Antibiotic use in livestock production

Certain bacteria not only cause illness in humans but also in livestock animals (poultry, swine, cattle) commonly raised for food. Thus, agriculture has also benefited by the discovery of antibiotics, gaining an important tool to treat bacterial infections. For example, antibiotics are commonly used to treat mastitis in lactating cows and respiratory disease in calves [5]. Today, antibiotics are used not only to treat individual animals, but also to control herd or flock disease outbreaks and to prevent disease by administration through food or water.

A more controversial use of antibiotics quickly developed in the 1940s when the poultry industry discovered that the use of tetracycline increased the rate of weight gain [6]. Although the reasons for this increased weight gain were (and remain) poorly understood, this practice quickly spread throughout the livestock sector. In the 1950s, the accelerated use of antibiotics in livestock production was concurrent with the rise of intensive feeding operations [7]. High animal densities facilitated the spread of infectious pathogens which antibiotics prophylactically countered.

In the US, farmers have been able to buy most antibiotics “over the counter,” or without a prescription from a medical professional, a practice not permitted with respect to human health. In addition, until recently US farmers have been able to purchase antibiotics for “growth promotion” or “prophylactically” without veterinarian oversight. In contrast, the European Union has banned the use of antibiotics in agriculture as growth promoters since January 1, 2006 [8]. The World Health Organization (WHO) has recommended that agriculture cease using antibiotics in livestock for either growth or disease prevention [9].

Much variation exists in animal husbandry practices among US food animal sectors. The cattle industry was responsible for 43% of the MIAs consumed by US livestock in 2016—the first year of mandatory reporting by animal species—compared to 6% for the chicken industry [10]. In contrast to the beef industry, the chicken industry has responded more quickly to consumer demand to offer more NAE or “No Antibiotics Ever” product lines. Chicken sold as NAE increased from 4% in 2013 to 13% in 2015 to over 50% in 2018 [11]. Interestingly, turkey operations, which comprise far less biomass production than chickens, account for roughly 10% of antibiotic consumption by livestock in years 2016–18 [10].

In order to assist the FDA in its analysis of agricultural antibiotic use and safety concerns, US animal drug sponsors have been required, since 2009, to report their sales of antibiotics to the FDA. Likewise, the FDA is required by law to publish a summary report by December 31 of the following year. Beginning in 2016, drug sponsors have also been required to report antibiotic distribution by animal species (i.e. cattle, swine, chicken, turkey). In the first three years of mandatory reporting, antibiotics sold for livestock consumption steadily increased, with the total amount of antibiotics sold in 2012 showing a 23% increase from the 2009 levels [10].

During this period, only two tools existed to regulate how antibiotics were being used by the food-animal sector, namely prescriptions (typically for administration through water) and a veterinary feed directive (VFD), that is, a written order from a veterinarian to administer antibiotics through feed [12]. The latter was rarely used, however, because most antibiotics were available over the counter.

In 2012, the FDA issued GFI (Guide for Industry) #209 entitled, The Judicious Use of Medically Important Antimicrobial Drugs in Food-Producing Animals, in which it outlined its concerns that antibiotics were losing their effectiveness against bacterial infections due to injudicious practices in both human and food-producing animal populations [13]. It also stated its thinking that using antibiotics for “production” or “feed efficiency” purposes were injudicious and expressed concerns over resistant bacteria being transmitted to humans. A year and a half later, the agency issued GFI #213 which established a timeline to implement the goals of GFI #209 and requested voluntary compliance by pharmaceutical companies and livestock producers [4]. A key part of GFI #213 was a revision of the veterinary feed directive (VFD) rules, which had been described as overly “burdensome” by producers [12]. The FDA published the VFD final rule in 2015, setting the stage for full implementation of these policies [12].

On January 1, 2017, full enforcement of GFI #213 began, which mandated new restrictions on the use of antibiotics in livestock operations. Most medically important antibiotics (MIA) intended for use in feed or water were no longer permitted to be sold “over the counter” but required oversight by a licensed veterinarian who had an established professional relationship with the client (farmer), known as the VCPR (Veterinarian Client Patient Relationship). Under GFI #213, most antibiotics administered through water required a prescription. Farm operators wishing to mix antibiotics into livestock feed–the most common route of administration–were required to obtain a written Veterinary Feed Directive (VFD). The use of antibiotics prophylactically (as preventative) was still permitted; however, the rule made the practice of using antibiotics for purposes of growth, “production”, and/or “feed efficiency” illegal.

