Contact with infected animals or consumption of contaminated water and food—including produce, meat, poultry, and processed products—can cause foodborne illness. Many different pathogens can contaminate food, including harmful bacteria such as Salmonella and Campylobacter. CDC reported that in 2015 there were 902 foodborne disease outbreaks reported in the United States that resulted in 15,202 illnesses, 950 hospitalizations, 15 deaths, and 20 food product recalls. According to CDC, fish, chicken, and pork were the most common single food categories implicated in these outbreaks. More recently, in 2016, there were 233 foodborne illnesses from 10 outbreaks linked to beef, 426 foodborne illnesses from 17 outbreaks linked to pork, and 417 foodborne illnesses from 20 outbreaks linked to poultry, according to CDC’s National Outbreak Reporting System (see fig. 1). Common symptoms of foodborne diseases include nausea, vomiting, stomach cramps, and diarrhea. Symptoms can sometimes be severe, and some foodborne illnesses can be life-threatening. Although anyone can get a foodborne illness, some people are more likely to have one. Those groups include young children, older adults, pregnant women, and people with immune systems weakened from medical conditions, such as diabetes, liver, and kidney disease. Patients receiving chemotherapy or radiation treatment are also more susceptible. We have previously reported that to improve its food safety approach, FSIS moved to an increasingly science-based, data-driven, risk-based approach by adopting the Pathogen Reduction; HACCP regulations in 1996. Under the HACCP approach, each plant is responsible for (1) identifying food safety hazards, such as fecal material, that are reasonably likely to occur and (2) establishing controls that prevent or reduce these hazards in its processes. As part of this approach, plants must develop plans that identify the point (known as the critical control point) where they will take steps to prevent, eliminate, or reduce each hazard identified. FSIS inspectors at slaughter and processing plants routinely check records to verify a plant’s compliance with those plans. FSIS inspectors also observe operations at plants as part of their inspection activities. Under the 1996 HACCP regulations, the agency also established Salmonella pathogen standards used to assess the effectiveness of plants’ controls in reducing levels of pathogens in meat and poultry products. According to the regulations, FSIS selected Salmonella for pathogen standards because, among other things, it was the most common bacterial cause of foodborne illness, and they believed that intervention strategies aimed at reducing fecal contamination and other sources of Salmonella on raw product should be effective against other pathogens. FSIS has a verification-testing program in which FSIS inspectors at plants collect samples of certain products and test them to determine whether plants meet the pathogen standards. Test results from this program help FSIS inspectors verify that plant HACCP plans are working and identify and assist plants whose process controls may be underperforming. FSIS also requires products to be labeled with instructions for safe handling. In contrast to Salmonella and Campylobacter, which are subject to pathogen standards, FSIS considers certain serotypes of Escherichia coli (E. coli), another type of disease-causing pathogen, adulterants under the definition of “adulterated” in the Meat Inspection Act and the Poultry Inspection Act. The acts define an adulterant in meat and poultry products to include, among other things, “any poisonous or deleterious substance which may render it injurious to health.” Meat and poultry products contaminated with any level of adulterants are not permitted to enter commerce—a stricter standard than the pathogen standards, which allow certain levels of contamination. FSIS initially declared E. coli O157:H7 as an adulterant in ground beef following an outbreak from 1992 to 1993 that involved Jack-in-the-Box hamburgers and, in 2011, declared an additional six non-O157 Shiga-toxin-forming E. coli in certain raw beef products as adulterants. In the early 1990s, a strain of Escherichia coli (E. coli) bacteria linked to hamburger resulted in a deadly foodborne outbreak and led to changes in food regulations. E. coli are bacteria found in the environment, food, and intestines of people and animals. E. coli are a large and diverse group of bacteria. Most strains of E. coli are generally harmless, but others can cause diarrhea, urinary tract infections, respiratory illness and pneumonia, other illnesses, and death. From November 1992 through February 1993, more than 500 laboratory-confirmed infections with E. coli O157:H7 and four associated deaths occurred in four states—Washington, Idaho, California, and Nevada. During the outbreak, contaminated hamburger patties were traced to a fast food restaurant chain and then ultimately to five slaughter plants in the United States and one in Canada as likely sources of carcasses used to produce the contaminated ground beef. No one slaughter plant or farm was identified as the source. In 1994, USDA’s Food Safety and Inspection Service declared that any raw ground beef found contaminated with E. coli O157:H7 would be adulterated under the Federal Meat Inspection Act—rendering the meat unlawful to sell in commerce. Meat and Poultry in the United States Beef: According to the U.S. Department of Agriculture (USDA), beef is a highly consumed meat in the United States, averaging 56 pounds per person per year. Beef comes from full-grown cattle that are about 2 years old and weigh about 1,000 pounds. There are at least 50 breeds of beef cattle, but fewer than 10 make up most cattle produced. Veal is meat from a calf (young cattle) that weighs about 150 pounds. Calves that are mainly milk-fed usually are less than 3 months old. Pork: According to the USDA, the United States is the world’s third-largest producer and consumer of pork and pork products. Pork is meat from hogs, or domestic swine, and is from young animals (6 to 7 months old) that weigh from 175 to 240 pounds. FSIS coordinates with numerous federal agencies, state agencies, and local entities to help ensure the safety of meat and poultry products from the farm to the consumer (known as the farm-to-table continuum). FSIS coordinates with USDA’s Animal and Plant Health Inspection Service (APHIS) to share information when investigating foodborne illnesses. FSIS also coordinates with the Department of Health and Human Services’ Food and Drug Administration (FDA) and with CDC on a number of activities. For example, FSIS works collaboratively with FDA and CDC through the Interagency Food Safety Analytics Collaboration to, among other things, estimate foodborne illness source attribution. Attribution entails identifying which foods are the most important sources of selected major foodborne illnesses. According to FSIS officials, determining the sources of illness is an important part of identifying opportunities to improve food safety. FSIS also coordinates with CDC and state health departments to respond to foodborne illness outbreaks, including identifying the pathogen, the product, and where the product became contaminated along the farm-to-table continuum (see fig. 2). Poultry: According to USDA, consumption of poultry (chicken and turkey) in the United States is higher than beef or pork. Chicken includes broiler-fryer chickens and roaster chickens. Broiler-fryer chickens are young, tender