Changes in perceptions and motivators that influence the implementation of on-farm Salmonella control measures by pig farmers in England

doi:10.1016/j.prevetmed.2016.09.009

Preventive Veterinary Medicine

Volume 133, 1 October 2016, Pages 22-30

https://doi.org/10.1016/j.prevetmed.2016.09.009 Get rights and content

Highlights

•
Farmers’ perception of implementing Salmonella control on pig farms studied.
•
Successful interventions on a demonstration farm would motivate farmers.
•
Positive attitude, responsibility towards control and support from peers confirmed.
•
Farmers had low confidence in their ability to control Salmonella over time.
•
Farmers trusted their veterinarian as a source of advice for implementing changes.

Abstract

This study presents British farmers’ perception of, and barriers to, implementing Salmonella control on pig farms. Four farms that had implemented interventions and their 33 close contacts (known to the intervention farmers) took part in interviews before (phase 1) and after (phase 2) intervention trials to assess the difference in perception over time. Their results were compared against those from nine randomly selected control farms. The hypothesis was that farms implementing interventions whether or not successful, would influence their close contacts’ opinion over time.

Based on a ‘pathway to disease control’ model, three intrinsic factors known to influence motivation – attitudes, social norms and self-efficacy – were evaluated.

Farmers mentioned that successful interventions on a farm would attract their attention. The use of an appropriate communication strategy is therefore recommended to stimulate farmers’ intent to implement control measures. Both before and after the intervention trials, all farmers had a positive attitude towards Salmonella control and felt that their peers and authorities were supportive of controlling Salmonella on farms. In phase 2, however, farmers were more likely to want to share the burden of control with other stakeholders along the food chain and their belief in self-efficacy had weakened. Whilst social norms were not associated with an intention to take action on control, a positive attitude towards Salmonella control and a belief in self-efficacy were more likely to result in an intent to control. In phase 2, farmers with an intent to implement an intervention appeared to have a greater, but not significant positive belief in self-efficacy (p = 0.108).

This study confirmed that farmers recognised their responsibility for controlling Salmonella in pork – even though their confidence in their ability to control Salmonella decreased over time – and believed that responsibility should be shared with the rest of the production chain. It showed that farmers trusted their veterinarian as a source of advice to guide them during the process of implementing change, though an increase in farms’ Salmonella seroprevalence score (Zoonosis National Control Programme (ZNCP) score) especially for those with a low ZNCP score was also likely to influence their behaviour. Getting concrete feedback from customers or a tangible benefit from their action was a strong incentive especially for farms with a ZNCP score higher than 50%. The study also revealed a need to validate which measures are effective as farmers did not perceive that the current advised interventions were worth the additional effort.

Introduction

In 2006–2007, a European Union (EU) baseline study estimated the prevalence of Salmonella in slaughter pigs sampled in abattoirs (Anon, 2008). In the United Kingdom (UK), lymph nodes of 21.2% of slaughtered pigs were infected with Salmonella (Anon, 2008, Marier et al., 2014). Another EU survey assessed the presence of Salmonella in breeding herds in 2008. The prevalence of Salmonella in the UK breeding pig holdings was the fourth highest of all participating countries (Anon, 2009a). In 2013, a third survey in UK abattoirs confirmed the presence of Salmonella in 30.5% of the caecal content of slaughtered pigs (Powell et al., 2015). Since pig meat products are a potential source of human salmonellosis (Hald et al., 2003), these results highlighted the need to reduce Salmonella prevalence in the UK pig herd.

In 2007, the British Pig Executive (BPEX, now AHDB Pork) commissioned a set of intervention trials, in which individual farmers could propose and apply for funds to support interventions against Salmonella (intervention trial). Farms with successful interventions would be used as demonstration farms to others. Separately, to monitor the seroprevalence of Salmonella, meat juice samples were tested (ELISA) periodically from each batch of pigs sent to the abattoir, as part of the Zoonoses National Control Programme (ZNCP score, 2008–2012, (BPEX, 2012)).

