Pankaj Dhaka,Ilias Chantziaras,Deepthi Vijay,Jasbir Singh Bedi,Iryna Makovska,Evelien Biebaut,Jeroen Dewulf
Can Improved Farm Biosecurity Reduce the Need for Antimicrobials in Food Animals? A Scoping Review
antimicrobial usage,cattle,farm biosecurity,herd health,pigs,poultry
Limited and judicious antimicrobial usage (AMU) is considered the key to saving the success of human and veterinary medicine in treating infections. With the limited alternatives for antimicrobials, farm biosecurity (and herd management) is considered a promising tool to mitigate the non-judicious AMU and to maintain animal health, production, and welfare. The present scoping review aims to analyse the effect of farm biosecurity on AMU in livestock systems and formulate recommendations. Peer-reviewed manuscripts published between 2001–2022 were analyzed using the PRISMA framework using PubMed, Scopus, and Science Direct databases. After applying the inclusion criteria, 27 studies were found to assess the effect of farm biosecurity (or management practices) on AMU at the herd/farm level in quantitative/semi-quantitative terms. These studies were carried out in 16 countries, of which 74.1% (20/27) were from 11 European countries. The highest number of studies were from pig farms [51.8% (14/27)], followed by poultry (chicken) farms [25.9% (7/27)], cattle farms [11.1% (3/27)], and a single study from a turkey farm. Two studies include both pig and poultry farms. Most of the studies were cross-sectional [70.4% (19/27)], seven were longitudinal, and one was a case-control study. Complex interactions were observed among factors influencing AMU, such as biosecurity measures, farm characteristics, farmers’ attitudes, availability of animal health services, stewardship, etc. A positive association between farm biosecurity and reduction in AMU was observed in 51.8% (14/27) of the studies, and 18.5% (5/27) showed that improvement in farm management practices was associated with a reduction in AMU. Two studies highlighted that coaching and awareness among farmers might lead to a decrease in AMU. A single study on economic assessment concluded biosecurity practices as a cost-effective way to reduce AMU. On the other hand, five studies showed an uncertain or spurious association between farm biosecurity and AMU. We recommend the reinforcement of the concept of farm biosecurity, especially in lower- and middle-income countries (LMICs). Further, there is a need to strengthen the evidence on the association between farm biosecurity and AMU in region- and species-specific farm settings.
Can Improved Farm Biosecurity Reduce the Need for Antimicrobials in Food Animals? A Scoping Review

Limited and judicious antimicrobial usage (AMU) is considered the key to saving the success of human and veterinary medicine in treating infections. With the limited alternatives for antimicrobials, farm biosecurity (and herd management) is considered a promising tool to mitigate the non-judicious AMU and to maintain animal health, production, and welfare. The present scoping review aims to analyse the effect of farm biosecurity on AMU in livestock systems and formulate recommendations. Peer-reviewed manuscripts published between 2001–2022 were analyzed using the PRISMA framework using PubMed, Scopus, and Science Direct databases. After applying the inclusion criteria, 27 studies were found to assess the effect of farm biosecurity (or management practices) on AMU at the herd/farm level in quantitative/semi-quantitative terms. These studies were carried out in 16 countries, of which 74.1% (20/27) were from 11 European countries. The highest number of studies were from pig farms [51.8% (14/27)], followed by poultry (chicken) farms [25.9% (7/27)], cattle farms [11.1% (3/27)], and a single study from a turkey farm. Two studies include both pig and poultry farms. Most of the studies were cross-sectional [70.4% (19/27)], seven were longitudinal, and one was a case-control study. Complex interactions were observed among factors influencing AMU, such as biosecurity measures, farm characteristics, farmers’ attitudes, availability of animal health services, stewardship, etc. A positive association between farm biosecurity and reduction in AMU was observed in 51.8% (14/27) of the studies, and 18.5% (5/27) showed that improvement in farm management practices was associated with a reduction in AMU. Two studies highlighted that coaching and awareness among farmers might lead to a decrease in AMU. A single study on economic assessment concluded biosecurity practices as a cost-effective way to reduce AMU. On the other hand, five studies showed an uncertain or spurious association between farm biosecurity and AMU. We recommend the reinforcement of the concept of farm biosecurity, especially in lower- and middle-income countries (LMICs). Further, there is a need to strengthen the evidence on the association between farm biosecurity and AMU in region- and species-specific farm settings.