GFI #213 and production concerns

Traditionally US meat-producers have opposed a ban on the use of antibiotics as growth promoters, arguing that animal health would suffer, meat production would decrease, and the industry would suffer economic harm [14]. These concerns were visible in the public debates over the GFI #213, where producer advocacy groups, such as the America Farm Bureau Federation, argued that restricting access to antibiotics posed a risk to animal health and the ability to produce safe product [15].

Meanwhile, evidence from the European Union (EU) suggested that these concerns may be overstated. Denmark was one of the first EU countries to limit such antibiotic use in the 1990s followed by a complete ban on antibiotics as growth promoters in 2000. Since the ban, poultry production has increased slightly while pork production has significantly increased [16]. These production changes corresponded with reductions of antibiotic use by 90% and 51%, in poultry and pork husbandry respectively [17].

Few studies exist that examine the preliminary ground-level impact of the VFD in the U.S. on livestock operations. After the first draft of the rule was proposed, Lee et al. (2017) surveyed beef producers across the US and found that over 80% of producers were familiar with the rule and expressed a mix of positive (27%), negative (41%), or mixed/indifferent (33%) opinions about its impacts [18]. Ekakoro, Caldwell, Strand, and Okafor investigated the impact of the VFD on Tennessee cattle producers during its first year of implementation. They conducted focus groups and distributed a survey to a large sample of beef and dairy producers in Tennessee to gather information about the impacts of the rule on their operations. They found that many producers had a negative perception of the rule, including perceptions that VFD was a top-down policy, limited their options to address animal health problems, and would likely cause economic losses (particularly for small producers) [19]. Roughly 40% of their respondents believed that VFD would lead to increased use of injectable antibiotics, perhaps compensating for some of the reductions in fed antibiotics [19]. That said, most respondents saw merit in the rule; for example, a majority of beef producers (55%) agreed that the VFD was somewhat or very useful. A significant minority of both beef and dairy operators also reported increasing their interactions with veterinarians as a result of the VFD [19].

In a separate paper, Ekakoro et al. reported that use of antibiotics in general varied by type of cattle operation (beef or dairy; size) and was influenced by both market pressures and interactions with veterinarians [20]. They documented an increase since the late 2000s in the proportion of producers keeping records on antibiotic use and a reduction in the off-label use of antibiotics; however, they did not link this to GFI #213 or the VFD [20].

Rademacher, Pudenz, and Schultz surveyed swine veterinarians before and after the first year of VFD implementation [21]. They found that because of the VFD, veterinarians were having more conversations with their swine producer clients regarding the judicious use of antibiotics [21]. The most commonly reported changes in operation management practices included increased vaccinations (81%), increased nutritional feed additives or supplements (57%), and modified biosecurity (49%) [21]. The veterinarians also reported the perception that antibiotic use by their clients had substantially decreased [21]. FDA Summary Reports published since confirm their perceptions [10].

Ohio as a representative agricultural state

Ohio is a major agricultural state with a diverse livestock sector and serves as an interesting place to investigate the impacts on and responses by livestock producers to GFI #213. According to the 2017 USDA Census, Ohio is home to over 25,000 farms that raise cattle, over 10,000 farms who raise poultry, and roughly 3,500 farms that raise swine [22]. Swine and poultry production in Ohio are highly integrated, meaning that the majority of the animals are owned by an “integrator,” a company that contracts farmers to raise the livestock animals in accordance with strict company mandated protocols. Access to these operations can be difficult due to biosecurity concerns. In contrast, the Ohio beef and dairy farms tend to be individually operated and thus are more diverse in their management practices. With its diverse farm management styles and scales of operation, Ohio cattle industry provides an excellent opportunity to explore stakeholder perspectives of the VFD and its impact on a local level.

The goal of GFI #213 was to promote judicious use of antibiotics in the livestock sector, however, a mandate is meaningless if it is too difficult or cumbersome to implement. In keeping with the “One Health” approach [23], our research sought multiple perspectives and had two foci. The first objective of this study was to explore the perceptions of Ohio cattle farmers (both beef and dairy) and Ohio large animal veterinarians regarding the VFD and its impact. Our second objective was to test the conventional hypothesis that the mandated restrictions on antibiotic use would negatively affect production. To our knowledge, this is the first study to explore the perceptions of the VFD by primary stakeholders in Ohio livestock production.