Implementation of Salmonella control on pig farms faces several challenges. Firstly, Salmonella is seldom associated with clinical disease (Alban and Stark, 2005, Wales et al., 2011, Wales and Davies, 2016) or apparent (perceived) production loss in pigs (Andres and Davies, 2015, Loughmiller et al., 2007), therefore control is believed to benefit public health rather than the farmer who has to implement interventions. Secondly, farmers may be unable to assess the effect of additional control efforts that they undertake (Evangelopoulou et al., 2015). Therefore, whilst farmers may accept a moral responsibility (Van Dam et al., 2010), the outcome appears remote from the primary producers’ perspective. Thirdly, the potential exists to mitigate or aggravate contamination risk at other stages along the food chain (Dickson et al., 2013), from abattoir through processing to consumption. Finally, whilst there is convincing evidence that some human cases of salmonellosis are caused by Salmonella strains that are found in pigs (Kirchner et al., 2011), the overall proportion of human salmonellosis that can be attributed to pigs remains uncertain. However, based on a “contribution of food sources to human salmonellosis” study using 2007–2009 data, it was estimated that, 26.9% and 11.7% of cases of human salmonellosis were attributable to pigs in the EU and in the UK respectively (Pires et al., 2011), while a more recent study estimated that 57% of the human salmonellosis cases were attributed to pigs in the EU (Hald et al., 2012).

This paper presents the outcomes of a two-phased study which aimed to use the intervention trials and the ZNCP scores as anchor points to investigate how pig farmers’ intention to control Salmonella changed in response to evidence of the effectiveness of interventions. The authors relied on a behavioural model according to which (i) intrinsic motivators (attitudes, perceived social norms and self-efficacy) affect the intent to take action and (ii) extrinsic circumstances (community and industry, culture and society, knowledge and skills) influence the step from intent to implementation (Ajzen, 1991, Ellis-Iversen et al., 2010). This paper focuses on the intrinsic factors that impeded farmers’ intention to control Salmonella before (phase 1) and after (phase 2) the intervention trials and describes the impact of the ZNCP score on these factors. It draws upon the data collected to identify strategies that may promote an intention amongst pig farmers to control Salmonella in the future.

Section snippets

Study population

Four farmers recruited by BPEX into the intervention trials (Table 1) were invited to participate in this study. For each of them, up to nine close-contact farms (referred to as ‘contact farms’) were enrolled to test whether the intervention farm influenced the uptake of control on the contact farms (Fig. 1). These contact farms were first identified by the intervention farmer as individuals with whom they had regular social or professional contact and at least occasionally discussed pig

Study population

A total of 46 farms were included in the study: four intervention, nine control and 33 contact farms. These were divided into three clusters of eight contact farms and their intervention farm and one cluster of nine contact farms with their intervention farm (Fig. 1).

The herd sizes of the clusters were compared at both visits and none of them varied significantly from the control group (p > 0.05) (Table 3).

The respondents were managers (22 %) and owners (78 %), mostly males (98 %) and over 45

Discussion

Farm characteristics were similar during both phases, indicating that the farms were generally stable over the period covered by this study. There was no significant difference between the geographical clusters and farm types at both visits. Whilst differences between the farms could have affected their answers, the sample size was relatively small and may have been insufficient to detect any modest association. Enrolment to the study was opportunistic and these results cannot be extrapolated

Conclusion

This study showed that the use of demonstration farms may not be farmers’ preferred knowledge transfer tool but could still have a positive effect on farmers if they were accompanied by appropriate communication strategies to disseminate results (including, in particular, positive results). Indeed, many farmers agreed that hearing of a successful intervention on a farm would be a motivation to consider adoption of the intervention themselves.

The study also highlighted that communication was

Acknowledgements

The authors would like to thank the UK Department for Environment, Food and Rural Affairs for funding this study within project OZ0148. Authors would also like to thank the farmers involved for their help and co-operation. Finally, they would like to thank the four contracted interviewers for their assistance with the interviews and Virginie Marier for her proof-reading work.

References (30)

I. Ajzen
The theory of planned behavior
Organ. Behav. Hum. Decis. Process.
(1991)
P. Alarcon et al.
Pig farmers’ perception, attitude, influences and management of information in the decision-making process for disease control
Prev. Vet. Med.
(2014)
L. Alban et al.
Where should the effort be put to reduce the Salmonella prevalence in the slaughtered swine carcass effectively?
Prev. Vet. Med.
(2005)
P.B. Bahnson et al.
Pork producers attitudes, knowledge, and production practices that relate to on-farm food safety
J. Food Prot.
(2001)
J. Ellis-Iversen et al.
Perceptions, circumstances and motivators that influence implementation of zoonotic control programs on cattle farms
Prev. Vet. Med.
(2010)
M. Laanen et al.
Pig, cattle and poultry farmers with a known interest in research have comparable perspectives on disease prevention and on-farm biosecurity
Prev. Vet. Med.
(2014)
E.A. Marier et al.
Abattoir based survey of Salmonella in finishing pigs in the United Kingdom 2006–2007
Prev. Vet. Med.
(2014)
C. Panter-Brick et al.
Culturally compelling strategies for behaviour change: a social ecology model and case study in malaria prevention
Soc. Sci. Med.
(2006)
E.L. Snary et al.
Zoonoses action plan Salmonella monitoring programme: an investigation of the sampling protocol
J. Food Prot.
(2010)
M.V. Andres et al.
Biosecurity measures to control salmonella and other infectious agents in pig farms: a review
Compr. Rev. Food Sci. Food Saf.
(2015)

