Norwegian farmers' vigilance in reporting sheep showing scrapie-associated signs.

Abstract

Scrapie is a chronic neurodegenerative disease affecting small ruminants and belongs to the transmissible spongiform encephalopathies. Scrapie is considered a serious animal disease and it has been notifiable in Norway since 1965. The clinical signs of scrapie might be vague and the farmers, if familiar with the signs of scrapie, are often in the best position for detecting scrapie suspects. In 2002, an anonymous questionnaire survey was conducted in order to assess Norwegian sheep farmers' vigilance of scrapie.
Although the potential detection of a scrapie-positive animal would lead to the destruction of the sheep flock concerned, almost all the farmers (97 %) expressed their willingness to report scrapie suspects. This was most certainly dependent on the Government taking the economic responsibility for the control programme as nearly all the farmers responded that this was an important condition. Listeriosis is relatively common disease in Norwegian sheep and a differential diagnosis for scrapie. In a multinomial logistic regression the reporting behaviour for non-recovering listeriosis cases, used as a measurement of willingness to report scrapie, was examined. The reporting of non-recovering listeriosis cases increased as the knowledge of scrapie-associated signs increased, and the reporting behaviour was dependent on both economic and non-economic values.
The results indicate that in 2002 almost all sheep farmers showed willingness to report any scrapie suspects. Nevertheless there is an underreporting of scrapie suspects and the farmers' awareness and hence their vigilance of scrapie could be improved. Furthermore, the results suggest that to ensure the farmers' compliance to control programmes for serious infectious diseases, the farmers' concerns of non-economic as well as economic values should be considered.

Full text

Page 1

BioMed Central
Page 1 of 9
(page number not for citation purposes)
BMC Veterinary Research
Open Access
Research article
Norwegian farmers' vigilance in reporting sheep showing
scrapie-associated signs
Petter Hopp*1, Synnøve Vatn2 and Jorun Jarp1
Address: 1Section of epidemiology, National Veterinary Institute Oslo, P.O. Box 8156 Dep., NO-0033 OSLO, Norway and 2The Norwegian Sheep
Health Service, P.O. Box 396 Økern, NO-0513 OSLO, Norway
Email: Petter Hopp* - Petter.Hopp@vetinst.no; Synnøve Vatn - Synnove.Vatn@animalia.no; Jorun Jarp - Jorun.Jarp@vetinst.no
* Corresponding author
Abstract
Background: Scrapie is a chronic neurodegenerative disease affecting small ruminants and belongs
to the transmissible spongiform encephalopathies. Scrapie is considered a serious animal disease
and it has been notifiable in Norway since 1965. The clinical signs of scrapie might be vague and the
farmers, if familiar with the signs of scrapie, are often in the best position for detecting scrapie
suspects. In 2002, an anonymous questionnaire survey was conducted in order to assess
Norwegian sheep farmers' vigilance of scrapie.
Results: Although the potential detection of a scrapie-positive animal would lead to the
destruction of the sheep flock concerned, almost all the farmers (97 %) expressed their willingness
to report scrapie suspects. This was most certainly dependent on the Government taking the
economic responsibility for the control programme as nearly all the farmers responded that this
was an important condition. Listeriosis is relatively common disease in Norwegian sheep and a
differential diagnosis for scrapie. In a multinomial logistic regression the reporting behaviour for
non-recovering listeriosis cases, used as a measurement of willingness to report scrapie, was
examined. The reporting of non-recovering listeriosis cases increased as the knowledge of scrapie-
associated signs increased, and the reporting behaviour was dependent on both economic and non-
economic values.
Conclusion: The results indicate that in 2002 almost all sheep farmers showed willingness to
report any scrapie suspects. Nevertheless there is an underreporting of scrapie suspects and the
farmers' awareness and hence their vigilance of scrapie could be improved. Furthermore, the
results suggest that to ensure the farmers' compliance to control programmes for serious
infectious diseases, the farmers' concerns of non-economic as well as economic values should be
considered.
Background
Scrapie is a fatal neurodegenerative disease affecting sheep
and goat. It belongs to the transmissible spongiform
encephalopathies (TSE), and there are at least two types:
classical and atypical scrapie [1]. From the 1960s, the Nor-
wegian Government has considered scrapie a serious ani-
mal disease, and if it was detected attempts would be
made to eradicate it [2]. During recent years there has
been growing international concern about TSEs in sheep
as sheep might have acquired bovine spongiform enceph-
Published: 12 December 2007
BMC Veterinary Research 2007, 3:34doi:10.1186/1746-6148-3-34
Received: 11 July 2007
Accepted: 12 December 2007
This article is available from: http://www.biomedcentral.com/1746-6148/3/34
© 2007 Hopp et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Page 2

