On April 13, 2012, the US Food and Drug Administration (FDA) issued Guidance for Industry (GFI) 209 “to inform the public of FDA’s current thinking on the use of medically important antimicrobial drugs in animal agriculture.”1,2 On December 12, 2013, FDA issued GFI 213 to provide “information to sponsors of certain antimicrobial new animal drug products who are interested in revising conditions of use for those products consistent with FDA’s Guidance for Industry (GFI) #209” and to “set timelines for stakeholders wishing to comply voluntarily with this guidance.”3,4 On June 3, 2015, FDA issued the revised Veterinary Feed Directive (VFD) which “established requirements relating to the distribution and use of VFD drugs and animal feeds containing such drugs,”5 and became effective on October 1, 2015. Full implementation of FDA’s GFIs and VFD final rule was set for December 2016 with enforcement commencing on January 1, 2017.

The GFIs and VFD final rule direct the use of medically important antibiotics (defined as antibiotics that are important for therapeutic use in human medicine) in livestock for therapeutic purposes only. Therapeutic purposes are defined as either treatment, control, or prevention of disease.2 These policies are focused on use of medically important antibiotics given in mass medication formats, either through the feed or the water. Use of medically important antibiotics in feed requires a VFD order from the veterinarian to the producer and feed manufacturer. Medically important antibiotics used in water requires a veterinary prescription. Another aim of these policies was to require that if producers wanted to use medically important antibiotics, they could only do so under the guidance of a veterinarian with a valid veterinarian-client-patient relationship (VCPR). This endows the veterinarian with the responsibility for making medical decisions for the farm, with the producer bearing responsibility in following the medical directions of the veterinarian. Another aim of these policies was to eliminate the use of medically important antibiotics for growth promotion use. Collectively, these new regulations have changed the ways that antibiotics are used in livestock production.

From a 2016 survey of practicing swine veterinarians on VFD preparation, Schulz and Rademacher6 reported that extensive preparation and education was being done by veterinarians and their producers to help ensure a smooth transition to the new antibiotic-use guidelines. The results also suggested that there were varying views on the definition of a VCPR, plans for meeting the additional record keeping requirement and delivery of VFDs, fees associated with providing VFDs, costs to swine veterinary business operations, and reduction in the use of antibiotics in feed as a result of the VFD. A follow-up survey was conducted in 2017 to assess post-enactment impacts of the revised VFD.

Materials and methods

The survey protocol was approved by the Iowa State University Institutional Review Board (IRB ID 16-489) prior to distribution of the survey. Data collection procedures for this study were similar to those used for the 2016 survey as described by Schulz and Rademacher.6 Questions from the 2016 survey were revised to reflect post-January 1, 2017 status of the new antibiotic-use guidelines. In addition, new questions were added to the survey to elicit information on the fee structure for writing VFDs and prescriptions, the level of production (ie, group or lot, site, flow, or system), and average number of pigs for which a VFD was written. The data for this study are from a convenience sample of practicing swine veterinarians. Swine veterinary practitioners attending the 2017 Iowa State University (ISU) James D. McKean Swine Disease Conference held in Ames, Iowa, on November 2-3, 2017 were surveyed. The conference attracts veterinarians, students, academic faculty and staff, and allied industry personnel. Of the 305 conference attendees, 125 practicing swine veterinarians were identified at conference check-in and given a paper survey.

To increase survey response and expand distribution, input was sought from ISU faculty and staff who were familiar with swine production systems and swine-focused veterinary clinics to identify additional practicing swine veterinarians to be surveyed. A convenience sample of 35 practicing swine veterinarians from the upper Midwest region of the United States who did not attend the conference were surveyed electronically using Qualtrics (Qualtrics, Provo, Utah). The Qualtrics survey questionnaire sent to practicing swine veterinarians was identical to the one distributed at the conference. A customized email invitation for the Qualtrics survey was sent on November 16, 2017 with reminders sent to non-respondents on 2 occasions 1 week apart. The Qualtrics survey was closed on December 18, 2017. Data retrieved from returned surveys were compiled and summarized using descriptive statistics.

After several introductory questions gathering practitioner demographic (ie, location, experience) and clientele base (ie, independent, contractor, or contract grower; phase of production; annual pig sales) information, the practitioners surveyed were asked a series of questions about how the VFD requirements impacted their business operations as well as swine production in general. Specifically, questions targeted veterinarian-client-patient relationships, client recruitment, VFD fees and creation, record keeping, education and training, business costs, and changes in antibiotic usage and on-farm management.