Sampling and recruitment

To assess the farm level impacts of the VFD, we conducted interviews with Ohio cattle producers (both beef and dairy) and veterinarians. The interviews were conducted in two phases. The first was in conjunction with a study by researchers from The Ohio State University (OSU), Assessing the Role of Cattle Production Systems and Landscape Characteristics in Antimicrobial Resistance Profiles using a Participatory Epidemiology Approach (R. Garabed PI). The team was conducting interviews with representative dairy and beef producers as part of a broader study of antibiotic management and the ways that landscape and producer diversity impacts the prevalence of antibiotic-resistant bacteria on working farms. The team agreed to incorporate additional questions regarding the impact of the VFD in their interview instrument (S1 File). Questions included both open- and closed-ended items. This phase included producers from three Ohio counties (Mercer, Wayne, and Muskingum) that represent different levels of landscape and farm diversity. Building upon the results of Phase I, we revised the interview instruments to gain a deeper and more nuanced understanding of the ground-level impact of the VFD and recruited additional cattle farm operators and large animal veterinarians (S2 and S3 Files). Phase II focused mainly on cattle farmers operating in Western Ohio (Adams, Clark, Highland, Mercer, and Montgomery counties) and veterinarians throughout the state.

In both phases, we initially identified potential interviewees through meetings and professional contacts with local OSU county extension educators, Soil and Water Conservation Service staff, leaders of the Ohio Farm Bureau and Ohio Cattleman’s Association, the Ohio State Veterinarian’s office, and publicly advertised cattle operations. At the end of each interview, respondents were asked to volunteer names (and contact information) for other livestock operations in their area who might be able to provide additional perspectives. Through this snowball sampling approach, we were able to identify and recruit a number of additional farms. Farmers and veterinarians were contacted by email and phone to gauge their interest in participating. While this approach was not designed to achieve a true random sample, we attempted to minimize sampling bias by purposively selecting participants who represented all farm sizes as classified by the USDA 2017 census, as well by soliciting both beef and dairy farm operators. Across the two phases of the study, we received useable interview data from 54 cattle farms, including 39 beef and 15 dairy operations (Table 1). Compared to census data, our final sample underrepresents the smallest cattle farms (< 50 head) but includes the full range of USDA farm size classes (Fig 1).

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Fig 1. Size distribution of Ohio cattle farms interviewed for this study.

Percent interviewed as compared to percentage of OH farms by USDA size class and percentage of animals (number head).

https://doi.org/10.1371/journal.pone.0255911.g001

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Table 1. Total cattle farm operators interviewed.

https://doi.org/10.1371/journal.pone.0255911.t001

Data collection and analysis

The interviews were semi-structured and occurred at a time and in a place of the participant’s convenience, either in person or by phone between May 2019 –January 2020. The Phase I interviews were conducted in pairs with one person asking questions and another taking notes. One or both of the authors were present at all but six of the Phase I interviews; the remaining six were facilitated by a third lead OSU interviewer. The lead author conducted 100% of the Phase II interviews. All interviews were recorded (with the participants’ permission), transcribed, and treated confidentially. Both authors had access to the recordings and transcripts from both phases of interviews.

The interview instruments contained a mixture of open-ended questions (exploring antibiotic use and philosophy, in addition to farm demographics and landscape characteristics) as well as a series of quantitative Likert scale questions which focused on the impact of the VFD. One week into Phase I, a Likert question assessing the VFD impact on the frequency of veterinarian interactions was added. In the Phase II producer instrument, many open-ended questions which did not pertain to the VFD or antibiotic use were deleted, and two additional Likert scale questions (regarding the impact on paperwork and fed antibiotics) were added. A similar parallel instrument was developed for the veterinarians.

The quantitative data from the six Likert scale questions common to both phases of producer interviews were combined. One of the additional questions (use of fed antibiotics) had no Phase I Likert counterpart, but it nearly always arose in answers to open-ended questions about the impacts of the VFD. Using the transcripts from the interviews, we were able to infer whether most Phase I farms had previously used fed antibiotics prior to the VFD, and by how much (or if) their use of fed antibiotics had changed since the implementation of the rule. We used descriptive statistics to analyze the frequency of quantitative (close-ended) questions.

