Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-22T13:25:23.212Z Has data issue: false hasContentIssue false

Mechanisms linking bovine viral diarrhea virus (BVDV) infection with infertility in cattle

Published online by Cambridge University Press:  09 September 2019

Chike F. Oguejiofor*
Affiliation:
Department of Veterinary Obstetrics and Reproductive Diseases, University of Nigeria, Nsukka410001, Nigeria Department of Pathobiology and Population Sciences, Royal Veterinary College, North Mymms, Hatfield, HertfordshireAL9 7TA, UK
Carole Thomas
Affiliation:
Department of Pathobiology and Population Sciences, Royal Veterinary College, North Mymms, Hatfield, HertfordshireAL9 7TA, UK
Zhangrui Cheng
Affiliation:
Department of Pathobiology and Population Sciences, Royal Veterinary College, North Mymms, Hatfield, HertfordshireAL9 7TA, UK
D. Claire Wathes
Affiliation:
Department of Pathobiology and Population Sciences, Royal Veterinary College, North Mymms, Hatfield, HertfordshireAL9 7TA, UK
*
Author for correspondence: Chike F. Oguejiofor, E-mail: [email protected]

Abstract

Bovine viral diarrhea virus (BVDV) is an important infectious disease agent that causes significant reproductive and economic losses in the cattle industry worldwide. Although BVDV infection is known to cause poor fertility in cattle, a greater part of the underlying mechanisms particularly associated with early reproductive losses are not clearly understood. Previous studies reported viral compromise of reproductive function in infected bulls. In females, BVDV infection is thought to be capable of killing the oocyte, embryo or fetus directly, or to induce lesions that result in fetal abortion or malformation. BVDV infections may also induce immune dysfunction, and predispose cattle to other diseases that cause poor health and fertility. Other reports also suggested BVDV-induced disruption of the reproductive endocrine system, and a disruption of leukocyte and cytokine functions in the reproductive organs. More recent studies have provided evidence of viral-induced suppression of endometrial innate immunity that may predispose to uterine disease. Furthermore, there is new evidence that BVDV may potentially disrupt the maternal recognition of pregnancy or the immune protection of the conceptus. This review brings together the previous reports with the more recent findings, and attempts to explain some of the mechanisms linking this important virus to infertility in cattle.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, H, Frech, B, Meier, P, Jungi, TW and Peterhans, E (1994) Noncytopathic strains of bovine viral diarrhea virus prime bovine bone marrow-derived macrophages for enhanced generation of nitric oxide. Biochemical and Biophysical Research Communications 202, 15621568.CrossRefGoogle ScholarPubMed
Adler, H, Jungi, TW, Pfister, H, Strasser, M, Sileghem, M and Peterhans, E (1996) Cytokine regulation by virus infection: bovine viral diarrhea virus, a flavivirus, downregulates production of tumor necrosis factor alpha in macrophages in vitro. Journal of Virology 70, 26502653.CrossRefGoogle ScholarPubMed
Anderson, CA, Higgins, RJ, Smith, ME and Osburn, BI (1987) Border disease. Virus-induced decrease in thyroid hormone levels with associated hypomyelination. Laboratory Investigation 57, 168175.Google ScholarPubMed
Aragaw, K, Sibhat, B, Ayelet, G, Skjerve, E, Gebremedhin, EZ and Asmare, K (2018) Seroprevalence and factors associated with bovine viral diarrhea virus (BVDV) infection in dairy cattle in three milksheds in Ethiopia. Tropical Animal Health and Production 50, 18211827.CrossRefGoogle ScholarPubMed
Archambault, D, Beliveau, C, Couture, Y and Carman, S (2000) Clinical response and immunomodulation following experimental challenge of calves with type 2 noncytopathogenic bovine viral diarrhea virus. Veterinary Research 31, 215227.CrossRefGoogle ScholarPubMed
Archbald, LF, Gibson, CD, Schultz, RH, Fahning, ML and Zemjanis, R (1973) Effects of intrauterine inoculation of bovine viral diarrhea-mucosal disease virus on uterine tubes and uterus of nonpregnant cows. American Journal of Veterinary Research 34, 11331137.Google ScholarPubMed
Archbald, LF, Fulton, RW, Seger, CL, Al-Bagdadi, F and Godke, RA (1979) Effect of the bovine viral diarrhea (BVD) virus on preimplantation bovine embryos: a preliminary study. Theriogenology 11, 8189.CrossRefGoogle Scholar
Arosh, JA, Banu, SK, Kimmins, S, Chapdelaine, P, Maclaren, LA and Fortier, MA (2004) Effect of interferon-tau on prostaglandin biosynthesis, transport, and signaling at the time of maternal recognition of pregnancy in cattle: evidence of polycrine actions of prostaglandin E2. Endocrinology 145, 52805293.CrossRefGoogle ScholarPubMed
Atluru, D, Gudapaty, S, Xue, W, Gurria, F, Chengappa, MM, McVey, DS, Minocha, HC and Atluru, S (1992) In vitro inhibition of 5-lipoxygenase metabolite, leukotriene B4, in bovine mononuclear cells by bovine viral diarrhea virus. Veterinary Immunology and Immunopathology 31, 4959.CrossRefGoogle ScholarPubMed
Baigent, SJ, Zhang, G, Fray, MD, Flick-Smith, H, Goodbourn, S and McCauley, JW (2002) Inhibition of beta interferon transcription by noncytopathogenic bovine viral diarrhea virus is through an interferon regulatory factor 3-dependent mechanism. Journal of Virology 76, 89798988.CrossRefGoogle ScholarPubMed
Baker, JC (1995) The clinical manifestations of bovine viral diarrhea infection. Veterinary Clinics of North America: Food Animal Practice 11, 425445.Google ScholarPubMed
Bazer, FW (2013) Pregnancy recognition signaling mechanisms in ruminants and pigs. Journal of Animal Science and Biotechnology 4, 23.CrossRefGoogle ScholarPubMed
Berke, IC, Li, Y and Modis, Y (2013) Structural basis of innate immune recognition of viral RNA. Cellular Microbiology 15, 386394.CrossRefGoogle ScholarPubMed
Bicalho, MLS, Machado, VS, Higgins, CH, Lima, FS and Bicalho, RC (2017 a) Genetic and functional analysis of the bovine uterine microbiota. Part I: metritis versus healthy cows. Journal of Dairy Science 100, 38503862.CrossRefGoogle ScholarPubMed
Bicalho, MLS, Santin, T, Rodrigues, MX, Marques, CE, Lima, SF and Bicalho, RC (2017 b) Dynamics of the microbiota found in the vaginas of dairy cows during the transition period: associations with uterine diseases and reproductive outcome. Journal of Dairy Science 100, 30433058.CrossRefGoogle ScholarPubMed
