Can Improved Farm Biosecurity Reduce the Need for Antimicrobials in Food Animals? A Scoping Review
Abstract
:1. Introduction
2. Methodology
2.1. Data Extraction
2.2. Data Analysis
3. Results and Discussion
3.1. Studies Characteristics
Sl. | Country/Groups | Livestock Type | Study Type | Number of Farms Involved | Study Year | Association of Farm Biosecurity Parameters and AMU | Reference |
---|---|---|---|---|---|---|---|
1. | Bangladesh * | Poultry (chicken) farms | Cross-sectional | 768 | 2021 | ‘Chicken morbidity’ and ‘farm location’ were significantly associated with increased AMU. | [28] |
2. | Bangladesh | Poultry (chicken) farms (layer and broiler) | Cross-sectional | 140 | 2019 | ‘Separation of sick from healthy birds’ was significantly associated with reducing AMU. ‘Farms that used shallow water’ were more likely to use antimicrobials. | [26] |
3. | Belgium | Pig farms | Longitudinal with intervention | Raising pigs without antibiotics (RWA) = 16; non-RWA = 12 | 2018–2021 | After farm-specific coaching, for non-RWA farms, there was a reduction in AMU of 61%, 38%, and 23%, for the suckling piglets, fattening pigs, and sows, respectively. | [29] |
4. | Belgium | Pig farms | Longitudinal with intervention | 50 | 2010–2012 | Costs incurred by new biosecurity measures (median +€3.96/sow/year), and new vaccinations (median €0.0/sow/year) didn’t exceed the cost reduction achieved by lowering AMU (median −€7.68/sow/year). | [30] |
5. | Belgium | Pig farms | Longitudinal with intervention | 61 | 2010–2014 | Biosecurity improvement led to a 52% decrease in AMU for pigs from birth to slaughter and a 32% decrease for breeding animals based on treatment incidences (TIs). | [31] |
6. | Belgium | Poultry (broiler) farm | Longitudinal with intervention | 15 | 2012–2013 | Farmers were advised to improve biosecurity after the first audit, and a second audit was conducted within a year to assess changes. Based on the second audit, the average AMU decreased by 29% (from 192 to 136 TIs). | [32] |
7. | Belgium | Pig farms | Cross-sectional | 95 | 2009–2011 | Improved biosecurity scores were associated with lower AMU, as indicated by lower TIs. The ‘disease management’ and ‘farrowing/suckling’ factors were also negatively associated with TIs. | [33] |
8. | European countries (Belgium and The Netherlands) | Poultry (broiler) and pig farms | Cross-sectional | 30 poultry (broiler) and 30 pig farms | 2017–2018 | Dutch farms had better overall biosecurity than Belgian farms. However, Belgian farms had higher AMU in pig weaners, finishers, and broilers compared to Dutch farms. | [22] |
9. | European countries (Germany, France, and Spain) | Turkey farms | Cross-sectional | 60 | 2014–2016 | The study showed unclear links between biosecurity and AMR, but some antimicrobial classes were positively associated with AMU and AMR. | [34] |
10. | European countries (Belgium, France, Germany and Sweden) | Pig farms | Cross-sectional | 227 | 2012–2013 | Better external biosecurity was associated with lower AMU, while ‘shorter farrowing rhythm’ and ‘younger weaning age’ were linked to higher AMU. | [18] |
11. | European countries (Belgium, France, Germany, and Sweden) | Pig farms | Cross-sectional | 227 | 2012–2014 | Compared to ‘regular farms’, the ‘top farms’ with high productivity and low AMU had a higher biosecurity status and fewer gastrointestinal symptoms in sucklers and clinical respiratory symptoms in fatteners. | [35] |
12. | European countries (Belgium, Bulgaria, Denmark, France, Germany, Italy, The Netherlands, Poland and Spain) | Poultry (chicken) farms (broiler) | Cross-sectional | 181 | 2014–2016 | Antimicrobial-resistant genes (ARGs) were positively associated with corresponding AMU. Higher internal biosecurity correlated with more oxazolidinone ARGs, despite not being used in broiler production. Evidence was insufficient to support the hypothesis that biosecurity affects the spread of ARGs. | [36] |
13. | European countries (Belgium, Bulgaria, Denmark, France, Germany, Italy, The Netherlands, Poland, and Spain) | Poultry (chicken) farms (broiler) | Cross-sectional | 181 | 2014 | Farm size, intensity, and having a hygiene lock were associated with lower AMU while obliging visitors to check in, vaccination protocols, and flock depopulation in steps were associated with higher AMU. | [9] |