Antibiotics are one of the most impactful public health-related discoveries of the 20th century [1,2]. Apart from its vital contribution to human health, the application of antimicrobials in the livestock sector played a significant role in upgrading animal health, production, and welfare [3]. Nevertheless, along with noteworthy benefits, indiscriminate antimicrobial usage (AMU) has been the driver for antimicrobial resistance (AMR) selection, which is continuously threatening the global public and animal health systems [4]. Previous studies have proposed a possible link between AMU in animal farming and the emergence of resistant pathogens that can affect the health of both animals and humans [5,6]. In China in 2013, Zhang et al. (2015) observed that after the metabolism of 36 antibiotics with a total usage of 92,700 tons, the total excretion amount was 54,000 tons (84% excreted by animals and 16% by humans), and eventually the emission to the environment was 53,800 tons (46% received by water and 54% to the soil) [7]. High AMU in animal husbandry can lead to resistant organisms and drug residues in animal-derived products [8,9]. Furthermore, using antimicrobials in animal products that are also employed in human medicine can lead to cross-resistance development [5,10]. This underscores the importance of reducing AMU in animal husbandry to alleviate selection pressure on bacteria and safeguard animal and human health [11]. Factors influencing AMU in animal farming are multifaceted and vary from one region to another [12,13]. Although measures have been taken to reduce the non-judicious use of antimicrobials through various policies and guidelines, using these drugs for non-therapeutic purposes, such as growth promotion, prophylaxis, and metaphylaxis, remains prevalent in many regions across the world [14]. The non-therapeutic use of antimicrobials is primarily intended to mask suboptimal farming conditions such as inferior feed, unclean water, improper housing, stressful transportation, poor farm hygienic conditions, and improper vaccination and deworming schedules [15]. Notably, variations in the amount, the timing of administration, and antimicrobial classes used can be observed both within and across livestock-rearing systems [16]. Furthermore, collecting farm-level AMU data is challenging, and results can vary depending on the collection methods and methodologies used [17]. Farm biosecurity is considered a valuable tool to limit the non-judicious use of antimicrobials and promote animal health, production, and welfare [9,18]. It involves measures to prevent the introduction and spread of infectious agents. It includes practices such as restricted movements, animal quarantine and isolation, fencing, transport, cleaning and disinfection protocols, and diagnostic facilities [19]. By implementing farm biosecurity and herd management practices, disease outbreaks and the incidence of infectious diseases among farm animals can be reduced, potentially mitigating the need for antimicrobial treatments and the risk of AMR development [20]. In addition, these measures are cost-effective for preventing infectious diseases in livestock [20,21], although there is limited research on their impact on AMU [22]. Adoption of farm biosecurity practices varies widely among geographic regions, social groups, and livestock production chains, with factors such as farmers’ socio-demographic characteristics and attitudes, farm’s physical and economic constraints, access to information, trust between farmers and animal health authorities, and the belief that biosecurity is primarily a government responsibility influencing farmers’ motivation to invest in biosecurity components [23,24,25]. Despite the practical advantages of farm biosecurity on animal health and welfare, farmers and animal health professionals in resource-limited regions may still be hesitant about its efficacy in substituting or replacing non-judicious AMU practices [18,26]. Therefore, it is crucial to assess herds’ biosecurity levels at regional and national levels and analyze the associations between biosecurity scores, management factors, and AMU to build trust among livestock producers, animal health professionals, and policymakers. This review aims to explore the relationship between antimicrobial usage (AMU) in livestock production and farm biosecurity measures by analyzing the existing literature. Through a thorough examination of available data, this review aims to provide a comprehensive understanding of the potential benefits of farm biosecurity in reducing AMU.