Bielanski, A, Loewen, KS, Del Campo, MR, Sirard, MA and Willadsen, S (1993) Isolation of bovine herpesvirus-1 (BHV-1) and bovine viral diarrhea virus (BVDV) in association with the in vitro production of bovine embryos. Theriogenology 40, 531538.CrossRefGoogle ScholarPubMed
Bielanski, A, Algire, J, Lalonde, A and Garceac, A (2013) Embryos produced from fertilization with bovine viral diarrhea virus (BVDV)-infected semen and the risk of disease transmission to embryo transfer (ET) recipients and offspring. Theriogenology 80, 451455.CrossRefGoogle ScholarPubMed
Bielanski, A, Algire, J, Lalonde, A and Nadin-Davis, S (2009) Transmission of bovine viral diarrhea virus (BVDV) via in vitro-fertilized embryos to recipients, but not to their offspring. Theriogenology 71, 499508.CrossRefGoogle Scholar
Bjorkman, C, Alenius, S, Manuelsson, U and Uggla, A (2000) Neospora caninum and bovine virus diarrhoea virus infections in Swedish dairy cows in relation to abortion. Veterinary Journal 159, 201206.CrossRefGoogle Scholar
Blanchard, PC, Ridpath, JF, Walker, JB and Hietala, SK (2010) An outbreak of late-term abortions, premature births, and congenital deformities associated with a bovine viral diarrhea virus 1 subtype b that induces thrombocytopenia. Journal of Veterinary Diagnostic Investigation 22, 128131.CrossRefGoogle ScholarPubMed
Bondurant, RH (1999) Inflammation in the bovine female reproductive tract. Journal of Animal Science 77(Suppl 2), 101110.CrossRefGoogle ScholarPubMed
Booth, PJ, Stevens, DA, Collins, ME and Brownlie, J (1995) Detection of bovine viral diarrhoea virus antigen and RNA in oviduct and granulosa cells of persistently infected cattle. Journal of Reproduction and Fertility 105, 1724.CrossRefGoogle ScholarPubMed
Booth, PJ, Collins, ME, Jenner, L, Prentice, H, Ross, J, Badsberg, JH and Brownlie, J (1998) Noncytopathogenic bovine viral diarrhea virus (BVDV) reduces cleavage but increases blastocyst yield of in vitro produced embryos. Theriogenology 50, 769777.CrossRefGoogle ScholarPubMed
Boyd, BL, Lee, TM, Kruger, EF and Pinchuk, LM (2004) Cytopathic and non-cytopathic bovine viral diarrhoea virus biotypes affect fluid phase uptake and mannose receptor-mediated endocytosis in bovine monocytes. Veterinary Immunology and Immunopathology 102, 5365.CrossRefGoogle ScholarPubMed
Brackenbury, LS, Carr, BV and Charleston, B (2003) Aspects of the innate and adaptive immune responses to acute infections with BVDV. Veterinary Microbiology 96, 337344.CrossRefGoogle ScholarPubMed
Brock, KV and Stringfellow, D (1993) Comparative effects of cytopathic and noncytopathic bovine viral diarrhea virus on bovine blastocysts. Theriogenology 39, 196.CrossRefGoogle Scholar
Brock, KV, Redman, DR, Vickers, ML and Irvine, NE (1991) Quantitation of bovine viral diarrhea virus in embryo transfer flush fluids collected from a persistently infected heifer. Journal of Veterinary Diagnostic Investigation 3, 99100.CrossRefGoogle ScholarPubMed
Brock, KV, Lapin, DR and Skrade, DR (1997) Embryo transfer from donor cattle persistently infected with bovine viral diarrhea virus. Theriogenology 47, 837844.CrossRefGoogle ScholarPubMed
Brodersen, BW and Kelling, CL (1998) Effect of concurrent experimentally induced bovine respiratory syncytial virus and bovine viral diarrhea virus infection on respiratory tract and enteric diseases in calves. American Journal of Veterinary Research 59, 14231430.Google ScholarPubMed
Brodersen, BW and Kelling, CL (1999) Alteration of leukocyte populations in calves concurrently infected with bovine respiratory syncytial virus and bovine viral diarrhea virus. Viral Immunology 12, 323334.CrossRefGoogle ScholarPubMed
Brown, GB, Bolin, SR, Frank, DE and Roth, JA (1991) Defective function of leukocytes from cattle persistently infected with bovine viral diarrhea virus, and the influence of recombinant cytokines. American Journal of Veterinary Research 52, 381387.Google ScholarPubMed
Brownlie, J (1991) The pathways for bovine virus diarrhoea virus biotypes in the pathogenesis of disease. Archives of Virology Supplementum 3, 7996.CrossRefGoogle ScholarPubMed
Brownlie, J, Booth, PJ, Stevens, DA and Collins, ME (1997) Expression of non-cytopathogenic bovine viral diarrhoea virus (BVDV) in oocytes and follicles of persistently infected cattle. Veterinary Record 141, 335337.CrossRefGoogle ScholarPubMed
Brownlie, J, Hooper, LB, Thompson, I and Collins, ME (1998) Maternal recognition of foetal infection with bovine virus diarrhoea virus (BVDV) – the bovine pestivirus. Clinical and Diagnostic Virology 10, 141150.CrossRefGoogle ScholarPubMed
Burgstaller, J, Obritzhauser, W, Kuchling, S, Kopacka, I, Pinior, B and Kofer, J (2016) The effect of bovine viral diarrhoea virus on fertility in dairy cows: two case-control studies in the province of Styria, Austria. Berliner und Munchener tierarztliche Wochenschrift 129, 103110.Google ScholarPubMed
Butt, BM, Senger, PL and Widders, PR (1991) Neutrophil migration into the bovine uterine lumen following intrauterine inoculation with killed Haemophilus somnus. Journal of Reproduction and Fertility 93, 341345.CrossRefGoogle ScholarPubMed
Chapwanya, A, Meade, KG, Doherty, ML, Callanan, JJ and O'Farrelly, C (2013) Endometrial epithelial cells are potent producers of tracheal antimicrobial peptide and serum amyloid A3 gene expression in response to E. coli stimulation. Veterinary Immunology and Immunopathology 151, 157162.CrossRefGoogle ScholarPubMed
Charleston, B, Fray, MD, Baigent, S, Carr, BV and Morrison, WI (2001) Establishment of persistent infection with non-cytopathic bovine viral diarrhoea virus in cattle is associated with a failure to induce type I interferon. Journal of General Virology 82, 18931897.CrossRefGoogle ScholarPubMed
Chase, CC (2013) The impact of BVDV infection on adaptive immunity. Biologicals 41, 5260.CrossRefGoogle ScholarPubMed
Chase, CC, Elmowalid, G and Yousif, AA (2004) The immune response to bovine viral diarrhea virus: a constantly changing picture. Veterinary Clinics of North America: Food Animal Practice 20, 95114.Google ScholarPubMed
Chase, CCL, Thakur, N, Darweesh, MF, Morarie-Kane, SE and Rajput, MK (2015) Immune response to bovine viral diarrhea virus – looking at newly defined targets. Animal Health Research Reviews 16, 414.CrossRefGoogle ScholarPubMed
Chen, Z, Rijnbrand, R, Jangra, RK, Devaraj, SG, Qu, L, Ma, Y, Lemon, SM and Li, K (2007) Ubiquitination and proteasomal degradation of interferon regulatory factor-3 induced by Npro from a cytopathic bovine viral diarrhea virus. Virology 366, 277292.CrossRefGoogle ScholarPubMed