14. | Finland | Pig farms | Longitudinal | 406 | 2011–2013 | Poor farm management (unhygienic drinking equipment, poor pen condition, poor air quality, poor cleanliness) leads to increased antimicrobial TIs. However, this poor management can also lead to musculoskeletal disorders, tail biting, joint infections, and respiratory diseases associated with high AMU. | [37] |
15. | Germany | Pig farms | Longitudinal | 200 | 2011, 2013, 2014 | Farm size, veterinarian, and farm category impacted TIs, while increased animal movement and pooling of animals from different stables increased the risk of infections and, thus, AMU. | [38] |
16. | Germany | Pig farms | Cross-sectional | 60 | 2012–2014 | Lower external biosecurity scores are associated with more antimicrobial treatments in pigs, particularly for lameness and gastrointestinal diseases in suckling pigs and lameness, respiratory diseases, and skin symptoms in weaned and fattening pigs. | [39] |
17. | Italy | Dairy cattle | Cross-sectional | 34 | 2018–2020 | Farms using replaceable bedding materials had lower AMU. No significant correlation between AMU and biosecurity/animal welfare scores was observed. The authors concluded that management factors have minimal effect on AMU. | [40] |
18. | Italy * | Pig farms | Cross-sectional | 14 | 2016 | Antibiotics were frequently used to treat gastroenteritis in 57% of farms and prophylactic/metaphylactic use in 50%. Vaccination and good management practices were recommended for high- and medium-risk farms. | [41] |
19. | Japan | Pig farms | Cross-sectional | 38 | 2015 | Higher external biosecurity scores and low-density isolated farms were linked to lower oral AMU. In addition, low post-weaning mortality, controlled pig flows, an all-in-all-out system, and good internal biosecurity were associated with lower AMU. | [42] |
20. | Mexico | Poultry (chicken) farms (layers and broilers) | Cross-sectional | 43 | 2017–2018 | Stronger biosecurity measures were linked to lower AMU in a cluster of farms. | [43] |
21. | The Netherlands | Dairy cattle | Longitudinal | 94 | 2005–2012 | Combining veterinarian awareness-raising on herd management and restrictive measures led to a reduction in AMU (−17% in 2012 vs. 2009), resulting in lower veterinary costs per cow. | [44] |
22. | The Netherlands | Dairy cattle | Case-control | 200 (100 high AMU and 100 low AMU) | 2012–2013 | Housing calves on partially slatted floors, high prevalence of respiratory disease, unfavorable Salmonella status, and lack of agreement with specific young stock management were associated with high AMU. | [45] |
23. | Spain | Pig farms | Cross-sectional | 37 | 2017–2018 | High AMU may lead to increased biosecurity, while poor biosecurity may increase the need for antimicrobials. Organic-extensive farms have lower AMU due to less animal density and confinement. | [46] |
24. | Sweden | Pig farms | Cross-sectional | 60 | 2013 | Low internal biosecurity is linked to high TI in weaners, fatteners, and adults, and external biosecurity linked to TI in weaners. | [47] |
25. | Thailand * | Pig farms | Cross-sectional | 114 | 2018 | Small pig farms resisted colistin and fluoroquinolones, while medium-sized farms showed resistance to streptomycin. | [5] |
26. | Vietnam * | Chicken (layer and broiler) and pig farmers | Cross-sectional | 540 each | 2018 | The lack of veterinary services, access to over-the-counter antimicrobials, and insufficient farm biosecurity were linked to high AMU. In addition, educating farmers was found to impact AMU compliance. | [13] |
27. | Vietnam * | Poultry (chicken) farms (layer/broiler/roosters) | Cross-sectional | 125 | 2020 | The farms under the company’s contract (Group A) had good biosecurity measures, infrastructure, and access to veterinarians during health emergencies, reducing AMU in the study region. | [48] |
3.2. Farm Biosecurity (or Management) Factors Affecting Antimicrobial Usage (AMU)
3.3. Interplay between Farm Structure, Management Factors, Biosecurity, and AMU