Anon

Report of the task force on zoonoses data collection on the analysis of the baseline survey on the prevalence of Salmonella in slaughter pigs, part A

EFSA J.

(2008)

Anon

Analysis of the baseline survey on the prevalence of Salmonella in holdings with breeding pigs, in the EU, 2008, part A: Salmonella prevalence estimates

EFSA J.

(2009)

Anon

Is It Worth Vaccinating Against Salmonella? Grower 4

(2009)

BPEX, 2012. Zoonoses National Control Programme (ZNCP). http://www.bpex-zncp.org.uk/zncp11/about/about.eb. (accessed...

COI, 2009, Communication and behaviour change. Government Communication Network....

Cited by (12)

Combining quantitative and qualitative approaches to determine viability of a potential Salmonella Typhimurium vaccination program in pigs in Belgium
2020, Preventive Veterinary Medicine
Citation Excerpt :
The plan should also be accepted by the pig sector. Several studies were conducted over the last 10 years on the general perception by farmers of risk mitigation and on their willingness to implement biosecurity measures in pig farms (Valeeva et al., 2011; Marier et al., 2016). However, none of them focused on the perceived barriers that block the implementation of vaccination programs by the different participants.
Vaccinating pigs against Salmonella Typhimurium (ST) might be a way to control ST infections at farm level and reduce human infections. Two main issues have to be addressed before such a mandatory vaccination program can be implemented: the effective reduction of attributable human incidence has to be demonstrated and all socio-economic barriers impacting the attitude and motivation of the pig sector have to be lifted.
The present research used a quantitative microbial risk assessment model to estimate the effect of different hypothetical Salmonella spp. and ST mitigation strategies on the annual prevalence of human salmonellosis along the minced pork production chain. In addition, a qualitative study aimed to list the potential concerns of the pig sector about the implementation of a hypothetical future vaccination program.
The following themes were the most often mentioned: awareness, vaccine cost-benefit/effectiveness, legislation, monovalent vaccine, time and labour required to vaccinate, vaccine registration and trade restriction. Cost-effectiveness and cost-benefit of vaccination were cited by all the key interviewees (n = 12). However, based on the quantitative microbial risk assessment model, vaccination alone may not be sufficiently effective to reduce the annual human salmonellosis prevalence. A combination of different control measures along the food chain, with a special focus on interventions at the slaughterhouse, might be more effective in achieving the desired goal than vaccination alone.
“They've got to be testing and doing something about it”: Farmer and veterinarian views on drivers for Johne's disease control in dairy herds in England
2020, Preventive Veterinary Medicine
Citation Excerpt :
It is recognised that the stakeholders involved in controlling disease and responding to voluntary and statutory policy initiatives in livestock health have an important influence on the success or otherwise of on-the-ground efforts (Garforth, 2015; Robinson, 2015; Ritter et al., 2017; Fortané, 2020). While research studies have demonstrated that veterinarians are regarded by many farmers as trusted disease control advisers (e.g. Richens et al., 2015; Marier et al., 2016), veterinary advice is not always implemented by farmers, perhaps determined by perceived feasibility or other on-farm priorities (Ritter et al., 2017; Svensson et al., 2019). As noted by Barkema et al., 2018, most Johne’s disease control programmes globally are voluntary, and their success depends ultimately on either the self-motivation of farmers to be involved, or the active encouragement of veterinarians, to promote enrolment and persistence for the long-term.
There needs to be an understanding of the reasons why key stakeholders engage in disease control efforts if disease is to be successfully and sustainably controlled. It is increasingly recognised within veterinary epidemiology and policy making in animal health that these ‘people factors’ are important influences on the success or otherwise of animal disease control programmes. Research methodologies adopted from the social sciences offer ways to understand this important dimension through investigating the attitudes and opinions of the key actors involved. The study reported in this paper, based on qualitative interview research, investigates the views of dairy farmers and cattle veterinarians on the drivers and incentives for controlling Johne’s disease in English dairy herds. Twenty semi-structured interviews involving 17 dairy farmers and seven veterinarians were conducted in two dairy-intensive regions of England. The findings demonstrate the varied influences of veterinary advice and encouragement; appreciation of the economic cost of the disease at herd level; a voluntary national control plan; and fear of a future consumer food scare as the main reasons to engage in Johne’s disease control on dairy farms. The study demonstrates how a combination of a voluntary industry-led control scheme, compulsory participation through retailer and processor contractual requirements, and threats of reputational harm and market loss have strongly influenced farmer and veterinary behaviour in relation to Johne’s control without statutory involvement. The findings illustrate the importance of considering the political economy and societal impact of animal disease.
Antibiotics use versus profitability on sow farms in the Netherlands
2020, Preventive Veterinary Medicine
Citation Excerpt :
Comparable results were found for broiler farmers by De Lauwere and Bokma (2019). Attitude, beliefs and self-efficacy are more often mentioned as drivers to take animal health related measures, for example by Jansen et al. (2010) with regard to mastitis control, Sok et al. (2015, 2016) with regard to a voluntary vaccination programme against Bluetongue, Marier et al. (2016) with regard to Salmonella control and Ritter et al. (2017) with regard to animal disease control programmes. The study showed that decrease in antibiotics use can be quite successful without compromising on the economic or technical performance, and moreover taking into account farmers’ attitudes, perceptions and preferences can be helpful to get a better understanding of farmers’ decision making and is useful for the design of tailor-made interventions.