Cheng, Z, Abudureyimu, A, Oguejiofor, CF, Ellis, R, Barry, AT, Chen, X, Anstaett, OL, Brownlie, J and Wathes, DC (2016) BVDV alters uterine prostaglandin production during pregnancy recognition in cows. Reproduction 151, 605614.CrossRefGoogle ScholarPubMed
Cheng, Z, Chauhan, L, Barry, AT, Abudureyimu, A, Oguejiofor, CF, Chen, X and Wathes, DC (2017) Acute bovine viral diarrhoea virus infection inhibits expression of interferon tau-stimulated genes in bovine endometrium. Biology of Reproduction 96, 11421153.Google ScholarPubMed
Cheng, Z, Brown, L and Wathes, C (2018) Bovine viral diarrhoea virus infection interrupts the regulatory pathways for uterine interferon stimulated gene expression in cows. Reproduction in Domestic Animals 53, 87.Google Scholar
Chernick, A and van der Meer, F (2017) Evolution of bovine viral diarrhea virus in Canada from 1997 to 2013. Virology 509, 232238.CrossRefGoogle ScholarPubMed
Collins, ME, Heaney, J, Thomas, CJ and Brownlie, J (2009) Infectivity of pestivirus following persistence of acute infection. Veterinary Microbiology 138, 289296.CrossRefGoogle ScholarPubMed
Dale, DC, Boxer, L and Liles, WC (2008) The phagocytes: neutrophils and monocytes. Blood 112, 935945.CrossRefGoogle ScholarPubMed
Darweesh, MF, Rajput, MKS, Braun, LJ, Rohila, JS and Chase, CCL (2018) BVDV NPro protein mediates the BVDV induced immunosuppression through interaction with cellular S100A9 protein. Microbial Pathogenesis 121, 341349.CrossRefGoogle ScholarPubMed
da Silva Cardoso Pinto, V, Alves, MF, de Souza Nunes Martins, M, Basso, AC, Tannura, JH, Pontes, JHF, Lima, MS, Garcia da Silva, T, Okuda, LH, Stefano, E, Romaldini, A, Arnold, DR and Pituco, EM (2017) Effects of oocytes exposure to bovine diarrhea viruses BVDV-1, BVDV-2 and Hobi-like virus on in vitro-produced bovine embryo development and viral infection. Theriogenology 97, 6772.CrossRefGoogle ScholarPubMed
Davies, D, Meade, KG, Herath, S, Eckersall, PD, Gonzalez, D, White, JO, Conlan, RS, O'Farrelly, C and Sheldon, IM (2008) Toll-like receptor and antimicrobial peptide expression in the bovine endometrium. Reproductive Biology and Endocrinology 6, 53.CrossRefGoogle ScholarPubMed
Deretic, V and Levine, B (2009) Autophagy, immunity, and microbial adaptations. Cell Host & Microbe 5, 527549.CrossRefGoogle ScholarPubMed
de Verdier Klingenberg, K (2000) Enhancement of clinical signs in experimentally rotavirus infected calves by combined viral infections. Veterinary Record 147, 717719.Google ScholarPubMed
Di Gennaro, A and Haeggstrom, JZ (2012) The leukotrienes: immune-modulating lipid mediators of disease. Advances in Immunology 116, 5192.CrossRefGoogle Scholar
Diskin, MG, Parr, MH and Morris, DG (2011) Embryo death in cattle: an update. Reproduction, Fertility, and Development 24, 244251.CrossRefGoogle ScholarPubMed
Done, JT, Terlecki, S, Richardson, C, Harkness, JW, Sands, JJ, Patterson, DS, Sweasey, D, Shaw, IG, Winkler, CE and Duffell, SJ (1980) Bovine virus diarrhoea-mucosal disease virus: pathogenicity for the fetal calf following maternal infection. Veterinary Record 106, 473479.CrossRefGoogle ScholarPubMed
Dorniak, P, Bazer, FW and Spencer, TE (2011) Prostaglandins regulate conceptus elongation and mediate effects of interferon tau on the ovine uterine endometrium. Biology of Reproduction 84, 11191127.CrossRefGoogle ScholarPubMed
Dorniak, P, Bazer, FW, Wu, G and Spencer, TE (2012) Conceptus-derived prostaglandins regulate endometrial function in sheep. Biology of Reproduction 87, 17.Google Scholar
Edwards, S, Wood, L, Hewitt-Taylor, C and Drew, TW (1986) Evidence for an immunocompromising effect of bovine pestivirus on bovid herpesvirus 1 vaccination. Veterinary Research Communications 10, 297302.CrossRefGoogle ScholarPubMed
Ellis, JA, Davis, WC, Belden, EL and Pratt, DL (1988) Flow cytofluorimetric analysis of lymphocyte subset alterations in cattle infected with bovine viral diarrhea virus. Veterinary Pathology 25, 231236.CrossRefGoogle ScholarPubMed
Emond, V, MacLaren, LA, Kimmins, S, Arosh, JA, Fortier, MA and Lambert, RD (2004) Expression of cyclooxygenase-2 and granulocyte-macrophage colony-stimulating factor in the endometrial epithelium of the cow is up-regulated during early pregnancy and in response to intrauterine infusions of interferon-tau. Biology of Reproduction 70, 5464.CrossRefGoogle ScholarPubMed
Erdem, H and Guzeloglu, A (2010) Effect of meloxicam treatment during early pregnancy in Holstein heifers. Reproduction in Domestic Animals 45, 625628.Google ScholarPubMed
Firat, I, Ak, S, Bozkurt, HH, Ak, K, Turan, N and Bagcigil, F (2002) Distribution of bovine viral diarrhoea virus (BVDV) in the genital system tissues of cattle. Veterinarski Arhiv 72, 235248.Google Scholar
Forde, N, Carter, F, Spencer, TE, Bazer, FW, Sandra, O, Mansouri-Attia, N, Okumu, LA, McGettigan, PA, Mehta, JP, McBride, R, O'Gaora, P, Roche, JF and Lonergan, P (2011) Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biology of Reproduction 85, 144156.CrossRefGoogle Scholar
Fray, MD, Prentice, H, Clarke, MC and Charleston, B (1998) Immunohistochemical evidence for the localization of bovine viral diarrhea virus, a single-stranded RNA virus, in ovarian oocytes in the cow. Veterinary Pathology 35, 253259.CrossRefGoogle ScholarPubMed
Fray, MD, Mann, GE, Clarke, MC and Charleston, B (1999) Bovine viral diarrhea virus: its effects on estradiol, progesterone and prostaglandin secretion in the cow. Theriogenology 51, 15331546.CrossRefGoogle ScholarPubMed
Fray, MD, Paton, DJ and Alenius, S (2000) The effects of bovine viral diarrhoea virus on cattle reproduction in relation to disease control. Animal Reproduction Science 60–61, 615627.CrossRefGoogle ScholarPubMed
Fray, MD, Mann, GE, Bleach, EC, Knight, PG, Clarke, MC and Charleston, B (2002) Modulation of sex hormone secretion in cows by acute infection with bovine viral diarrhoea virus. Reproduction 123, 281289.CrossRefGoogle ScholarPubMed
Fredriksen, B, Press, CM, Loken, T and Odegaard, SA (1999 a) Distribution of viral antigen in uterus, placenta and foetus of cattle persistently infected with bovine virus diarrhoea virus. Veterinary Microbiology 64, 109122.CrossRefGoogle ScholarPubMed
Fredriksen, B, Press, CM, Sandvik, T, Odegaard, SA and Loken, T (1999 b) Detection of viral antigen in placenta and fetus of cattle acutely infected with bovine viral diarrhea virus. Veterinary Pathology 36, 267275.CrossRefGoogle ScholarPubMed
