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While the prevalence of infectious bursal disease virus (IBDV) on chicken farms in some provinces of Canada has been documented, the economic impact of variant IBDV infection on the broiler chicken industry in Saskatchewan has not. The objectives of this study were to identify the variant strains of IBDV circulating on Saskatchewan chicken farms and evaluate their economic impact on broiler production. Infection due to IBDV was detected in 43% of Saskatchewan chicken farms, with variant strains detected in infected birds closely related predominantly to NC171, 586, and Delaware-E. Infected flocks showed an IBDV antibody titer of 4236 geometric mean (GM), whereas an antibody titer of 157 GM was measured in uninfected flocks. Infected flocks had very low (0.06) bursa-to-body-weight (BBW) ratio (an indicator of immunity) compared to high BBW ratio (0.17) in uninfected flocks, which suggests a significant immunosuppression in the former. Flocks positive for IBDV had mean mortality of 8.6% and mean condemnation of 1.5%. In contrast, mean mortality in uninfected flocks was 6.1% and mean condemnation was 1.1%. The live market weight per grow area at 37 d of age was 29.3 kg/m2 in infected flocks and 34.0 kg/m2 in flocks without IBDV infection. Flock mortality and condemnation rate were positively correlated with IBDV infection, whereas low BBW ratio was inversely correlated, as expected. Overall, IBDV-infected flocks had higher mortality, bursal atrophy, poorer feed conversion ratio (FCR), and decreased meat production. Our data suggest that the broiler chicken industry in Saskatchewan loses 3.9 million kilograms of meat production per year due to variant IBDV strains.
Bien que la prévalence du virus de la maladie infectieuse de la bourse (VMIB) sur les fermes de poulets dans quelques provinces canadiennes ait été documentée, l’impact économique d’infections par des variants du VMIB sur l’industrie du poulet à griller en Saskatchewan ne l’est pas. Les objectifs de la présente étude étaient d’identifier les souches variantes du VMIB circulant au sein des fermes de poulet de la Saskatchewan et d’évaluer leur impact économique sur la production de poulets à griller. L’infection due au VMIB a été détectée sur 43 % des fermes de poulet de la Saskatchewan, avec des souches variantes détectées chez des oiseaux infectés étant fortement apparentées en prédominance aux souches NC171, 586, et Delaware-E. Les troupeaux infectés présentaient une moyenne géométrique (MG) des titres d’anticorps contre le VMIB de 4236, alors que la MG des titres d’anticorps des oiseaux provenant de troupeaux non-infectés était de 157. Les troupeaux infectés avaient un très faible ratio (0,06) du poids bourse-poids corporel (BPC) (un indicateur de l’immunité) comparativement au ratio BPC élevé (0,17) dans les troupeaux non-infectés, ce qui suggère une immunosuppression significative dans les troupeaux infectés. Les troupeaux positifs au VMIB avaient un taux de mortalité moyen de 8,6 % et un taux de condamnation moyen de 1,5 %. À l’opposé, dans les troupeaux non-infectés le taux de mortalité moyen était de 6,1 % et le taux de condamnation moyen de 1,1 %. Le poids vif de marché à 37 j d’âge par surface de croissance était de 29,3 kg/m2 dans les troupeaux infectés et de 34,0 kg/m2 dans les troupeaux sans infection par VMIB. La mortalité dans le troupeau et le taux de condamnation étaient corrélés positivement avec l’infection par VMIB, alors qu’un faible ratio BPC était corrélé, tel qu’attendu, de manière inverse. De manière générale, les troupeaux infectés par le VMIB présentaient une mortalité plus élevée, une atrophie de la bourse, un mauvais ratio de conversion alimentaire, et une production de viande réduite. Nos données suggèrent que l’industrie du poulet à griller en Saskatchewan perd annuellement 3,9 millions de kilogrammes de production de viande à cause des souches variantes du VMIB.
