Localized reactive badger culling increases risk of

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Electronic supplementary material: Localized reactive badger
culling increases risk of bovine tuberculosis in nearby cattle
herds.
Flavie Vial and Christl A. Donnelly*
MRC Centre for Outbreak Analysis and Modelling, Department of Infectious Disease Epidemiology,
Imperial College London, Norfolk Place, London, UK.
*
c.donnelly@imperial.ac.uk
1. Reactive culling
The RBCT reactive treatment involved a series of localized badger culls carried out in
response to confirmed bTB herd breakdowns (Table 1). When bTB was confirmed in a cattle herd
within a reactive trial area, field staff mapped the land used by the affected herd (“reactor land”).
Survey data were then used to estimate the likely home ranges of badgers using this land, and to
identify their setts (sometimes on neighbouring properties). The average reactive culling operation
captured badgers within an area of 5.3km2 (Table 2). A detailed account of the RBCT reactive
treatment can be found in a 2005 report to the Independent Scientific Group on Cattle TB [1].
Reactive culling was suspended in November 2003, after data on the incidence of herd
breakdowns up to August 2003 [2] revealed that reactive badger culling was associated with an
estimated increase of 27% in the incidence of confirmed cattle herd breakdowns (95% CI: 2.4%
decrease to 65% increase after adjustment for overdispersion).
Table 1 : Approximate dates of reactive culling, by triplet and culling year (defined to run from 1 May
– 31 January).
Triplet 1999
2000
2002
2003
A
Jul-Nov 2000
Jan 2003
May 2003
B
May-Dec 1999 Aug-Sept 2000 Sept 2002- Jan 2003 May-July 2003
C
May-Aug 2000 Jul 2002- Jan 2003
D
May 2003
Aug-Sept 2003
E
Jun 2002-Jan 2003
Jul-Oct 2003
F
Jul 2002- Jan 2003
Jun-Sept 2003
G
Aug 2002- Jan 2003
Sept-Oct 2003
H
Jan 2003
Sept-Oct 2003
I
May-Sep 2003
Triplet J was eligible for reactive culling in 2003 but no culls had been performed when reactive culling was
suspended in November 2003.
No culling took place in 2001 during the foot-and-mouth disease outbreak.
Table 2: Total numbers of badgers culled in reactive areas, by triplet and culling year.
Triplet 1999 2000 2002 2003
Total
A
B
73
C
34
47
36
117
34
84
110
301
179
115
101
395
122
122
D
E
62
126
188
F
145
291
436
G
172
84
256
H
17
143
160
94
94
I
J
Total
0
73
247
642
1,107 2,069
Triplet J was eligible for reactive culling in 2003 but no culls had been performed when reactive culling was
suspended in November 2003.
No culling took place in 2001 during the foot-and-mouth disease outbreak.
Reactive trial areas
Although the boundaries of the RBCT trial areas were at least 3 km apart, the reactive trial
area and the proactive trial area in some triplets were geographically close. Some of the herds within
the reactive areas were within <5 km of other herds in proactive areas and vice versa. The treatment
boundaries of proactive areas extended slightly beyond the trial area boundaries as culling
performed on the land parcels belonging to the herd near/on the trial boundaries would have
affected badger groups with territories which extended beyond the boundaries of the trial areas.
Since proactive badger culling started before reactive badger culling, some of our case herds
within reactive areas have had badgers culled within 3km of their lands (those badgers were
proactively culled inside the proactive trial areas) during the time period between the start of the
first proactive cull and the first reactive cull. Although those badgers were proactively culled prior to
the onset of reactive culled, they are still in the proximity of farms within the reactive areas and may
therefore conceivably have influenced bTB risks for those reactive herds. This is the reason why the
number of badgers proactively culled prior to the onset of reactive culling within 3 and 5kms of the
reactive herds was considered in our analyses.
Selection of case and control herds.
The Defra animal health information system (VETNET) provided data on cattle bTB tests and
herd breakdowns. Each case was matched to a control selected randomly from herds within the
same triplet that had a clear herd test within a year of the breakdown disclosure date and that had
no associated land within 5km of the reactor land. As a result of this study design, and because trial
areas were roughly 10km across, the control herds thus selected tended to be located closer to the
trial area boundaries than case herds. Median distance to the trial area boundary was 1094m (min =
0, max = 4470) for case herds, with control herds being somewhat closer to the edge of the trial area
(median = 871, min = 0, max = 4541) (Figure 1).
Figure 1: Stacked histogram of the distribution of herd distance to the trial area boundary (n = 1207) for case
and control herds.
2. Local bTB risk factors
A number of local herd-level risk factors have been identified inside all three treatment groups
of the RBCT by previous analyses [3]. Some of these risk factors had also been described for herds
outside the RBCT area.
Herd size
Herd size has repeatedly been identified as one of the major bTB herd-level risk factor [4-6].
Large herds tend to pasture on larger areas, with higher probabilities of contiguous herds thereby
facilitating cattle to cattle spread of M. bovis [7]. A comparative case-control study in England
between 1995 and 1999 revealed that herd size was a significant predictor of both transient and
persistent bTB breakdowns and associated herd size with management-related risk factors such as
turnover rates, stocking density, farm enterprise and feeding [8].
In our reactive herds case-control study, median herd size was estimated at 73 head of cattle
(min = 0, max = 1073), with case herds being usually larger than control herds (Figure 2 & Table 5).
Figure 2: Stacked histogram of the distribution of herd size (n = 1207) for case and control herds.
400
Count
300
type
case
200
control
100
0
0
200
400
600
Herd size
800
1000
Historic incidence
Historic incidence of bTB (Tables 3 & 4) was found to be a robust predictor of the rate of
future outbreaks in both Irish [9] and British [6] herds. Herd breakdowns tend to be recurrent [10]
possibly as a result of the failure to clear the source of the disease, especially from larger herds, by
test and slaughter [11]. Subsequent breakdowns could therefore arise from undetected (tuberculinnegative) infected animals. This factor is probably exacerbated for dairy herds for which turnover is
less important than for stores or beef enterprises. Other permanent factors (such as the presence of
badgers and/or contiguous herds) may make these areas particularly prone to bTB reemergence.