Biosecurity (or Management) Component | Role in Mitigating the Infection Rate and Curbing AMU |
---|---|
Introduction and movement of livestock | When adding new animals to the herd, proper “quarantine” methods are essential to preventing the spread of any infections. Also, checking animals’ health status before purchase, segregating suspected animals, and maintaining adequate farm fencing is essential to avoid contact with stray and wild animals. Isomura et al. (2018) observed the effect of ‘better site condition’ and the ‘all-in-all-out’ system on the AMU reduction in pig farms [42]. ‘All-in-all-out’ practice interrupts the routes of disease transmission and thereby reduces the incidence of infections in the herd [56]. |
Separation of sick animals | Separating sick animals helps to stop the infection from spreading, which lowers AMU. A study demonstrated that the farms practising separation of sick birds use significantly less antimicrobials as prophylactic [26]. |
Stocking density | High stocking density is considered a social stressor for the livestock, which might result in decreased performance and an increased risk of infectious diseases. For example, chicken farms with high density and inadequate biosecurity were linked to a higher prevalence of diseases and a rise in AMU [28]. Similarly, researchers have linked organic and extensive pig production systems with low AMU, likely attributed to low animal density and reduced risks associated with confinement [46]. |
Colostrum and weaning age | Adequate quantity and quality of colostrum are crucial for the offspring(s) to fight against infections in the early stages of life and post-natal intestinal development [57]. In addition, researchers have observed that early weaning introduces various stress factors that may influence immune function and intestinal microflora [58]. These disturbances might be associated with the risk of enteric disorders such as post-weaning colibacillosis [59]. |
Feed hygiene | The feed can become contaminated during the production cycle with many pathogens and toxins (e.g., Salmonella spp., Escherichia coli, Clostridium spp., Aspergillus spp., and mycotoxins) [33]. Ingestion of contaminated feed may introduce infection in the herd and thereby increase the AMU. |
Transportation | Improper transportation of animals may cause severe stress (especially young ones). The transportation-associated stressful activities include long-distance associated dehydration and fasting periods, handling of animals during loading and unloading, mixing with unfamiliar groups etc. In addition, animals from different farms brought together might cause stress and increase the risk of infections [60]. Contaminated animal transport vehicles can also spread infectious agents [61]. Therefore, vehicle washing, disinfection, and animal welfare-friendly measures are essential during transportation. |
Farm microclimate | Poor farm microclimate was associated with a 20% increase in calf mortality, lowering farm profitability by 60% [62,63]. The livestock performance may be significantly impaired by poor air quality parameters, like the accumulation of dust particles, microorganisms and toxins, ammonia, CO2, etc., in the farm environment. Proper ventilation, thorough cleaning of pens, and a reduction in stocking density can help to ensure good air quality in the farms. Researchers found up to 78.9% of AMU was due to respiratory illnesses in young bulls and veal calves [64]. |
Accessibility to clean water | Contaminated water can act as a vehicle for many pathogens, especially associated with enteric disorders. Therefore, water must be stored in a well-closed reservoir to avoid contamination via dust, wild birds, or rodents. Researchers found that farms with shallow water sources for drinking, cleaning, and washing had higher rates of therapeutic use of antimicrobials than deep tube well water [26]. |
Cleaning and disinfection | Routine cleaning and disinfection of farm equipment, waterers, feeders, loading areas, and farm premises can reduce pathogens’ load, vectors (e.g., flies, ticks and mosquitoes) and pollutants that can impair the immune system of livestock [65,66]. |