Fu, Y, Liu, B, Feng, X, Liu, Z, Liang, D, Li, F, Li, D, Cao, Y, Feng, S, Zhang, X, Zhang, N and Yang, Z (2013) Lipopolysaccharide increases Toll-like receptor 4 and downstream Toll-like receptor signaling molecules expression in bovine endometrial epithelial cells. Veterinary Immunology and Immunopathology 151, 2027.CrossRefGoogle ScholarPubMed
Gamlen, T, Richards, KH, Mankouri, J, Hudson, L, McCauley, J, Harris, M and Macdonald, A (2010) Expression of the NS3 protease of cytopathogenic bovine viral diarrhea virus results in the induction of apoptosis but does not block activation of the beta interferon promoter. Journal of General Virology 91, 133144.CrossRefGoogle Scholar
Gard, JA, Givens, MD, Marley, MS, Galik, PK, Riddell, KP, Stringfellow, DA, Zhang, Y and Edmondson, MA (2009) Bovine viral diarrhea virus (BVDV) associated with single in vivo-derived and in vitro-produced preimplantation bovine embryos following artificial exposure. Theriogenology 71, 12381244.CrossRefGoogle ScholarPubMed
Garoussi, MT and Mehrzad, J (2011) Effect of bovine viral diarrhoea virus biotypes on adherence of sperm to oocytes during in-vitro fertilization in cattle. Theriogenology 75, 10671075.CrossRefGoogle ScholarPubMed
Gilbert, RO (2012) The effects of endometritis on the establishment of pregnancy in cattle. Reproduction, Fertility, and Development 24, 252257.CrossRefGoogle Scholar
Givens, MD and Marley, MS (2013) Immunology of chronic BVDV infections. Biologicals 41, 2630.CrossRefGoogle ScholarPubMed
Givens, MD and Newcomer, BW (2015) Perspective on BVDV control programs. Animal Health Research Reviews 16, 7882.CrossRefGoogle ScholarPubMed
Givens, MD, Galik, PK, Riddell, KP, Brock, KV and Stringfellow, DA (2000) Replication and persistence of different strains of bovine viral diarrhea virus in an in vitro embryo production system. Theriogenology 54, 10931107.CrossRefGoogle Scholar
Givens, MD, Heath, AM, Brock, KV, Brodersen, BW, Carson, RL and Stringfellow, DA (2003) Detection of bovine viral diarrhea virus in semen obtained after inoculation of seronegative postpubertal bulls. American Journal of Veterinary Research 64, 428434.CrossRefGoogle ScholarPubMed
Glew, EJ, Carr, BV, Brackenbury, LS, Hope, JC, Charleston, B and Howard, CJ (2003) Differential effects of bovine viral diarrhoea virus on monocytes and dendritic cells. Journal of General Virology 84, 17711780.CrossRefGoogle ScholarPubMed
Gonzalez Altamiranda, EA, Kaiser, GG, Mucci, NC, Verna, AE, Campero, CM and Odeon, AC (2013) Effect of bovine viral diarrhea virus on the ovarian functionality and in vitro reproductive performance of persistently infected heifers. Veterinary Microbiology 165, 326332.CrossRefGoogle ScholarPubMed
Grooms, DL (2004) Reproductive consequences of infection with bovine viral diarrhea virus. Veterinary Clinics of North America: Food Animal Practice 20, 519.Google ScholarPubMed
Grooms, DL, Ward, LA and Brock, KV (1996) Morphologic changes and immunohistochemical detection of viral antigen in ovaries from cattle persistently infected with bovine viral diarrhea virus. American Journal of Veterinary Research 57, 830833.Google ScholarPubMed
Grooms, DL, Brock, KV, Pate, JL and Day, ML (1998 a) Changes in ovarian follicles following acute infection with bovine viral diarrhea virus. Theriogenology 49, 595605.CrossRefGoogle ScholarPubMed
Grooms, DL, Brock, KV and Ward, LA (1998 b) Detection of bovine viral diarrhea virus in the ovaries of cattle acutely infected with bovine viral diarrhea virus. Journal of Veterinary Diagnostic Investigation 10, 125129.CrossRefGoogle ScholarPubMed
Gunn, GJ, Stott, AW and Humphry, RW (2004) Modelling and costing BVD outbreaks in beef herds. Veterinary Journal 167, 143149.CrossRefGoogle ScholarPubMed
Han, DG, Ryu, JH, Park, J and Choi, KS (2018) Identification of a new bovine viral diarrhea virus subtype in the Republic of Korea. BMC Veterinary Research 14, 233.CrossRefGoogle ScholarPubMed
Hansen, PJ (2011) The immunology of early pregnancy in farm animals. Reproduction in Domestic Animals 46(Suppl 3), 1830.CrossRefGoogle ScholarPubMed
Hansen, TR and Pru, JK (2014) ISGylation: a conserved pathway in mammalian pregnancy. Advances in Experimental Medicine and Biology 759, 1331.CrossRefGoogle ScholarPubMed
Hansen, TR, Smirnova, NP, Van Campen, H, Shoemaker, ML, Ptitsyn, AA and Bielefeldt-Ohmann, H (2010) Maternal and fetal response to fetal persistent infection with bovine viral diarrhea virus. American Journal of Reproductive Immunology 64, 295306.CrossRefGoogle ScholarPubMed
Harding, MJ, Cao, X, Shams, H, Johnson, AF, Vassilev, VB, Gil, LH, Wheeler, DW, Haines, D, Sibert, GJ, Nelson, LD, Campos, M and Donis, RO (2002) Role of bovine viral diarrhea virus biotype in the establishment of fetal infections. American Journal of Veterinary Research 63, 14551463.CrossRefGoogle ScholarPubMed
Headley, SA, Voltarelli, D, de Oliveira, VH, Bronkhorst, DE, Alfieri, AF, Filho, LC, Okano, W and Alfieri, AA (2015) Association of Histophilus somni with spontaneous abortions in dairy cattle herds from Brazil. Tropical Animal Health and Production 47, 403413.CrossRefGoogle ScholarPubMed
Herath, S, Lilly, ST, Fischer, DP, Williams, EJ, Dobson, H, Bryant, CE and Sheldon, IM (2009) Bacterial lipopolysaccharide induces an endocrine switch from prostaglandin F to prostaglandin E2 in bovine endometrium. Endocrinology 150, 19121920.CrossRefGoogle ScholarPubMed
Hertzog, PJ and Williams, BRG (2013) Fine tuning type I interferon responses. Cytokine & Growth Factor Reviews 24, 217225.CrossRefGoogle ScholarPubMed
Hickey, DK, Patel, MV, Fahey, JV and Wira, CR (2011) Innate and adaptive immunity at mucosal surfaces of the female reproductive tract: stratification and integration of immune protection against the transmission of sexually transmitted infections. Journal of Reproductive Immunology 88, 185194.CrossRefGoogle ScholarPubMed
Houe, H (1993) Survivorship of animals persistently infected with bovine virus diarrhoea virus (BVDV). Preventive Veterinary Medicine 15, 275283.CrossRefGoogle Scholar
Houe, H (2003) Economic impact of BVDV infection in dairies. Biologicals 31, 137143.CrossRefGoogle ScholarPubMed
Houe, H, Pedersen, KM and Meyling, A (1993) The effect of bovine virus diarrhoea virus infection on conception rate. Preventive Veterinary Medicine 15, 117123.CrossRefGoogle Scholar
