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Risk factors associated with clinical Bacterial Kidney Disease (BKD) in marine farmed Atlantic Salmon (Salmo salar L.) in New Brunswick, Canada

Annette S. Boerlage1, Adel Elghafghuf1, Henrik Stryhn1* and K. Larry Hammell1
  • 1 UPEI, Department of Health Management, Canada

Introduction In a retrospective study of a large number of Atlantic Canadian salmon aquaculture sites between 2006 and 2012, more than half experienced cases of Bacterial Kidney Disease (BKD) (Boerlage et al., in press). Salmon infections with Renibacterium salmoninarum can be subclinical or clinical. In the latter case there are increased levels of mortality and/or clinical signs (Murray et al., 2011). Transmission of BKD can occur vertically (Evelyn et al., 1984; Lee and Evelyn, 1989) and horizontally (Balfry et al., 1996; Evenden et al., 1993). Little analytical research has been done to establish risk factors for mortality attributed to BKD in marine salmon aquaculture. Objective was to identify production and environmental factors associated with infection transmission leading to clinical BKD at marine sites in eastern Canada. Material and Methods The data consisted of 1225 weekly, pen-level records on production information of fish between smolt stocking and harvesting in marine pens between 2006 and 2012. Data structure is depicted in Figure 1. Case definitions for clinical and subclinical BKD were based on industry records of weekly production data including mortalities, field observations compatible with BKD using reports of veterinarians or fish health technicians, diagnostic submissions and test results, and treatments intended for control of BKD (Boerlage et al., in press). There were 215 clinical cases detected using this approach. Hypothesized risk factors for presence of BKD during site production cycles that we could obtain data for, were the vertical transmission factor first hatchery, i.e. the hatchery where eggs were hatched, and last hatchery, i.e. the last hatchery prior to delivery to marine cages. Horizontal transmission factors, grouped in 5 groups, were: 1) Pen-level production characteristics of which some were time-dependent: year, season, stocking year, stocking weight, stocking season (categorized in spring, summer and autumn), weight after first year, percentage of mortality in the first year, percentage of mortality in the first four weeks, harvest weight, duration of previous pen level fallow period, duration of previous site level fallow period, and Food Conversion Ratio (FCR). 2) Clustering factors: the site-level geographical region factor Bay Management Area (BMA), and hatchery system that distinguishes flow-through versus recirculation as the water source for last hatchery. 3) Time dependent treatment information: week of treatment for sea lice, and other diseases. 4) Time-varying horizontal transmission pathway by seaway distances: distance to closest site with subclinical or clinical BKD, and distance to closest site with clinical BKD. 5) Historical BKD status: clinical BKD in the same pen in the previous cycle, clinical BKD in the site in the previous cycle, subclinical BKD in the same pen in the previous cycle, subclinical BKD in the site in the previous cycle. We used Bayesian MCMC estimation of a mixed logistic model, using 20,000 samples as burn-in and 50,000 samples from the posterior distribution obtained after a thinning of 10, with last hatchery, first hatchery, site, and site cycle (i.e. consecutive periods in which at least one pen per site was stocked with fish) as cross-classified random effects to associate the time-independent risk factors with the probability of a pen becoming clinically infected with BKD during its production cycle. The analysis was carried out in STATA 14 (StataCorp, 2015) and MLwiN (www.bristol.ac.uk/cmm). Results The Bayesian model shown has the best (lowest) DIC among models considered with fewer hierarchical levels. BMA was not included because only one BMA of limited practical interest and with no cases had a significant impact. Stocking season and stocking year each had significant effects. Compared to pens stocked in the spring, fewer clinical BKD cases were associated with both summer (OR=0.45; 95% posterior interval 0.17-1.17) and fall stocking (OR=0.10; 0.03-0.32). Clinical BKD cases occurred less frequently for the stocking year 2006 compared to later stocking years (2007 through 2011). Variance components showed that there was an effect of last hatchery (variance = 0.38; 0.01-2.15), little from first hatchery (var = 0.03; 0.00-1.07) but most due to site cycle (var = 3.75;1.83-7.36), and to a much lesser extent to site effects (var = 0.06;0.00-1.92) across site cycles per site. Discussion BKD prevention and management are primarily focused on broodstock screening and preventive treatments (DFO, 2010; Wiens, 2011). This study utilized marine production records, including hatchery and broodstock sources. Although first hatchery was used as an indicator of broodstock origin and, as such, expected to reflect a source for vertical transmission of R. salmoninarum, it explained little of the variation observed. Horizontal transmission within the hatchery may enhance the prevalence of infection if introduced during the freshwater life phase, either through low level vertical transmission or exposure to other infection sources, such as wild freshwater fish populations or contaminated environments. This study detected a small effect related to last hatchery, reflecting a potential component of the risk contributed from freshwater to marine grow out. Similar to findings in Scotland (MSS, 2014), clinical BKD was more frequent if smolt were stocked in the spring compared to the summer and fall. In our study, there was more BKD in stocking years after 2006, but we could not identify any consistent trends beyond this difference. This was consistent with expert opinions reporting no differences in BKD prevalence in saltwater reared salmon in the East coast of Canada during 2000 – 2010 (DFO, 2010). Experts from that same study perceived that a higher prevalence of BKD occurred in certain production sites, regardless of hatcheries (DFO, 2010), thus reflecting perceived importance of site influences. However, we could not find quantitative evidence for this observation. Site cycle, rather than site, explained more variation, but duration of fallow period, a management practice meant to separate different site cycles on the same site, was not significant. Also occurrence of BKD in the previous site cycle had no effect on BKD in the subsequent cycle. This study was meant as a preliminary study to identify risk factors for BKD on sites. Survival analysis modeling is being investigated to elucidate more details about factors affecting the time to a first clinical occurrence of BKD in a pen.