chickens about 7 weeks old that weigh from 2 ½ to 4 ½ pounds. Roaster chickens are young chickens from 8 to 12 weeks old with a ready-to-cook carcass weight of 5 pounds or more. Turkey is a large, widely domesticated North American bird. They grow to full maturity in about 4 to 5 months, depending on the desired market weight. USDA’s FSIS has developed or revised pathogen standards for assessing the effectiveness of plants’ controls in reducing the level of pathogens in certain meat and poultry products. More specifically, the agency has developed pathogen standards for some beef, pork, chicken, and turkey products but not for other products that are widely available, and its basis for deciding which products to consider for new pathogen standards is unclear. In addition, as of 2011, the agency has revised pathogen standards for chicken and turkey products, but standards for other products are outdated, with no time frames for revision. FSIS has developed pathogen standards for beef, pork, chicken, and turkey carcasses; specific chicken parts (i.e., breasts, thighs, and legs); and ground beef, chicken, and turkey (see Figure 3). The initial pathogen standards FSIS developed in 1996 were all for Salmonella because, among other things, it was the most common bacterial cause of foodborne illness and intervention strategies aimed at reducing Salmonella in raw products might be effective against other pathogens, according to agency documents. Subsequently, in 2011, FSIS developed Campylobacter standards for chicken and turkey carcasses and in 2016 developed Salmonella and Campylobacter standards for chicken parts. FSIS has not developed pathogen standards for other widely available products, such as pork cuts (e.g., pork chops), turkey parts (e.g., turkey breasts), and ground pork. The agency is taking steps that may lead to the development of new pathogen standards for additional products. For example, according to FSIS documents, the agency is collecting information on the presence of Salmonella and other pathogens in pork cuts and ground pork, among other pork products. According to FSIS officials, this could lead to the development of new standards. However, the agency’s process for deciding which products to consider for new pathogen standards is unclear because it is not fully documented. In December 2016, the agency documented a part of its process: who will make the decisions about which products to consider. According to the December 2016 document, certain agency officials are to meet as needed to discuss emerging food safety risks and propose related data collection efforts to senior management, who will decide which products to consider for new standards. However, the document does not explain the basis for management’s decisions. FSIS has informed stakeholders that it will take into account factors including consumption and foodborne- illness data, as it did when setting standards for chicken parts, but the agency has not documented this process going forward. Several researchers and consumer advocacy representatives we interviewed questioned whether the agency’s process proactively addresses food safety risks. Previously, FSIS developed new pathogen standards after the agency was directed to do so or after widespread outbreaks indicated the need. For example, in 2011, FSIS revised Salmonella standards for chicken and turkey carcasses and developed new standards for Campylobacter in these same products after being charged with doing so by the Presidential Food Safety Working Group. Additionally, in a 2016 Federal Register notice, FSIS, after reviewing outbreaks from these products in 2011, 2013, and 2015—outbreaks in which 794 people were sickened and 1 died—concluded that new pathogen standards were needed for comminuted (including ground and other mechanically separated) poultry and chicken parts. Under federal standards for internal control, federal entities are to design control activities to achieve objectives and respond to risks, including appropriate documentation of transactions and internal control. With appropriate documentation of internal control, management clearly documents internal control and allows the documentation to be readily available for examination; the documentation may appear in management directives, administrative policies, or operating manuals. Until FSIS clearly documents its process for deciding which products to consider for new pathogen standards, including the basis on which such decisions should be made, FSIS will not have assurance that its decisions are risk- based and that agency personnel will know the process when making such decisions. USDA’s FSIS has revised Salmonella standards for chicken and turkey carcasses and for comminuted chicken and turkey but has not revised other Salmonella standards since 1996, and the agency has not set time frames for determining whether revisions are needed. Specifically, as noted above, FSIS revised Salmonella standards for chicken and turkey carcasses in 2011 in response to a charge from the President’s Food Safety Working Group that the agency develop new or revised standards to reduce the prevalence of Salmonella in poultry products. The agency revised the pathogen standards for comminuted chicken and turkey in 2016 to help achieve public health goals for reducing human illness from Salmonella, among other things. The revisions have generally involved reductions in the maximum allowable percentage of products that test positive for this pathogen. For example, in 2016, when the agency revised the Salmonella standards for comminuted chicken, the allowable percentage changed from 44.6 to 25.0. (See table 1.) However, FSIS has not revised the Salmonella standards for beef and pork carcasses and ground beef since they were first developed in 1996. Although USDA announced in a 2014 Federal Register notice that it intended to propose new pathogen standards for ground beef, FSIS has not done so. Furthermore, FSIS set the pathogen standards for beef and pork carcasses and ground beef at industry-wide prevalence levels found at that time, not at levels intended to be protective of human health. In 2017, FSIS reviewed data on Salmonella in beef carcasses and ground beef and determined that the agency will not reach public health goals for reducing foodborne illness from Salmonella without further reduction in Salmonella contamination in beef. FSIS officials said that the agency is developing options for how it might move forward and could determine that revised or new standards are not needed and that other policies could suffice in addressing pathogens in beef. In the meantime, however, the agency in 2014 suspended monitoring against the existing Salmonella standards for ground beef until the agency develops a revised standard. The agency also suspended monitoring whether plants were meeting the pathogen standard for Salmonella on pork carcasses because, according to agency officials, the percentage of pork carcass samples that tested positive for Salmonella was consistently low. FSIS officials said that the agency is collecting data on pathogens in pork that could lead to new standards for pork products. In the absence of testing against the standards, the agency has other tools to ensure plants are controlling pathogens. For example, the agency continues to test beef for levels of E. coli, and FSIS inspectors at plants are to routinely check records to verify a plant’s compliance with its HACCP plans. FSIS officials told us that they would begin monitoring against the Salmonella