Antibiotic Resistance: More Information Needed to Oversee Use of Medically Important Drugs in Food Animals
Published: 2017-03-02T00:00:00

Fast Facts:
Antibiotic-resistant bacteria are one of the biggest threats to global health, sickening an estimated 2 million people in the United States each year. There is strong evidence that some resistance in bacteria is caused by antibiotic use in food animals (cattle, poultry, swine).
We found gaps in FDA's oversight of antibiotic use in food animals and USDA’s and HHS’s data collection, among other things. For example, they lack farm-specific data, do not have metrics to assess their actions to manage antibiotics use, and have not conducted on-farm investigations during foodborne illness outbreaks.
We made recommendations to address these concerns.

Highlights:
section_title: Why GAO Did This Study
paragraphs: According to the World Health Organization, antibiotic resistance is one of the biggest threats to global health. CDC estimates antibiotic-resistant bacteria cause at least 2 million human illnesses in the United States each year, and there is strong evidence that some resistance in bacteria is caused by antibiotic use in food animals (cattle, poultry, and swine). HHS and USDA are primarily responsible for ensuring food safety, including safe use of antibiotics in food animals. In 2011, GAO reported on antibiotic use and recommended addressing gaps in data collection. GAO was asked to update this information. This report (1) examines actions HHS and USDA have taken to manage use of antibiotics in food animals and assess the impact of their actions, (2) identifies actions selected countries and the EU have taken to manage use of antibiotics in food animals, and (3) examines the extent to which HHS and USDA conducted on-farm investigations of foodborne illness outbreaks from antibiotic-resistant bacteria in animal products.
GAO reviewed documents and interviewed officials and stakeholders. GAO selected three countries and the EU for review because they have taken actions to mitigate antibiotic resistance.
section_title: What GAO Found
paragraphs: Since 2011, when GAO last reported on this issue, the Department of Health and Human Services (HHS) has increased veterinary oversight of antibiotics and, with the Department of Agriculture (USDA), has made several improvements in collecting data on antibiotic use in food animals and resistance in bacteria. For example, HHS's Food and Drug Administration (FDA) issued a regulation and guidance for industry recommending changes to drug labels. However, oversight gaps still exist. For example, changes to drug labels do not address long-term and open-ended use of antibiotics for disease prevention because some antibiotics do not define duration of use on their labels. FDA officials told GAO they are seeking public comments on establishing durations of use on labels, but FDA has not clearly defined objectives for closing this gap, which is inconsistent with federal internal control standards. Without doing so, FDA will not know whether it is ensuring judicious use of antibiotics. Moreover, gaps in farm-specific data on antibiotic use and resistance that GAO found in 2011 remain. GAO continues to believe HHS and USDA need to implement a joint on-farm data collection plan as previously recommended. In addition, FDA and USDA's Animal and Plant Health Inspection Service (APHIS) do not have metrics to assess the impact of actions they have taken, which is inconsistent with leading practices for performance measurement. Without metrics, FDA and APHIS cannot assess the effects of actions taken to manage the use of antibiotics.
Three selected countries and the European Union (EU), which GAO reviewed, have taken various actions to manage use of antibiotics in food animals, including strengthening oversight of veterinarians' and producers' use of antibiotics, collecting farm-specific data, and setting targets to reduce antibiotic use. The Netherlands has primarily relied on a public-private partnership, whereas Canada, Denmark, and the EU have relied on government policies and regulations to strengthen oversight and collect farm-specific data. Since taking these actions, the use or sales of antibiotics in food animals decreased and data collection improved, according to foreign officials and data reports GAO reviewed. Still, some U.S. federal officials and stakeholders believe that similar U.S. actions are not feasible because of production differences and other factors.
HHS and USDA officials said they have not conducted on-farm investigations during foodborne illness outbreaks including those from antibiotic-resistant bacteria in animal products. In 2014, USDA agencies established a memorandum of understanding to assess the root cause of foodborne illness outbreaks. However, in 2015 in the agencies' first use of the memorandum, there was no consensus among stakeholders on whether to conduct foodborne illness investigations on farms and the memorandum does not include a framework to make this determination, similar to a decision matrix used in other investigations. According to a directive issued by USDA's Food Safety and Inspection Service, foodborne illness investigations shall include identifying contributing factors and recommending actions or new policies to prevent future occurrences. Developing a framework, in coordination with HHS's Centers for Disease Control and Prevention (CDC) and other stakeholders, would help USDA identify factors that contribute to or cause foodborne illness outbreaks, including those from antibiotic-resistant bacteria in animal products.
section_title: What GAO Recommends
paragraphs: GAO is making six recommendations, including that HHS address oversight gaps, HHS and USDA develop metrics for assessing progress in achieving goals, and USDA develop a framework with HHS to decide when to conduct on-farm investigations. USDA agreed and HHS neither agreed nor disagreed with GAO's recommendations.

section_title: Letter
paragraphs: Antibiotics are essential to treat infections caused by bacteria, and the  rise of antibiotic resistance is one of the biggest threats to global health,  according to the World Health Organization (WHO). In 2013, the U.S.  Department of Health and Human Services’ (HHS) Centers for Disease  Control and Prevention (CDC) estimated that antibiotic-resistant bacteria  cause at least 2 million illnesses and 23,000 deaths in humans each year  in the United States alone. WHO has stated that the emergence and  spread of antibiotic-resistant bacteria have been linked to the overuse  and misuse of antibiotics in veterinary and human medicine. According to  CDC’s website, there is strong evidence that some antibiotic resistance in  bacteria is caused by antibiotic use in food animals—dairy and beef  cattle, poultry (chicken and turkey), and swine raised for human  consumption. Antibiotics are used in food animals to prevent, control, and  treat disease as well as to promote efficient growth. Although any use of  antibiotics can lead to resistance, certain uses in food animals expose  bacteria to low doses of these drugs over a long period. This long-term,  low-level exposure to antibiotics may lead to the survival and growth of  resistant bacteria, according to CDC. Also, once the resistant bacteria  grow in food animals, they may pass to humans through the consumption  or handling of meat, poultry, or other food animal products; contact with  animals by farm workers or food processors; or runoff of animal waste  into water or soil used for growing food crops. This can lead to foodborne  illness, including outbreaks from resistant bacteria in animal products.  Federal agencies responding to outbreaks of foodborne illness from  pathogens, including those involving antibiotic-resistant bacteria, may  conduct investigations at the farm, slaughter processing plant, and other  points where bacteria from food animals can be transferred to the human  population.
Two federal departments are primarily responsible for ensuring the safety  of the food supply, including the safe use of antibiotics in food animals— HHS and the U.S. Department of Agriculture (USDA). Within HHS, the  Food and Drug Administration (FDA) approves for sale, and regulates the  manufacture and distribution of, antibiotics used in animals. Agencies  within USDA including the Food Safety and Inspection Service (FSIS) and  the Animal and Plant Health Inspection Service (APHIS), collect  information about antibiotic use and resistance in food animals and  educates producers and other users about appropriate antibiotic use,  respectively, among other things.
Antibiotic resistance is a global issue, and WHO and countries including  the United States have been examining the emergence of antibiotic  resistance. In January 2014, WHO recommended that the World Health  Assembly adopt a resolution on antibiotic resistance that urges countries  to take action at the national level to combat antibiotic-resistant bacteria.  In the United States, in September 2014, the President signed Executive  Order 13676, which, among other things, established the interagency  Task Force for Combating Antibiotic-Resistant Bacteria and directed agencies to use enhanced surveillance activities, as appropriate, to  prevent and respond to antibiotic-resistant outbreaks. Also, in September  2014, the President’s Council of Advisors on Science and Technology  released a report on antibiotic resistance that recommended strong  federal coordination and oversight of efforts to combat antibiotic  resistance. In March 2015, the White House released the National Action  Plan for Combating Antibiotic-Resistant Bacteria to provide a roadmap for  federal agencies’ actions and response to the rise of antibiotic-resistant  bacteria. According to the National Action Plan, implementation of the  plan supports the World Health Assembly resolution.
For more than 15 years, we have reported on federal efforts to address  the use of antibiotics in food animals and recommended actions to  improve these efforts. For example, in 2004, we found that federal  agencies needed to better focus efforts to address risk to humans from  antibiotic use in food animals. We also found that federal agencies did not  have critical data on antibiotic use in food animals that would help them  assess the relative contribution of such use to resistance in humans. To  address these gaps, we recommended that HHS and USDA develop and  implement a joint plan to collect data on antibiotic use in animals that  would adequately (1) support research on the relationship between use  and resistance, (2) help assess the human health risk related to antibiotic  use in animals, and (3) help agencies develop strategies to mitigate  antibiotic resistance. HHS and USDA generally agreed with our findings,  but they did not jointly develop a plan for data collection. In 2011, we  again found that HHS and USDA had made limited progress in  addressing antibiotic use in food animals and continued to have gaps in data collection. We recommended that the agencies take three actions:  (1) identify and evaluate approaches to collect detailed data on antibiotic  use, and utilize these data to evaluate FDA’s voluntary strategy; (2)  collect more representative data on resistance; and (3) assess previous  efforts on antibiotic alternatives to identify where research is needed.  HHS and USDA agreed with our recommendations and took several  steps to address them. However, their actions did not fully address our  recommendations to identify and evaluate approaches to collect detailed  data on antibiotic use and to assess previous efforts to identify where  research on antibiotic alternatives were needed.
You asked us to provide an update on U.S. federal agencies and other  countries’ efforts to address the use of antibiotics in food animals, among  other things. This report (1) examines actions HHS and USDA have taken  since 2011 to manage the use of antibiotics in food animals and to assess  the impact of their actions, (2) identifies actions that selected countries  and the European Union (EU) have taken to manage the use of  antibiotics in food animals, and (3) examines the extent to which HHS and  USDA have conducted on-farm investigations of outbreaks of foodborne  illness from antibiotic-resistant pathogens in animal products.
To examine actions HHS and USDA have taken since 2011 to manage  the use of antibiotics in food animals and to assess the impact of their  actions, we reviewed relevant statutes and regulations, agencies’ plans  and guidance, and stakeholders’ reports related to managing the use of  antibiotics in food animals. Also, we reviewed federal data reports on the  collection of data on antibiotic sales, use, and resistance. We compared  information from federal agencies on actions taken with federal standards  for internal controls. We identified any relevant goals, performance  measures, and targets developed by federal agencies to gauge the  impact of their efforts and compared them with agencies’ goals, National  Action Plan goals and milestones, and leading practices for improving  agency performance, specifically practices identified in the GPRA  Modernization Act of 2010 (GPRAMA) and our prior work on performance  management. We also interviewed federal officials and representatives  of stakeholder organizations—national food animal industry,  pharmaceutical (drug), veterinary, consumer advocacy, and other  groups—about federal actions taken to manage the use of antibiotics  since 2011. We also interviewed representatives of several companies  (producers and restaurants) that provide food products from animals  raised without antibiotics to obtain a better understanding of production  practices, the types of antibiotic use data available at the farm level, and  perspectives on federal efforts to educate producers about antibiotics. In  addition, we compared federal agencies’ actions with relevant goals  outlined in national and agencies’ plans and interviewed representatives  of stakeholder organizations to obtain views on agencies’ efforts taken to  date.