(Traduit par Docteur Serge Messier)
Infectious bursal disease (IBD) is a highly contagious immunosuppressive disease that causes serious problems for the poultry industry worldwide (1). The disease is also known as Gumboro disease as it was first recognized in the United States near the town of Gumboro, Delaware (2). Infectious bursal disease is caused by the IBD virus (IBDV), a double-stranded ribonucleic acid (RNA) virus that belongs to the genus Avibirnavirus of the family Birnaviridae (3). The IBD virus exists in classical and variant forms that are antigenically distinct (2). Emergence of variant IBDV strains has caused substantial losses in the poultry industry. Most IBDV strains circulating in the United States (2) and Canada (4) are variant strains. Infection by IBDV can cause direct economic loss due to specific mortality (1,2). The indirect economic impact of IBD is profound, however, due to IBDV-induced immunosuppression that predisposes chickens to secondary infections by bacteria, viruses, and parasites, and results in increased mortality, growth retardation, and condemnation (5–7).
Infection by the IBD virus targets the bursa of Fabricius (BF) and results in severe immunosuppression due to loss of lymphocytes in the BF (8,9). There is strong evidence that surface immunoglobulin M-bearing B-lymphocytes are the major targets for IBDV (8,10). Variant IBDV strains (11,12) in neonatal chickens can escape from the maternal antibodies (MAb) against IBDV that are produced by broiler breeders immunized with standard or classic IBDV strain vaccines (7) and induce severe bursal damage (13–16). This results in profound immunosuppression and subclinical infections (16,17). Immunosuppression is greatest when infection occurs early post-hatch and is permanent because the damaged BF does not regenerate normal immune function. As the immunosuppression resulting from an IBDV infection is often the underlying cause of respiratory and enteric disease in chickens, as well as vaccination failures, IBD is an economically significant disease throughout the world (11). It may also precipitate a variety of other diseases or conditions that could play a role in airsacculitis, septicemia, toxemia, increasing condemnations, and decreasing broiler growth rate (10,13).
Although variant IBDV infection has recently been confirmed on Canadian chicken farms (18), its economic impact on the Saskatchewan broiler chicken industry has not been studied. The objectives of this study were to identify the incidence of variant IBDV infection and to evaluate the associated economic losses in the broiler chicken industry in Saskatchewan, Canada.
This study was conducted over a 5-year period, with sample collection occurring in 2007, 2009, and 2011. According to the Chicken Farmers of Saskatchewan, there were 63 broiler farms in the Saskatchewan broiler chicken industry from 2007 to 2011. In 2007, the incidence of IBDV was studied by histologic examination of the bursa of Fabricius (BF) and polymerase chain reaction (PCR). A follow-up survey was conducted in 2009 to obtain major economic parameters, such as farm and flock (birds kept in a barn on a poultry farm) information, feed conversion ratio (FCR), and stocking density, in addition to histologic examination of BF, bursa-to-body-weight (BBW) ratio, and serology against IBDV. Another follow-up study was conducted in 2011 at those farms that were found to have been infected with IBDV in 2007 and 2009.
In 2007, 177 flocks managed by 58 of 63 broiler farms (92%) were chosen for this study. Bursas were collected from 40 randomly selected birds from farms with multiple barns (flocks) and from 20 birds from farms with only 1 barn (flock) at the time of processing for histologic examination throughout the 1-year period. Tissue sections of bursae were fixed in 10% neutral-buffered formalin, embedded in paraffin, sectioned at a thickness of 5 μm, and stained with hematoxylin and eosin (H&E). A histologic score from 0 to 3 (0 = no visible lesions; 1 = mild, focal lymphoid depletion; 2 = moderate, multifocal lymphoid depletion; and 3 = moderate to severe multifocal lymphoid depletion) was assigned based on the tissue reactions of the BF (Figure 1). A bursal score was assigned to each bird and a cumulative score was determined per flock with the lowest score being 0 (no bursal atrophy) and the highest score being 60 (20 birds per flock with severe bursal atrophy). All farms with bursal atrophy and 10 farms with no bursal atrophy on histologic examination were further examined by collecting bursae from 10 randomly selected birds at 19 d of age for identifying IBDV by real-time polymerase chain reaction (RT-PCR) and nucleotide sequence analysis of the viral protein 2 (VP2) hypervariable region (19). This was carried out at the Animal Health Laboratory (AHL), University of Guelph, Ontario, as described previously (4). Chickens were vaccinated for IBDV 10 to 14 d post-hatch in 4 out of 58 farms (2 farms with IBDV infection and another 2 farms without IBDV infection) with Clonevac D-78 (Intervet Canada, Whitby, Ontario).
