Food Safety: USDA Needs to Strengthen Its Approach to Protecting Human Health from Pathogens in Poultry Products
Released: 2014-10-20T00:00:00

Letter

Background

Salmonella and Campylobacter are bacteria that can cause disease in humans and animals. More than 2,500 different types of Salmonella— known as serotypes— exist, and 17 different types of Campylobacter exist—known as species. Salmonella live in the intestinal tracts of humans and animals, while Campylobacter live in the intestinal tracts of animals. Some serotypes cause illness in humans or in animals. According to CDC officials, Salmonella Enteritidis is a common serotype frequently associated with poultry. Salmonella Enteritidis causes the most human illnesses among other Salmonella serotypes, according to CDC’s 2011 Salmonella annual report.is caused by one species of the pathogen, called Campylobacter jejuni.

For Campylobacter, most human illness Foodborne illness occurs when bacteria or other harmful substances are ingested. Poultry is an important source of human Salmonella and Campylobacter infections, but Salmonella and Campylobacter transmission is not limited to poultry products. Contact with infected animals and consumption of contaminated water and foods, including milk, eggs, and produce can also transmit the bacteria to humans. According to CDC’s website, typical symptoms of illness from Salmonella or Campylobacter are abdominal cramps, fever, and diarrhea. Salmonella infections are more likely than Campylobacter infections to lead to bloodstream infections, particularly for infants, the elderly, and people with weak immune systems. Salmonella bloodstream infections can lead to life-threatening conditions including meningitis. In rare cases, both Salmonella and Campylobacter infections can result in long-term secondary complications such as reactive arthritis, according to CDC’s website.

To improve its food safety approach, FSIS has moved to an increasingly science-based, data-driven, risk-based approach. In 1996, FSIS adopted the risk-based Pathogen Reduction: Hazard Analysis and Critical Control Point (HACCP) regulations. rather than federal inspectors—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. As part of this approach, slaughter 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. Under FSIS regulations, all plants must also have site-specific standard operating procedures for sanitation. FSIS inspectors at slaughter plants routinely check records to verify a plant’s compliance with those procedures. FSIS also has a verification testing program in which FSIS inspectors at slaughter plants collect samples of poultry products to determine whether a pathogen is present (known as positive rate). Test results help FSIS inspectors to verify that plant sanitation procedures are working and to identify and assist plants whose process controls may be underperforming.

61 Fed. Reg. 38806 (July 25, 1996).

FSIS coordinates with numerous federal agencies, state agencies, and local entities to help ensure a safe poultry product from the farm to the consumer (known as the farm-to-table continuum—see fig. 1). For example, on the farm, USDA’s Animal and Plant Health Inspection Service (APHIS) administers voluntary programs to evaluate and certify that poultry are free of certain diseases. FSIS coordinates with APHIS to share information when investigating foodborne illnesses. FSIS also works with the Department of Health and Human Services’ Food and Drug Administration (FDA) to, for example, approve chemical interventions that slaughter plants use to reduce or eliminate Salmonella and Campylobacter.departments to respond to foodborne illness outbreaks, among other things.

USDA Actions Have Largely Sought to Reduce Salmonella in Poultry, with Campylobacter More Recently Addressed

USDA’s actions in recent years to reduce Salmonella and Campylobacter contamination in poultry products have largely focused on reducing Salmonella, with the agency addressing Campylobacter more recently and to a lesser degree.

For Salmonella, USDA Took Actions, Including Revising Existing Standards, Promoting Information Sharing, and Developing an Action Plan

Since 2006, USDA’s FSIS has taken a number of actions intended to reduce Salmonella contamination in poultry products. These actions include revising existing Salmonella standards; taking steps to develop standards; promoting enhanced information sharing with industry; publicizing noncompliance for chicken slaughter plants not meeting the agency’s Salmonella standards; developing a Salmonella Action Plan; and finalizing a rule to modernize the poultry slaughter inspection process.

Revising Standards

In March 2011, FSIS finalized revisions to the agency’s Salmonella standards for young chicken and turkey carcasses to further limit the amount of allowable contamination. Specifically, the revised standards set the expectation that no more than 7.5 percent of a plant’s young chicken carcasses (reduced from 20 percent) and 1.7 percent of a plant’s young turkey carcasses (reduced from 19.6 percent) will be contaminated with Salmonella. When FSIS revised the standards, it also made corresponding changes to the maximum number of samples allowed to test positive for contamination during agency testing; the results from the agency’s testing are used to determine whether or not a plant is in compliance with the agency’s standards. Specifically, for young chicken carcasses, FSIS now allows a maximum of 5 out of 51 samples collected by the agency to test positive for Salmonella, compared with the previous allowed positive rate of 12 out of 51. Similarly, for young turkey carcasses, FSIS now allows a maximum positive rate of 4 out of 56 samples tested by the agency, compared with the previous allowed positive rate of 13 out of 56. To help industry meet these revised standards, FSIS issued an update to its compliance guideline for Specifically, the guidelines controlling Salmonella and Campylobacter.articulate how industry can meet FSIS expectations regarding control of food safety hazards, including control points for Salmonella and Campylobacter.

To verify a chicken slaughter plant’s compliance with the agency’s Salmonella standard, FSIS inspectors collect and test one young chicken carcass per day for 51 consecutive days and determine whether the number of positive results in that sample set of 51 is above the maximum allowed. For turkey slaughter plants, FSIS inspectors collect and test one young turkey carcass per day for 56 consecutive days and likewise determine whether the number of positive results is above the maximum allowed.

In addition, the agency has recently begun taking steps to strengthen its Salmonella standards for ground poultry. More specifically, in December 2012, FSIS announced that it planned to perform additional Salmonella sampling and testing of ground chicken and ground turkey products as part of an agency effort to revise the existing standards for those products—which currently set the expectation that no more than 44.6 percent of a plant’s ground chicken and 49.9 percent of a plant’s ground turkey will be contaminated with Salmonella. FSIS officials told us the agency has begun performing additional Salmonella sampling and testing of these products. According to an April 2014 Federal Register notice, FSIS intends to announce and request comment in the Federal Register on the proposed revisions to the ground poultry standards before the end of fiscal year 2014. (See table 1 for details regarding FSIS Salmonella standards for poultry products.)

Since 2012, FSIS has taken steps to develop standards for poultry parts and mechanically separated poultry, for which there currently are no standards. For example, FSIS intends to develop a Salmonella standard for raw chicken parts. According to FSIS officials, the agency is determining which chicken parts, such as thighs, breasts, and wings, will be subject to the new standard and intends to announce that information in a future Federal Register notice. Moreover, in June 2013, FSIS began additional Salmonella sampling to determine the estimated prevalence of Salmonella in mechanically separated poultry products. FSIS announced in April 2014 that it would continue to test samples of mechanically separated poultry products for Salmonella and analyze the results as part of the agency’s efforts to develop Salmonella standards for those products. According to the agency’s December 2013 Salmonella Action Plan, FSIS plans to complete a risk assessment, which will be used to estimate the impact of this action, including any potential change in human health, and develop new standards for poultry parts and mechanically separated poultry by the end of fiscal year 2014.

Promoting Information Sharing

71 Fed. Reg. 9772 (Feb. 27, 2006). plants agreed to collect their own product samples every day during each shift, test the samples for common foodborne pathogens including Salmonella and Campylobacter, and then share these data with FSIS. In July 2011, FSIS announced that plants operating under regulatory waivers previously granted by the agency would have to join the Salmonella Initiative Program in order to continue operating under those waivers. In September 2013, FSIS completed initial analyses of program data showing that participating plants have maintained consistent process controls to keep levels of Salmonella within the standards while operating under waivers from the time and temperature chilling requirements. FSIS reported that, as of June 2014, 158 of 281 (56 percent) poultry slaughter plants were participating in the program.