Transcripts of the interviews were systematically analyzed and coded for emergent themes and patterns using established methods of qualitative data analysis [24, 25]. Specifically, both authors independently identified components of answers to each question that could be coded into distinct themes, and collaboratively refined the criteria for code assignment until both authors converged on similar coding assignments. Both the qualitative and quantitative results were compared and contrasted across farm types and stakeholder groups.

To examine production trends, we compiled state and national-level data on cattle production between 2009–2018 from annual reports issued by the USDA National Agricultural Statistics Service (NASS) ‘QuickStats’ tool [26]. Ohio ten-year trend lines were graphed with the corresponding national data for context. We examined the trend lines for obvious deflection points coinciding with the implementation of GFI #213 to determine if additional statistical analysis was warranted.

The impact of the VFD on cattle producers

Table 2 reports the percent of farmers in our sample who reported changes in various management practices and other on-farm outcomes as a result of the VFD. Most farmers reported no or minimal impacts, with 90% of responses to most items either “no change,” “decreased a little” or “increased a little.” The greatest variations were seen in response to questions regarding the use of fed antibiotics (30% reported a decline), interactions with veterinarians (23% reported an increase), and amount of paperwork (50% reported an increase).

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Table 2. Changes due to VFD reported by interviewed Ohio cattle operations.

https://doi.org/10.1371/journal.pone.0255911.t002

Further analysis revealed that the reported effects of the VFD on Ohio cattle operations varied by three key farm characteristics:

1. Whether or not the farm operator had used fed antibiotics prior to the implementation of the feed directive
2. Type of operation (dairy versus beef)
3. Herd size

Prior administration of antibiotics through animal feed.

Roughly 44% (24 out of 54) of the cattle operations interviewed had not been using fed antibiotics prior to the VFD. Unsurprisingly, this group reported being generally unaffected by the VFD. Of the roughly 56% (30 out of 54) cattle operators who had previously used fed antibiotics (at least occasionally) in the past, their reported impact varied by type of farm (beef or dairy) and size of operation. Farms that fed antibiotics prior to the VFD were much more likely to experience impacts from the policy change.

Dairy operations. The dairy farmers who reported pre-GFI #213 use of fed antibiotics (11 of 15 interviewed), reported having little trouble complying with the VFD. This was largely because dairies generally avoid use of antibiotics with their milking cows because milk must be discarded during a “withhold” period after a cow receives antibiotics. The dairy operators reported that use of fed antibiotics occurred mainly with groups of calves. Additionally, dairy farmers interact more frequently with their veterinarians as part of regular herd health checks, so obtaining a feed directive, when needed, was relatively easy (typically reported as merely an extra step, not something onerous).

Among those who previously fed antibiotics, the most commonly reported impacts of the VFD on dairy operations reflected a significant decrease in the use of fed antibiotics (AB) for calves and a slight increase in the use of nutritional supplements and interactions with their veterinarians (Fig 2).

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Fig 2. Impact of VFD on subset of Ohio dairy and beef operations using fed antibiotics prior to the VFD.

Mean score for impact on various aspects of farm management and performance. Responses to 1–5 Likert Scale in which 1 = Decrease a lot, 2 = Decrease a little, 3 = No Change, 4 = Increase a little, 5 = Increase a lot. Horizontal line represents no reported change.

https://doi.org/10.1371/journal.pone.0255911.g002

Interviewee comments provided greater nuance. In response to “How did the VFD change your dairy operation?”, operators consistently reported that feeding Aureomycin (tetracycline) “crumbles” to calves during weaning or transitions was less convenient after the VFD, therefore operations tended to reduce the practice. To compensate, some shifted to treating sick calves with electrolytes or individually with injectable antibiotics. Some representative quotes were:

There’s nothing to the milking cows; and the calf side, I would say we use less strictly because of the hassle. (Dairy, large)

We were giving quite a bit of antibiotics for scours. We pretty much stopped that and we’re doing more of a electrolytes treatments and that kind of thing. They seem to respond pretty well. (Dairy, large)

The calves, I would say, I probably do use more injectable. (Dairy, medium)

They also commented on the need for more frequent interactions with their veterinarians, but suggested it represented a minor increased demand on time:

You gotta get a VFD from the vet if you want to use an antibiotic in the feed. Other than that, it’s not too horrible. (Dairy, medium)

Probably the biggest challenges is it created a different set of hoops to go through to be able to get the antibiotic that we’ve used to put in the feed. (Dairy, large)

Just to remember to get the VFD we need when it was up and make sure we had everything in line. (Dairy, medium)

To summarize, all of the dairies reported little to no difficulty with compliance. Typical comments included “It hasn’t been that hard,” “Very easy,” “Oh, it’s been fine. It’s a little more hassle,” and “Actually, it’s more of a nuisance than it is anything else.”