In 2009, the Dutch government provided policy objectives (i.e., targets) for a reduction in veterinary antibiotics use of −20 % in 2011, −50 % in 2013 and −70 % in 2015 relative to the use in 2009. The relationship between antibiotics use and performance of Dutch sow farms during this policy reform was analysed using the Farm Accountancy Data Network database comprising cross-sectional farm data from 2004 to 2016. The results show that there is a significant downward trend in antibiotics use of 57 %. Panel data analysis (n = 74 sow farms) revealed that the reduction in antibiotic use did not lead to negative effects on technical or economic farm results. A follow-up survey was conducted on measures taken to improve animal health, which made the reduction in antibiotic use feasible. Of the 79 sow farmers approached, 55 participated in this survey. Sow farmers used a variety of relatively easy and affordable measures, such as more attention to hygiene, use of pain killers and anti-inflammatory agents, or applied more preventive vaccinations. Multivariable linear regression models showed that the intention, perceived risk and uncertainty, and perceived capability (to keep or get the use of antibiotics under the target value) were the most important predictors for antibiotics use from 2014 to 2016. Sow farmers who used more antibiotics were more concerned that low antibiotics use compromises their farm results, perceived more risk and uncertainty, and thought to a lesser extent that they have enough knowledge and time. These results indicate that providing these farmers with knowledge and information on management practices to reduce the use of antibiotics may be helpful. Thereby, it would be useful to focus on continuous involvement of the veterinarian and possibly the feed supplier, preferably by means of individual advice, as the results showed that individual advice was the preferred way to gather knowledge for the interviewed sow farmers and the veterinarian appeared to be the most important source of information to the interviewed sow farmers, followed by the feed supplier. In summary, the study shows that decrease in antibiotics use can be quite successful without compromising on the economic or technical performance, and moreover taking into account farmers’ attitudes, perceptions and preferences can be helpful to get a better understanding of farmers’ decision making and is useful for the design of tailor-made interventions.
Controlling hepatitis E virus in the pig production sector: Assessment of the technical and behavioural feasibility of on-farm risk mitigation strategies
2020, Preventive Veterinary Medicine
Citation Excerpt :
The efficacy and the cost-effectiveness of recommended strategies, as well as their feasibility and practicality, are also known to be strong drivers for farmers to adopt recommended disease prevention and control measures (Gunn et al., 2008; Valeeva et al., 2011; Garforth et al., 2013; Alarcon et al., 2014; Toma et al., 2015). Regarding the farmer’s professional environment, several studies have shown that veterinarians and farming advisors play a significant role in spreading information and motivating farmers to adopt best management practices (Alarcon et al., 2014; Laanen et al., 2014; Marier et al., 2016; Mahon et al., 2017; Poizat et al., 2017). However, their own mind-set and opinions, for example on the effectiveness of control and prevention measures, and self-efficacy, in other words their belief in their ability to perform a behaviour and obtain a desired outcome (Bandura, 1977), have only been partially explored so far (Ritter et al., 2017; Hidano et al., 2018).
Hepatitis E virus (HEV) is a zoonotic agent with pigs as the main reservoir in industrialised countries. Recent studies conducted on pig farms, in experimental conditions or through modelling approaches, have led to a better understanding of the spread of HEV on pig farms. The findings have also made it possible to define a set of measures to reduce HEV prevalence and the risk of marketing contaminated products. The objective of this study was to assess the feasibility of a set of HEV control strategies on pig farms. Individual semi-structured interviews were conducted with farmers, veterinarians and farming advisors to collect general data, their level of knowledge of HEV, their opinion on the technical feasibility of certain changes in practices, their perception of the respective responsibilities of the different stakeholders, and their feelings about the importance of the issue, following the framework of the Theory of Planned Behaviour. The interviews made it possible to highlight potential barriers and preferred motivators for the implementation of on-farm risk mitigation strategies. Barriers included lack of knowledge, scientific gaps, perceived inability to control HEV, and low perception of the importance of the issue. Motivators included professional satisfaction, family recognition, and the opportunity to achieve higher quality standards. Three clusters of stakeholders were also identified, with a group of leaders who could help unlock reluctance and disseminate innovations. This type of behavioural approach appeared useful to help risk managers facilitate zoonotic control on pig farms.
Are French pig farmers and veterinarians knowledgeable about emerging foodborne pathogens? The case of hepatitis E virus
2018, Preventive Veterinary Medicine
Citation Excerpt :
Marvin et al. (2010), for example, reported that veterinarians were more familiar with food safety issues than were other professional groups. Moreover, a number of publications noted that farmers considered private veterinarians as the most knowledgeable and trustworthy regarding animal diseases, zoonoses and antimicrobial use (Alarcon et al., 2014; Laanen et al., 2014; Marier et al., 2016; Mahon et al., 2017; Poizat et al., 2017). If sufficiently informed, veterinarians may therefore be an efficient channel through which to pass food safety fundamentals on to farmers.
Hepatitis E virus (HEV) is an emerging zoonotic pathogen mainly transmitted via food in developed countries, and for which domestic pigs are recognised as the main reservoir. To implement an efficient HEV surveillance and control plan in the pig production sector, it is first necessary to assess the level of knowledge of pig-farming main actors about this pathogen. To this aim, an online survey was conducted between September and October 2017 to evaluate pig farmers’ and veterinarians’ knowledge about HEV epidemiology and its zoonotic potential. The questionnaire was filled in by 383 pig farmers and 46 pig veterinarians. Of this population, 77.8% of farmers and 8.7% of veterinarians had never heard of HEV. Our results highlight knowledge gaps among responding farmers, especially regarding the clinical and epidemiological features of HEV, while veterinarians appear to be well-informed about this pathogen. These findings indicate significant room for further improvement and the need for more information aimed at French pig farmers, with veterinarians acting as a priority channel through which information may be transferred from scientists to farmers. These educational efforts will facilitate farmers’ involvement in future HEV surveillance and control plans.
Salmonella Control in Fattening Pigs through the Use of Esterified Formic Acid in Drinking Water Shortly before Slaughter
2023, Animals