Table 3: Number of confirmed bTB breakdowns in the previous year for case and control herds.
Number of confirmed
Case Control
bTB breakdown in previous herds herds
1 year
0
557
559
1
47
45
Table 4: Number of confirmed bTB breakdowns in the previous two years for case and control herds.
Number of confirmed
Case Control
bTB breakdown in previous herds herds
2 years
0
433
491
1
153
106
2
18
7
Farm area
Farm area has been found to be associated with an increased bTB risk beyond any effect of
herd size as show in England [12]. Larger farms, regardless of the number of land parcels, may
include more active badger setts or more contiguous herds, both risk factors identified in other
studies [7, 12-14]. Median farm area (combined area of all the land parcels belonging to a farm) was
estimated at 0.61 km2 (min = 0.01, max = 5.18), with case herds associated with larger farms (Figure
3 & Table 5).
Figure 3: Stacked histogram of the distribution of farm area (n = 1187) for case and control herds.
500
400
300
Count
type
case
control
200
100
0
0
1
2
3
Farm area (km^2)
4
5
6
Dairy herds have been found to be more at risk of a confirmed bTB outbreak (Table 5).
Animals in dairy herds tend to have a longer life expectancy, and thus a longer exposure to bTB and
increased risk of breakdown [15], than beef cattle that are slaughtered at a young age. Unlike beef
farms that use a variety of breeds and crossbred animals, dairy farms in the UK predominantly use
one breed of cattle (Ivan Morrison pers. comm.). A breed-related difference in susceptibility may
ensue [16] although it is difficult to disentangle its potential effects from higher production stress
under more intensive management conditions for dairy cattle for example [17]. Interestingly, dairy
herds within the RBCT tended to be much larger than other enterprise types [13] .
Table 5: The average herd size, % of dairy herds, farm area and number of confirmed bTB breakdowns
in the previous year and the previous two years.
Leading
Case
During
Control Case
Post1
Control Case
Post2
Control Case
Control
Herd size
135.27 82.05
161.61 87.30
138.16 79.24
135.34 76.28
% dairy herds
43%
17%
34%
18%
33%
17%
33%
19%
Farm area (km2)
0.79
0.53
0.93
0.53
1.04
0.59
0.99
0.56
Number of confirmed
0.035
0.078
0.08
0.063
0.12
0.09
0.10
0.08
0.23
0.21
0.26
0.17
0.42
0.23
0.40
0.23
bTB breakdowns
(previous year)
Number of confirmed
bTB breakdowns
(previous two years)
3. Summary of variables
Data were analysed for four time periods, with both the breakdown disclosure date of the
case and the clear herd test of the control required to be within the time period under analysis:
a) from the completion of the initial proactive cull (Table 6) until the first reactive culling operation
(Table 1) in each triplet (“leading”);
b) from the first reactive culling operation in each triplet until the suspension of reactive culling in
November 2003 (“during”);
c) from the suspension of reactive culling in November 2003 to 1 year after the end of the last
proactive cull (Table 6) (“post1”); and
d) from the suspension of reactive culling in November 2003 until the compilation of the database
on 21 January 2007 (“post2”).
Table 6: Dates of initial and follow-up culls in proactive areas, by triplet.
Triplet
Initial cull
2nd cull
3rd cull
4th cull
5th cull
A
Jan 2000
May 2002
Nov 2003
May 2004
Oct 2005
B
Dec 1998
Oct 1999
D
Dec 2002
May 2003
Au 2000– Nov–Dec
Jan 2001
2002
Aug–Nov Oct 2003
2002
Sep 2004
Jun 2003
C
Nov–Dec
1999
Jan 2001
E
May 2000
Jan 2001
Jun 2003
Jul 2004
F
Jul 2000
May 2002
May2002–
2005
Jun
Jan 2003
Dec 2003
Sep 2004
Jun 2005
G
Oct–Nov
2000
Dec 2000
Jul 2002
Jul 2003
Jun 2004
Jun 2005
Jun–Jul
2002
Sep–Oct
2003
Jul–Aug
2003
Sep 2003
May 2004
Jul–Aug
2005
Oct–Nov
2004
Oct–Nov
2004
Jul 2005
H
I
J
Sept–Oct
2002
Oct 2002
Jun 2004
6th cull
7th cull
Jul–Aug
2004
Sep
2005
Oct 2005
Sep
2005
May 2005
Data on whether any reactive culling had taken place and the number of badgers culled
nearby (defined as within 1, 3, or 5km) cases and controls were extracted from the RBCT
geodatabase (ArcGIS version 9, ESRI). Because reactive badger culling operations were prompted by
nearby confirmed bTB breakdowns, the number of nearby confirmed breakdowns within 1, 3 or 5km
of each case and control was also extracted. The number of nearby tested cattle herds not under
bTB-related movement restrictions (again within 1, 3 or 5km) were recorded as a measure of the
herd population at risk. Each of these variables was calculated for one year prior to the date the
breakdown was detected in the case herd and the herd test date of the control [see main text], and
separately for the previous two years (Table 7). Variables were log transformed before being
screened using conditional logistic regression and after adjusting for the local bTB risk factors listed
above.
Table 7: Average number of culled badgers, confirmed bTB breakdowns and tested herds not under bTB
restriction for cases and controls by time period (all variables measured in the previous two years).
Distance Leading
During
Case
Control Case
Post1
Control Case
Post2
Control Case
Control
3.40
Nearby RBCT
1
0
0.04
11.56 5.89
4.39
2.57
5.61
culled badgers 1
3
0.28
0.49
41.67 21.67
17
9.68
22.01 12.78
5
1.44
1.56
71.82 43.74
31.64 17.66
40.98 23.13
Nearby confirmed
1
5.96
4.03
6.73
7.90
8.15
bTB breakdowns
3
17.48 14.08
19.19 16.2
23.06 18.27
23.93 18.48
5
33.22 28.66
35.57 32.33
42.62 36.62
44.03 37.16
Nearby tested
1
13.04 10.23
11.79 9.51
10.64 8.14
10.40 8.10
herds not under
3
47.34 39.03
39.67 35.49
36.49 30.79
36.52 30.78
bTB restrictions 2
5
96.02 81.23
80.37 75.32
74.16 65.06
74.07 64.48
1
4.94
5.55
5.72
During the “Leading” period from the completion of the initial proactive cull until the first reactive culling
operation small numbers of badgers were proactively culled within 3 or 5km of a case or control within a
reactive area. Proactively culled badgers may contribute similarly to numbers in the later time periods.