Beef and/or replacement heifer operations. The non-dairy cattle operations interviewed were primarily cow/calf operations, though our sample also included some finishing operations (both grass-fed and feedlot), some backgrounders (pre-finishing), and a couple of replacement dairy heifer operations. All the cattle were ultimately being raised for beef with the exception of two replacement heifer operations associated with dairies. For simplicity, we will refer to this entire group as ‘beef operations.’

The beef producers tended to be more diverse in terms of their approaches to antibiotic use and management. As opposed to the dairy interviews, where most of the operations had regularly used fed antibiotics prior to the VFD, the beef operations reported closer to an even split with 19 of 39 operators reporting at least some use of fed antibiotics prior to the feed directive and 20 of 39 reporting that they never used fed antibiotics.

Of the latter group (never fed antibiotics), beef farmers’ reasons were obviously different from dairy farm operators who need be more cognizant of the “withhold” requirement. Among the “no fed antibiotic” beef producers, some held deep convictions regarding the need to use antibiotics as sparingly as possible, often employing strong preventative measures. These included regimented vaccination schedules, good ventilation and regularly cleaned bedding for animals when in barns, and providing shelter for the herd from wind/sun when outdoors. Many cited the need to reduce stress, and therefore susceptibility to disease, such as one producer who managed his herd by “walking” versus “driving” cattle to new grazing grounds.

Typical comments included:

Really.,,, I love this barn because the ventilation keeps us from having any air, respiratory problems…But, I mean, just little easy management of stuff and I just don’t have much in the way of health problems. (Small, beef)

What I’ve learned is … for the cattle-wise, keeping the bedding just clean. Two times a week I scrape the barns and scrape the lots, and make sure that they’re in a good clean environment and that really helps. (medium, beef)

Others in the “no fed” group, usually medium to smaller operations (~ 100 heads or fewer), simply took a more “laissez-faire” approach to management in general, often not even vaccinating their cattle. To summarize, in response to “What is your philosophy or general approach to antibiotic use?” many beef producers articulated a range of personal values that highlighted their preference for judicious or minimal antibiotic use:

I try to avoid it at all costs…I’m a physician … and I’ve seen within medicine what’s happened to our antibiotic resistance. It’s just dramatic. And so I was 100% in favor of restricting antibiotic usage. (Beef, medium)

It’s mostly nonexistent… Never. Hardly ever…Because we don’t have a way to catch our cows, so hardly ever anything’s done. (Beef, medium)

Of the nineteen interviewed beef farmers who used fed antibiotics prior to GFI

#213, many reported that it was “not difficult” to comply VFD, often citing they already had established a good relationship with their veterinarian. Of those operations affected by the VFD, the most commonly reported changes included reduced use of fed antibiotics (crumbles) for calves, changes in management practices, increased interactions with vets, and increased paperwork (Fig 2; Table 2). Overall, beef producers were also more likely than dairy to report that they increased their interactions with veterinarians.

Before the VFD mandate, antibiotic “crumbles” were readily available over the counter and routinely mixed into livestock food by feed mills. The following comments illustrate the reduced use of fed antibiotics and/or a change in management practices due to the VFD.

… now I would say that we’d probably do that less (use fed antibiotics with calves) and we probably get in individual calves, and give them a shot of antibiotic rather than feeding the whole group. (Beef, large)

Now we’ve combated that, and we’ve implemented a different vaccination program, so now we’re trending (economically), working better than they were before, but we’re getting it in a different way. (Beef, large)

We would use more injectable antibiotics, as opposed to feed grade antibiotics. (Beef, medium)

Size of operation. The interviews included farms across a wide range of herd sizes (from a handful of cattle to herds of more than 1000). Many informants felt that the larger operations would be more greatly impacted by the VFD, especially the feedlots, as they were more likely to be using fed antibiotics. This perspective was overall supported by the data. The percentage of beef operators using fed antibiotics generally increased by class of herd size, while fed antibiotics were commonly used on both medium and large dairies (Fig 3A and 3B).

