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

Letter

Background

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.

Avian Influenza Viruses

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.

Avian Influenza Transmission

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.

Poultry in the United States

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.

Our Related Prior Work

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.)

Federal Agencies’ Roles in Avian Influenza Response, Research, Surveillance, and Other Related Activities

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.)

Avian Influenza Has Harmed Human Health, Animal Health, and the U.S. Economy

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.

Avian Influenza Rarely Infects Humans, but the Mortality Rate for Those Infected Has Been Relatively High

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.

Outbreaks of Avian Influenza Have Killed Millions of Poultry Worldwide but Caused Few Fatalities in Other Species

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.

Cats Infected with Avian Influenza in New York City Animal Shelters

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.

Recent Outbreaks Have Cost the Federal Government and the U.S. Economy Billions of Dollars

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.

USDA Has Taken Corrective Actions to Address Lessons Learned but Does Not Have Plans to Evaluate Their Effectiveness

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.

USDA Has Identified Lessons Learned from the 2014 and 2016 Outbreaks and Taken Numerous Corrective Actions

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.

USDA Does Not Have Plans to Evaluate the Effectiveness of its Corrective Actions

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.

Federal Agencies Face Ongoing Challenges and Associated Issues in Their Efforts to Mitigate the Potential Harmful Effects of Avian Influenza

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.

Ongoing Challenges that Federal Agencies Face in Mitigating the Potential Harmful Effects of Avian Influenza

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.

Protecting Domesticated Poultry from the Threat of Avian Influenza Carried by Wild Birds Is a Challenge

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.

Reliance on Voluntary Actions by a Wide Range of Poultry Producers to Prevent Flocks from Avian Influenza Infections Is a Challenge

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.

Federal Agencies Face Other Issues Associated with Mitigating the Potential Harmful Effects of Avian Influenza

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.

Poultry Used to Produce Critical Human Vaccine Are Susceptible to Influenza Outbreaks

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.

Funding for a Federal Effort to Monitor Swine for Influenza That Could Threaten Human Health Will Run Out in Fiscal Year 2017

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.

Conclusions

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.

Recommendation for Executive Action

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.

Agency Comments

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.

Appendix I: Selected Agencies with Responsibilities Related to Avian Influenza

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.

Appendix II: Results of Surveillance of Wild Birds for Avian Influenza, December 2014 through March 2017

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.

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

Appendix IV: GAO Contact and Staff Acknowledgments

GAO Contact

Staff acknowledgments

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.

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