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.

Summary:
Why GAO Did This Study

USDA is responsible for ensuring the safety of poultry products. The Centers for Disease Control and Prevention (CDC) report the U.S. food supply is one of the safest in the world, yet estimate that Salmonella and Campylobacter contamination in food causes more than 2 million human illnesses per year. Poultry products contaminated with pathogens cause more deaths than any other commodity. GAO was asked to examine USDA's approach to reduce these pathogens in poultry products.
GAO's objectives were to (1) describe actions USDA has taken since 2006 to reduce Salmonella and Campylobacter contamination in poultry products, (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 challenges USDA faces in reducing these pathogens in poultry products. GAO reviewed relevant regulations and documents and interviewed officials from USDA and CDC, as well as 11 industry, consumer, and government employee stakeholder groups selected based on knowledge of USDA's poultry slaughter inspections and food safety.

What GAO Found

Since 2006, the U.S. Department of Agriculture (USDA) has taken a number of actions to reduce contamination from Salmonella and Campylobacter (disease-causing organisms, i.e., pathogens) in poultry (chicken and turkey) products. USDA's actions to reduce these pathogens include, for example, tightening existing standards limiting the allowable amount of Salmonella contamination in young poultry carcasses, implementing the first standards limiting Campylobacter contamination in young poultry carcasses in 2011, and developing an action plan detailing a priority list of actions, such as developing new enforcement strategies, to reduce Salmonella . More recently, in August 2014, USDA published its final rule to modernize poultry slaughter inspections, which according to the agency, will play a role in reducing Salmonella and other poultry pathogen contamination by allowing better use of agency resources, among other things.
To help assess the effects of these actions on the incidence of human illness from Salmonella and Campylobacter , USDA conducted research on the effects of agency actions to reduce these pathogens and developed performance measures for certain poultry products to help monitor progress toward agency goals. For example, USDA developed a measure to indicate whether agency actions to ensure compliance with the standard for Salmonella contamination in young chicken carcasses are helping the agency achieve its goal of maximizing domestic compliance with food safety policies. However, USDA has not developed measures for Salmonella contamination in ground poultry or young turkey carcasses, even though standards for such contamination have been in place since 1996 and 2005, respectively, or for Campylobacter contamination in young poultry carcasses. USDA believes it is not appropriate to establish measures for ground poultry until the agency has revised standards, or for Campylobacte r contamination until the agency has obtained more information on compliance levels—both of which the agency expects to do by the end of 2014. USDA officials stated that they will review the agency's strategic plan to determine what performance measures, if any, are needed. USDA does not believe a measure for young turkey carcasses is needed since historically data have shown that plants are meeting the standard but, in calendar year 2013, two plants did not meet it; USDA officials told GAO that these plants are no longer noncompliant. Without performance measures for these standards, USDA is not publicly reporting performance information and cannot assess the effects of its actions related to these standards in meeting the goal of maximizing domestic compliance with food safety policies and, ultimately, protecting public health.
GAO identified several challenges—based, in part, on the views of 11 stakeholder groups—that could hinder USDA's ability to reduce contamination in poultry products. For example, contamination of poultry products can be affected by practices on poultry farms. To help overcome this challenge, the agency developed guidelines in 2010 on practices for controlling Salmonella and Campylobacter on farms, but the guidelines did not include information on the effectiveness of each of these practices, consistent with a recommendation from an agency advisory committee. USDA did not confirm that it plans to include this information in future guidelines. Without providing this information in future guidelines, USDA is not fully informing the poultry industry of the potential benefits of adopting these practices and encouraging their implementation.

What GAO Recommends

Salmonella and Campylobacter on farms include information on the effectiveness of each practice. USDA agreed with GAO's recommendations.