To identify actions that selected countries and the EU have taken to  manage the use of antibiotics in food animals, we reviewed documents  and interviewed officials from Canada, Denmark, the Netherlands, and  the EU. We selected these countries and region because they have taken  actions to mitigate antibiotic resistance.
To examine the extent to which HHS and USDA conducted on-farm  investigations of outbreaks of foodborne illness from antibiotic-resistant  pathogens in animal products, we reviewed relevant documentation,  including directives on investigations of foodborne illness outbreaks from  CDC, APHIS, and FSIS. We also reviewed a 2014 APHIS-FSIS  memorandum of understanding to access farms for investigations during  these outbreaks, as well as documentation on a 2015 Salmonella  outbreak—identified as the only outbreak in which APHIS and FSIS used their memorandum of understanding. We interviewed federal and state  officials who investigated the 2015 Salmonella outbreak. We also  interviewed federal officials about the agencies’ authority to conduct on- farm investigations during foodborne illness outbreaks, including those  involving antibiotic-resistant pathogens. Appendix I contains more  detailed information on the scope and methodology of our review.
We conducted this performance audit from August 2015 to March 2017 in  accordance with generally accepted government auditing standards.  Those standards require that we plan and perform the audit to obtain  sufficient, appropriate evidence to provide a reasonable basis for our  findings and conclusions based on our audit objectives. We believe that  the evidence obtained provides a reasonable basis for our findings and  conclusions based on our audit objectives.
subsections: section_title: Background
paragraphs: Antimicrobial drugs are a broad class of drugs that combat many  pathogens, including bacteria, viruses, fungi, or parasites. Antibiotics are  a subset of these drugs that work against bacteria. Antibiotics work by  killing the bacteria directly or halting their growth. According to WHO, the  evolution of strains of bacteria that are resistant to antibiotics is a natural  phenomenon that occurs when microorganisms exchange resistant traits;  however, WHO also states that the use and misuse of antimicrobial  drugs, including antibiotics, accelerates the emergence of resistant  strains. Antibiotic resistance began to be recognized soon after penicillin,  one of the first antibiotics, came into use over 70 years ago. Antibiotic- resistant bacteria can spread from animals and cause disease in humans  through a number of pathways (see fig. 1).
The use of antibiotics in animals is an integral part of food animal  production. To improve efficiencies, modern industrial farms raise animals  in high concentrations, but this practice has the potential to spread  disease because animals live in close confinement. Long-term, low-dose  treatments with antibiotics may help prevent diseases, particularly where  animals are housed in large groups in close confinement facilities, such  as concentrated animal feed operations. The concentrated nature of such  agricultural operations means that a disease, if it occurs, can spread  rapidly and become quickly devastating—increasing the need to rely on  antibiotics as a preventive measure.
The purposes for which FDA approves the use of antibiotics can be  divided into four categories:  to treat animals that exhibit clinical signs of disease;  to control a disease in a group of animals when a proportion of them  exhibit clinical signs of disease;  to prevent disease in a group of animals when none are exhibiting  clinical signs of disease, but disease is likely to occur in the absence  of an antibiotic; or  to promote faster weight gain (growth promotion) or weight gain with  less feed (feed efficiency).
Antibiotics for food animals are administered either by mixing them into  feed or water, or by injection and other routes. For example, according to  representatives from the poultry industry, the majority of antibiotics used  in poultry production are administered through feed and water. In lactating  dairy cattle, mastitis—an inflammation of the udder—is the most common  reason for antibiotic use and antibiotics are given by injection either to  treat or prevent disease, according to representatives from the National  Milk Producers Federation.
Antibiotics for food animals may be sold or dispensed in several ways,  with varying levels of restriction.
Some antibiotics may be purchased over-the-counter and used by  producers without veterinarian consultation or oversight.
Certain antibiotics added to feed must be accompanied by a  veterinary feed directive, a type of order for this use. The directive  authorizes the producer to obtain and use animal feed containing a  certain drug or drug combination to treat the producer’s animals in  accordance with the conditions for use approved by FDA.
Some antibiotics may require a prescription from a licensed  veterinarian.
Although veterinarians may prescribe most approved drugs “extra label”  (for a species or indication other than those on the drug label), restrictions  on the extra-label use of antibiotics in food animals exist. For example, no  extra-label use of approved drugs, including antibiotics, is legally  permissible in or on animal feed, according to FDA officials. Certain types  of drugs, including some types of antibiotics, are prohibited from extra- label use in food animals under any circumstances because the use of  these drugs may lead to antibiotic resistance in humans (e.g.,  fluoroquinolones—broad-spectrum antibiotics that play an important role  in treatment of serious bacterial infections, such as hospital-acquired  infections).
Antibiotics used for food animals can be the same, or belong to the same  drug classes, as those used in human medicine. FDA and WHO have  sought to identify antibiotics that are used in both animals and humans  and that are important to treat human infections—such antibiotics are  known as medically important antibiotics. In 2003, FDA issued guidance  to industry on the use of antibiotics in food animals, which included a list  of antibiotics that it considers important to human medicine. In this  guidance, FDA ranked each antibiotic according to its importance in  human medicine, as “critically important” (the highest ranking), “highly  important,” or “important” based on criteria that focused on antimicrobials,  including antibiotics, used to treat foodborne illness in humans. Similarly,  WHO developed criteria for ranking antimicrobials, including antibiotics,  according to their importance in human medicine and first ranked them in  2005.
Two federal departments are primarily responsible for ensuring the safety  of the U.S. food supply, including the safe use of antibiotics in food  animals—HHS and USDA. Each department contains multiple agencies  that contribute to the national effort to control, monitor, and educate  others on antibiotic use and resistance. For example, HHS’s CDC and  FDA as well as USDA’s APHIS and FSIS have responsibilities related to  the White House’s 2015 National Action Plan for Combating Antibiotic- Resistant Bacteria. The plan identifies several goals, including a goal to  slow the development of resistant bacteria and prevent the spread of  resistant infections as well as a goal to strengthen national “one-health”  surveillance efforts to combat resistance, which include collecting data on  antibiotic use and resistance. The “one-health” concept recognizes that  the health of humans, animals, and the environment are interconnected.  Table 1 provides information on selected agencies’ efforts related to  antibiotic resistance.
To help ensure public health and the safety of the food supply, HHS’s  CDC leads investigations of multi-state foodborne illness outbreaks,  including those involving antibiotic-resistant pathogens, and collaborates  with USDA, FDA, and state public health partners in this effort. To identify  an outbreak, CDC monitors data voluntarily reported from state health  departments on cases of laboratory-confirmed illness and analyzes these  data to identify elevated rates of disease that may indicate an outbreak,  according to CDC officials. According to CDC’s website, determining the  food source of human illness is an important part of improving food  safety. In general, foods often associated with foodborne illnesses include  raw foods of animal origin—meat, poultry, eggs, and shellfish, and also  unpasteurized (raw) milk—that can cause infections if undercooked or  through cross-contamination.
section_title: HHS and USDA Increased Oversight and Data Collection for Antibiotic Use in Animals, but Gaps Exist, and the Impact of These Actions Is Unknown
paragraphs: Since 2011, HHS has increased veterinary oversight of antibiotics in food  animals and, along with USDA, collected additional data on antibiotic use  and resistance, but gaps exist in oversight and data collection, and the  impact of the agencies’ efforts is unknown. For medically important  antibiotics administered in animal feed and water, HHS’s FDA increased  veterinary oversight and prohibited certain uses through a combination of  guidance and regulation. In addition, agencies in HHS and USDA made  several improvements in collecting and reporting data on antibiotic sales,  resistance, and use. However, the agencies’ actions do not address  oversight gaps such as long-term and open-ended use of medically  important antibiotics for disease prevention or collection of farm-specific  data, and FDA and APHIS do not have measures to assess the impact of  their actions.
subsections: section_title: HHS Increased Veterinary Oversight of Medically Important Antibiotics Used in Food Animals
paragraphs: To promote the judicious use of antibiotics in food animals, FDA  increased veterinary oversight of medically important antibiotics in feed  and water through voluntary guidance to industry and revising the  veterinary feed directive regulation. As a result, as of January 2017,  medically important antimicrobials, including antibiotics, in the feed and  water of food animals may only be used under the supervision of licensed  veterinarians, according to FDA officials (see app. II for a list of these  drugs).
Voluntary Guidance to Industry. In 2012, FDA finalized guidance that  lays out a strategy for phasing out the use of medically important  antibiotics for growth promotion or feed efficiency, and for bringing other  uses under veterinary oversight. Specifically, in Guidance for Industry  #209, FDA outlined and recommended adoption of two principles for  judicious use of antibiotics in food animals: (1) limit medically important  antibiotics to uses that are considered necessary for assuring animal  health, such as to prevent, control, and treat diseases, and (2) limit  antibiotic uses to those that include veterinary oversight. In 2013, to help  ensure implementation of its strategy, FDA issued Guidance for Industry  #213, which asked animal drug companies to voluntarily stop labeling  antibiotics for growth promotion or feed efficiency within 3 years. The  guidance also recommended more veterinary oversight. Specifically,  FDA (1) asked drug companies to voluntarily revise labels of medically  important antibiotics to remove the use for growth promotion and feed  efficiency; (2) outlined procedures for adding, where appropriate,  scientifically supported uses for disease treatment, control, or prevention;  and (3) recommended that companies change the means of sale or  dispensation from over-the-counter to require veterinary oversight—either  through a veterinary feed directive for antimicrobials administered through  feed or through a prescription for antimicrobials administered through  water—by December 31, 2016. According to FDA, as of January 3, 2017,  all applications for medically important antimicrobials, including  antibiotics, for use in the feed or water for food animals have been  aligned with the judicious use principles as recommended in Guidance for  Industry #213, or their approvals have been voluntarily withdrawn.  As a  result of these actions, these products cannot be used for production  purposes (e.g., growth promotion) and may only be used under the  authorization of a licensed veterinarian, according to FDA.
Agencies Respond to Colistin Resistance  In May 2016, the U.S. Department of Defense  identified the first person in the United States  to be carrying E.coli bacteria with a gene that  makes bacteria resistant to colistin. The U.S.  Department of Agriculture (USDA) also found  colistin-resistant E. coli in samples collected  from the intestines of two pigs. According to  the U.S. Department of Health and Human  Services (HHS), these discoveries are of  concern because colistin is used as a last- resort drug to treat patients with multidrug-  resistant infections. Finding colistin-resistant  bacteria in the United States is important  because in 2015 scientists in China first  reported that colistin resistance can be  transferred across bacteria via a specific  gene. HHS and USDA are continuing to  search for evidence of colistin-resistant  bacteria in the United States through the  National Antimicrobial Resistance Monitoring  System, according to the HHS website.  According to officials from HHS’s Centers for  Disease Control and Prevention, the agency is  also expanding the capability of public health  laboratories to conduct surveillance.