Figure 1
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Acknowledgements

Acknowledgements
The authors wish to acknowledge the industry partner, Cooke Aquaculture, and their veterinary team for their cooperation. This research was undertaken thanks to funding from the Canada Excellence Research Chairs program and Innovation PEI. The authors wish to thank William Chalmers for editorial assistance with the manuscript.

References

References
Balfry, S., Albright, L., Evelyn, T., 1996. Horizontal transfer of Renibacterium salmoninarum among farmed salmonids via the fecal-oral route. Diseases of Aquatic Organisms 25, 63-69.
Boerlage, A., Stryhn, H., Sanchez, J., Hammell, K.L., in press. Case definition for clinical and subclinical Bacterial Kidney Disease (BKD) in Atlantic Salmon (Salmo salar L.) in New Brunswick, Canada.
DFO, B.c.f.a.h.s.f., 2010. Evaluation of Bacterial Kidney Disease (BKD) impacts on the Canadian salmon aquaculture industry, p. 32.
Evelyn, T., Ketcheson, J., Prosperi-Porta, L., 1984. Further evidence for the presence of Renibacterium salmoninarum in salmonid eggs and for the failure of povidone‐iodine to reduce the intra‐ovum infection rate in water‐hardened eggs. Journal of fish diseases 7, 173-182.
Evenden, A., Grayson, T., Gilpin, M., Munn, C., 1993. Renibacterium salmoninarum and bacterial kidney disease—the unfinished jigsaw. Annual Review of Fish Diseases 3, 87-104.
Lee, E., Evelyn, T., 1989. Effect of Renibacterium salmoninarum levels in the ovarian fluid of spawning chinook salmon on the prevalence of the pathogen in their eggs and progeny. Diseases of Aquatic Organisms 7, 179-184.
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Murray, A.G., Hall, M., Munro, L.A., Wallace, I.S., 2011. Modelling management strategies for a disease including undetected sub-clinical infection: Bacterial kidney disease in Scottish salmon and trout farms. Epidemics 3, 171-182.
StataCorp, 2015. Stata Statistical Software: Release 14. College Station, TX: StataCorp LP.
Wiens, G.D., 2011. Bacterial kidney disease (Renibacterium salmoninarum). in: Woo, P.T.K., Bruno, D.W. (Eds.), Fish diseases and disorders. Volume 3: viral, bacterial and fungal infections. 2nd edition. CABI, Wallingford, pp. 338-374.

Keywords: Bacterial Kidney Disease, survival analysis, Atlantic salmon, Canada, transmission, Risk factors

Conference: AquaEpi I - 2016, Oslo, Norway, 20 Sep - 22 Sep, 2016.

Presentation Type: Oral

Topic: Aquatic Animal Epidemiology

Citation: Boerlage AS, Elghafghuf A, Stryhn H and Hammell K (2016). Risk factors associated with clinical Bacterial Kidney Disease (BKD) in marine farmed Atlantic Salmon (Salmo salar L.) in New Brunswick, Canada. Front. Vet. Sci. Conference Abstract: AquaEpi I - 2016. doi: 10.3389/conf.FVETS.2016.02.00059

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Received: 30 May 2016; Published Online: 14 Sep 2016.

* Correspondence: PhD. Henrik Stryhn, UPEI, Department of Health Management, Charlottetown, PE, C1A 4P3, Canada, hstryhn@upei.ca