Transplacental Transmission of BTV-8 in Cattle | CDC EID

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Volume 15, Number 12–December 2009
Dispatch
Transplacental Transmission of Bluetongue Virus 8 in Cattle, UK
Karin E. Darpel, Carrie A. Batten, Eva Veronesi, Susanna Williamson, Peter Anderson, Mike Dennison, Stuart Clifford, Ciaran Smith, Lucy Philips, Cornelia Bidewell, Katarzyna Bachanek-Bankowska, Anna Sanders, Abid Bin-Tarif, Anthony J. Wilson, Simon Gubbins, Peter P.C. Mertens, Chris A. Oura, and Philip S. Mellor
Author affiliations: Institute for Animal Health, Pirbright, UK (K.E. Darpel, C.A. Batten, E. Veronesi, K. Bachanek-Bankowska, A. Sanders, A. Bin-Tarif, A.J. Wilson, S. Gubbins, P.P.C. Mertens, C.A. Oura, P.S. Mellor); Veterinary Laboratories Agency, Bury St. Edmunds, UK (S. Williamson, C. Bidewell); Animal Health Divisional Office, Bury St. Edmunds (P. Anderson, S. Clifford, C. Smith, L. Philips); and Animal Health Divisional Office, Chelmsford, UK (M. Dennison)

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Abstract
To determine whether transplacental transmission could explain overwintering of bluetongue virus in the United Kingdom, we studied calves born to dams naturally infected during pregnancy in 2007–08. Approximately 33% were infected transplacentally; some had compromised health. In all infected calves, viral load decreased after birth; no evidence of persistent infection was found.

Bluetongue virus (BTV) is generally transmitted between ruminant hosts by Culicoides biting midges, and infection may result in the disease called bluetongue. In 2006, a strain of BTV-8 caused the first outbreak of bluetongue in northern Europe (1). Although adult Culicoides midges are absent from this region during winter for long enough to interrupt normal transmission, BTV-8 survived the winters of 2006–07 and 2007–08.

Several mechanisms have been suggested to explain the overwintering of BTV, one of which is transplacental transmission (2). Tissue-attenuated strains of BTV are sometimes capable of crossing the placenta and infecting fetuses in utero (3), and transplacental infection has been reported from the field after use of live attenuated vaccines (4). However, many wild-type strains of BTV failed to cross the placental barrier when cows were infected during pregnancy (5). Additionally, although a few studies have reported experimental transplacental infection with wild-type strains, these studies did not recover infectious virus from live offspring (although many field strains do not grow in tissue culture) and suggested that fetal infection often resulted in deformation, stillbirth, or abortion (6,7). Collectively, this information led to the assumption that only viruses passaged in tissue culture had the potential to overwinter by transplacental transmission (8). However, in 2008, nonlethal transplacental transmission of BTV-8 was detected in Northern Ireland (9). To examine the occurrence, rate, and consequences of transplacental BTV-8 transmission in the United Kingdom, we studied calves born to dams naturally infected with BTV-8 during pregnancy.

The Study
After obtaining owners' permission, we sampled calves born to previously infected dams during the vector-free period of December 20, 2007 to March 15, 2008. Farmers were also asked to report any births, abortions, or stillbirths from BTV-infected dams outside the vector-free period. Blood samples from live calves were taken as soon as possible after birth (usually within 4 days) and tested by using a real-time reverse transcription–PCR (rRT-PCR) (10) and the Pourquier c-ELISA kit (IDEXX, Chalfont St. Peter, UK). When possible, information about the health of the calf was obtained, dams were sampled alongside their calves, and placenta samples were collected. Calves with positive BTV RNA results were resampled at 2–3 week intervals. In total, 61 calves were tested and 21 (including 1 set of twins) had detectable levels of BTV RNA in their blood or organs (Appendix Table). The transplacental transmission rate was 33% (95% confidence interval 22%–47%).

All calves except calf 21 and calf X, each of which had not consumed colostrum before sampling, had antibodies against BTV. Calf 21 was also negative for BTV RNA, but calf X showed the highest viral load in the blood (Appendix Table). Virus isolation in KC cells (11) was attempted for all calf blood samples with a cycle threshold (Ct) <29, but virus was isolated from calf X only. Viral RNA load in all calves tested declined over time, and almost all calves were rRT-PCR negative by the end of the study (Table).

When the calves were first sampled, 52 dams were also tested. The RNA load in the calves always exceeded that of their dams, and 7 of the 20 dams giving birth to BTV-positive calves had no detectable viremia.

Of the 21 BTV RNA–positive calves, 5 had compromised health. Calves Y, X, and 33 were born weak and died within hours, days, and weeks after birth, respectively, and calves 13 and 29 exhibited dummy calf syndrome (12). All calves except calf 33 were examined postmortem and had negative PCRs for bovine viral diarrhea virus (S.W., pers. comm.). Although calf X died of colisepticemia, this illness probably resulted from the calf's weakness and inability to consume colostrum. No infectious cause for the early postnatal death of calf Y, other than bluetongue, was identified; pathologic findings for calves 13 and 29 are described elsewhere (S.W. et al., unpub. data). Calf 27, which had negative BTV test results, was born with hypermobility of the fetlock joints, unilateral carpal valgus, and arthrogryposis. All other calves were reported to be healthy.

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