Article Case-control study investigating an anthrax outbreak in Saskatchewan, Canada — Summer 2006 Tasha Epp, Cheryl Waldner, Connie K. Argue Abstract — In 2006, an outbreak of anthrax in Saskatchewan affected several species but most of the losses occurred in cattle. Potential risk factors contributing to this outbreak were investigated through questionnaires involving 117 case farms and 259 control farms geographically representative of the Saskatchewan beef herd. The occurrence of flooding [odds ratio (OR) = 3.4; 95% confidence interval (CI): 1.8 to 6.4], wetter pastures (Good: OR = 3.5; 95% CI: 1.4 to 8.5; Wet: OR = 7.2; 95% CI: 2.9 to 18.1), shorter pasture grass length (OR = 3.0; 95% CI: 1.4 to 6.4), and higher density of the animals on pasture (OR = 3.0; 95% CI: 1.6 to 5.7) were more likely to have been reported for case herds than for control herds. Case farms were more likely than control farms to have vaccinated more than 1 week after the first reported case in the rural municipality (OR = 6.3; 95% CI: 2.6 to 15.3). Timing of vaccination in case herds was also significantly associated with the occurrence of subsequent deaths on these farms (P = 0.001). Résumé — Étude de cas témoins examinant une éclosion d’anthrax en Saskatchewan, au Canada — Été 2006. En 2006, une éclosion d’anthrax en Saskatchewan a touché plusieurs espèces mais la plupart des pertes se sont produites chez le bétail. Les facteurs de risque potentiels contribuant à cette éclosion ont été étudiés en utilisant des questionnaires touchant 117 exploitations agricoles ayant observé des cas et 259 exploitations agricoles témoins représentatives du troupeau bovin de la Saskatchewan. Il était plus probable que la présence d’inondations [ratio d’incidence approché (RI) = 3,4; intervalle de confiance de 95 % (IC) : de 1,8 à 6,4], de pâturages plus humides (bons : RI = 3,5; 95 % IC : de 1,4 à 8,5; humides : RI = 7,2; 95 % IC : de 2,9 à 18,1), de pâturages avec de l’herbe plus courte (RI = 3,0; 95 % IC : de 1,4 à 6,4) et d’une densité supérieure d’animaux sur le pâturage (RI = 3,0; 95 % IC : de 1,6 à 5,7) ait été signalée pour les troupeaux de cas que pour les troupeaux témoins. Il était plus probable que les exploitations agricoles de cas aient procédé à la vaccination plus de 1 semaine après le premier cas signalé dans la municipalité rurale que les exploitations témoins (RI = 6,3; 95 % IC : de 2,6 à 15,3). Le moment de la vaccination des troupeaux de cas était aussi significativement associé à la présence de morts subséquentes dans ces exploitations (P = 0,001). (Traduit par Isabelle Vallières) Can Vet J 2010;51:973–978
A
Introduction
nthrax can affect all mammals, but is most commonly seen in grazing animals that acquire infection with the sporeforming bacteria Bacillus anthracis from contaminated vegetation or soil (1,2). Under the Health of Animals Act and Regulations, all cases of anthrax in Canada must be reported to the Canadian
Food Inspection Agency (CFIA) (http://www.inspection.gc.ca). Anthrax is also an annually reportable disease with the Office international des épizooties (OIE). In 2006, 59 countries confirmed at least 1 outbreak of anthrax (3). Canada reports outbreaks sporadically in wild bison in northern Canada and domestic livestock herds on the prairie provinces, particularly cattle (1,2).
Large Animal Clinical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, 52 Campus Drive, Saskatoon, Saskatchewan S7N 5B4 (Epp, Waldner); Canadian Food Inspection Agency, Terrestrial Animal Health Division, 1115–57th Avenue NE, Calgary, Alberta T2E 9B2 (Argue). Address all correspondence to Dr. Tasha Epp; e-mail:
[email protected] Reprints will not be available from the authors. Financial support was provided by the Canadian Food Inspection Agency. Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (
[email protected]) for additional copies or permission to use this material elsewhere. CVJ / VOL 51 / SEPTEMBER 2010
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In 2006, the CFIA investigated more than 800 livestock deaths at over 150 farm locations in the province of Saskatchewan (4). The first case of anthrax was diagnosed in mid to late June and the outbreak continued until September 21. The most commonly affected animals were cattle. The control strategy of the CFIA included a combination of quarantine, vaccination, and proper carcass handling and disposal. Vaccination was mandatory on infected premises and was suggested for all susceptible animals on other premises within the outbreak area (4). The initial investigators speculated that meteorological conditions in 2006 could have increased exposure to anthrax spores in the environment (4). The area involved had experienced higher than average precipitation levels since the fall of the previous year, which was followed by a hot, dry summer. Past research into anthrax outbreaks in North America indicated that flooding and drought, one or more land disturbances, biological vectors (birds, insects, or other scavengers), or exposure to grazing of previous low-lying sloughs or temporary areas of standing water may precipitate outbreaks (2,5–9). Vaccination has been highly effective in preventing anthrax on farms, specifically if given prior to the season in which outbreaks generally occur (6–9). A case-control study designed to examine risk factors associated with farms reporting cases of anthrax in cattle in Saskatchewan in 2006 is described herein. Investigators focused on farm-level management and environmental risk factors associated with anthrax occurrence. In addition, investigators explored the importance of the timing of vaccination during an outbreak on its effectiveness as a control measure.