Results

Response rate and respondent profile

The response rate for the survey distributed at the ISU James D. McKean Swine Disease Conference was 23.2%, 29 of 125 practitioners who received a paper survey returned a completed survey. Thirteen of 35 practitioners who received a Qualtrics survey returned a completed survey, a 37.1% response rate. Therefore, there were 42 practicing swine veterinarians in the final sample. However, a few participants only partially completed the survey. The number of respondents for each question of interest are presented in Tables 1 through 12.

Comprehensive questions about veterinarian demographic details (eg, private vs corporate practice or employed by an integrator) were not included in the survey and, therefore, it cannot be confirmed if the study sample is representative of the entire practicing swine veterinarian population. Respondents’ primary geographic location were in states with the largest number of swine operations and inventories: 24 veterinarians practiced in Iowa and 9 in Minnesota. Other states represented include Illinois (3 respondents), Indiana (2 respondents), Kansas (1 respondent), Missouri (1 respondent), and Nebraska (1 respondent). According to the 2012 US Census of Agriculture, these states represent 30% of US swine operations and 67% of the US pig inventory.7

The average number of hogs marketed annually by the responding veterinarians’ clientele were 0 (1.5% of clients), 1 to 4999 (13.1% of clients), 5000 to 19,999 (23.0% of clients), 20,000 to 49,999 (23.2% of clients), and 50,000 or more (39.2% of clients). For the 7 states represented, 74% of all operations have annual sales of 1 to 4999 hogs, while 26% of operations have annual sales of 5000 or more hogs according to the 2012 US Census of Agriculture.7 Thus, the clients served by the veterinarians within our sample had larger operations than the census averages.

The largest percentage of swine clients served by veterinarians had farrow-to-finish production (39.2%), followed by wean-to-finish (21.3%), breeding-farrowing (18.8%), finishing (12.2%), nursery (5.6%), gilt developer unit (2.7%), boar stud (0.2%), and other (0.1%). The largest segment of swine clients were independent producers (64.5%), followed by contractors or integrators (21.7%) and contract growers (13.8%).

These general demographic characteristics of the survey participants suggests a reasonable degree of representation of clients served by veterinarians was achieved despite use of convenience recruitment techniques. However, due to not asking certain questions in the survey and the small sample size, we were not able to make comparisons across several factors that characterize the entire population of swine veterinary practitioners. Therefore, the study results may not be generalizable to all practicing swine veterinarians and may not represent the entire US swine industry. Nonetheless, this work reports one of the first attempts to track progress toward adjusting to the new antibiotic-use guidelines.

Veterinarian-client-patient relationship

All respondents were aware of their respective state’s VCPR definition. Twenty-one of the 41 responding veterinarians (51.2%) believed that only 1 visit per year was needed to maintain a VCPR, whereas 11 veterinarians (26.8%) thought 2 visits and 7 veterinarians (17.1%) thought 4 visits were needed to maintain a VCPR (Table 1). Two veterinarians replied that they did not know how many visits were required to have a VCPR. One common concern often voiced from practicing veterinarians was an obligation to make site visits solely for the purpose of writing VFDs. More than half of 41 survey respondents (24 veterinarians; 58.5%) felt as though they were conducting more site visits per operation with the new VFD regulations. Veterinarians were asked how many sites within an operation they felt were necessary to visit to fulfill the VCPR requirements. The majority of respondents (26 of 41; 63.4%) felt it necessary to visit all sites, while 14 respondents (34.1%) felt that they had to visit more than 1 site, but not all sites. Only 1 veterinarian replied that visiting 1 site was sufficient to satisfy the VCPR requirement. These results differ somewhat from the 2016 survey responses where a larger proportion of veterinarians (56.0%) envisioned visiting 2 or more sites, but not all sites, compared to the proportion (40.0%) that anticipated visiting all sites.

Client recruitment

Regarding client recruitment, 17 veterinarians (41.5%) reported being approached by new clients for the purpose of writing VFDs (Table 2). Fourteen veterinarians (34.1%) accepted new clients that approached them specifically to provide VFDs, but only 6 of them (14.6%) admitted to actively recruiting new clients to meet minimum requirements to provide VFDs. These results would only apply to veterinarians working for veterinary clinics. Prior to the new regulations, there were anecdotal reports of some producers who would purchase their medically important antibiotics over-the-counter from local feed suppliers rather than routinely use veterinarians. Once VFDs or prescriptions were required for antibiotic administration of a medically important antibiotic to a population of pigs, it is reasonable to hypothesize that the client pool for veterinarians increased.

