Avian Influenza: USDA Has Taken Actions to Reduce Risks but Needs a Plan to Evaluate Its Efforts
Released: 2017-05-11T00:00:00


Highlights: section_title: Why GAO Did This Study
paragraphs: Avian influenza is an extremely infectious and potentially fatal disease in poultry. In 2014 and 2016, two outbreaks of avian influenza led to the deaths of millions of poultry in 15 states and prompted emergency spending to control the disease. While the health risk to humans is low, humans have been infected with these viruses, sometimes fatally. A spike in fatal human infections in Asia began in late 2016.

GAO was asked to review several issues related to avian influenza. This report examines (1) how outbreaks of avian influenza have affected human health, animal health, and the U.S. economy, (2) the extent to which USDA has taken actions to address any lessons learned from its responses to the outbreaks in 2014 and 2016, and how it plans to evaluate the actions' effectiveness, and (3) ongoing challenges and associated issues, if any, federal agencies face in their efforts to mitigate the potential harmful effects of avian influenza. GAO reviewed global and domestic data on the effects of avian influenza and USDA reports and corrective action data associated with its responses to the recent outbreaks, and interviewed federal officials and stakeholders from state agencies and the poultry industry.

section_title: What GAO Found
paragraphs: When avian influenza outbreaks occur, they can have significant effects on human and animal health and the U.S. economy. With regard to human health, avian influenza rarely affects humans, but the World Health Organization estimates that two particular types of the virus have caused more than 2,100 human infections and more than 800 deaths since 1997, primarily in Asia and the Middle East. With regard to animal health, avian influenza outbreaks can lead to large numbers of poultry deaths as a result of efforts to control and prevent the spread of the disease. For example, from December 2014 to June 2015, more than 50 million birds were destroyed in the largest outbreak in U.S. history. The effect of avian influenza on the health of other animal species varies. Swine are susceptible to both avian and human influenza viruses that, if mixed, could create a new virus to which humans are vulnerable. An outbreak can also have significant economic consequences; for example, the economic impacts of the 2014 outbreak in the United States have been estimated to range from $1.0 to $3.3 billion.

USDA identified 15 areas with lessons learned from its responses to the 2014 and 2016 outbreaks of avian influenza and 308 associated corrective actions. For example, one lesson learned in the area of depopulation (mass culling of flocks) is that there were not enough skilled personnel available for depopulating infected poultry, leading to delays and possibly increasing the spread of disease. USDA has identified as completed about 70 percent of the 308 corrective actions to address all of the lessons learned. However, the agency has not evaluated the extent to which completed corrective actions—such as encouraging states to form depopulation teams—have helped resolve the problems identified, and it does not have plans for doing so. GAO has previously found that agencies may use evaluations to ascertain the success of corrective actions, and that a well-developed plan for conducting evaluations can help ensure that agencies obtain the information necessary to make effective program and policy decisions. Such a plan would help USDA ascertain the effectiveness of the actions it took to resolve problems identified during recent outbreaks.

On the basis of GAO's analysis of federal efforts to respond to outbreaks and of stakeholders' views, GAO identified ongoing challenges and associated issues that federal agencies face in mitigating the potential harmful effects of avian influenza. For example:

One challenge is that federal efforts to protect poultry from avian influenza rely on voluntary actions by a wide range of poultry producers to take routine preventative measures—known as biosecurity— to protect their flocks from disease. USDA has two major initiatives under way to encourage improvements to biosecurity.

An associated issue that federal agencies face is that the chickens used to produce the eggs needed to manufacture critical human influenza vaccine are susceptible to influenza outbreaks. The Department of Health and Human Services is supporting the development of new vaccine manufacturing technologies to reduce reliance on eggs.

section_title: What GAO Recommends
paragraphs: GAO recommends that USDA develop a plan for evaluating the effectiveness of the corrective actions it has taken. USDA agreed with GAO's recommendation.

section_title: Letter
paragraphs: Avian influenza is a highly infectious and, in some circumstances, fatal  disease in poultry, including chickens, turkeys, ducks, geese, and other  domesticated fowl. Most avian influenza viruses have low pathogenicity,  meaning that they cause no signs or only minor clinical signs of infection  in poultry. In contrast, highly pathogenic avian influenza can cause a high  death rate in poultry. Two separate outbreaks of highly pathogenic avian  influenza in the United States, one in 2014 and another in 2016, led to the  deaths of millions of domesticated poultry in 15 states, caused economic  losses for the U.S. poultry industry, and prompted emergency  government spending on control measures. According to the Department of Health and Human Services’ (HHS) Centers for Disease Control and  Prevention (CDC), while the risk posed to the general public by the avian  influenza viruses that circulated in the 2014 and 2016 outbreaks was low,  people in other countries have been infected, sometimes fatally, by  similar viruses. For example, a similar avian influenza virus caused a  spike in human infections and fatalities in China in late 2016 and early  2017, particularly among people in direct contact with poultry. The U.S.  outbreaks did not cause infections in humans. However, we previously  found in June 2007 that health experts were concerned that if a subtype  of avian influenza develops the capacity to spread easily from person to  person, a pandemic could occur. According to the World Health  Organization, controlling the virus in poultry is the principal way to reduce  opportunities for human infection and, therefore, for a pandemic to  emerge.

The U.S. Department of Agriculture (USDA) is responsible for acting to  prevent, control, and eradicate any disease or pest of livestock, including  foreign animal diseases such as highly pathogenic avian influenza, in  domestic livestock and poultry. In doing so, USDA typically partners with  states and industry in eradicating such diseases, with the agency’s level  of involvement dependent upon states’ preparedness and the size of the  outbreak. USDA’s Animal and Plant Health Inspection Service (APHIS),  state and local animal health officials, and the poultry industry collaborate  to eradicate avian influenza by, for example, depopulating (culling)  affected poultry flocks to halt spread of the disease, cleaning and  disinfecting premises and equipment, and testing for the presence of the  virus. USDA compensates—indemnifies—poultry producers for birds and  eggs lost to the disease and pays for cleaning, disinfection, and testing.

CDC collaborates with USDA and with state and local public health  agencies to monitor people who are involved in activities to control and  eradicate an outbreak to determine whether they experience influenza- like illness that may be associated with an outbreak in poultry. The  Department of the Interior’s (Interior) U.S. Geological Survey and U.S.  Fish and Wildlife Service collaborate with USDA, HHS, state and local  governments, and private interests to conduct surveillance of wild birds  and other animals for avian influenza.

You asked us to review several issues related to avian influenza. Our  objectives were to (1) provide information on how avian influenza has  affected human health, animal health, and the U.S. economy; (2) examine  the extent to which USDA has taken actions to address any lessons  learned from its responses to the avian influenza outbreaks in 2014 and  2016 and how it plans to evaluate the effectiveness of such actions; and  (3) identify what ongoing challenges and associated issues, if any, federal  agencies face in their efforts to mitigate the potential harmful effects of  avian influenza.

To provide information on how avian influenza has affected human  health, animal health, and the U.S. economy, we reviewed data from the  CDC, World Health Organization, and World Organisation for Animal  Health, among other sources. Specifically, to provide information on  human health, we reviewed global and U.S. data on avian influenza- related human mortality and morbidity dating back to 1918, the first  recorded pandemic of probable avian origin. Regarding animal health, we  reviewed USDA data and scientific literature on highly pathogenic avian  influenza outbreaks among poultry dating back to 1924, the first recorded  outbreak of highly pathogenic avian influenza in the United States. For  low pathogenic avian influenza outbreaks among poultry, we obtained  USDA data starting in 2002 that were readily available in proceedings of  the U.S. Animal Health Association’s annual meetings. For information  regarding influenza in other mammals, we reviewed agency information,  scientific literature, and interviewed federal, state, and industry officials.  For wild birds, we reviewed scientific literature on federal monitoring from 2006 to 2011 and monitoring data from 2014 to 2016, when Interior’s U.S.  Geological Survey and USDA began their current wild bird surveillance  program. Regarding impacts on the U.S. economy, we focused on the  2014 outbreak of highly pathogenic avian influenza since it was the  largest recent outbreak. We reviewed a variety of economic literature for  information on the estimated costs of the 2014 outbreak to U.S.  agriculture and consumers. We obtained data on USDA obligations for its  responses to that outbreak, the January 2016 outbreak, and a May 2016  low pathogenic avian influenza outbreak. To assess the reliability of the  data sources noted above, we reviewed the data and supporting  documentation and interviewed officials familiar with the data, and we  determined that the data were sufficiently reliable for providing  information on the effects of avian influenza on human and animal health  and the economy. We also asked for observations on the federal  responses to the outbreaks of avian influenza through interviews with  officials from USDA, HHS, Interior, and state and industry representatives  in six states. We selected the six states—California, Indiana, Iowa,  Minnesota, North Carolina, and Ohio—either because they were affected  by the 2014 and 2016 highly pathogenic avian influenza outbreaks or  because they have large poultry industries.