Huszenicza, G, Fodor, M, Gacs, M, Kulcsar, M, Dohmen, MJW, Vamos, M, Porkolab, L, Kegl, T, Bartyik, J, Lohuis, J, Janosi, S and Szita, G (1999) Uterine bacteriology, resumption of cyclic ovarian activity and fertility in postpartum cows kept in large-scale dairy herds. Reproduction in Domestic Animals 34, 237245.CrossRefGoogle Scholar
Jabbour, HN, Sales, KJ, Catalano, RD and Norman, JE (2009) Inflammatory pathways in female reproductive health and disease. Reproduction 138, 903919.CrossRefGoogle ScholarPubMed
Jeffrey, M and Hogg, RA (1988) Concurrent bovine virus diarrhoea virus and Campylobacter fetus infection in an aborted bovine fetus. Veterinary Record 122, 8990.CrossRefGoogle Scholar
Jeon, SJ, Cunha, F, Vieira-Neto, A, Bicalho, RC, Lima, S, Bicalho, ML and Galvão, KN (2017) Blood as a route of transmission of uterine pathogens from the gut to the uterus in cows. Microbiome 5, 109.CrossRefGoogle ScholarPubMed
Kafi, M, McGowan, MR, Kirkland, PD and Jillella, D (1997) The effect of bovine pestivirus infection on the superovulatory response of Friesian heifers. Theriogenology 48, 985996.CrossRefGoogle ScholarPubMed
Kale, M, Yavru, S, Ata, A, Kocamuftuoglu, M, Yaplcl, O and Haslrcloglu, S (2011) Bovine viral diarrhea virus (BVDV) infection in relation to fertility in heifers. Journal of Veterinary Medical Science 73, 331336.CrossRefGoogle ScholarPubMed
Kale, M, Ata, A, Yavru, S, Yapkic, O, Bulut, O and Gulay, M (2006) The effect of infection with bovine viral diarrhea virus on the fertility of cows and heifers. Acta Veterinaria 56, 467477.Google Scholar
Kalinski, P (2012) Regulation of immune responses by prostaglandin E2. The Journal of Immunology 188, 2128.CrossRefGoogle ScholarPubMed
Kelling, CL, Steffen, DJ, Topliff, CL, Eskridge, KM, Donis, RO and Higuchi, DS (2002) Comparative virulence of isolates of bovine viral diarrhea virus type II in experimentally inoculated six- to nine-month-old calves. American Journal of Veterinary Research 63, 13791384.CrossRefGoogle ScholarPubMed
Kennedy, J (2005) Putting BVD Control on Your Radar Screen. Range Beef Cow Symposium. Paper 43. Animal Science Department, University of Nebraska-Lincoln.Google Scholar
Kimura, K, Spate, LD, Green, MP, Murphy, CN, Seidel, GE Jr and Roberts, RM (2004) Sexual dimorphism in interferon-tau production by in vivo-derived bovine embryos. Molecular Reproduction and Development 67, 193199.CrossRefGoogle ScholarPubMed
Kirkbride, CA (1992) Etiologic agents detected in a 10-year study of bovine abortions and stillbirths. Journal of Veterinary Diagnostic Investigation 4, 175180.CrossRefGoogle Scholar
Kirkland, PD, Richards, SG, Rothwell, JT and Stanley, DF (1991) Replication of bovine viral diarrhoea virus in the bovine reproductive tract and excretion of virus in semen during acute and chronic infections. Veterinary Record 128, 587590.CrossRefGoogle ScholarPubMed
Kirkland, PD, Mackintosh, SG and Moyle, A (1994) The outcome of widespread use of semen from a bull persistently infected with pestivirus. Veterinary Record 135, 527529.CrossRefGoogle ScholarPubMed
Kommisrud, E, Vatn, T, Lang-Ree, JR and Loken, T (1996) Bovine virus diarrhoea virus in semen from acutely infected bulls. Acta Veterinaria Scandinavica 37, 4147.Google ScholarPubMed
Kumar, H, Kawai, T and Akira, S (2009) Pathogen recognition in the innate immune response. Biochemical Journal 420, 116.CrossRefGoogle ScholarPubMed
Kumar, H, Kawai, T and Akira, S (2011) Pathogen recognition by the innate immune system. International Reviews of Immunology 30, 1634.CrossRefGoogle ScholarPubMed
Lang-Ree, JR, Vatn, T, Kommisrud, E and Loken, T (1994) Transmission of bovine viral diarrhoea virus by rectal examination. Veterinary Record 135, 412413.CrossRefGoogle ScholarPubMed
Lanyon, SR, Hill, FI, Reichel, MP and Brownlie, J (2014) Bovine viral diarrhoea: pathogenesis and diagnosis. Veterinary Journal 199, 201209.CrossRefGoogle ScholarPubMed
Larsson, B, Niskanen, R and Alenius, S (1994) Natural infection with bovine virus diarrhoea virus in a dairy herd: a spectrum of symptoms including early reproductive failure and retained placenta. Animal Reproduction Science 36, 3748.CrossRefGoogle Scholar
Laureyns, J, Ribbens, S and de Kruif, A (2010) Control of bovine virus diarrhoea at the herd level: reducing the risk of false negatives in the detection of persistently infected cattle. Veterinary Journal 184, 2126.CrossRefGoogle ScholarPubMed
LeBlanc, SJ (2014) Reproductive tract inflammatory disease in postpartum dairy cows. Animal: An International Journal of Animal Bioscience 8(Suppl 1), 5463.CrossRefGoogle ScholarPubMed
Lee, KM and Gillespie, JH (1957) Propagation of virus diarrhea virus of cattle in tissue culture. American Journal of Veterinary Research 18, 952953.Google ScholarPubMed
Lee, SR, Pharr, GT, Boyd, BL and Pinchuk, LM (2008) Bovine viral diarrhea viruses modulate toll-like receptors, cytokines and co-stimulatory molecules genes expression in bovine peripheral blood monocytes. Comparative Immunology, Microbiology and Infectious Diseases 31, 403418.CrossRefGoogle ScholarPubMed
Lee, SR, Nanduri, B, Pharr, GT, Stokes, JV and Pinchuk, LM (2009) Bovine viral diarrhea virus infection affects the expression of proteins related to professional antigen presentation in bovine monocytes. Biochimica et Biophysica Acta 1794, 1422.CrossRefGoogle ScholarPubMed
Lewis, GS (2003) Role of ovarian progesterone and potential role of prostaglandin F and prostaglandin E2 in modulating the uterine response to infectious bacteria in postpartum ewes. Journal of Animal Science 81, 285293.CrossRefGoogle ScholarPubMed
Li, J and Roberts, RM (1994) Interferon-τ and interferon-α interact with the same receptors in bovine endometrium. Use of a readily iodinatable form of recombinant interferon-tau for binding studies. Journal of Biological Chemistry 269, 1354413550.Google ScholarPubMed
Liebler-Tenorio, EM, Ridpath, JF and Neill, JD (2003) Lesions and tissue distribution of viral antigen in severe acute versus subclinical acute infection with BVDV2. Biologicals 31, 119122.CrossRefGoogle ScholarPubMed
Lindberg, A and Houe, H (2005) Characteristics in the epidemiology of bovine viral diarrhea virus (BVDV) of relevance to control. Preventive Veterinary Medicine 72, 5573.CrossRefGoogle Scholar
Lonergan, P and Forde, N (2014) Maternal-embryo interaction leading up to the initiation of implantation of pregnancy in cattle. Animal: An International Journal of Animal Bioscience 8(Suppl 1), 6469.CrossRefGoogle ScholarPubMed