BMC Veterinary Research 2007, 3:34 http://www.biomedcentral.com/1746-6148/3/34
Page 2 of 9
(page number not for citation purposes)
alopathy (BSE) from concentrated feeds contaminated
with the BSE agent [3], and BSE and scrapie cannot be dif-
ferentiated by clinical signs or histopathological findings
in the sheep [4]. This has led to the implementation of
extensive surveillance programmes and strict control
measures for TSEs in small ruminants in several countries
[5].
The first case of scrapie in indigenous Norwegian sheep
was detected in 1981 and an increasing number of cases
was detected in the 1990s [6] leading to the introduction
of the Norwegian scrapie surveillance and control pro-
gramme in 1997. The programme comprises an informa-
tion campaign aimed at Norwegian sheep farmers, a
surveillance programme, control measures in the flocks
where scrapie-positive animals have been detected (here-
after referred to as scrapie-positive flocks), and measures
at the national level restricting the movement of sheep [7].
From the first scrapie case in 1981, all small ruminants in
scrapie-positive flocks were culled [7]. The additional con-
trol measures at the flock level included extensive sanita-
tion measures (removal of manure, removal of material
unsuited for disinfection, cleaning and disinfection of
buildings, changing of upper layer on surrounding roads,
ploughing and/or burning of grazing areas and fitting of
new fences where in contact with sheep), an empty period
of two (three since 2005) years, and the flock being sub-
ject to restrictions for five years after restocking. These
control measures may also be implemented in flocks that
have had contact with scrapie-positive flocks by move-
ment of animals. Until 2004, the control measures
applied were equal regardless of whether classical or atyp-
ical scrapie was diagnosed. Thereafter, partial depopula-
tion has been used in flocks where atypical scrapie has
been found. The farmers receive full compensation for the
costs of the animals and the control measures [8]. More
than 60 scrapie-positive flocks of totally approximately
20,000 flocks in Norway had been destroyed by the start
of this study in 2002. In addition between 600 and 700
contact flocks were depopulated in 1996 to curb the trend
of increasing numbers of scrapie-positive flocks [7]. The
magnitude of the measures applied to control scrapie sur-
passes the control measures applied for any other disease
experienced by the Norwegian sheep industry at least
since the 1950s [9]. We therefore expect the sheep farmers
to be especially concerned about the detection of scrapie.
Scrapie has been notifiable in Norway since 1965 [2] and
the detection of scrapie was first based on passive surveil-
lance only. In 1997 an active surveillance programme of
slaughtered animals was introduced, and in 2002 surveil-
lance of slaughtered animals and fallen stock was imple-
mented in accordance with the Commission Regulation
(EC) 999/2001 [5]. In1997, all farmers were given written
information that animals showing typical signs of scrapie
such as pruritus and neurological signs should be reported
to the District Veterinary Officer (DVO) [10] and thereaf-
ter all farms have been visited and given information on
scrapie by the DVO every second or third year as a part of
the scrapie surveillance and control programme. In the
early clinical stage, the signs are often vague, such as a
change of behaviour, and typical clinical signs may not be
seen until late in the incubation period [11] which might
last for several years [4]. Important differential diagnoses
of scrapie are other diseases that produce neurological
signs, including listeriosis [12]. Hence, cases that show
signs of listeriosis and do not recover after treatment
should be regarded as scrapie suspects.
If the farmer is familiar with the signs of scrapie, he is in
the best position to detect scrapie suspects. However,
whether the farmer decides to report suspicious clinical
cases and found-dead animals or to conceal them will
depend on his motivation to report the disease [13].
Therefore, the reporting of scrapie suspects by the farmers
is dependent on their knowledge and awareness of the
disease and their willingness to report the disease which
might be summarised as their vigilance towards the dis-
ease [14].
Acknowledging the importance of the farmers for the per-
formance of the scrapie surveillance programmes, a ques-
tionnaire survey among Norwegian sheep farmers was
conducted in 2002. The aims of the study were to analyse
the sheep farmers' vigilance in reporting animals with a
higher risk of having scrapie, measured as reporting ani-
mals showing typical scrapie-associated signs and non-
recovering cases showing signs of listeriosis. In this study
no differentiation was made between classical scrapie and
atypical scrapie as the same control measures were
applied to the two scrapie types in 2002.
Results
Response rate
The questionnaires were returned from 2125 of 3000
farmers. Of these, 55 farmers who reported having less
than ten breeding sheep were excluded from the study,
giving a response rate of 70%. Farmers were considered as
drop-outs when they had given no information on region,
flock size, scrapie status, and reporting behaviour of non-
recovering listeriosis cases or if they gave no answer to any
of the questions concerning their knowledge or their will-
ingness to report. In total 97 questionnaires were drop-
outs, giving information from 1973 questionnaires (67%)
that were available for analysis.