To examine the extent to which USDA has taken actions to address any  lessons learned from its responses to the 2014 and 2016 avian influenza  outbreaks and how it plans to evaluate the effectiveness of such actions,  we reviewed USDA’s after action reports of its responses to the 2014  outbreak in western and midwestern states and the 2016 outbreak in  Indiana. We also reviewed USDA’s Corrective Action Program database  for tracking the agency’s progress in completing tasks identified in its after  action reports and USDA documentation of specific steps taken in  response to lessons learned. To examine USDA’s tracking of corrective  actions in the database, we conducted an in-depth review of a  nongeneralizable sample of 10 corrective actions listed in the database.

For this sample, we randomly selected actions from each of six  preparedness and response areas that fit within the scope of our overall  review and that USDA classified in its database as priority 1 items with a  status of “closed,” “completed,” or “in progress.” We requested and  reviewed agency documents and information from officials describing the  steps taken to close, complete, or make progress on the actions in our  sample. Our review of this sample of actions provides general information  about the steps USDA has taken related to these 10 actions; however,  the results from this sample are not generalizable to all corrective actions  in the database. To assess the overall reliability of the Corrective Action  Program database for use in our report, we reviewed management  controls over the information systems that maintain the data and  interviewed USDA officials who manage the database. We determined  that the database was sufficiently reliable to describe the general status  of corrective actions and to provide examples of specific actions identified  for addressing lessons learned.

To determine what ongoing challenges and associated issues, if any,  federal agencies face in their efforts to mitigate the potential harmful  effects of avian influenza, we reviewed our prior findings and  recommendations on preparing for and responding to animal diseases;  the views of stakeholders from the six selected states about challenges  related to federal efforts to mitigate the potential harmful effects of highly  pathogenic avian influenza; and other sources of information related to  wildlife surveillance, domestic poultry and swine surveillance, biosecurity  measures to reduce the risk of disease, depopulation of poultry, disposal  of poultry carcasses, vaccines for poultry, research on disease  transmission and prevention, and protecting the egg supply for human  vaccine production. We selected these categories on the basis of  preliminary discussions with agency officials and industry representatives  and our 2007 report on avian influenza. We gathered the views of  stakeholders through interviews with 6 state veterinarians; 10 state public  health officials, including public health veterinarians and epidemiologists;  and 6 poultry industry representatives from the six states selected. We  also interviewed an official from the Canadian Food Inspection Agency  (CFIA) about the responses to 2014 and 2015 outbreaks of highly  pathogenic avian influenza in British Columbia and Ontario that involved  the same viruses that caused the U.S. outbreaks.

We conducted this performance audit from March 2016 to March 2017 in  accordance with generally accepted government auditing standards.  Those standards require that we plan and perform the audit to obtain  sufficient, appropriate evidence to provide a reasonable basis for our  findings and conclusions based on our audit objectives. We believe that  the evidence obtained provides a reasonable basis for our findings and  conclusions based on our audit objectives.
subsections: section_title: Background
paragraphs: This section provides information on avian influenza viruses; avian  influenza transmission in and between humans and animals; commercial  and noncommercial poultry production in the United States; our prior work  on avian influenza; and the responsibilities that USDA, HHS, and Interior  have with respect to avian influenza response, research, surveillance,  and other related activities.
subsections: section_title: Avian Influenza Viruses
paragraphs: Avian influenza is caused by a “Type A” influenza virus (influenza A).  Avian-origin  influenza viruses are broadly categorized based on a  combination of two groups of proteins on the surface of the influenza A  virus: hemagglutinin or “H” proteins, of which there are 16 (H1-H16), and  neuraminidase or “N” proteins, of which there are 9 (N1-N9). Many  different combinations of “H” and “N” proteins are possible. Each H and N  combination is considered a different subtype, and related viruses within  a subtype may be referred to as a lineage. Avian influenza viruses can be  divided into two groups based on the specific genetic features and  severity of the disease they cause in 4- to 8-week old chickens in a  laboratory setting: low pathogenic and the more severe highly pathogenic.  Influenza A has the potential to cause human pandemics, regardless of  its pathogenicity in poultry.

section_title: Avian Influenza Transmission
paragraphs: Wild aquatic birds—such as waterfowl, gulls, and shorebirds—are the  natural hosts for influenza A viruses. Direct or indirect contact with  infected wild birds can expose poultry to avian influenza viruses.  Similarly, infected poultry may spread avian influenza into wild bird  populations. Avian influenza viruses can also be moved from place to  place—including between farms—by people, equipment, vehicles, feed,  insects, rodents and other animals, water, and wind-blown dust as shown  in figure 1. Poultry producers may implement biosecurity measures to  reduce the risk that diseases such as avian influenza will be transmitted  to their flocks. For example, producers may disinfect vehicles arriving at  and leaving a farm or direct employees to disinfect boots and hands  before entering a poultry barn. During an outbreak in poultry, additional  biosecurity measures may be used to prevent the disease from further  spreading. For example, USDA personnel and contractors working to  control an outbreak would be expected to restrict their movements among  locations to prevent carrying the virus to an uninfected site.

One form of highly pathogenic avian influenza has become endemic in  several countries, including China, Indonesia, and Vietnam; this means  that the virus has become entrenched in poultry populations in those  countries. USDA considers highly pathogenic avian influenza a “foreign  animal disease” in the United States, meaning U.S. poultry are normally  free from the disease. The United States, as a member of the World  Organisation for Animal Health, has agreed (through USDA), along with  other member countries, to notify the organization and its members of any  detection of highly pathogenic avian influenza. Member countries also  agree to report cases of low pathogenic H5 or H7 avian influenza found in  poultry or other birds because these viruses have the potential to mutate  to a highly pathogenic form in poultry and may infect other species. When  a country’s poultry tests positive for “notifiable” avian influenza, its  international trading partners may restrict trade with that country until the  partners believe the virus is eradicated—an outcome that can take many  months to achieve. Therefore, when a flock is infected with notifiable H5  or H7 avian influenza, the goal of the poultry industry and government  agencies is to control and eradicate the virus as rapidly as possible in  order to prevent its spread and regain the confidence of trading partners  that any future imports of poultry or poultry products will be virus free. To  this end, USDA and other federal, state, and industry partners aim to act  quickly in the affected area to, among other things: (1) quarantine  susceptible animals; (2) implement biosecurity measures; (3) depopulate  infected and exposed birds; (4) dispose of contaminated and potentially  contaminated materials, including animal carcasses; and (5) clean and  disinfect the infected premises. Once the virus is eradicated, USDA,  states, and the poultry industry resume routine surveillance for notifiable  avian influenza.

section_title: Poultry in the United States
paragraphs: According to USDA’s Economic Research Service, the U.S. poultry  industry is the world’s largest producer and second-largest exporter of  poultry. The most recent Census of Agriculture reported 233,770 poultry  farms in the United States in 2012, but the U.S. poultry industry consists,  in large part, of a relatively small number of large companies that own all  aspects of the production process—from the hatchery to the processing  facility. The most common types of poultry raised commercially are  chickens for consumption (broilers) and chickens that lay eggs (layers),  as well as turkeys. There are also poultry that are genetic breeding stock  and whose main function is to produce offspring that facilitate mass  production and are economical to raise. Additionally,  there are poultry  raised specifically for producing eggs to make human vaccines.  Commercial poultry operations typically raise tens of thousands of birds in  confined poultry houses. Such operations can include multiple houses  located close to each other. Because of the environment in which  commercial birds are raised, if one bird becomes infected with a notifiable  avian influenza, hundreds of thousands of birds can be exposed and will  need to be depopulated.