Publicizing Noncompliance on Agency Website

In February 2006, to encourage industry to produce safer poultry products, FSIS announced in a Federal Register notice that completed sample set results would be recorded in one of three categories based on the plants’ ability to meet existing Salmonella standards.according to an FSIS document on inspection methods, those plants in Category 1 are said to be demonstrating consistent process controls to meet the existing Salmonella standards and that plants in Categories 2 and 3 are not. Specifically, FSIS defines the three categories as follows:

Category 1 plants have results from their two most recently completed sample sets that are at or below half of the existing standard, meaning, for example, that for young chicken carcasses, this would be 2 positive samples out of a set of 51;

Category 2 plants have results from their most recently completed sample set that are higher than half of the existing standard but do not exceed the standard, meaning, for example, that for young chicken carcasses, this would be 3 to 5 positive samples out of a set of 51; and

Category 3 plants have results from their most recently completed sample set that exceed the existing standard for Salmonella, meaning, for example, that for young chicken carcasses, this would be 6 or more positive samples out of 51.

In the February 2006 Federal Register notice, FSIS also announced that it would use the categories to determine the frequency of the agency’s Salmonella verification testing. According to FSIS’s sampling methodology, Category 1 plants are tested at least once every 2 years; Category 2 plants are scheduled for testing at least once a year until their category changes (e.g., a plant improves to Category 1); and Category 3 plants are scheduled for testing as close to continuously as possible until they produce better results and their category changes.

In addition, in a January 2008 Federal Register notice, FSIS announced that it planned to begin publishing on the agency’s website the results for young chicken slaughter plants that were inconsistent in complying with existing Salmonella standards, stating that it believed making such information available to the public would provide an incentive to industry to attain “consistent, good control for Salmonella.” The agency began publishing this information on its website in March 2008. At present, FSIS publishes the names of young chicken slaughter plants that are in Category 3. For example, in August 2014, FSIS published on its website the names of seven young chicken slaughter plants found to be in Category 3. Under FSIS policy, the names of young turkey slaughter plants not in compliance with the agency’s young turkey standard can also be published on FSIS’s website. As of August 2014, there are no names of turkey plants posted on the website because no turkey plants were in Category 3 based on recent testing.

Developing a Salmonella Action Plan

FSIS’s Salmonella Action Plan, issued in December 2013, details a priority list of actions the agency plans to undertake as part of its continued efforts to address Salmonella in poultry products. According to the plan, FSIS intends to, among other things, (1) conduct food safety assessments at plants that produce ground and mechanically separated poultry products by the end of fiscal year 2014; (2) consider modifying the way it publishes the category status of poultry plants, such as by publishing on its website the names of plants in Category 1 and Category 2, in addition to those in Category 3, by the end of fiscal year 2014; (3) develop new enforcement strategies that take into account plants’ compliance history and Salmonella category under the standards, among other things, which, according to the plan, will take over a year to accomplish; and (4) host a meeting with APHIS and other stakeholders to focus on poultry farm practices that could help decrease Salmonella contamination on FSIS-regulated poultry products and use the information gathered to inform best practice guidelines, requiring the completion of additional actions prior to the meeting.

Finalizing a Rule to Modernize Poultry Slaughter Inspection

On August 21, 2014, FSIS published its final rule to amend the agency’s poultry slaughter inspection process. Young chicken and turkey slaughter plants may choose to operate under the new poultry inspection system included in the rule or may continue to operate under the current inspection system. According to FSIS’s final rule, modernizing poultry slaughter inspections will play a role in reducing Salmonella and other poultry pathogen contamination. Currently, FSIS inspectors conduct a variety of duties at positions on and off the slaughter line. For example, FSIS inspectors positioned on the line conduct inspections of every poultry carcass and its parts for defects, and inspectors working off the line move freely about the plant and collect samples of carcasses to test for pathogens (e.g., Salmonella); perform food safety checks, such as verifying that carcasses are free of fecal material; and ensure that carcasses comply with the agency’s food quality standards for defects such as bruises on chickens, which do not affect food safety. For those poultry slaughter plants that choose to operate under the new poultry inspection system, plant employees would assume more responsibility for conducting the types of activities currently performed by FSIS inspectors on the slaughter line. For example, plant personnel would be responsible for identifying defects in carcasses, taking corrective actions if the defects can be corrected through trimming, and condemning unacceptable carcasses as part of on-line inspections. According to FSIS’s final rule, these changes will allow FSIS to assign fewer inspectors for on-line inspections and allow inspectors to conduct more off-line inspections in plants operating under the new poultry inspection system. Moreover, according to the rule, the new poultry inspection system may facilitate reduction of pathogen levels in poultry by permitting FSIS to conduct more food-safety-related off-line inspection activities and allowing better use of FSIS inspection resources, among other things. In particular, in July 2014, FSIS issued an updated risk assessment that estimated that there would be a reduction of 3,980 Salmonella illnesses attributable to young chicken and turkey plants combined.

Other Actions

FSIS has also taken other actions that are intended to help reduce Salmonella contamination in poultry products. For example, in light of several Salmonella outbreaks associated with the consumption of ground turkey products, FSIS announced in a December 2012 Federal Register notice that it was requiring all poultry plants producing ground or mechanically separated chicken and turkey products to reassess their HACCP plans. In May 2013, FSIS instructed its inspectors at plants producing these types of products to verify that the plants had reassessed their HACCP plans. In addition, FSIS announced that it would expand its Salmonella verification testing program—which previously was limited to ground chicken and ground turkey—to include plants producing all forms of ground and mechanically separated chicken and turkey products.

For Campylobacter, USDA Established Standards and Began Considering Further Actions

FSIS began taking actions specifically aimed at reducing Campylobacter contamination in poultry products in 2011. Specifically, in July 2011, FSIS implemented the first standards that define the amount of allowable contamination from Campylobacter for young chicken and turkey carcasses. Under the new standards, FSIS set the expectation that no more than 10.4 percent of a plant’s young chicken carcasses and 0.79 percent of a plant’s young turkey carcasses will be contaminated with Campylobacter. In addition, FSIS established maximum numbers of positive samples allowed during agency testing: 8 out of 51 samples for young chicken carcasses and 3 out of 56 samples for young turkey carcasses (see table 2).

FSIS is also considering other actions to address Campylobacter contamination in poultry products. According to FSIS officials, the agency plans to announce and request comment on a proposed standard for Campylobacter for raw chicken parts in the Federal Register by the end of fiscal year 2014. Furthermore, according to a May 2014 letter from the Secretary of USDA, FSIS is investigating the appropriateness of Campylobacter standards for ground and mechanically separated poultry products.

FSIS did not take actions specifically aimed at reducing Campylobacter contamination before 2011, in part, because the agency believed its actions to reduce Salmonella would also reduce other pathogens such as Campylobacter. Moreover, according to documents from FSIS and the National Advisory Committee on Microbiological Criteria for Foods, it was not until 2005 that the agency began using a less time-consuming and more reliable sampling method for determining the presence of Campylobacter on poultry products. In addition, the agency was concerned about the observed increases in Salmonella rates, such as an increase in the percentage of positive Salmonella results during agency testing from 11.5 percent in 2002 to 16.3 percent in 2005.