Page 3

BMC Veterinary Research 2007, 3:34http://www.biomedcentral.com/1746-6148/3/34
Page 3 of 9
(page number not for citation purposes)
Description of the study population
Farmers' willingness to report scrapie suspects
Most farmers (97%) answered that they would be willing
to report scrapie suspects. The remainder constituted
those who would slaughter or kill the animal (2%) and
those who did not know how they would act in the situa-
tion (1%). When there was a non-recovering listeriosis
case, 21% of the farmers would report the animal as a
scrapie suspect and 51% of the farmers would have the
animal re-examined by a veterinary practitioner. The
remaining farmers would cull the animal.
Farmers' knowledge of scrapie-associated signs
Each of the scrapie-associated signs listed were correctly
checked by 34% to 69% of the farmers. Itching and trem-
bling were the most well-known signs, being recognised
by 69% and 67% of the farmers, respectively. At least two
associated and zero non-associated signs were checked by
71% of the farmers, and at least three associated and zero
non-associated signs were checked by 47% of the farmers.
Each of the signs considered as not being associated with
scrapie was checked by 0.5% to 4% of the farmers.
Approximately 2% of the farmers were not familiar with
any scrapie-related symptoms, and approximately 6% did
not answer the question.
Farmers' anticipated reactions if scrapie were to be detected in their
flock
In the hypothetical situation where scrapie was detected
in one of the farmer's sheep, the statement "Satisfied that
the detection of scrapie would enable the eradication of
the disease from the flock" was considered to be very
important by 55% of the farmers and important or very
important by 81% of them (Table 1).
If scrapie should be detected in the farmer's flock, the con-
cerns "Worried about losing income", "Worried about the
emotional distress of losing the animals", and "Worried
about loss of breeding material" were expected to be very
important for 48%, 42% and 35% of the farmers respec-
tively (Table 1). The concern "Worried about being
accused of spreading scrapie" was expected to be consid-
ered very important by 26% of the farmers. For both the
concerns "Worried about blaming oneself for having got
scrapie" and "Worried about losing work", less than 14%
of the farmers considered these as very important.
The farmers' opinion of factors potentially important for reporting
behaviour
The statement that "The Government compensates for the
cost of the control measures when scrapie is detected" was
considered to be very important by 71% of the farmers
and important or very important by 87% of the farmers.
"Having easy access to a DVO" and "Being offered free
examination of scrapie suspects" were considered impor-
tant or very important by 88% and 70% of the farmers
respectively (Table 1).
Multivariate analysis
In the multivariate analysis (Table 2), the relative risk
ratio (RRR) for "Notifying" or "Re-examine" as compared
to "Not report" the non-recovering listeriosis cases
increased significantly as the farmers' knowledge of
scrapie-associated signs increased. For the farmers who
would find it very important to be offered free examina-
tion of the animal, the RRR for "Notifying" were signifi-
cantly higher compared to those who would "Re-
examine" the animal (RRR = 1.6). The RRR for "Notify-
ing" the non-recovering listeriosis cases was significantly
higher for those who would find it very important that the
detection of scrapie would enable eradication of scrapie
compared both to those who would "Not report" (RRR =
2.4) and those who would "Re-examine" the animal (RRR
= 1.2). For the farmers who were concerned that they
would be worried about blaming themselves for having
got scrapie, the RRR for "Re-examine" was significantly
higher compared to "Not report". The variables "Satisfied
that the detection of scrapie would enable the eradication
of the disease from the flock" and "Worried about blam-
ing themselves for having got scrapie" significantly modi-
fied the effect of each other (in the model), so that the
effect of these two variables were antagonistic. The RRR
for reporting was significantly higher for flocks of less
than 50 sheep compared to larger flocks, while geograph-
ical region was not a significant explanation variable in
the final model.
Discussion
It is a great strength for the Norwegian scrapie surveillance
and control programme that almost all Norwegian sheep
farmers in our study answered that they would be willing
to report scrapie suspects in their flock. The results indi-
cate that they support the programme, despite the fact that
the consequence of detecting a scrapie-positive animal in
their flock would be the destruction of all small ruminants
in their flock. This was supported by the result that most
of the farmers stated that they would consider it impor-
tant that the detection of scrapie would enable the eradi-
cation of the disease from the flock, indicating that the
individual farmer takes responsibility for the sheep indus-
try. The active involvement of the farmers' organisations
has been important for the implementation of national
disease control programmes – for example the pro-
gramme for bovine virus diarrhoea in cattle [15] – and the
result of this study might be interpreted as support from
the individual farmer to such a policy.
The high percentage of the farmers who were willing to
report scrapie is most certainly dependent on the Govern-
ment taking the economic responsibility for the control