2
Some of the herds which have been tested twice in the 24 months period under study were also counted twice.
Estimating odds ratio (OR) corresponding to covariate.
Throughout the text, we present the risk (OR and their 95% confidence interval) of a herd
experiencing a confirmed bTB breakdown following a doubling in the value of one of the covariates
tested. Imagine the estimate of the log odds ratio = 0.2 and the standard error (SE) of this estimate =
0.07. In this case the OR associated with a doubling of the covariate is given by:
OR = exp(0.2 * ln(2)) = 1.149
And the 95% confidence interval is obtained by:
Lower confidence limit = exp (0.2 * ln(2) - 1.96*SE*ln(2) )
= exp (0.2 * ln(2) - 1.96 * 0.07 * ln(2))
= 1.044
Upper confidence limit = exp (0.2 * ln(2) + 1.96*SE*ln(2) )
= exp (0.2 * ln(2) + 1.96 * 0.07 * ln(2))
= 1.263
4. Further results from analyses based on variables
measured in the year previous to the bTB breakdown (main
text).
Univariable associations with the numbers of nearby culled badgers and confirmed bTB breakdowns
in the previous year.
While reactive culling was taking place, the univariable models showed strong associations
between cases and increased numbers of badgers culled in the previous year (Table 8). The number
of (proactively) culled badgers within 3 and 5km of a herd significantly decreased its bTB risk prior to
the onset of reactive culling. Cases were consistently associated with increased numbers of nearby
confirmed bTB breakdowns in all four time periods and all three distances (Table 9); with a doubling
in the number of nearby confirmed bTB breakdowns always resulting in estimated increases in bTB
risk from 34% to 231%.
5. Analyses based on variables measured in the two years
previous to the bTB breakdown.
Nearby reactive culling and TB risk.
The presence of any reactive culling activity within 1km of a herd, in the previous two years,
significantly increased its bTB risk (OR: 1.81, 95% CI: 1.31-2,48, p < 0.001), even after adjusting for
the number of nearby confirmed bTB breakdowns. The detrimental effect of reactive culling
remained as the distance to the herd increased (3km: OR: 2.45, 95% CI: 1.59-3.78, p < 0.001; 5km:
OR: 3.29, 95% CI: 1.69-6.39, p < 0.001).
Associations with the numbers of nearby culled badgers and confirmed bTB breakdowns in the
previous two years.
The univariable models showed a strong association between case herds and a greater
number of badgers culled in the previous two years both during and after, but not before, reactive
culling (Table 10). Case herds were also associated with increased numbers of nearby confirmed bTB
breakdowns in all four time periods (Table 11).
Interestingly, when both variables were included in a multivariable model, the number of
nearby badgers culled significantly decreased a herd’s bTB risk prior to the onset of reactive culling,
while the number of nearby confirmed bTB breakdowns remained a significant risk factor for herds
(Table 12). During reactive culling, the number of nearby badgers culled remained a significant bTB
risk factor for herds within 3 and 5km (Table 12), although the number of nearby confirmed bTB
breakdowns retained a non-significant trend towards an increased bTB risk. After the end of reactive
culling, the number of nearby confirmed bTB breakdowns remained the only significant bTB risk
factor (Table 12), although the number of nearby badger culled retained a non-significant trend
towards an increased bTB risk.
Table 8: Odds ratios (OR) with 95% confidence intervals for the univariable models of the association of cases with increased numbers of culled badgers in the previous
year.
Leading
During
Post1
Post2
Distance (km)
1
3
5
1
3
5
1
3
5
1
3
5
Nearby RBCT
----
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
----
p = 0.10
p = 0.38
----
p = 0.11
p = 0.43
OR: 0.45
OR: 0.74
OR: 1.31
OR: 1.33
OR: 1.38
OR: 0.74
OR: 0.92
OR: 0.77
OR: 0.93
(0.29-0.70)
(0.54-1.02)
(1.18-1.47)
(1.20-1.47)
(1.23-1.55)
(0.51-1.06)
(0.77-1.10)
(0.56-1.06)
(0.79-1.11)
culled badgers
Herd type
p < 0.001
p < 0.001
p < 0.001
p = 0.02
p = 0.02
p = 0.02
p = 0.005
p = 0.003
p = 0.002
p = 0.01
p = 0.005
p = 0.004
[Dairy]
OR: 7.05
OR: 8.72
OR: 8.19
OR: 2.07
OR: 2.03
OR: 2.06
OR: 2.19
OR: 2.25
OR: 2.27
OR: 2.18
OR: 2.24
OR: 2.27
(2.86-20.89)
(3.33-28.11)
(3.12-26.00)
(1.16-3.81)
(1.12-3.80)
(1.13-3.87)
(1.29-3.84)
(1.33-3.92)
(1.35-3.93)
(1.15-3.93
(1.30-4.01)
(1.32-4.03)
p = 0.08
p = 0.11
p = 0.09
p = 0.57
p = 0.64
p = 0.86
p = 0.69
p = 0.63
p = 0.66
p = 0.69
p = 0.62
p = 0.66
OR: 0.88
OR: 0.89
OR: 0.88
OR:0.96
OR: 0.97
OR: 0.99
OR: 0.98
OR: 0.98
OR: 0.98
OR: 0.98
OR: 0.98
OR: 0.98
(0.76-1.02)
(0.76-1.03)
(0.76-1.02)
(0.85-1.09)
(0.86-1.10)
(0.88-1.12)
(0.90-1.07)
(0.90-1.07)
(0.90-1.07)
(0.89-1.08)
(0.89-1.07)
(0.89-1.07)
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
OR: 15.77
OR: 13.85
OR: 14.75
OR: 21.06
OR: 18.64
OR: 20.56
OR: 11.55
OR: 11.23
OR: 11.96
OR: 10.53
OR: 10.34
OR: 11.03
(3.57-69.71)
(3.00-64.06)
(3.19-68.25)
(6.98-63.55)
(6.18-56.26)
(6.76-62.54)
(4.97-26.88)
(4.83-26.12)
(5.14-27.84)
(4.30-25.77)
(4.24-25.23)
(4.50-27.03)
bTB historic
p = 0.02
p = 0.047
p = 0.055
p = 0.81
p = 0.71
p = 0.40
p = 0.79
p = 0.78
p = 0.78
p = 0.79
p = 0.77
p = 0.76
incidence
OR: 0.37
OR: 0.41
OR: 0.42
OR: 0.93
OR: 0.88
OR: 0.75
OR: 1.07
OR: 1.07
OR: 1.08
OR: 1.08
OR: 1.08
OR: 1.09
(0.16-0.87)
(0.17-0.99)
(0.17-1.02)
(0.51-1.70)
(0.46-1.69)
(0.39-1.45)
(0.64-1.78)
(0.65-1.78)
(0.65-1.79)
(0.63-1.83)
(0.64-1.84)
(0.64-1.85)
Herd size
Farm area
Models are adjusted for herd type, herd size, farm area and historic incidence (in grey). Significant associations are denoted in bold.
