Coaching Belgian and Dutch Broiler Farmers Aimed at Antimicrobial Stewardship and Disease Prevention
Abstract
:1. Introduction
2. Results
2.1. Evolution of Farm Parameters
2.1.1. ADKAR® Scores
2.1.2. Farm Interventions
2.1.3. Biosecurity
2.1.4. Antimicrobial Use
2.1.5. Technical Performance Parameters
2.2. Associations between Parameters
3. Discussion
4. Materials and Methods
4.1. Study Design
4.2. Farm Selection
4.3. Coaching Methodology
4.4. Data Collection
4.5. Data Analysis
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Chantziaras, I.; Boyen, F.; Callens, B.; Dewulf, J. Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: A report on seven countries. J. Antimicrob. Chemother. 2014, 69, 827–834. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roca, I.; Akova, M.; Baquero, F.; Carlet, J.; Cavaleri, M.; Coenen, S.; Cohen, J.; Findlay, D.; Gyssens, I.; Heure, O.E.; et al. The global threat of antimicrobial resistance: Science for intervention. New Microbes New Infect. 2015, 6, 22–29. [Google Scholar] [CrossRef] [Green Version]
- Dorado-García, A.; Mevius, D.J.; Jacobs, J.J.H.; Van Geijlswijk, I.M.; Mouton, J.W.; Wagenaar, J.A.; Heederik, D.J. Quantitative assessment of antimicrobial resistance in livestock during the course of a nationwide antimicrobial use reduction in the Netherlands. J. Antimicrob. Chemother. 2016, 71, 3607–3619. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Roope, L.S.J.; Smith, R.D.; Pouwels, K.B.; Buchanan, J.; Abel, L.; Eibich, P.; Butler, C.C.; Tan, P.S.; Walker, A.S.; Robotham, J.V.; et al. The challenge of antimicrobial resistance: What economics can contribute. Science 2019, 364, eaau4679. [Google Scholar] [CrossRef] [PubMed]
- FAOSTAT. Available online: http://www.fao.org/faostat/en/#compare (accessed on 9 September 2020).
- Sciensano. Antimicrobial Resistance in Commensal E. coli from Livestock in Belgium: Analysis 2011–2018. 2019. Available online: https://www.favv-afsca.be/professionelen/publicaties/thematisch/verslagamcra/_documents/5_AMRpresentationjune2018-micar_EN.pdf (accessed on 5 January 2021).
- Veldman, K.; Mevius, D.; Wit, B.; Van Pelt, W.; Franz, E.; Heederik, D.J.J. MARAN 2019: Consumption of Antimicrobial Agents and Antimicrobial Resistance among Medically Important Bacteria in the Netherlands. Available online: http://www.rivm.nl/documenten/nethmap-2019 (accessed on 16 September 2020).
- Ceccarelli, D.; Hesp, A.; van der Goot, J.; Joosten, P.; Sarrazin, S.; Wagenaar, J.A.; Dewulf, J.; Mevius, D.J. Antimicrobial resistance prevalence in commensal Escherichia coli from broilers, fattening turkeys, fattening pigs and veal calves in European countries and association with antimicrobial usage at country level. J. Med. Microbiol. 2020, 69, 537–547. [Google Scholar] [CrossRef]
- Muloi, D.; Ward, M.J.; Pedersen, A.B.; Fèvre, E.M.; Woolhouse, M.E.J.; van Bunnik, B.A.D. Are food animals responsible for transfer of antimicrobial-resistant Escherichia coli or their resistance determinants to human populations? A systematic review. Foodborne Pathog. Dis. 2018, 15, 467–474. [Google Scholar] [CrossRef] [Green Version]
- European Food Safety Authority and European Centre for Disease Prevention and Control. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J. 2019, 17. [Google Scholar] [CrossRef]
- Speksnijder, D.C.; Mevius, D.J.; Bruschke, C.J.M.; Wagenaar, J.A. Reduction of veterinary antimicrobial use in the Netherlands. The Dutch success model. Zoonoses Public Health 2015, 62, 79–87. [Google Scholar] [CrossRef]
- World Health Organization. Global Action Plan on Antimicrobial Resistance. Available online: https://www.who.int/antimicrobial-resistance/global-action-plan/en/ (accessed on 13 November 2020).