Work routine and separate housing | Young and newly born animals are more vulnerable to infections than older animals. These infections can be prevented by providing them with separate housing and following working procedures where newborn/young animals are not visited after contact with older animals on the farm [19]. |
Carcass, effluent, and waste management | It is essential to manage the disposal of farm waste and deceased animals appropriately. As the rendering vehicles have previously been linked to the transmission of infections, the cadaver storage room must be situated outside the farm so that the rendering firm can collect the cadavers without accessing the farm [67]. In addition, the environment and public health must be considered when disposing of carcasses and farm waste. The details on various carcass disposal methods are provided in a review by Gwyther et al. (2011) [68]. |
Farm personnel and visitor hygiene | Farm employees and visitors can spread infectious agents to cattle farms by acting as fomites. Due to their frequent interaction with potentially contaminated sources, the boots, clothing, and hands/gloves are at a high risk of becoming fomites. For example, in a study done on poultry farms in the Netherlands, it was observed that the significant transmission pathways of infections for poultry from an external source were staff’s non-adherence to the hygiene standards and not wearing exclusive working clothing before entering the poultry living area [69]. |
3.4. Constraints for Establishing the Association between Biosecurity (or Management) and AMU
4. Recommendations
- (a)
- Review the role of animal health professionals
- (b)
- Building the farmers’ attitude towards farm biosecurity and judicious AMU
- (c)
- Advocating the adoption of biosecurity quantification tools
- (d)
- Development of monitoring and surveillance system for AMU
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Cook, M.A.; Wright, G.D. The past, present, and future of antibiotics. Sci. Transl. Med. 2022, 14, eabo7793. [Google Scholar] [CrossRef] [PubMed]
- Friedman, M.; Friedland, G.W. Medicine’s 10 Greatest Discoveries; Yale University Press: New Haven, CT, USA, 1998; ISBN 978-0-300-17355-0. [Google Scholar]
- Low, C.X.; Tan, L.T.-H.; Ab Mutalib, N.-S.; Pusparajah, P.; Goh, B.-H.; Chan, K.-G.; Letchumanan, V.; Lee, L.-H. Unveiling the Impact of Antibiotics and Alternative Methods for Animal Husbandry: A Review. Antibiotics 2021, 10, 578. [Google Scholar] [CrossRef] [PubMed]
- Ikhimiukor, O.O.; Odih, E.E.; Donado-Godoy, P.; Okeke, I.N. A bottom-up view of antimicrobial resistance transmission in developing countries. Nat. Microbiol. 2022, 7, 757–765. [Google Scholar] [CrossRef] [PubMed]
- Pires, J.; Huber, L.; Hickman, R.A.; Dellicour, S.; Lunha, K.; Leangapichart, T.; Jiwakanon, J.; Magnusson, U.; Sunde, M.; Järhult, J.D.; et al. Genome-associations of extended-spectrum ß-lactamase producing (ESBL) or AmpC producing E. coli in small and medium pig farms from Khon Kaen province, Thailand. BMC Microbiol. 2022, 22, 253. [Google Scholar] [CrossRef]
- Tang, K.L.; Caffrey, N.P.; Nóbrega, D.B.; Cork, S.C.; Ronksley, P.E.; Barkema, H.W.; Polachek, A.J.; Ganshorn, H.; Sharma, N.; Kellner, J.D.; et al. Restricting the use of antibiotics in food-producing animals and its associations with antibiotic resistance in food-producing animals and human beings: A systematic review and meta-analysis. Lancet Planet. Health 2017, 1, e316–e327. [Google Scholar] [CrossRef]
- Zhang, Q.-Q.; Ying, G.-G.; Pan, C.-G.; Liu, Y.-S.; Zhao, J.-L. Comprehensive Evaluation of Antibiotics Emission and Fate in the River Basins of China: Source Analysis, Multimedia Modeling, and Linkage to Bacterial Resistance. Environ. Sci. Technol. 2015, 49, 6772–6782. [Google Scholar] [CrossRef]
- Ma, F.; Xu, S.; Tang, Z.; Li, Z.; Zhang, L. Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. Biosaf. Health 2021, 3, 32–38. [Google Scholar] [CrossRef]
- Mallioris, P.; Teunis, G.; Lagerweij, G.; Joosten, P.; Dewulf, J.; Wagenaar, J.A.; Stegeman, A.; Mughini-Gras, L. Biosecurity, and antimicrobial use in broiler farms across nine European countries: Towards identifying farm-specific options for reducing antimicrobial usage. Epidemiol. Infect. 2022, 151, e13. [Google Scholar] [CrossRef]
