuHKonnoYet al. Effect of freezing treatment on colostrum to prevent the transmission of bovine leukemia virus. J Vet Med Sci. (2014) 76:255ā7. 10.1292/jvms.13-0253
74.
ChelackBJMorleyPSHainesDM. Evaluation of methods for dehydration of bovine colostrum for total replacement of normal colostrum in calves. Can Vet J. (1993) 34:407ā12.
75.
LomonacoMSowulMMalacariDGutierrezGRuizVSuarez ArchillaGet al. Pasteurization and Spray-drying Heat Treatment are Effective to Inactivate Bovine Leukemia Virus in Milk and Colostrum. 18th International Conference on Human Retorovirology HTLV Relat Viruses (2017).
76.
RubinoMJDonhamKJ. Inactivation of bovine leukemia virus-infected lymphocytes in milk. Am J Vet Res. (1984) 45:1553ā6.
77.
BaumgartenerLOlsonCOnumaM. Effect of pasteurization and heat treatment on bovine leukemia virus. J Am Vet Med Assoc. (1976) 169:1189ā91.
78.
StabelJRLambertzA. Efficacy of pasteurization conditions for the inactivation of Mycobacterium avium subsp. paratuberculosis in milk. J Food Prot. (2004) 67:2719ā26. 10.4315/0362-028X-67.12.2719
79.
IkemoriYKurokiMPeraltaRCYokoyamaHKodamaY. Protection of neonatal calves against fatal enteric colibacillosis by administration of egg yolk powder from hens immunized with K99-piliated enterotoxigenic Escherichia coli. Am J Vet Res. (1992) 53:2005ā8.
80.
KurokiMOhtaMIkemoriYIcatloFCKobayashiCYokoyamaHet al. Field evaluation of chicken egg yolk immunoglobulins specific for bovine rotavirus in neonatal calves. Arch Virol. (1997) 142:843ā51. 10.1007/s007050050123
81.
MineYKovacs-NolanJ. Chicken egg yolk antibodies as therapeutics in enteric infectious disease: a review. J Med Food (2002) 5:159ā69. 10.1089/10966200260398198
82.
Kovacs-NolanJMineY. Egg yolk antibodies for passive immunity. Annu Rev Food Sci Technol. (2012) 3:163ā82. 10.1146/annurev-food-022811-101137
83.
VegaCBokMSaifLFernandezF. Egg yolk IgY antibodies: a therapeutic intervention against group a rotavirus in calves. Res Vet Sci. (2015) 103:1ā10. 10.1016/j.rvsc.2015.09.005
84.
VegaCBokMChacanaPSaifLFernandezFParreƱoV. Egg yolk IgY: protection against rotavirus induced diarrhea and modulatory effect on the systemic and mucosal antibody responses in newborn calves. Vet Immunol Immunopathol. (2011) 142:156ā69. 10.1016/j.vetimm.2011.05.003
85.
LeBlancSJLissemoreKDKeltonDFDuffieldTFLeslieKE. Major advances in disease prevention in dairy cattle. J Dairy Sci. (2006) 89:1267ā79. 10.3168/jds.S0022-0302(06)72195-6
Summary
Keywords
bovine leukemia virus, neonatal calves, colostrum, milk, dairy farms, proviral load
Citation
Ruiz V, Porta NG, LomĆ³naco M, Trono K and Alvarez I (2018) Bovine Leukemia Virus Infection in Neonatal Calves. Risk Factors and Control Measures. Front. Vet. Sci. 5:267. doi: 10.3389/fvets.2018.00267
Received
20 July 2018
Accepted
05 October 2018
Published
25 October 2018
Volume
5 - 2018
Edited by
Enrique Leopoldo Louge Uriarte, Instituto Nacional de TecnologĆa Agropecuaria (INTA), Argentina
Reviewed by
Paul M. Coussens, Michigan State University, United States; Giuseppe Bertoni, Institute of Virology and Immunology (IVI), Switzerland; Guillermina Laura Dolcini, National University of Central Buenos Aires, Argentina
Updates
Copyright
Ā© 2018 Ruiz, Porta, LomĆ³naco, Trono and Alvarez.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Vanesa Ruiz ruiz.vanesa@inta.gob.ar
This article was submitted to Veterinary Infectious Diseases, a section of the journal Frontiers in Veterinary Science
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