- European Commission. A European One Health Action Plan against Antimicrobial Resistance (AMR). Available online: https://ec.europa.eu/health/sites/health/files/antimicrobial_resistance/docs/amr_2017_action-plan.pdf (accessed on 13 November 2020).
- AMCRA. Antibioticagebruik op Bedrijfsniveau: Resultaten Sanitel-Med en Ab Register. Adviesraad AMCRA, Brussel, Belgium, 19 June 2019. Available online: https://www.amcra.be/swfiles/files/3_Wannes%20Vanderhaeghen%20-%20AMCRA_NL_289.pdf (accessed on 14 August 2020).
- Sanders, P.; Vanderhaeghen, W.; Fertner, M.; Fuchs, K.; Obritzhauser, W.; Agunos, A.; Carson, C.; Høg, B.B.; Andersen, V.D.; Chauvin, C.; et al. Monitoring of farm-level antimicrobial use to guide stewardship: Overview of existing systems and analysis of key components and processes. Front. Vet. Sci. 2020, 7, 540. [Google Scholar] [CrossRef]
- Visschers, V.H.M.; Backhans, A.; Collineau, L.; Iten, D.; Loesken, S.; Postma, M.; Belloc, C.; Dewulf, J.; Emanuelson, U.; Grosse Beilage, E.; et al. Perceptions of antimicrobial usage, antimicrobial resistance and policy measures to reduce antimicrobial usage in convenient samples of Belgian, French, German, Swedish and Swiss pig farmers. Prev. Vet. Med. 2015, 119, 10–20. [Google Scholar] [CrossRef]
- Visschers, V.H.M.; Postma, M.; Sjölund, M.; Backhans, A.; Collineau, L.; Loesken, S.; Belloc, C.; Dewulf, J.; Emanuelson, U.; Grosse Beilage, E.; et al. Higher perceived risks of antimicrobial use are related to lower usage among pig farmers in four European countries. Vet. Rec. 2016, 179, 490. [Google Scholar] [CrossRef]
- Dewulf, J.; Van Immerseel, F. (Eds.) General principles of biosecurity in animal production and veterinary medicine. In Biosecurity in Animal Production and Veterinary Medicine: From Principles to Practice, 1st ed.; Acco Uitgeverij: Leuven, Belgium, 2018; pp. 64–94. [Google Scholar]
- Aarestrup, F.M. The livestock reservoir for antimicrobial resistance: A personal view on changing patterns of risks, effects of interventions and the way forward. Philos. Trans. R. Soc. B 2015, 370, 20140085. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Laanen, M.; Persoons, D.; Ribbens, S.; de Jong, E.; Callens, B.; Strubbe, M.; Maes, D.; Dewulf, J. Relationship between biosecurity and production/antimicrobial treatment characteristics in pig herds. Vet. J. 2013, 198, 508–512. [Google Scholar] [CrossRef] [PubMed]
- Postma, M.; Backhans, A.; Collineau, L.; Loesken, S.; Sjölund, M.; Belloc, C.; Emanuelson, U.; Grosse Beilage, E.; Okholm Nielsen, E.; Stärk, K.D.C.; et al. Evaluation of the relationship between the biosecurity status, production parameters, herd characteristics and antimicrobial usage in farrow-to-finish pig production in four EU countries. Porc. Health Manag. 2016, 2, 9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Collineau, L.; Rojo-Gimeno, C.; Léger, A.; Backhans, A.; Loesken, S.; Okholm Nielsen, E.; Postma, M.; Emanuelson, U.; Grosse Beilage, E.; Sjölund, M.; et al. Herd-specific interventions to reduce antimicrobial usage in pig production without jeopardising technical and economic performance. Prev. Vet. Med. 2017, 144, 167–178. [Google Scholar] [CrossRef]
- Collineau, L.; Stärk, K.D.C. How to motivate farmers to implement biosecurity measures. In Biosecurity in Animal Production and Veterinary Medicine: From Principles to Practice, 1st ed.; Dewulf, J., Van Immerseel, F., Eds.; Acco Uitgeverij: Leuven, Belgium, 2018; pp. 96–113. [Google Scholar]
