Introduction

Antibiotics are frequently overused, which is a major driver of antibiotic resistance. Antibiotic use in agriculture is concerning due to the risk of transmission of bacteria containing antibiotic resistance genes (ARGs) to people [1]. Use of antibiotics on dairy farms is a potential risk to human health by increasing the risk of exposure via foodstuffs as well as potentially driving selection of ARGs, although direct evidence is scant [2–5]. However, for ARGs to move from farms into the human population, critical events would have to occur such as contaminated animal products [6] or through direct contact with animals [7] and contaminated environments [8]. In particular, workers on dairy farms are in frequent close contact with cattle and cattle manure and may be at high risk of encountering potentially resistant pathogens [9]. These workers may act as “entry points” for ARGs into the human population with the potential to travel beyond the dairy farm [10]. A wide range of activities and tasks take place on a dairy farm, and all pose varying levels of ARG exposure risk to workers [9, 11]. For example, working with sick animals or handling manure may pose a greater risk for encountering enteric pathogens whereas working in the milking parlor with healthy cows may pose a lower risk. Largely missing from such studies; however, are assessments of dairy workers knowledge about ARG transmission on farms and how this affects risk their risk of carriage and infection as well as the greater community.

Much research to date has focused on farm manager/owner perceptions and knowledge. Several studies have shown US dairy farms to not be concerned with antibiotic overuse leading to the transmission of ARGs and antibiotic resistant bacteria to workers [12]. A study of New York farms found conventional dairy farms had low levels of concern for the effects of on-farm antibiotic use impacting human health and worried more about their cattle’s health with organic farmer being slightly more concerned about the impact of antibiotic use on farms [13]. A study of dairy farmers in Tennessee found only 9.1% of the farmers surveyed were very concerned about antimicrobial resistance with 61.4% mildly concerned, and 22.7% not concerned at all [14]. Farm workers are also important stakeholders who are at risk of acquiring ARGs and contracting infections and who may play important roles in policy decisions. Information gained from discussions with workers may provide insight on what types of education programs or changes to farms may be beneficial to reducing exposure risk.

Focus group designs using semi-structured interviews have previously been used to assess worker knowledge on farms. The Systems Engineering Initiative for Patient Safety (SEIPS) model is a framework allowing for a comprehensive assessment of the work system improving the understanding of structures, process, and outcomes. While SEIPS was originally created for use in healthcare settings, the underlying premise that each task is both impacted by and impacts the work system can be applied to agriculture as well. Similarly to hospital settings, large dairy farms are complex and interconnected systems. Unlike traditional focus group models, SEIPS allows a comprehensive assessment of this dairy farm through investigating the interactions between workers, workers and animals, workers and the environment, as well as workers and the organization (management).

The objective of this cross-sectional study was to develop a better understanding of dairy farm worker perceptions and practices related to bacterial transmission. Without a comprehensive understanding of worker practices, it is not possible to devise and implement effective interventions. The evaluation of beliefs and practices obtained in this study will be helpful in identifying modifiable behaviors that could be targeted in future interventions to reduce ARG exposure risks. We hypothesized that a potential lack of awareness may be a root cause of risky behaviors, policies, or practices (both at the worker and organization levels), which in turn may put workers at risk. We used a human factors and systems engineering framework which allows for a comprehensive assessment of the activities occurring on a farm.

Methods

We conducted focus groups with dairy farm workers to understand the human and system level factors related to ARG transmission involving dairy farm workers on farms and into the greater community. Focus groups were chosen over individual interviews as they allow for the generation of multiple perspectives in an interactive setting [15]. To do this, we adapted the Systems Engineering Initiative for Patient Safety (SEIPS) model [16] for an agricultural setting. SEIPS highlights the interplay between work system elements (organization, environment, tasks, tools/technology) and people. The SEIPS model allows researchers to identify known barriers and facilitators to organizational outcomes which can contribute to the development of well-informed and targeted interventions to reduce exposure and other risk factors. Although SEIPS has been extensively used to examine healthcare work systems [17, 18], to our knowledge, the SEIPS model has not previously been used to examine agricultural work systems nor has it been used to specifically examine dairy operations. Using a systems engineering approach such as SEIPS allows for a comprehensive assessment of the work-system including interactions among workers, between workers and animals, and workers and the environment and equipment. Fig 1 illustrates how the SEIPS model was adapted for use on dairy farms in this study.

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Fig 1. Systems Engineering in Patient Safety (SEIPS) model adapted for use on dairy farms.

