Abstract
The Centers for Disease Control and Prevention (CDC) transformed its approach to preparing for and responding to public health emergencies following the anthrax attacks of 2001. The Office of Public Health Preparedness and Response, an organizational home for emergency response at CDC, was established, and 4 programs were created or greatly expanded after the anthrax attacks: (1) an emergency management program, including an Emergency Operations Center; (2) increased support of state and local health department efforts to prepare for emergencies; (3) a greatly enlarged Strategic National Stockpile of medicines, vaccines, and medical equipment; and (4) a regulatory program to assure that work done on the most dangerous pathogens and toxins is done as safely and securely as possible. Following these changes, CDC led responses to 3 major public health emergencies: the 2009-10 H1N1 influenza pandemic, the 2014-16 Ebola epidemic in West Africa, and the ongoing Zika epidemic. This article reviews the programs of CDC's Office of Public Health Preparedness, the major responses, and how these responses have resulted in changes in CDC's approach to responding to public health emergencies.
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Within weeks of the 9/11 World Trade Center attack, CDC responded to a biological attack with anthrax involving numerous domestic jurisdictions. The anthrax attack required CDC to provide the public with frequent updates on the progress of the investigation. The volume of information and the expectations of the public created a need for CDC to operate at an unprecedented scale and tempo. 3 To meet the challenges identified in the response to the anthrax attacks, CDC created a new organizational unit and approach to respond to large, complex public health emergencies, whether naturally occurring, intentional, or accidental. CDC's approach to emergency response continues to evolve.
In addition to the potential for bioterror attacks, such as the anthrax attack, 2 global trends required that CDC develop an expanded capability to respond at speed and scale to future emergencies. 4 First, the speed and volume of long-distance travel have increased substantially. Over the past 75 years, the widespread availability of air travel has reduced the time for intercontinental travel from weeks to hours. 5 Along with shorter travel times, the volume of intercontinental travel has increased exponentially. With increased and faster global travel, the opportunity for a person infected with a pathogen to travel to another part of the world within hours has become increasingly likely. 6 Second, global population increases concentrated in Africa, the Indian subcontinent, and East Asia have resulted in a dramatic increase in the number of cities with populations over 10 million. 7 Ease of travel and urbanization, particularly the concentration of poverty in urban areas, is creating the opportunity for an increasing number of large infectious disease epidemics affecting multiple urban areas.
Technological advances in medicine and public health have created new tools to diagnose and quickly respond to public health emergencies. Rapid and specific diagnostic methods, vastly improved communication systems, and evolving therapeutic and vaccine technologies create opportunities to detect and respond to health emergencies that were unimaginable in the past. Unfortunately, these same scientific and technologic advances allow the possibility to create more deadly or transmissible pathogens that could be released, intentionally or not, into the community. 8
In this article we describe how CDC's emergency response preparations and execution have evolved with these changing realities and expectations, with a particular focus on changes beginning with the 2009 H1N1 pandemic.
Creation of the Office of Public Health Preparedness and Response
After the 2001 anthrax attacks, the nation readied itself for additional bioterror attacks. Government policymakers and public health officials created lists of microorganisms and chemical and biological toxins that could be used as terror agents. Government funding created a scientific-medical-production enterprise to develop medical countermeasures—diagnostics, vaccines, and therapeutics—to address these threats. 9
The concerns and activities following the 2001 attacks were similar to those that led to the 1951 creation of the CDC Epidemic Intelligence Service, a 2-year training program in field epidemiology, as part of a response to fears of an attack with bioweapons during the Cold War. 1 In 2002 CDC created a new organization—the Office of Terrorism Preparedness and Emergency Response, later the Coordinating Office for Terrorism Preparedness and Emergency Response, predecessors to the current Office of Public Health Preparedness and Response (OPHPR)—with responsibility for preparing for large-scale emergencies, including terrorism attacks. The office combined 3 smaller existing programs: support of state and local emergency preparedness activities, the Strategic National Stockpile, and the regulatory program for select agents and toxins. In addition, the Bernie Marcus Foundation, through the CDC Foundation, funded renovations and equipment procurement for CDC's first Emergency Operations Center. 10
Each division or program in the Office of Public Health Preparedness and Response has specific responsibilities to assure that CDC and the nation's public health system is as ready as possible to respond to future health threats (Table 1).