In 2009, a follow-up survey was conducted to collect data from the same 58 farms (177 barns) on the following broiler production variables: number of barns (flocks) per farm; type of barn; age and flooring of barns; total number of birds placed; stocking density; downtime between flocks; vaccines administered; FCR; age at slaughter; market weight; total birds processed; and total flock mortality, including culled birds and total condemnations at the time of processing. For each barn, data were collected from 1 production cycle from April to June, 2009. In addition to collecting production data at all participating locations, additional studies were done on some farms. At the time of processing, sets of 20 birds were randomly selected from 52 of 177 barns for IBDV serology, BBW ratio, and histologic examination of BF.
In 2011, a follow-up serological study for IBDV was conducted in 82 of 177 barns (located on 25 of 58 farms) that were confirmed to have had IBDV infection in 2007 and 2009. Confirmation of IBDV in farms was defined as the presence of 2 out of 3 criteria associated with IBDV infection, namely IBDV titer, BBW ratio, or bursal atrophy score. Infectious bursal disease (IBD) virus titers were assayed using commercial enzyme-linked immunosorbent assay (ELISA) kits according to manufacturer’s instructions (IDEXX, Westbrook, Maine, USA) at the AHL, University of Guelph, Ontario.
Descriptive statistics and correlations among observed variables were calculated using Prism 5.0 (GraphPad Software, San Diego, California, USA). Geometric means (GM) were used to describe the central tendency of variables that were not normally distributed (antibody titer) and arithmetic means were used for the remaining variables. The indicators of infection and disease (cumulative histopathology score of the BF, BBW ratio, and IBDV GM titer) were considered individually in order to determine the classification of farms. Wilcoxon Rank-Sum Test was used to demonstrate the significance of differences in the central values of samples from each category of farm. Stepwise logistic regression was used to analyze the production variables [downtime between flocks, FCR, and meat production per square meter at 37 d of age (kg37/m2)] in flocks with or without IBDV infection using Statistix 7 (Analytical Software, Tallahassee, Florida, USA).
The histologic study conducted in 2007 classified 33 of 58 farms (57%) with minimal to no bursal damage and a mean cumulative score of 0.24 per farm. In contrast, 25 of 58 premises (43%) had moderate to severe bursal damage, with a mean cumulative score of 40.3 per farm (Figure 1). No variant IBDVs were isolated in 10 of 33 farms with minimal to no bursal atrophy on histologic examination. In contrast, variant IBDV strains similar to NC171, 586, and Delaware E were isolated from 19-day-old broilers in 12 of the 25 farms with moderate to severe bursal atrophy (Figure 2).
Production variables were collected from 58 broiler farms (177 barns) in Saskatchewan. Of 58 farms, 10 farms had a single barn, 15 farms had 2 barns, 18 farms had 3 barns, 10 farms had 4 barns, and the remaining 5 farms had 5 to 13 barns. The barns on 36 of 58 farms were ≥ 10 years old and 1 to 9 years old on 22 of 58 farms. Forty-seven of 58 farms had single-story barns, 5 of 58 farms had double-story barns, and the remaining 6 farms had both single- and double-story barns. Twenty-seven of 58 farms had concrete floors and the remaining farms had a combination of partial concrete, clay, sand, wood, or soil floors. The mean floor area of a barn was 4143 m2 and ranged from 743 to 14 864 m2. The median distance between processing plant and farm was 160 km, with a range of 2 to 411 km (Table I).
The mean placement on a farm was 69 048 birds, ranging from 13 000 to 217 700 birds. The mean bird density was 0.06 m2/bird, ranging from 0.04 to 0.09 m2/bird. The mean age at marketing was 37 d and ranged from 33 to 45 d. The mean market weight of a bird was 2.02 kg and ranged from 1.60 to 2.58 kg. The mean FCR was 1.83 and ranged from 1.59 to 2.22. The mean live bird production was 32.36 kg/m2 and ranged from 21.48 to 49.60 kg/m2. The mean mortality, including culled birds, was 7.04% and ranged from 1.26 to 20.7%. The mean BBW on a farm was 0.11% and ranged from 0.04% to 0.21%. The mean condemnation was 1.25% and ranged from 0.07% to 4.94%. Thirty-six of 58 farms maintained 9 d or longer downtime between flocks after cleaning and disinfection were completed. All broiler placements in Saskatchewan were supplied by 2 hatcheries and all broiler flocks were processed by 2 processing plants (Table I).