Mann, GE, Lamming, GE, Robinson, RS and Wathes, DC (1999) The regulation of interferon-tau production and uterine hormone receptors during early pregnancy. Journal of Reproduction and Fertility Supplement 54, 317328.Google ScholarPubMed
Mansouri-Attia, N, Aubert, J, Reinaud, P, Giraud-Delville, C, Taghouti, G, Galio, L, Everts, RE, Degrelle, S, Richard, C, Hue, I, Yang, X, Tian, XC, Lewin, HA, Renard, JP and Sandra, O (2009) Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiological Genomics 39, 1427.CrossRefGoogle ScholarPubMed
McGowan, MR and Kirkland, PD (1995) Early reproductive loss due to bovine pestivirus infection. British Veterinary Journal 151, 263270.CrossRefGoogle ScholarPubMed
McGowan, MR, Kirkland, PD, Richards, SG and Littlejohns, IR (1993 a) Increased reproductive losses in cattle infected with bovine pestivirus around the time of insemination. Veterinary Record 133, 3943.CrossRefGoogle ScholarPubMed
McGowan, MR, Kirkland, PD, Rodwell, BJ, Kerr, DR and Carroll, CL (1993 b) A field investigation of the effects of bovine viral diarrhea virus infection around the time of insemination on the reproductive performance of cattle. Theriogenology 39, 443449.CrossRefGoogle ScholarPubMed
McGowan, MR, Kafi, M, Kirkland, PD, Kelly, R, Bielefeldt-Ohmann, H, Occhio, MD and Jillella, D (2003) Studies of the pathogenesis of bovine pestivirus-induced ovarian dysfunction in superovulated dairy cattle. Theriogenology 59, 10511066.CrossRefGoogle ScholarPubMed
Meyling, A and Mikél Jensen, A (1988) Transmission of bovine virus diarrhoea virus (BVDV) by artificial insemination (AI) with semen from a persistently-infected bull. Veterinary Microbiology 17, 97105.CrossRefGoogle ScholarPubMed
Monroe, KM, McWhirter, SM and Vance, RE (2010) Induction of type I interferons by bacteria. Cellular Microbiology 12, 881890.CrossRefGoogle ScholarPubMed
Morarie-Kane, SE, Smirnova, NP, Hansen, TR, Mediger, J, Braun, L and Chase, C (2018) Fetal hepatic response to bovine viral diarrhea virus infection in utero. Pathogens (Basel, Switzerland) 7, 54.Google ScholarPubMed
Munoz-Zanzi, CA, Thurmond, MC and Hietala, SK (2004) Effect of bovine viral diarrhea virus infection on fertility of dairy heifers. Theriogenology 61, 10851099.CrossRefGoogle ScholarPubMed
Murray, RD (1991) Lesions in aborted bovine fetuses and placenta associated with bovine viral diarrhoea virus infection. Archives of Virology Supplementum 3, 217224.CrossRefGoogle ScholarPubMed
Newcomer, BW, Toohey-Kurth, K, Zhang, Y, Brodersen, BW, Marley, MS, Joiner, KS, Galik, PK, Riddell, KP and Givens, MD (2014) Laboratory diagnosis and transmissibility of bovine viral diarrhea virus from a bull with a persistent testicular infection. Veterinary Microbiology 170, 246257.CrossRefGoogle ScholarPubMed
Newcomer, BW, Walz, PH, Givens, MD and Wilson, AE (2015) Efficacy of bovine viral diarrhea virus vaccination to prevent reproductive disease: a meta-analysis. Theriogenology 83, 360365.e361.CrossRefGoogle ScholarPubMed
Niskanen, R, Emanuelson, U, Sundberg, J, Larsson, B and Alenius, S (1995) Effects of infection with bovine virus diarrhoea virus on health and reproductive performance in 213 dairy herds in one county in Sweden. Preventive Veterinary Medicine 23, 229237.CrossRefGoogle Scholar
Noakes, D (2001 a) Endogenous and exogenous control of ovarian cyclicity. In Noakes, D, Parkinson, T and England, G (eds), Arthur's Veterinary Reproduction and Obstetrics, 8th Edn.Edinburgh, UK: Saunders, pp. 353.Google Scholar
Noakes, D (2001 b) The puerperium and the care of the newborn. In Noakes, D, Parkinson, T and England, G (eds), Arthur's Veterinary Reproduction and Obstetrics, 8th Edn.Edinburgh, UK: Saunders, pp. 189202.Google Scholar
Oguejiofor, CF, Cheng, Z, Abudureyimu, A, Anstaett, OL, Brownlie, J, Fouladi-Nashta, AA and Wathes, DC (2015 a) Global transcriptomic profiling of bovine endometrial immune response in vitro. II. Effect of bovine viral diarrhea virus on the endometrial response to lipopolysaccharide. Biology of Reproduction 93, 101, 116.Google ScholarPubMed
Oguejiofor, CF, Cheng, Z, Abudureyimu, A, Fouladi-Nashta, AA and Wathes, DC (2015 b) Global transcriptomic profiling of bovine endometrial immune response in vitro. I. Effect of lipopolysaccharide on innate immunity. Biology of Reproduction 93, 100, 113.Google ScholarPubMed
Oguejiofor, CF, Cheng, Z, Fouladi-Nashta, AA and Wathes, DC (2017 a) Bovine endometrial cells mount innate immune response to the intracellular ligands CL097 and poly (dA:dT) indicating roles against uterine viruses. Open Journal of Animal Sciences 7, 110126.CrossRefGoogle Scholar
Oguejiofor, CF, Cheng, Z and Wathes, DC (2017 b) Regulation of innate immunity within the bovine endometrium during infection. CAB Reviews 12, 114.CrossRefGoogle Scholar
Olafson, P, Mac, CA and Fox, FH (1946) An apparently new transmissible disease of cattle. Cornell Veterinarian 36, 205213.Google ScholarPubMed
Opsomer, G, Grohn, YT, Hertl, J, Coryn, M, Deluyker, H and de Kruif, A (2000) Risk factors for post partum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology 53, 841857.CrossRefGoogle ScholarPubMed
Parkin, J and Cohen, B (2001) An overview of the immune system. Lancet 357, 17771789.CrossRefGoogle ScholarPubMed
Penny, CD, Low, JC, Nettleton, PF, Scott, PR, Sargison, ND, Strachan, WD and Honeyman, PC (1996) Concurrent bovine viral diarrhoea virus and Salmonella typhimurium DT104 infection in a group of pregnant dairy heifers. Veterinary Record 138, 485489.CrossRefGoogle Scholar
Perry, AK, Chen, G, Zheng, D, Tang, H and Cheng, G (2005) The host type I interferon response to viral and bacterial infections. Cell Research 15, 407422.CrossRefGoogle ScholarPubMed
Peterhans, E and Schweizer, M (2010) Pestiviruses: how to outmaneuver your hosts. Veterinary Microbiology 142, 1825.CrossRefGoogle ScholarPubMed
Peterhans, E and Schweizer, M (2013) BVDV: a pestivirus inducing tolerance of the innate immune response. Biologicals 41, 3951.CrossRefGoogle ScholarPubMed
Piccinini, R, Luzzago, C, Frigerio, M, Dapra, V, Liandris, E and Zecconi, A (2006) Comparison of blood non-specific immune parameters in bovine virus diarrhoea virus (BVDV) persistently infected and in immune heifers. Journal of Veterinary Medicine B: Infectious Diseases and Veterinary Public Health 53, 6267.CrossRefGoogle ScholarPubMed