Programs in CDC's Office of Public Health Preparedness and Response
Regulatory Program on Select Agents and Toxins
The mission of the Division of Select Agents and Toxins (DSAT) is to assure that work done with dangerous pathogens and toxins in the United States is done as safely and securely as possible (Table 1). The Federal Select Agent Program consists of CDC's DSAT and the US Department of Agriculture's Agriculture Select Agent Services Program. Examples of select agents and toxins include the organisms that cause anthrax, smallpox, and bubonic plague, as well as the toxins ricin and botulinum neurotoxin. The program has an enabling mission: to assure that laboratories working with select agents and toxins are able to do their work, to create new knowledge to detect and respond to the threats these pathogens and toxins could cause. 11 As of November 2016, 279 laboratories were registered with the Federal Select Agent Program (a decrease from a high of 336 laboratories in 2006); 241 are registered with CDC's Select Agent and Toxins program and 38 with USDA's Agriculture Select Agent Services Program. The CDC Select Agent Program conducted 183 inspections in 2015, including 72 unannounced inspections. Since its inception, the program has denied 361 individuals access to select agent laboratories through the Security Risk Assessment process, which includes background investigations conducted by the FBI.
The underlying challenge for the Federal Select Agent Program is to balance competing priorities: (1) transparency to the public regarding the work and safety of the laboratories registered with the program with the need to protect information about the work from those that might use such information to cause harm; (2) the regulatory burden necessary to assure safety and security with fostering an environment where the greatest scientific output is possible; and (3) ultimately, assuring that the benefits of the research justify its inherent risks. Even the most stringent regulations cannot ensure that work with select agents and toxins has zero risk; the program works to keep risk to the minimum possible. Determining whether potential benefit outweighs irreducible risks is complex and requires reconciling numerous points of view.
Within the purview of the regulatory program, work continues to improve in the following areas: (1) standardizing the inspection process through ongoing efforts to improve training of inspectors, (2) improving the science of biosafety and biosecurity, and (3) preparing for biosafety and biosecurity risks of the future as a result of the ongoing revolution in biology. These ongoing advances in biology, including sequencing technologies and synthetic biology, will make regulation and oversight in these areas increasingly complex.
Emergency Operations at CDC
The Division of Emergency Operations manages CDC's Emergency Operations Center (EOC). The division's mission is to serve as a hub for communication, decision making, and operations during emergency activations and to plan and train for that function. When activated, the EOC serves as a temporary home for responders: scientists, communication specialists, laboratory experts, and program managers from throughout CDC who are deployed to respond to a specific emergency. Since April 2009, the start of the H1N1 pandemic response, CDC's EOC has been activated over 91% of the time. 12
By activating the EOC, CDC is able to perform many of the functions it was not able to carry out during the 2001 anthrax attack: managing a scalable system for travel and shipping of equipment; recruiting and managing volunteer responders; assuring a uniform system of deployment, including predeployment, during deployment, and postdeployment activities; and providing software tools to visualize data, thereby improving situational awareness. Although the health and safety of deployed staff have always been of concern during responses, the risks in the Ebola response led to the creation of a Deployment Risk Mitigation Unit, which provided a focal point for assuring a standard approach to safety and security training for staff deployed in responses.
The division has taken on an important new activity: training future incident commanders to lead CDC emergency responses. The training is based on the real-world experiences of large emergency responses in which CDC has played a leading role. The intent is to provide a setting for experiential learning in initiating a response, making recommendations or decisions, and understanding the needs of senior leaders during a large emergency response and how to meet those needs.
Improving emergency response capacity globally is a second, related function the division has undertaken as part of the Global Health Security Agenda. 13 CDC staff have led emergency management training sessions in 40 countries since 2014. This training has been put to use in 6 countries in 2015 and 2016, where ministry of health officials have activated their emergency operations centers 11 times to respond to emergencies ranging from cholera and influenza outbreaks to a train derailment. The training sessions and establishment of emergency operations centers have resulted in earlier and more effective responses to health emergencies. For those emergencies that have the potential to spread, more effective responses overseas protect Americans.
The Strategic National Stockpile
The Strategic National Stockpile's purpose is to assure that medical material needed to respond to a public health emergency is available when, where, and in the quantity needed to respond effectively. The stockpile's inventory includes vaccines, medications, chemical antidotes, ancillary supplies needed to administer the countermeasures, mechanical ventilators, respirators, and other medical equipment. The stockpile is a part of the Public Health Emergency Medical Countermeasure Enterprise, an interagency committee led by the Department of Health and Human Services' (HHS) Assistant Secretary of Preparedness and Response. The Public Health Emergency Management Countermeasure Enterprise is charged with developing and implementing the medical countermeasure strategy from basic science, to product development, licensing, stockpiling, distribution, and dispensing. 14 As of November 2016, the stockpile contains material worth approximately $7 billion, with annual funding of $575 million in 2016.