Infectious bursal disease (IBD) virus titers were positively correlated with the cumulative histologic score of the BF (r = 0.71, P = 0.0001), flock mortality (r = 0.47, P = 0.02), condemnation rates (r = 0.44, P = 0.02) and negatively correlated with BBW ratio (r = −0.79, P = 0.000001). The condemnation rates at the time of processing were negatively correlated with the downtime between flocks (r = −0.31, P = 0.02) and BBW ratio (r = −0.53, P = 0.005). There is no significant correlation between broiler breeder IBDV vaccination against bursal atrophy, BBW ratio, or IBDV titer (r = 0.25, P = 0.25; r = −0.27, P = 0.19; and r = 0.30, P = 0.19, respectively).
Confirmation of IBDV in farms was defined as the presence of 2 of 3 criteria associated with IBDV infection, namely IBDV titer, BBW ratio, or bursal atrophy on histologic examination, as already described. Birds from farms with IBDV infection had a GM titer of 4236 (1578 to 7466) to IBDV. In contrast, farms with no IBDV infection had a GM titer of 157 (2 to 788) to IBDV. Farms with IBDV infection had a BBW ratio of 0.06 (0.04 to 0.08), while farms with no IBDV infection had a BBW ratio of 0.17 (0.13 to 0.21). Farms with IBDV infection had a cumulative histologic score of 49.58 (20.30 to 58.75), while farms with no IBDV infection had a cumulative histologic score of 2.11 (0.50 to 4.75). The FCR on farms with IBDV infection was 1.87, while the FCR was 1.81 in farms with no IBDV infection. The mean mortality was 8.6% (4.35% to 20.7%) in farms with IBDV infection and 6.1% (1.26% to 18.6%) on farms with no IBDV infection. The mean condemnation rate was 1.48% (0.25% to 4.94%) on farms with IBDV infection and 1.12% (0.07% to 4.6%) on farms with no IBDV infection. The live market weight per grow area (meat production) was 29.3 kg37/m2 on farms with IBDV infection and 34.0 kg37/m2 on farms with no IBDV infection (Table II).
On average, broiler producers repeat 6.5 production cycles per year. Based on our data (number of barns infected with IBDV, number of birds in barns infected with IBDV, difference in kg37/m2 meat production in barns with and without IBDV infection, and number of production cycles per year), the broiler chicken industry in Saskatchewan loses approximately 3.9 million kg per year due to “variant” IBDV infection. In 2014, this amount of chicken had a wholesale market value of over $13 million. (The wholesale price of chicken was $3.58/kg in 2014, according to the 2014 Annual Report of the Chicken Farmers of Canada.)
Of 58 farms studied, 10 out of 33 farms were without any sign of IBDV infection, i.e., no bursal atrophy, no IBDV detection, and low titers against IBDV in 2007 and 2009, and had an average IBDV GM titer of 42.6 (27 to 336) in 2011. In contrast, 23 out of 25 farms (92%) with a history of IBDV infection in 2007 and 2009 had an average IBDV GM titer of 4063 (1104 to 9412). Only 2 out of 25 farms (8%) with IBDV infection in both 2007 and 2009 had a GM IBDV titer in 2011 that was classified as low (< 50). These 2 farms had a GM IBDV titer of 34.5 (26 to 43). Twenty-three of 25 farms (92%) maintained IBDV infection from 2007 to 2011.
The economic impact of infectious bursal disease (IBD) on the chicken industry is difficult to assess due to the complex nature of losses associated with this disease. In addition to direct losses, IBDV infection-induced immunodeficiency in chickens opens the door to other viral, bacterial, and parasitic infections, thus inflicting heavy indirect losses due to increased morbidity, mortality, and condemnation (6). Moreover, IBD viruses are resistant to many disinfectants and environmental factors. Once a poultry house becomes contaminated with IBDV, viruses persist on the premises and disease tends to reappear in subsequent flocks (20). An effective IBDV prevention and control program must involve an effective surveillance strategy. This 5-year study was started in 2007 to investigate the prevalence and persistence of IBDV on Saskatchewan chicken farms and assess the financial impact on the chicken industry.
In 2007, histologic study identified 43% of farms with bursal atrophy, where RT-PCR and sequencing associated these 43% of farms with variant IBDV infection. The remaining 57% of premises showed no bursal atrophy and IBDV infection was not detected. Bursal atrophy, low BBW ratio, and high IBDV titers were noted in farms with 5 or more barns, hence bursal atrophy was noted in 93 of 177 barns or broiler flocks (53%) in 2007 (Table II).