Materials and methods Study area The study area was defined as the southern portion of the province of Saskatchewan (SK), Canada. This is the geographical extent of most of the land mass dedicated to agriculture in the province and the majority of both human and livestock populations.
Case farm selection An individual case was defined as an animal with classic symptoms of anthrax, including sudden death, sudden illness characterized by bleeding, difficulty breathing, or edema that rapidly progressed to death. All individual anthrax cases were either confirmed as a positive by the CFIA Lethbridge Laboratory (Lethbridge, Alberta), an OIE Reference Laboratory for anthrax, or were located on a premise with a previously confirmed positive animal (4). Any suspected-positive samples diagnosed in the non-accredited Prairie Diagnostic Services laboratory, Saskatoon, SK, were sent to the CFIA laboratory in Lethbridge for confirmation. A case farm was defined as a farm with 1 or more animals confirmed with anthrax. These farms were entered into a database which contained the legal land location, date of first death, date of last death, number of deaths, date of vaccination for anthrax, species affected, and the total number of animals on the farm. If a farm had more than 1 parcel of land with anthrax cases separated by a distance of 1.6 km (1 mile) or a physical barrier such as a road, they were considered separate 974
farm locations for the analysis. Of all case farms involved in the outbreak, only those which had at least 1 bovine animal on the premise (which may or may not have been affected by anthrax) were included in the analysis. Once anthrax was either suspected or confirmed by the laboratory, a CFIA inspector declared the farm an anthrax positive location and visited the site to ensure that carcasses were disposed of appropriately. At that time (summer of 2006), the CFIA inspector administered a questionnaire that had been developed by the CFIA. The questionnaire was designed to collect information from the herd owner on animal management, location, number of deaths, and disposal method. In 2007, all case farms fitting the criteria for this study were identified using both the CFIA internal electronic database and completed paper copies of the questionnaire information collected in 2006.
Control farm selection In early 2007, the study area was divided into 17 agricultural census divisions based on defined Statistic Canada geographical boundaries to develop a geographically stratified sampling frame for the selection of control or reference herds for a casecontrol study. The goal of this selection process was to enroll a minimum of 250 control farms across the entire study area. Within each of these agricultural census divisions, Statistics Canada 2006 agriculture census database information was used to determine the minimum number of beef farms to contact per census division to create a control group that represented the geographic distribution of beef cow herds in Saskatchewan. Investigators contacted veterinary clinics in each census division until at least 1 agreed to help identify suitable control farms. Participating veterinary clinics provided a list of clients who indicated that they would be willing to complete a short telephone survey and whose operation met the study definition for a control farm. A “control farm” was a farm that had had no evidence of anthrax or suspicious deaths in 2006. Study personnel employed by the CFIA contacted farm owners by phone in the summer of 2007. Those owners who agreed to participate were interviewed using a standardized interview format about farm management practices and environmental conditions from 2006.