Guidance for Industry #213 further defined medically important  antimicrobials, including antibiotics, as those listed in FDA’s ranking of  drug classes and class-specific products based on importance to human  medicine. According to FDA officials, the agency plans to update this list  in the near future, and the update will address whether to add or remove  drug classes and class-specific products, as well as the need to update  the relative rankings of these drug classes and class-specific products.  Colistin—an antibiotic used as the last line of medical treatment for  certain infections—is not listed in the ranking of drugs and drug classes.  However, according to FDA officials, the ranking of a closely related drug  (polymixin B) covers colistin’s relative importance to human medicine and  colistin has never been marketed for use in animals in the United States.
Veterinary Feed Directive Final Rule. In light of the 2013 guidance  asking animal drug companies to change the labels of medically  important antibiotics to bring them under veterinary oversight (Guidance  for Industry #213), in June 2015, FDA issued a final rule revising its  existing veterinary feed directive regulation to define minimum  requirements for a valid veterinarian-client-patient relationship, among  other things. The final rule requires a licensed veterinarian to issue the  directive in the context of a valid veterinarian-client-patient relationship as  defined by the state where the veterinarian practices medicine or by the  federal standard in the absence of an appropriate state standard that  applies to veterinary feed directive drugs. There are three key elements of  the veterinarian-client-patient relationship: (1) the veterinarian engages  with the client (e.g., animal producer) to assume responsibility for making  clinical judgments about animal health, (2) the veterinarian has sufficient  knowledge of the animal by virtue of an examination and visits to the  facility (e.g., farm) where the animal is managed, and (3) the veterinarian  provides for any necessary follow-up evaluation or care. The veterinarian  is also responsible for ensuring the directive is complete and accurate.  For example, the directive must include the approximate number of  animals to be fed the medicated feed. The final rule also (1) established a  6-month expiration date for directives unless an expiration date shorter  than 6 months is specified in the drug’s approved labeling; (2) limited  refills to those listed on the product’s label; and (3) established a 2-year  recordkeeping requirement for producers, veterinarians, and feed  distributors.
section_title: HHS and USDA Have Gathered Additional Data about Antibiotic Sales, Resistance, and Use in Animals
paragraphs: Since 2011, agencies within HHS and USDA have made several  improvements in collecting and reporting data on antibiotic sales,  resistance, and use.
subsections: section_title: Sales Data
paragraphs: In 2014, FDA enhanced its annual summary report on antimicrobials sold  or distributed for use in food animals. The enhanced annual report  includes additional data tables on the importance of each drug class in  human medicine; the approved routes of administration for antibiotics;  whether antibiotics are available over-the-counter or require veterinary  oversight; and whether the drug products are approved for therapeutic  (disease prevention, control, or treatment) purposes, production purposes  (e.g., growth promotion), or both therapeutic and production purposes. In  2016, FDA finalized a rule requiring drug companies to report sales and  distribution of antimicrobials, including medically important antibiotics  approved for use in specific food animals (cattle, swine, and poultry— chickens and turkeys) based on an estimated percentage of total annual  sales. According to FDA documents, the additional data will improve  FDA’s understanding of how antibiotics are sold or distributed for use in  food animals and help the agency further target its efforts to ensure  judicious use of medically important antibiotics. Before the rule was  finalized, however, some organizations cautioned that the proposed  requirement for drug companies to submit species-specific estimates of  antibiotic product sales and distribution for use in food animal species  would not result in useful data, in part, because sales are not a proxy for  antibiotic use. FDA’s action partially addressed our 2011 recommendation  to provide sales data by food animal group and indication for use.
section_title: Antibiotic Resistance Data
paragraphs: Federal agencies have made several improvements to the National  Antimicrobial Resistance Monitoring System—the national public health  surveillance system that tracks changes in the antibiotic susceptibility of  bacteria found in ill people, retail meats, and food animals. Specifically,  beginning in 2013, FSIS collected random samples from animal intestines  at slaughter plants, including chickens, turkeys, swine, and cattle, in  addition to non-random sampling under its regulatory program. In 2013,  FDA also expanded its retail meat sampling to collect data from  laboratories in three new states: Louisiana, Missouri, and Washington.  This increased the number of states from 11 to 14. In addition, FDA  increased retail meat samples from 6,700 in 2015 to 13,400 in 2016 by  requiring the 14 participating laboratories to double the amount of food  samples purchased and tested. In 2017, FDA plans to add another five  states (Iowa, Kansas, South Carolina, South Dakota, and Texas) to retail  meat testing, which will raise the total retail meat samples to more than  17,000 annually, according to FDA officials. FSIS and FDA actions addressed our recommendation from 2011 to modify slaughter and retail  meat sampling to make the data more representative of antibiotic  resistance in bacteria in food animals and retail meat throughout the  United States. Figure 2 summarizes the data collected through the  National Antimicrobial Resistance Monitoring System.
Since 2011, FDA in collaboration with USDA’s Agricultural Research  Service has also initiated pilot projects to explore antibiotic-resistant  bacteria on the farm and at slaughter for each major food animal group  (swine, beef and dairy cattle, chickens, and turkeys). The purpose of the  pilot projects was (1) to begin assessing similarities and differences  between bacteria and antibiotic resistance on the farm and at the  slaughter plant and (2) to determine the feasibility and value of  surveillance on farms as a possible new element of the National  Antimicrobial Resistance Monitoring System, including the collection of  antibiotic use information from farms in a confidential manner. To collect  data from farms, federal agencies collaborated with academia to obtain  data from producers. According to FDA officials, USDA can use  information from the pilot projects to determine options for examining  antibiotic resistance in a group of food animals over time (e.g.,  longitudinal on-farm studies).
In 2016, for the first time, CDC, FDA, and USDA published the National  Antimicrobial Resistance Monitoring System report with data from whole  genome sequencing—cutting-edge technology which characterizes an  organism’s (individual bacterium) complete set of genes. According to  FDA officials, this represents a very significant advancement in  surveillance that will provide definitive information about the genes  causing resistance, including resistance compounds not currently  fingerprinted, along with details on other important features of a  bacterium. In addition, new reporting tools are being deployed to foster  timely data sharing via web tools and they allow stakeholders to explore  isolate-level antibiotic-resistance data in new ways. For example, in  August 2015, FDA made available on its website 18 years of National  Antimicrobial Resistance Monitoring System isolate-level data on  bacteria.
section_title: Antibiotic Use Data
paragraphs: Since 2011, USDA agencies have collected additional antibiotic use data  through national surveys of producers and engaged in efforts to leverage  industry data. In particular, APHIS, through the National Animal Health  Monitoring System, collected additional antibiotic use data through its  national survey of producers of dairy cattle (2011 and 2014), beef cattle  (2011), laying hens (2013), and swine (2012). Using these surveys,  generally APHIS collects information on the amount and duration of  antibiotic use; reason for use; antibiotic name; and the route of  administration, such as feed, water, and injection; among other things.  APHIS also may collect biological samples from animals and test these  samples for antibiotic resistance of foodborne pathogens; producers  receive results of biological sample testing. According to APHIS officials,  the agency is planning to collect data annually on antibiotic use on swine  farms and beef cattle feedlots using similar surveys, with additional  questions on stewardship and judicious use of antibiotics.
USDA’s Economic Research Service and National Agricultural Statistics  Service also conducted national surveys of producers of swine (2015)  and chicken (2011) to collect data on farm finances and production  practices, including antibiotic use. The surveys were components of the  annual Agricultural Resource Management Survey, which is primarily  focused on farm finances, commodity costs of production, and farm  production practices. The surveys captured quantitative information on  the extent of antibiotic use and the types of farms that use antibiotics for  growth promotion and prevention. USDA has used these data to estimate  the impact of antibiotic use on production outcomes.
Furthermore, APHIS provided input on a survey as part of the poultry  industry effort begun in 2015 to develop a survey to collect farm-specific  data. Representatives from the poultry industry told us that they plan to  share aggregated survey data with APHIS and FDA when the data  collection and report are finalized.
section_title: Gaps Exist in Oversight of Antibiotics and Persist in Farm-Specific Data
paragraphs: Despite agencies’ enhanced oversight and data collection efforts, several  gaps exist in the oversight of medically important antibiotics in food  animals—specifically, antibiotics with no defined duration of use on their  labels and antibiotics administered by routes other than feed and water  (e.g., injection). Moreover, gaps that we identified in 2011 in farm-specific  data on antibiotic use and resistance in bacteria persist.
subsections: section_title: Gaps in Oversight of Antibiotics in Food Animals
paragraphs: FDA’s guidance to industry has improved oversight of some antibiotics,  but it does not address long-term and open-ended use of medically  important antibiotics for disease prevention because some antibiotics do  not have defined durations of use on their labels. For example, some  currently approved labels do not have defined duration of use such as  “feed continuously for 5 days”; instead labels may read “feed  continuously,” according to FDA officials. In September 2016, FDA issued  a notice in the Federal Register seeking public comment on how to  establish appropriately targeted durations of use for medically important  antimicrobial drugs including the approximately 32 percent of therapeutic  antibiotic products affected by Guidance for Industry #213 with no defined  duration of use. FDA officials told us the agency will consider public  comments as it develops a process for animal drug companies to  establish appropriate durations of use for labels already in use.  However, FDA has yet to develop this process, including time frames for  implementation. In an October 2016 report, one stakeholder organization  recommended that FDA announce a plan and timeline for making all label  revision changes regarding duration limits and other aspects of  appropriate use as quickly as possible to ensure labels follow the  judicious use of antibiotics in food animals. Under federal standards for  internal control, management should define objectives clearly to enable  the identification of risk and define risk tolerances; for example, in  defining objectives, management may clearly define what is to be  achieved, who is to achieve it, how it will be achieved, and the time  frames for achievement. Without developing a process, which may  include time frames, to establish appropriate durations of use on labels of  all medically important antibiotics, FDA will not know whether it is  achieving its objective of ensuring judicious use of medically important  antibiotics in food animals.
FDA’s Guidance for Industry #213 also does not recommend veterinary  oversight of over-the-counter medically important antibiotics administered  in injections or through other routes besides feed and water (e.g., tablets).  According to FDA officials, the agency focused first on antibiotics  administered in feed and water because officials believed these  antibiotics represent the majority of antibiotics sold and distributed and  therefore they posed a higher risk to human health. According to FDA’s  2014 sales data report on antimicrobials, approximately 5 percent of  medically important antibiotics are sold for use in other routes.