In 2009, a positive correlation of IBDV antibody titer with bursal atrophy and a negative correlation of IBDV antibody titer with BBW ratio were observed. Bursa-to-body-weight (BBW) ratio was also negatively correlated with condemnation rates. Phylogenetic analysis of VP2 sequences (19) obtained from the viruses isolated from the BF of 19-day-old broilers revealed that the IBDV strains circulating on Saskatchewan chicken farms with bursal atrophy are variant strains closely related to NC171, 586, and Delaware-E (Figure 2).
Flocks at premises infected with variant IBDV in 2007 and 2009 were tested again for the presence of IBDV antibodies in 2011 and 92% of these premises were serologically positive. It appeared that IBDV infection persisted for at least 4 y in broiler farms once they were infected. Infectious bursal disease (IBD) virus infection was controlled in only 2 of 25 farms that had few (3 or 4) barns. This indicates that control of IBDV infection was manageable in small farms with few barns. Furthermore, the incidence of IBDV infection remained very low (10%; 1 of 10 farms) in farms with a single broiler barn. In contrast, farms with 4 or more barns had a much higher incidence (87%; 13 of 15 farms) of IBDV infection.
Farms with IBDV infection had higher IBDV titers, poorer FCR, higher mortality, more bursal atrophy, higher condemnation rates, and less meat production than premises without IBDV infection. Farms with no detectable IBDV infection had better economical parameters, including better feed conversion ratio (FCR), lower mortality, and decreased condemnation rates. The live market weight per grow area was 29.3 kg37/m2 in farms with IBDV infection and 34.0 kg37/m2 in farms with no IBDV infection. Broiler farms in Saskatchewan follow 6.5 production cycles per year. Since IBDV infection was noted in 53% of barns [25 of 58 (43%) of farms] in the Saskatchewan broiler industry, the projected total production loss was 3.9 million kg in barns infected with IBDV.
While the present data showing significant economic losses due to IBDV infection is in agreement with previous studies (21), it is difficult to determine whether all the losses were due to IBDV alone or there were other contributing factors related to management, environment, and feed. We have seen a reduced weight gain of 160 to 200 g per bird at 35 d old in commercial broilers after experimental infection with NC171 compared to control birds receiving no IBDV in our level-2 animal isolation facility (22).
Less downtime between flocks was correlated with increased condemnation rates. Infectious bursal disease (IBD) virus titer was not correlated with downtime, however, which reflects the persistence of IBDV in a broiler barn for a long duration, as reported previously (23). According to the survey data, the Saskatchewan industry practiced downtime of 1.5 to 22 d between flocks. It is likely that this duration of downtime is not sufficient to reduce IBDV load in a barn, especially when thorough cleaning and disinfection are not practiced. Infectious bursal disease (IBD) virus is very resistant to most disinfectants and environmental factors and persists for months in contaminated poultry houses and for weeks in water, feed, and fecal droppings (23). Although barns were cleaned and disinfected after each cycle of birds in the study area, we have shown that IBDV infection was more prevalent in older barns and barns with no concrete floors probably because these types of facilities are more difficult to thoroughly clean and disinfect.
Based on our data, it is concluded that unique variant IBDV strains were prevalent on Saskatchewan farms and probably attributed to substantial economic losses of about 3.9 million kg per year in the broiler chicken industry in Saskatchewan. Furthermore, it may suggest that current broiler and broiler breeder vaccination programs are not effective for controlling variant IBDV infections. Studies to identify potential vaccine candidates to control variant IBDV in Saskatchewan are urgently needed.
Financial grants were provided by the Chicken Farmers of Saskatchewan (Saskatchewan Chicken Industry Development Fund), Saskatchewan Agriculture Development Fund, and Natural Sciences and Engineering Research Council. Special thanks are extended to all broiler producers in Saskatchewan who participated in this study. Special thanks also to Sofina Foods Inc. (Lilydale Inc.), Wynyard, Saskatchewan and Prairie Pride Natural Foods Ltd., Saskatoon, Saskatchewan for helping with sample collection. Thanks to Drs. Azita Taghavi, Angela Oranchuk, Brenda Bryan, and Tara Funk for assisting with data collection and histologic examinations.