Headers represent the original SEIPS categories and bullet points represent how these categories related to dairy operations.

https://doi.org/10.1371/journal.pone.0258290.g001

In this study, we explored daily routine practices, knowledge and experiences among farmworkers–obtaining a snapshot of activities related to antibiotic use on eight farms in Wisconsin selected to represent a range of antibiotic use in cattle. Farmworkers were asked to describe common tasks and work routines including hand hygiene, laundry and eating practices, use of personal protective equipment (PPE) and communication with managers in the context of farm guidelines and policies. The focus group question guide can be found in the supplemental documents (S1 Fig).

Study population and recruitment

As part of a related study, we collected antibiotic use data from 40 large dairy farms in Wisconsin and ranked farms based on daily doses of antibiotics per 1000 cow-days used [19]. From this data, four low use farms and four high use farms were enrolled. High use and low use farms were necessary for a separate aim of the study quantifying ARGs on farms. Fig 2 provides an overview of study enrollment. Eligible farm owners were sent a letter inviting them to participate. When farms agreed to participate, owners were provided with study information posters (in English and Spanish) to be displayed in common areas. Participants were recruited via convenience sampling. The posters alerted workers to the purpose of the research and the times researchers would be visiting the farm. Workers who were interested in participating and available during our visit, were invited to attend the focus group session. When scheduling farm visits, we worked with the farm owners to visit the farms at times when the greatest number of workers involved in all aspects of farm work would be present. Workers provided verbal informed consent and were compensated $25 for participation. All study documents and activities were approved by the University of Wisconsin-Madison Institutional Review Board (application ID: 2017–1333) prior to the start of research.

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Fig 2. Flowchart of study enrollment.

HU = high use farms; LU = Low use farms. *Two separate focus groups were conducted on two of the farms.

https://doi.org/10.1371/journal.pone.0258290.g002

Focus group semi-structured interviews were conducted in both English and Spanish by trained researchers. The focus group question guide was developed by the research team according to the adapted SEIPS model. When possible, a representative sample of workers with a range of duties on the farm (calf care, sick animal care, maternity care, milking, farm maintenance, etc.) were invited to participate in the study. Depending on the size of the farm, workers may have been responsible for multiple types of tasks. Initial groups (n = 3) included both English and Spanish speakers. In subsequent groups (n = 8), English and Spanish speakers were divided to allow for a more fluid discussion. Focus group discussions took place on the farm and farm managers/owners were asked to avoid the area where focus groups were conducted in order to allow workers to speak freely about their work life. The full dataset of the focus group transcriptions can be found in the supplemental documents (S1 File).

Results

We conducted 11 focus groups across the eight farms enrolled into the study between December 2018 and October 2019. Observations of the facilities, equipment, PPE and worker behaviors were conducted on all eight farms prior to focus group interviews. A total of 60 farm workers participated in focus groups with a range of 2–10 workers per farm.

Table 1 lists SEIPS elements and sub-elements identified from the transcripts during the analysis as well as the number of times an element was coded as either a facilitator or a barrier to maintaining a healthy and safe work environment. Overall, facilitators (n = 1041) were identified more often than barriers (n = 307) across the farms. Quotations representative of themes discussed by farm workers from each SEIPS element can be found in Table 2.

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Table 1. Number of barriers and facilitators associated with each SEIPS element.

https://doi.org/10.1371/journal.pone.0258290.t001

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Table 2. Representative quotes associated with each SEIPS element.

https://doi.org/10.1371/journal.pone.0258290.t002

Tasks

The culture around eating (meals and snacks eaten by workers) varied across farms. On some farms workers reported always eating only in the breakroom while on other farms, workers stated they ate wherever was most convenient or while performing their work duties, such as eating in the milking parlor or while driving around on the farm:

“We always eat in there. When I was on day crew, occasionally, they would, when they’re doing the expansions, they would have people in here, and they would be talking. So sometimes we would eat upstairs, or we would go into this room or that room”

While six of the eight (75%) farms provided a clean place for preparing and eating food, the observer noted food wrappers and drink containers in other zones on four (50%) of the farms (Table 3).

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Table 3. Observations of general biosafety practices on the farms.

https://doi.org/10.1371/journal.pone.0258290.t003

Many workers demonstrated an understanding of the importance minimizing the spread of infectious organisms on the farm. Workers told us their farms had policies (either written or verbal) related to working with sick animals.

“They’ve gotten a bit more strict on the sick cattle and on the calving, when a cow is calving. They like it when you, they tell us that we have to keep our boots clean if we deal with a sick cow, and then we go in by a calf, we have to make sure that it is clean, because we don’t want to spread it.”