Page 4

BMC Veterinary Research 2007, 3:34http://www.biomedcentral.com/1746-6148/3/34
Page 4 of 9
(page number not for citation purposes)
Table 1: The Norwegian farmers' responses to a questionnaire study in 2002
Reporting behaviour
No. of responses (row %)
Explanatory variable/Category N for variable Not reportRe-examine Notifying
Region
Northern Norway
Middle Norway
Western Norway
South-Eastern Norway
Flock size
≥ 100 breeding sheep
50–99 breeding sheep
10–49 breeding sheep
Knowledge of scrapie-associated symptoms
0 signs recognised
1 signs recognised
2 signs recognised
3 signs recognised
4 signs recognised
5 signs recognised
I need more knowledge of scrapie symptoms
Very important
Less important †
Having easy access to a District Veterinary Officer (DVO)
Very important
Less important †
Being offered free examination of scrapie suspects
Very important
Less important †
The Government compensates for the cost of the control
measures when scrapie is detected
Very important
Less important †
Worried about losing income
Very important
Less important †
Worried about losing work
Very important and Important
Of minor Importance and Not important
Worried about loss of breeding material
Very important
Less important †
Worried about the emotional distress of losing animals
Very important
Less important †
Worried about being accused of spreading scrapie
Very important and Important
Of minor Importance and Not important
Worried about blaming oneself for having got scrapie
Very important and Important
Of minor Importance and Not important
Satisfied that the detection of scrapie would enable the
eradication of the disease from the flock
Very important
Less important †
1973
76 (31)
102 (32)
211 (25)
167 (30)
133 (53)
154 (48)
448 (53)
276 (50)
40 (16)
64 (20)
190 (22)
112 (20)
1973
111 (40)
209 (32)
236 (23)
119 (43)
330 (50)
562 (54)
47 (17)
122 (18)
237 (23)
1852
13 (37)
105 (36)
147 (29)
143 (27)
87 (27)
24 (15)
22 (63)
138 (47)
248 (49)
290 (55)
157 (48)
91 (56)
0 (0)
49 (17)
115 (23)
92 (18)
83 (25)
48 (29)
1697
185 (27)
297 (30)
354 (51)
511 (51)
157 (23)
193 (19)
1856
236 (24)
286 (34)
523 (52)
418 (49)
244 (24)
149 (17)
1748
244 (29)
260 (28)
376 (45)
501 (55)
213 (26)
154 (17)
1815
404 (29)
111 (27)
692 (49)
221 (54)
310 (22)
77 (19)
1737
279 (30)
222 (28)
447 (48)
424 (53)
215 (23)
150 (19)
1622
200 (29)
267 (29)
339 (49)
483 (52)
153 (22)
180 (19)
1683
188 (27)
296 (30)
350 (51)
506 (51)
147 (21)
196 (20)
1720
207 (25)
288 (32)
440 (54)
433 (48)
174 (21)
178 (20)
1631
278 (26)
189 (33)
551 (52)
276 (48)
222 (21)
115 (20)
1616
220 (26)
250 (33)
455 (53)
361 (48)
181 (21)
149 (20)
1711
264 (24)
212 (34)
548 (50)
327 (52)
276 (25)
84 (13)
The distribution of the responses is given with regard to the reporting behaviour for non-recovering listeriosis cases.
† Less important includes the categories: Important, Of minor importance, and Not important.

Page 5

BMC Veterinary Research 2007, 3:34
http://www.biomedcentral.com/1746-6148/3/34
Page 5 of 9
(page number not for citation purposes)
Table 2: The results from the regression analyses of a questionnaire survey performed among Norwegian sheep farmers.
Explanatory variable/Category Notifying vs Not reportRe-examine vs Not report Notifying vs Re-examineWald type III p-value
BetaRRR RRR 95% CIBetaRRRRRR 95% CI Beta RRRRRR 95% CI
Knowledge of scrapie-associated signs
Continuous
Being offered free examination of scrapie
suspects
Very important
Less important ‡
That the detection of scrapie would enable
eradication of scrapie from the flock
Very important
Less important ‡
Worried about blaming oneself for having got
scrapie for the farmers who considered
detection of scrapie Very important
Very important and Important
Of minor Importance and Not
important
Worried about blaming oneself for having got
scrapie for the farmers who considered
detection of scrapie Less important ‡
Very important and Important
Of minor Importance and Not
important
Flock size
≥ 100 breeding sheep
50–99 breeding sheep
10–49 breeding sheep
< 0.001
0.3 1.4 †
1.2 – 1.6 0.21.3 †
1.1 – 1.40.09 1.11.0 – 1.2
0.003
0.31.3
1
1.0 – 1.8 -0.20.8
1
0.6 – 1.10.51.6 †
1
1.2 – 2.1
< 0.001
0.9 2.4 †
1
1.7 – 3.4 0.2 1.2
1
1.0 – 1.60.7 2.0 †
1
1.4 – 2.7
0.74
0.2 1.3
1
0.7 – 2.50.51.7
1
1.0 – 2.8 -0.3 0.8
1
0.4 – 1.4
< 0.001
0.3 1.4
1
0.7 – 3.0 0.8 2.3 †
1
1.3 – 3.9-0.50.6
1
0.3 – 1.2
< 0.001
-0.9
-0.9
0.4 †
0.4 †
1
0.2 – 0.9
0.2 – 0.9
-0.9
-0.5
0.4 †
0.6
1
0.2 – 0.8
0.4 – 1.1
-0.01
-0.4
1.0
0.7 †
1
0.5 – 2.1
0.3 – 1.4
The results from the multinomial logistic regression analyses with the reporting behaviour of non-recovering listeriosis cases as the response variable in a questionnaire survey performed
among Norwegian sheep farmers in 2002 (N = 1416). Not report was used as the reference group. The parameter estimates for "Worried about blaming oneself for having got scrapie" were
presented for each level of the variable "That the detection of scrapie would enable eradication of scrapie from the flock" due to interaction between the variables. The contrast Notifying vs Re-
examine is mathematically redundant with the two first contrasts, but is presented for comparative purposes.
Likelihood ratio (chi-square) = 246.8, degrees of freedom = 254, p-value of the final model = 0.62
† p-value of estimate < 0.05
‡ Less important includes the categories: Important, Of minor importance, and Not important.