The manuscripts published between 2001–2022 were analyzed for conducting a scoping review as per the procedures established by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement extension for scoping reviews (PRISMA-ScR) (checklist provided as Supplementary Table S1) [27]. The study’s research question was, “Is there an association between farm biosecurity and antimicrobial usage (AMU) in food animals?”. The articles were searched from three electronic databases (PubMed, Scopus, and Science Direct), all through “Title-Abstract-Keywords”. The inclusion criteria were (a) studies published in peer-reviewed journals in the English language; (b) studies published between 2001–2022; and (c) studies which are assessing the effect of farm biosecurity measures (or herd management practices) on antimicrobial usage (AMU) in livestock systems (including poultry). The search was conducted from 16 December 2022 to 2 January 2023, and the search algorithms consisted of various combinations of keywords to enforce the Boolean search strategy. The used keywords and their strings [i.e., (“biosecurity” OR “farm biosecurity” OR “animal biosecurity” OR “preventive veterinary medicine” OR “herd health management”) AND (“antimicrobial resistance” OR “antibiotic resistance” OR “antimicrobial usage” OR “antibiotic usage”) AND (“Livestock” OR “poultry” OR “farm” OR “animal production” OR “cattle” OR “dairy animals” OR “dairy cattle” OR “beef production” OR “beef cattle” OR “buffalo*” OR “pig” OR “swine” OR “goat” OR “sheep” OR “chicken” OR “broiler” OR “layer” OR “turkey” OR “duck”)] were adjusted as per the targeted electronic database (Supplementary Table S2). Only peer-reviewed original research articles were included in the analysis to gather evidence related to the research question. Therefore, literature reviews, editorials, commentaries, and papers published in languages other than English were excluded. Articles that only explored farm biosecurity (or management issues) without mentioning the effect of AMU on livestock or that only mentioned AMU practices without mentioning the status of farm biosecurity (or management practices) were also excluded. Additionally, review articles were explored to identify any additional original research articles not identified through the search algorithm.

An initial screening of the articles was independently carried out by two researchers using the inclusion criteria. Then, the selected articles were moved to Zotero reference management software for full-text analysis. Finally, all authors reviewed the selected manuscripts and revision was made based on the individual’s feedback. After selecting the relevant articles, data were extracted and recorded in a Microsoft Excel worksheet (Microsoft Corp., Santa Rosa, CA, USA). The data include the country where the study was conducted, year and duration of the study, animal species and farm size, study type, data on AMU, data on-farm biosecurity, the association between farm biosecurity and AMU (if any), and study citation.

The data from the studies included in this analysis were examined based on various factors, including geographic location, study type, livestock species, and the relationship between farm biosecurity or management practices and AMU. A hypothetical causal diagram was created to understand better the impact of farm biosecurity or management practices on AMU at the farm/herd level, which outlined direct and indirect pathways involving one or more intervening variables. This analysis formulated recommendations to further reduce non-judicious AMU in livestock systems based on carefully evaluating the included studies.

The initial search hits resulted in extracting 1040 articles from PubMed, Science Direct, and Scopus. After the removal of duplicates and applying the inclusion criteria, a total of 63 articles were selected for full-text review. Out of 63 articles, 27 studies observed the effect of farm biosecurity (or management practices) on AMU at the herd/farm level in quantitative/semi-quantitative terms (Figure 1 and Table 1). The selected studies (n = 27) were carried out among 16 countries across the globe (Figure 2), and most of these studies [74.1% (20/27)] were conducted in European countries (n = 11) (Table 1). In terms of targeted livestock species, the highest number of studies were carried out at pig farms [51.8% (14/27)], followed by poultry (chicken) farms [25.9% (7/27)], cattle farms [11.1% (3/27)], and a single study from a turkey farm. In addition, two studies include both pig and poultry farms. Among the 27 studies, the majority (70.4%, n = 19) were cross-sectional studies or observational surveys. In comparison, seven studies were longitudinal (including four with intervention measures), and one was a case-control study (Table 1).