In addition to poultry raised commercially, numerous types of birds are  raised in backyards, with flocks of up to 1,000 birds. These “backyard  birds” are typically chickens used for personal egg production and  consumption; they also can include game birds, such as quail and  pheasant. These birds may roam free or be confined to a poultry house.  In addition, there are birds in live bird markets—facilities that sell live  poultry, typically slaughtered on-site, to the general public—and some are  sold at auctions and swap meets.

section_title: Our Related Prior Work
paragraphs: In a June 2007 report, we found that USDA had made important strides to  prepare for highly pathogenic avian influenza outbreaks but that  incomplete planning and other unresolved issues could slow a  response. There were several unresolved issues at the time that, absent  advance consideration, could hinder response. For example, we found  that disposal of carcasses and materials infected with highly pathogenic  avian influenza could be problematic because operators of landfills were  reluctant to accept materials infected with even low pathogenic avian  influenza because of the perceived human health risk. To increase the  likelihood of rapidly containing a highly pathogenic avian influenza  outbreak, we made seven recommendations to USDA, including that the  agency develop a response plan that identifies critical tasks for  responding to an outbreak and address concerns about antiviral  medication for humans. USDA generally agreed with our  recommendations and took action to implement all seven  recommendations. (A list of prior related GAO work is included at the end  of this report.)

section_title: Federal Agencies’ Roles in Avian Influenza Response, Research, Surveillance, and Other Related Activities
paragraphs: Multiple  organizations within USDA support its animal health mission.  When notifiable avian influenza outbreaks occur, APHIS is the lead  agency within USDA for preventing and responding to animal disease  outbreaks. USDA derives its authority to carry out operations and  measures to prevent, detect, control, and eradicate notifiable avian  influenza, among other diseases, from the Animal Health Protection Act.  The act authorizes the Secretary of Agriculture to hold, seize, quarantine,  treat, destroy, or dispose of any animal, means of conveyance, or object  that can harbor the disease, or to restrict their movement in interstate  commerce. The act also authorizes the Secretary to transfer necessary  funds from other USDA appropriations or available funds to manage an  emergency in which a disease of livestock threatens any segment of  agricultural production in the United States, in order to arrest, control,  eradicate, or prevent the spread of the disease. USDA’s Wildlife Services,  a program unit within APHIS, conducts research on wildlife diseases,  such as avian influenza, that may affect agriculture and human health and  safety. USDA’s Agricultural Research Service conducts research on,  among other things, poultry diseases and vaccines for those diseases.  For example, the agency published a report in 2014 on experts’ analyses  of gaps in knowledge about influenzas in poultry and other animals and  about effective countermeasures to control and mitigate outbreaks of  disease.

HHS is responsible for, among other things, research on human disease,  disease surveillance, and vaccine production and distribution. Within  HHS, the Influenza Division of CDC’s National Center for Immunization  and Respiratory Diseases conducts surveillance of influenza in humans,  including human infections caused by viruses with animal origins; the  division also conducts laboratory studies on influenza viruses of concern  to characterize them and assess their risks to humans. HHS’s Food and  Drug Administration (FDA) is responsible for protecting the public health  by ensuring the safety and efficacy of veterinary drugs and medical  devices and by licensing biological products that are safe, pure, and  potent, including vaccines for pandemic influenza. In addition, FDA is  responsible for ensuring the safety and proper labeling of more than 80  percent of the U.S. food supply.

In cooperation with USDA’s Wildlife Services program and state  agencies, Interior participates in the federal government’s surveillance of  wild migratory birds for the presence of avian influenza and provides  leadership and support in the area of wildlife disease research and  diagnostics. Interior’s U.S. Geological Survey maintains the National  Wildlife Health Center, which identifies, controls, and prevents wildlife  losses from diseases; conducts research to understand the impact of  diseases on wildlife populations; and devises methods to more effectively  manage these disease threats. (See app. I for more detail on the roles of  federal departments and their component agencies as related to avian  influenza.)

section_title: Avian Influenza Has Harmed Human Health, Animal Health, and the U.S. Economy
paragraphs: Avian influenza viruses have harmed global human and animal health  and the U.S. economy. These viruses rarely infect humans, but some  viruses may have high rates of mortality when they do. Avian influenza  outbreaks have led to the deaths of hundreds of millions of domesticated  poultry in dozens of countries, either directly or through depopulation to  prevent spread of the disease. The 2014 and 2016 outbreaks among U.S.  poultry led to costs to the federal government of about $930 million and  additional costs to the U.S. economy of an estimated $1 billion or more.
subsections: section_title: Avian Influenza Rarely Infects Humans, but the Mortality Rate for Those Infected Has Been Relatively High
paragraphs: As of March 2017, two lineages of avian influenza—Asian H5N1, which  emerged in 1997, and a new strain of H7N9, which emerged in 2013— have together infected more than 2,100 humans and killed more than  900, primarily in Asia and Africa. Neither lineage has developed the  capacity to be easily transmissible from birds to humans or from person to  person. However, there have been other instances in which influenza A  viruses of avian origin have become more easily transmissible and have  caused global pandemics that led to large numbers of fatalities in the  United States and around the world. Table 1 summarizes occurrences of  fatal influenza A infections in humans that are known to have or are  suspected of having an avian origin. The likelihood that an influenza A  virus of avian origin will evolve into a form easily transmissible among  humans is small, according to officials from HHS, but if such a change  occurs, it could lead to serious disease among humans and possibly  another pandemic. For example, the World Health Organization has  expressed concern that the Asian lineage H5N1 and H7N9 viruses that  have sporadically infected humans in Asia, Northern Africa, and the  Middle East could evolve to become more easily transmissible to or  between humans and lead to serious disease or another pandemic.  According to CDC’s website, of the novel influenza A viruses that are of  special concern to public health, the agency rates the Asian lineage H7N9  virus as having the greatest potential to cause a pandemic, as well as  potentially posing the greatest risk to severely impact public health.

section_title: Outbreaks of Avian Influenza Have Killed Millions of Poultry Worldwide but Caused Few Fatalities in Other Species
paragraphs: Avian influenza outbreaks—both highly pathogenic and low pathogenic— have led to the deaths of hundreds of millions of domesticated poultry in  dozens of countries, either directly or through depopulation to prevent  spread of the disease. For example, the H5N1 highly pathogenic avian  influenza outbreak that led to human fatalities in China in 1997 also led to  the deaths of an estimated 220 million birds in China and Hong Kong. In  the United States, outbreaks of highly pathogenic avian influenza have  led to the deaths of more than 67 million birds since 1983, with the most  recent outbreaks beginning in December 2014 and ending in June 2015  and, in unrelated incidents, in January 2016 and March 2017. (See table  2 for details of known outbreaks of highly pathogenic avian influenza in  commercial U.S. poultry.)

USDA identified the first U.S. cases of the 2014 outbreak of highly  pathogenic avian influenza H5 viruses in captive wild birds or backyard  flocks in Washington and Oregon in December 2014 and in Idaho the  following month. Also in December 2014, USDA identified another  subtype, H5N8, in Washington and Oregon. By the time USDA and its  state and industry partners eradicated the diseases in June 2015, the  related H5N2 and H5N8 viruses had infected poultry flocks on 232 farms  in 15 states, with the largest number of affected farms being in Minnesota  (110 farms) and Iowa (77 farms). (See fig. 2 for a map showing the 15  states and the approximate number of birds killed or depopulated as a  result of the outbreak that began in 2014.)

Avian influenza is an extremely infectious and,  in some circumstances, fatal disease in  poultry, including chickens and turkeys. Avian  influenza viruses are classified as either “low   pathogenic” or “highly pathogenic” based on  their genetic features and the severity of the  disease they cause in poultry. Beginning in  early December 2014, the Canadian Food  Inspection Agency (CFIA), w hich leads  responses to avian influenza outbreaks in  Canada, learned of highly pathogenic avian  influenza on 13 poultry farms in British  Columbia;  these included turkey and chicken  farms. To eradicate the virus, CFIA  depopulated 240,000 birds. Wild birds  migrating along the Pacific Flyw ay were the  most likely cause of the outbreak, according  to CFIA. In April 2015, CFIA identified highly  pathogenic avian influenza in 1 chicken farm  and 2 turkey farms in Ontario. The agency  controlled the virus by depopulating 79,700  birds. According to a CFIA  official, two  characteristics of the Canadian poultry  industry that facilitate the adopting of  biosecurity measures in poultry farms helped  limit  the size of the 2014 and 2015 Canadian  outbreaks. First, poultry farms in Canada are  relatively small compared w ith those in the  United States, w hich reduces the number of  birds infected and the chance that influenza  w ill replicate and spread. Second, Canadian  poultry companies are not heavily integrated;  therefore there is little movement of birds,  feed, equipment, and people that could carry  the virus from one farm to another.

State(s)

Reported number and type of birds  depopulated  4.7 million turkeys, including breeders, and  chicken broilers, breeders, and layers  Layers  Turkey breeders  100,000 layers  30,000 layers  84,000 broilers  328,000 broilers  51,000 breeder chickens  145,000 turkeys  54,000 turkeys  25,600 turkeys   30,300 game birds  16,000 breeder chickens  500,000 turkeys  20,000 broiler breeders  29,000 turkeys  3,000 turkeys  9,800 broiler breeders  95,000 quail and 21,000 Peking ducks  352,114 turkeys and layers  39,000 turkeys  84,000 turkeys held in quarantine  100,585 broiler breeders and backyard birds   24,700 broiler breeders and backyard birds  The Indiana outbreak w as restricted in size and scope to a single county and 12 premises. This table  reports on poultry at sites associated with low  pathogenic avian influenza. In all, more than 414,000  birds w ere affected.
subsections: section_title: Cats Infected with Avian Influenza in New York City Animal Shelters
paragraphs: According to the Centers for Disease Control  and Prevention (CDC), in November 2016, a  low  pathogenic avian influenza A (H7N2) virus  infected cats in New  York City animal  shelters. Some affected cats showed mild flu- like symptoms such as sneezing or runny  noses, and 450 w ere quarantined until they  no longer show ed symptoms of infection. A  veterinarian collecting respiratory samples  from exposed cats contracted the virus and  subsequently recovered. According to CDC’s  w ebsite, known human infections with H7N2  are uncommon and have not led to deaths.  How ever, the agency noted that finding avian  influenza virus in an unexpected animal, such  as a cat, is alw ays concerning because it  means the virus has changed in a w ay that  may pose a new  health threat.