In Assessing Its Actions, USDA Does Not Have Measures for All Poultry Pathogen Standards to Track Progress in Protecting Human Health and Relies on Data with Limitations

To help assess the effects of the agency’s actions on the incidence of human illnesses from Salmonella and Campylobacter contamination in poultry products, FSIS has developed performance measures and conducted research, but these efforts fall short in two ways: (1) the agency did not establish performance measures for certain commonly consumed poultry products or Campylobacter and (2) the agency has relied on data with limitations that affect their usefulness.

FSIS Did Not Establish Performance Measures for Certain Commonly Consumed Poultry Products or Campylobacter

First, consistent with requirements of the Government Performance and Results Act of 1993 (GPRA) to measure performance toward the achievement of agency strategic goals, FSIS established a performance measure for Salmonella contamination in young chicken carcasses. We previously concluded that performance measures, which typically have numerical targets, are important management tools that help an agency monitor and report progress toward its goals. FSIS’s Salmonella measure indicates whether agency actions to ensure compliance with the applicable standard are helping the agency meet its goal. The agency’s goal is to maximize domestic and international compliance with food safety policies, which aligns with USDA’s objective of protecting public Specifically, the measure tracks the health by ensuring food is safe.percentage of poultry slaughter plants complying with the Salmonella standard for young chicken carcasses; the agency then compares this percentage to a target level of compliance to monitor progress in meeting its goal. For example, FSIS set the fiscal year 2013 target at 91 percent compliance and reported that 90 percent of plants complied with the standard. According to FSIS’s 2011-2016 strategic plan and a National Academy of Sciences report, verification testing data available on the exposure of the public to raw poultry products contaminated with Salmonella, including young chicken carcasses, provide a reasonable proxy for the relative risk associated with those products.

However, the agency has not established similar performance measures and targets for other types of commonly consumed poultry products for which it has established Salmonella standards—that is, young turkey carcasses, ground chicken, and ground turkey. The agency has not established performance measures even though the standards for young turkey carcasses have been in place since 2005, with a revision in 2011, and the standards for ground chicken and ground turkey have been in place for more than a decade. The majority of poultry that industry markets and Americans consume is ready-to-eat and further processed products, such as ground poultry and poultry parts, according to the United States International Trade Commission 2014 report. Salmonella- contaminated ground poultry and poultry parts put consumers at greater risk of becoming ill than whole poultry carcasses because these products generally are more likely to be contaminated. As previously noted, FSIS is developing a Salmonella standard for raw chicken parts; therefore, the agency has not developed corresponding performance measures and targets. Moreover, FSIS has not established performance measures for Campylobacter contamination, even though it implemented standards for this pathogen in 2011. According to FSIS officials, at the time that the 2011 to 2016 strategic plan was written, FSIS had only recently implemented the first ever Campylobacter standards for poultry, and so the agency did not have a basis to create a performance measure for that pathogen. FSIS officials also stated that, in the absence of performance measures, the agency routinely collects and reviews data on individual plants’ compliance with Salmonella and Campylobacter standards and reports quarterly the results of pathogen testing on its website. According to FSIS officials, these data are sent to FSIS leadership, and trends are highlighted, as appropriate.

FSIS officials agreed that performance measures and targets should be developed for additional poultry products and stated that the agency will review its current strategic plan to determine what further updates are needed, namely new performance measures for ground chicken and ground turkey. As previously mentioned, FSIS established Salmonella standards for ground chicken and ground turkey in 1996, and the agency has yet to establish corresponding performance measures and targets. According to FSIS officials, it is not appropriate for the agency to set a performance measure or target for Salmonella contamination in ground chicken or ground turkey until it finishes revising the standards for those products, which it expects to do by the end of fiscal year 2014. In addition, for Campylobacter contamination in young chicken and turkey carcasses, FSIS officials told us that the agency has not developed performance measures in part because it is still in the process of to developing plant categories, similar to those for Salmonella,determine levels of plant compliance with Campylobacter standards. The agency will publish Campylobacter categories before December 31, 2014, according to FSIS’s fiscal year 2014 annual performance plan. FSIS officials told us that the agency has not developed a performance measure for determining the agency’s success in controlling Salmonella in young turkey carcasses because testing data have shown that young turkey plants where the agency has routinely collected and reviewed data are meeting the standard. However, FSIS stated in its fourth quarter calendar year 2013 report on pathogen testing that 2 out of 35 (about 6 percent) of the turkey slaughter plants were in Category 3, meaning these plants did not meet the standard. In July 2014, FSIS officials told us these plants are no longer in Category 3 based on recent testing. However, without performance measures and targets for compliance with standards for these pathogens in commonly consumed poultry products, FSIS cannot quantitatively gauge its progress in assessing the effects of its actions related to these standards toward meeting the agency’s goal of maximizing domestic compliance with food safety policies and, ultimately, protecting public health. Performance measures and targets are reported in the agency’s strategic and annual plans but, in the absence of such measures and targets, performance information such as the trends supplied to FSIS leadership, is not being publicly reported. Without publicly reporting such information, FSIS loses the opportunity to enhance transparency by providing this information to the public and Congress about its progress in meeting this important goal, potentially limiting oversight and accountability.

In addition to the performance measure for young chicken carcasses, FSIS established, in 2009, an “all-illness” performance measure to evaluate its efforts to reduce foodborne human illness resulting from consumption of FSIS-regulated products contaminated with Salmonella and two other pathogens. According to FSIS officials, the all-illness measure is an estimate of the number of illnesses from these pathogens resulting from the consumption of all FSIS-regulated products—including meat, poultry, and processed egg products. The officials said FSIS develops this estimate using CDC laboratory-confirmed illness data, CDC outbreak data, U.S. census data, and foodborne illness estimation data from a CDC peer-reviewed publication. The all-illness measure has an associated target level of performance, set by the agency, for the maximum number of human illnesses from these pathogens attributed to FSIS-regulated products. For example, FSIS set the fiscal year 2013 target at 394,770 human illnesses from the three pathogens, including Salmonella. USDA reported in 2013 that FSIS did not meet its target; there were 427,171 human illnesses. As part of the all-illness measure, FSIS also set individual targets for the maximum number of human illnesses from each of the three pathogens attributed to FSIS-regulated products, including a Salmonella target. The annual report did not break out the results for each of the three pathogens, but the agency’s fiscal year 2013 year-in-review report showed that FSIS did not meet the Salmonella target specifically. According to FSIS officials, historically the agency has not met the Salmonella target for the all-illness measure. However, recent actions FSIS has taken and plans to take are intended to address human illnesses from Salmonella attributed to FSIS regulated products, according to the agency’s Salmonella Action Plan.

FSIS Has Relied on Data with Limitations That Affect Their Usefulness

According to USDA’s National Advisory Committee on Microbiological Criteria for Foods, which provides impartial, scientific advice to federal food safety agencies, the impact of FSIS’s regulatory activities on the incidence of human illnesses from pathogens cannot be measured directly because of limitations in the foodborne illness attribution data the agency uses.

For example, the outbreak data available from CDC depend on voluntary reporting of illnesses and do not always identify the food product that caused an outbreak; we have previously found limitations in these data, including delayed reporting and incompleteness. According to FSIS officials, as with most performance measures that seek to evaluate human health outcomes, the all-illness measure is subject to limitations based on the availability of data and the challenges in capturing accurate foodborne illness attribution. In commenting on this report, USDA agreed that there are limitations in the data but stated the agency uses the best available data. FSIS is considering including Campylobacter in the all-illness measure as well, but there is no broadly accepted estimate for the proportion of illnesses attributed to Campylobacter, according to FSIS officials.