--- denotes that odds ratios were not estimable.
Table 9: Odds ratios (OR) with 95% confidence intervals for the univariable models of the association of cases with increased numbers of confirmed bTB
breakdowns in the previous year.
Leading
During
Post1
Post2
Distance (km)
1
3
5
1
3
5
1
3
5
1
3
5
Nearby confirmed
p = 0.02
p < 0.001
p = 0.005
p < 0.001
p = 0.003
p = 0.02
p = 0.005
p = 0.002
p = 0.04
p = 0.003
p = 0.001
p = 0.03
bTB breakdowns
OR: 1.34
OR: 2.08
OR: 2.31
OR: 1.50
OR: 1.72
OR: 1.73
OR: 1.44
OR: 1.80
OR: 1.63
OR: 1.53
OR: 2.01
OR: 1.75
(1.04-1.72)
(1.39-3.12)
(1.29-4.13)
(1.20-1.88)
(1.20-2.47)
(1.08-2.77)
(1.12-1.85)
(1.24-2.62)
(1.03-2.58)
(1.15-2.02)
(1.32-3.05)
(1.06-2.88)
Herd type
p < 0.001
p < 0.001
p < 0.001
p = 0.14
p = 0.11
p = 0.09
p = 0.01
p = 0.05
p = 0.01
p = 0.01
p = 0.08
p = 0.02
[Dairy]
OR: 6.12
OR: 6.79
OR: 5.80
OR: 1.54
OR: 1.58
OR: 1.64
OR: 2.04
OR: 1.75
OR: 2.03
OR: 2.05
OR: 1.72
OR: 1.98
(2.58-16.98)
(2.81-19.18)
(2.46-15.87)
(0.87-2.76)
(0.91-2.82)
(0.93-2.93)
(1.20-3.58)
(1.00-3.14)
(1.19-3.57)
(1.17-3.72)
(0.94-3.20)
(1.12-3.60)
p = 0.13
p = 0.10
p = 0.17
p = 0.87
p = 0.99
p = 0.95
p = 0.60
p = 0.78
p = 0.86
p = 0.73
p = 0.08
p = 0.94
OR: 0.90
OR: 0.89
OR: 0.91
OR: 1.01
OR: 1.00
OR: 1.00
OR: 0.98
OR: 10.99
OR: 0.99
OR: 0.98
OR: 1.45
OR: 1.00
(0.78-1.03)
(0.77-1.02)
(0.79-1.04)
(0.90-1.13)
(0.89-1.12)
(0.90-1.12)
(0.89-1.07)
(0.90-1.08)
(0.91-1.08)
(0.89-1.108)
(0.95-2.22)
(0.90-1.10)
p = 0.003
p = 0.002
p = 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
OR: 7.16
OR: 8.07
OR: 8.10
OR: 21.73
OR: 21.03
OR: 20.21
OR: 9.21
OR: 11.77
OR: 12.16
OR: 8.84
OR: 10.92
OR: 11.25
(1.96-26.13)
(2.19-29.74)
(2.29-28.66)
(7.33-64.37)
(7.23-61.20)
(7.11-57.45)
(3.80-22.34)
(4.72-29.37)
(5.03-29.42)
(3.41-22.90)
(4.08-29.24)
(4.38-28.95)
bTB historic
p = 0.02
p = 0.01
p = 0.02
p = 0.55
p = 0.48
p = 0.64
p = 0.85
p = 0.62
p = 0.78
p = 0.72
p = 0.42
p = 0.65
incidence
OR: 0.36
OR: 0.32
OR: 0.38
OR: 0.83
OR: 0.81
OR: 0.87
OR: 1.05
OR: 1.15
OR: 1.08
OR: 1.10
OR: 1.27
OR: 1.14
(0.16-0.82)
(0.14-0.75)
(0.17-0.88)
(0.45-1.53)
(0.45-1.47)
(0.48-1.57)
(0.63-1.76)
(0.66-1.99)
(0.64-1.83)
(0.65-1.89)
(0.72-2.27)
(0.565-1.98)
Number of herd tested
p = 0.50
p = 0.59
p = 0.17
p = 0.18
p = 0.13
p = 0.09
p = 0.15
p = 0.10
p = 0.11
p = 0.23
p = 0.108
p = 0.12
not under bTB restriction
OR: 1.11
OR: 0.88
OR: 0.68
OR: 0.85
OR: 0.78
OR: 0.74
OR: 1.23
OR: 1.48
OR: 1.51
OR: 1.21
OR: 1.56
OR: 1.55
(0.82-1.50)
(0.56-1.39)
(0.39-1.17)
(0.67-1.08)
(0.57-1.07)
(0.52-1.05)
(0.92-1.65)
(0.93-2.33)
(0.91-2.51)
(0.89-1.66)
(0.95-2.57)
(0.89-2.71)
Herd size
Farm area
Models are adjusted for herd type, herd size, farm area, historic incidence and the number of nearby herds (in grey). Significant associations are denoted in bold.