The effect of avian influenza on the health of other animal species varies.  Avian influenza generally causes few signs of illness and is rarely fatal  when it circulates in waterfowl and shorebirds. Because wild birds are  rarely sickened by the virus, they are able to move it efficiently along  migratory flyways. Interior officials told us, however, that incidents in  which wild birds have been killed by highly pathogenic avian influenza  have become more common; these officials noted in particular incidents  in Asia involving the H7N9 virus. According to the World Health  Organization, some mammal species, including swine, can be infected  with avian influenza but may show few, if any, observable symptoms, and  others, such as ferrets, may experience high morbidity and mortality.  Infections in waterfowl and swine are of concern because they can  spread the virus to poultry and humans, according to the World  Organisation for Animal Health. Swine can also serve as “mixing  vessels” in which different influenza viruses come into contact, exchange  genetic material, and possibly produce a new virus that is more easily  transmissible to or between humans. The H1N1 virus that emerged in  2009 contained gene segments from swine, avian, and human influenza  viruses. According to the World Health Organization, the virus caused a  global pandemic with up to 550,000 human deaths worldwide from April  2009 to April 2010; the CDC estimates that up to 18,000 of those human  deaths occurred in the United States. In addition, a 1976 outbreak of  H1N1 swine influenza at Fort Dix, New Jersey, infected up to 230 humans  and killed 1 person. More recently, according to CDC documents, more  than 360 people in the United States were infected with influenza A  (H3N2) variant influenza from August 2011 through September 2016, with  one fatality. Also according to CDC, these infections have mostly been  associated with prolonged exposure to pigs at agricultural fairs.

section_title: Recent Outbreaks Have Cost the Federal Government and the U.S. Economy Billions of Dollars
paragraphs: Outbreaks of avian influenza in poultry in the United States in 2014 and  2016 cost the federal government about $930 million, according to USDA  documents, and the 2014 outbreak cost the economy from $1 billion to  $3.3 billion, according to two studies by USDA and a private firm.  According to USDA budget documents for fiscal years 2015 and 2016,  the agency obligated a total of about $869 million for the responses to the  2014 outbreak in 15 states, the January 2016 outbreak in Indiana,  and a  May 2016 outbreak of low pathogenic avian influenza in Missouri. As  shown in table 4, the largest portion of these obligations was for response  operations, including depopulation, disposal, composting, and cleaning  and disinfection. Indemnity payments to poultry producers were another  large category of obligations. Nearly all of the funds were transferred from  the Commodity Credit Corporation.

In addition, USDA obligated about $60 million in funds transferred from  the Commodity Credit Corporation in fiscal year 2015 on fixed costs— such as salaries, benefits, and supplies—and other activities related to  preparing for the possible return of the virus in the fall of 2015, such as  wild bird surveillance and vaccine research.

With respect to the U.S. economy, two separate analyses have examined  and produced national estimates of the economic impacts from the highly  pathogenic avian influenza outbreak that began in 2014. A national  analysis conducted by USDA economists measured the 2014 outbreak’s  impact to U.S. livestock and feed sectors, including poultry and poultry  products, at $1 billion. The estimates in the analysis take into  consideration producer and consumer behavior as prices and production  changed in response to the reduction in production and the trade  embargoes linked to the outbreak. The effects were measured throughout  the course of the outbreak, allowing for estimates based on changes over  time. According to this analysis, U.S. turkey producers lost an estimated  $214 million in sales (a decline of 6.8 percent from 2014 levels), and  broiler producers lost $276 million (a decline of 1.5 percent from 2014).

While broilers were only negligibly affected by the virus, as separately  reported by APHIS, the sector still suffered losses because of large  decreases in demand from countries that extended full or partial bans on  poultry and poultry products, including broilers, from the United States. In  addition, because crops (e.g., corn and soybeans) are essential to the  poultry sector, those commodities also experienced losses estimated at  $373 million because of the reduction in number of birds fed. On the other  hand, the reduced egg supply caused by the outbreak raised the price of  eggs for consumers and, according to the analysis, led to an increase of  $53 million in sales for U.S. egg and layer producers (an increase of 26.7  percent from 2015 levels).

The second national analysis contained a preliminary estimate of $3.3  billion in total economy-wide losses through June 29, 2015, from the 2014  outbreak of highly pathogenic avian influenza. This included direct  losses to the turkey and egg processing sectors of $1.6 billion, with  losses of $530 million for turkeys and $1.04 billion for laying hens. The  $3.3 billion estimate included macroeconomic impacts due to losses to  other indirect sectors, such as retail and foodservice, but did not include  activities such as clean-up, restocking, or future lost production while the  producer prepares to resume production at a pre-disease level. Also,  unlike the first analysis noted above, this analysis did not include  consumer or producer responses to changes in prices or production, such  as increases in egg prices due to production losses.

Starting from the beginning of the avian influenza outbreak in December  2014, 18 trading partner nations imposed bans on all shipments of U.S.  poultry and products, and 38 trading partners imposed partial, or regional,  bans on shipments from states or parts of states experiencing outbreaks.  According to USDA officials, as of January 2017, China, Kyrgyzstan,  Russia, and Thailand continued to impose national bans on U.S. poultry  imports that were attributed to concerns about highly pathogenic avian  influenza, and Jamaica had imposed a state ban on U.S. poultry imports  from several Midwestern states. Total U.S. poultry and product exports  declined in value from about $6.4 billion in 2014 to $4.9 billion in 2015.  The largest of these declines was from the U.S. broiler meat industry,  which fell from $4.1 billion to $3.0 billion over that period. While a USDA  report attributed part of this decline in exports to a strong U.S. dollar, the  report also noted that the avian influenza outbreak that began in 2014  caused the poultry industry to lose market share to other poultry exporters  such as Brazil. According to a September 2016 USDA report, export  levels of broiler chickens—the largest poultry export sector—were  modestly rebounding in 2016 from the levels that followed the end of the  highly pathogenic avian influenza outbreak in 2015, although these 2016  levels were still at their lowest since 2011. In addition, according to the  USDA report, turkey exports remained weak compared to the pre-avian  influenza trends, and egg exports in July 2016 were 6 percent lower than  the previous year. USDA noted that some major importing countries had  lifted trade bans since the 2014 outbreak and that other factors, such as  the strength of the dollar, have also affected exports. USDA officials  involved in the response also said that the negative effect on U.S. poultry  exports was partially mitigated by the fact that some countries imposed  regional, rather than national, bans on U.S. poultry products. In addition,  the agency’s implementation of secure food supply plans allowed poultry  producers to move non-infected products during the outbreaks. A goal  of these plans is to continue business operations from locations that are  not infected with disease.

After the March 2017 detections of highly pathogenic H7N9 avian  influenza in two commercial flocks in Lincoln County, Tennessee,  numerous countries imposed trade restrictions on U.S. poultry exports.  For example, the Republic of Congo (Brazzaville) imposed restrictions on  poultry imports from the entire United States. Some countries, such as  South Africa, Taiwan, and Uruguay, placed restrictions on poultry imports  from the entire state of Tennessee while others, such as Jamaica and the  European Union, imposed restrictions on certain geographic areas or  counties. Similarly, after detections of low pathogenic avian influenza in  March 2017, countries placed restrictions on imported poultry from all or  parts of Alabama, Georgia, Kentucky, and Wisconsin.

section_title: USDA Has Taken Corrective Actions to Address Lessons Learned but Does Not Have Plans to Evaluate Their Effectiveness
paragraphs: USDA identified lessons learned from its responses to the 2014 and 2016  highly pathogenic avian influenza outbreaks and has taken numerous  corrective actions to address them. However, USDA does not have plans  for evaluating the extent to which the corrective actions have helped  resolve the problems that they were intended to address.
subsections: section_title: USDA Has Identified Lessons Learned from the 2014 and 2016 Outbreaks and Taken Numerous Corrective Actions
paragraphs: After the outbreaks of highly pathogenic avian influenza in 2014 and  2016, USDA identified lessons learned related to its response activities  and has taken numerous corrective actions to address those lessons  learned. To identify the lessons learned from both the widespread  outbreak that began in 2014 and the limited 2016 outbreak in Indiana,  USDA proactively collected feedback about its performance during and  after the outbreaks from federal and state animal health officials and from  industry representatives involved in the responses. The agency then  summarized this feedback into after action reports that included  observations about strengths and weaknesses in the responses. The  identified lessons learned covered a wide range of response areas,  including the depopulation  of infected birds, disposal of bird carcasses,  and surveillance of flocks for infection. For example, according to USDA  documents, rapid depopulation is critical to help prevent or mitigate the  spread of the disease by eliminating infected, exposed, or potentially  exposed animals. However, USDA noted that during the 2014 outbreak,  there were substantial delays in completing depopulation, with producers  reporting that it took as long as 11 days to begin depopulation on many  premises.