standards for these products if the standards are revised or determined to be sufficient (in the case of beef and pork carcasses and ground beef) or if the agency develops new standards (in the case of pork cuts and ground pork). Generally, FSIS begins monitoring against a standard once the agency announces a standard and after a phase-in period has ended. For example, when FSIS developed new Campylobacter and Salmonella standards for chicken parts in 2016, the agency began monitoring whether plants met the standard 5 months after the standards were announced in the Federal Register. Monitoring for compliance with pathogen standards is a key tool as envisioned by the 1996 Pathogen Reduction; HACCP Systems final rule for verifying the effectiveness of a plant’s processing controls to prevent, eliminate, or reduce food safety hazards. It is unclear when FSIS plans to resume the use of this tool and complete the revisions of the Salmonella standards for beef carcasses or ground beef or develop new standards for additional pork products because the agency has not set time frames for doing so. According to FSIS officials, developing or revising pathogen standards takes time and resources, in part because the agency must first collect and analyze data to estimate the prevalence of pathogens in FSIS-regulated products, notify the public of proposed standards, and open a comment period, all of which can take years. However, according to FSIS officials, the agency has no time frames for determining what actions to take. Program schedule planning is recognized as a leading practice to ensure organizational activities are completed as planned, according to the Project Management Institute’s Standard for Program Management. Such planning includes setting time frames for completing a project. By setting time frames for determining what pathogen standards or additional policies are needed to address pathogen levels in beef carcasses, ground beef, and pork products, FSIS could better ensure it completes these activities in a timely manner to protect human health. In addition to taking steps to develop or revise pathogen standards, USDA’s FSIS is addressing other challenges we identified in September 2014 with respect to poultry pathogens, but these challenges are ongoing and also apply to meat products. These challenges include FSIS’s limited control over factors that affect the level of pathogens outside of plants, pathogens not designated as hazards, the complex nature of Salmonella, limited Campylobacter research and testing, limited enforcement authority, absence of mandatory recall authority, and insufficient prevalence estimates. Limited Control Outside of Plants In September 2014, we found that the U.S. Department of Agriculture’s (USDA) Food Safety and Inspection Service (FSIS) faced a challenge in reducing levels of Salmonella and Campylobacter in poultry products in part because the agency did not have regulatory jurisdiction over farm practices to reduce contamination in poultry before they reach a plant for slaughter and processing. At the time, we noted that FSIS had worked to address the on-farm limitation by issuing guidelines that detailed, among other things, several on-farm practices to reduce Salmonella and Campylobacter in live poultry. We recommended that in future revisions of the guidelines, FSIS include information on the effectiveness of on-farm practices to explain the potential benefits of adopting such practices on poultry farms. USDA concurred with our recommendation. In addition, we found that once poultry products leave a plant, factors beyond FSIS’s control may affect contamination of poultry products, such as cross-contamination from poultry products (i.e., when bacteria spread from a food to a surface, from a surface to another food, or from one food to another) that can occur at retail establishments, in restaurants, and in consumers’ homes, according to a food safety researcher we interviewed. Pathogen Contamination after Products Leave the Plant According to the Centers for Disease Control and Prevention (CDC), even if meat and poultry products leave the processing or slaughter plant with no detectable pathogen, it does not ensure that the products are safe, as opportunities exist for them to become contaminated at any point along the farm-to- table continuum. To illustrate, frozen hamburger patties might be trucked from a plant to a supplier, stored in the supplier’s warehouse for a few days, trucked again to a local distribution facility, and then delivered to a restaurant. According to CDC, if refrigerated food is left on a loading dock during transportation for an extended time in warm weather, the food could reach temperatures that allow pathogens to grow. among other things, on-farm practices to reduce levels of Salmonella contamination in hogs. The draft Salmonella guidelines are available on the agency’s website. Even though the guidelines are not yet finalized, FSIS encourages producers to use them, according to agency officials we interviewed. However, unlike the poultry and beef cattle guidelines, the draft Salmonella guidelines do not contain information on the effectiveness of on-farm practices, as recommended in 2011 by USDA’s National Advisory Committee on Meat and Poultry Inspection. According to the draft guidelines, when a plant makes changes at the appropriate processing location, process control should result in raw pork products that have less contamination with pathogens, including Salmonella. FSIS officials we interviewed told us that there is not as much research available for such practices for hogs as there is for beef cattle and poultry. However, the officials agreed that including available information would be beneficial. By including available information on the effectiveness of these practices to reduce the level of pathogens as it finalizes its guidelines for controlling Salmonella in hogs, FSIS would have better assurance that it is keeping industry informed of the potential benefits of adopting on-farm practices and encourage their implementation. Contamination can also occur during preparation in consumers’ homes if food is not properly stored, prepared, heated, or served. For example, according to CDC, once contamination occurs, if meat and poultry are stored or cooked at unsafe temperatures, pathogens will grow quickly, which may lead to foodborne illness. With respect to reducing pathogens after slaughter, FSIS continues to update its guidance to consumers and work with federal partners to ensure the safety of meat and poultry products after they leave the plant. For example: In 2015, the agency developed the FoodKeeper mobile application to educate consumers on how to use food while at peak quality and store food properly. It updated the application in 2017 so users could receive automatic notifications when FDA or FSIS announces food safety recalls. In 2016, FSIS and FDA announced that they would work together to revise the FDA Food Code—a model that local, state, tribal, and federal regulators use to ensure food safety at retail stores, restaurants, and institutions such as nursing homes, among others— to ensure consistency with FSIS regulations and guidance. In 2017, FSIS expanded the operating hours for its Meat and Poultry Hotline, through which consumers could speak with an agency representative or listen to recorded messages regarding food safety, such as the proper storage, handling, and preparation of meat and poultry products. Pathogens Not Designated as Hazards In September 2014, we