The present scoping review found a limited number of studies (n = 27) that have investigated the association between farm biosecurity and AMU at the farm or herd level. Out of these, 51.8% (14/27) showed a positive association between the implementation of farm biosecurity and reduction in AMU, while 18.5% (5/27) demonstrated that improved farm management practices were associated with lower AMU. Furthermore, two studies indicated that coaching and awareness among farmers could lead to reduced AMU, while a single economic assessment study concluded that implementing biosecurity practices is a cost-effective strategy for reducing AMU (Table 1). On the other hand, five studies reported an uncertain or spurious association between farm biosecurity and AMU, which could be attributed to confounders such as recent outbreaks, underreporting of AMU, misclassification, or missing information on AMU and/or biosecurity [9,34,36,40,46] (Table 1). The review summarizes the current scientific evidence on the relationship between biosecurity measures and AMU reduction in livestock production. Biosecurity measures such as following an all-in-all out system, high weaning age, use of hygienic locks, proper disease management, use of hospital pens, and compliance with vaccination protocols have been associated with low infection rates and reduced AMU [18,33,42,49]. Conversely, poor pen conditions, contaminated drinking equipment, poor air quality, and high stocking density have increased AMU [37]. Table 2 (2a and 2b) summarizes the critical farm biosecurity and management factors that have been identified as necessary in reduction (2a) and increase (2b) in AMU across different types of livestock. Research examining biosecurity measures in calf management has shown that implementing measures such as cleaning and disinfecting calf housing, using dedicated equipment for each calf, ensuring proper colostrum management, implementing vaccination protocols, and monitoring herd health can help decrease AMU by reducing the occurrence of respiratory and gastrointestinal infections in calves [45]. Higher cleaning and disinfection scores, hygienic feed, water, and equipment supply have also been associated with lower resistance to tested antibiotics, suggesting that such biosecurity interventions support AMR mitigation [46]. In addition, high biosecurity farms have been associated with fewer clinical symptoms, lower use of antimicrobials, and better performance [35]. However, animals that move around more frequently and are mixed with animals from different stables without adequate biosecurity measures are more likely to be exposed to germs, leading to an elevated risk of infection [38]. Animal species-specific production issues may also contribute to AMU. For instance, high milk production has been positively correlated with high AMU due to a higher incidence of mastitis [40]. Table 3 outlines the critical farm biosecurity measures and their role in preventing infections and reducing AMU. In low and middle-income countries (LMICs), raising farmer awareness about the negative effects of untargeted AMU and promoting good farming practices, biosecurity, diagnostic services, and vaccination programs is essential [13]. Studies have shown that proper emphasis on hand hygiene at poultry farms and sensitization about biosecurity management can decrease AMU [43]. Initiatives to better inform farmers and veterinarians on appropriate AMU and farm biosecurity could help reduce AMU on farms [5]. In a study of poultry farms in Belgium, sensitization about biosecurity management with specific advice resulted in a 29% reduction in AMU, as indicated by lower treatment incidences during subsequent audits [32]. The impact of the awareness campaigns (or coaching) and the economic benefits of farm biosecurity interventions in curbing AMU has been assessed in several studies [29,30,31,44]. In a study on Dutch dairy herds, a combination of awareness-raising and restrictive measures was found to reduce antibiotic use by 17% in 2012 compared to 2009 [44]. Another study on raising pigs without antibiotics (RWA) reported that farmers could achieve and maintain RWA status through farm-specific coaching related to prudent AMU and improved biosecurity [29]. A study on pig farms found that implementing new biosecurity measures and vaccinations led to an increase in enterprise profit of +€2.67/finisher pig/year [30]. Also, biosecurity interventions resulted in improved technical results such as the number of weaned piglets/sow/year (+1.1), daily weight gain (+5.9 g/day), and decreased mortality in the finisher period (−0.6%) [31]. These observations provide valuable insights for veterinarians and other stakeholders to encourage livestock farmers to adopt farm biosecurity practices as a cost-effective way to reduce AMU. It is important to note that not all studies have found a straightforward association between farm biosecurity and reduced AMU. For example, a study on dairy cattle in North-eastern Italy found that there may not be a significant effect of management factors or farm biosecurity on AMU, as the levels of AMU in dairy cattle were not as high as in pig farms in the same region [40]. Similarly, a study on pig farms suggested that there may be a reverse causality effect, where high AMU (due to high disease incidences) may lead to an increase in biosecurity standards, and poor biosecurity may be linked to an increased need for antimicrobial treatments. Furthermore, both AMU and biosecurity can be influenced by various factors (e.g., farm size, animal species, geographic location, etc.), which can act as confounders and mask the association between the two [46]. A study on pig farms revealed a significant link between implementing internal and external biosecurity measures and reducing treatment incidences in pigs. However, when the statistical model analysis included farm and farmer characteristics, this association lost its significance, suggesting the presence of other contributing factors [47]. One possible explanation could be that Swedish herds, which have otherwise good pig health, might have experienced a disease outbreak leading to temporarily high AMU [47]. Moreover, the researchers noted that the tool used to evaluate farm biosecurity may not have been appropriate for Swedish conditions. Thus, when analyzing the findings of studies on-farm biosecurity and AMU, it is vital to consider these subtleties and complexities. Overall, the literature results suggest that implementing effective farm biosecurity practices and improving farm management practices can reduce AMU on farms or in herds. However, further research is needed to understand these associations’ mechanisms and determine the most effective strategies for promoting and adopting biosecurity practices among farmers.