USDA developed a corrective action program to identify, prioritize, and  implement corrective actions that are intended to address the root causes  of the lessons learned. The agency identified 308 corrective actions  across 15 response areas and created a corrective action database to  track the actions (see table 5 for the list of 15 response areas and  examples of lessons learned and corrective actions associated with each  area.)

USDA prioritized the corrective actions according to their implications for  future outbreaks and, for the highest priority actions, their time frame for  completion. Specifically, USDA defined priority 1 corrective actions as  those that would have immediate, critical implications for a future  outbreak and that could be completed in less than 1 year; priority 2  actions as those that would have positive implications for a future  outbreak or would have immediate, important implications but that may  not be completed within 1 year; and priority 3 actions as those that are  under consideration or that would have less critical implications for a  future outbreak.

According to our review and summary of USDA’s corrective action  database, the agency has marked as completed about 70 percent of its  corrective actions, including about 86 percent of the priority 1 actions (see  table 6). As of January 2017, USDA did not have time frames for  completing about 82 percent of the uncompleted priority 2 and priority 3  corrective actions. For example, USDA has not established a time frame  for completing a priority 2 corrective action related to depopulation that  calls for the agency to develop training materials for contracted  responders to help ensure there are enough skilled personnel available  for depopulation. This action is marked as “in progress” in the database.  When we raised this issue during the course of our review, USDA officials  responsible for the database said they are working with the groups in  charge of taking corrective actions to identify time frames for the  remaining priority 2 and priority 3 actions, but they said that it is complex  and difficult to do so in light of other agency disease response activities.  For example, they said that responding to an outbreak of New World  screwworm in Florida in fall 2016 had caused the agency to pause some  of its efforts to address corrective actions from the highly pathogenic  avian influenza outbreaks. Nonetheless, agency officials acknowledged  that time frames are important and said they will continue to develop  them.

section_title: USDA Does Not Have Plans to Evaluate the Effectiveness of its Corrective Actions
paragraphs: USDA has taken steps to implement corrective actions, but it does not  have plans to evaluate the extent to which completed corrective actions  have effectively helped to resolve the problems the agency identified in its  responses to the recent outbreaks. We have previously found that  agencies may use evaluations to ascertain the success of corrective  actions, and that a well-developed plan for conducting evaluations can  help ensure that agencies obtain the information necessary to make  effective program and policy decisions. An evaluation plan should  include, among other things, evaluative  criteria or comparisons, or how or  on what basis program performance will be judged or evaluated. We also  found that one approach agencies can use to evaluate changes in events  that occur infrequently and unpredictably, such as disease outbreaks, is  to conduct simulations or exercises to assess how well an agency’s plans  anticipate the nature of its threats and vulnerabilities. Homeland Security  Exercise and Evaluation Program guidance, which USDA officials told us  they used in developing the corrective action program, states that  agencies should put in place a system to test and validate corrective  actions that have been implemented. This guidance states that  agencies can identify the corrective actions that require validation and  then conduct exercises to test whether those corrective actions have led  to improvements.

In our review of a nongeneralizable sample of 10 completed corrective  actions designated as priority 1, it was unclear to what extent such  actions were effective because, while USDA marked in its database that it  had completed the corrective actions, it had not evaluated the extent to  which these actions achieved the desired outcome. For example, one  lesson learned that USDA identified was that many producers lack a  strong culture of biosecurity. However, although USDA completed  corrective actions associated with that lesson—creating a joint biosecurity  website with the U.S. Poultry and Egg Association and putting greater  emphasis on biosecurity in conferences with producers—it did not  evaluate to what extent taking these actions created a strong culture of  biosecurity among producers. In another lesson learned, USDA identified  that states and producers encountered impediments in transporting bird  carcasses to landfills, such as federal and state rules restricting the  movement of bird carcasses along transportation routes in close proximity  to other producers. USDA completed corrective actions associated with  that lesson—providing guidance, training, and encouragement to states  and producers to develop disposal plans—but did not evaluate to what  extent taking these actions helped overcome the impediments observed.  In addition, depopulation experts we interviewed raised concerns about  whether USDA’s planned and completed corrective actions will effectively  address the challenges with depopulation experienced during the 2014  and 2016 outbreaks. For example, these experts questioned whether a  sufficient number of federal employees and contracted responders have  been trained in using depopulation equipment to address a lesson  learned that there were not enough skilled personnel available for  depopulation during recent outbreaks.

USDA documents state that the 2016 outbreak provided an opportunity to  see that some of the corrective actions taken following the 2014 outbreak  resulted in an improved response. For example, according to USDA’s  after action report on the 2016 outbreak, the changes that USDA made to  the process for compensating poultry producers for losses after the 2014  outbreak resulted in a faster and more efficient process during the 2016  outbreak. Nonetheless, USDA officials acknowledged that they are not  certain whether completing other corrective actions will be sufficient to  address the lessons learned from both outbreaks. They acknowledged  the importance of evaluating corrective actions to determine whether  additional steps are needed but said that the agency does not yet have  plans to do so. Agency officials also told us that evaluating the  effectiveness of these corrective actions will need to be a continuous  process and should be considered within the broader context of USDA’s  emergency preparedness for disease response. For example, USDA  officials told us they intend to incorporate lessons learned and corrective  actions from the agency’s response to the 2016 New World screwworm  outbreak into the corrective action database for highly pathogenic avian  influenza, so that the database becomes a broader tool that the agency  can use to track corrective actions related to its overall disease response  efforts. By developing a plan for evaluating completed corrective actions  and, as part of this plan, considering whether any completed corrective  actions require validation through simulations or exercises, USDA could  better determine the effectiveness of these actions.

section_title: Federal Agencies Face Ongoing Challenges and Associated Issues in Their Efforts to Mitigate the Potential Harmful Effects of Avian Influenza
paragraphs: On the basis of stakeholders’ views and our analysis of federal efforts to  respond to outbreaks, we identified ongoing challenges and associated  issues that federal agencies face in mitigating the potential harmful  effects of avian influenza. These challenges are in protecting  domesticated poultry from the threat of avian influenza that circulates  naturally in wild birds and in relying on voluntary actions by a wide range  of poultry producers to prevent poultry flocks from becoming infected.  Federal agencies also face other issues associated with mitigating the  potential harmful effects of avian influenza: the virus could infect poultry  needed to produce eggs used in manufacturing critical human vaccines  against pandemic influenza, and federal funding will soon be exhausted  for a voluntary surveillance program that gathers information about the  presence of influenza viruses in swine that could pose a threat to human  health.
subsections: section_title: Ongoing Challenges that Federal Agencies Face in Mitigating the Potential Harmful Effects of Avian Influenza
paragraphs: We identified two ongoing challenges that federal agencies face in  mitigating the potential harmful effects of avian influenza. First, federal  agencies are challenged in protecting domesticated poultry from avian  influenza because the disease naturally circulates in migratory birds,  which may spread the disease. Second, federal efforts to prevent poultry  flocks from infection are challenged because these efforts rely on  voluntary biosecurity measures by poultry producers.
subsections: section_title: Protecting Domesticated Poultry from the Threat of Avian Influenza Carried by Wild Birds Is a Challenge
paragraphs: Federal agencies face an ongoing challenge in protecting domesticated  poultry from avian influenza because the disease naturally circulates in  migratory birds, such as ducks and geese, which are hard to control and  which may come into contact with poultry. Because of their migratory  behavior, wild birds infected with avian influenza can spread the disease  across long distances, including from as far away as Asia. Federal  agencies and others are authorized under the Migratory Bird Treaty Act to  sample ducks, geese, and other migratory birds to confirm the presence  of an infectious disease, including influenza. According to Interior  officials, the Act also provides agencies the authority to control migratory  birds infected with avian influenza, but the officials noted that experience  has shown that such efforts are ineffective. As reported in a text on avian  influenza, humans have had and will continue to have minimal impact on  control of low pathogenic avian influenza viruses in wild bird  populations.

