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

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 Norwegian Government has considered scrapie a serious animal 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 encephalopathy (BSE) from concentrated feeds contaminated with the BSE agent [3], and BSE and scrapie cannot be differentiated 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 programme in 1997. The programme comprises an information campaign aimed at Norwegian sheep farmers, a surveillance programme, control measures in the flocks where scrapie-positive animals have been detected (hereafter 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 control measures at the flock level included extensive sanitation 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 subject 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 movement of animals. Until 2004, the control measures applied were equal regardless of whether classical or atypical scrapie was diagnosed. Thereafter, partial depopulation 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 surpasses 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 surveillance only. In 1997 an active surveillance programme of slaughtered animals was introduced, and in 2002 surveillance of slaughtered animals and fallen stock was implemented 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 thereafter 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 disease [14].

Acknowledging the importance of the farmers for the performance of the scrapie surveillance programmes, a questionnaire 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 animals 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.

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 indicate 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 important that the detection of scrapie would enable the eradication of the disease from the flock, indicating that the individual farmer takes responsibility for the sheep industry. The active involvement of the farmers' organisations has been important for the implementation of national disease control programmes – for example the programme 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 Government taking the economic responsibility for the control 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 common funds or other insurance systems. In Norway, a standardised compensation per animal destroyed is offered, and the sanitary measures applied are fully covered by the Government. In addition, production subsidies 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 situation. 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 listeriosis 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 "Notifying" 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-associated 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 identified 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 undermine 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 compensation as well as considering the farmers' non-economic 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 neurological disorders should be regarded as scrapie suspects. Consequently 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 suspicious 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 considered an indirect measure for the farmers' vigilance. Nevertheless, 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 concerning 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 situation 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 anonymous 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 farmers' anticipated reactions if scrapie was detected in their flock, which could indicate a non-response bias. We received no indications that these questions were controversial for the farmer, but the farmer might have considered 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 transmissibility of the disease [26]. The farmers' motivation to report scrapie might therefore have been reduced and hence lead to reduced reporting of scrapie.

The farmers' vigilance is essential for the detection of classical scrapie as, despite the extensive surveillance programmes, 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 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. Consequently, it will be important to continue to motivate the farmers to report, to improve their awareness of scrapie, and to communicate 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 serious infectious diseases, the farmers' concerns of non-economic as well as economic values should be considered.