found that the U.S. Department of Agriculture’s Food Safety and Inspection Service (FSIS) faced a challenge in reducing Salmonella and Campylobacter contamination in poultry products when plants do not designate these pathogens as hazards. Under the Hazard Analysis and Critical Control Point (HACCP) approach, plants have discretion about whether to include Salmonella or Campylobacter as a hazard “reasonably likely to occur” in their HACCP plans and develop mitigation strategies to reduce these pathogens. FSIS’s 2014 final rule for modernizing poultry slaughter inspection requires plants to develop, implement, and maintain written procedures to prevent contamination of carcasses and parts by enteric pathogens—bacteria that normally reside in the intestines of many animals, including humans, such as Salmonella and Campylobacter—as well as fecal material. Plants must incorporate these procedures into their HACCP plans, sanitation procedures, and other programs. Since our September 2014 report, FSIS has not required hog and beef plants to designate Salmonella or Campylobacter as hazards likely to occur, but it has taken other steps to reduce Salmonella and Campylobacter contamination when plants do not designate these pathogens as hazards. More specifically, in February 2018, FSIS proposed a rule to modernize hog slaughter inspections. The proposed rule would require plants to develop, implement, and maintain written procedures to prevent contamination by enteric pathogens in pork. Stakeholders we interviewed representing industry and consumer advocacy groups disagreed on whether plants should be required to designate specific pathogens as a hazard reasonably likely to occur. However, in response to instances in which inadequate validation of HACCP plans led to the production of adulterated food, and in some cases illnesses, FSIS released compliance guidance outlining best practices for designing and implementing adequate HACCP plans for all plants in 2015. According to FSIS, plants can use the guidance to properly design and execute HACCP plans and reduce the likelihood of contamination of the products they produce. Specifically, the guidance outlines, among other things, best practices for gathering scientific and technical support, as part of the HACCP plan validation process, to demonstrate that the plants’ processes prevent, reduce, or eliminate the hazards identified. Complex Nature of Salmonella In September 2014, we found that the U.S. Department of Agriculture’s Food Safety and Inspection Service (FSIS) faced a challenge in reducing Salmonella contamination in poultry products because of the complex nature of this pathogen. The majority of the representatives from industry and consumer groups we interviewed at the time, as well as FSIS officials, agreed that Salmonella is difficult to control in poultry products because it is widespread in the natural environment. According to Centers for Disease Control and Prevention officials we interviewed for our past work, there are more than 2,500 serotypes of Salmonella (with different strains), some of which pose greater risk to human health than others. Therefore, it is important to understand the genetic makeup of each to determine which ones are more or less likely to cause human illness. FSIS officials said that, in the future, there may be opportunities to improve how the agency protects human health by focusing inspections on plants and products that have tested positive for the more dangerous strains of Salmonella in meat and poultry products. To this end, FSIS collaborates with USDA’s Agricultural Research Service and APHIS, CDC, FDA, and local and state public health partners to develop new technologies that can more precisely determine if a strain of Salmonella detected is particularly dangerous to people. One such technology is whole genome sequencing, which allows the agency to determine the complete set of genes, or strain, within a Salmonella serotype. According to FSIS officials, it is more challenging to link the strain associated with an illness to a specific meat or poultry product that has sickened consumers; whole genome sequencing technology can more definitively identify the strain involved in an outbreak and help reduce incidents of illness or death due to foodborne pathogens. FSIS is currently planning how to integrate this technology into its food safety program. For example, current pathogen standards are based on the presence or absence of generic Salmonella, not on specific strains. FSIS held a public meeting in October 2017 to get input from state, federal, and international public health partners and other stakeholders on the use of this technology in a regulatory setting to improve food safety and public health. Limited Campylobacter Research and Testing In September 2014, we found that the U.S. Department of Agriculture’s Food Safety and Inspection Service faced a challenge in reducing levels of Campylobacter in poultry products in part because less was known about Campylobacter than about Salmonella. Specifically, technologies, such as clinical diagnostics, used to detect Campylobacter may have underdiagnosed cases of illness from this pathogen, and the methods used by many diagnostic laboratories to isolate Campylobacter from samples were not standardized, according to a 2012 World Health Organization report on illnesses from the pathogen. Additionally, the agency’s ability to measure a reduction in Campylobacter illnesses depended on its ability to attribute Campylobacter illnesses to poultry and other food types, according to agency officials, and attribution analyses needed improvement. Since our report in September 2014, FSIS has had efforts under way with other agencies to improve foodborne illness source attribution to meat and poultry products and has independent data collection efforts under way to determine the presence of Campylobacter on these products. More specifically, in collaboration with CDC and FDA through the Interagency Food Safety Analytics Collaboration, FSIS has taken steps to improve and standardize methods to estimate the source attribution for Campylobacter foodborne illness. In 2015, this interagency collaboration improved the method for estimating the number of Campylobacter illnesses from meat and poultry products by standardizing the approach used by all three food safety agencies. The interagency collaboration’s new estimates for the proportion of Campylobacter illnesses included all food products—including beef, pork, and poultry. The interagency collaboration also released updated foodborne illness source attribution estimates in December 2017. According to FSIS officials, the three agencies are collaborating on multiple analytic projects, in line with the interagency collaboration’s 2017–2021 strategic plan, to improve models to estimate foodborne illnesses from Campylobacter and other pathogens. These projects involve using new methods and whole genome sequencing and other data sources. In addition to this interagency effort, in 2015, FSIS tested about 200 samples of pork products for Campylobacter as part of an exploratory sampling effort, according to agency documents summarizing the efforts. FSIS found that about 1 percent of products tested were positive for Campylobacter and, therefore, chose not to continue testing pork products for this pathogen. For poultry, in 2016, FSIS revised a laboratory guidebook describing standard protocols for isolating and analyzing Campylobacter in raw products. In 2017, the agency concluded a