In 2011, FSIS, CDC, and FDA formed an interagency group to improve food safety data and coordinate analyses. Some of the group’s efforts involve identifying links between contamination of poultry products and human illness, among other things.are working collaboratively to perform a detailed analysis of data on Salmonella outbreaks to better estimate the proportion of human illnesses caused by different food sources, including poultry products. According to FSIS officials, this effort will assist in better estimating the proportion of Salmonella illnesses associated with poultry products, and the agencies plan to present results from ongoing projects in 2015.

For example, FSIS, CDC, and FDA In addition to performance measures, FSIS conducted research to assess the effects of its actions on the incidence of human illnesses from the consumption of poultry products, but this research also has data limitations. For example, in February 2012, after revising its Salmonella standards for young chicken carcasses, FSIS completed research evaluating whether reductions of Salmonella contamination from young chicken carcasses across the industry would offer public benefits, in the form of reduced human illness rates. However, in attempting to evaluate the effect of reductions of Salmonella contamination across the industry, FSIS relied on its verification testing data from individual plants, which the agency later concluded in April 2012 cannot be used to estimate prevalence across the industry because the agency does not randomly select plants for verification testing, among other things. FSIS also used CDC outbreak and individual illness case data in its research to identify the number of human illness from Salmonella contamination but, as we mentioned above, these data do not always distinguish illnesses derived from poultry products specifically.

While FSIS’s research efforts are a positive step, data limitations make it difficult to directly correlate agency actions to reductions in the rates of human illness from poultry products contaminated with Salmonella. To help address these limitations, FSIS has taken steps, such as developing a statistical model in 2012, to estimate the reduction in human illnesses from revised Salmonella and newly created Campylobacter standards. More importantly, in 2013, FSIS created a new testing approach for ground poultry to estimate prevalence of Salmonella, among other things. According to FSIS officials, the new verification testing program includes continuous weekly sampling and testing at all poultry slaughter plants producing raw ground poultry and increases the sensitivity of analysis so that lower levels of contamination can be detected. FSIS officials told us that the agency plans to expand this approach to other poultry products. According to FSIS’s working group on prevalence estimates, testing for prevalence is necessary in order for the agency to effectively measure or understand how contamination rates change over time; set standards; develop targeted interventions; and measure the agency’s performance toward meeting FSIS long-term strategic goals. The new testing approach using continuous sampling affords a more direct measure of prevalence across the industry, according to FSIS officials.

USDA Faces Several Challenges in Reducing Salmonella and Campylobacter in Poultry Products across the Farm-to- Table Continuum

We identified several challenges that FSIS faces in reducing Salmonella and Campylobacter contamination in poultry products and one potential challenge. These include limited control outside of slaughter plants, pathogens not designated as hazards, limited enforcement authority, absence of mandatory recall authority, outdated or nonexistent standards, insufficient prevalence estimates, the complex nature of Salmonella, and limited Campylobacter research and testing. We identified these challenges and the potential challenge based on our analyses and the views of representatives of 11 stakeholder groups, a number of academic researchers, and FSIS officials; the stakeholder groups representing consumers and those representing industry generally had differing views.

Limited Control Outside of Plants

FSIS faces a challenge in reducing Salmonella and Campylobacter contamination in poultry products outside of slaughter plants because the agency does not have regulatory jurisdiction over (1) farm practices to reduce contamination in live poultry before they reach a plant or (2) some factors that may affect contamination of poultry products once they leave a plant. According to FSIS officials, they would like to address on-the- farm problems, but the agency is limited in its activities related to farms because its jurisdiction starts when products enter slaughter plants. In 2010, FSIS published updated compliance guidelines that detail, among other things, several on-farm practices to reduce Salmonella and Campylobacter in live poultry. For example, the guidelines recommend that farms test water to make sure it is free of pathogens and ensure water stations are free of leaks. As of July 2014, FSIS’s compliance guidelines do not discuss the effectiveness of each recommended practice to reduce pathogens in live poultry. Thus, FSIS has not provided complete information to the poultry industry about the potential benefits of adopting certain practices. In contrast, when the agency developed guidelines for on-farm practices for reducing E. coli O157:H7 in beef cattle, it described several practices and their effectiveness.

In 2011, USDA’s National Advisory Committee on Meat and Poultry Inspection recommended that (1) FSIS coordinate with APHIS, among other agencies, to develop best practices on the farm and (2) develop compliance guidelines for livestock and poultry producers, including information on the effectiveness of the practices in controlling pathogens. Representatives from two consumer groups told us that because the poultry industry is vertically integrated—meaning that individual poultry companies own or contract for all phases of production and processing—it is well suited to implement on-farm best practices to help ensure healthier birds prior to slaughter. As previously mentioned, according to FSIS’s December 2013 Salmonella Action Plan, the agency will continue to work with industry to identify on-farm best practices, host a meeting with APHIS and other stakeholders to focus on on-farm practices that could help decrease Salmonella contamination on FSIS- regulated poultry products, and use the information gathered from these actions to inform future policies and compliance guidelines. FSIS officials told us that the agency is currently working with stakeholders such as FDA and APHIS to gather information about on-farm practices. However, even with the planned actions identified in the agency’s Salmonella Action Plan, it remains unclear whether FSIS intends to incorporate information on the effectiveness of all practices in the guidelines as the National Advisory Committee on Meat and Poultry Inspection recommended. FSIS officials told us that the agency will publish another revision of the compliance guidelines by the end of calendar year 2014 but did not respond when asked directly about whether they would incorporate such information. Without providing information on the effectiveness of these practices in future guidelines, FSIS is not fully informing industry of the potential benefits of adopting them to encourage implementation of recommended practices.

However, after poultry products leave a plant, FSIS has authority to ensure that poultry products are correctly labeled and packaged. contamination of poultry products. For example, cross-contaminationfrom poultry products can occur at retail establishments, in restaurants, and in consumers’ homes, according to a food safety researcher we interviewed. According to FSIS officials, the agency has been aggressive in educating consumers on the importance of safe handling of raw poultry products, such as through an advertising campaign and changes to the safe handling label. In 2014, FSIS proposed enhancing the safe food handling label for poultry products packaged for consumers to include updated information on proper handling.

Pathogens Not Designated as Hazards

Federal regulations require plants to conduct a hazard analysis to determine food safety hazards “reasonably likely to occur” in the production process and identify the preventive measures the plant can apply to control those hazards. According to FSIS directive 5000.6, Rev.-1, all plants must conduct a hazard analysis that is an evaluation by a plant of its operations to determine the food safety hazards specific to the plant’s operations that, if not controlled, are reasonably likely to occur and to cause injury or illness. Some plants may not have a HACCP plan because they can support that there is not a food safety hazard that is reasonably likely to occur; instead, the plants would maintain a record of their hazard analysis for inspection purposes. reviewed, FSIS issued a “Notice of Intended Enforcement” action, which warns the plant before the initiation of a specific enforcement action, based on the company’s inability to support why it had not designated Salmonella as a hazard reasonably likely to occur in its HACCP plan. FSIS officials we interviewed believe the agency should require plants to identify Salmonella and Campylobacter in their HACCP plans as hazards reasonably likely to occur. FSIS’s final rule for modernizing poultry slaughter inspection requires plants to develop, implement, and maintain written procedures to prevent contamination by enteric pathogens,as Salmonella and Campylobacter.