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Fig 3. Use of fed antibiotics by Ohio cattle operations, percent by herd size.

a. Dairy (size of milking herd) b. Beef (total head).

https://doi.org/10.1371/journal.pone.0255911.g003

On the other hand, many of the larger farm operators shared their impressions that smaller operations would be more impacted, primarily due to their lack of routine access to a veterinarian. Typical comments included:

I think the farmers that it hit were the guys that were small, smaller and don’t have the vet on the farm all the time. (medium, dairy operator)

Most of the cattle operations who got any amount of numbers, they follow ‘to the T’ …the Veterinary Directive. The ones where you run into trouble is the guys that have maybe five or 10. They’re not big enough to handle any larger amount, so they just have a real battle. (large, beef operator)

It puts the small guy like me and anybody that can’t have the vet on staff, at a major disadvantage. (medium, beef)

These perspectives were supported by the interviews. The two interviewed small (1–19 head) beef operations that had previously used fed antibiotics reported that they had stopped due to the inconvenience/hassle of compliance with the VFD and difficulty in finding an available veterinarian. Perhaps the impact of the VFD on Ohio cattle operations can best be summarized by the following operator comment:

It’s probably not that much of an issue for large or small, but they both have some times when it could be a challenge. (Beef, medium)

Impact of the VFD on veterinarians

We interviewed eight large animal veterinarians practicing in Ohio. The percentage of their clients who were cattle producers ranged from less than 10% to 80%. They represented a wide range of experience in the profession, from newly graduated from veterinary school to over forty years in practice. Additionally, they represented counties from the most northern to the most southern regions of Ohio. Almost all had established VCPRs (Veterinary Client Patient Relationships), with both beef and dairy producers, collectively representing interactions with hundreds of cattle operations.

The veterinarians interviewed were overwhelming positive about the goal of the VFD as expressed in this representative comment:

I was pretty positive about it. I thought it was necessary. I feel like there was too many antibiotics used without direction. Things were just dumped in without even having any knowledge of why or what for. And even after it started, we found lots or those situations where people couldn’t understand why they couldn’t just dump a bag of antibiotics in their feed without some direction.

Despite supporting the goal of the VFD, many were quite worried or concerned about its impact prior to implementation:

Everybody was kind of freaking out about it when it came out. Nobody really knew what was going on. The listserv for AABP was rife with discussion for months; we just had so much hype that this was what we had to do, and we had to do this correctly, and USDA’s going to be watching us, and on and on. And about how this is going to be a major change to the way we practice veterinary medicine, and it was not so.

So it hadn’t been that big a deal…people were scared to death it was going to be.

Consistent with the cattle producers, the veterinarians reported that despite the initial misgivings, compliance with the feed directive was not very difficult. The reported areas of greatest impacts were also consistent with the producer interviews (Table 2; Fig 2): increased number of VCPRs, a decreased amount of fed antibiotics (AB), increased number of client interactions (farm visits), and increased record keeping and paperwork (Fig 4).

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Fig 4. Mean scores for veterinarian responses describing the impact of VFD.

Likert scale responses (n = 8) in which 1 = Decrease a lot, 2 = Decrease a little, 3 = No Change, 4 = Increase a little, 5 = Increase a lot. Vertical line represents the response of “No Change”.

https://doi.org/10.1371/journal.pone.0255911.g004

The value for “amount of scripts (prescriptions) written for feed” may be underreported. The veterinarians in our earlier interviews were not sure how to respond to this question; the latter participants emphatically stated that this value increased a lot, as they were not writing any feed directives prior to implantation of GFI #213, due to the fact that fed antibiotics were freely available over the counter (OTC).

The increase in client interactions was due, in part, by the requirement that feed directives can only be issued in the context of an established VCPR. In other words, veterinarians were required to visit the farms and have some first-hand knowledge of the operations. Vets reported that this provided them the opportunity to discuss appropriate use of antibiotics with the producers. Representative comments include:

Oh yes. Yes. There was a significant amount of education about the process, about why we had to do it and that I was just not trying to make more money off of them.

I think more than anything, it allowed us to create a discussion on farms to determine why do we need it and what can we do to prevent the need for it.