Table 10: Odds ratios (OR) with 95% confidence intervals for the univariable models of the association of cases with increased numbers of culled badgers in the
previous two years.
Leading
During
Post1
Post2
Distance (km)
1
3
5
1
3
5
1
3
5
1
3
5
Nearby RBCT
----
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p = 0.07
p = 0.01
p = 0.007
p = 0.07
p = 0.01
p = 0.005
OR: 0.46
OR: 0.65
OR: 1.21
OR: 1.32
OR: 1.51
OR: 1.12
OR: 1.15
OR: 1.14
OR: 1.12
OR: 1.15
OR: 1.16
(0.30-10.71)
(0.54-0.80)
(1.10-1.33)
(1.19-1.46)
(1.30-1.75)
(0.99-1.27)
(1.03-1.28)
(1.04-1.26)
(0.99-1.27)
(1.03-1.27)
(1.04-1.28)
culled badgers
Herd type
p < 0.001
p < 0.001
p < 0.001
p = 0.03
p = 0.02
p = 0.02
p = 0.005
p = 0.006
p = 0.004
p = 0.005
p = 0.007
p = 0.005
[Dairy]
OR: 6.70
OR: 8.27
OR: 6.84
OR: 1.91
OR: 2.13
OR: 2.05
OR: 2.17
OR: 2.14
OR: 2.21
OR: 2.22
OR: 2.19
OR: 2.26
(2.78-19.19)
(3.21-26.02)
(2.78-19.67)
(1.08-3.45)
(1.17-3.98)
(1.12-3.88)
(1.28-3.77)
(1.26-3.74)
(1.30-3.88)
(1.28-3.97)
(1.26-3.94)
(1.29-4.08)
p = 0.17
p = 0.19
p = 0.15
p = 0.74
p = 0.65
p = 0.98
p = 0.58
p = 0.49
p = 0.50
p = 0.59
p = 0.48
p = 0.46
OR: 0.91
OR: 0.91
OR: 0.91
OR:0.98
OR: 0.97
OR: 1.00
OR: 0.98
OR: 0.97
OR: 0.97
OR: 0.97
OR: 0.97
OR: 0.96
(0.80-1.04)
(0.79-1.05)
(0.79-1.04)
(0.87-1.10)
(0.86-1.10)
(0.88-1.13)
(0.90-1.06)
(0.89-1.06)
(0.89-1.06)
(0.89-1.07)
(0.88-1.72)
(0.88-1.06)
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
OR: 13.85
OR: 12.68
OR: 12.23
OR: 16.92
OR: 18.98
OR: 23.88
OR: 10.84
OR: 11.01
OR: 11.04
OR: 10.31
OR: 10.50
OR: 10.52
(3.37-56.92)
(2.95-54.47)
(3.00-49.82)
(5.88-48.69)
(6.34-56.80)
(7.52-75.82)
(4.59-25.57)
(1.28-2.20)
(4.63-26.33)
(4.15-25.63)
(4.17-26.45)
(4.18-26.47)
bTB historic
p = 0.25
p = 0.64
p = 0.61
p = 0.50
p = 0.48
p = 0.83
p = 0.13
p = 0.08
p = 0.06
p = 0.36
p = 0.25
p = 0.22
incidence
OR: 0.78
OR: 0.90
OR: 0.790
OR: 1.13
OR: 1.14
OR: 1.04
OR: 1.28
OR: 1.33
OR: 1.36
OR: 1.17
OR: 1.22
OR: 1.24
(0.51-1.19)
(0.58-1.39)
(0.58-1.38)
(0.79-1.60)
(0.79-1.66)
(0.71-1.53)
(0.93-1.77)
(0.97-1.84)
(0.98-1.87)
(0.83-1.64)
(0.87-1.72)
(0.88-1.75)
Herd size
Farm area
Refer to footnotes from Table 8
Table 11: Odds ratios (OR) with 95% confidence intervals for the univariable models of the association of cases with increased numbers of confirmed bTB
breakdowns in the previous two years.