- Kristensen, E.; Jakobsen, E.B. Challenging the myth of the irrational dairy farmer; understanding decision-making related to herd health. N. Z. Vet. J. 2011, 59, 1–7. [Google Scholar] [CrossRef]
- Marcdante, K.; Simpson, D. Choosing when to advise, coach, or mentor. J. Grad. Med. Educ. 2018, 10, 227–228. [Google Scholar] [CrossRef] [Green Version]
- Postma, M.; Vanderhaeghen, W.; Sarrazin, S.; Maes, D.; Dewulf, J. Reducing antimicrobial usage in pig production without jeopardizing production parameters. Zoonoses Public Health 2017, 64, 63–74. [Google Scholar] [CrossRef] [PubMed]
- Raasch, S.; Collineau, L.; Postma, M.; Backhans, A.; Sjölund, M.; Belloc, C.; Emanuelson, U.; Grosse Beilage, E.; Stärk, K.; Dewulf, J. Effectiveness of alternative measures to reduce antimicrobial usage in pig production in four European countries. Porc. Health Manag. 2020, 6, 6. [Google Scholar] [CrossRef] [Green Version]
- Houben, M.; Caekebeke, N.; van den Hoogen, A.; Ringenier, M.; Tobias, T.; Jonquiere, F.; Sleeckx, N.; Velkers, F.; Stegeman, J.; Dewulf, J.; et al. The ADKAR® change management model for farmer profiling with regard to antimicrobial stewardship in livestock production. Vlaams Diergeneeskd. Tijdschr. 2020, 89, 309–314. [Google Scholar] [CrossRef]
- Caekebeke, N.; Jonquiere, F.J.; Ringenier, M.; Tobias, T.; Postma, M.; van den Hoogen, A.; Houben, M.A.M.; Velkers, F.C.; Sleeckx, N.; Stegeman, J.A.; et al. Comparing farm biosecurity and antimicrobial use in high antimicrobial consuming broiler and pig farms in the Belgian-Dutch border region. Front. Vet. Sci. 2020, 7, 558455. [Google Scholar] [CrossRef]
- Rojo-Gimeno, C.; Postma, M.; Dewulf, J.; Hogeveen, H.; Lauwers, L.; Wauters, E. Farm-economic analysis of reducing antimicrobial use whilst adopting improved management strategies on farrow-to-finish pig farms. Prev. Vet. Med. 2016, 129, 74–87. [Google Scholar] [CrossRef] [PubMed]
- Hiatt, J. ADKAR: A Model for Change in Business, Government, and Our Community, 1st ed.; Prosci Research: Loveland, CO, USA, 2006. [Google Scholar]
- Anonymous. Deskundigenberaad RIVM en Reductie Antibioticumgebruik. Letters to the Parliament (09-04-2010). VDC 10.117. 2010. Available online: https://rijksoverheid.archiefweb.eu/#archive (accessed on 25 January 2021).
- Ssematimba, A.; Hagenaars, T.J.; de Wit, J.J.; Ruiterkamp, F.; Fabri, T.H.; Stegeman, J.A.; de Jong, M.C.M. Avian Influenza transmission risks: Analysis of biosecurity measures and contact structure in Dutch poultry farming. Prev. Vet. Med. 2013, 109, 106–115. [Google Scholar] [CrossRef] [PubMed]
- Postma, M.; Backhans, A.; Collineau, L.; Loesken, S.; Sjölund, M.; Belloc, C.; Emanuelson, U.; Grosse Beilage, E.; Stärk, K.D.C.; Dewulf, J. The Biosecurity status and its associations with production and management characteristics in farrow-to-finish pig herds. Animal 2015, 10, 478–489. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Laanen, M.; Beek, J.; Ribbens, S.; Vangroenweghe, F.; Maes, D.; Dewulf, J. Bioveiligheid op varkensbedrijven: Ontwikkeling van een online scoresysteem en de resultaten van de eerste 99 deelnemende bedrijven. Vlaams Diergeneeskd. Tijdschr. 2010, 79, 302–306. [Google Scholar]
- Van Limbergen, T.; Dewulf, J.; Klinkenberg, M.; Ducatelle, R.; Gelaude, P.; Méndez, J.; Heinola, K.; Papasolomontos, S.; Szeleszczuk, P.; Maes, D.; et al. Scoring biosecurity in European conventional broiler production. Poult. Sci. 2018, 97, 74–83. [Google Scholar] [CrossRef] [PubMed]