State and Local Readiness
The Division of State and Local Readiness is responsible for assuring that state, local, tribal, and territorial health departments are as ready as possible to respond to any health emergency. The division manages the Public Health and Emergency Preparedness cooperative agreement and program, with annual funding of $660 million in 2016. This cooperative agreement funds personnel in state and local jurisdictions responsible for emergency response, planning and exercising, and costs associated with small-scale responses (as a means of testing and improving systems that would be needed in larger responses). Through this program, state and local health departments have become part of the emergency response structure in their jurisdictions. This functionality includes the ability to rapidly mobilize for an event that requires a large-scale response. The cooperative agreement also supports the Laboratory Response Network, which has the capability to detect pathogens that might be used in a bioterror attack. The network has proved adaptable in quickly adding diagnostic tests to detect novel infectious diseases. Risk communication staff are now available in state and local health departments to assure that the public is informed about emerging health threats.
Experience in Responding to Large-Scale Emergencies
In the years since the restructuring of emergency response at CDC, public health emergencies have become increasingly frequent. Since 2001, CDC has mounted major responses to the SARS epidemic, Hurricane Katrina, and more recently to the H1N1 influenza pandemic and Ebola and Zika virus epidemics (Table 2). 15 Since 2009, CDC has activated its Emergency Operations Center 17 times (Tables 2 and 3). The median duration of activation has been 85 days, and most have been for infectious disease emergencies, frequently beginning overseas but with the potential to spread to the United States. 15 Natural threats, rather than accidental or intentional events, have predominated. Brief summaries help to understand the results and lessons of these responses (Tables 2 and 3).
Major CDC Responses 2009–2016
WHO Public Health Emergency of International Concern (PHEIC) declaration date.
Lower-level CDC Responses, 2010-2016
Activation levels are 1-3. Level 1: The highest, reserved for critical emergencies 24/7; Level 2: CDC SME's and other programs lead with EOC assistance; Level 3: CDC SME's lead with their staff and EOC may assist.
Responses occurred prior to the initiation of formal systems (Time Tracker) to track personnel participation time.
Department of Defense
2009 H1N1 Pandemic
In mid-April 2009, CDC confirmed several human infections with a novel H1N1 influenza virus. When cases of severe respiratory illness in Mexico, including deaths, were confirmed to be caused by the same virus, CDC activated its Emergency Operations Center to the highest response level. 16 Within weeks, CDC had developed and distributed a PCR diagnostic test to state health department laboratories and influenza laboratories throughout the world. The Biomedical Advanced Research and Development Authority (BARDA), operating in the HHS Office of the Assistant Secretary of Health for Preparedness and Response, worked with vaccine manufacturers to produce monovalent H1N1 vaccine. CDC coordinated the distribution of 126.9 million doses of monovalent H1N1 vaccine in 330,000 separate shipments to more than 72,000 providers using the same system that is used to distribute childhood vaccines through the Vaccines for Children's Program. Eventually, an estimated 81 million US residents were vaccinated against the pandemic strain of H1N1 influenza. 17 CDC distributed 12 million treatment courses of antiviral drugs to treat influenza, approximately one-quarter of the quantity stockpiled. To keep the public informed, CDC conducted 39 press conferences and 21 telebriefings and convened a pandemic influenza “boot camp” for media in August 2009. CDC coordinated closely with state and local health departments, other federal departments, and clinician organizations.
In a public opinion poll conducted in January 2010 regarding the federal government response to H1N1, 59% of respondents rated the government response as good or excellent. 18 Despite delayed production of vaccine, produced and procured through contracts managed by BARDA, CDC's work to rapidly distribute vaccine as soon as it became available and encourage use of antiviral medications prevented at least 1 million cases of influenza, 18,000 hospitalizations, and 600 deaths.19,20 Public Health Emergency Preparedness grantees were able to track cases of H1N1 disease and mobilize planning and communication efforts for the vaccination campaign because of investments in these capabilities before the pandemic. Similarly, the investments and training in CDC's Emergency Operations Center facilitated CDC's uniform and prioritized approach to the response.