Leading
During
Post1
Post2
Distance (km)
1
3
5
1
3
5
1
3
5
1
3
5
Nearby confirmed
p = 0.004
p = 0.007
p = 0.11
p < 0.001
p < 0.001
p = 0.006
p < 0.001
p = 0.001
p = 0.01
p = 0.001
p = 0.001
p = 0.008
bTB breakdowns
OR: 1.48
OR: 1.72
OR: 1.60
OR: 1.82
OR: 2.16
OR: 2.05
OR: 1.72
OR: 1.96
OR: 2.02
OR: 1.73
OR: 2.09
OR: 2.25
(1.13-1.93)
(1.16-2.954)
(0.91-2.82)
(1.35-2.44)
(1.39-3.35)
(1.23-3.42)
(1.26-2.36)
(1.30-2.97)
(1.15-3.55)
(1.25-2.40)
(1.34-3.26
(1.23-4.10)
Herd type
p < 0.001
p < 0.001
p < 0.001
p = 0.10
p = 0.15
p = 0.12
p = 0.03
p = 0.06
p = 0.02
p = 0.03
p = 0.06
p = 0.03
[Dairy]
OR: 6.18
OR: 6.12
OR: 5.48
OR: 1.62
OR: 1.53
OR: 1.59
OR: 1.86
OR: 1.72
OR: 1.89
OR: 1.90
OR: 1.74
OR: 1.89
Herd size
(2.62-16.83)
p = 0.19
(2.61-16.64)
p = 0.20
(2.38-14.52)
p = 0.28
(0.91-2.94)
p = 0.99
(0.86-2.75)
p = 0.99
(0.90-3.86)
p = 0.88
(1.07-3.31)
p = 0.44
(0.99-3.05)
p = 0.63
(1.10-3.33)
p = 0.70
(1.06-3.50)
p = 0.57
(0.97-3.19)
p = 0.70
(1.07-3.43)
p = 0.79
OR: 0.91
OR: 0.92
OR: 0.93
OR: 1.00
OR: 1.00
OR: 1.01
OR: 0.96
OR: 0.98
OR: 0.98
OR: 0.97
OR: 0.98
OR: 0.99
(0.80-1.05)
(0.80-1.05)
(0.82-1.06)
(0.89-1.13)
(0.89-1.12)
(0.90-1.13)
(0.88-1.06)
(0.89-1.07)
(0.90-1.08)
(0.88-1.07)
(0.89-1.08)
(0.89-1.09)
p = 0.005
p = 0.002
p = 0.002
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p = 0.001
p < 0.001
p < 0.001
OR: 6.10
OR: 6.77
OR: 7.05
OR: 17.44
OR: 1.82
OR: 16.56
OR: 5.72
OR: 8.85
OR: 9.76
OR: 5.28
OR: 7.61
OR: 8.92
(1.71-21.80)
(1.96-23.34)
(2.09-23.75)
(5.76-52.82)
(1.35-2.44)
(5.89-46.56)
(2.26-14.50)
(3.56-21.99)
(4.01-23.76)
(1.96-14.26)
(2.87-20.16)
(3.45-23.05)
bTB historic
p = 0.07
p = 0.08
p = 0.14
p = 0.39
p = 0.47
p = 0.35
p = 0.09
p = 0.06
p = 0.09
p = 0.28
p = 0.19
p = 0.25
incidence
OR: 0.66
OR: 0.67
OR: 0.73
OR: 1.17
OR: 1.14
OR: 1.18
OR: 1.34
OR: 1.38
OR: 1.33
OR: 1.22
OR: 1.27
OR: 1.22
Farm area
(0.42-1.03)
(0.43-1.05)
(0.48-1.11)
(0.82-1.67)
(0.80-1.62)
(0.83-1.67)
(0.96-1.86)
(0.98-1.92)
(0.96-1.84)
(0.85-1.73)
(0.89-1.82)
(0.87-1.73)
Number of herd tested
p = 0.08
p = 0.19
p = 0.28
p = 0.34
p = 0.28
p = 0.12
p = 0.17
p = 0.43
p = 0.29
p = 0.14
p = 0.27
p = 0.32
not under bTB restriction
OR: 1.38
OR: 1.47
OR: 1.50
OR: 0.85
OR: 0.78
OR: 0.66
OR: 1.28
OR: 1.24
OR: 1.37
OR: 1.32
OR: 1.38
OR: 1.39
(0.96-1.97)
(0.83-2.61)
(0.72-3.13)
(0.62-1.18)
(0.51-1.22)
(0.39-1.11)
(0.90-1.82)
(0.73-2.11)
(0.76-2.44)
(0.91-1.92)
(0.78-2.45)
(0.73-2.62)
Refer to footnotes from Table 9
Table 12: Odds ratios (OR) with 95% confidence intervals for the multivariable models of the associations of cases with increased numbers of RBCT culled badgers
and increased numbers of confirmed bTB breakdowns in the previous two years.
Leading
During
Post1
Post2
Distance (km)
1
3
5
1
3
5
1
3
5
1
3
5
Nearby RBCT
----
p < 0.001
p < 0.001
p = 0.04
p < 0.001
p < 0.001
p = 0.54
p = 0.27
p = 0.07
p = 0.54
p = 0.35
p = 0.06
OR: 0.44
OR: 0.56
OR: 1.12
OR: 1.31
OR: 1.54
OR: 1.04
OR: 1.07
OR: 1.71
OR: 1.04
OR: 1.06
OR: 1.11
(0.29-0.66)
(0.44-0.71)
(1.00-1.25)
(1.16-1.48)
(1.31-1.81)
(0.91-1.20)
(0.95-1.21)
(0.99-1.23)
(0.91-1.20)
(0.94-1.20)
(0.99-1.25)
culled badgers
Nearby confirmed
p < 0.001
p = 0.002
p = 0.01
p = 0.01
p = 0.52
p = 0.92
p = 0.003
p = 0.01
p = 0.07
p = 0.004
p = 0.01
p = 0.048
bTB breakdowns
OR: 1.86
OR: 2.03
OR: 2.64
OR: 1.53
OR: 1.19
OR: 0.97
OR: 1.66
OR: 1.79
OR: 1.71
OR: 1.66
OR: 1.91
OR: 1.88
(1.36-2.55)
(1.29-3.22)
(1.26-5.55)
(1.10-2.13)
(0.71-1.98)
(0.52-1.79)
(1.19-2.32)
(1.15-2.79)
(0.95-3.09)
(1.17-2.35)
(1.18-3.09)
(1.00-5.52)
Herd type
p < 0.001
p < 0.001
p < 0.001
p = 0.06
p = 0.02
p = 0.01
p = 0.03
p = 0.05
p = 0.02
p = 0.03
p = 0.06
p = 0.03
[Dairy]
OR: 8.21
OR: 9.50
OR: 6.91
OR: 1.77
OR: 2.19
OR: 2.36
OR: 1.87
OR: 1.75
OR: 2.36
OR: 1.91
OR: 1.76
OR: 1.94
Herd size
(3.05-26.78)
p = 0.05
(3.38-33.44)
p = 0.07
(2.63-21.40)
p = 0.09
(0.98-3.25)
p = 0.89
(1.17-4.23)
p = 0.69
(1.23-4.73)
p = 0.99
(1.07-3.33)
p = 0.43
(1.00-3.11)
p = 0.56
(1.23-4.73)
p = 0.59
(1.07-3.51)
p = 0.55
(0.98-3.25)
p = 0.63
(1.09-3.57)
p = 0.61
OR: 0.85
OR: 0.86
OR: 0.87
OR: 0.99
OR: 0.97
OR: 1.00
OR: 0.96
OR: 0.97
OR: 0.97
OR: 0.97
OR: 0.97
OR: 0.97
(0.72-1.00)
(0.73-1.01)
(0.75-1.02)
(0.88-1.12)
(0.86-1.10)
(0.88-1.13)
(0.88-1.06)
(0.89-1.07)
(0.89-1.07)
(0.88-1.07)
(0.88-1.08)
(0.88-1.08)
p < 0.001
p = 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p <0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
OR: 14.87
OR: 1.76
OR: 12.32
OR: 17.23
OR: 20.12
OR: 27.66
OR: 5.81
OR: 8.96
OR: 9.85
OR: 5.38
OR: 7.70
OR: 8.91
(3.10-71.42)
(0.89-3.48)
(2.83-53.58)
(5.64-52.66)
(6.65-68.85)
(8.33-91.86)