Representatives of two veterinary organizations we interviewed support  veterinary oversight of medically important antibiotics administered by  other routes such as injections. In October 2016, FDA officials told us the  agency is developing a plan that outlines its key activities over the next 5  years to further support antimicrobial stewardship in veterinary settings,  including addressing veterinary oversight of other dosage forms of  medically important antibiotics. According to FDA officials, the agency  intended to publish the plan by the end of 2016 and to initiate steps by the  end of fiscal year 2019. However, FDA was unable to provide us with this  plan or specifics about the steps outlined in the plan because it was still  under development. In the interim, on January 3, 2017, FDA broadly  outlined on its website its key initiatives to support antimicrobial  stewardship in veterinary settings, but it does not provide enough detail to  know if steps will be established to increase veterinary oversight of  medically important antibiotics administered in routes other than feed and  water. As previously discussed, under federal standards for internal  control, management should define objectives clearly to enable the  identification of risk and define risks tolerances; for example, in defining  objectives, management may clearly define what is to be achieved and  the time frames for achievement, among other things. Without a  published plan documenting the steps to increase veterinary oversight of  medically important antibiotics administered through routes other than  feed and water, such as injections and tablets, FDA will not know whether  it is making progress in achieving its objective of ensuring judicious use of  medically important antibiotics in food animals.
Stakeholders we spoke with also identified and reported other potential  gaps in FDA’s actions to increase veterinary oversight, such as (1) gaps  in oversight of antibiotics used for disease prevention and (2) gaps in  some producers’ knowledge of FDA’s actions and in their access to  veterinarians.
Representatives of consumer advocacy organizations told us the use  of antibiotics for disease prevention in food animals is a problem  because it promotes the routine use of antibiotics in healthy food  animals. According to FDA documents, the agency believes that the  use of antibiotics for disease prevention is necessary to assure the  health of food animals and that such use should be appropriately  targeted to animals at risk for a specific disease. Some producers and  companies have already taken steps to eliminate the use of medically  important antibiotics in food animals, including uses for disease  prevention. For example, we interviewed representatives from  companies (restaurant and producers) that sell meat and poultry  products with “no antibiotic use” label claims, denoting products from  animals raised without the use of any antibiotics or medically  important antibiotics, even for disease prevention (see app. III for  more information on companies’ efforts).
In 2016, the Farm Foundation summarized findings from 12  workshops on FDA’s actions and one of the findings was that small- and medium-sized producers did not have sufficient knowledge about  FDA’s actions to increase veterinary oversight of medically important  antibiotics. In addition, some producers may lack access to  veterinarians. In 2015, FDA announced the availability of a guidance  document in the form of answers to questions about veterinary feed  directive final rule implementation to help small businesses, including  producers, comply with the revised regulation. According to FDA  officials, the agency continues to respond to questions from  stakeholders regarding the use of medically important antimicrobials,  including antibiotics, in food animals and has planned numerous  outreach activities in 2017.
section_title: Gaps in Farm-Specific Data Persist
paragraphs: Gaps in farm-specific data on antibiotic use and resistance in food  animals persist since we last reported on this in 2011. Agencies are  making efforts to address these gaps, but they are doing so without a joint plan, as we previously recommended. A joint plan is necessary to further  assess the relationship between antibiotic use and resistance in bacteria,  and it could help ensure efficient use of resources in a time of budget  constraints. In 2004 and 2011, we found numerous gaps in farm-specific  data stemming from limitations in the data collected by the agencies. In  this review, we found that the limitations we identified in 2011 remain, and  that data gaps have not been fully addressed. For example, according to  CDC officials, there are still critical gaps in antibiotic use data, including  the amount and specific types of antibiotics used across the various food  animals and the indications for their use; these data are needed to further  assess the relationship between antibiotic use and resistance in bacteria.  Moreover, these data are important for assessing the impact of actions  being implemented by FDA to foster the judicious use of medically  important antimicrobial drugs, including the use of antibiotics in food  animals, according to FDA officials. Table 2 shows limitations in federal  efforts to collect farm-specific data on antibiotic use and resistance in  bacteria in food animals.
HHS and USDA are making individual efforts to gather additional data on  antibiotic use and resistance at the farm level, but officials stated that they  face funding constraints. For example, in 2014, APHIS proposed  initiatives as part of USDA’s plan to improve collection of antibiotic use  and resistance data on farms, including enhancements to two on-farm  surveys and the initiation of longitudinal on-farm studies to collect data  across time on antibiotic use, antibiotic resistance in bacteria, and  management practices. According to USDA’s fiscal year 2016 budget  summary and annual performance plan, the President’s budget included  a $10 million increase for APHIS’ contribution to the government-wide  initiative to address antimicrobial resistance. APHIS would have used the  increased funding to implement the farm-specific data collection  initiatives, according to APHIS officials. However, according to USDA’s  Office of Inspector General, the funding was not approved. As noted  above, in 2016 APHIS developed study designs for the two proposed on- farm surveys for antibiotic use on cattle feedlots and at swine operations,  but the agency has not collected data because, according to USDA,  additional funding has not been secured. In March 2016, USDA’s Office  of Inspector General found inadequate collaboration in USDA’s budget  process to request funds for antibiotic resistance efforts and  recommended that the Agricultural Research Service, FSIS, and APHIS  work together to establish antibiotic resistance priorities related to budget  requirements that also communicate agency interdependency.  Subsequently, APHIS collaborated with FSIS and the Agricultural  Research Service in developing its fiscal year 2017 budget request to  increase the likelihood of receiving funding.
Similarly, according to the fiscal year 2016 HHS’s FDA justification of  estimates for appropriations committees, the President requested a  funding increase of $7.1 million for FDA to achieve its antibiotic  stewardship goals, including collection of data related to the use of  antibiotics in food animals. According to the Presidential Advisory Council  on Combating Antibiotic-Resistant Bacteria, however, FDA did not receive  those funds. According to FDA, using existing fiscal year 2016 funds, in  March 2016, the agency made some progress in data collection and  issued a request for proposals to collect antibiotic use and resistance  data on farms. In August 2016, FDA entered into two cooperative  agreements with researchers for antibiotic use and resistance data collection; the awardees will develop a methodology to collect detailed  information on antibiotic drug use in one or more of the major food animal  groups (cattle, swine, chickens, and turkeys), according to FDA officials.  The data collection efforts are expected to provide important information  on data collection methodologies to help optimize long-term strategies for  collecting and reporting such data, according to FDA officials. Moreover,  FDA, CDC, and USDA formed a working group and proposed an analytic  framework to associate foodborne bacteria resistance with antibiotic use  in food animals.
However, the agencies are conducting these efforts without a joint data  collection plan, thus risking inefficient use of their limited resources. In  2004, we recommended that HHS and USDA jointly develop and  implement a plan for collecting data on antibiotic use in food animals. In  addition, in 2011, we recommended that HHS and USDA identify potential  approaches for collecting detailed data on antibiotic use in food animals,  collaborate with industry to select the best approach, seek any resources  necessary to implement the approach, and use the data to assess the  effectiveness of policies to curb antibiotic resistance. HHS and USDA  generally agreed with our recommendations but have still not developed a  joint plan or selected the best approach for collecting these data. HHS  and USDA officials told us they are continuing to make progress towards  developing a joint data collection plan but that funding has been an  impediment. In September 2015, FDA, CDC, and USDA agencies,  including APHIS, held a jointly sponsored public meeting to present  current data collection efforts and obtain public input on possible  approaches for collecting additional farm-specific antibiotic use and  resistance data. In June 2016, FDA stated that it is collaborating with  USDA and CDC to develop the data collection plan and is still reviewing  September 2015 public comments on data collection; however, the  continued lack of funding will significantly impact the ability to move  forward with a plan, according to FDA, APHIS, and CDC officials.
The White House’s 2015 National Action Plan for Combating Antibiotic- Resistant Bacteria calls for agencies to strengthen one-health  surveillance through enhanced monitoring of antibiotic-resistance  patterns, as well as antibiotic sales, usage, and management practices, at  multiple points in the production chain for food animals and retail meat.
Moreover, in the 1-year update on the National Action Plan, the  President’s task force recommended that federal agencies coordinate  with each other to ensure maximum synergy, avoidance of duplication,  and coverage of key issues. It is unclear whether FDA, CDC, and APHIS  will develop a joint plan to collect antibiotic use and resistance data at the  farm level and whether agencies’ individual current data collection efforts  are coordinated to ensure the best use of resources. We continue to  believe that developing a joint plan for collecting data to further assess  the relationship between antibiotic use and resistance in bacteria at the  farm level is essential and will help maximize resources and reduce the  risk of duplicating efforts at a time when resources are constrained.
section_title: FDA and APHIS Do Not Have Measures to Assess the Impact of Actions Taken
paragraphs: FSIS has developed a performance measure to assess the impact of its  actions to manage the use of antibiotics in food animals, but FDA and  APHIS have not done so. The GPRA Modernization Act of 2010  requires federal agencies such as HHS and USDA to develop and report  performance information—specifically, performance goals, measures,  milestones, and planned actions. We have previously found that these  requirements can also serve as leading practices for planning at lower  levels (e.g., FDA and APHIS) within agencies; moreover, developing  goals and performance measures can help an organization balance  competing priorities, particularly if resources are constrained, and help an  agency assess progress toward intended results. Numerical targets are  a key attribute of performance measures because they allow managers to  compare planned performance with actual results.
In this context, FSIS’s performance measure, included in its fiscal year  2017-2021 strategic plan, relates to sampling of antibiotic-resistant  bacteria. Specifically, the performance measure is the percentage of  FSIS slaughter meat and poultry samples that will undergo whole genome  sequencing, including antibiotic-resistance testing, to assess the impact  of the agency’s surveillance of antibiotic-resistant bacteria in slaughtered  food animals.
FDA and APHIS officials agree that performance measures are needed to  assess the impact of their actions to manage the use of antibiotics in food  animals. According to the White House’s 2015 National Action Plan for  Combating Antibiotic-Resistant Bacteria, metrics should be established  and implemented to foster stewardship of antibiotics in food animals  within 3 years. FDA has a goal to enhance the safety and effectiveness of  antibiotics and an objective to reduce risks in antibiotics by supporting  efforts to foster the judicious use of medically important antibiotics in food  animals. FDA’s actions to achieve this objective include developing  voluntary guidance to industry and revising its veterinary feed directive  regulation, as noted above. However, FDA does not yet have  performance measures to assess the impact of these actions in achieving  its goal and objective even though its revised regulation has already been  implemented and actions recommended in its guidance were  implemented as of January 2017. FDA officials told us the agency is  taking steps to develop performance measures. In July 2016, FDA began  reaching out to APHIS and producer groups to collaboratively develop  metrics, according to FDA and APHIS officials. Furthermore, according to  agency officials, FDA is collecting data in a pilot program for the  veterinary feed directive to establish a baseline for compliance, which is  needed to develop a measure. FDA officials told us developing  measures is a challenge without funding to support farm-specific data to  assess changes in antibiotic use practices and adherence to its guidance  documents. It is unclear when FDA’s efforts to develop performance  measures will be completed. Without developing performance measures  and targets for its actions, FDA cannot assess the impact of its guidance  to industry and its revised regulation in meeting the goal of enhancing the  safety and effectiveness of antibiotics by fostering the judicious use of  medically important antibiotics in food animals.