Page 6

BMC Veterinary Research 2007, 3:34http://www.biomedcentral.com/1746-6148/3/34
Page 6 of 9
(page number not for citation purposes)
programme since nearly all the farmers responded that
this was an important condition. Although depopulation
of scrapie-positive flocks might be a cost-effective control
option at the national level, the individual farmer may not
be able to manage the economic loss imposed by such a
policy alone. In many countries the farmers' economic
loss resulting from depopulation is therefore partly or
fully compensated by the Government, or by using com-
mon funds or other insurance systems. In Norway, a
standardised compensation per animal destroyed is
offered, and the sanitary measures applied are fully cov-
ered by the Government. In addition, production subsi-
dies are given for the empty period (up to three years) at
the same level as the year prior to the diagnosis [8]. The
economic loss is thus at least partly compensated.
Although the farmers might express their true intention of
reporting scrapie suspects, it is difficult to know what their
behaviour would be when confronted with the actual sit-
uation. Results of surveys performed in the Netherlands
and Great Britain have shown an underreporting of
scrapie suspects [16-18]. During the period from 2000 to
2002, the number of scrapie suspects annually reported
decreased from 47 to 39 [19] and decreased further to 25
in 2006. In the Norwegian sheep population more than
2000 clinical listeriosis cases have been reported annually
[20]. Assuming 40% to 50% mortality from listeriosis
[21] there should be at least 800 found-dead sheep that
have shown signs of neurological disorders. Hence, the
low number of submitted scrapie suspects indicates an
underreporting of these cases in Norway despite that the
farmers have expressed willingness to report them.
The fact that only 21% would notify non-recovering liste-
riosis cases while almost all would notify suspect scrapie
cases supports that there is an underreporting in Norway.
One explanation might be that listeriosis is a well known
disease and that the farmers don't find it necessary to
report it as scrapie suspects. However, the fact that "Noti-
fying" non-recovering listeriosis cases was associated with
better knowledge of scrapie-associated signs suggests that
underreporting might partly be due to lack of knowledge
of which signs should be reported as suspicious of scrapie.
Whatever the reason, this does not necessarily represent a
deliberate underreporting of scrapie to hide the disease.
This might seem to be in contrast to the fact that 88% of
the farmers recognised at least one of the scrapie-associ-
ated signs. Furthermore, the fact that each of the scrapie-
associated signs were correctly identified by 34% to 69%
of the Norwegian farmers, seems comparable with the
results of studies from Ireland and the Netherlands where
each of the scrapie-associated signs was correctly identi-
fied by 25% to 50% of the farmers [16,22] However,
scrapie has been detected in less than 0.5% of the sheep
flocks in the population, and most of the scrapie-positive
flocks have been detected in a limited geographical area
[6]. Consequently most farmers have had no practical
experience of scrapie, and the typical farmer might not be
able to recognise the many vague signs of the disease [11],
although in theory he is able to identify at least one typical
sign.
To control serious infectious diseases it is important to
ensure that the behaviour of the farmers does not under-
mine the disease control programmes. The results of the
multivariate analysis indicate that farmers' attitudes and
concerns of non-economic values might be important for
their reporting behaviour. Therefore, both economic com-
pensation as well as considering the farmers' non-eco-
nomic values should be taken into account when
designing a control programme. This might be valid for all
diseases where extensive control measures are put in force.
We are not aware that the importance of non-economic
values for the reporting behaviour of serious diseases has
been examined, and we would suggest that this is
explored further in a sociological context.
The disease produces neurological signs that most farmers
are expected to be aware of, and the farmers have been
given the information that animals that show neurologi-
cal disorders should be regarded as scrapie suspects. Con-
sequently we chose to use the reporting behaviour of non-
recovering listeriosis cases as a measurement of the
farmer's vigilance in reporting animals with signs suspi-
cious of scrapie. However, as listeriosis as such is not a
notifiable disease, the reporting behaviour of the farmers
reflects both their knowledge of scrapie-associated signs
and their willingness to report scrapie. The reporting of
non-recovering listeriosis cases must therefore be consid-
ered an indirect measure for the farmers' vigilance. Never-
theless, we consider the fact that the factors farmers'
knowledge, economy and non-economic values were
important for the reporting behaviour to be reasonable
for non-recovering listeriosis cases, as well as for scrapie
suspects.
In accordance with previous questionnaire surveys con-
cerning scrapie [16-18,23] the questionnaire survey was
performed as an anonymous study to reduce the potential
problem of farmers concealing their true opinion.
Although the problem of misleading answers cannot be
totally avoided through anonymity, the results of the
study indicate that when considering a hypothetical situa-
tion most of the respondents were willing to report
scrapie suspects in 2002.
The response rate in this study, 70%, is high compared
with the typical anonymous postal survey within health
sciences [24] as well as other scrapie studies using anony-