VFD fees

The mean fee per VFD written for existing clients was $23.75 and for new clients was $24.19 (Table 3). Only 36 and 31 veterinarians, respectively, responded to this question which is most likely due to some respondents being employed by production companies and therefore do not charge for VFDs they write. Based on client operation size, a median difference of approximately $2.50 to $5.00 per VFD was found for operations who marketed between 1 and 49,999 pigs. Similarly, a median difference of $2.50 to $7.50 per prescription was observed across client operation sizes (Table 3). In general, it appears that veterinarians charged clients with larger operations more for VFDs and prescriptions. Thirty-five of the 40 responding veterinarians (87.5%) that are charging for a VFD include this expense as a separate line item in their invoice. When compared to veterinarians who also write prescriptions, only 21 of the 37 responding veterinarians (56.8%) include prescriptions as a separate line item, rather than writing prescriptions as part of a consultation or service fee.

VFD creation

Veterinary Feed Directives can be written for various levels of production. When the 42 respondents were asked for which level of production they most frequently wrote VFDs, 18 (42.9%) responded the pig flow level, while 12 (28.6%) responded the site level and 9 (21.4%) responded the group or lot level (Table 4). The mean number of pigs covered by a written VFD was 5916 pigs with a median of 2600 and a standard deviation of 9070 (Table 5). Over half of the respondents (22 of 39) wrote VFDs for 2400 to 9999 pigs, while 11 (28.2%) respondents wrote VFDs for fewer than 2400 animals and 6 respondents (15.4%) wrote VFDs for more than 9999 animals. To generate VFDs, veterinarians predominately used an electronic VFD service (34 of 41; 82.9%) but had also made their own VFDs (7 of 41; 17.1%) or used a VFD form from a drug sponsor (4 of 41; 9.8%) (Table 6). For drug prescriptions, most veterinarians responded that they used a form they had created (28 of 41; 68.3%), while others used an electronic prescription service (13 of 41; 31.7%) or a prescription form provided by a drug sponsor (4 of 41; 9.8%).

VFD record keeping

Veterinary Feed Directives must be retained for 2 years by the producer, feed distributor, and the veterinarian. Almost two-thirds of the 41 responding veterinarians (63.4%) had used a third-party service (eg, Global VetLink [GVL]) in order to meet this requirement, while 11 (26.8%) used existing staff (Table 7). Independent of how the VFD was generated, veterinarians reported to have delivered VFDs to producers via a third-party electronic service (28 of 41; 68.3%), email (22 of 41; 53.7%), hard copies (18 of 41; 43.9%), fax (12 of 41; 29.3%), and method of producer (8 of 41; 19.5%) or feed supplier (6 of 41; 14.6%) preference.

Education and training

Since the implementation of the new guidelines, veterinarians and staff had attended meetings (including webinars) (34 of 41; 82.9%), read literature (32 of 41; 78.0%), and created information bulletins to distribute to staff (13 of 41; 31.7%) to learn about the VFD requirements (Table 8). To help educate their clients, veterinarians sponsored in-clinic meetings (including webinars) (16 of 40; 40.0%), met with clients in person (35 of 40; 87.5%), sent a notice of requirements in a regularly published newsletter (20 of 40; 50.0%), and created an information bulletin (15 of 40; 37.5%). The frequency of updated training on VFD requirements varied, but the largest percentage of respondents believed updated training should occur annually for both staff (26 of 40; 65.0%) and clients (26 of 39; 66.7%).

Cost of VFD regulation implementation

When evaluating the business costs associated with VFD regulation implementation, there were more non-responders (n = 19) than for most of the other survey questions. This is most likely due to responding veterinarians either being employed by production companies or being young, associate veterinarians who are not involved in the financial dealings of the clinic. Six survey respondents (14.6%) had 1 to 5 years of experience in swine veterinary practice and an additional 6 respondents (14.6%) had 6 to 10 years of experience.