- Shepherd, M.L.; Harris, M.L.; Chung, H.; Himes, E.M. Using the Awareness, Desire, Knowledge, Ability, Reinforcement Model to build a shared governance culture. J. Nurs. Educ. Pract. 2014, 4, 90–104. [Google Scholar] [CrossRef] [Green Version]
- Da Veiga, A. An approach to information security culture change combining ADKAR and the ISCA questionnaire to aid transition to the desired culture. Inf. Comput. Secur. 2018, 26, 584–612. [Google Scholar] [CrossRef]
- Gelaude, P.; Schlepers, M.; Verlinden, M.; Laanen, M.; Dewulf, J. Biocheck.UGent: A quantitative tool to measure biosecurity at broiler farms and the relationship with technical performances and antimicrobial use. Poult. Sci. 2014, 93, 2740–2751. [Google Scholar] [CrossRef]
- Rodrigues da Costa, M.; Gasa, J.; Calderón Díaz, J.A.; Postma, M.; Dewulf, J.; Mccutcheon, G.; Garcia Manzanilla, E. Using the Biocheck.UGent scoring tool in irish farrow-to-finish pig farms: Assessing biosecurity and its relation to productive performance. Porc. Health Manag. 2019, 5, 4. [Google Scholar] [CrossRef] [Green Version]
- Cuc, N.T.K.; Dinh, N.C.; Quyen, N.T.L.; Tuan, H.M. Biosecurity level practices in pig and poultry production in Vietnam. Adv. Anim. Vet. Sci. 2020, 8, 1068–1074. [Google Scholar] [CrossRef]
- Tanquilut, N.C.; Espaldon, M.V.O.; Eslava, D.F.; Ancog, R.C.; Medina, C.D.R.; Paraso, M.G.V.; Domingo, R.D.; Dewulf, J. Quantitative assessment of biosecurity in broiler farms using Biocheck.UGent in Central Luzon, Philippines. Poult. Sci. 2020, 99, 3047–3059. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. Critically Important Antimicrobials for Human Medicine. 6th Revision 2018. Available online: https://apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf?ua=1 (accessed on 26 January 2021).
- European Medicines Agency. Revised ESVAC Reflection Paper on Collecting Data on Consumption of Antimicrobial Agents per Animal Species, on Technical Units of Measurement and Indicators for Reporting Consumption of Antimicrobial agents in Animals. 2013. Available online: https://www.ema.europa.eu/en (accessed on 10 November 2020).
- Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D.; R Core Team. Nlme: Linear and Nonlinear Mixed Effect Models. 2020. Available online: https://CRAN.R-project.org/package=nlme (accessed on 30 September 2020).
Belgium (n = 15) | Period | A | D | K | Ab | R | |
1 | Mean | 2.93 | 3.33 | 3.00 | 2.67 | NA | |
Median | 3.00 | 3.00 | 3.00 | 2.00 | |||
2 | Mean | 3.20 | 3.20 | 3.67 | 3.13 | 2.60 | |
Median | 4.00 | 4.00 | 4.00 | 3.00 | 4.00 | ||
3 | Mean | 3.47 | 3.53 | 3.13 | 3.20 | 3.27 | |
Median | 4.00 | 4.00 | 3.00 | 3.00 | 4.00 | ||
The Netherlands (n = 13) | Period | A | D | K | Ab | R | |
1 | Mean | 4.80 | 4.40 | 2.40 | 4.10 | NA | |
Median | 5.00 | 5.00 | 2.00 | 4.00 | |||
2 | Mean | 4.78 | 4.67 | 2.78 | 4.44 | 4.78 | |
Median | 5.00 | 5.00 | 3.00 | 4.00 | 5.00 | ||
3 | Mean | 4.86 | 4.43 | 3.71 | 4.29 | 4.57 | |
Median | 5.00 | 5.00 | 4.00 | 4.00 | 5.00 |
Category | Improvements | Participating Farms (%) |
---|---|---|
Hygiene | The layout of the hygiene lock, farm-specific clothing and footwear for the catching team, more regular washing of hands, vehicles should always be empty upon arrival | 61 |
Quality of the drinking water | More frequent testing of the drinking water and analysis of the results, thorough cleaning and disinfection of the drinking lines within the houses | 54 |
Management 1-day-old chicks | Always purchasing from the same hatchery, reducing the amount of time between hatching and transportation to the farm, appropriate floor temperature in the houses | 43 |