Similar to FDA, APHIS does not have performance measures to assess  the impact of its antibiotic use and resistance data collection efforts. In  March 2016, APHIS agreed to develop goals and identify measures for its  antibiotic resistance efforts by March 2017 as recommended by the  USDA Office of Inspector General. However, little progress has been  made. According to APHIS officials, if the agency does not receive new  funding in fiscal year 2017 for antibiotic use and resistance activities,  development of related goals and measures will be delayed. According to  USDA’s 2012 report on antibiotic resistance, few useful metrics (i.e.,  performance measures) exist for gauging progress toward stated data  collection goals. The report also stated that having defined metrics  available would allow more appropriately focused efforts for monitoring  antibiotic use and resistance and allow greater “buy in” among  stakeholder groups for the monitoring efforts and their resulting actions.  APHIS officials told us that performance measures and targets are  needed and in July 2016, the agency began discussions with FDA and  others about developing metrics, as noted above. Without developing  performance measures and targets for its actions, APHIS cannot assess  the impact of collecting farm-specific data on antibiotic use and resistance  in meeting its goal to protect agricultural resources through surveillance  for antibiotic-resistant bacteria.
section_title: Selected Countries and the EU Have Taken Various Actions to Manage Use of Antibiotics
paragraphs: To manage the use of antibiotics in food animals and combat the  emergence and spread of antibiotic-resistant bacteria, the Netherlands,  Canada, Denmark and the EU have taken actions to strengthen the  oversight of veterinarians’ and producers’ use of antibiotics and to collect  farm-specific data. In addition, the Netherlands and Denmark have set  targets for reducing the use of antibiotics, and the EU has called for  measurable goals and indicators for antimicrobial use and resistance.
subsections: section_title: For Oversight and Data Collection, the Netherlands Relied on a Public-Private Partnership, and the EU and Other Countries Used Government Policies and Regulations
paragraphs: To strengthen oversight and collect farm-specific data on antibiotic use in  food animals, the Netherlands primarily relied on a public-private  partnership, whereas Canada, Denmark, and the EU relied on  government policies and regulations. After taking these actions, the use  or sales (depending how the data were reported) of antibiotics for food  animals decreased in Denmark, the Netherlands, and the EU, and data  collection on antibiotic use improved in all three countries and the EU.
subsections: section_title: Netherlands
paragraphs: Beginning in 2008, the Netherland’s food animal (cattle, veal, chicken,  and swine) industries, national veterinary association, and government  developed a public-private partnership to strengthen oversight of  veterinarians’ prescriptions and producers’ use of antibiotics. This  partnership was also used to collect farm-specific data. Government  officials we interviewed from the Ministries of Health and Economic Affairs  told us that in the past the Netherlands was one of the highest users of  antibiotics in food animals in Europe. As a result of the partnership’s  actions, from 2009 through 2015, antibiotic sales fell by over 50 percent,  according to government documents. As part of the partnership,  industry strengthened oversight of producers’ use of antibiotics through  quality assurance programs—producer education and certification  programs that set standards for animal production including the use of  antibiotics—and the national veterinary association established additional  guidelines and policies for veterinarians. According to the Ministry of  Economic Affairs, building on these actions, the government adopted new  statutes and regulations that incorporated some of the oversight activities  that industry and veterinary organizations had established, such as  restricting the use of antibiotics that are important to human health,  implementing herd health plans, and developing prudent use guidelines.  Similar to the Netherlands, U.S. producers and veterinarians participate in  quality assurance programs and take action to promote judicious use of  antibiotics, according to documents we reviewed from U.S. industry and  veterinarian organizations. For example, some producers in the United  States stopped the use of antibiotics for growth promotion prior to U.S.  government action. The public-private partnership in the Netherlands also  established a process for the continuous collection of farm-specific  antibiotic use data. Specifically, in 2011, the different food animal  industries and veterinary organizations leveraged their existing processes  and infrastructure to create one centralized database for veterinarians  and producers to report antibiotic prescriptions and use. In contrast, the  United States relies primarily on an on-farm survey to collect antibiotic  use data on a specific food animal every 5 to 7 years, as noted above.
In 2010, the Netherlands’ government, food animal industries, and  national veterinary association jointly financed an independent entity, the  Netherlands Veterinary Medicines Authority, to analyze antibiotic use data  and veterinary prescription patterns to produce annual antibiotic use  reports, according to Dutch government documents. Representatives  from the independent entity told us that the Netherlands’ government  funds 50 percent of the cost and the food animal industries and  veterinarians fund the remaining 50 percent. The Netherlands Veterinary  Medicines Authority uses the data submitted by producers and  veterinarians to define annual benchmarks regarding both the quantity  and the types of antibiotics used within each sector. The industries use  this information to monitor producers’ antibiotic use and veterinarians’  prescriptions, and they work with individuals who exceeded the  benchmark to reduce use. According to Dutch government documents  and officials, anonymized and aggregated data—including the amounts of  antibiotics given, types of antibiotics, and number of animals that each  veterinarian oversees—are shared with government for a variety of  purposes, such as annual reports and other studies. Additionally, in 2016  the Netherlands Veterinary Medicines Authority published a report finding  that reductions in antimicrobial usage, including antibiotics, were  associated with reductions in the prevalence of antimicrobial-resistant  E.coli in fecal samples from veal, calves, pigs, and young chickens.  Dutch government officials told us that moving forward a variety of issues  must be addressed, including overuse of antibiotics by veterinarians and  producers—for example, in the veal and cattle sectors, which are  challenged in decreasing antibiotics while keeping animals healthy.  Similarly, a representative from a veterinary organization told us that  under the new policies, veterinarians are challenged with greater  administrative and record-keeping burdens. The Netherlands’  collaboration with industry is similar to some actions taken in the United  States, such as the U.S. poultry industry’s effort to develop an on-farm  antibiotic use survey and its plan to share aggregate survey data with  APHIS and FDA, as discussed above. Additionally, FDA is actively  engaging stakeholders to leverage public-private partnerships and  collaboration to collect farm-specific data, according to FDA officials.  However, the United States has no practice comparable to benchmarking.  According to APHIS officials, benchmarking and measuring producers’  use and veterinarians’ prescriptions of antibiotics would require major  infrastructure and technological investments for data capture, analysis,  and reporting, and for educating producers and veterinarians regarding  use of the data. According to representatives from an animal health  company, it may not be feasible for the United States to adopt practices  from the Netherlands because it would require similar or equal veterinary  practice laws across all states.
section_title: Canada
paragraphs: The Canadian government is working toward integrating federal and  province-level policies on antibiotic use and collects farm-specific  antibiotic use and resistance data on some species. The 2015 Canadian  national action plan on antibiotic use and resistance calls for integration of  federal-level and province-level policies and lists specific activities along  with completion dates. Officials we interviewed from a Canadian food  safety agency told us that Canada is developing a framework to align  national and province-level veterinary oversight efforts and increase  collaboration between these levels of government. Additionally, officials  from a Canadian agency that regulates medical products told us that the  federal government is working on a policy initiative to increase veterinary  oversight over all medically important antimicrobials used in food animal  production and that, as part of this initiative, they are working with  provinces to ensure the streamlined transition of over-the-counter  medically important antibiotics to prescription status.
The national action plan also identifies the need for continued  government support of industry-led quality assurance programs that  address judicious use of antibiotics in food animals. For example, the  Chicken Farmers of Canada’s On-Farm Food Safety Assurance program  requires producers to keep records, called flock sheets, on each chicken  flock. These sheets capture information related to animal health, including  any antibiotics given to the bird during production, and must be presented  prior to slaughtering. This differs from the United States where the poultry  industry is vertically integrated—meaning that individual poultry  companies own or contract for all phases of production and processing.  Because of this integration, flock health information and production  practices in the United States, including antibiotics used in feed or  administered by a veterinarian, are maintained by the poultry company  and not individual farmers. The national action plan also states that  Canada is working toward removing growth promotion claims on  antibiotics labels, similar to the U.S. approach, and that the  pharmaceutical industry has voluntarily committed to comply by  December 2016.
According to one Canadian government official, data on antibiotic use in  food animals have improved in recent years as a result of refinements to  antibiotic sales data as well as farm-specific monitoring of antibiotic use in  chickens, which has allowed officials to observe a relationship between  changes in antibiotic use and resistance. For example, current data from  the Canadian Integrated Program for Antimicrobial Resistance  Surveillance show changes in resistant bacteria, isolated from chickens,  associated with an intervention led by the poultry industry that focused on  reducing the preventative use of a type of antibiotic called cephalosporin,  according to Canadian government documents. According to an official  from the Canadian Integrated Program for Antimicrobial Resistance  Surveillance that we interviewed, the Canadian system is similar to the  National Antimicrobial Resistance Monitoring System in the United  States; however, unlike the U.S. system, the Canadian system has a farm  surveillance component that captures information on antibiotic use,  antibiotic resistance, and farm characteristics. The 2013 annual report  from the Canadian Integrated Program for Antimicrobial Resistance  Surveillance states that Canada initiated this surveillance component in a  sample of farms in five major pork-producing provinces and in four major  poultry-producing provinces in 2006 and 2013, respectively. In 2014, a  total of 95 swine farms and 143 chicken farms participated in this  voluntary program, according to the most recent (2014) annual report.  The Canadian government compensates veterinarians to collect samples  and gather data from each participating farms, according to a Canadian  government official. Representatives from a veterinary organization we  interviewed told us that surveillance data are good for looking at trends  but that such data are limited and not appropriate to determine whether a  producer is misusing antibiotics. One representative of the swine industry  similarly told us that data collected from sample pig farms are limited and,  to be more statistically representative of the industry, should be  broadened to be more geographically representative and cover all types  of pig production. While the Canadian farm surveillance program does not  currently monitor antibiotic use and resistance in beef cattle on farms, the  Canadian beef industry has funded research to develop an on-farm data  collection framework and would welcome the addition of farm-specific  antibiotic use and resistance surveillance to the program, according to  representatives from a Canadian beef industry group we interviewed.  Similar to the Canadian farm surveillance program, United States  producers voluntarily participate in periodic surveys to provide antibiotic  use data at the farm level, as part of National Animal Health Monitoring  System; however, no U.S. program conducts longitudinal studies to  collect data across time on antibiotic use, as noted above.