- Ungemach, F.R.; Müller-Bahrdt, D.; Abraham, G. Guidelines for prudent use of antimicrobials and their implications on antibiotic usage in veterinary medicine. Int. J. Med. Microbiol. 2006, 296, 33–38. [Google Scholar] [CrossRef]
- Holmes, A.H.; Moore, L.S.P.; Sundsfjord, A.; Steinbakk, M.; Regmi, S.; Karkey, A.; Guerin, P.J.; Piddock, L.J.V. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 2016, 387, 176–187. [Google Scholar] [CrossRef]
- Lhermie, G.; Gröhn, Y.T.; Raboisson, D. Addressing Antimicrobial Resistance: An Overview of Priority Actions to Prevent Suboptimal Antimicrobial Use in Food-Animal Production. Front. Microbiol. 2017, 7, 2114. [Google Scholar] [CrossRef] [PubMed]
- Luu, Q.H.; Nguyen, T.L.A.; Pham, T.N.; Vo, N.G.; Padungtod, P. Antimicrobial use in household, semi-industrialized, and industrialized pig and poultry farms in Viet Nam. Prev. Vet. Med. 2021, 189, 105292. [Google Scholar] [CrossRef] [PubMed]
- Dutra, M.C.; Moreno, L.Z.; Dias, R.A.; Moreno, A.M. Antimicrobial Use in Brazilian Swine Herds: Assessment of Use and Reduction Examples. Microorganisms 2021, 9, 881. [Google Scholar] [CrossRef]
- Teillant, A.; Brower, C.H.; Laxminarayan, R. Economics of Antibiotic Growth Promoters in Livestock. Annu. Rev. Resour. Econ. 2015, 7, 349–374. [Google Scholar] [CrossRef]
- Joosten, P.; Sarrazin, S.; Van Gompel, L.; Luiken, R.E.C.; Mevius, D.J.; Wagenaar, J.A.; Heederik, D.J.J.; Dewulf, J. EFFORT consortium Quantitative and qualitative analysis of antimicrobial usage at farm and flock level on 181 broiler farms in nine European countries. J. Antimicrob. Chemother. 2019, 74, 798–806. [Google Scholar] [CrossRef] [PubMed]
- Sarrazin, S.; Joosten, P.; Van Gompel, L.; Luiken, R.E.C.; Mevius, D.J.; Wagenaar, J.A.; Heederik, D.J.J.; Dewulf, J. Quantitative and qualitative analysis of antimicrobial usage patterns in 180 selected farrow-to-finish pig farms from nine European countries based on single batch and purchase data. J. Antimicrob. Chemother. 2019, 74, 807–816. [Google Scholar] [CrossRef] [PubMed]
- Postma, M.; Backhans, A.; Collineau, L.; Loesken, S.; Sjölund, M.; Belloc, C.; Emanuelson, U.; Grosse Beilage, E.; Nielsen, E.O.; 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]
- Dewulf, J.; Van Immerseel, F. Biosecurity in Animal Production and Veterinary Medicine; CABI: Wallingford, UK, 2019. [Google Scholar]
- Robertson, I.D. Disease Control, Prevention and On-Farm Biosecurity: The Role of Veterinary Epidemiology. Engineering 2020, 6, 20–25. [Google Scholar] [CrossRef]
- Pritchard, G.; Dennis, I.; Waddilove, J. Biosecurity: Reducing disease risks to pig breeding herds. Practice 2005, 27, 230–237. [Google Scholar] [CrossRef]
- Caekebeke, N.; Jonquiere, F.J.; Ringenier, M.; Tobias, T.J.; 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]
- Albernaz-Gonçalves, R.; Olmos, G.; Hötzel, M.J. Exploring Farmers’ Reasons for Antibiotic Use and Misuse in Pig Farms in Brazil. Antibiotics 2021, 10, 331. [Google Scholar] [CrossRef]
- Higgins, H.M.; Mouncey, J.; Nanjiani, I.; Cook, A.J.C. Understanding how new evidence influences practitioners’ beliefs regarding dry cow therapy: A Bayesian approach using probabilistic elicitation. Prev. Vet. Med. 2017, 139, 115–122. [Google Scholar] [CrossRef] [PubMed]
- Maye, D.; Chan, K.W. (Ray) On-farm biosecurity in livestock production: Farmer behaviour, cultural identities, and practices of care. Emerg. Top. Life Sci. 2020, 4, 521–530. [Google Scholar] [CrossRef] [PubMed]
- Imam, T.; Gibson, J.S.; Gupta, S.D.; Hoque, M.A.; Fournié, G.; Henning, J. Association between farm biosecurity practices and antimicrobial usage on commercial chicken farms in Chattogram, Bangladesh. Prev. Vet. Med. 2021, 196, 105500. [Google Scholar] [CrossRef] [PubMed]
- Tricco, A.C.; Lillie, E.; Zarin, W.; O’Brien, K.K.; Colquhoun, H.; Levac, D.; Moher, D.; Peters, M.D.J.; Horsley, T.; Weeks, L.; et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): Checklist and Explanation. Ann. Intern. Med. 2018, 169, 467–473. [Google Scholar] [CrossRef]
