1. Introduction
Antibiotics are one of the most impactful public health-related discoveries of the 20th century
[1][2][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][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][8,9]. Furthermore, using antimicrobials in animal products that are also employed in human medicine can lead to cross-resistance development
[5][10][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][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][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][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][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][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.
2. Farm Biosecurity (or Management) Factors Affecting Antimicrobial Usage (AMU)
The present scoping re
svie
archw 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. 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][27][28][29][30][9,34,36,40,46].
The re
svie
archw 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][31][32][33][18,33,42,49]. Conversely, poor pen conditions, contaminated drinking equipment, poor air quality, and high stocking density have increased AMU
[34][37].
Table 1 (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.
Table 1. Farm biosecurity and management factors were observed to be associated with AMU among various livestock species.
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 |
- ▪
-
All-in and all-out system at all stages
- ▪
-
Complete control of pig flow
- ▪
-
Farms with low stocking density
- ▪
-
Disinfection of the loading area
- ▪
-
Weaning age > 24 days
- ▪
-
High cleaning and disinfection score
- ▪
-
Control of feed, water and equipment supply
- ▪
-
Pen cleanliness
- ▪
-
Well-ventilated farm
- ▪
-
Work line from younger pigs to older ones
- ▪
-
Hygienic drinking equipment
- ▪
-
Anthelmintic therapy
- ▪
-
Vaccination
- ▪
-
Disease management (i.e., use of hospital pens, handling of diseased animals)
- ▪
-
Rapid diagnostic methods
|
- ▪
-
Low chance of having other herds located within a radius of 500 m
- ▪
-
Proper quarantine measures for new animals brought onto the farm
- ▪
-
Organic-extensive farms
- ▪
-
Pest control
|
Poultry |
- ▪
-
Separation of sick from healthy birds
- ▪
-
Stable-specific clothing
- ▪
-
House-specific and recognizable materials and farm clothing
- ▪
-
Cleaning the drinking water system after every production round
- ▪
-
Having proper vaccination protocols
- ▪
-
Use of personal protective equipment
- ▪
-
Low chicken morbidity
- ▪
-
Vermin control program
- ▪
-
Disinfection of stables after every production round
|
- ▪
-
Farmers with large flocks and high experience and education
- ▪
-
Footbath at the entrance
- ▪
-
Farm hygiene lock
- ▪
-
Hygiene protocol before and after entering the farm
- ▪
-
Hand washing before and after entering the farm
- ▪
-
Use of exclusive working clothes by staff and visitors
- ▪
-
Proper mortality disposal strategy
|
Cattle |
- ▪
-
Age-specific management
- ▪
-
Cleaning and disinfection of barn
- ▪
-
Use of replaceable bedding materials (e.g., straw, sawdust etc.)
- ▪
-
Proper udder health management
|
- ▪
-
Avoidance of contact with other herds, such as fencing or avoiding shared grazing areas
- ▪
-
Quarantine measures for new animals brought onto the farm
|
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 |
- ▪
-
Intensive farms with large herds
- ▪
-
Specialized fattening farms
- ▪
-
Shorter farrowing rhythm
- ▪
-
Younger weaning age
- ▪
-
Poor air quality causes respiratory diseases
- ▪
-
Post-weaning mortality risk, lameness, tail biting, gastrointestinal diseases, and skin symptoms in the herd
- ▪
-
Pneumonia and oedema disease in piglets
|
- ▪
-
Increased animal movement and pooling of animals from different stables
|
Poultry |
- ▪
-
The high number of broilers per round
- ▪
-
Flock group treatments among broilers
- ▪
-
High chicken morbidity
- ▪
-
Performing flock depopulation in two or more steps
|
- ▪
-
The high number of farm workers and visitors
- ▪
-
Farms using shallow water as compared to the deep tube well
|
Cattle |
- ▪
-
Low hygiene during milking routines
- ▪
-
Housing calves on partially slatted floors
- ▪
-
Negligence of udder health
- ▪
-
Respiratory and gastrointestinal problems in calves
|
- ▪
-
Presence of vectors and pests in the region
- ▪
-
Advocacy for high AMU to address the prevention of infections during the dry period and treatment of subclinical and clinical mastitis
|
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
[35][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
[30][46]. In addition, high biosecurity farms have been associated with fewer clinical symptoms, lower use of antimicrobials, and better performance
[36][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
[37][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
[29][40].
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
[38][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
[39][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
[40][41][42][43][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
[43][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
[40][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
[41][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%)
[42][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
[29][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
[30][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
[44][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
[44][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.