(2.29-14.77)
(3.58-22.40)
(4.00-24.21)
(1.98-14.57)
(2.88-20.59)
(3.40-23.37)
bTB historic
p = 0.03
p = 0.18
p = 0.22
p = 0.51
p = 0.525
p = 0.89
p = 0.10
p = 0.07
p = 0.07
p = 0.31
p = 0.18
p = 0.22
incidence
OR: 0.58
OR: 0.71
OR: 0.74
OR: 1.13
OR: 1.13
OR: 1.03
OR: 1.32
OR: 1.37
OR: 1.35
OR: 1.20
OR: 1.27
OR: 1.25
(0.35-0.95)
(0.44-1.17)
(0.46-1.20)
(0.79-1.62)
(0.78-1.64)
(0.70-1.51)
(0.95-1.84)
(0.98-1.91)
(0.97-1.87)
(0.84-1.71)
(0.89-1.82)
(0.88-1.77)
Number of herd tested
p = 0.13
p = 0.10
p = 0.11
p = 0.39
p = 0.20
p = 0.17
p = 0.15
p = 0.38
p = 0.25
p = 0.12
p = 0.23
p = 0.25
not under bTB restriction
OR: 1.36
OR: 1.76
OR: 2.17
OR: 0.87
OR: 0.74
OR: 0.67
OR: 1.30
OR: 1.27
OR: 1.41
OR: 1.34
OR: 1.42
OR: 1.46
(0.92-2.01)
(0.89-3.48)
(0.85-5.56)
(0.62-1.21)
(0.47-1.18)
(0.38-1.18)
(0.91-1.85)
(0.74-2.17)
(0.78-2.54)
(0.92-1.96)
(0.80-2.54)
(0.76-2.79)
Farm area
Models are adjusted for herd type, herd size, farm area, historic incidence and the number of nearby herds (in grey). Significant associations are denoted in bold.
--- denotes that odds ratios were not estimable.
6. Alternative analyses
Permutation tests
Herds geographically close to one another are more likely to have similar covariates.
Furthermore, if bTB is present in an area, then the areas around it are more likely to also be affected.
We investigated any impact of unmodelled spatial correlation on our results using permutation
tests. For each univariable and multivariable model, paired herds were randomly relabelled as “case
herd” or “control herd” and new estimates were derived. We fitted each model and calculated the
proportion of permutations for which we observed, for each variable, an effect at least as significant
as the one in the model fitted to the observed (non-randomised data) to obtain permutation-based
p-values. We found that the standard p-values (as reported in the main text) were very similar to
those obtained from the permutation tests (Table 13) and thus any unmodelled spatial correlation
within the data had not affected the significance of our reported results.
Inclusion of the herd’s distance to the trial boundary
We observed an apparently protective effect of the number of badgers proactively culled
before the onset of reactive culling (main text Table 2). A possible explanation could be that, as a
result of the selection process for control herds (see above), control herds were more likely to be
located close to the trial area boundary and therefore more likely to have had badgers proactively
culled in their vicinity. To allow for this potential effect, we re-fitted all models adjusting for herds’
distances to the trial area boundary. We found that the output from the models adjusted for the
distance to the trial area boundary (Table 14) were very similar to those without this adjustment
(main text). We also observed that the number of badgers proactively culled before the onset of
reactive culling remained a significant protective factor, even after adjusting for the herds’ distances
to the trial area boundary.
Table 13: P-values of the permutation tests for the multivariable models of the associations of cases with increased numbers of RBCT culled badgers and increased
numbers of confirmed bTB breakdowns in the previous year.
Leading
During
Post1
Post2
Distance (km)
1
3
5
1
3
5
1
3
5
1
3
5
Nearby RBCT
----
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
----
p = 0.047
p = 0.21
----
p = 0.04
p = 0.22
p = 0.003
p = 0.001
p = 0.02
p = 0.10
p = 0.67
p = 0.75
p = 0.003
p < 0.001
p = 0.03
p < 0.001
p < 0.001
p = 0.02
Herd type [Dairy]
p < 0.001
p < 0.001
p < 0.001
p = 0.03
p = 0.01
p = 0.004
p = 0.03
p = 0.11
p = 0.02
p = 0.04
p = 0.15
p = 0.03
Herd size
p = 0.03
p = 0.04
p = 0.03
p = 0.64
p = 0.53
p = 0.62
p = 0.64
p = 0.80
p = 0.86
p = 0.79
p = 0.87
p = 0.92
Farm area
p < 0.001
p = 0.003
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
bTB historic
p = 0.003
p < 0.001
p = 0.01
p = 0.83
p = 0.74
p = 0.62
p = 0.95
p = 0.74
p = 0.84
p = 0.82
p = 0.52
p = 0.71
p = 0.44
p = 0.43
p = 0.27
p = 0.13
p = 0.03
p = 0.49
p = 0.31
p = 0.12
p = 0.12
p = 0.51
p = 0.07
p = 0.12
culled badgers
Nearby confirmed
bTB breakdowns
incidence
Number of herd tested
not under bTB restriction
Refer to footnotes from Table 12
Table 14: Odds ratios (OR) with 95% confidence intervals for the multivariable models of the associations of cases with increased numbers of RBCT culled badgers
and increased numbers of confirmed bTB breakdowns in the previous year and accounting for herds’ distance to the trial area boundary.