Questionnaire data for risk factor analysis Owners of both case and control farms were asked questions pertaining to the environmental conditions of the farm site and management of the livestock on the premises. The owner was directed to answer the pasture-related questions for the field in which cases had occurred or, for control farms, the specific field(s) used the most during the months of June, July, and August in 2006. These yes or no questions included: whether or not running water was present on the farm site, if a mineral supplement had been used, if there had been any unexplained deaths on the farm in previous years (not related to this anthrax outbreak), if any dead wildlife had been found on the farm in previous years, whether or not there had been surface disruption in the previous 3 mo, if there had been flooding (beyond expected spring runoff for their property) on the farm location in the previous 3 mo, and whether or not insect repellent had CVJ / VOL 51 / SEPTEMBER 2010
Table 1. Summary of the questionnaire information comparing case and control farms and the results of the unconditional logistic regression analysis for the association between each variable and farm status Variables
Total number of herds (N)
Case farms
Control farms
P-value
Stagnant 376 Fresh Combination Unknown
50 32 17 18
140 70 45 4
0.55
Running water
No 344 Yes
47 42
146 109
0.47
Mineral use
No 345 Yes
20 69
57 199
0.97
Wildlife deaths
No 349 Yes
80 12
222 35
0.89
Standing water
None 346 0–25% 25–50% 50–100%
12 67 9 1
31 215 10 1
0.14
Bush cover
None 347 0–25% 25–50% 50–100%
19 52 20 3
66 138 42 7
0.61
Surface disruptions
No 346 Yes
82 9
211 44
0.1
Unexplained deaths
No 349 Yes
67 25
218 39
0.01
Flooding
No 347 Yes
24 67
145 111
, 0.001
Grass length
Very short/short 337 Adequate/long
21 61
37 218
0.02
Pasture condition
Dry 348 Good Wet/very wet
9 39 43
82 114 61
, 0.001
Insecticide — eartags
No 345 Yes
88 2
243 12
0.32
Insecticide — oiler
No 345 Yes
72 18
186 69
0.19
Density — categorical
Up to 1 animal/acre 343 1 or more animals/acre
50 37
219 37
, 0.001
Timing of vaccinationa (in relation to first case in RM)
Not vaccinated
218
2
216
NA
Vaccinated before or within 1 wk of first RMb case
157
51
35
, 0.001
Vaccinated . 1 wk after first RM case
64
7
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Source of water
a Timing
of vaccination was examined only for those herds that were vaccinated because all case farms were required to vaccinate other remaining animals on pasture. — rural municipality.
b RM
been used during the summer months of 2006. Answers to additional questions about the source of water, what percentage of the farm location was covered in bush or standing water, grass length, and pasture condition (wetness) were reported as categories (Table 1). The density of animals per acre of land was estimated from data gathered on the questionnaires and was defined as the number of animals recorded on the premise divided by the total number of acres of the contiguous pasture(s). The contiguous pastures were those where the cases occurred, or the specific CVJ / VOL 51 / SEPTEMBER 2010
field used most during the 2006 season. Grazing density was categorized into , 1 animal/acre and $ 1 animal/acre. Finally, the owners were asked whether or not they vaccinated for anthrax, and, if so, the date of vaccination and if a booster was given.
Data analysis Data were analyzed using logistic regression (SPSS, Chicago, Illionois, USA) where the outcome of interest was farm status (case or control). The strength of association between farm 975
Case and control farm locations within Saskatchewan
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Cases Controls
occurred within that RM, the vaccination was listed as before the first RM case. In a similar fashion, investigators assessed if the timing of vaccination was associated with the occurrence of subsequent death losses on case farms. All vaccinated case farms were categorized as to whether or not any deaths occurred that might have been prevented by earlier vaccination. A case herd with vaccine preventable deaths was defined as one in which anthrax deaths occurred more than 17 d after the index case within the same RM. The 17-day period was chosen because this allowed time for the farm to administer the vaccine within 7 d of the index anthrax death in the same RM and the estimated time (approximately 10 d) required for maximum vaccine effectiveness (3). Logistic regression analysis, as described, was used to determine if vaccination of a herd within 1 wk of the index case within the same RM (risk factor) was associated with the occurrence of any vaccine-preventable deaths in that herd (outcome).
Results Description of control herds
Figure 1. Case and control farm locations used in the analysis showing the extent of the study area (lower half of province indicated by RM divisions).
From the 51 listed private veterinary clinics within the study area, the first 21 contacted were willing to participate in the study, but 3 were dropped due to an inability to follow-through in an acceptable time period. With help from these 19 clinics, a total of 271 potential control farms were identified and 259 eligible farms were investigated by telephone during the summer of 2007 (Figure 1).