Limited Enforcement Authority

FSIS faces a potential challenge in reducing Salmonella contamination in poultry products because, according to the agency and some stakeholder groups, its authority to enforce its Salmonella standards is limited for two reasons: (1) a federal court ruling and (2) FSIS has not classified Salmonella as an adulterant in raw poultry products.

First, in 2000, a federal court ruled that FSIS could not withdraw inspectors, which would effectively shut down the plant, based solely on a plant’s failure to meet Salmonella standards. A federal appeals court upheld the decision in 2001. Subsequently, the agency adopted the position that the court ruling did not affect its ability to use the standards as part of verifying a plant’s sanitation and HACCP plans. For example, after a plant fails Salmonella testing for its first sample set, FSIS can require a reassessment of the plant’s HACCP plan and then conduct a food safety assessment (evaluation of a plant’s food safety system); conduct additional sampling; or issue a “Notice of Intended Enforcement” action, according to FSIS officials. FSIS can also condemn products that are contaminated with filth (or otherwise adulterated) or mislabeled, or it can condemn parts of products, and detain them so they cannot progress down the marketing chain. Even with these tools, representatives from four out of six consumer groups we interviewed told us that the agency does not have sufficient authority to ensure plants comply with FSIS’s standards because FSIS cannot shut down plants when they fail Salmonella standards alone. Representatives of all four industry groups we interviewed disagreed and stated that FSIS has sufficient authority to ensure plants comply with standards because the agency has broad statutory authority and oversight.

Second, because FSIS has not classified Salmonella as an adulterant in raw poultry products, products contaminated with this pathogen generally are permitted to enter commerce. However, according to FSIS officials, the agency can consider raw poultry products contaminated with Salmonella as adulterated on a case-by-case basis—for example, during a voluntary recall, as discussed later in this report. Representatives from five out of six of the consumer groups we interviewed said they believe that some serotypes of Salmonella should be declared an adulterant, such as those with specific antibiotic-resistance patterns. According to CDC officials, antibiotic resistance can be associated with a higher risk of hospitalization in infected individuals. For example, in two of the four Salmonella outbreaks we reviewed, ill persons were hospitalized twice as frequently as is normally seen in Salmonella outbreaks, according to CDC officials. Since 2013, more than a dozen consumer groups have supported a petition for FSIS to declare specific antibiotic-resistant serotypes of Salmonella as adulterants when found in poultry. In July 2014, FSIS denied one of the consumer group’s petitions to have antibiotic-resistant Salmonella declared an adulterant. FSIS officials told us that they have found no conclusive scientific evidence that antibiotic- resistant strains of Salmonella or Campylobacter have a greater resistance to interventions currently used in FSIS-inspected poultry plants, but the agency continues to review the relevant scientific evidence to identify any potential challenges that these serotypes may present to public health.

Representatives from a government employee stakeholder group we interviewed said that rather than classifying all of Salmonella an adulterant in raw poultry products, FSIS should consider the top Salmonella serotypes causing most human illnesses. For example, the representatives said that FSIS should consider declaring a narrow range of Salmonella serotypes in select raw poultry products as adulterants similar to the classification of E. coli O157:H7 as an adulterant in beef. CDC has identified three Salmonella serotypes in poultry associated with causing the highest number of human illnesses: Salmonella Enteritidis, Salmonella Typhimurium, and Salmonella Heidelberg. According to FSIS’s risk-based inspection protocols, FSIS considers the top Salmonella serotypes identified through CDC data when ranking plants to determine the frequency of verification testing and inspections. Moreover, according to FSIS documents, the agency provides plants with data on which Salmonella serotypes were identified through verification testing. FSIS officials told us prior court cases have set a precedent that the presence of Salmonella in raw poultry products is not sufficient to declare the pathogen an adulterant because Salmonella can be killed through proper cooking.

Representatives from all four industry groups we interviewed disagreed that any serotypes of Salmonella should be classified as adulterants for several reasons. Representatives from two industry groups told us rapid identification of the serotype is not available and that it can take several weeks for FSIS to identify specific serotypes from positive Salmonella verification test results. Representatives from another industry group we spoke with said Salmonella is already classified as an adulterant in fully cooked poultry products and that, for raw poultry products, FSIS includes instructions on proper handling and thorough cooking to prevent cross- contamination and eliminate the pathogen. In contrast with Salmonella, Campylobacter has received less attention from FSIS and stakeholder groups, in part because the pathogen is not frequently associated with outbreaks, making it difficult to attribute illnesses to this pathogen.

No Mandatory Recall Authority

FSIS faces a challenge in reducing Salmonella and Campylobacter contamination in poultry products because it does not have mandatory food recall authority similar to that of FDA. In 2011, Congress passed the FDA Food Safety Modernization Act, giving FDA mandatory recall authority. We recommended in October 2004 that Congress should consider legislation to increase FSIS’s authority to include mandatory recalls, but the agency continues not to have such enforcement authority. Instead, FSIS can issue public health alerts or request voluntary recalls, among other actions, to protect human health from potentially contaminated meat and poultry products. Before requesting a voluntary recall, FSIS must gather sufficient evidence through its investigation and determine that a product is adulterated or mislabeled, among other things. According to FSIS officials, the agency requests a voluntary recall when the agency links a product to an ill person and obtains specific information on the source of the product (plant), product type, production date, and product distribution. In the five outbreaks we reviewed, three of the five companies voluntarily recalled or stopped distributing poultry products implicated in outbreaks before FSIS requested a recall. For the fourth outbreak, in July 2014, FSIS requested that Foster Farms conduct a voluntary recall of select chicken parts involved in an outbreak, which had been ongoing since March 2013, after definitively linking the product to an ill person; the company recalled the products. By contrast, in the fifth outbreak, CDC reported that collaborative investigative efforts by local, state, and federal officials indicated that Foster Farms chicken products were the most likely source of an outbreak of Salmonella Heidelberg that took place from June 2012 until May 2013. However, FSIS did not request, and Foster Farms did not conduct, a voluntary recall because the agency was unable to definitively link the company’s product to an ill person (see app. II). FSIS officials told us that, rather than focusing on the lack of mandatory recall authority, it is more productive to work aggressively with the tools they have. For example, FSIS officials told us that withdrawing inspectors or withholding the agency’s mark of inspection, thus preventing poultry products from entering commerce, can be as effective and faster tool for keeping unsafe food from the marketplace than FDA’s recall authority.

Outdated or Nonexistent Standards

Poultry Production and Consumption U.S. consumption of poultry products (chicken and turkey) is considerably higher than pork or beef, but less than total red meat consumption. According to USDA’s Economic Research Service, the U.S. poultry industry is the world's largest producer and the second- largest exporter of poultry. Before the 1970s, poultry was largely retailed on a “whole bird” basis. For example, chicken meat sold as parts, such as wings and breasts, was a small component of the domestic U.S. market. Chicken meat retailed as parts came about largely as a consequence of the inspection process at slaughter plants; that is, the carcass of a whole raw chicken that failed inspection would be cut to remove the part of the whole bird that caused inspection failure. The remainder of the bird was then further broken down and marketed as chicken parts. Market changes began to indicate to processors that consumers preferred particular chicken parts rather than whole birds. To satisfy consumers, processors began to break whole chickens into parts for retail sale. Trays of whole birds broken into constituent parts evolved into packages or bags of drumsticks, wings, and breasts, among other products.