- Chowdhury, S.; Fournié, G.; Blake, D.; Henning, J.; Conway, P.; Hoque, M.A.; Ghosh, S.; Parveen, S.; Biswas, P.K.; Akhtar, Z.; et al. Antibiotic usage practices and its drivers in commercial chicken production in Bangladesh. PLoS ONE 2022, 17, e0276158. [Google Scholar] [CrossRef]
- Bernaerdt, E.; Maes, D.; Van Limbergen, T.; Postma, M.; Dewulf, J. Determining the Characteristics of Farms That Raise Pigs without Antibiotics. Animals 2022, 12, 1224. [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]
- 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]
- 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]
- 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. Lond. Engl. 1997 2013, 198, 508–512. [Google Scholar] [CrossRef] [PubMed]
- Horie, M.; Yang, D.; Joosten, P.; Munk, P.; Wadepohl, K.; Chauvin, C.; Moyano, G.; Skarżyńska, M.; Dewulf, J.; Aarestrup, F.M.; et al. Risk Factors for Antimicrobial Resistance in Turkey Farms: A Cross-Sectional Study in Three European Countries. Antibiot. Basel Switz. 2021, 10, 820. [Google Scholar] [CrossRef]
- Collineau, L.; Backhans, A.; Dewulf, J.; Emanuelson, U.; Grosse Beilage, E.; Lehébel, A.; Loesken, S.; Okholm Nielsen, E.; Postma, M.; Sjölund, M.; et al. Profile of pig farms combining high performance and low antimicrobial usage within four European countries. Vet. Rec. 2017, 181, 657. [Google Scholar] [CrossRef] [PubMed]
- Luiken, R.E.C.; Van Gompel, L.; Munk, P.; Sarrazin, S.; Joosten, P.; Dorado-García, A.; Borup Hansen, R.; Knudsen, B.E.; Bossers, A.; Wagenaar, J.A.; et al. Associations between antimicrobial use and the faecal resistome on broiler farms from nine European countries. J. Antimicrob. Chemother. 2019, 74, 2596–2604. [Google Scholar] [CrossRef] [PubMed]
- Stygar, A.H.; Chantziaras, I.; Toppari, I.; Maes, D.; Niemi, J.K. High biosecurity and welfare standards in fattening pig farms are associated with reduced antimicrobial use. Anim. Int. J. Anim. Biosci. 2020, 14, 2178–2186. [Google Scholar] [CrossRef]
- Hemme, M.; Ruddat, I.; Hartmann, M.; Werner, N.; van Rennings, L.; Käsbohrer, A.; Kreienbrock, L. Antibiotic use on German pig farms—A longitudinal analysis for 2011, 2013 and 2014. PLoS ONE 2018, 13, e0199592. [Google Scholar] [CrossRef]
- Raasch, S.; Postma, M.; Dewulf, J.; Stärk, K.D.C.; Grosse Beilage, E. Association between antimicrobial usage, biosecurity measures as well as farm performance in German farrow-to-finish farms. Porc. Health Manag. 2018, 4, 30. [Google Scholar] [CrossRef]
- Menegon, F.; Capello, K.; Tarakdjian, J.; Pasqualin, D.; Cunial, G.; Andreatta, S.; Dellamaria, D.; Manca, G.; Farina, G.; Di Martino, G. Antibiotic Use in Alpine Dairy Farms and Its Relation to Biosecurity and Animal Welfare. Antibiot. Basel Switz. 2022, 11, 231. [Google Scholar] [CrossRef]
- Scoppetta, F.; Sensi, M.; Franciosini, M.P.; Capuccella, M. Evaluation of antibiotic usage in swine reproduction farms in Umbria region based on the quantitative analysis of antimicrobial consumption. Ital. J. Food Saf. 2017, 6, 6886. [Google Scholar] [CrossRef]
- Isomura, R.; Matsuda, M.; Sugiura, K. An epidemiological analysis of the level of biosecurity and animal welfare on pig farms in Japan and their effect on the use of veterinary antimicrobials. J. Vet. Med. Sci. 2018, 80, 1853–1860. [Google Scholar] [CrossRef]
- Ornelas-Eusebio, E.; García-Espinosa, G.; Laroucau, K.; Zanella, G. Characterization of commercial poultry farms in Mexico: Towards a better understanding of biosecurity practices and antibiotic usage patterns. PLoS ONE 2020, 15, e0242354. [Google Scholar] [CrossRef] [PubMed]
- Kuipers, A.; Koops, W.J.; Wemmenhove, H. Antibiotic use in dairy herds in the Netherlands from 2005 to 2012. J. Dairy Sci. 2016, 99, 1632–1648. [Google Scholar] [CrossRef] [PubMed]
- Holstege, M.M.C.; de Bont-Smolenaars, A.J.G.; Santman-Berends, I.M.G.A.; van der Linde-Witteveen, G.M.; van Schaik, G.; Velthuis, A.G.J.; Lam, T.J.G.M. Factors associated with high antimicrobial use in young calves on Dutch dairy farms: A case-control study. J. Dairy Sci. 2018, 101, 9259–9265. [Google Scholar] [CrossRef] [PubMed]