literature review of Campylobacter contamination in beef and, as of October 2017, is discussing the development of an exploratory sampling project to test for Campylobacter in beef products, according to agency officials. Limited Enforcement Authority In September 2014, we found that the U.S. Department of Agriculture’s Food Safety and Inspection Service (FSIS) faced a potential challenge in reducing Salmonella contamination in poultry products, according to agency officials and representatives of some stakeholder groups we interviewed, because (1) a 2000 federal court ruling stated that FSIS could not withdraw inspectors, effectively shutting down the plant, solely because a plant did not meet Salmonella pathogen standards, and (2) FSIS has not classified Salmonella as an adulterant in raw poultry products, so products contaminated with this pathogen generally may be permitted to enter commerce. FSIS adopted the position that the court ruling did not affect its ability to use the Salmonella pathogen standards as part of verifying a plant’s sanitation and Hazard Analysis and Critical Control Point plans and that it had tools, such as food safety assessments (an evaluation of a plant’s food safety system), to prevent contaminated products from entering the market. Representatives from consumer groups we interviewed at the time said that even with these tools, the agency does not have sufficient authority to ensure plants comply with the standards because FSIS cannot shut down plants when they fail the Salmonella standards alone. Representatives from industry groups we interviewed at the time disagreed and stated that FSIS has sufficient authority to ensure plants comply with standards because the agency has broad statutory authority and oversight. Regarding FSIS not classifying Salmonella as an adulterant, representatives from consumer groups we interviewed for our previous work said that the agency should declare some serotypes of Salmonella as adulterants, such as those with specific antibiotic-resistant patterns. FSIS officials we interviewed for our previous work said they found no conclusive evidence that antibiotic-resistant strains of Salmonella or Campylobacter have a greater resistance to the interventions used in plants but that the agency would continue to review relevant scientific evidence to identify any potential challenges these serotypes may present to public health. Since our report in September 2014, FSIS continues to stand by the position that the 2000 court ruling does not affect its ability to use pathogen standards as a tool to prevent contaminated products from entering the market. FSIS reaffirmed its position in a 2016 Federal Register notice. Our review of FSIS data from 2016 through 2017 for poultry plants shows that some plants are still not meeting pathogen standards—in some cases repeatedly not meeting the standards—and are allowed to operate. We were unable to review similar data for beef or hog plants since, as noted above, FSIS suspended monitoring these plants against pathogen standards. FSIS stands by its assessment that its enforcement tools are sufficient. Moreover, in 2015, FSIS announced an additional tool to help FSIS identify and assess problems or trends that may be of concern. Specifically, FSIS investigators must now conduct a public health risk evaluation at every plant that does not meet a pathogen standard. This is a positive step for those products that have pathogen standards, such as chicken parts. However, as previously stated, FSIS does not test for whether plants producing beef carcasses, ground beef, and pork carcasses meet the pathogen standards for those products, and other products such as ground pork do not have pathogen standards. Representatives from consumer groups and industry we interviewed continue to disagree on whether FSIS’ existing enforcement tools are sufficient to ensure that meat and poultry plants meet pathogen standards. Regarding antibiotic-resistant strains of Salmonella, FSIS officials continue to state that the pathogen does not meet the criteria for classifying it as an adulterant and that the agency will continue to examine options for regulating the presence of antibiotic-resistant strains of Salmonella in raw meat and poultry products. Agency officials told us that to classify a pathogen as an adulterant in raw meat and poultry products, FSIS must determine that the pathogen meets certain criteria established both in its authorizing statutes and by case law. Specifically, in American Public Health Association v. Butz, a federal appeals court in 1974 held that Salmonella did not adulterate raw poultry because ordinary consumer methods of preparing and cooking the product would eliminate the pathogen. In contrast, FSIS declared certain types of E. coli as adulterants in beef, as discussed above, because ordinary consumer cooking does not eliminate the pathogen. According to FSIS officials, the available data do not appear to indicate that Salmonella presents the same issues as E. coli or meets the necessary criteria, regardless of whether it is resistant or susceptible to antibiotics. This issue continues to be contentious among the stakeholders we interviewed. Six of the seven industry stakeholders we interviewed stated that FSIS’s current enforcement authority is sufficient. Two of four food safety researchers we interviewed stated that the agency does not need additional authority to label Salmonella as an adulterant because FSIS has labeled other pathogens as adulterants when it made sense to do so, such as E. coli¸ and there is no need to label naturally occurring bacteria as adulterants on raw product. In contrast, all four of the consumer advocacy groups and two of the four food safety researchers we interviewed stated that FSIS needs more authority to label Salmonella as an adulterant. No Mandatory Recall Authority In September 2014, we found that the U.S. Department of Agriculture’s Food Safety and Inspection Service (FSIS) faced a challenge in reducing Salmonella and Campylobacter contamination in poultry products because it did not have mandatory food recall authority similar to that of the Food and Drug Administration (FDA) for the food products FDA regulates, such as milk, seafood, fruits, and vegetables. In 2011, Congress passed the FDA Food Safety Modernization Act, giving FDA mandatory recall authority. We recommended in October 2004 that Congress consider legislation to increase FSIS’s authority to include mandatory recalls, but the agency continues to not have such authority. Instead, to protect human health from potentially contaminated meat and poultry products, FSIS can issue public health alerts, which notify the public on specific actions to take to avoid illness, or request voluntary recalls, which are voluntary actions taken by plants, among other actions. Before requesting a voluntary recall, FSIS must gather sufficient evidence through its investigation and determine that a product is adulterated and mislabeled, among other things. In September 2014, we reported that this can be challenging to do. FSIS officials told us at the time that rather than focusing on the lack of mandatory recall authority, it was more productive to work aggressively with the tools they had, such as withdrawing inspectors, thus preventing products from entering commerce. According to FSIS officials, this can be as effective for keeping unsafe food from the marketplace as FDA’s recall authority. To encourage poultry slaughter and processing plants to control for Salmonella and