FSIS faces a challenge in reducing Salmonella and Campylobacter contamination in poultry products because of outdated or nonexistent standards. FSIS does not revise and develop standards frequently enough to reflect changes in industry practices and poultry consumption patterns. For example, it has taken FSIS nearly 2 decades to begin revising its Salmonella standard for ground chicken. The FSIS standard established in 1996 for ground chicken set an expectation that up to 44.6 percent of a plant’s production could be contaminated with Salmonella without the plant being required to take corrective action. According to industry groups we spoke with, since the implementation of the standard, industry developed newer technologies to reduce contamination below the levels in the standard. FSIS officials agreed and stated that the majority of poultry slaughter plants perform at levels better than the standard.

In addition, as noted earlier, FSIS has not completed development of a Salmonella standard for chicken parts, even though chicken parts are now more frequently consumed than whole chickens. As a result, plants are able to meet standards for young chicken carcasses but then have an outbreak associated with chicken parts, such as occurred with the 2013 Foster Farms Salmonella outbreak. According to FSIS officials, revising standards takes time and resources, in part because the agency must first collect 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. As previously mentioned, FSIS expects to announce and request comment on the proposed Salmonella standard for chicken parts by the end of fiscal year 2014.

Insufficient Prevalence Estimates

FSIS faces a challenge in reducing Salmonella and Campylobacter contamination in poultry products as a result of not having sufficient prevalence estimates. FSIS collects and analyzes data to estimate the prevalence of pathogens when the agency revises or creates standards for its regulated products. However, as discussed above, standards are not created or revised often, and agency officials we interviewed agree that this type of data collection and analysis is done infrequently. Moreover, the data from FSIS’s verification testing program makes it difficult for the agency to assess contamination levels of poultry pathogens across the entire industry because the verification testing program was not designed to assess prevalence of pathogens industry- wide, and the agency does not randomly select plants for inspection. Also, as we said earlier, in April 2012, FSIS concluded that its verification testing data from individual plants cannot be used to estimate prevalence across the industry because the agency does not randomly select plants for verification testing.

According to USDA’s National Advisory Committee on Microbiological Criteria for Foods, 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. Similarly, the majority of representatives of consumer groups and some industry groups we spoke with stated that FSIS needs estimates of prevalence of Salmonella in poultry products to set its Salmonella public health goal. As previously mentioned, FSIS recently created a new testing According to FSIS approach for ground poultry to estimate prevalence. officials, the agency plans to propose adopting this new testing approach for all of its poultry products, which would allow for more frequent data collection and improve prevalence estimates, among other things.

The agency is using the results from the new testing approach to revise its performance standards for raw ground poultry products and create new standards for mechanically separated poultry.

Salmonella’s Complex Nature

FSIS faces a challenge in reducing Salmonella contamination in poultry products because of the complex nature of Salmonella. The majority of the representatives from industry and consumer groups we interviewed, as well as FSIS officials, agreed that Salmonella is difficult to control in poultry products because it is widespread in the natural environment. For example, according to CDC officials, there are over 2,500 serotypes of Salmonella that have been identified—not all of which are equally harmful to humans. In many cases, most serotypes are rarely involved in human illness cases and outbreaks. In addition, a food safety researcher we interviewed mentioned that some serotypes of Salmonella are more likely to cause human illness; therefore, it is important to understand the genetic makeup of each serotype to determine which ones are more or less likely to cause human illness. Furthermore, the serotypes that are important in human disease and food contamination can differ considerably in different parts of the world, and different serotypes may also be associated with different animal hosts, habitats, and paths of transmission, according to CDC officials.

Limited Campylobacter Research and Testing

Reducing levels of Campylobacter in poultry products poses a challenge for FSIS in part because less is known about Campylobacter. In addition, CDC officials told us that Campylobacter is less likely to be associated with outbreaks. Furthermore, technologies to detect Campylobacter might underdiagnose cases and the methods used by many diagnostic laboratories to isolate Campylobacter from samples are not standardized. Therefore, the efficacy of these tests varies considerably. Some countries such as New Zealand experienced greater success in reducing Campylobacter levels from poultry products, where Campylobacter cases were reduced by approximately 59 percent from 2006-2008 after its government and industry implemented several proactive measures and alterations to critical control points. New Zealand is leading the international risk-based framework for Campylobacter control in poultry. Representatives from an industry group cautioned, however, that although the decline in illnesses in New Zealand is impressive, it is difficult to extrapolate this success to other parts of the world. FSIS officials also cautioned that the agency’s ability to measure a reduction in Campylobacter illnesses will depend on its ability to attribute Campylobacter illnesses to poultry and other food types and said that an interagency analysis with CDC is under way to improve such attribution.

Conclusions

Ensuring the safety of poultry products is critical because Americans consume considerably more poultry products than beef or pork. To help ensure the safety of poultry products, USDA’s FSIS has transitioned to an increasingly science-based, data-driven, risk-based approach. As a part of this approach, USDA’s FSIS has taken several actions to reduce Salmonella and Campylobacter contamination in poultry products to protect human health, including tightening existing standards for Salmonella contamination in young chicken and turkey carcasses, as well as developing a Salmonella Action Plan. FSIS has also finalized a rule to modernize the poultry slaughter inspection process which, according to the agency, will play a role in reducing Salmonella and other poultry pathogen contamination. To assess the effects of its actions on the incidence of human illness from Salmonella and Campylobacter, FSIS has developed performance measures and associated targets for young chicken carcasses to monitor whether activities to bring plants into compliance with the standards are meeting the agency’s goals, which is consistent with requirements of GPRA to measure performance toward achievement of agency strategic goals. However, the agency has not developed performance measures and targets for certain commonly consumed poultry products, in particular ground chicken and ground turkey, even though the standards for Salmonella contamination in these products have been in place since 1996. Similarly, it has not developed performance measures for Campylobacter contamination in young chicken and turkey carcasses, or for Salmonella contamination in turkey carcasses.

FSIS believes it is not appropriate to establish measures for ground poultry until it has revised Salmonella standards for it; similarly, FSIS believes it is not appropriate to establish measures for Campylobacter until it has established plant compliance categories for Campylobacter in young chicken and turkey carcasses. According to agency officials, revised standards will be proposed and plant compliance categories for Campylobacter established by the end of 2014. FSIS officials told us that a performance measure is not necessary for Salmonella in young turkey carcasses because young turkey plants are meeting the standard, but an agency report on pathogen testing results from the fourth quarter of calendar year 2013 indicated that not all turkey slaughter plants met the standard. FSIS officials told us that all turkey slaughter plants are meeting the standard as of July 2014. As previously mentioned, FSIS is developing a Salmonella standard for raw chicken parts; therefore, the agency has not developed corresponding performance measures and targets.

In the absence of performance measures and associated targets for these pathogens in commonly consumed poultry products, FSIS cannot quantitatively assess the effects of its actions related to these standards in meeting the agency’s goal of maximizing domestic compliance with food safety policies and, ultimately, protecting public health. Performance measures and targets are reported in the agency’s strategic and annual plans but, in the absence of such measures and targets, performance information, such as data and trends supplied to FSIS leadership, is not being publicly reported. Without publicly reporting such information, FSIS loses the opportunity to enhance transparency by providing this information to the public and Congress about its progress in meeting this important goal, potentially limiting oversight and accountability. Expeditious development of these measures and targets is particularly important for ground poultry given that these products are a higher risk for contamination than whole carcasses and that the popularity of these products has grown over the years.

