Risk factors associated with exposure to bovine respiratory disease pathogens during the peri-weaning period in dairy bull calves

Research article Open Access Risk factors associated with exposure to bovine respiratory disease pathogens during the peri-weaning period in dairy bull calves Gerard M. Murray1Email author, Simon J. More2, Tracy A. Clegg2, Bernadette Earley3, Rónan G. O’Neill4, Dayle Johnston3, John Gilmore5, Mikhail Nosov5, Máire C. McElroy4, Thomas J. Inzana6 and Joseph P. Cassidy7 BMC Veterinary ResearchBMC series – open, inclusive and trusted201814:53 https://doi.org/10.1186/s12917-018-1372-9 ©  The Author(s). 2018 Received: 11 October 2017Accepted: 14 February 2018Published: 27 February 2018 Abstract Background Bovine respiratory disease (BRD) remains among the leading causes of death of cattle internationally. The objective of this study was to identify risk factors associated with exposure to BRD pathogens during the peri-weaning period (day (d)-14 to d 14 relative to weaning at 0) in dairy bull calves using serological responses to these pathogens as surrogate markers of exposure. Clinically normal Holstein-Friesian and Jersey breed bull calves (n = 72) were group housed in 4 pens using a factorial design with calves of different breeds and planes of nutrition in each pen. Intrinsic, management and clinical data were collected during the pre-weaning (d − 56 to d − 14) period. Calves were gradually weaned over 14 days (d − 14 to d 0). Serological analysis for antibodies against key BRD pathogens (BRSV, BPI3V, BHV-1, BHV-4, BCoV, BVDV and H. somni) was undertaken at d − 14 and d 14. Linear regression models (for BVDV, BPI3V, BHV-1, BHV-4, BCoV and H. somni) and a single mixed effect random variable model (for BRSV) were used to identify risk factors for changes in antibody levels to these pathogens. Results BRSV was the only pathogen which demonstrated clustering by pen. Jersey calves experienced significantly lower changes in BVDV S/P than Holstein-Friesian calves. Animals with a high maximum respiratory score (≥8) recorded significant increases in H. somni S/P during the peri-weaning period when compared to those with respiratory scores of ≤3. Haptoglobin levels of between 1.32 and 1.60 mg/ml at d − 14 were significantly associated with decreases in BHV-1 S/N during the peri-weaning period. Higher BVDV S/P ratios at d − 14 were significantly correlated with increased changes in serological responses to BHV-4 over the peri-weaning period. Conclusions Haptoglobin may have potential as a predictor of exposure to BHV-1. BRSV would appear to play a more significant role at the ‘group’ rather than ‘individual animal’ level. The significant associations between the pre-weaning levels of antibodies to certain BRD pathogens and changes in the levels of antibodies to the various pathogens during the peri-weaning period may reflect a cohort of possibly genetically linked ‘better responders’ among the study population. Keywords CalvesAntibodiesBovine respiratory diseaseDairyExposure Background Bovine respiratory disease (BRD) remains among the leading causes of death of dairy and beef cattle of all ages in Ireland [1] and internationally [2]. Dairy calf pneumonia (enzootic calf pneumonia) represents an epidemiologically distinct component of the BRD complex, typically affecting 2 to 6 month old calves; shipping fever of feedlot cattle and atypical interstitial pneumonia are other recognised syndromes [3]. While indoor or outdoor individual housing of calves has been recognised as beneficial to dairy calf health [4] legislative changes in animal welfare in Ireland and Europe (EU Directive 91/629/EC and EU Decision 97/182/EC) have encouraged group housing of calves, which also facilitates more efficient use of labour and space. However, this shift has presented the dairy industry with new challenges in disease control [5] and increased the risk of BRD among young dairy calves [6–8]. Stress is an important co-factor in the pathogenesis of BRD [9, 10]. Clinically affected calves shedding large numbers of pathogens into the environment act as an important source of exposure for other calves. In addition, BRD pathogens can also be carried and shed by apparently healthy animals [11, 12]. Weaning has been traditionally recognised as a stressful time for calves with both nutritional and non-nutritional factors contributing to weaning distress [13]. Non-nutritional factors such as the breaking of the maternal bond and the rearrangement of the social group tend to be critical factors for beef suckled calves in particular. As dairy calves are generally separated from the dam shortly after birth, weaning distress in the dairy calf typically arises predominantly from nutritional factors [14]. When coupled with the increased interaction and contact of calves in group housing, weaning distress can facilitate the efficient spread of BRD pathogens leading to exposure and, potentially, disease. Inevitably there are interactions and cross-effects between pathogens which together lead to variable and complex immunological and pathological effects in each calf. Many studies have examined the effects of intrinsic [15], management [16, 17] or clinical [18] risk factors for BRD; however, reports as to the various potential risks these variables pose in exposing calves to BRD pathogens are lacking. The objective of this study was to identify risk factors associated with exposure to BRD pathogens during the peri-weaning period in dairy bull calves using serological responses to these pathogens as surrogate markers of exposure. These responses were determined by calculating changes in sample to positive ratios (S/P), percentage positivity (PP) or sample to negative ratios (S/N), to a wide range of recognised BRD pathogens during the peri-weaning period (day (d) -14 to d 14 relative to weaning at d 0). Methods Animal management This study was conducted as part of a larger study designed to examine changes in haematological profiles and gene expression in response to gradual weaning. Ethical approval for this study was sought, and received, from the Teagasc Animal Ethics Committee. Animal management, sample collection and haematological analysis have been outlined previously by Johnston et al. [14]. Briefly, 72 clinically normal bull calves of Jersey or Holstein-Friesian breed were sourced from 2 preferential supplier farms at a mean age of 19 (S.D. 8) days and were group housed indoors in 4 sawdust-floored pens (16, 18, 18 and 20 per pen) from d − 56 (relative to weaning (d 0)) to d 28 of the study. A sample size calculation for linear regression based on a power level of 0.8, significance level of 0.05 and a range of anticipated effects and numbers of predictors suggested a minimum sample range of 59 to 65 animals. Calves were immunised on arrival against bovine herpesvirus 1 (BHV-1; Rispoval IBR Marker Live administered intramuscularly, Zoetis), and, using a combined vaccine (Bovilis Bovipast RSP, MSD, inactivated vaccine administered subcutaneously), they were also (...truncated)