Infrastructure of the farm | Having dedicated clean and dirty areas on the farm, grids in front of air inlets | 36 |
Treatments | Improvements to vaccination schemes, more prudent use of antimicrobials | 36 |
Follow-up of farm data | Evaluation of past rounds, receiving post-mortem reports from the slaughterhouse | 18 |
Quality of the feed | Improving feed composition, adding less homegrown crops | 7 |
Management of the farm | No partial depopulation, all-in/all-out | 4 |
Period | TI Relative to Median | A | D | K | Ab | |||||
Low | High | Low | High | Low | High | Low | High | |||
Belgium (n = 15) | 1 | < | 4 | 4 | 4 | 4 | 5 | 3 | 6 | 2 |
≥ | 6 | 1 | 4 | 3 | 6 | 1 | 5 | 2 | ||
2 | < | 3 | 5 | 2 | 6 | 2 | 6 | 4 | 4 | |
≥ | 4 | 3 | 3 | 4 | 4 | 3 | 5 | 2 | ||
3 | < | 4 | 4 | 3 | 5 | 4 | 4 | 5 | 3 | |
≥ | 3 | 4 | 4 | 3 | 6 | 1 | 4 | 3 | ||
Period | A | D | K | Ab | ||||||
Low | High | Low | High | Low | High | Low | High | |||
The Netherlands (n = 13) | 1 | < | 0 | 7 | 1 | 6 | 5 | 2 | 0 | 7 |
≥ | 0 | 6 | 1 | 5 | 5 | 1 | 1 | 5 | ||
2 | < | 1 | 6 | 1 | 6 | 5 | 2 | 0 | 7 | |
≥ | 1 | 5 | 2 | 4 | 4 | 2 | 0 | 6 | ||
3 | < | 0 | 6 | 0 | 6 | 0 | 6 | 0 | 6 | |
≥ | 1 | 5 | 1 | 5 | 2 | 4 | 1 | 5 |
Dependent Variable | Independent Variables (Fixed) | Independent (Random) |
---|---|---|
AMU | Awareness, Desire, Knowledge, Ability, external biosecurity, internal biosecurity, mortality, period, country | Farm, period in farm |
Mortality | Awareness, Desire, Knowledge, Ability, external biosecurity, internal biosecurity, AMU, period, country | Farm, period in farm |
FCR | Awareness, Desire, Knowledge, Ability, external biosecurity, internal biosecurity, AMU, period, country, mortality | Farm, period in farm |
External biosecurity | Awareness, Desire, Knowledge, Ability, internal biosecurity, period, country | Farm |
Internal biosecurity | Awareness, Desire, Knowledge, Ability, external biosecurity, period, country | Farm |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Caekebeke, N.; Ringenier, M.; Jonquiere, F.J.; Tobias, T.J.; Postma, M.; van den Hoogen, A.; Houben, M.A.M.; Velkers, F.C.; Sleeckx, N.; Stegeman, A.; et al. Coaching Belgian and Dutch Broiler Farmers Aimed at Antimicrobial Stewardship and Disease Prevention. Antibiotics 2021, 10, 590. https://doi.org/10.3390/antibiotics10050590
Caekebeke N, Ringenier M, Jonquiere FJ, Tobias TJ, Postma M, van den Hoogen A, Houben MAM, Velkers FC, Sleeckx N, Stegeman A, et al. Coaching Belgian and Dutch Broiler Farmers Aimed at Antimicrobial Stewardship and Disease Prevention. Antibiotics. 2021; 10(5):590. https://doi.org/10.3390/antibiotics10050590
Chicago/Turabian StyleCaekebeke, Nele, Moniek Ringenier, Franca J. Jonquiere, Tijs J. Tobias, Merel Postma, Angelique van den Hoogen, Manon A. M. Houben, Francisca C. Velkers, Nathalie Sleeckx, Arjan Stegeman, and et al. 2021. "Coaching Belgian and Dutch Broiler Farmers Aimed at Antimicrobial Stewardship and Disease Prevention" Antibiotics 10, no. 5: 590. https://doi.org/10.3390/antibiotics10050590
APA StyleCaekebeke, N., Ringenier, M., Jonquiere, F. J., Tobias, T. J., Postma, M., van den Hoogen, A., Houben, M. A. M., Velkers, F. C., Sleeckx, N., Stegeman, A., Dewulf, J., & on behalf of the i-4-1-Health Study Group. (2021). Coaching Belgian and Dutch Broiler Farmers Aimed at Antimicrobial Stewardship and Disease Prevention. Antibiotics, 10(5), 590. https://doi.org/10.3390/antibiotics10050590