In addition, USDA faces several challenges that could hinder its ability to reduce contamination in poultry products. For example, practices outside the slaughter plant, such as conditions on poultry farms, can affect contamination of poultry products. To help overcome this challenge, the agency has developed guidelines on practices for controlling Salmonella and Campylobacter on farms, but the guidelines do not include information on the effectiveness for each practice, as recommended by an internal agency committee. FSIS is working with industry, APHIS, and other stakeholders to collect information on on-farm practices to inform future guidelines, but the agency has not confirmed that it would include information on the effectiveness of each on-farm practice. Without providing this information in future revisions of the guidelines, USDA is not fully informing industry of the potential benefits of adopting these practices and encouraging implementation of such practices.

Recommendations for Executive Action

We recommend that the Secretary of Agriculture direct the Administrator of the Food Safety and Inspection Service (FSIS) to take the following four actions to help ensure that FSIS efforts protect human health by reducing Salmonella and Campylobacter contamination in FSIS-regulated poultry products:

Once FSIS revises its Salmonella standards for ground chicken and ground turkey, the agency should expeditiously develop Salmonella performance measures with associated targets for these products to monitor whether activities to bring plants into compliance with the standards are meeting the agency’s goals.

Once FSIS establishes plant compliance categories for Campylobacter in young chicken and turkey carcasses, the agency should expeditiously develop Campylobacter performance measures with associated targets for these products to monitor whether activities to bring plants into compliance with the standards are meeting the agency’s goals.

FSIS should expeditiously develop Salmonella performance measures with associated targets for young turkey carcasses to monitor whether activities to bring plants into compliance with the standards are meeting the agency’s goals.

In future revisions of the compliance guidelines on controlling Salmonella and Campylobacter, FSIS should ensure the inclusion of information on the effectiveness of each recommended farm practice to reduce these pathogens in live poultry.

Agency Comments and Our Evaluation

We provided a draft of this report for review and comment to the Department of Agriculture and Department of Health and Human Services. In written comments, USDA concurred with our four recommendations; USDA’s written comments and our detailed response are presented in appendix III. According to USDA, the agency will establish appropriate measures and targets after collecting adequate data to determine whether establishments are meeting the standards for Salmonella in ground chicken and turkey and in young turkey carcasses, and for Campylobacter in young chicken and turkey carcasses. USDA also stated that it is committed to decreasing the number of Salmonella and Campylobacter illnesses associated with its regulated products, including poultry products, and to using performance standards and performance measures to achieve that reduction. Concerning the agency’s compliance guidelines on controlling Salmonella and Campylobacter, USDA said that it is currently revising the guidelines to address the reduction of Salmonella and Campylobacter in live poultry and will include all available scientific information on the effectiveness of each recommended farm practice to reduce Salmonella in live poultry.

USDA also provided technical comments, as did the Department of Health and Human Services, and we incorporated those comments 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 gomezj@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 IV.

Appendix I: Objectives, Scope, and Methodology

This report responds to your request that we review U.S. Department of Agriculture’s (USDA) approach to protecting human health by reducing Salmonella and Campylobacter contamination in poultry products. Our objectives for this report were to: (1) describe actions USDA has taken since 2006 to reduce Salmonella and Campylobacter contamination in poultry products that it regulates; (2) evaluate USDA’s efforts to assess the effects of these actions on the incidence of human illnesses from Salmonella and Campylobacter in poultry products; and (3) determine what challenges, if any, USDA faces in reducing these pathogens in poultry products.

To describe actions USDA has taken since 2006 to reduce Salmonella and Campylobacter contamination in poultry products that it regulates, we reviewed USDA regulations and documentation on actions taken from February 2006 to June 2014, including Federal Register notices, USDA’s Food Safety and Inspection Service (FSIS) notices, directives, and the December 2013 Salmonella Action Plan. We chose the time frame because FSIS introduced several initiatives in 2006 to reduce Salmonella. We also reviewed FSIS budget documents from fiscal year 2006 to fiscal year 2015, including the agency’s budget explanatory notes. It is not clear how much FSIS has spent or will continue to spend on these actions because our review of FSIS budget documents from fiscal year 2006 to fiscal year 2015 found that the agency does not provide cost data on specific poultry pathogen reduction actions, and the agency was unable to provide such data other than $2.5 million spent on poultry-related sampling programs. We interviewed officials at FSIS headquarters and district offices about recent actions taken to directly address Salmonella and Campylobacter contamination of poultry products including actions identified in Federal Register notices.

To evaluate USDA’s efforts to assess the effects of actions taken on the incidence of human illnesses from Salmonella and Campylobacter in poultry products, we reviewed USDA and FSIS strategic plans, as well as USDA annual performance reports to identify relevant performance measures, targets, and goals. We also reviewed FSIS quarterly progress reports on Salmonella and Campylobacter testing of poultry products. We evaluated the source data, statistical methodology, and results of FSIS research articles and a study to determine whether the conclusions drawn on the effects of agency actions were adequately supported by the evidence. We interviewed FSIS headquarters officials about the effects of actions taken on the incidence of human illnesses from these pathogens. We reviewed FSIS, Centers for Disease Control and Protection (CDC), and Food and Drug Administration (FDA) interagency group (Interagency Food Safety Analytics Collaboration) documentation to describe the purpose of the group, as well as completed and planned analytic projects. We also interviewed FSIS and CDC officials about the group’s projects to improve food attribution data.

To determine any challenges USDA faces to reduce Salmonella and Campylobacter in poultry products it regulates, we reviewed FSIS, USDA Office of Inspector General, and National Academy of Sciences reports on FSIS’s inspections and management challenges. We also interviewed officials from USDA’s Animal and Plant Health Inspection Service (APHIS),USDA. Additionally, we conducted interviews with stakeholder groups.

FSIS, and CDC to identify and describe any challenges facing We conducted a two-stage interview process with industry, consumer, and government employee stakeholder groups. We selected an initial set of 12 stakeholder groups identified based on our previous experience with large national groups with food safety and slaughter inspection knowledge from our August 2013 report on poultry and hog inspections.

These stakeholder groups were the American Meat Institute, the Center for Foodborne Illness Research and Prevention, the Center for Science in the Public Interest, the Consumer Federation of American, Food and Water Watch, the Government Accountability Project, the National Association of Federal Veterinarians, the National Chicken Council, the National Turkey Federation, the North American Meat Association and the Pew Charitable Trusts. We conducted an initial interview with the American Federation of Government Employees/National Joint Council of Food Inspection Locals to identify potential challenges, but we were unsuccessful in obtaining a subsequent structured interview. The sample captures a broad range of major stakeholder groups but, because it is a nongeneralizable sample, it is possible that this group did not include opinions that some experts on the topic may have. During the first round, we conducted exploratory interviews. We analyzed the results by identifying common challenges. During the second round, we conducted structured interviews using questions that covered the most common potential challenges cited in the exploratory interviews.

We list the five key structured interview questions we are reporting on that stakeholders previously identified as challenges and potential challenges during exploratory interviews. For questions listed below, respondents had the following choices as responses: definitely yes, probably yes, definitely no, probably no, or don’t know. There were several questions that would have required respondents to have in-depth information about FSIS, such as details about the technology the agency uses for identifying specific serotypes or specifics about how the agency would implement actions from its Salmonella Action Plan. Lacking this information, many respondents were only able to give us qualified answers with caveats. Therefore, we concluded that these responses were not standardized to be reported, and we excluded them from our report.

List of Selected Structured Interview Questions

FSIS sets performance standards for Salmonella and Campylobacter. Do you think FSIS has sufficient authority to ensure that poultry plants comply with FSIS performance standards?