Pineda, MH (2003) Female reproductive system. In Pineda, MH (ed.), McDonald's Veterinary Endocrinology and Reproduction, 5th Edn.Ames, Iowa, USA: Iowa State Press, pp. 283340.Google Scholar
Potgieter, LN (1997) Bovine respiratory tract disease caused by bovine viral diarrhea virus. Veterinary Clinics of North America: Food Animal Practice 13, 471481.Google ScholarPubMed
Pritchard, GC, Borland, ED, Wood, L and Pritchard, DG (1989) Severe disease in a dairy herd associated with acute infection with bovine virus diarrhoea virus, Leptospira harjo and Coxiella burnetii. Veterinary Record 124, 625629.CrossRefGoogle Scholar
Randall, RE and Goodbourn, S (2008) Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. Journal of General Virology 89, 147.CrossRefGoogle ScholarPubMed
Ravetch, JV and Clynes, RA (1998) Divergent roles for Fc receptors and complement in vivo. Annual Review of Immunology 16, 421432.CrossRefGoogle ScholarPubMed
Reichel, MP, Hill, FI and Voges, H (2008) Does control of bovine viral diarrhoea infection make economic sense? New Zealand Veterinary Journal 56, 6066.CrossRefGoogle ScholarPubMed
Revell, SG, Chasey, D, Drew, TW and Edwards, S (1988) Some observations on the semen of bulls persistently infected with bovine virus diarrhoea virus. The Veterinary Record 123, 122125.CrossRefGoogle ScholarPubMed
Richards, JS, Liu, Z and Shimada, M (2008) Immune-like mechanisms in ovulation. Trends in Endocrinology and Metabolism 19, 191196.CrossRefGoogle ScholarPubMed
Richter, V, Lebl, K, Baumgartner, W, Obritzhauser, W, Kasbohrer, A and Pinior, B (2017) A systematic worldwide review of the direct monetary losses in cattle due to bovine viral diarrhoea virus infection. Veterinary Journal 220, 8087.CrossRefGoogle ScholarPubMed
Ridpath, J (2010 a) The contribution of infections with bovine viral diarrhea viruses to bovine respiratory disease. Veterinary Clinics of North America: Food Animal Practice 26, 335348.Google ScholarPubMed
Ridpath, JF (2010 b) Bovine viral diarrhea virus: global status. Veterinary Clinics of North America: Food Animal Practice 26, 105121.Google ScholarPubMed
Rikula, U, Nuotio, L, Laamanen, UI and Sihvonen, L (2008) Transmission of bovine viral diarrhoea virus through the semen of acutely infected bulls under field conditions. Veterinary Record 162, 7982.CrossRefGoogle ScholarPubMed
Robert, A, Beaudeau, F, Seegers, H, Joly, A and Philipot, JM (2004) Large scale assessment of the effect associated with bovine viral diarrhoea virus infection on fertility of dairy cows in 6149 dairy herds in Brittany (Western France). Theriogenology 61, 117127.CrossRefGoogle Scholar
Roberts, RM, Ezashi, T, Rosenfeld, CS, Ealy, AD and Kubisch, HM (2003) Evolution of the interferon tau genes and their promoters, and maternal-trophoblast interactions in control of their expression. Reproduction Supplement 61, 239251.Google ScholarPubMed
Robinson, RS, Fray, MD, Wathes, DC, Lamming, GE and Mann, GE (2006) In vivo expression of interferon tau mRNA by the embryonic trophoblast and uterine concentrations of interferon tau protein during early pregnancy in the cow. Molecular Reproduction and Development 73, 470474.CrossRefGoogle ScholarPubMed
Rodriguez-Martinez, H (2007) Role of the oviduct in sperm capacitation. Theriogenology 68(Suppl 1), S138S146.CrossRefGoogle ScholarPubMed
Rufenacht, J, Schaller, P, Audige, L, Knutti, B, Kupfer, U and Peterhans, E (2001) The effect of infection with bovine viral diarrhea virus on the fertility of Swiss dairy cattle. Theriogenology 56, 199210.CrossRefGoogle ScholarPubMed
Santman-Berends, I, Mars, MH, Van Duijn, L, Van den Broek, KWH and Van Schaik, G (2017) A quantitative risk-analysis for introduction of bovine viral diarrhoea virus in the Netherlands through cattle imports. Preventive Veterinary Medicine 146, 103113.CrossRefGoogle ScholarPubMed
Scharnbock, B, Roch, FF, Richter, V, Funke, C, Firth, CL, Obritzhauser, W, Baumgartner, W, Kasbohrer, A and Pinior, B (2018) A meta-analysis of bovine viral diarrhoea virus (BVDV) prevalences in the global cattle population. Scientific Reports 8, 14420.CrossRefGoogle ScholarPubMed
Schaut, RG, McGill, JL, Neill, JD, Ridpath, JF and Sacco, RE (2015) Bovine viral diarrhea virus type 2 in vivo infection modulates TLR4 responsiveness in differentiated myeloid cells which is associated with decreased MyD88 expression. Virus Research 208, 4455.CrossRefGoogle ScholarPubMed
Schaut, RG, Ridpath, JF and Sacco, RE (2016) Bovine viral diarrhea virus type 2 impairs macrophage responsiveness to Toll-like receptor ligation with the exception of Toll-like Receptor 7. PLoS One 11, e0159491.CrossRefGoogle ScholarPubMed
Schweizer, M and Peterhans, E (2001) Noncytopathic bovine viral diarrhea virus inhibits double-stranded RNA-induced apoptosis and interferon synthesis. Journal of Virology 75, 46924698.CrossRefGoogle ScholarPubMed
Senger, P (2003) The organisation and function of the female reproductive tract. In Pathways to Pregnancy and Parturition, 2nd Edn.Pullman, WA, USA: Current Conceptions Inc., Washington State University, pp. 1043.Google Scholar
Sheldon, IM, Cronin, J, Goetze, L, Donofrio, G and Schuberth, HJ (2009) Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biology of Reproduction 81, 10251032.CrossRefGoogle ScholarPubMed
Simmons, RM, Satterfield, MC, Welsh, TH Jr, Bazer, FW and Spencer, TE (2010) HSD11B1, HSD11B2, PTGS2, and NR3C1 expression in the peri-implantation ovine uterus: effects of pregnancy, progesterone, and interferon tau. Biology of Reproduction 82, 3543.CrossRefGoogle ScholarPubMed
Singh, J, Murray, RD, Mshelia, G and Woldehiwet, Z (2008) The immune status of the bovine uterus during the peripartum period. Veterinary Journal 175, 301309.CrossRefGoogle ScholarPubMed
Sinowatz, F, Topfer-Petersen, E, Kolle, S and Palma, G (2001) Functional morphology of the zona pellucida. Anatomia Histologia Embryologia 30, 257263.CrossRefGoogle ScholarPubMed
Sprecher, DJ, Baker, JC, Holland, RE and Yamini, B (1991) An outbreak of fetal and neonatal losses associated with the diagnosis of bovine viral diarrhea virus. Theriogenology 36, 597606.CrossRefGoogle Scholar
Ssentongo, YK, Johnson, RH and Smith, JR (1980) Association of bovine viral diarrhoea-mucosal disease virus with ovaritis in cattle. Australian Veterinary Journal 56, 272273.CrossRefGoogle ScholarPubMed
Stetson, DB and Medzhitov, R (2006) Type I interferons in host defense. Immunity 25, 373381.CrossRefGoogle ScholarPubMed