Page 7

BMC Veterinary Research 2007, 3:34 http://www.biomedcentral.com/1746-6148/3/34
Page 7 of 9
(page number not for citation purposes)
mous questionnaires [16-18,22,23]. Although a potential
non-response bias was not formally tested, a higher
response rate should reduce the non-response bias [25];
however, a non-response bias might still exist.
Information from 557 farmers was not included in the
final model due to non-responses (missing) of one or
more questions. There were from 10% to 20% non-
responses for each of the questions concerning the farm-
ers' anticipated reactions if scrapie was detected in their
flock, which could indicate a non-response bias. We
received no indications that these questions were contro-
versial for the farmer, but the farmer might have consid-
ered these questions difficult due to their hypothetical
form. The non-responses did not show any significantly
different distribution for any of the response variables.
Therefore, we do not expect that any substantial problem
with non-response bias was created by this.
The farmers' awareness of scrapie and their willingness to
report scrapie should not be considered static. After this
study was conducted, scrapie Nor98 – an atypical scrapie
– has constituted most of the scrapie cases detected in
Norway [26]. The control measures of scrapie Nor98 have
been considered too strict [8] considering the low trans-
missibility of the disease [26]. The farmers' motivation to
report scrapie might therefore have been reduced and
hence lead to reduced reporting of scrapie.
Conclusion
The farmers' vigilance is essential for the detection of clas-
sical scrapie as, despite the extensive surveillance pro-
grammes, most flocks with classical scrapie have been
detected due to cases being notified or animals submitted
to the laboratory for disease examination [19]. The results
of this study indicate that in 2002 almost all sheep farm-
ers showed willingness to report any scrapie suspects.
Nevertheless there is an underreporting of scrapie suspects
and the farmers' awareness and hence their vigilance of
scrapie could be improved. Consequently, it will be
important to continue to motivate the farmers to report,
to improve their awareness of scrapie, and to communi-
cate the importance of also reporting animals showing
only vague signs or signs typical of differential diagnoses
for scrapie. Furthermore, the results suggest that to ensure
the farmers' compliance to control programmes for seri-
ous infectious diseases, the farmers' concerns of non-eco-
nomic as well as economic values should be considered.
Methods
Design and study population
The study was designed as a cross-sectional study. Three
thousand sheep farmers were randomly selected from the
Register of Production Subsidies using a pseudo random
number procedure [27]. To exclude hobby farmers, only
sheep farmers who had ten or more breeding sheep were
considered for selection. Altogether 18,404 sheep farmers
were eligible.
Data collection
The data were collected by an anonymous questionnaire
survey. The four-page questionnaire contained questions
concerning location and flock characteristics, contact pat-
terns and management, and the farmer's knowledge of
scrapie and his attitude towards the Norwegian scrapie
surveillance and control programme. The questionnaire
(in Norwegian) is available from the corresponding
author.
The questionnaire was accompanied by a covering letter
and a free-post return envelope. It was mailed to all par-
ticipants in March 2002 followed by a reminder card in
April 2002. The data from the questionnaires were entered
into an MS access database (Microsoft® Access 2000 Ver-
sion 9. Microsoft Corporation, WA, USA, 1992–2001).
The farmers' willingness to report scrapie
The farmers were asked how they would act if they discov-
ered an animal showing signs suggestive of scrapie. Those
answering "Report to DVO" or "Submit the material to a
diagnostic laboratory" were considered to be "Willing to
report scrapie suspects", while those only marking "Send
to slaughter" or "Cull the animal" were considered not
willing to report these cases. The answer "Don't know"
were treated as missing.
Furthermore, the farmers were asked for their reporting
behaviour in the situation where an animal had shown
clinical signs of listeriosis and did not recover after treat-
ment (hereafter "non-recovering listeriosis cases"). The
answers "Contact DVO for examination regarding
scrapie" (in short "Notifying") and "Contact veterinary
practitioner for further examination" (in short "Re-exam-
ine") were kept as separate categories, while the answers
"Send to slaughter" or "Kill the animal" were grouped
together in the category "Not report" giving three different
categories in total. The answer "Don't know" was treated
as missing.
Explanatory variables
Demographic information
The farms were located in four geographical regions:
South-Eastern, Western, Middle and Northern Norway,
based on county. The farmers were asked to specify the
flock size within one of four groups: 1–10, 10–49, 50–99
or ≥ 100 breeding sheep.
The farmers' knowledge of scrapie signs
Using check-boxes, the farmers were asked to mark the
clinical signs they considered as associated with scrapie