Descriptive statistics and distribution of annual cost estimates regarding writing and delivery of VFDs, maintaining records for VFDs, educating clients and others (eg, nutritionists and feed suppliers), training staff on VFD requirements, and other components are presented in Table 9. Writing and delivering VFDs was the largest annual cost across all respondents with a mean value of $4051 and a median value of $3000. The annual cost for maintaining VFD records was similar in expense with a mean value of $3561 and a median value of $1000. The lowest annual cost to business operations was training staff on VFD requirements (mean of $787; median of $500). Costs recorded in the “other” category by 2 respondents were listed as the cost of the GVL software and additional staff required to write and store the VFDs. Generally, the costs slightly increased as client operation size increased, most likely due to the increase in the number of VFDs that would be written annually.

Table 10 shows the perceived amount of burden the respondents felt that VFD requirement compliance has had on veterinarians, feed suppliers, producers, and consulting nutritionists. Overall, burden to comply with the VFD is considered moderate. The highest amount of burden is believed to be on feed suppliers followed closely by producers and veterinarians.

Impact of antibiotic-use regulations

The reality of FDA’s antibiotic-use guidelines is that producers and veterinarians have had more conversations about judicious antibiotic use of medically important antibiotics in feed or water. Overall, a perceived reduction in the amount of antibiotics used was reported, however, the magnitude of the reduction varied. The largest percentage of responding veterinarians (9 of 20; 22.5%) indicated a 21% to 30% perceived reduction in the use of antibiotics in feed by their clients as a result of the new antibiotic regulations (Table 11). Thirteen (32.5%) respondents perceived a 51% to 100% reduction of antibiotic use in feed among their clients. Swine veterinarians also reported a perceived increase in the amount of injectable (19 of 40 respondents; 47.5%) and water-soluble antibiotics used (30 of 41 respondents; 73.2%) since the VFD regulations were implemented.

Management changes due to regulations

One of the most important changes in the new regulations was the removal of medically important antibiotics for growth promotion. In response, it appears that most clients dealt with this change by eliminating all uses of antibiotics for growth promotion (58.8%), while another 17.0% of clients reduced use of antibiotics for growth promotion (Table 12). About 24% of clients changed to the use of non-medically important antibiotics for growth promotion. These results were different than those reported in the 2016 survey where veterinarians were predominately recommending replacing the medically important antibiotics with non-medically important antibiotics for growth promotion (52.9%).6

Responding veterinarians (n = 37) reported that increased vaccinations (30; 81.1%) were the primary management change made due to the new antibiotic regulations. Increasing non-antibiotic feed additives (21; 56.8%), modifying biosecurity (18; 48.6%), and modifying nutrition (14; 37.8%) were other common responses. One of the concerns veterinarians had during the previous survey regarding the new regulations was having enough documentable evidence to justify their recommendations to use medically important antibiotics. Thirty-nine of the 41 responding veterinarians in the present survey (95.1%) felt they had collected the needed health diagnostic information to defend or justify their antibiotic-use recommendations.

Discussion

On January 1, 2017, GFIs 209 and 213 and the revised VFD took effect. With a 3-year implementation timeline from the time the GFIs were published, these regulations had already begun to influence antibiotic-use practices. According to the FDA 2016 Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals, sales of medically important antibiotics decreased by 14%.8 Sales to US swine producers made up 37% of the medically important antibiotics that were sold to livestock in 2016, so it is reasonable to assume that a portion of this overall decrease was in preparation for the new regulations to take effect. In 2016, there were many conversations among veterinarians and regulatory officials about how many visits to each site would fulfill the VCPR definition of timely visits. Some states have defined what constitutes timely, whereas others have not. Our survey results were varied with 51.2% of veterinarians thinking an annual visit would suffice, but the rest of the respondents felt it would take 2 or 4 visits per year to be considered timely. Many swine owners today have pigs that are raised on many different sites. Most of the veterinarians surveyed felt that they needed to visit all sites to have a valid VCPR, but there was a significant number of veterinarians that felt they needed to visit more than one site, but not all sites, within the operation to be in compliance.

For those veterinarians who charge for writing VFDs, the mean fee for both new and existing clients was approximately $24 per VFD (median fee of $25), in contrast to an anticipated fee of $27 to $30 per VFD based on the 2016 survey.6 The standard deviation was also cut in half compared to the 2016 survey, indicating that charges for VFDs are much more consistent across the industry. Prescription prices were less than the price of VFDs (median value of $20). While most of the VFDs are listed as a separate line item on a veterinary invoice, it is more common for prescriptions to be included as part of a consultation fee.