section_title: Denmark
paragraphs: Since we reported on Denmark’s actions to regulate antibiotic use in  2011, Denmark has developed a variety of policies focused on both  producers’ and veterinarians’ use of antibiotics and has continued to  monitor levels of antibiotic use, according to Danish government  documents we reviewed and officials we interviewed. For example,  officials from the Danish Veterinary and Food Administration explained  that in 2013, they implemented a tax on the sale of antimicrobials,  including antibiotics, and other drugs used in veterinary medicine. They  told us that the initiative aims to strengthen veterinarians’ and producers’  incentive to choose alternatives to antimicrobial, including antibiotic,  treatment or to choose the most responsible antimicrobial or antibiotic  treatment—using antibiotics judiciously. One Danish industry  representative told us that it is yet to be determined if the tax will be  effective in reducing use, and that a high tax may lead to the illegal import  of antibiotics. Officials from the Danish Veterinary and Food  Administration also explained that other actions since 2011 include the  introduction of legislation in 2014 on the treatment of swine herds. They  stated that when veterinarians prescribe antibiotics to be administered  through feed or water for respiratory or gastrointestinal infections,  veterinarians must take samples from the herd for laboratory testing to  verify the clinical diagnosis. Officials from the Danish Veterinary and Food  Administration also indicated that Denmark has leveraged voluntary  industry initiatives to manage the use of antibiotics, such as the cattle  industry’s ban on the use of an antibiotic deemed critically important to  human medicine. Denmark continues to collect farm-specific antibiotic  use data through veterinary prescriptions and reports results along with  resistance data annually via the Danish Integrated Antimicrobial  Resistance Monitoring and Research Program, according to Danish  government documents and officials. The most recent report states that  antibiotic consumption was 47 percent lower in 2015 than in 1994 and  decreased slightly from 2014 through 2015. As we previously reported,  the lower levels of antibiotic beginning after 1994 coincide with changes  to government policies on growth promotion and veterinarians’ sales  profits. Representatives of U.S. industry and veterinary organizations  we interviewed questioned whether the actions taken by Denmark were  successful. They said while antibiotic use decreased, Denmark  experienced issues with animal welfare, such as greater levels of  disease, and increased the use of antibiotics for disease treatment.  Danish officials acknowledged the concerns for animal welfare associated  with reductions in antibiotic use, but documents they provided stated that  they have not seen any evidence of decreased animal welfare or  increases in infection prevalence. Representatives from a U.S. food  industry organization and a veterinary organization told us that actions  taken by Denmark are not feasible in the United States because of  differences between the countries. For example, the food production  industries in Denmark are different in size and production volume when  compared with those in the United States, according to representatives  from the U.S. poultry industry.
Since 2011, when we last reported on the EU’s efforts, the EU has  developed an antibiotic-resistance action plan, reported reductions in  sales of antibiotics, and made associations between antibiotic use and  resistance in a new report. The EU action plan calls for various actions to  strengthen judicious use, oversight, and surveillance of antibiotics.  According to EU documents, steps taken to implement the plan include,  publishing guidelines for prudent use of antibiotics in veterinary medicine  in 2015, enacting an animal health law in March 2016 that emphasizes  prevention of disease rather than cure, and revising legislation for  veterinary medicinal products and for medicated feed. In 2011, we  reported on EU efforts to collect sales data; at that time only nine  European countries had submitted data. For the 2016 report on EU sales,  29 European countries had submitted data, and the data show that from  2011 to 2014 sales of antibiotics for use in animals fell by approximately 2  percent in 25 European countries. One difference between the United  States and the EU is the classification of certain antimicrobials, including  antibiotics, in sales reports; for example, in the EU a group of medications  called ionophores are not included in antimicrobial sales reports, but in  the United States ionophores are included.
According to EU documents we reviewed, other actions since 2011  include activities to promote the collection of on farm data, mainly through  developing guidance and a pilot project. For example, a report from the  European Medicines Agency, an agency within the EU, describes a trial  conducted in 2014 to test a protocol and template for data collection on  antimicrobial use in pigs. The report states that based on results from the  trial the agency is preparing guidance, including a protocol and template,  for member states on antibiotic use data collection. Additionally, the EU  agency began a pilot study to collect antibiotic use data from twenty pig  farms per country, but there was insufficient support among member  states to continue the study, according to EU documents. Officials from  the European Medicines Agency told us that the pilot project underscored  the challenges in collecting farm-specific data which include producer  confidentiality and resource constraints. However, these officials also told  us that they have limited access to farm-specific data from certain  countries, including Denmark, the Netherlands, and Norway. The EU also  took steps to compare surveillance data on antibiotic use and resistance  in pathogens in humans, food, animals, and environment. Specifically, in  2015 three EU agencies published the first integrated analysis report that  found a positive association between the use of certain antibiotics in food  animals and resistance in humans. For example, the report cited that a  positive association was observed between fluoroquinolone resistance in  E. coli from humans and the total consumption in animals. The report  also explains that the agencies analyzed existing data from five separate  monitoring systems, including sales data, to create the integrated report.  In the United States, no such comparisons in surveillance reports have  been made, in part because antibiotic use data are limited, as previously  discussed.
section_title: The Netherlands and Denmark Set Reduction Targets and the EU Called for Measurable Goals and Indicators
paragraphs: The Netherlands and Denmark set antibiotic use reduction targets to help  manage the use of antibiotics in food animals. According to government  officials in both countries, the targets were a critical component of their  strategies to reduce antibiotics use. The Netherlands and Denmark used  reduction targets to measure the progress and impact of actions taken,  and as existing targets are reached these countries continue to set new  targets. Similarly, the EU outlined its next steps for combating antibiotic  resistance in a June 2016 document that calls for measureable goals that  lead to reductions in infections in humans and animals and reductions in  antibiotic use and resistance, among other things. U.S. federal officials  and representatives of industry and veterinary organizations whom we  interviewed questioned the usefulness of setting antibiotic use reduction  targets in the United States, in part, because targets may reduce animal  welfare.
subsections: section_title: Netherlands
paragraphs: The Netherlands policy on reducing antibiotic use, implemented through  the public-private partnership discussed above, set the following  reduction targets on antibiotics used in food animals: 20 percent reduction  in the sales of all antibiotics used in food animal production by 2011, 50  percent by 2013, and 70 percent by 2015. According to Dutch  government officials, the first two targets were met and exceeded, but the  70-percent reduction by 2015 was not met; a 58-percent reduction was  achieved from 2009 through 2015, according to government documents.  Indicators used to measure the policy’s impact included antibiotic use and  resistance levels in swine, mortality of swine, and veterinary cost per  swine. According to a Dutch industry representative, to reduce the use of  antibiotics, food animal industries optimized feed, housing, vaccines, and  hygiene (see fig. 3).
In a June 2015 letter to parliament, government officials proposed the  Netherlands approach to antibiotic resistance for 2015 through 2019,  which includes taking additional action to achieve the 70-percent  reduction goal and developing species-specific measures and reduction  targets. Representatives from veterinary and industry organizations in the  Netherlands told us that setting targets has proven to be effective, but  that there is concern that further reductions may pose some risk to animal  health and welfare. For example, piglets may be at risk of premature  death if certain antibiotics are prohibited or fewer antibiotics are used,  according to Dutch veterinary and industry representatives.  Representatives of veterinary and producer organizations we spoke with  in the United States expressed similar concerns that reductions in  antibiotic use may compromise animal health and welfare.
section_title: Denmark
paragraphs: In 2011, we reported on Denmark’s Yellow Card initiative, which set  regulatory limits on antibiotic use and subjected pig producers exceeding  limits to increased monitoring by government officials. The goal of the  Yellow Card initiative was to achieve a 10-percent reduction in antibiotic  use by 2013 from 2009 levels. According to government officials, the goal  was met and exceeded. In 2016, Denmark expanded the Yellow Card  initiative in pigs to focus more on antibiotics that are important for human  health. It also developed an action plan to address methicillin-resistant  Staphylococcus aureus (MRSA). Included in this plan is a new target of  a 15 percent reduction in antibiotic use in swine by 2018. According to a  representative from a Danish industry organization that represents  producers across many food animal production sectors, producers who  used antibiotics below the permitted levels began increasing their use to  the maximum amounts allowed, and the new reduction target is a  response to these increases. The representative also told us that  reduction targets are critical because they place the responsibility for  reduction on the producer or farmer—the person who determines what  farm practices are implemented—and that reducing antibiotic use and  setting reduction targets must be done with involvement of producers and  veterinarians because the need for antibiotics varies across animals. For  example, dairy cattle in different age groups use varying amounts of  antibiotics, and setting one target may put the more susceptible age  group at greater risk of infection or death, according to industry officials.  In addition to the government targets, industry set its own targets to  reduce the use of antibiotics. For example, the dairy and beef cattle  industries set a target in 2014 to reduce use by 20 percent by 2018.  Some U.S. officials and stakeholders question the benefits of antibiotic  use targets and reductions in Denmark because while antibiotic use was  reduced, changes in resistance are less clear. Representatives from the  U.S. swine industry told us that targets based on volume of antibiotics  used do not take into account the potency of the antibiotics, and that a  mandatory reduction target could take antibiotic use in an unfavorable  direction, such as a shift from veterinarians and producers using older  drugs that are less potent, to using drugs that are more potent, newer, or  important to human health.
In 2016, the EU Council published a statement of its conclusions on the  next steps for its member states to combat antimicrobial resistance  including setting goals and targets. The statement calls for EU member  states to have a one-health action plan by 2017 with measureable goals,  qualitative or quantitative, that lead to reduction in infections in humans  and animals, reductions in antimicrobial use and resistance, and prudent  antimicrobial use. The statement also calls for EU officials and member  states to jointly develop a new EU action plan on antimicrobial resistance,  indicators to assess the progress made on addressing antibiotic  resistance, and indicators to assess progress in implementing the new  action plan. EU officials told us that the EU is seeking to develop  indicators that are easy to measure, are not too costly, and can be  applied across its member states. Representatives of U.S. industry and  veterinary organizations we interviewed stated that they would support  measures and targets that focus on compliance with judicious use  policies, but not on reductions.
section_title: HHS and USDA Have Not Conducted On- Farm Investigations and No Consensus Exists on When Such Investigations Are Warranted
paragraphs: CDC, APHIS, and FSIS officials told us they have not conducted on-farm  investigations during outbreaks from foodborne illness including those  from antibiotic-resistant pathogens in animal products. Moreover, there is  no consensus about when an on-farm investigation is needed. In 2014,  recognizing the importance of the one-health concept (health of humans,  animals, and the environment are interconnected) FSIS and APHIS  created a memorandum of understanding and standard operating  procedures for APHIS to investigate the root cause of foodborne illness  outbreaks, given APHIS’s regular interactions with producers on farms  and expertise in veterinary epidemiology. Under the memorandum of  understanding, APHIS will conduct epidemiological investigations—which  includes examining the spread of disease by time, place, and animal as  well as the mode of transmission and source of entry of disease—to  determine the root cause of foodborne illness, which may be related to  factors at the farm level, according to FSIS officials. Such investigations  can be used to identify on-farm risk factors for disease occurrence or  spread that might be controlled or mitigated by some intervention in  current or future situations.
For multistate foodborne illness outbreaks, CDC is to identify the outbreak  and lead the investigation by determining the DNA fingerprint of the  bacteria that cause the outbreak as well as whether or not the bacteria is  resistant to any antibiotics. According to CDC officials, with increasing  use of whole genome sequencing—an advanced technique to fingerprint  bacteria—federal agencies may prioritize foodborne outbreak  investigations from antibiotic-resistant bacteria because they can identify  these outbreaks sooner. CDC is to coordinate with state health  departments and FSIS if a meat or poultry product is implicated (see fig. 4  for more information on the investigation process for multistate foodborne  illness outbreaks).