Use of Vaccines to Eradicate Avian  Influenza  According to the U.S. Department of  Agriculture (USDA), poultry vaccination has  been part of control or eradication programs  for avian influenza viruses in a number of  countries. Effective vaccination can decrease  transmission betw een animals by decreasing  their susceptibility to infection and reducing  the amount of virus an infected animal may  shed. Vaccination has been used in some  successful eradication campaigns for low   pathogenic avian influenza outbreaks in the  United States but never for highly pathogenic  avian influenza outbreaks such as those that  occurred in 2014 and 2016, according to  USDA.  Stakeholders w e interviewed characterized  the decision to use poultry vaccines to control  and eradicate the 2014 and 2016 outbreaks  as having both scientific and economic  components. From a scientific perspective, a  vaccine needs to be able to protect against a  specific influenza virus to be effective and  merit use. In June 2015, USDA announced  that the vaccines available at the time w ere  not w ell matched to the virus that w as  infecting poultry in numerous states. As an  example of the economic implications of  vaccines, USDA also announced in June  2015 that significant trading partners had  indicated that, if USDA began vaccinating,  they w ould ban all U.S. poultry and egg  exports until they could complete a risk  assessment. For these and other reasons,  USDA decided against using vaccines.  USDA’s Agricultural Research Service  continues to develop enhanced vaccines for  use in poultry against avian influenza. A 2014  USDA report concluded the poultry industry  needs highly effective vaccines that can  prevent transmission and that can be mass- delivered in w ater, in eggs, or in feed.

Although federal agencies are unlikely to control avian influenza viruses  in wild birds, they can monitor the viruses circulating in this population.  Specifically, USDA, Interior’s U.S. Geological Survey and U.S. Fish and  Wildlife Service, and state and tribal agencies collaborated on a national  program for wild bird surveillance that sampled more than 283,000 wild  birds from April 2006 through March 2011, when the program ended.  The federal effort resumed in December 2014 in response to the  outbreaks of highly pathogenic avian influenza on the West Coast of  North America. In response to the outbreaks, personnel from USDA and  Interior re-convened the Interagency Wild Bird Avian Influenza Steering  Committee in January 2015. The Steering Committee developed a wild  bird surveillance plan for avian influenzas that may pose a threat to  human health or domestic poultry. The plan encourages federal and  state agencies and others to use a variety of sampling methods to test  live and dead wild birds for avian influenza. According to data recorded as  of March 24, 2017, the surveillance program had collected test results  from more than 88,000 wild birds since December 2014. The data for that  time period show that the program detected 102 cases (about 0.12  percent) of highly pathogenic avian influenza from the same lineage that  caused the 2014 and 2016 outbreaks in the United States (see app. II for  details on the results of this surveillance program). On the other hand,  monthly detection rates for low pathogenic avian influenza A viruses in  wild birds were often above 10 percent for those tested. According to  USDA and Interior officials, continued monitoring of wild birds will help  identify the presence of avian influenza subtypes and help agencies to  mitigate the persistent challenge that wild birds pose to domesticated  poultry. The state veterinarians we interviewed from California, Indiana,  Iowa, Minnesota, North Carolina, and Ohio generally agreed with the  need for wildlife surveillance.

section_title: Reliance on Voluntary Actions by a Wide Range of Poultry Producers to Prevent Flocks from Avian Influenza Infections Is a Challenge
paragraphs: Federal efforts to ensure routine biosecurity and prevent poultry flocks  from becoming infected with avian influenza face an ongoing challenge  because these efforts depend on voluntary actions by a wide range of  poultry producers. While USDA’s approach to addressing this challenge  varies for different types of poultry producers, such as those who manage  large commercial operations and those who manage small backyard  flocks, the approach primarily relies on using incentives and education to  promote voluntary actions.

According to USDA officials, state stakeholders, and poultry industry  representatives we interviewed, sound biosecurity practices are important  for all types of poultry facilities. This is also evident from the 2014 and  2016 outbreaks of highly pathogenic avian influenza, which affected large  commercial and small backyard flocks, including turkeys, laying hens, and  ducks. USDA found that lapses in routine preventative biosecurity allowed  the initial introduction of disease and enabled it to spread from farm to  farm. To gather information on biosecurity practices, USDA analyzed self- assessments completed by 850 poultry producers on the status of their  biosecurity practices. While large producers generally indicated more  frequently than small producers that they had certain practices in place,  the nongeneralizable data showed that important practices were not  consistently in place. For example, less than 60 percent of respondents  had biosecurity officers or training in place. According to USDA’s self- assessment document, biosecurity officers and training could help reduce  the threat of infection by improving biosecurity practices. Similarly, less  than 60 percent of respondents had delineated lines of separation in their  facilities to reduce the risk of contamination. Lines of separation are  intended to reduce the risk that contaminated materials come into contact  with poultry. In addition, less than 60 percent of respondents said that  they had practices in place for personnel to shower or change into clean  clothes immediately prior to arriving at a poultry site, or upon arrival, to  reduce the risk of introducing an avian influenza virus.

While USDA can impose biosecurity measures during its response to an  emergency, the agency does not have the authority to require producers  to routinely employ preventative biosecurity measures. Instead, USDA  relies on producers to take voluntary action to prevent the introduction of  avian influenza and other diseases. Toward that end, USDA recently  initiated two interrelated efforts—independent of the corrective action  program described above—that may help overcome this challenge  among commercial farms. In addition, USDA has continued its efforts,  through public education and outreach, to encourage backyard poultry  farmers to practice biosecurity.

USDA’s first initiative to improve biosecurity involves linking producers’  eligibility  for indemnity payments to a biosecurity plan. Specifically, USDA  issued an interim rule in February 2016 requiring large poultry producers  seeking indemnity payments in the future to provide a statement that, at  the time highly pathogenic avian influenza was detected in their facilities,  they had in place and were following a written biosecurity plan to address  the potential spread of the virus. According to USDA officials, this  regulatory change provides a strong incentive to members of the poultry  industry to have a biosecurity plan in place. As of February 2017, USDA  continues to operate under the interim rule issued in February 2016.

The second and related initiative concerns changes to the National  Poultry Improvement Plan. According to USDA officials, poultry industry  representatives who commented on the interim indemnity rulemaking  suggested that the agency use the National Poultry Improvement Plan to  promote biosecurity. The improvement plan is a voluntary program  administered by USDA under which participating commercial poultry  flocks are tested to ensure they are free from diseases, including H5 and  H7 subtypes of avian influenza. If a flock tests negative for avian  influenza, USDA certifies to trading partners and others that the flock is  free of the disease. In September 2016, delegates to the program—who  included poultry industry representatives—gave interim approval to add a  set of 14 biosecurity principles to the plan’s national program standards.  The biosecurity principles call for, among other things, training poultry  producers about biosecurity; taking steps to protect against infection from  wild birds, rodents, and insects; cleaning vehicles and equipment to  reduce risk; and managing manure and litter to prevent the exposure of  susceptible poultry to disease agents. Those principles would apply to the  poultry producers who participate in the program; according to USDA  officials, most commercial poultry producers participate. According to  USDA officials, these initiatives will encourage commercial producers to  adopt preventative biosecurity measures.

Commercial poultry flocks may also be raised outdoors and thus are at  greater risk of contact with wild birds infected with avian influenza. For  example, turkeys and chickens must have access to outdoor space to be  certified by USDA as organically raised. Organically raised poultry are a  rapidly growing segment of the industry, according to USDA documents.  Stakeholders told us that they were concerned that producers of  organically raised poultry do not have to follow the same biosecurity  principle—namely, keeping birds indoors—that producers of conventional  poultry are encouraged to follow. USDA has acknowledged that  organically raised birds are at a greater risk than birds raised indoors.  USDA’s policy is that if it is determined that temporary confinement of  birds is needed to protect the health, safety, and welfare of organic flocks,  then producers and certifiers may work together to determine an  appropriate method and duration of confinement of such flocks without a  loss of organic certification.

Stakeholders we interviewed told us backyard poultry flocks are a  concern for contracting and spreading avian influenzas to commercial  poultry because these flocks are raised outdoors and are more likely to  come into contact with wild birds. According to USDA’s website, raising  backyard poultry is a growing trend across the United States. USDA  manages the “Biosecurity for Birds” campaign to help raise awareness  among backyard, hobby, and pet bird owners about the risks of avian  influenza. The biosecurity principles that USDA promotes to backyard  poultry producers include separating the domesticated flock from other  birds, including game birds and wild waterfowl, because the latter can  carry disease. According to an agency document, USDA works  cooperatively with state animal health officials and the poultry industry to  look for disease in breeding flocks, in backyard poultry, and at live bird markets, livestock auctions, poultry dealer locations, and small bird sales,  fairs, and shows.

section_title: Federal Agencies Face Other Issues Associated with Mitigating the Potential Harmful Effects of Avian Influenza
paragraphs: We identified two other issues that federal agencies face associated with  mitigating the potential harmful effects of avian influenza. First, outbreaks  of the disease threaten the poultry that produce the eggs used in the  production of human pandemic influenza vaccine. Second, funding for a  voluntary surveillance program that gathers data on influenza A viruses in  swine that could pose a threat to human health will be exhausted in fiscal  year 2017.
subsections: section_title: Poultry Used to Produce Critical Human Vaccine Are Susceptible to Influenza Outbreaks
paragraphs: Protecting the chickens that lay the eggs needed to produce human  pandemic influenza vaccines is an issue for federal agencies because  these birds, like others, are susceptible to avian influenza. HHS has an  obligation under the National Strategy for Pandemic Influenza to promote  capabilities that assure a pandemic vaccine can be produced at a U.S.- licensed influenza vaccine facility at any time of the year, without  limitations imposed by the availability  of essential supplies. Pandemic  influenza vaccines may be manufactured using several technologies. To  date, the most commonly used technology has relied on fertilized eggs as  a raw material. According to HHS officials, 90 to 95 percent of the  current national stockpile of pandemic influenza vaccines is derived from  eggs. According to an HHS official, the agency has a stockpile of egg- based and cell-based pre-pandemic influenza vaccines supplied by four  companies. Of the four companies, however, only one has an egg-based  vaccine manufacturing facility in the United States. If an influenza  pandemic is declared, according to this official, the U.S. government may  not be able to rely on foreign countries to allow exports of pandemic  vaccine because each country will likely prioritize those vaccines for its  own population. Therefore, the U.S. government considers the one U.S.- based company as the only dependable manufacturer for producing egg- based vaccine for rapid pandemic mitigation.