FSIS has declared some pathogen strains adulterants, such as E-coli 0157. Do you think it is necessary for FSIS to declare some strains of Salmonella, particularly strains more likely to cause severe illness, as adulterants in order to meet its Salmonella public health goal?

Currently, poultry plants decide whether Salmonella and Campylobacter are hazards reasonably likely to occur in their HACCP. Do you think this approach is adequate to keep contamination at FSIS regulated plants within FSIS performance standards?

Verification Testing and Sampling FSIS recently evaluated its pathogen sampling program and assessed that it could not measure prevalence of Salmonella in poultry products over time, in part because it does not conduct random sampling. Do you think FSIS needs estimates of prevalence of Salmonella in poultry products to set its Salmonella public health goal?

Salmonella is known to be ubiquitous and persistent in the natural environment. Do you think these traits make it difficult to control Salmonella in poultry products FSIS regulates?

To make sure that our results were presented in an accurate and balanced manner, we evaluated responses in terms of the extent of agreement among the three stakeholder groups. Where there was stark disagreement among the groups, we presented the results separately. Where there was general agreement, we reported overall results. We conducted 11 structured phone interviews from March 2014 to May 2014. We selected 4 of the 11 stakeholder groups and pretested the initial structured interview questions to ensure that the questions were relevant and clearly stated; based on those results, we made adjustments to the structured interview as necessary. Apart from the stakeholder interviews, we also spoke with two academic food safety researchers we identified based on academic work and participation in a 2014 food safety conference and discussed challenges related to controlling Salmonella and Campylobacter in poultry products.

Additionally, we reviewed five Salmonella and Campylobacter outbreaks attributed to poultry products with the highest number of illnesses to better understand any challenges that may have contributed to the outbreaks; these outbreaks started during the time period from fiscal year 2011 through fiscal year 2013. The case study included four Salmonella outbreaks from poultry products and one Campylobacter outbreak from poultry products. These outbreaks are not generalizeable to all outbreaks from Salmonella and Campylobacter contaminated poultry products. The selected outbreaks provided illustrative examples of challenges USDA faces. To describe the selected outbreaks, we interviewed state officials from departments of health or agriculture from California, New York, Texas, Vermont, and Washington. These states had the highest number of illnesses for each outbreak in our review. We also interviewed CDC officials with knowledge of the outbreaks and FSIS officials familiar with each outbreak investigation to learn about any challenges USDA faced and other challenges related to investigating outbreaks. We also reviewed states’, CDC, and FSIS documentation on each outbreak to describe each outbreak.

For our three objectives, we visited poultry plants in California to gain a better understanding of poultry plant operations and FSIS inspection activities. We chose California because the state has a number of small and large chicken and turkey plants. California also produces a high volume of chicken and turkey in the United States. We reviewed prior GAO reports on food safety, surveillance systems, and performance management.

We conducted this performance audit from July 2013 to September 2014 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.

Appendix II: Case Study Outbreak Summary Tables

During the course of our review, we examined a nongeneralizable sample of recent Salmonella and Campylobacter outbreaks linked to poultry products since 2011. We limited the scope of our review to four of the six most recent Salmonella outbreaks that had the highest number of confirmed illnesses that the Centers for Disease Control and Prevention (CDC) and the U.S. Department of Agriculture’s Food Safety and Inspection Service (FSIS) investigated since 2009. In addition, we also identified one Campylobacter outbreak that occurred within the time period established for those Salmonella outbreaks included in our review. As this was a review of a nongeneralizable sample of outbreaks, the information is not generalizable to all outbreaks but provides important illustrative information.

In addition to the information provided for each of the five outbreaks in the summary tables below (see tables 3-7), other findings from our review included the following:

Each plant linked to the four Salmonella outbreaks included in our review was a Category 1 plant at the time the outbreaks occurred, meaning that the plants were considered by FSIS to be demonstrating consistent process controls to meet the agency’s existing Salmonella standards.

During the five outbreaks, FSIS requested that one company conduct a voluntary recall. FSIS made the request after the agency and CDC linked a person sickened by an outbreak strain of Salmonella Heidelberg to chicken produced by that company and collected from the ill person’s home. According to FSIS officials, FSIS did not request voluntary recalls during the other outbreaks for several reasons. First, for two of the Salmonella outbreaks, the companies initiated voluntary recalls before FSIS could make a formal request. Second, for the remaining Salmonella outbreak, FSIS did not identify the level of information necessary to request a voluntary recall. Finally, for the Campylobacter outbreak, the company voluntarily elected to cease harvesting and selling of raw chicken livers.

During the five outbreaks, FSIS issued two public health alerts.

Specifically, FSIS issued an alert for the outbreak of Salmonella linked to ground turkey products and another for the outbreak of Salmonella linked to specific brands of chicken products.

FSIS found that each of the plants linked to three of the four Salmonella outbreaks had inadequate Hazard Analysis and Critical Control Point (HACCP) plans.

FSIS found that each of the plants linked to three of the four Salmonella outbreaks failed to maintain sanitary conditions and comply with the agency’s regulatory requirements for sanitation.

FSIS determined that each of the plants linked to three of the four Salmonella outbreaks had not adequately supported parts of their hazard analyses because they did not identify Salmonella as a food safety hazard reasonably likely to occur during certain production processes.

In response to the Campylobacter outbreak, FSIS conducted a food safety assessment and found that the plant failed to correctly identify Campylobacter as a pathogen of concern in its hazard analyses, a noncompliance with FSIS regulations.

Appendix III: Comments from the U.S. Department of Agriculture

See comment 5

The following are GAO’s comments on the U.S. Department of Agriculture’s (USDA) letter dated September 15, 2014. 1. USDA commented that, throughout our report, we use the terms “mechanically separated” and “ground” when referring to poultry products and that the agency prefers the term “comminuted” and its standard definition. USDA defines comminuted poultry products as “poultry (chicken or turkey) products that have been ground, mechanically separated, or hand- or mechanically-deboned and further chopped, flaked, minced, or otherwise processed to reduce particle size.” For our report, it is important to distinguish among these products because there are standards for ground poultry products but not for mechanically separated or other products that are included under the umbrella of “comminuted” poultry. 2. USDA commented that our use of data from the Centers for Disease Control and Prevention (CDC) for describing the incidence of Salmonella and Campylobacter is misleading and provides an inaccurate assessment of the burden of Salmonella illnesses specifically attributed to products regulated by USDA’s Food Safety and Inspection Service (FSIS). The purpose of these data in the introduction is to provide general context for our review, not to provide information on illnesses specifically attributed to FSIS-regulated products, which are discussed later in the report. We modified our report to note that CDC’s data for describing the incidence of Salmonella and Campylobacter include illnesses attributed to other sources in addition to FSIS-regulated products. 3. USDA commented that it agrees that there are limitations in the data that it relies upon for measuring illness but stated that the agency uses the best data that are available. We modified our report to state that, according to USDA, the agency is using the best data available. 4. We provided a draft of this report to the Department of Health and Human Services, which includes CDC. We incorporated the agency’s technical comments as appropriate. 5. USDA commented that our statement about an example of limited enforcement authority did not include a new requirement under the agency’s final rule to modernize poultry slaughter inspection. We modified our report to note this new requirement.

Appendix IV: GAO Contact and Staff Acknowledgments

GAO Contact

Staff Acknowledgments

In addition to the individual named above, Mary Denigan-Macauley (Assistant Director), Carl Barden, Kevin Bray, Mark Braza, Nkenge Gibson, Cynthia Norris, Josephine Ostrander, and Kevin Remondini made key contributions to this report.