Through analyzing the literature, it has been established that besides biosecurity, several other farm management factors influence AMU at the herd or farm level. These factors include farm structure, animal health status, disease prevalence or risk of outbreaks, farmers’ socioeconomic and educational status, farmers’ and animal health professionals’ attitudes towards biosecurity and management practices, and regional or national stewardship policies. To illustrate the relationship between these factors and farm biosecurity and AMU, 12 commonly mentioned factors were selected and analyzed. A hypothetical causal diagram was created to show these factors’ direct or indirect effects on farm biosecurity and AMU (Figure 3). Factors such as biosecurity, vaccination, stewardship, alternatives to antibiotics, and availability of diagnostics can directly affect reducing AMU at the farm level. However, factors such as herd size, farmers’ education, and veterinarians’ attitudes may positively and negatively affect AMU. For example, large herd sizes and livestock species-specific systems can motivate farmers to invest in better management facilities or use antimicrobials for prophylaxis or therapy. Similarly, suppose the farmer is educated more towards infection and treatment perspectives. In that case, there are chances of increased AMU, while education in disease prevention and farm biosecurity would motivate farmers towards decreased use of antimicrobials. The same concept applies to veterinarians’ preferences for therapeutic or preventive aspects. The relationship between farm size and AMU in livestock production remains complex, and evidence on this topic is mixed. Some studies indicate that among bigger and more intensive farms, biosecurity levels are better as compared to smaller farms, and farmers have more awareness about prudent AMU [9,46]. However, large herds also have several risk factors for disease transmission, and farmers may be more concerned about infections in their herds, leading to increased AMU as prophylaxis or metaphylaxis [50,51,52,53]. Studies in poultry production showed that the increase in herd size could positively impact farm biosecurity practices and a reduction in non-therapeutic usage of antimicrobials, possibly due to contract farming or specific technical inputs from animal health professionals [26,48]. Moreover, herd size may be positively correlated with farmers’ economic condition and educational level, leading to large farms adopting biosecurity measures more efficiently due to better access to resources [33,49,54]. On the other hand, small farms may place less emphasis on management and hygiene procedures, necessitating more treatment to reduce illness rates [55]. Therefore, it is essential to consider other factors, such as management practices and production systems, when assessing the relationship between farm size and AMU. A more refined understanding of this relationship is necessary to develop effective strategies for reducing AMU and promoting sustainable livestock production across all farm sizes.

Establishing a causal relationship between biosecurity (or management) factors and AMU requires addressing several methodological constraints. For instance, many studies only report the overall effect of a group of biosecurity practices, which makes it difficult to measure the impact of individual interventions [9,38,46]. Moreover, most of the studies are cross-sectional, which limits the ability to infer causality between risk factors and outcomes. Additionally, selection bias is possible due to the voluntary nature of the participation, which may overestimate the effectiveness of interventions [39]. Further, there is limited research on the association between specific biosecurity measures and AMU, particularly in low- and middle-income countries (LMICs) where the burden of animal diseases is high [9]. The use of biosecurity quantification tools is also limited in LMICs, indicating a need for more comprehensive and standardized data collection methods. To establish a robust association between biosecurity (or management) factors and AMU, well-designed intervention field studies controlling for potential confounders and interactions are necessary [32,70]. We acknowledge the limitations of the present study and agree that the specialized nature of farm biosecurity, which involves region, species, and farm-specific factors, makes it challenging to generalize the concept. The exclusion of non-peer-reviewed or grey literature may have resulted in overlooking relevant local or regional content. Additionally, mainly cross-sectional studies were included, limiting the possibility of assessing temporal trends. Moreover, due to insufficient studies, the impact of individual farm biosecurity parameters on AMU could not be conclusively analyzed, although this was not the primary objective of the current review. Nonetheless, we encourage future researchers to consider conducting a meta-analysis when sufficient studies become available in this field.