There is a fair amount of variation regarding what level of production a VFD is written for. Flow (generally defined as pigs that originated from the same breeding herd but raised in several different locations after weaning) was the most common production level, but there were many veterinarians who wrote VFDs specifically for the site and some even down to the individual lot level. Most veterinarians surveyed used an electronic service to both issue and store written VFDs. However, many veterinarians surveyed still used computer-generated forms rather than utilizing an electronic prescription service.  

These survey results provide evidence that the new regulations have resulted in a perceived decreased usage of antibiotics in feed. The most common response was a 21% to 30% perceived decrease in antibiotic usage, but nearly a third of respondents believe that the reduction is anywhere from 50% to 100%. One of the biggest changes in antibiotic usage was their overall removal for growth promotion. In the 2016 survey, the majority of respondents predicted that their clients would shift from medically important to non-medically important antibiotics for growth promotion as there are several products now available and new products being evaluated. It appears though, that most of their clients eliminated either all or part of their antibiotics used for growth promotion, thus most likely contributing to the overall decrease in antibiotic usage.

Due to this survey using a convenience sample, there are some limitations to this data. There is certainly potential for biases based on the sampling technique and the geographic region from which the sample was derived. The readers should take this into consideration and not extrapolate the results of this survey to the entire US swine industry. The low response rate also necessitates caution when interpreting results. It is unknown whether collecting survey responses by type of veterinary practice, eg, private vs corporate practice or employed by a large integrator, would have affected the results. However, the swine veterinary practice demographics collected did demonstrate variability and responses were from US states with the highest concentration of swine production. Informed by these results, future surveys should employ a randomized questionnaire distribution method and include questions to provide a more complete picture of how the antibiotic-use guidelines continue to impact pork production and the practice of swine veterinary medicine in the United States.

Implications

• Improved veterinarian oversight of antibiotics used in US swine production was a key response from survey participants.
• Survey respondents reported the occurrence of more discussions between swine veterinarians and producers about the use of antibiotics and antibiotic alternatives.
• Survey respondents perceived a reduction of antibiotic use in feed as a result of the VFD regulations.

Acknowledgments

Conflict of interest

None reported.

Disclaimer

Scientific manuscripts published in the Journal of Swine Health and Production are peer reviewed. However, information on medications, feed, and management techniques may be specific to the research or commercial situation presented in the manuscript. It is the responsibility of the reader to use information responsibly and in accordance with the rules and regulations governing research or the practice of veterinary medicine in their country or region.

References

*1. Guidance for Industry on the judicious use of medically important antimicrobial drugs in food-producing animals; Availability. Fed Regist. 2012;77(72):22328-22329.

*2. US Department of Health and Human Services, Food and Drug Administration, Center for Veterinary Medicine. Guidance for Industry #209, The judicious use of medically important antimicrobial drugs in food producing animals. April 13, 2012. http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM216936.pdf. Accessed June 6, 2017.

*3. Guidance for Industry on new animal drugs and new animal drug combination products administered in or on medicated feed or drinking water of food-producing animals: Recommendations for drug sponsors for voluntarily aligning product use conditions with Guidance for Industry #209; Availability. Fed Regist. 2013;78(239):75570-75571.

*4. US Department of Health and Human Services, Food and Drug Administration, Center for Veterinary Medicine. Guidance for Industry #213, New animal drugs and new animal drug combination products administered in or on medicated feed or drinking water of food-producing animals: Recommendations for drug sponsors for voluntarily aligning product use conditions with GFI #209. December 2013. http://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM299624.pdf. Accessed June 6, 2017.

*5. Veterinary Feed Directive; Final Rule. Fed Regist. 2015;80(106):31708-31735. To be codified at 28 CFR §514 and §558.

6. Schulz LL, Rademacher CJ. Food and Drug Administration Guidance 209 and 213 and Veterinary Feed Directive regulations regarding antibiotic use in livestock: A survey of preparation and anticipated impacts in the swine industry. J Swine Health Prod. 2017;25(5):247-255.

*7. US Department of Agriculture, National Agricultural Statistics Service. 2012 census of agriculture, United States summary and state data. http://www.agcensus.usda.gov/Publications/2012/Full_Report/Volume_1,_Chapter_1_US/usv1.pdf. Published May 2014. Accessed June 6, 2017.

* 8. US Food and Drug Administration. 2016 summary report on antimicrobials sold or distributed for use in food-producing animals. https://www.fda.gov/downloads/forindustry/userfees/animaldruguserfeeactadufa/ucm588085.pdf. Published December 2017. Accessed July 9, 2018.

* Non-refereed references.