This company contracts with suppliers to provide it with the necessary  egg supply. HHS officials and company representatives told us that the  company has an egg production network that includes flocks located on  numerous farms. According to company officials, protecting the company’s current network of egg suppliers is critical because the  company cannot rely on other suppliers for eggs if its own network is  compromised; the officials told us the company would not be able to  make vaccine with eggs raised outside its control.

According to HHS officials, the agency recognizes that avian influenza  poses a risk to the production of pandemic influenza vaccines. To  address that risk, HHS has contracted with the company to protect the  egg supply chain and ensure a year-round supply of vaccine-quality  fertilized eggs for the company to use in its vaccine manufacturing  process. HHS awarded the current 3-year, $42 million contract for a year- round supply of eggs in September 2014. The contract requires that the  company have a risk management plan; the company’s plan contains  both a physical security program and a biosecurity program to provide  protection against man-made and natural threats.

HHS officials said they are confident that the company’s biosecurity  program is sound. According to company representatives, the company  mitigates risks by limiting the density of the birds on each farm and by  using farms that are not in close proximity. In addition, company  employees routinely audit the flocks and incubation facilities, and the  company periodically tests the flocks of layer hens for avian influenza  using USDA’s National Poultry Improvement Plan testing procedures.  Furthermore, according to HHS officials, the agency conducts annual  security audits of a portion of the facilities in the company’s network.

According to company representatives, the company has standard  operating procedures for biosecurity in its network of egg suppliers that  are based on state department of agriculture guidelines. Company  representatives said that because the company contracts with its  suppliers and can require specific conditions, it has more control over  what is done on the farms and in the incubation facilities than it does with  farms that only comply with either USDA or state agriculture department  requirements. While the 2014 and 2016 outbreaks did not affect this egg  supply, a previous outbreak of highly pathogenic avian influenza caused  the deaths of laying hens and reduced the supply of eggs used to  produce human vaccines by about 50 percent.

HHS has sought to diversify vaccine production through technologies that  are not egg-based. Specifically, HHS has promoted technologies known  as cell-based and recombinant technologies to produce vaccine.  According to agency officials, these technologies will help offset the risk  avian influenza poses to vaccine production. We have reported  separately on federal efforts to diversify the pandemic vaccine supply.  According to HHS’s website, three Centers for Innovation  in Advanced  Development and Manufacturing—in Maryland,  North Carolina, and  Texas—will provide a significant domestic infrastructure in the United  States capable of producing medical countermeasures to protect  Americans from the health impacts of bioterrorism as well as pandemic  influenza and other diseases. However, the centers are not yet able to  manufacture the contracted quantity of pandemic influenza vaccine.  According to HHS’s Office of the Assistant Secretary for Preparedness  and Response, as of February 2017, it was yet to be determined when  the three CIADMs would be fully operational, but contractor officials  indicated that one of the three is expected to become fully operational in  2017.

section_title: Funding for a Federal Effort to Monitor Swine for Influenza That Could Threaten Human Health Will Run Out in Fiscal Year 2017
paragraphs: USDA and HHS have collaborated to monitor swine for influenza A  viruses because swine may act as a “mixing vessel” in which influenza  viruses recombine to pose new threats to human health. However, the  agencies face the issue that funding for a voluntary surveillance program  will be exhausted in fiscal year 2017. According to HHS officials, this  surveillance program is the only federal source of data for understanding  the types of influenza circulating in swine. Because influenza is endemic  in swine worldwide, swine producers are not required to report the  disease to USDA, and USDA is not required to report swine influenza to  the World Organisation for Animal Health. However, since 2009, when  H1N1 swine-origin influenza caused a global human pandemic, USDA  has used funding from HHS to collect voluntary data from the U.S. swine  industry on the incidence of swine influenza. As we reported in May  2013, there are limitations in the reliability of the data collected by this  voluntary program; in particular, it may not accurately represent all of the  conditions circulating across the country. Nevertheless, this program  has provided useful data on the presence of various subtypes of influenza  virus in swine herds, according to HHS and USDA officials. Moreover,  representatives from the pork industry we interviewed stated the  surveillance data are beneficial to both public and animal health.  However, according to USDA officials, funding for the swine surveillance  program is expected to be fully expended in fiscal year 2017. USDA  officials said that the agency will once again seek additional funding for  the program in fiscal year 2018 and beyond, through appropriated  funding, but that funding beyond fiscal year 2017 is uncertain. In addition,  the U.S. Animal Health Association provided support for the program’s  continuation through a 2016 resolution asking Congress to appropriate  funding for the swine surveillance program; furthermore, according to its  representative, the National Pork Producers Council has advocated for  continued funding for the program. According to HHS officials, the agency  will continue to be supportive of USDA’s efforts to continue the program.  It is too early to say whether USDA will continue to gather data on  influenza in swine beyond fiscal year 2017.

section_title: Conclusions
paragraphs: The federal government has taken important steps to mitigate the  significant risks posed by avian influenza to the health of humans,  animals, and the economy. However, experience in the United States and  around the world has shown that it is challenging to protect domesticated  poultry from infection and control the disease when it does strike. USDA  proactively identified numerous lessons learned, across a wide range of  response areas, from the 2014 and 2016 outbreaks of avian influenza,  and it identified more than 300 associated corrective actions. USDA has  marked as completed about 70 percent of these actions, but it does not  have plans for evaluating the extent to which its completed corrective  actions have effectively helped to resolve the problems the agency  identified in its responses to the 2014 and 2016 outbreaks. By developing  a plan for evaluating completed corrective actions and, as part of this  plan, considering whether any completed corrective actions require  validation through simulations or exercises, USDA could better assess  the effectiveness of these actions. This is particularly important in light of  new outbreaks among commercial poultry in 2017 that continue to  challenge the nation’s efforts to control this devastating disease.

section_title: Recommendation for Executive Action
paragraphs: We recommend that the Secretary of Agriculture direct the Administrator  of the Animal and Plant Health Inspection Service to develop a plan for  evaluating completed corrective actions to determine their effectiveness  and, as appropriate, consider whether any completed corrective actions  require validation through simulations or exercises.

section_title: Agency Comments
paragraphs: We provided a draft of this report to USDA, HHS, and Interior for review  and comment. USDA provided written comments on the draft, which are  presented in appendix III,  and provided technical comments, which we  incorporated as appropriate. USDA agreed with our recommendation.  HHS and Interior did not provide written comments but provided technical  comments, which we incorporated as appropriate.

In its written comments, USDA said that APHIS agreed with our  recommendation to develop a plan for evaluating completed corrective  actions to determine their effectiveness. Further, USDA said that APHIS  will incorporate simulations and exercises in its plan and that, in the event  of an actual outbreak, APHIS will evaluate the effectiveness of the  response through an after action report. Finally, USDA said that APHIS  will continually review the criteria and hierarchy of corrective actions, both  completed and ongoing, with respect to avian influenza policies,  emergency management activities, and critical communications with  states, tribes, poultry producers, and poultry industry partners.