Tools and technology

Worker perceptions on the tools and technology related to antibiotic use on farms were variable. Use and availability of PPE was inconsistent across farms. While some farms provided coveralls and/or boots for workers to wear, others expected the worker to provide these items themselves. Some workers reported cleaning their boots before getting into personal vehicles or leaving for the day, while others said boot cleaning was not something they often did. Similarly, on some farms it seemed normal for workers to change out of their work clothes before leaving for the day and to wash them on the farm using the farms dedicated laundry equipment, while on other farms workers tended to wear their work clothes home. During the observations, the observer noted workers laundering work clothes on the farm and washing or changing boots before leaving on five (62.5%) of the eight farms.

Many workers felt PPE use was important on the farm. When asked about handwashing practices, one worker stated:

“Yes, every time a calf is born, you have to change all the, if you are milking, you’re using gloves, you have to change. You change the [milk] tank, you have to wash your boots, change gloves, so they’re clean, and change yourself so that, to not contaminate the milk at all. That’s what we do”.

Glove use was supported by observations where we identified 100% of workers using gloves in the milking parlor; most workers identified this practice as mandatory on their farm. On seven (87.5%) of the farms, workers were observed wearing PPE in the calf housing zones. Hand hygiene stations were available and contained appropriate materials (hand sanitizer, soap and water, paper towels or air dryers) in 100% of the bathroom and breakroom facilities in most high-risk areas (calving pen, calf housing). However, only three (37.5%) of the farms had a hand hygiene station in the hospital/isolation pen, another high risk zone, although five (62.5%) provided easily accessible gloves in this zone. Easily accessible gloves were noticeably available in six (75%) milking parlors. Hand hygiene stations were only available in three (37.5%) of milking parlors (Table 4). Workers reported changing gloves most frequently after coming in contact with a sick and/or mastitis cow, eating, drinking, when gloves rip, when changing the line to the milk tank, and after going to the bathroom. Workers also reported they did not think there were necessarily specific rules around hand hygiene, but it was important to use common sense. Boot washing stations (presence of a hose at a minimum) were inconsistently available across farms, and not available in most zones. Calf housing was the exception to this with six (75%) of the farms having some type of boot washing station available near the entry.

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Table 4. Observations of biosafety, personal protective equipment use and availability by farm zone.

https://doi.org/10.1371/journal.pone.0258290.t004

Discussion

We conducted focus groups and observations across eight large farms in Wisconsin to assess farm culture and behaviors potentially relating to ARG spread on farms using a systems engineering approach. Overall, farm owners/managers have successfully implemented several biosecurity protocols associated with mitigating ARG transmission and have implemented a positive culture around worker safety and antibiotic use. A majority of farms had written protocols on antibiotic use and handling that were understood and followed by the workers. Additionally, most farm workers used gloves and PPE in high risk areas such as the milking parlor and calf housing, though workers indicated PPE use was often left to common sense and were not aware of written PPE policies on the farm. The use of the adapted SEIPS model allowed us to identify barriers and facilitators to reducing the spread of ARGs on farms and identified several factors to considered when developing interventions to reduce the spread of ARGs.

Previous research has shown that U.S. dairy farmers are not very concerned about the impact of antibiotic use on the presence of ARGs in humans and in the community [12, 13, 20]. Studies have also documented lack of knowledge/belief among farmers about relationships between antibiotic use in livestock leads to antibiotic resistant infections in humans [12]. Other research has shown that farmers in our study believe they are using the appropriate amount of antibiotics [14, 21] and feel they have a “moral obligation” to use antibiotics in their herds [22]. A recent study of New York dairy farmers found conventional farmers had little concern for the impact of antibiotic use on the larger community and were skeptical of policies to reduce antibiotic use on farms [13]. Additionally, a study of beef cattle producers in Tennessee found producers were not overly concerned with antibiotic use in livestock leading to antibiotic resistance in human populations, but instead believed antibiotic resistance in humans was solely due to human overuse of antibiotics. Furthermore, several producers in the Tennessee study did not believe any risks from livestock to human health were evidence-based and that the public was misinformed [5].

In contrast, the workers in our study seemed to understand the importance of antibiotic stewardship for both animal and human health. Workers in our study also demonstrated a knowledge of how wearing PPE, particularly gloves, was important for reducing transmission of ARGs. The difference in beliefs between our study and the existing literature may be due to who was interviewed. In our study, the focus was on workers while prior research focused on farm managers and owners [12, 13]. Farm manager interest in antibiotic use have been reported to be associated with costs, time, and veterinary guidance [23] with conventional farmers concerned about the negative impact on animal health when reducing antibiotic use [13]. Farm workers likely have different priorities than managers and owners and further research is needed to understand these dynamics. In the study of New York farm managers, the driving forces behind reducing antibiotic use on their farms were financial [13], which was not a concern brought up by the workers in our study. The profitability of the farm as a driver of antibiotic use has been reported previously in both US studies [14] as well as studies in other countries [24, 25].