Campylobacter—disease-causing pathogens that can sicken consumers—USDA publicly releases information on individual plant performance for reducing these pathogens. According to the agency’s 2017 annual plan, publishing plant-specific data allows consumers to make more informed choices, motivates individual plants to improve performance, and leads to industry-wide improvements in food safety. USDA’s Economic Research Service found that publicly releasing the identities of plants with poor or mediocre performance on tests for Salmonella is strongly correlated with about a 60 percent decline of chicken carcass samples testing positive for Salmonella from 2006 to 2010. In 2016, USDA temporarily replaced posting information on individual plants’ performance for chicken and turkey carcasses, chicken parts, and comminuted poultry (e.g., ground), with information on aggregate results to allow time for plants to update their food safety systems. In January 2018, FSIS began reposting individual plants’ category status for poultry carcasses on a monthly basis. According to the agency’s annual plan for fiscal year 2017, USDA intends to resume publicly releasing individual plant performance information for turkey carcasses and to add data for plants producing chicken parts and comminuted chicken and turkey. The agency also intends to release data for plants producing some beef products, according to its 2016 strategic plan on publicly releasing data. Since our September 2014 report, FSIS officials said that they continue to believe that mandatory recall authority is not necessary for the reasons previously mentioned. According to FSIS officials, the agency continues to refine and improve its procedures for requesting voluntary recalls of adulterated and misbranded meat and poultry products, confirming the effectiveness of these recalls, and alerting the public about adulterated and misbranded products that may remain in commerce. Therefore, FSIS officials stated that the agency does not see the lack of mandatory recall authority as an obstacle or hindrance to its efforts to protect public health and ensure that meat and poultry products are safe, wholesome, and properly labeled. In contrast, FDA officials told us that having mandatory recall authority protects human health from foodborne illness because the agency does not have to rely upon manufacturers’ voluntary recall efforts or obtain a court order to remove contaminated or misbranded food, other than infant formula, from the food supply. In our review of FDA’s annual reports to Congress on the use of mandatory recall authority from 2013 to 2016, the most recent available, the agency has used its mandatory recall authority twice. The majority (12 of 17) of the stakeholders we interviewed stated that the absence of mandatory recall authority is not a challenge for FSIS in reducing pathogen contamination of meat and poultry products. However, according to 3 of 4 stakeholders from consumer groups and 1 of 4 food safety researchers we interviewed, acquiring mandatory recall authority would enable FSIS to better protect human health because the agency would then have an additional tool to stop an outbreak of foodborne illness and address the level of pathogens in products once they leave the plant. Insufficient Prevalence Estimates In September 2014, we found that the U.S. Department of Agriculture’s (USDA) Food Safety and Inspection Service (FSIS) faced a challenge in reducing Salmonella and Campylobacter contamination in poultry products as a result of not having sufficient prevalence estimates. Prevalence is the proportion of a product that would test positive for a pathogen if the entire population of that product was sampled and analyzed during a specific period of time. FSIS collects and analyzes data to estimate the prevalence of pathogens when the agency develops or revises pathogen standards for products it regulates. However, we reported that there were numerous problems with the data FSIS used to estimate prevalence. For example, assessing levels of poultry pathogens across the entire industry was difficult using data from FSIS’s verification-testing program because the program was not designed to assess prevalence of pathogens industry-wide and the agency does not randomly select plants for inspection. According to USDA’s National Advisory Committee on Microbiological Criteria for Food, estimating the prevalence of pathogens in food is critical to understanding and addressing the public health risk of foodborne illness, and these estimates provide a mechanism for measuring performance against public health goals, among other things. FSIS officials told us at that time that the agency had plans to propose a new testing approach for all of its poultry products, which would allow for more frequent data collection and improve prevalence estimates, among other things. In 2016, FSIS implemented this new testing approach for all poultry products for which there are pathogen standards and for some meat products, but according to officials, the agency did not do so for all products that it regulates because of resource constraints. Specifically, according to a 2016 Federal Register notice, FSIS now routinely samples chicken and turkey carcasses, chicken parts (legs, wings, and breasts), and comminuted chicken and turkey for Salmonella and Campylobacter pathogens over an entire year—rather than a set period of time—based on the volume of poultry products produced in plants. It also uses this approach to test for Salmonella in ground beef, beef manufacturing trimmings, and other ground beef components, according to a 2014 Federal Register notice. This new approach allows for better prevalence estimates and for monitoring changes in prevalence over time, according to agency officials. As discussed earlier, FSIS began exploratory sampling of pork products, including pork cuts and comminuted (including ground) pork, in 2015. According to a 2017 agency notice describing the sampling, FSIS collects and analyzes samples of pork products in a way that allows for prevalence estimates. FSIS does not use the same approach to sample other products, such as raw components used in ground beef (e.g., esophagus, head meat, cheek meat, and hearts), chicken half carcasses, and chicken necks, because of limited resources, according to agency officials. These officials stated that the agency first conducts exploratory sampling—such as its current program for pork products—to determine if FSIS should allocate resources for routine sampling of these products that would allow for prevalence estimates. To help ensure the safety of meat and poultry products and protect against foodborne illness, USDA’s FSIS has transitioned to an increasingly science-based, data-driven, risk-based approach. As part of this approach, FSIS has taken several actions to reduce levels of Salmonella and Campylobacter in poultry products, including strengthening existing pathogen standards for Salmonella in poultry carcasses and developing new Salmonella and Campylobacter standards for certain chicken parts. However, the agency has not set pathogen standards for many widely available products, such as pork cuts and ground pork, and the agency’s process for deciding which products to consider for new pathogen standards is not fully documented. Previously, FSIS has developed new pathogen standards after the agency has been directed to do so or after widespread outbreaks indicated the need. Until FSIS clearly documents its process for deciding which products to