View all citing articles on Scopus

¹: Current address: One Epi Consultancy, Weidekampsgade 27, 4. Th, 230, CPH S, Denmark.

²: Current address: National Milk Laboratories, Bellinger Close, Chippenham, Wiltshire, SN15 1BN, United Kingdom.

³: Current address: School of Veterinary Medicine, Faculty of Health & Medical Sciences, University of Surrey, Guildford Surrey, GU2 7TE, United Kingdom.

View full text

Changes in perceptions and motivators that influence the implementation of on-farm Salmonella control measures by pig farmers in England

Highlights

Abstract

Introduction

Section snippets

Study population

Study population

Discussion

Conclusion

Acknowledgements

Organ. Behav. Hum. Decis. Process.

Prev. Vet. Med.

Prev. Vet. Med.

J. Food Prot.

Prev. Vet. Med.

Prev. Vet. Med.

Prev. Vet. Med.

Soc. Sci. Med.

J. Food Prot.

Biosecurity measures to control salmonella and other infectious agents in pig farms: a review

Compr. Rev. Food Sci. Food Saf.

Report of the task force on zoonoses data collection on the analysis of the baseline survey on the prevalence of Salmonella in slaughter pigs, part A

EFSA J.

Analysis of the baseline survey on the prevalence of Salmonella in holdings with breeding pigs, in the EU, 2008, part A: Salmonella prevalence estimates

EFSA J.

Is It Worth Vaccinating Against Salmonella? Grower 4