Page 8

BMC Veterinary Research 2007, 3:34http://www.biomedcentral.com/1746-6148/3/34
Page 8 of 9
(page number not for citation purposes)
among ten different clinical signs, where emaciation, hair
loss, lip smacking, pruritus and trembling were consid-
ered as scrapie-associated signs, and abortion, coughing,
diarrhoea, fever, and frequent urinating were considered
as not associated with scrapie. The question was consid-
ered answered when at least one of the check-boxes was
marked. The information was collated into one variable
by summing the number of correctly checked scrapie-
associated signs. In the multivariate analysis, the variable
was treated as a numerical variable.
The farmers' anticipated reactions if scrapie should be detected
The information that the detection of a scrapie-positive
animal would lead to the destruction of all the sheep in
the flock was presented in the questionnaire. The farmers
were then asked to give their anticipated reaction to seven
concerns regarding the potential detection of scrapie in
their flock (Table 1). The reactions were graded in four
levels: not important, of minor importance, important,
and very important. For the multivariate analysis, each
variable was dichotomised to derive two evenly-sized
groups (Table 1).
The farmers' opinion on factors potentially important for reporting
behaviour
The farmers were asked about the importance of four fac-
tors which might affect whether they would report an ani-
mal with signs suggestive of scrapie. These were: "I need
more knowledge of scrapie symptoms", "Having easy
access to a DVO", "Being offered free examination of
scrapie suspects", and "The Government compensates for
the cost of the control measures when scrapie is detected".
The answers were graded in four levels: not important, of
minor importance, important, and very important. For
the multivariate analysis, each variable was dichotomised
to derive two evenly-sized groups (Table 1).
Statistical analyses
The farmers' reporting of non-recovering listeriosis was
used as a measurement of the farmers' vigilance in report-
ing scrapie. The reporting behaviour of non-recovering lis-
teriosis was analysed in a multinomial logistic regression
with the farmer as the statistical unit and the response var-
iable categorized in the three nominal categories: Notify-
ing, Re-examine and Not report.
The explanatory variables region, flock size, knowledge of
scrapie-associated signs, each of the seven anticipated
concerns of the farmer if scrapie were to be detected in
their flock, and each of the four factors of potential impor-
tance for the reporting of scrapie suspects were considered
as candidates for the multivariate analysis. All candidate
variables were included in the initial model. Maximum
likelihood estimation was used for model fitting, and the
likelihood ratio test was used to assess the overall signifi-
cance of the model. The best model fit was found by using
backward stepwise deletion of insignificant terms. For
each step the single least explanatory variable was
removed until there were no significant difference
between the full and all possible reduced models when
using the likelihood ratio test with significance level of
0.05. Thereafter, all two-way interaction terms between
the remaining explanatory variables were tested one by
one for significance in the final multivariate model.
The adjusted RRR (corresponding to the adjusted Odds
ratio estimated in binomial logistic regression) were used
as measures of association between the response variable
and the explanatory variable [28]. For each explanatory
variable a separate estimate of the RRR was given for the
responses "Notifying" and "Re-examine" relative to the
category "Not report" (reference group). For complete-
ness, the RRR for "Notifying" relative to "Re-examine" was
calculated from the two other contrasts.
All variable processing and statistical analyses were per-
formed in SAS-PC System® for Windows (SAS Institute
Inc., Cary, NC, USA). The descriptive analyses were con-
ducted by using PROC FREQ and missing observations
were included when calculating the population percent-
ages. The multinomial logistic regression was conducted
by using PROC CATMOD.
Authors' contributions
PH were main responsible for the design of the study, col-
lecting the data, performing the statistical analysis and
drafted the manuscript. SV participated in the design of
the study and helped to draft the manuscript. JJ supervised
in the design, the statistical analysis and the writing of the
manuscript. All authors read and approved the final man-
uscript.
Acknowledgements
We would like to thank all the sheep farmers for their active participation
in the study and Hulda Bysheim for accurately entering the data. This study
was supported by the Research Council of Norway project no. 146916/
140.
References
1.European Food Safety Authority: Opinion of the scientific panel
on biological hazards on classification of atypical transmissi-
ble spongiform encephalopathy (TSE) cases in small rumi-
nants. EFSA J 2005, (2005) 276:1-30 [http://www.efsa.europa.eu/
EFSA/Scientific_Opinion/
biohaz_op_ej_276_atypicalscrapiedefinition_en_vf1,1.pdf].
2.
Kongelig resolusjon. 19. mars. In Nor Lovtidend Avd I Volume 89.
Oslo, Det kgl. Statsrådssekretariat; 1965:493-495.
3.Butler D: Doubts over ability to monitor risks of BSE spread
to sheep. Nature 1998, 395:6-7.
4.Foster JD, Parnham D, Chong A, Goldmann W, Hunter N: Clinical
signs, histopathology and genetics of experimental transmis-
sion of BSE and natural scrapie to sheep and goats. Vet Rec
2001, 148:165-171.
5.European Commission: Regulation (EC) No 999/2001 of the
European Parliament and of the Council of 22 May 2001 lay-