Description of case herds status and each variable of interest was evaluated in a final multivariable model and reported as an odds ratio (OR) with 95% confidence intervals (CI). All environmental and management variables, except vaccination status, were screened before developing the final multivariable model. These variables were considered in the final analysis of the full data set if their unconditional association with farm status was potentially important (P , 0.20). Factors were identified as confounders and retained in the final model if removing or adding the factor changed the effect estimate for another variable by more than 10%. Manual backwards elimination of variables was used to achieve a final model containing only the statistically significant variables that were either significant or acted as important confounders. Biologically reasonable 2-way interactions were assessed between significant risk factors (P , 0.05) and included in the final model only if they were statistically significant. Because all case farms were required to vaccinate, the comparison of the odds of vaccination between case and control herds was not investigated using the full data set. A subset of the data was used instead to determine if herds that were vaccinated earlier were less likely to be case herds than those that were vaccinated later. Timing of vaccination was examined in a logistic regression model, as described, using only those farms in which vaccination had occurred. The variable, timing of vaccination, was derived by defining date of vaccination in relation to the index case in each rural municipality (RM) where the farm was situated. If the farm was a control farm and no index case 976
Based on a minimum distance of separation, 157 separate farm locations were available for analysis but only 143 had completed questionnaires. Of those with completed questionnaires, 117 had cattle on the premises and were included in this analysis (Figure 1). Of these 117 farms, 81 had only bovine animals on the premises, while 36 had bovine and other animal species present. There were 448 bovine cases in this subset of farms and 79 cases from other species including bison, swine, sheep, equine, and goats (4). The risk of mortality in the case herds varied from 0.6% to 100.0% [mean, 6.5%; standard deviation (s), 10.99%]. Anthrax cases in these herds were reported (in the final CFIA database) as having occurred between June 18th, 2006 and September 21st, 2006, and a detailed description of the cases has been published (4).
Comparison of case and control farms Only a few environmental and management variables were significantly associated (P , 0.05) with farm status in the initial unconditional analysis including: undiagnosed deaths on farm, density of animals on pasture, flooding, pasture condition, and grass length (Table 1). Other associations with farm status approached significance (P , 0.20) including: history of surface disruptions, standing water on pasture, and use of oilers for insect control (Table 1). Timing of vaccination was significantly associated (P , 0.05) with farm status in the subset model containing only vaccinated herds (Table 1). In the final multivariable model of the full data set examining only the environmental and management risk factors, the odds CVJ / VOL 51 / SEPTEMBER 2010
Table 2. Summary of the environmental and management factors that were significantly associated with case herd status for anthrax in the final multivariable analyses Final models
ORa
Variables
95% CIb
P-value
Up to 1 animal/acre 1 or more animals/acre 3.0 1.6, 5.7
0.001
Grass length
Adequate/long Very short/short 3.0 1.4, 6.4
0.006
Flooding
No Yes 3.4 1.8, 6.4
, 0.001
Pasture condition
Dry Good 3.5 1.4, 8.5 Wet/very wet 7.2 2.9, 18.1
, 0.001
Subset: Timing of vaccination herds that were vaccinated (n = 157 herds)
Vaccinated before or within 1 week of first RM case
Vaccinated . 1 week after first RM case
6.3
, 0.001
2.6, 15.3
a OR b CI
— Odds ratio. — Confidence interval.
that a herd had had an anthrax case were significantly higher in herds where flooding was reported, pasture condition was reported as good, wet or very wet, grass length was short or very short, and the density of animals on pasture was high (Table 2). Timing of vaccination was significantly associated with farm status in the final subset model limited to just those herds that had been vaccinated (n = 157) (Table 2). The odds that a herd had reported a case of anthrax were highest in those herds that did not vaccinate before or within a week of the first case in their RM. No other factors remained significant in this subset model. Timing of vaccination was also significantly associated with the occurrence of subsequent deaths on case farms (n = 115). The odds of a vaccine-preventable death were 11.2 times (95% CI: 4.3 to 28.9, P , 0.001) higher on case farms that vaccinated more than 1 wk after the index case within the same RM than on case farms where vaccination occurred before or within 1 wk of the index case within the same RM.