Leading
During
Post1
Post2
Distance (km)
1
3
5
1
3
5
1
3
5
1
3
5
Nearby RBCT
----
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
----
p = 0.06
p = 0.26
----
p = 0.06
p = 0.32
OR: 0.42
OR: 0.53
OR: 1.26
OR: 1.35
OR: 1.47
OR: 0.66
OR: 0.90
OR: 0.68
OR: 0.91
(0.26-0.70)
(0.38-0.72)
(1.12-1.42)
(1.20-1.53)
(1.27-1.69)
(0.43-1.01)
(0.74-1.09)
(0.46-1.01)
(0.75-1.10)
culled badgers
Nearby confirmed
p = 0.02
p = 0.003
p = 0.04
p = 0.13
p = 0.76
p = 0.60
p = 0.002
p = 0.001
p = 0.03
p = 0.001
p < 0.001
p = 0.02
bTB breakdowns
OR: 1.46
OR: 2.18
OR: 2.09
OR: 1.22
OR: 1.20
OR: 0.86
OR: 1.51
OR: 1.93
OR: 1.70
OR: 1.63
OR: 2.15
OR: 1.84
(1.08-1.97)
(1.30-3.66)
(1.03-4.23)
(0.44-1.59)
(0.69-1.66)
(0.49-1.50)
(1.16-1.96)
(1.30-2.87)
(1.06-2.74)
(1.21-2.19)
(1.37-3.36)
(1.09-3.08)
Herd type
p < 0.001
p < 0.001
p < 0.001
p = 0.02
p = 0.007
p = 0.003
p = 0.02
p = 0.09
p = 0.02
p = 0.03
p = 0.14
p = 0.03
[Dairy]
OR: 8.98
OR: 10.85
OR: 9.23
OR: 2.19
OR: 2.45
OR: 2.89
OR: 1.91
OR: 1.65
OR: 1.97
OR: 1.90
OR: 1.61
OR: 1.92
(3.22-31.24)
(3.65-41.75)
(3.15-34.23)
(1.18-4.20)
(1.31-4.78)
(1.48-5.95)
(1.10-3.40)
(0.93-3.01)
(1.14-3.47)
(1.06-3.52)
(0.86-3.04)
(1.08-3.49)
p = 0.02
p = 0.04
p = 0.02
p = 0.40
p = 0.33
p = 0.32
p = 0.64
p = 0.80
p = 0.88
p = 0.80
p = 0.89
p = 0.98
OR: 0.82
OR: 0.83
OR: 0.82
OR: 0.94
OR: 0.93
OR: 0.93
OR: 0.98
OR: 0.99
OR: 0.99
OR: 0.99
OR: 0.99
OR: 1.00
(0.70-0.97)
(0.70-0.99)
(0.69-0.97)
(0.83-1.08)
(0.82-1.07)
(0.82-1.07)
(0.89-1.07)
(0.90-1.08)
(0.91-1.09)
(0.89-1.02)
(0.89-1.10)
(0.90-1.10)
p < 0.001
p = 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
p < 0.001
OR: 19.35
OR: 14.31
OR: 17.22
OR: 27.66
OR: 26.18
OR: 34.66
OR: 8.87
OR: 10.19
OR: 11.23
OR: 8.72
OR: 9.37
OR: 10.49
(3.83-97.65)
(2.80-73.13)
(3.50-84.68)
(8.63-88.68)
(8.09-84.67)
(10.05-119.57)
(3.60-21.85)
(4.05-25.67)
(4.57-27.60)
(3.28-23.18)
(3.45-25.42)
(3.98-27.67)
bTB historic
p = 0.007
p = 0.006
p = 0.02
p = 0.85
p = 0.99
p = 0.83
p = 0.93
p = 0.74
p = 0.80
p = 0.81
p = 0.51
p = 0.65
incidence
OR: 0.28
OR: 0.25
OR: 0.29
OR: 1.06
OR: 1.00
OR: 0.92
OR: 1.02
OR: 1.10
OR: 1.071
OR: 1.07
OR: 1.21
OR: 1.14
(0.11-0.70)
(0.09-0.67)
(0.10-0.81)
(0.56-2.02)
(0.51-1.99)
(0.45-1.90)
(0.61-1.72)
(0.63-1.90)
(0.63-1.81)
(0.62-1.84)
(0.68-2.17)
(0.66-1.97)
Number of herd tested
p = 0.63
p = 0.47
p = 0.33
p = 0.10
p = 0.04
p = 0.08
p = 0.33
p = 0.10
p = 0.13
p = 0.51
p = 0.08
p = 0.16
not under bTB restriction
OR: 1.09
OR: 1.23
OR: 1.45
OR: 0.81
OR: 0.70
OR: 0.71
OR: 1.16
OR: 1.47
OR: 1.49
OR: 1.12
OR: 1.58
OR: 1.51
(0.77-1.54)
(0.70-2.16)
(0.69-3.05)
(0.63-1.04)
(0.50-0.98)
(0.49-1.04)
(0.86-1.57)
(0.92-2.33)
(0.89-2.49)
(0.80-1.55)
(0.95-2.63)
(0.85-2.67)
Distance to trial area
p = 0.04
p = 0.30
p = 0.17
p = 0.02
p = 0.03
p = 0.006
p = 0.67
p = 0.82
p = 0.45
p = 0.44
p = 0.62
p = 0.25
boundary
OR: 2.24
OR: 1.55
OR: 1.47
OR: 2.24
OR: 2.19
OR: 2.83
OR: 1.14
OR: 1.08
OR: 1.27
OR: 1.29
OR: 1.19
OR: 1.47
(1.05-4.78)
(0.67-3.56)
(0.79-3.92)
(1.14-4.39)
(1.08-4.43)
(1.36-5.92)
(0.62-2.11)
(0.57-2.03)
(0.68-2.35)
(0.67-2.48)
(0.60-2.34)
(0.76-2.85)
Herd size
Farm area
Models are adjusted for herd type, herd size, farm area, historic incidence, the number of nearby herds and the distance to the trial area boundary (in grey). Significant
associations are denoted in bold. --- denotes that odds ratios were not estimable.
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badger culling versus no culling on TB incidence in British cattle: a randomised trial. 2005 [cited
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