Page 9

Publish with BioMed Central and every
scientist can read your work free of charge
"BioMed Central will be the most significant development for
disseminating the results of biomedical research in our lifetime."
Sir Paul Nurse, Cancer Research UK
Your research papers will be:
available free of charge to the entire biomedical community
peer reviewed and published immediately upon acceptance
cited in PubMed and archived on PubMed Central
yours — you keep the copyright
Submit your manuscript here:
http://www.biomedcentral.com/info/publishing_adv.asp
BioMedcentral
BMC Veterinary Research 2007, 3:34 http://www.biomedcentral.com/1746-6148/3/34
Page 9 of 9
(page number not for citation purposes)
ing down rules for the prevention, control and eradication of
certain transmissible spongiform encephalopathies. Off J Eur
Communities 2001, 44(L147):1-40.
Hopp P, Bratberg B, Ulvund MJ: Skrapesjuke hos sau i Norge.
Historikk og epidemiologi. Nor Vet Tidsskr 2000, 112:368-375.
Hagen G, Thorud KE, Hoel K, Støvring M: Skrapesjuke og andre
overførbare spongiforme encefalopatier. Forvaltningsmes-
sige forhold i Norge. Nor Vet Tidsskr 2000, 112:381-385.
Alvseike KR, Melkild I, Thorud K: Scrapie control at the national
level: the Norwegian example. In Prions in humans and animals
Edited by: Hörnlimann B, Riesner D and Kretzschmar H. Berlin, de
Gruyter; 2006:648-653.
Sandvik O: Animal health standards in Norway. A historical perspective and
assessment of the existing situation Edited by: Næss B. Oslo, The Royal
Ministry of Agriculture; 1994:1-108.
Animal Health Authority: Overvåkings- og kontrollprogram
mot skrapesjuke. Oslo, Statens dyrehelsetilsyn; 1997:1-12.
Parry HB: Clinical features of natural scrapie. In Scrapie disease
in sheep. Historical, clinical, epidemiological, pathological and practical
aspects of the natural disease Edited by: Oppenheimer DR. London,
Academic Press; 1983:60-72.
Ulvund MJ: Clinical findings in scrapie. In Prions in humans and ani-
mals Edited by: Hörnlimann B, Riesner D and Kretzschmar H. Berlin,
de Gruyter; 2006:398-407.
Kuchler F, Hamm S: Animal disease incidence and indemnity
eradication programs. Agric Econ 2000, 22:299-308.
Cuenot M, Calavas D, Abrial D, Gasqui P, Cazeau G, Ducrot C: Tem-
poral and spatial patterns of the clinical surveillance of BSE
in France, analysed from January 1991 to May 2002 through
a vigilance index. Vet Res 2003, 34:261-272.
Sandvik T: Progress of control and prevention programs for
bovine viral diarrhea virus in Europe. Vet Clin North Am Food
Anim Pract 2004, 20:151-169.
Schreuder BEC, de Jong MCM, Pekelder JJ, Vellema P, Bröker AJM,
Betcke H: Prevalence and incidence of scrapie in the Nether-
lands: a questionnaire survey. Vet Rec 1993, 133:211-214.
Sivam SK, Baylis M, Gravenor MB, Gubbins S: Descriptive analysis
of the results of an anonymous postal survey of the occur-
rence of scrapie in Great Britain in 2002. Vet Rec 2006,
158:501-506.
Hoinville LJ, Hoek A, Gravenor MB, McLean AR: Descriptive epi-
demiology of scrapie in Great Britain: results of a postal sur-
vey. Vet Rec 2000, 146:455-461.
Valheim M, Hopp P, Alvseike KR, Ruud C, Bratberg B: Overvåking
av skrapesjuke i Norge 1997-2003. Nor Vet Tidsskr 2003,
115:773-781.
Animal Health Authority: Sjukdomsstatistikk 1996. Animal disease report
1996 Oslo, Statens dyrehelsetilsyn; 1996:1-35.
Stuen S, Ulvund MJ, Waldeland H: Sjukdom hos sau. In Saueboka
2nd edition. Edited by: Dahl S and Lystad ML. Oslo, Landbruksfor-
laget; 1998:287-352.
Healy AM, Morgan KL, Hannon D, Collins JD, Weavers E, Doherty
ML: Postal questionnaire survey of scrapie in sheep flocks in
Ireland. Vet Rec 2004, 155:493-494.
Baumgarten L, Heim D, Fatzer R, Zurbriggen A, Doherr MG: Assess-
ment of the Swiss approach to scrapie surveillance. Vet Rec
2002, 151:545-547.
Asch DA, Jedrziewski MK, Christakis NA: Response rates to mail
surveys published in medical journals. J Clin Epidemiol 1997,
50:1129-1136.
Dohoo I, Martin W, Stryhn H: Validity in observational studies.
In Veterinary epidemiologic research Charlottetown, Canada, AVC Inc.;
2003:207-234.
Hopp P, Omer MK, Heier BT: A case-control study of scrapie
Nor98 in Norwegian sheep flocks. J Gen Virol 2006,
87:3729-3736.
Clark MR, Woodward DE: Generating random numbers with
base SAS software. Observations Tech J SAS Software Users 1992,
1(4):12-19.
Dohoo I, Martin W, Stryhn H: Modelling multinomial data. In
Veterinary epidemiologic research Charlottetown, Canada, AVC Inc.;
2003:373-390.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.