Discussion This outbreak was unusual for Saskatchewan because of the number of animals and premises affected as well as the duration of the outbreak and the extent of the locations involved (2,4). Exposure to anthrax spores in the soil and outbreaks of disease have been associated with flooding, drought, and human-induced land disturbances (2,6–10). This outbreak was originally postulated by the CFIA to be related to the extensive flooding in this region followed by drying temperatures (2,4); the analysis reported here supports this assumption. Case herds were more likely than control herds to be in areas that had experienced flooding, and areas where pastures were considered wet or very wet prior to the outbreak. It has been established that anthrax spores float on water and can be dispersed under wet conditions leading to concentration of the spores in low lying areas when the waters recede (11). One or more localized depositions of spores could have been dispersed throughout the larger outbreak area by flood conditions prior to the 2006 CVJ / VOL 51 / SEPTEMBER 2010
grazing season. This theory could be explored by examining the natural drainage patterns of the region. Other environmental and management factors associated with this outbreak included grass length and density of animals on pasture. Case farms were more likely to have had pastures where the grass was short and had stocking densities that were relatively high. These findings are consistent with previous reports suggesting that anthrax exposure in herbivores is often associated with overgrazing or when low-lying wet areas become available for grazing (1,8,11). Spores can survive for decades in the correct soil conditions and then, under the right conditions, infect grazing animals that come in contact with them (11). One common exposure pathway occurs when cattle enter newly exposed low-lying areas or depressions during droughtlike conditions (2,8,11). A survey of sites in an endemic region in northern Canada showed that up to 11% of previous carcass disposal sites contained viable anthrax spores (12). Anthrax cases had not been previously reported in the outbreak area; however, it is possible that undiagnosed cases in livestock or wildlife had occurred previously in these areas. It is also possible that known carcass sites further away could have been the source of the spores which were transported through waterways, natural drainage patterns, insects, or by scavengers to the locations of the case farm (6,11–13). In the past, the use of lime was advocated during the burial of anthrax carcasses; however, recent findings suggest that calcium is important to the viability of spores in the environment and the CFIA has discontinued the use of lime in burial sites (11,14). Proper disposal of carcasses, particularly burning, burial, and disinfection, is necessary to prevent further contamination of and from affected sites. Proper disposal together with the identification of high-risk areas based on the characteristics of previous anthrax outbreak sites (where proper or adequate disposal was not employed) can help decrease the potential for exposure to this pathogen (7,10,14). While the available data did not allow a direct examination of the benefits of vaccination as a control measure, investigators 977
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Full model with all study herds Density — category (N = 331 herds)
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examined timing of vaccination and related it to the occurrence of disease in these herds. Control herds were more likely to have vaccinated within 1 wk of the first confirmed case of anthrax within the same RM as case herds. Further analysis supported the benefits of promoting early vaccination in minimizing deaths on affected premises. Deaths more than 17 d after the index case were significantly less likely in case herds that had vaccinated within a wk of their first death than in those that had vaccinated later. Additional cost-benefit analysis should be considered to compare the economic losses associated with deaths (including indemnity payments and disposal fees) that might have been prevented by prompt herd diagnosis and vaccination with the increased cost of rapid identification and vaccination of affected and surrounding herds. An outbreak of similar magnitude was recorded in Australia in 1997; however, it occurred in a relatively small geographical area (9,15). After the number of affected properties escalated in the second and third weeks of the outbreak, all farms in the surrounding area were vaccinated. The area of the outbreak was small which made the mandatory vaccination of an area 30 km 3 20 km possible in a 3-week period. Following implementation of the general area vaccination, the number of confirmed new cases of anthrax dropped dramatically on infected properties around 10 d after vaccination. In a similar outbreak in North Dakota in 2005, vaccination was shown to be preventative specifically when implemented prior to the outbreak (6,7). Even with the large geographical area involved in the Saskatchewan outbreak, there could have been a financial and animal-related benefit from immediate implementation of vaccination programs within affected RMs or based on the identification of a case in a neighboring RM. While vaccination is a key component of the response to anthrax outbreaks in other countries, pre-season vaccination is recognized as the most reliable prevention method (6,7,16). Routine vaccination, however, is not widely used by producers probably because of the perceived cost-to-benefit ratio (16). Because of the retrospective nature of the data collection, there is potential in this study for recall bias, specifically with the control farms. However, most of the variables for which information was collected would have been verifiable by the herd owner’s personal records, memorable due to infrequent occurrence, or consistent from year to year. In addition, due to the wording of the data collection questionnaire, some of the variables could have been mis-categorized. For example, pasture condition was recorded as dry, good, wet, and very wet; however, no consistent definition of the meaning of these categories or the time frame on which to base the answer was provided to study participants. An alternative source of data would have been satellite imagery which depicts greenness, brightness, and wetness. This remote sensing approach would have provided a reliable estimate of pasture conditions for specific time frames. Unfortunately, due to the large geographic range of the outbreak, it was not feasible to obtain and analyze the relevant data for this study. Instead, categories were combined to decrease the chances of substantial mis-categorization between similar categories.
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There has been much speculation about the effects meteorological conditions, soil and vegetation characteristics, and management factors might have on the timing and location of anthrax outbreaks. This analysis estimates the contribution of several of these factors to the largest recorded anthrax occurrence recorded to date in western Canada by the CFIA. Additional data sources and analytical methods will be used in future studies to better understand the impact environmental factors had on the occurrence and magnitude of this extensive anthrax event. The data from this analysis also support the idea that even during an outbreak early vaccination is beneficial to prevent disease and reduce subsequent deaths in affected herds. Lessons learned from this experience associated with the timing of vaccination should be considered in planning for and responding to future outbreaks.
Acknowledgments Special thanks to the employees of the CFIA; district veterinarians, administrative staff and summer students in 2007 for their effort to have all of the questionnaires completed during the outbreak in 2006 and over the summer of 2007. CVJ
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