Workers identified substantially more facilitators to reducing ARGs than barriers. The most commonly identified facilitators were related to communication on the farm. Workers felt they had someone on the farm (herdsman, manager, or owner) they were able to talk to about any issues or needs. Most workers reported a positive culture around the use of PPE and hand hygiene. These feelings were supported by our observations on most farms. However, observations revealed boot washing and hand hygiene stations were not available in all high-risk areas and were frequently lacking in the hospital/ isolation pens. Although worker knowledge of antibiotic resistance and its associated risks was higher than expected and previously reported, workers identified a lack of written protocols as a barrier. As previously noted, communication between workers and management was good and therefore deemed sufficient by most workers. While workers primarily identified laundry practices and access to clean clothing and coveralls as facilitators, our observer noted dirty laundry facilities on several farms. Additionally, the observer noted milk and cow towels being washed with worker clothing on several farms. A recent study by Evanowski et al., 2020 found an intervention involving cow hygiene in the milking parlor (teat-end cleaning) and improved laundering practices (using chlorine bleach, detergent, thorough high heat drying) significantly reduce the number of spore-forming bacteria identified in the raw milk bulk tank, with the largest reductions occurring after education sessions [26]. This indicates interventions improving farm hygiene and laundering practices may help reduce the risk of bacterial transmission on farms. Interventions such as improved laundering procedures and clothing/coveralls provided by the farm and laundered on the farm may be beneficial and are likely feasible.

Interventions to reduce ARG spread need to be seen as both financially feasible and perceived as effective for farmers to be willing to undertake. Further education on antibiotic resistance for both the workers and managers/ owners may be a potentially effective and inexpensive intervention to reduce the spread of ARGs on farms. Workers noted a lack of education from managers/owners on this subject, though workers did have awareness of the importance of reducing resistance. Educational efforts could include signage on ways to reduce the spread of ARGs around the farms, reminders on how and when to perform hand hygiene, and when to change PPE. Furthermore, adding boot wash and hand hygiene stations may be potentially beneficial. While it may not be feasible to ask farms to add these stations where plumbing does not already exist, our observer noted sinks on several farms where no soap and/or disinfectants or towels were available.

Our study has several strengths. To our knowledge this is the first study to our knowledge to apply a systems engineering approach to assess farm workers beliefs and behaviors related to ARG transmission points. The use of the SEIPS model allowed us to identify aspects of the dairy farm’s work systems–such as laundering and proper PPE use–might be able to be intervened upon to reduce ARG carriage and transmission. We complemented the focus group surveys with observations of worker practices on the farm as well as the availability of PPE and hand hygiene on the farms. The methods used here can be applied to future studies addressing a wide variety of farm safety topics. Additionally, these methods can be used to assess future interventions aimed at reducing ARG spread on farms.

Our study also has several limitations. Whenever workers are being observed, there is a risk they may change their behaviors while under observation (Hawthorne effect) [27] which might have led to an overestimation of glove and other PPE use. Similarly, it is possible workers told the interviewer what they thought the interviewer wanted to hear during focus group discussions. To minimize these effects, observations were conducted prior to the group discussions and interviewers were trained to keep a neutral tone during discussions. Another limitation may be the size of the farms in our study–all were large operations with over 250 cows using an electronic records system to document antibiotic use, a requirement for a different aim of the project. It is possible the culture on larger farms is different than on smaller or family-run operations. We also interviewed only workers for this study and not include farm managers. As previous studies have shown, farm managers and owners may have different beliefs and priorities than workers which we were likely not captured in this study. However, farm managers’ and owners’ perceptions will be essential to developing, implementing and sustaining interventions to reduce ARG transmission.

Conclusions

Knowledge and beliefs related to ARG transmission among dairy workers were varied and viewed in a positive light, although worker knowledge was not always accurate. Interventions to reduce ARGs on dairy farms should focus on access to education on how ARGs may spread on a farm and how to reduce spread through hand hygiene practices and PPE use. The mixed methods design used (adapted SEIPS model plus direct observations) was useful in identifying barriers and facilitators relating to ARG transmission and current farm practices and identifying potential systems-level interventions demonstrating its utility in future studies of related issues, such as farm worker safety. Future research exploring worker and manager beliefs around ARGs is needed to better understand the extent to which knowledge and beliefs impacts ARG transmission.

Supporting information