Much of the interactions with producer clients centered on communicating a judicious approach to antibiotic use as well as changing producer mindsets that antibiotics should be the first course of action for disease control or prevention. Consistent with many producers, veterinarians emphasized the importance of good preventative management practices which reduce, and at times, even eliminate, the need for antibiotics.

I think that they do get overused. I don’t tend to use them as a first line. I would rather prevent disease…I think they’re definitely necessary to save animals and help them, but they should not be used to manage them.

Better vaccination programs, better nutrition, weaning their cattle better, planning better. It’s just changed everything.

We have a major slant towards judicious use, which means that we have written protocols for the diseases of interest on our dairies. And we’re in the process of updating them right now for our annual update. We are inclined towards injectable for individual animal treatment.

The farmer invested in a positive pressure tube ventilation system. And what we found is he doesn’t need to give those antibiotics anymore … both feed through antibiotics and injectable antibiotics in that barn.

Also, consistent with the cattle producers, veterinarians reported increased record- keeping and paperwork as a major impact of the VFD on their practice. They also reported VFD-related frustrations. Despite these reported frustrations, a commonly heard theme from the veterinarians was that the VFD prodded them to become better and more responsible veterinarians. Sample responses were:

And then as far as the paperwork goes, it’s figuring out the stinking dosages on those things. They can’t even make them consistent across the board. It was just irritating, trying to get that… Two years into it, we’re still figuring it out.

Well, I think the paperwork is the biggest thing.

And so what the VFD has done is targeted that and made the veterinarian responsible and accountable, which is the way it should be.

I think it’s kind of accentuated the VCPR, it kind of gave credibility to the veterinary of record. Veterinarian oversight has become more defined and I think it’s good for the industry, not just for me, but I think for the whole industry.

Ohio livestock ten-year production trends

In general, longitudinal data on the level of Ohio and US cattle production suggest that there were no obvious negative impacts on overall production output associated with the implementation of GFI #213 and the revised Veterinary Feed Directive (VFD). The vertical lines in Fig 5 represent the years when voluntary (left line) and mandatory (right line) compliance were initiated, respectively. Both US and Ohio cattle production have been steadily increasing since the implementation of GFI #213 (Fig 5), suggesting that production by Ohio cattle operations have not been negatively impacted by the new FDA regulations.

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Fig 5. Cattle production, measured in pounds, 2009–2018.

(Source, USDA). Vertical lines indicate the beginning of voluntary (left) and mandatory (right) compliance with the FDA’s GFI #213, restricting use of antibiotics in livestock.

https://doi.org/10.1371/journal.pone.0255911.g005

These data are consistent with our cattle producer interviews. The overwhelming majority of interviewees reported “no impact” on production as the result of the VFD. During the interviews, some farm operators reported challenges in 2019 due to political and/or economic reasons (e.g. China tariffs, changing economies of scale); however, none listed the VFD as a negative driver of production.

Recommendations for further research

The goal of the FDA in implementing the revised VFD and GFI #213 was to promote a decreased and a more judicious use of medically important antibiotics in livestock production. Federal statistics suggest that antibiotic consumption in livestock nationwide has significantly decreased since the implementation of GFI #213 [10]. Similar statistics are not available at the state-level. To fill this gap, future farm-level research in Ohio would benefit by tracking overall volumes of antibiotic use over time on a representative sample of farms. It would also be interesting to replicate this work in other states to see if the patterns found in Ohio are similar or different to the experiences in regions with different types of cattle enterprises.

Producers themselves have voiced a greater need for more scientific research, especially in the area of genetics, specifically citing both the need for more disease-resistant livestock and continued research into greater feed conversion. Finally, in January 2022, the FDA plans to issue another rule (GFI #263) which will move the remaining OTC antibiotics, including injectables, under the supervision of veterinarians. A similar post-implementation farm-level study could help identify how this next policy change impacts different types of cattle producers.

Study limitations

To our knowledge, this is the first study to investigate the impact of the revised VFD on Ohio livestock operations; however, our work has several limitations. The farms included in our interviews were not randomly selected, although we did try to achieve a theoretical quota sample to get a range of farm types and sizes. Our producer interviews focused only on cattle operations, and did not include poultry and swine production. Finally, our investigation of local level impacts of the VFD were restricted to Ohio operations and the experiences may differ in other states, particularly those with a greater predominance of large-scale cattle feedlot operations.