However, APHIS and FSIS did not conduct on-farm investigations in  response to a multistate foodborne illness outbreak in 2015 involving an  antibiotic-resistant strain of Salmonella in roaster pigs, the first attempt to  use the 2014 memorandum of understanding. We determined this is  because stakeholders—industry, state agencies, and federal agencies— did not agree on whether on-farm investigations were needed as part of  the 2015 outbreak investigation. Specifically, FSIS, the pork industry, and  a state agriculture agency agreed that the slaughter plant was the source  of the outbreak, negating the need for an on-farm investigation in their  view, while state public health agencies wanted on-farm investigations to  determine whether the pigs from the five farms supplying the slaughter  plant were carriers of the outbreak strain and to identify the slaughter  plants that received the pigs. CDC and APHIS deferred to FSIS on  whether an on-farm investigation was needed. According to FSIS officials,  the outbreak was attributed to conditions and practices at the slaughter  plant and the company implemented extensive corrective actions at the  plant in response to the 2015 outbreak. However, in July 2016, FSIS  issued a public health alert because of concerns about illnesses from  another outbreak linked to the Salmonella strain from the 2015 outbreak  involving whole roaster pigs; the same slaughter plant was implicated in  the 2016 outbreak. CDC officials told us that resistance for this specific  strain of Salmonella has increased for a variety of drugs and that an on- farm investigation would have been useful in the original outbreak to  explore whether the outbreak strain was present in pigs while they were  still on the farm. FSIS and the Washington State Department of Health  investigated the 2016 outbreak, but no on-farm investigations were  conducted. The implicated slaughter plant recalled products and the  outbreak ended, according to Washington state officials. As of October  2016, FSIS and APHIS were continuing discussions and making plans on  how best to address the need to enhance understanding of this  Salmonella strain in live pigs, especially how to identify on-farm  interventions that may prevent future illness, according to FSIS officials.
APHIS and FSIS officials told us that deciding when to conduct  investigations on the farm is complex. First, the memorandum of  understanding requires producer’s consent to conduct an on-farm  investigation. The memorandum of understanding outlines the need for  producer’s consent, in part, because neither APHIS nor FSIS has  authority to access farms during foodborne illness outbreaks without the  cooperation of the producer. APHIS will contact the producer or  company involved to discuss the specifics of an investigation and to gain  voluntary participation in any investigation. CDC has authority to take  actions to prevent the interstate spread of communicable diseases,  which, according to CDC legal officials, would include diseases  originating on farms that may relate to foodborne illness from antibiotic- resistant pathogens. Specifically, CDC has authority to take measures in  the event of inadequate state or local control to prevent interstate  communicable disease spread. To the extent that CDC would use this  authority, CDC would generally work with APHIS and FSIS on issues  relevant to their expertise, according to CDC officials. Second, deciding  whether an outbreak is likely due to on-farm risk factors versus ones that  are largely the result of in-plant problems is difficult because every  outbreak is unique, according to FSIS officials. FSIS is less likely to  request APHIS assistance if there is evidence of insanitary conditions—a  condition in which edible meat and poultry products may become  contaminated or unsafe—at the slaughter plant. However, the APHIS and  FSIS memorandum of understanding does not include a decision-making  framework to determine the need for an on-farm investigation; instead it  focuses on the procedures for and division of responsibilities in assessing  the root cause of an outbreak. In contrast, APHIS uses a decision matrix  when determining whether it will pursue epidemiological assessments on  the farm during other types of investigations, such as investigations of  animal disease outbreaks.
According to FSIS Directive 8080.3, the objectives of foodborne illness  investigation include identifying contributing factors to the foodborne  illness, including outbreaks, and recommending actions or new policies to  prevent future occurrences. The White House’s 2015 National Action  Plan for Combating Antibiotic-Resistant Bacteria includes a 3-year  milestone for USDA to begin coordinated investigations of emerging  antibiotic-resistant pathogens on the farm and at slaughter plants under  the one-health surveillance goal. The objective for this milestone  emphasizes coordination among federal agencies, producers, and other  stakeholders. Coordination with the stakeholders who have the authority  and who control access to the farm could help APHIS and FSIS fully  investigate an outbreak. Specifically, CDC has authority to cooperate with  and assist state and local governments with epidemiologic investigations  and to take actions to prevent the spread of communicable diseases in  the event of inadequate local control, including diseases originating on  farms. In addition, involving stakeholders from industry and state  departments of agriculture could increase the likelihood of obtaining  producers’ consent to on-farm investigations. Developing a framework for  deciding when on-farm investigations are warranted during outbreaks, in  coordination with CDC and other stakeholders, would help APHIS and  FSIS identify factors that contribute to or cause foodborne illness  outbreaks, including those from antibiotic-resistant pathogens in animal  products.
section_title: Conclusions
paragraphs: Ensuring the continued effectiveness of antibiotics, particularly those  used in human medicine, is critical because the rise of antibiotic-resistant  bacteria poses a global threat to public health. Since 2011, HHS and  USDA agencies have taken actions to increase veterinary oversight of  medically important antibiotics used in the feed and water of food animals  and to collect more detailed antibiotic sales, use, and resistance data.  However, these actions do not address long-term and open-ended use of  medically important antibiotics because some antibiotics do not have  defined durations of use on their labels. Without developing a process to  establish appropriate durations of use on labels of all medically important  antibiotics, FDA will not know whether it is ensuring judicious use of  medically important antibiotics in food animals. In addition, FDA officials  told us the agency is developing a plan that outlines its key activities over  the next 5 years to further support antimicrobial stewardship in veterinary  settings, including steps to bring the use of medically important antibiotics  administered in other dosage forms (not feed or water) under veterinary  oversight. However, FDA was unable to provide us with this plan or  provide specifics about the steps outlined in the plan because it was still  under development. A published plan with steps is critical to guide FDA’s  efforts in ensuring the judicious use of medically important antibiotics in  food animals.
HHS and USDA agencies continue to move forward with data collection  activities including new initiatives, but data gaps remain. For more than a  decade, we have reported on the need for HHS and USDA to work  together to obtain more detailed farm-specific data on antibiotic use and  resistance to address the risk of antibiotic resistance. In 2004, we  recommended that HHS and USDA jointly develop and implement a plan  for collecting data on antibiotic use in food animals that would support  understanding the relationship between use and resistance, among other  things. In 2011, we again recommended that HHS and USDA identify  approaches for collecting detailed data on antibiotic use to assess the  effectiveness of policies to curb antibiotic resistance, among other things.  Although HHS and USDA agreed with these recommendations, they have  not developed a joint plan to collect such data. We continue to believe  that developing a joint plan for collecting data to further assess the  relationship between antibiotic use and resistance at the farm level is  essential and will help maximize resources and reduce the risk of  duplicating efforts at a time when resources are constrained.
To assess the impact of agency actions to manage the use of antibiotics  in food animals, FSIS finalized a performance measure, but FDA and  APHIS have not developed any such measures or related targets, which  is not consistent with leading practices for federal strategic planning and  performance measurement. Without developing performance measures  and targets for their actions, FDA and APHIS cannot assess impacts of  their efforts to manage the use antibiotics in food animals.
In addition, although APHIS and FSIS established a memorandum of  understanding in 2014 to assess the root cause of foodborne illness  outbreaks, the memorandum does not include a decision-making  framework for determining when on-farm investigations are needed. In  the first use of the memorandum in a 2015 outbreak, there was no  consensus among stakeholders on when such investigations were  needed. Developing a framework for deciding when on-farm  investigations are warranted during outbreaks, in coordination with CDC  and other stakeholders, would help APHIS and FSIS identify factors that  contribute to or cause foodborne illness outbreaks, including those from  antibiotic-resistant pathogens in animal products.
section_title: Recommendations for Executive Action
paragraphs: The Secretary of Health and Human Services should direct the  Commissioner of FDA to take the following three actions:
Develop a process, which may include time frames, to establish  appropriate durations of use on labels of all medically important  antibiotics used in food animals.
Establish steps to increase veterinary oversight of medically  important antibiotics administered in routes other than feed and  water, such as injections and tablets.
Develop performance measures and targets for actions to manage  the use of antibiotics such as revising the veterinary feed directive  and developing guidance documents on judicious use.
The Secretary of Agriculture should take the following three actions:
Direct the Administrator of APHIS to develop performance  measures and targets for collecting farm-specific data on antibiotic use in food animals and antibiotic-resistant bacteria in food animals.
Direct the Administrator of APHIS and the Administrator of FSIS to  work with the Director of CDC to develop a framework for deciding  when on-farm investigations are warranted during outbreaks.
section_title: Agency Comments
paragraphs: We provided a draft of this report to the Secretaries of Agriculture and  Health and Human Services for review and comment. USDA and HHS  provided written comments, reproduced in appendixes IV and V,  respectively. USDA agreed with our recommendations. The department  stated that it will develop performance measures and targets for collecting  farm-specific data on antibiotic use in farm animals and antibiotic- resistant bacteria. USDA also agreed that a decision matrix to support  multi-agency cooperation and to determine when on farm investigations  are warranted, could be a useful addition, and noted that it has similar  matrices that can serve as a model for antimicrobial resistance  investigations. HHS neither agreed nor disagreed with our  recommendations. USDA and HHS also provided technical comments,  which we incorporated as appropriate.
As agreed with your offices, unless you publicly announce the contents of  this report earlier, we plan no further distribution until 30 days from the  report date. At that time, we will send copies to the appropriate  congressional committees, the Secretary of Agriculture, the Secretary of  Health and Human Services, and other interested parties. In addition, the  report will be available at no charge on the GAO website at  http://www.gao.gov.
If you or your staff members have any questions about this report, please  contact me at (202) 512-3841 or neumannj@gao.gov. Contact points for  our Offices of Congressional Relations and Public Affairs may be found  on the last page of this report. GAO staff who made key contributions to  this report are listed in appendix VI.
section_title: Appendix I: Objectives, Scope, and Methodology
paragraphs: This report (1) examines actions the U.S. Department of Health and  Human Services (HHS) and U.S. Department of Agriculture (USDA) have  taken since 2011 to manage the use of antibiotics in food animals and to  assess the impact of their actions, (2) identifies actions that selected  countries and the European Union (EU) have taken to manage the use of  antibiotics in food animals, and (3) examines the extent to which HHS and  USDA have conducted on-farm investigations of outbreaks of foodborne  illness from antibiotic-resistant pathogens in animal products.