consider for new pathogen standards, including the basis on which such decisions should be made, FSIS will not have assurance that its decisions will be risk-based and that agency personnel will know the process when making such decisions. As part of its new approach, FSIS is collecting data that could enable it to set new pathogen standards for pork cuts and ground pork, and the agency is analyzing data that could lead to revising the Salmonella standards for beef carcasses and ground beef—which are decades old and not set at levels that are health protective. However, the agency has not set time frames for completing these efforts. In the absence of pathogen standards against which the agency tests, the agency is not using a valuable tool that could be used to help verify that plants’ processing controls to prevent, eliminate, or reduce food safety hazards are working. By setting time frames for determining what pathogen standards or additional policies are needed to address pathogens in these products, FSIS could better ensure it completes these activities in a timely manner to better protect human health. In addition, FSIS continues to face several challenges that hinder its ability to reduce the level of pathogens in meat and poultry products. For example, practices outside the slaughter plant, such as conditions on cattle, hog, and poultry farms, can affect levels of pathogens on meat and poultry products. To help overcome this challenge, the agency has developed draft guidance on practices for controlling levels of Salmonella and Campylobacter on beef cattle, hog, and poultry farms, but the draft guidance for hogs does not include available information on the effectiveness for each practice, as an internal agency committee recommended. As FSIS finalizes this guidance, FSIS could better inform industry of the potential benefits of adopting on-farm practices and encourage implementation of these practices by including available information on their effectiveness. We are making three recommendations to FSIS. Specifically: The Administrator of FSIS should document the agency’s process for deciding which products to consider for new pathogen standards, including the basis on which such decisions should be made. (Recommendation 1). The Administrator of FSIS should set time frames for determining what pathogen standards or additional policies are needed to address pathogens in beef carcasses, ground beef, pork cuts, and ground pork. (Recommendation 2). The Administrator of FSIS should include available information on the effectiveness of on-farm practices to reduce the level of pathogens as it finalizes its guidelines for controlling Salmonella in hogs. (Recommendation 3). We provided a draft of this report to USDA and the Department of Health and Human Services. In written comments, reproduced in appendix II, USDA agreed with our three recommendations and described actions it will take to implement them. In particular, with respect to our first recommendation, USDA stated that FSIS will complete an internal document that delineates the agency’s process for creating or updating pathogen standards. However, USDA stated that although it agrees it can take additional steps to document its process, it does not agree that FSIS does not have assurance its decisions are risk based. In particular, it cited a Federal Register notice indicating that it designed its pathogen standards for chicken parts and comminuted chicken and turkey to achieve certain reductions in illnesses from Salmonella and Campylobacter. USDA also stated that FSIS has consistently documented and published its process in the Federal Register, and it noted that agency personnel use these Federal Register notices as guidance and historical reference. While these notices can be a useful historical record and document the steps FSIS took to ensure that agency decisions were risk-based, we continue to believe that, until FSIS clearly documents its process for deciding which products to consider for new pathogen standards going forward—including the basis on which such decisions should be made—FSIS will not have assurance that its decisions will be risk-based and that agency personnel know the process when making such decisions in the future. Completing documentation of the agency’s process would address our recommendation. Concerning our second recommendation, USDA stated that in 2018 FSIS will continue to assess data from sampling projects, along with baseline data and outbreak/illness data, to determine whether new or revised standards or additional policies are needed to address Salmonella in beef products. USDA further stated that in 2019, it will use data collected during its raw pork exploratory study to determine whether standards or additional policies (e.g., training, guidance to industry, or instructions to field personnel) are needed to address Salmonella in pork products. Finalizing analysis of these data and determining if additional standards or policies are needed to address Salmonella in beef in 2018 or pork in 2019 would address our recommendation. In response to our third recommendation, USDA stated that FSIS will include available scientific information on the effectiveness of each recommended farm practice in the guidelines for reducing Salmonella in market hogs. Doing so would address our recommendation. USDA also provided technical comments. We incorporated these comments as appropriate. The Department of Health and Human Services did not have any comments. As agreed with your offices, unless you publicly announce the contents earlier, we plan no further distribution of this report until 30 days from the report date. At that time, we will send copies of this report to the appropriate congressional committees, the Secretary of Agriculture, the Administrator of the Food Safety and Inspection Service, 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 have any questions about this report, please contact me at (202) 512-3841 or morriss@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 III. In addition to regulating meat and poultry sold in commerce, the U.S. Department of Agriculture (USDA) also purchases food and, in some cases, has additional food safety requirements for food it purchases. USDA’s Agricultural Marketing Service (AMS) purchases beef and other food for various federal nutrition assistance programs, including the National School Lunch Program. USDA provides this food to states in support of about 100,000 public and private nonprofit schools that provide lunches to about 30 million children. Ground beef is a staple of school menus. For example, according to AMS officials, during fiscal year 2016, the agency purchased more than 110 million pounds of raw beef, over 90 percent of which was delivered to the National School Lunch Program. Further, according to AMS officials, about 41 million pounds (37 percent) were delivered raw while the rest was delivered to a federally inspected processing facility for cooking prior to delivery to school lunch program agencies. Beef to be delivered raw to the National School Lunch program is tested for pathogens (Salmonella and Shiga-toxin-producing E. coli, two pathogens that can cause foodborne illness in humans) and certain microorganisms such as aerobic plate count bacteria, coliform bacteria, and generic E. coli that serve as indicators of the effectiveness of slaughter and processing plants’ process controls to limit pathogens. National School Lunch Program According to USDA, the National School Lunch Program is a federally