Based on the literature analysis, we recommend the following measures to strengthen farm biosecurity and promote judicious AMU. (a) Review the role of animal health professionals Effective biosecurity measures require the involvement of all stakeholders in the production chain. Successfully implementing a farm biosecurity protocol or herd health program requires a comprehensive approach that involves setting goals, planning, executing, and evaluating the program. Animal health professionals possess the necessary expertise to oversee and guide these processes, making their role crucial in promoting and implementing farm biosecurity practices to reduce AMU. Therefore, it is recommended to review and enhance the role of animal health professionals in providing support and guidance for farmers to establish effective farm biosecurity protocols and herd health programs [71,72]. Examples of successful collaborations between government, veterinary organizations, and livestock industry stakeholders in the Netherlands resulted in a 56% reduction in AMU in farm animals during 2007–2012 [73]. Therefore, there is a need to foster collaboration between animal health professionals and farmers to develop effective biosecurity plans tailored to individual farms’ specific needs. This may involve providing support and advice to farmers on the selection and use of antimicrobials and other treatments and assisting with implementing biosecurity measures. (b) Building the farmers’ attitude towards farm biosecurity and judicious AMU To foster a positive attitude towards farm biosecurity, a change in strategy is necessary as farmers often seek biosecurity-related consulting only when they encounter health problems on their farms and desire quick solutions. The fundamentals of farm biosecurity measures should be presented with regular evaluations by veterinarians and animal health professionals to encourage farmers to appreciate their significance. Additionally, communication of the risks associated with antimicrobial use and resistance is crucial. Conducting a cost-benefit analysis to demonstrate the overall benefits of biosecurity interventions over prophylactic use of antimicrobials is also recommended. To overcome the barriers to adopting biosecurity practices, it may be necessary to provide financial incentives or support and tailored information and resources. (c) Advocating the adoption of biosecurity quantification tools Encouraging farmers and veterinarians to use biosecurity quantification tools can aid in identifying and prioritizing biosecurity risks on farms. Training and support for these tools can promote their adoption, and continued research and development can ensure their effectiveness in addressing biosecurity risks associated with antimicrobial use. Collaborative efforts between farmers, veterinarians, and researchers can help to ensure that these tools are relevant and practical for use in different farming systems and contexts. (d) Development of monitoring and surveillance system for AMU The availability of quantitative data on AMU in European countries is due to their well-established monitoring and surveillance systems. The details on these systems can be accessed through the AACTING network, which stands for ‘Network on quantification of veterinary Antimicrobial usage at herd level and Analysis, CommunicaTion and benchmarkING to improve responsible usage’ “weblink: https://aacting.org/about-aacting/ (accessed on 8 March 2023)”. However, most low- and middle-income countries (LMICs) lack centralized recording of AMU in food animals, and data sources are limited to aggregated data of imports or sales. This leads to a lack of detailed information on quantities used in various animal species or locations. Despite minimal regulation of antimicrobials in small-scale production systems in LMICs, research on AMU in these systems remains limited. Further, to effectively monitor and compare AMU, standardized definitions and calculation methods are necessary, and data transfer should be streamlined. Therefore, there is a need for increased efforts to fill these gaps and improve data availability and comparability across countries.

The review has provided valuable insights into the link between farm biosecurity and AMU, and it confirms that biosecurity plays a vital role in the effort to reduce AMU. The study findings suggest a lack of emphasis on quantifying farm biosecurity and herd health management practices. Most studies conducted in European regions focused on piggeries and poultry farms, indicating a knowledge gap in LMICs. Most studies were cross-sectional, highlighting the need for longitudinal studies to establish strong evidence on the targeted associations. The limited application of region- and species-specific quantitative biosecurity scoring systems and AMU monitoring systems outside of Europe suggest applying tools for categorising farm biosecurity and benchmarking antimicrobial consumption to formulate an evidence-based sustainable plan for judicious AMU. Further research is necessary to understand the interrelatedness of biosecurity parameters and their impact on herd health, farm production, and AMU. LMIC stakeholders and policymakers need to be made aware of the benefits of adopting farm biosecurity, and field-level studies can be conducted to establish this. Finally, additional research is required to develop evidence-based guidelines for farmers to promote optimal farm biosecurity practices and antimicrobial usage.