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, the Secretary of the Interior, 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 morriss@gao.gov. Contact points for our  Offices of Congressional Relations and Public Affairs may be found on  the last page of this report. GAO staff who made key contributions to this  report are listed in appendix IV.

section_title: Appendix I: Selected Agencies with Responsibilities Related to Avian Influenza
paragraphs: Numerous federal agencies have responsibilities related to reducing the  risks posed by avian influenza to human health, animal health, and the  economy. Table 7 provides a summary of those responsibilities for  agencies within the U.S. Department of Agriculture, the Department of  Health and Human Services, and the Department of the Interior.

section_title: Appendix II: Results of Surveillance of Wild Birds for Avian Influenza, December 2014 through March 2017
paragraphs: In response to the outbreak of highly pathogenic avian influenza in  December 2014, personnel from the U.S. Department of Agriculture  (USDA) and the Department of the Interior re-convened the Interagency  Wild Bird Avian Influenza Steering Committee in January 2015. The  steering committee developed a wild bird surveillance plan for avian  influenzas that may pose a threat to human health or domestic poultry.  The plan encourages federal and state agencies and others to use a  variety of sampling methods to test live and dead wild birds to detect both  low pathogenic and highly pathogenic avian influenza. According to data  recorded as of March 24, 2017, the surveillance program had collected  test results from more than 88,000 wild birds since December 2014. The  number of monthly highly pathogenic avian influenza detections was  highest during the period from December 2014 through June 2015 before  declining during the period from July 2015 through March 24, 2017,  despite an increase in testing over this period of time. In total, the  program detected highly pathogenic avian influenza in 102 birds, or 0.12  percent of those tested. (See table 8 for a summary of the monitoring  data.) The surveillance program also detected low pathogenic influenza A  virus in some wild birds; program data show that the percentage of wild  duck samples that tested positive for low pathogenic influenza A virus in  each month ranged from about 7 percent to about 30 percent in 2015 and  2016 (data not shown in table 8). The state veterinarians we interviewed  from six states (California, Indiana, Iowa, Minnesota, North Carolina, and  Ohio) generally agreed with the need for wildlife surveillance. At the same  time, while monitoring can serve as an early warning system to alert  poultry owners and public health agencies, among others, of the  presence of influenza A viruses in wild birds, it cannot eliminate wild birds  as potential sources of the virus.

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

section_title: Appendix IV: GAO Contact and Staff Acknowledgments
subsections: section_title: GAO Contact

section_title: Staff acknowledgments
paragraphs: In addition to the individual named above, Mary Denigan-Macauley  (Assistant Director), Kevin Bray, Ross Campbell, Barbara El Osta, Kevin  R. Fish, Katherine Killebrew, Erik Kjeldgaard, Cynthia Norris, and Amber  Sinclair made key contributions to this report. Ashley Grant, Sara  Sullivan, Kiki Theodoropoulos, and Rajneesh Kumar Verma also made  important contributions to this report.

section_title: Related GAO Products
paragraphs: Biodefense: The Nation Faces Multiple Challenges in Building and  Maintaining Biodefense and Biosurveillance. GAO-16-547T. Washington,  D.C: April 14, 2016.

Emerging Animal Diseases: Actions Needed to Better Position USDA to  Address Future Risks. GAO-16-132. Washington, D.C.: December 15,  2015.

Biosurveillance: Challenges and Options for the National Biosurveillance  Integration Center. GAO-15-793. Washington, D.C: September 24, 2015.

National Preparedness: HHS Has Funded Flexible Manufacturing  Activities for Medical Countermeasures, but It Is Too Soon to Assess  Their Effect. GAO-14-329. Washington, D.C.: March 31, 2014.

National Preparedness: HHS is Monitoring the Progress of Its Medical  Countermeasure Efforts but Has Not Provided Previously Recommended  Spending Estimates. GAO-14-90. Washington, D.C.: December 27, 2013.

Homeland Security: An Overall Strategy Is Needed to Strengthen Disease  Surveillance in Livestock and Poultry. GAO-13-424. Washington, D.C.:  May 21, 2013.

Influenza: Progress Made in Responding to Seasonal and Pandemic  Outbreaks. GAO-13-374T. Washington, D.C.: February 13, 2013.

National Preparedness: Improvements Needed for Acquiring Medical  Countermeasures to Threats from Terrorism and Other Sources.   GAO-12-121. Washington, D.C.: October 26, 2011.

Influenza Pandemic: Lessons from the H1N1 Pandemic Should Be  Incorporated into Future Planning. GAO-11-632. Washington, D.C.: June  27, 2011.

Influenza Vaccine: Federal Investments in Alternative Technologies and  Challenges to Development and Licensure. GAO-11-435. Washington,  D.C.: June 27, 2011.

National Preparedness: DHS and HHS Can Further Strengthen  Coordination for Chemical, Biological, Radiological, and Nuclear Risk  Assessments. GAO-11-606. Washington, D.C.: June 21, 2011.

Public Health Preparedness: Developing and Acquiring Medical  Countermeasures Against Chemical, Biological, Radiological, and  Nuclear Agents. GAO-11-567T. Washington, D.C.: April 13, 2011.

Influenza Pandemic: Monitoring and Assessing the Status of the National  Pandemic Implementation Plan Needs Improvement. GAO-10-73.  Washington, D.C.: November 24, 2009.

Influenza Pandemic: Sustaining Focus on the Nation’s Planning and  Preparedness Efforts. GAO-09-334. Washington, D.C.: February 26,  2009.

Avian Influenza: USDA Has Taken Important Steps to Prepare for  Outbreaks, but Better Planning Could Improve Response. GAO-07-652.  Washington, D.C.: June 11, 2007.

Fast facts: Avian influenza is an extremely infectious and potentially fatal disease in poultry. In 2014 and 2016, outbreaks in the U.S. led to the death of more than 50 million chickens, turkeys, and other birds, and cost billions of dollars.

Controlling avian influenza viruses in poultry is crucial to preventing those viruses from evolving to infect people.

The U.S. Department of Agriculture has taken actions to address lessons learned from its responses to the outbreaks, such as encouraging states to form response teams. However, it does not have a plan to evaluate the effectiveness its efforts. We recommended that USDA develop such a plan.

Question-summary annotations: questions: question: What sectors are affected by avian influenza outbreaks?
answer: When avian influenza outbreaks occur, they can have significant effects on human and animal health and the U.S. economy.
child_questions: question: What was the impact of the 2014 outbreak in the United States?
answer: An outbreak can also have significant economic consequences; for example, the economic impacts of the 2014 outbreak in the United States have been estimated to range from $1.0 to $3.3 billion.

question: What regions have been affected by avian influenza in the last 20 years?
answer: With regard to human health, avian influenza rarely affects humans, but the World Health Organization estimates that two particular types of the virus have caused more than 2,100 human infections and more than 800 deaths since 1997, primarily in Asia and the Middle East.
child_questions: question: How does avian influenza affect animals?
answer: With regard to animal health, avian influenza outbreaks can lead to large numbers of poultry deaths as a result of efforts to control and prevent the spread of the disease. For example, from December 2014 to June 2015, more than 50 million birds were destroyed in the largest outbreak in U.S. history.

question: How does avian influenza affect other species?
answer: The effect of avian influenza on the health of other animal species varies. Swine are susceptible to both avian and human influenza viruses that, if mixed, could create a new virus to which humans are vulnerable.

questions: question: How has USDA learned from the most recent outbreaks?
answer: USDA identified 15 areas with lessons learned from its responses to the 2014 and 2016 outbreaks of avian influenza and 308 associated corrective actions.
child_questions: question: What is one example of a lesson learned?
answer: For example, one lesson learned in the area of depopulation (mass culling of flocks) is that there were not enough skilled personnel available for depopulating infected poultry, leading to delays and possibly increasing the spread of disease.

question: To what extent have these corrective actions been completed?
answer: USDA has identified as completed about 70 percent of the 308 corrective actions to address all of the lessons learned.
child_questions: question: What is missing in this evaluation?
answer: However, the agency has not evaluated the extent to which completed corrective actions—such as encouraging states to form depopulation teams—have helped resolve the problems identified, and it does not have plans for doing so.

question: What has GAO found about corrective actions?
answer: GAO has previously found that agencies may use evaluations to ascertain the success of corrective actions, and that a well-developed plan for conducting evaluations can help ensure that agencies obtain the information necessary to make effective program and policy decisions.
child_questions: question: How would such a plan help USDA?
answer: Such a plan would help USDA ascertain the effectiveness of the actions it took to resolve problems identified during recent outbreaks.

questions: question: How does avian influenza affect poultry?
answer: Avian influenza is an extremely infectious and potentially fatal disease in poultry.
child_questions: question: What were the effects of the 2014 and 2016 outbreaks?
answer: In 2014 and 2016, two outbreaks of avian influenza led to the deaths of millions of poultry in 15 states and prompted emergency spending to control the disease.

question: How does avian influenza affect humans?
answer: While the health risk to humans is low, humans have been infected with these viruses, sometimes fatally.
child_questions: question: What is the most recent spike?
answer: A spike in fatal human infections in Asia began in late 2016.

questions: question: What was GAO asked to review?
answer: GAO was asked to review several issues related to avian influenza.

question: What does this report examine?
answer: This report examines (1) how outbreaks of avian influenza have affected human health, animal health, and the U.S. economy, (2) the extent to which USDA has taken actions to address any lessons learned from its responses to the outbreaks in 2014 and 2016, and how it plans to evaluate the actions' effectiveness, and (3) ongoing challenges and associated issues, if any, federal agencies face in their efforts to mitigate the potential harmful effects of avian influenza.

question: How did GAO conduct its review?
answer: GAO reviewed global and domestic data on the effects of avian influenza and USDA reports and corrective action data associated with its responses to the recent outbreaks, and interviewed federal officials and stakeholders from state agencies and the poultry industry.