Stott, AW, Humphry, RW, Gunn, GJ, Higgins, I, Hennessy, T, O'Flaherty, J and Graham, DA (2012) Predicted costs and benefits of eradicating BVDV from Ireland. Irish Veterinary Journal 65, 12.CrossRefGoogle ScholarPubMed
Stringfellow, DA, Riddell, KP, Brock, KV, Riddell, MG, Galik, PK, Wright, JC and Hasler, JF (1997) In vitro fertilization and in vitro culture of bovine embryos in the presence of noncytopathic bovine viral diarrhea virus. Theriogenology 48, 171183.CrossRefGoogle ScholarPubMed
Stringfellow, DA, Riddell, KP, Galik, PK, Damiani, P, Bishop, MD and Wright, JC (2000) Quality controls for bovine viral diarrhea virus-free IVF embryos. Theriogenology 53, 827839.CrossRefGoogle ScholarPubMed
Swangchan-Uthai, T, Lavender, CR, Cheng, Z, Fouladi-Nashta, AA and Wathes, DC (2012) Time course of defense mechanisms in bovine endometrium in response to lipopolysaccharide. Biology of Reproduction 87, 135, 113.CrossRefGoogle ScholarPubMed
Thomann, B, Tschopp, A, Magouras, I, Meylan, M, Schupbach-Regula, G and Hasler, B (2017) Economic evaluation of the eradication program for bovine viral diarrhea in the Swiss dairy sector. Preventive Veterinary Medicine 145, 16.CrossRefGoogle ScholarPubMed
Thurmond, MC (2005) Virus transmission. In Goyal, SM and Ridpath, JF (Eds), Bovine Viral Diarrhea Virus: Diagnosis, Management, and Control. Ames, Iowa: Blackwell Publishing, pp. 91104.CrossRefGoogle Scholar
Tsuboi, T and Imada, T (1996) Noncytopathogenic and cytopathogenic bovine viral diarrhea-mucosal disease viruses do not affect in vitro embryonic development into the blastocyst stage. Veterinary Microbiology 49, 127134.CrossRefGoogle Scholar
Tsuboi, T, Osawa, T, Hirata, TI, Kawashima, K, Kimura, K and Haritani, M (2013) Experimental infection of pregnant cows with noncytopathogenic bovine viral diarrhoea virus between days 26 and 50 postbreeding. Research in Veterinary Science 94, 803805.CrossRefGoogle ScholarPubMed
Turvey, SE and Broide, DH (2010) Innate immunity. Journal of Allergy and Clinical Immunology 125, S24S32.CrossRefGoogle ScholarPubMed
Ulbrich, SE, Schulke, K, Groebner, AE, Reichenbach, HD, Angioni, C, Geisslinger, G and Meyer, HH (2009) Quantitative characterization of prostaglandins in the uterus of early pregnant cattle. Reproduction 138, 371382.CrossRefGoogle ScholarPubMed
Valle, PS, Martin, SW and Skjerve, E (2001) Time to first calving and calving interval in bovine virus diarrhoea virus (BVDV) sero-converted dairy herds in Norway. Preventive Veterinary Medicine 51, 1736.CrossRefGoogle ScholarPubMed
Van Reeth, K and Adair, B (1997) Macrophages and respiratory viruses. Pathologie Biologie 45, 184192.Google ScholarPubMed
Vanroose, G, Nauwynck, H, Van Soom, A, Vanopdenbosch, E and de Kruif, A (1998) Replication of cytopathic and noncytopathic bovine viral diarrhea virus in zona-free and zona-intact in vitro-produced bovine embryos and the effect on embryo quality. Biology of Reproduction 58, 857866.CrossRefGoogle ScholarPubMed
Velasova, M, Damaso, A, Prakashbabu, BC, Gibbons, J, Wheelhouse, N, Longbottom, D, Van Winden, S, Green, M and Guitian, J (2017) Herd-level prevalence of selected endemic infectious diseases of dairy cows in Great Britain. Journal of Dairy Science 100, 2159233.CrossRefGoogle ScholarPubMed
Virakul, P, Fahning, ML, Joo, HS and Zemjanis, R (1988) Fertility of cows challenged with a cytopathic strain of bovine viral diarrhea virus during an outbreak of spontaneous infection with a noncytopathic strain. Theriogenology 29, 441449.CrossRefGoogle ScholarPubMed
Voges, H, Horner, GW, Rowe, S and Wellenberg, GJ (1998) Persistent bovine pestivirus infection localized in the testes of an immuno-competent, non-viraemic bull. Veterinary Microbiology 61, 165175.CrossRefGoogle ScholarPubMed
Voges, H, Young, S and Nash, M (2006) Direct adverse effects of persistent BVDV infection in dairy heifers – a retrospective case control study. VetScript 19, 2225.Google Scholar
Walker, CG, Meier, S, Littlejohn, MD, Lehnert, K, Roche, JR and Mitchell, MD (2010) Modulation of the maternal immune system by the pre-implantation embryo. BMC Genomics 11, 474.CrossRefGoogle ScholarPubMed
Walz, PH, Bell, TG, Wells, JL, Grooms, DL, Kaiser, L, Maes, RK and Baker, JC (2001) Relationship between degree of viremia and disease manifestation in calves with experimentally induced bovine viral diarrhea virus infection. American Journal of Veterinary Research 62, 10951103.CrossRefGoogle ScholarPubMed
Walz, PH, Grooms, DL, Passler, T, Ridpath, JF, Tremblay, R, Step, DL, Callan, RJ and Givens, MD (2010) Control of bovine viral diarrhea virus in ruminants. Journal of Veterinary Internal Medicine 24, 476486.CrossRefGoogle ScholarPubMed
Weldegebriel, HT, Gunn, GJ and Stott, AW (2009) Evaluation of producer and consumer benefits resulting from eradication of bovine viral diarrhoea (BVD) in Scotland, United Kingdom. Preventive Veterinary Medicine 88, 4956.CrossRefGoogle Scholar
Welsh, MD, Adair, BM and Foster, JC (1995) Effect of BVD virus infection on alveolar macrophage functions. Veterinary Immunology and Immunopathology 46, 195210.CrossRefGoogle ScholarPubMed
Wernike, K, Gethmann, J, Schirrmeier, H, Schroder, R, Conraths, FJ and Beer, M (2017) Six years (2011–2016) of mandatory nationwide bovine viral diarrhea control in Germany – a success story. Pathogens (Basel, Switzerland) 6, 50.Google Scholar
Williams, EJ, Fischer, DP, Pfeiffer, DU, England, GC, Noakes, DE, Dobson, H and Sheldon, IM (2005) Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63, 102117.CrossRefGoogle ScholarPubMed
Wray, C and Roeder, PL (1987) Effect of bovine virus diarrhoea-mucosal disease virus infection on Salmonella infection in calves. Research in Veterinary Science 42, 213218.CrossRefGoogle ScholarPubMed
Wu, R, Van der Hoek, KH, Ryan, NK, Norman, RJ and Robker, RL (2004) Macrophage contributions to ovarian function. Human Reproduction Update 10, 119133.CrossRefGoogle ScholarPubMed
Yavru, S, Kale, M, Gulay, MS, Yapici, O, Bulut, O and Ata, A (2013) Effects of bovine viral diarrhoea virus on the fertility of cows. Acta Veterinaria Hungarica 61, 281289.CrossRefGoogle ScholarPubMed
Yesilbag, K, Alpay, G and Becher, P (2017) Variability and global distribution of subgenotypes of bovine viral diarrhea virus. Viruses 9, 128.CrossRefGoogle ScholarPubMed
Zhou, Y, Ren, Y, Cong, Y, Mu, Y, Yin, R and Ding, Z (2017) Autophagy induced by bovine viral diarrhea virus infection counteracts apoptosis and innate immune activation. Archives of Virology 162, 31033118.CrossRefGoogle ScholarPubMed