assisted meal program operating in public and nonprofit private schools and residential childcare institutions. It provides nutritionally balanced, low-cost or free lunches to children each school day. The program was established under the National School Lunch Act, signed by President Harry Truman in 1946. USDA’s Food and Nutrition Service administers the program at the federal level. At the state level, the program is administered by state agencies, operating through agreements with school food authorities. Participating school districts and independent schools receive cash subsidies and food. In exchange, participating institutions must serve lunches that meet federal nutrition requirements and offer the lunches at a free or reduced price to eligible children. USDA’s Agricultural Marketing Service purchases beef and other food for various federal nutrition assistance programs, including the National School Lunch Program. According to AMS officials, these indicator microorganisms indicate the quality of the food safety controls at the plant. For raw beef products that AMS considers for purchase for its programs, the agency rejects any beef that tests positive for Salmonella, a pathogen that can cause foodborne illness in humans. According to AMS officials, this requirement that beef purchased for these programs not test positive for Salmonella differs from the regulatory standard for beef inspected by USDA’s Food Safety and Inspection Service (FSIS). Further, according to AMS officials, AMS set this requirement because raw beef was considered the product with the most risk for recipients and enough plants were able to meet the requirement. AMS officials said that as a purchaser for various federal nutrition assistance programs, the agency has discretion to set requirements for qualified suppliers, and plants can choose whether to become qualified suppliers. In addition to the contact named above, Mary Denigan-Macauley (Assistant Director); Thomas Cook (Assistant Director); James R. Jones, Jr. (Assistant Director); David Bennett (Analyst in Charge); Kevin Bray; Cindy Gilbert; Cynthia Norris; Gloria Ross; and Kiki Theodoropoulos made key contributions to this report. Foot-and-Mouth Disease: USDA’s Evaluations of Foreign Animal Health Systems Could Benefit from Better Guidance and Greater Transparency. GAO-17-373. Washington, D.C.: April 28, 2017. Antibiotic Resistance: More Information Needed to Oversee Use of Medically Important Drugs in Food Animals. GAO-17-192. Washington, D.C.: March 2, 2017. Food Safety: A National Strategy Is Needed to Address Fragmentation in Federal Oversight. GAO-17-74. Washington, D.C.: January 13, 2017. Seafood Safety: Status of Issues Related to Catfish Inspection. GAO-17-289T. Washington, D.C.: December 7, 2016. Imported Food Safety: FDA’s Targeting Tool Has Enhanced Screening, but Further Improvements Are Possible. GAO-16-399. Washington, D.C.: May 26, 2016. Food Safety: FDA Coordinating with Stakeholders on New Rules but Challenges Remain and Greater Tribal Consultation Needed. GAO 16- 425. Washington, D.C.: May 19, 2016. Federal Food Safety Oversight: Additional Actions Needed to Improve Planning and Collaboration. GAO-15-180. Washington, D.C.: December 18, 2014. Food Safety: USDA Needs to Strengthen Its Approach to Protecting Human Health from Pathogens in Poultry Products. GAO-14-744. Washington, D.C.: September 30, 2014. Food Safety: More Disclosure and Data Needed to Clarify Impact of Changes to Poultry and Hog Inspections. GAO-13-775. Washington, D.C.: August 22, 2013.
The U.S. food supply is generally considered safe, but the Centers for Disease Control and Prevention (CDC) estimate that Salmonella and Campylobacter in food cause about 2 million human illnesses per year in the United States. In 2014, GAO identified challenges USDA faced in reducing pathogens in poultry products, including standards that were outdated or nonexistent and limited control over factors that affect pathogen contamination outside of meat and poultry slaughter and processing plants, such as practices on the farm. GAO was asked to review USDA's approach to reducing pathogens in meat and poultry products. This report examines (1) the extent to which USDA has developed standards for meat and poultry products and (2) any additional steps USDA has taken to address challenges GAO identified in 2014. GAO reviewed relevant regulations, documents, and data and interviewed officials from USDA and CDC, as well as 17 stakeholders representing industry, consumer groups, and researchers selected based on their knowledge of USDA's meat and poultry slaughter inspections and food safety. To help ensure the safety of our nation's food supply, the U.S. Department of Agriculture (USDA) has developed standards limiting the amount of Salmonella and Campylobacter —pathogens that can cause foodborne illness in humans—permitted in certain meat (beef and pork) and poultry (chicken and turkey) products, such as ground beef, pork carcasses, and chicken breasts. However, the agency has not developed standards for other products that are widely available, such as turkey breasts and pork chops. Further, its process for deciding which products to consider for new standards is unclear because it is not fully documented, which is not consistent with federal standards for internal control. For example, USDA has informed stakeholders that it will take into account factors including consumption and illness data, but the agency has not documented this process going forward. Previously, USDA had developed new standards after widespread outbreaks indicated the need. For example, in 2016, USDA concluded that new standards were needed for certain poultry products to reduce Salmonella after reviewing outbreaks from these products in 2011, 2013, and 2015—outbreaks in which 794 people were sickened and 1 died. By documenting the agency's process for deciding which products to consider for new standards, USDA could better ensure that such decisions will be risk-based. USDA is taking steps to address challenges GAO identified in 2014 for reducing pathogens in poultry products, but these challenges are ongoing and could affect USDA's ability to reduce pathogens in meat as well. For example, one challenge GAO identified is that the level of pathogens in poultry products can be affected by practices on farms where poultry are raised. GAO recommended in 2014 that to help overcome this challenge, USDA guidelines on practices for controlling Salmonella and Campylobacter on farms include information on the effectiveness of each of the practices, consistent with a recommendation from a USDA advisory committee. Since GAO's 2014 report, USDA drafted revised guidelines to include information on the effectiveness of on-farm practices for controlling pathogens in poultry and beef cattle, in 2015 and 2017, respectively. However, USDA's draft guidelines for controlling Salmonella in hogs do not contain such information. By including such information as it finalizes its draft guidelines, USDA could better inform industry of the potential benefits of adopting on-farm practices included in the guidelines and encourage implementation of such practices. GAO is making three recommendations, including that USDA document its process for deciding which products to consider for new standards and that it include information on the effectiveness of on-farm practices in its guidelines for Salmonella control in hogs. USDA agreed with GAO's recommendations and described actions it will take to implement them.