- Mencía-Ares, O.; Argüello, H.; Puente, H.; Gómez-García, M.; Manzanilla, E.G.; Álvarez-Ordóñez, A.; Carvajal, A.; Rubio, P. Antimicrobial resistance in commensal Escherichia coli and Enterococcus spp. is influenced by production system, antimicrobial use, and biosecurity measures on Spanish pig farms. Porc. Health Manag. 2021, 7, 27. [Google Scholar] [CrossRef]
- Backhans, A.; Sjölund, M.; Lindberg, A.; Emanuelson, U. Antimicrobial use in Swedish farrow-to-finish pig herds is related to farmer characteristics. Porc. Health Manag. 2016, 2, 18. [Google Scholar] [CrossRef]
- Bâtie, C.; Ha, L.T.T.; Loire, E.; Truong, D.B.; Tuan, H.M.; Cuc, N.T.K.; Paul, M.; Goutard, F. Characterisation of chicken farms in Vietnam: A typology of antimicrobial use among different production systems. Prev. Vet. Med. 2022, 208, 105731. [Google Scholar] [CrossRef]
- Mallioris, P.; Dohmen, W.; Luiken, R.E.C.; Wagenaar, J.A.; Stegeman, A.; Mughini-Gras, L. Factors associated with antimicrobial use in pig and veal calf farms in the Netherlands: A multi-method longitudinal data analysis. Prev. Vet. Med. 2022, 199, 105563. [Google Scholar] [CrossRef]
- Bos, M.E.H.; Taverne, F.J.; van Geijlswijk, I.M.; Mouton, J.W.; Mevius, D.J.; Heederik, D.J.J.; on behalf of the Netherlands Veterinary Medicines Authority (SDa). Consumption of Antimicrobials in Pigs, Veal Calves, and Broilers in The Netherlands: Quantitative Results of Nationwide Collection of Data in 2011. PLoS ONE 2013, 8, e77525. [Google Scholar] [CrossRef]
- Gardner, I.A.; Willeberg, P.; Mousing, J. Empirical and theoretical evidence for herd size as a risk factor for swine diseases. Anim. Health Res. Rev. 2002, 3, 43–55. [Google Scholar] [CrossRef]
- Lekagul, A.; Tangcharoensathien, V.; Yeung, S. The use of antimicrobials in global pig production: A systematic review of methods for quantification. Prev. Vet. Med. 2018, 160, 85–98. [Google Scholar] [CrossRef]
- Woolums, A.R.; Berghaus, R.D.; Smith, D.R.; White, B.J.; Engelken, T.J.; Irsik, M.B.; Matlick, D.K.; Jones, A.L.; Ellis, R.W.; Smith, I.J.; et al. Producer survey of herd-level risk factors for nursing beef calf respiratory disease. J. Am. Vet. Med. Assoc. 2013, 243, 538–547. [Google Scholar] [CrossRef]
- Bokma, J.; Dewulf, J.; Deprez, P.; Pardon, B. Risk factors for antimicrobial use in food-producing animals: Disease prevention and socio-economic factors as the main drivers? Vlaams Diergeneeskd. Tijdschr. 2018, 87, 188–200. [Google Scholar] [CrossRef]
- Vieira, A.R.; Pires, S.M.; Houe, H.; Emborg, H.-D. Trends in slaughter pig production and antimicrobial consumption in Danish slaughter pig herds, 2002–2008. Epidemiol. Infect. 2011, 139, 1601–1609. [Google Scholar] [CrossRef] [PubMed]
- Eriksen, E.Ø.; Pedersen, K.S.; Larsen, I.; Nielsen, J.P. Evidence-Based Recommendations for Herd Health Management of Porcine Post-Weaning Diarrhea. Animals 2022, 12, 1737. [Google Scholar] [CrossRef] [PubMed]
- Hammon, H.M.; Liermann, W.; Frieten, D.; Koch, C. Review: Importance of colostrum supply and milk feeding intensity on gastrointestinal and systemic development in calves. Animal 2020, 14, s133–s143. [Google Scholar] [CrossRef] [PubMed]
- Blavi, L.; Solà-Oriol, D.; Llonch, P.; López-Vergé, S.; Martín-Orúe, S.M.; Pérez, J.F. Management and Feeding Strategies in Early Life to Increase Piglet Performance and Welfare around Weaning: A Review. Animals 2021, 11, 302. [Google Scholar] [CrossRef]
- Wellock, I.J.; Fortomaris, P.D.; Houdijk, J.G.M.; Kyriazakis, I. Effects of dietary protein supply, weaning age and experimental enterotoxigenic Escherichia coli infection on newly weaned pigs: Performance. Anim. Int. J. Anim. Biosci. 2008, 2, 825–833. [Google Scholar] [CrossRef]
- Pardon, B.; Catry, B.; Dewulf, J.; Persoons, D.; Hostens, M.; De Bleecker, K.; Deprez, P. Prospective study on quantitative and qualitative antimicrobial and anti-inflammatory drug use in white veal calves. J. Antimicrob. Chemother. 2012, 67, 1027–1038. [Google Scholar] [CrossRef]
- Lowe, J.; Gauger, P.; Harmon, K.; Zhang, J.; Connor, J.; Yeske, P.; Loula, T.; Levis, I.; Dufresne, L.; Main, R. Role of Transportation in Spread of Porcine Epidemic Diarrhea Virus Infection, United States. Emerg. Infect. Dis. 2014, 20, 872–874. [Google Scholar] [CrossRef]