To examine actions HHS and USDA have taken since 2011 to manage  the use of antibiotics in food animals and to assess the impact of their  actions, we reviewed relevant statutes and regulations, agencies’ plans  and guidance, and stakeholders’ reports related to managing the use of  antibiotics in food animals. We also reviewed USDA’s Office of Inspector  General report on USDA’s actions to manage the use of antibiotics in  food animals. We reviewed federal data reports on antibiotic sales, use,  and resistance and asked officials about the quality of these data. Based  on these steps, we determined that the data were sufficiently reliable for  our purpose of illustrating actions taken to improve data collection. We  compared information from federal agencies about actions taken to  manage the use of antibiotics with federal standards for internal controls.  We also reviewed public comments submitted to HHS regarding data  collection on farms and changes to the Animal Drug User Fee Act. We  interviewed federal officials and representatives of stakeholder  organizations about federal actions taken to manage the use of antibiotics  since 2011. These stakeholder organizations, represented national food  animal industries (National Chicken Council, National Turkey Federation,  U.S. Poultry and Egg Association, National Pork Producers Council,  National Pork Board, and National Milk Producers Federation);  veterinarians (American Association of Avian Pathologists, American  Association of Bovine Practitioners, American Association of Swine  Veterinarians, and American Veterinary Medicine Association); the  pharmaceutical industry (Animal Health Institute and Zoetis); consumer  advocates (Keep Antibiotics Working, National Resource Defense  Council, and Center for Science in the Public Interest); and others (Cattle  Empire, American Feed Industry Association, Farm Foundation, and Pew  Charitable Trusts). In addition, we interviewed representatives of several  companies (producers and restaurants) that provide food products from  animals raised without antibiotics to obtain a better understanding of  production practices; the types of antibiotic use data available at the farm  level; and perspectives on federal efforts to educate producers about  antibiotics. The views of representatives we spoke with are not  generalizable to other companies. In addition, we compared federal  agencies’ actions with relevant goals outlined in the 2015 National Action  Plan for Combating Antibiotic-Resistant Bacteria and interviewed  representatives of stakeholder organizations to obtain views on agencies’  efforts taken to date. To examine agencies’ efforts to assess the impact of  their actions, we reviewed HHS and USDA agencies’ strategic plans and  we identified any relevant goals, measures, and targets developed by  federal agencies. We compared the measures and targets with agencies’  goals, National Action Plan goals and milestones, and leading practices  for improving agency performance—specifically, practices identified in the  GPRA Modernization Act of 2010 and our prior work on performance  management.
To identify actions that selected countries and the EU have taken to  manage the use of antibiotics in food animals since 2011, we reviewed  documents, statutes, regulations, published studies, and surveillance  reports regarding animal antibiotic use and resistance in Canada,  Denmark, the Netherlands, and the EU. We selected these countries and  this region because they have taken actions to mitigate antibiotic  resistance by managing the use of antibiotics in food animals.
Additionally, each country and region met at least one of the following  criteria: (1) have food animal production practices similar to those of the  United States (Canada); (2) have taken actions over the last 10 years to  manage the use of antibiotics in food animals (the EU and Denmark); and  (3) have novel practices to manage the use of antibiotics in food animals  (the Netherlands). Moreover, Denmark and the Netherlands are EU  members that have made changes beyond EU directives to manage the  use of antibiotics in food animals. We interviewed government officials  either in person or by phone from Health Canada, the Public Health  Agency of Canada, Agriculture and Agri-Food Canada, the Canadian  Food Inspection Agency, and the Office of the Auditor General of  Canada; the Danish Veterinary and Food Administration; the Netherlands  Ministry of Health, Welfare and Sport, the Netherlands Ministry of  Economic Affairs and Netherlands Food and Consumer Product Safety  Authority; and the European Union Directorate General for Health and  Food Safety and the European Medicines Agency. Additionally, we visited  a swine facility in the Netherlands to learn about production practices. We  also interviewed representatives of the Netherlands Veterinary Medicines  Authority, an independent agency that monitors the use of antibiotics in  food animals, defines antibiotic use benchmarks, and reports on antibiotic  use trends, among other things. Finally, we interviewed representatives  from veterinary and food animal industry organizations in the United  States, Canada, Denmark, and the Netherlands; a U.S. organization that  represents pharmaceutical companies that manufacture animal health  products; as well as researchers in the field. We did not independently  verify statements made about the EU practices or about the selected  countries’ statutes and regulations. We reviewed the methodologies of  the studies provided to us and found them reasonable for presenting  examples of the selected countries and the EU efforts.
To examine the extent to which HHS and USDA conducted on-farm  investigations of outbreaks of foodborne illness from antibiotic-resistant  pathogens in animal products, we reviewed HHS’s Centers for Disease  Control and Prevention and USDA’s Animal and Plant Health Service  (APHIS) and Food Safety and Inspection Service (FSIS) documentation,  including directives, relevant to investigations of foodborne illness  outbreaks, as well as the 2014 APHIS-FSIS memorandum of  understanding and corresponding standard operating procedures to  access farms for investigations during such outbreaks. We also reviewed  documentation on a 2015 Salmonella outbreak that we identified as the  only outbreak in which APHIS and FSIS used their memorandum of  understanding. We interviewed federal and state officials (Washington  and Montana) who investigated the 2015 outbreak. We also interviewed  federal officials about the agencies’ authority to conduct on-farm  investigations during foodborne illness outbreaks, including those  involving antibiotic-resistant pathogens.
We conducted this performance audit from August 2015 to March 2017 in  accordance with generally accepted government auditing standards.  Those standards require that we plan and perform the audit to obtain  sufficient, appropriate evidence to provide a reasonable basis for our  findings and conclusions based on our audit objectives. We believe that  the evidence obtained provides a reasonable basis for our findings and  conclusions based on our audit objectives.
section_title: Appendix II: Medically Important Antibiotics That Changed Dispensing Status
paragraphs: As of January 2017, medically important antimicrobials, including  antibiotics, identified by the U.S. Department of Health and Human  Services’ Food and Drug Administration (FDA) may only be used in the  feed and water of food animals under the supervision of licensed  veterinarians, according to FDA officials. Table 3 shows the antibiotics  which changed dispensing status to require veterinary oversight.
section_title: Appendix III: Companies That Sell Products with No Antibiotic Use Claims
paragraphs: Some companies that sell meat and poultry products have taken steps to  eliminate or reduce the use of antibiotics in food animals and label  products coming from these animals with claims related to “no antibiotic  use.” We interviewed representatives of six such companies—specifically,  three producers and three restaurants. Representatives of four of the six  companies—three producers and one restaurant—told us that consumer  demand was one of the main reasons why their companies took action to  reduce or eliminate the use of antibiotics in food animals, and  representatives of the two other companies—both restaurants—stated  that their companies took action for reasons related to human and animal  health. As part of their efforts, companies implemented various on-farm  practices, such as changing animal housing and using alternatives to  antibiotics. For example, according to one company representative, the  company provided larger housing to reduce crowding and promoted the  use of probiotics to improve animal health. Representatives told us that  their companies seek to ensure animal welfare and will use antibiotics to  treat sick animals; however, these animals are removed from the product  line and sold as conventional products.
Representatives of these companies also shared challenges they face in  raising animals and selling food animal products without antibiotics. For  example, one producer told us there is a lack of antibiotic alternatives,  and that drug companies do not always produce alternatives for all  species of food animals. Restaurant representatives with whom we spoke  said that a challenge in providing meat and poultry products from animals  raised without antibiotics is that supply is limited; for example, companies  only buy certain parts of the animal, but the supplier needs to sell all  parts, which may limit the availability of suppliers willing to specialize in  animals raised without antibiotics. Additionally, company representatives  told us that it is more difficult for pork and beef producers than poultry  producers to raise animals without antibiotics because the supply chain  for poultry is vertically integrated—meaning that the same company  generally owns the animal from birth through processing—but the supply  chains for pork and beef are not.
The companies we interviewed use various terms for their label claim  related to no antibiotic use, such as “no antibiotics ever,” “no human  antibiotics,” “raised without antibiotics,” and “raised without antibiotics  important to human health.” To include these or similar claims on their  product labels, companies must submit to the U.S. Department of  Agriculture’s (USDA) Food Safety and Inspection Service (FSIS) detailed  records from the production process that support the accuracy of the  claim. All company representatives we interviewed told us their  companies collect and report data related to the production practices for  their products. For example, one company requires its suppliers to report  quarterly on antimicrobials used and the reason for use. Another  representative told us that the company collects numerous data points  throughout the year, including all medicines used on the farm and feed  history, to validate antibiotic use compliance by its suppliers with  company policies.
Company representatives we spoke with agreed that there is some  confusion among consumers regarding products sold and marketed as  being from animals raised without antibiotics. One company  representative told us that consumers are unaware that antibiotic use  claims refer to animal raising practices rather than the presence of  antibiotics in food products and that all meat and poultry products are  tested when presented for slaughter to ensure antibiotic residues are  below allowable government limits. Under its National Residue Program,  FSIS monitors meat, poultry, and processed egg products for chemical  residues, including antibiotics. Additionally, the Food and Drug  Administration requires, as a condition of use on the product label,  withdrawal periods for antibiotics—that is, periods of time prior to  slaughter when antibiotics cannot be used. Another company  representative told us that there is confusion about the various marketing  claims used by companies, such as “no hormones” and “no antibiotics.”  FSIS officials told us that the agency is aware of the concerns industry  and consumers may have regarding the various claims on products  currently in the marketplace. In September 2016, FSIS released labeling  guidance that provides information about claims frequently used on  products, what they mean, and how they are evaluated for accuracy. In  regard to label claims related to antibiotic use, the guidance describes the  requirements needed to make a claim, provides examples of terms that  may be used, and lists the documentation needed for approval of the  claim. FSIS is also considering rulemaking to define and clarify the varied  language used in the “raised without antibiotics” claim, according to  officials.
Companies may choose to further differentiate their products in the  marketplace through participating in certification, audit, or other programs,  such as USDA’s National Organic Program or Process Verified Program.  Products may carry the USDA organic seal if companies and their  products are certified by a USDA certifying agent to be in accordance with  USDA organic regulations, which include not treating animals with  antibiotics. Similarly, a company may use the process verified seal on  their products if one or more of their agricultural processes, such as  raising animals without antibiotics, is verified through an audit by USDA.  Unlike the National Organic Program, under the Process Verified  Program companies establish their own processes and standards. As a  result, processes and standards may vary across the companies. In  addition, the constraints on antibiotic use do not need to meet statutory or  regulatory requirements, leading to differing standards. For example, one  company may have a process verified program for no antibiotics ever,  and another may have a program for no antibiotics important to human  health. Representatives from five of the six companies we spoke with told  us that for some products they participate in USDA’s Process Verified  Program to verify antibiotic use claims.
section_title: Appendix IV: Comments from the Department of Agriculture
section_title: Appendix V: Comments from the Department of Health and Human Services
section_title: Appendix VI: GAO Contact and Staff Acknowledgments
subsections: section_title: GAO Contact
section_title: Staff Acknowledgments
paragraphs: In addition to the contact named above, Mary Denigan-Macauley  (Assistant Director), Nkenge Gibson, Cynthia Norris, Benjamin Sclafani,  and Bryant Torres made significant contributions to the report. Also  contributing to the report in their areas of expertise were Kevin Bray, Gary  Brown, Robert Copeland, Michele Fejfar, Benjamin Licht, Sushil Sharma,  and Sara Sullivan.