- Gauly, M.; Bollwein, H.; Breves, G.; Brügemann, K.; Dänicke, S.; Daş, G.; Demeler, J.; Hansen, H.; Isselstein, J.; König, S.; et al. Future consequences and challenges for dairy cow production systems arising from climate change in Central Europe—A review. Animal 2013, 7, 843–859. [Google Scholar] [CrossRef]
- Herbut, P. Air movement characteristics inside a cow barn with natural ventilation under no-wind conditions in the winter season. Infrastruktura Ekol. Teren. Wiej. 2010, 11, 159–164. [Google Scholar]
- Fertner, M.; Toft, N.; Martin, H.L.; Boklund, A. A register-based study of the antimicrobial usage in Danish veal calves and young bulls. Prev. Vet. Med. 2016, 131, 41–47. [Google Scholar] [CrossRef] [PubMed]
- De Busser, E.V.; De Zutter, L.; Dewulf, J.; Houf, K.; Maes, D. Salmonella control in live pigs and at slaughter. Vet. J. 2013, 196, 20–27. [Google Scholar] [CrossRef] [PubMed]
- Rasschaert, G.; De Zutter, L.; Herman, L.; Heyndrickx, M. Campylobacter contamination of broilers: The role of transport and slaughterhouse. Int. J. Food Microbiol. 2020, 322, 108564. [Google Scholar] [CrossRef]
- McQuiston, J.H.; Garber, L.P.; Porter-Spalding, B.A.; Hahn, J.W.; Pierson, F.W.; Wainwright, S.H.; Senne, D.A.; Brignole, T.J.; Akey, B.L.; Holt, T.J. Evaluation of risk factors for the spread of low pathogenicity H7N2 avian influenza virus among commercial poultry farms. J. Am. Vet. Med. Assoc. 2005, 226, 767–772. [Google Scholar] [CrossRef]
- Gwyther, C.L.; Williams, A.P.; Golyshin, P.N.; Edwards-Jones, G.; Jones, D.L. The environmental and biosecurity characteristics of livestock carcass disposal methods: A review. Waste Manag. 2011, 31, 767–778. [Google Scholar] [CrossRef]
- 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]
- Rodrigues da Costa, M.; Gasa, J.; Calderón Díaz, J.A.; Postma, M.; Dewulf, J.; McCutcheon, G.; Manzanilla, E.G. Using the Biocheck.UGentTM 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]
- Derks, M.; van de Ven, L.M.A.; van Werven, T.; Kremer, W.D.J.; Hogeveen, H. The perception of veterinary herd health management by Dutch dairy farmers and its current status in the Netherlands: A survey. Prev. Vet. Med. 2012, 104, 207–215. [Google Scholar] [CrossRef]
- Jansen, J.; Steuten, C.D.M.; Renes, R.J.; Aarts, N.; Lam, T.J.G.M. Debunking the myth of the hard-to-reach farmer: Effective communication on udder health. J. Dairy Sci. 2010, 93, 1296–1306. [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 models. Zoonoses Public Health 2015, 62 (Suppl. S1), 79–87. [Google Scholar] [CrossRef] [PubMed]
2a: Biosecurity or Management Factors Related to a Reduction in Antimicrobial Usage (AMU) | ||
Species | Internal (Biosecurity or Management) Factors | External (Biosecurity or Management) Factors |
Pigs |
|
|
Poultry |
|
|
Cattle |
|
|
2b: Biosecurity or Management Factors Related to the Increase in Antimicrobial Usage (AMU) | ||
Species | Internal (Biosecurity or Management) Factors | External (Biosecurity or Management) Factors |
Pigs |
|
|
Poultry |
|
|
Cattle |
|
|
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 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
Dhaka, P.; Chantziaras, I.; Vijay, D.; Bedi, J.S.; Makovska, I.; Biebaut, E.; Dewulf, J. Can Improved Farm Biosecurity Reduce the Need for Antimicrobials in Food Animals? A Scoping Review. Antibiotics 2023, 12, 893. https://doi.org/10.3390/antibiotics12050893
Dhaka P, Chantziaras I, Vijay D, Bedi JS, Makovska I, Biebaut E, Dewulf J. Can Improved Farm Biosecurity Reduce the Need for Antimicrobials in Food Animals? A Scoping Review. Antibiotics. 2023; 12(5):893. https://doi.org/10.3390/antibiotics12050893
Chicago/Turabian StyleDhaka, Pankaj, Ilias Chantziaras, Deepthi Vijay, Jasbir Singh Bedi, Iryna Makovska, Evelien Biebaut, and Jeroen Dewulf. 2023. "Can Improved Farm Biosecurity Reduce the Need for Antimicrobials in Food Animals? A Scoping Review" Antibiotics 12, no. 5: 893. https://doi.org/10.3390/antibiotics12050893
APA StyleDhaka, P., Chantziaras, I., Vijay, D., Bedi, J. S., Makovska, I., Biebaut, E., & Dewulf, J. (2023). Can Improved Farm Biosecurity Reduce the Need for Antimicrobials in Food Animals? A Scoping Review. Antibiotics, 12(5), 893. https://doi.org/10.3390/antibiotics12050893