The West African Ebola Epidemic
In March 2014, the global public health community was alerted to an outbreak of Ebola in West Africa. First identified in a remote area of Guinea bordering Liberia and Sierra Leone, this was the first Ebola outbreak in West Africa. 21 Over the next 8 weeks, cases were identified in Conakry, Guinea's capital, and in Liberia. When measures to identify suspect cases, isolate them to prevent transmission, and conduct laboratory testing to distinguish cases from non-cases were implemented in March and April 2014, initial reports indicated a fall in incidence. The global public health response largely demobilized, allowing transmission to continue and leading to the world's first Ebola epidemic. 21 The epidemic ultimately involved more than 28,000 cases and more than 11,000 deaths in Guinea, Sierra Leone, and Liberia—the 3 most highly affected countries—with imported cases and limited transmission in 3 neighboring countries (Nigeria, Mali, and Senegal) and more than a dozen medical evacuations and single generations of transmission in developed countries (Spain and the United States). The outbreak was not brought fully under control until March 2016. 22
Severe as the epidemic was, rapid response to a cluster of cases in Lagos, Nigeria, as well as effective work to end the epidemic in West Africa prevented a catastrophe that could have resulted in hundreds of thousands of deaths and widespread dissemination of Ebola.23,24 Two cases were diagnosed in the United States in returning travelers; Public Health Emergency Preparedness grantees implemented a system to track returning travelers from Guinea, Sierra Leone, and Liberia to quickly identify people with possible Ebola.
The epidemic serves as a vivid example of the consequences of the ease of travel to and from any location in the world and has spurred efforts to assure that every country has the ability to detect and respond to disease outbreaks, the goal of the Global Health Security Agenda. 25 In addition to local capability, the West Africa Ebola epidemic showed the need for the global community to have the resources and training in place to be able to support local response efforts rapidly anywhere in the world when the need arises.
The Zika Epidemic
Even before the response to the Ebola epidemic was over, a new disease had emerged requiring a global response. Zika virus was little more than an arboviral curiosity until the fall of 2015. 26 The mosquito-transmitted virus was first identified in the late 1940s and was recognized as causing only mild symptoms among the 1 in 5 human infections who had any symptoms.26,27 In May 2015, a large outbreak was reported in Brazil, similar epidemiologically to outbreaks that had occurred in the Western Pacific in the preceding decade. 28 In November 2015, investigators in Brazil reported an unexpected finding: an association between the Zika virus epidemic and large numbers of babies born with microcephaly. 29 Over the next several months, epidemiologic and pathologic evidence mounted that Zika virus was the cause of this severe and previously extremely rare birth defect. 30 Protecting pregnant women from Zika virus infection became a high priority. In addition to mosquito-borne transmission and the association with birth defects, the Zika virus epidemic differed from the Ebola epidemic or H1N1 pandemic; in those earlier events, there was a good understanding of the pathophysiology of the disease and the effectiveness of control measures. In the case of Zika virus, new knowledge continues to emerge. For example, sexual transmission of Zika virus infection, though documented previously, is not a characteristic known to be shared with other arboviruses. 31
The public health community in the continental United States has little recent experience in controlling diseases spread by Aedes mosquitoes. In addition, the eventual public health burden of the epidemic has been challenging to communicate because the disease is most often asymptomatic and the severe consequences occur in babies, months after infection of pregnant women.
The Zika virus epidemic has required an unprecedented scientific, operational, and communication response. Above all, the outbreak has shown the need to be able to respond rapidly to an event that was unpredictable. The response has required expertise in reproductive health, vector biology, arbovirology, birth defects, sexually transmitted diseases, laboratory test development, risk communication, and community engagement.
Major Observations from Responses
Several observations emerge from the experience over the past 15 years using the CDC Emergency Operations Center to respond to large, complex health events. The first is that experience, whether acquired through plans and exercises or through real-life response, pays dividends. CDC's response to the H1N1 pandemic was based on plans and exercises to prepare for a severe influenza pandemic emerging overseas. 32 The rapid spread of H5N1 in wild birds and poultry and the high mortality rate among human H5N1 cases in 2005 and 2006 provided an urgency to this preparation. 33 The work to plan and exercise for a response to H5N1 was put to the test in the 2009 H1N1 influenza pandemic response. The plans and exercises to prepare for a severe influenza pandemic established a framework to understand and respond to the H1N1 pandemic, even though it was less severe than assumptions in H5N1 planning scenarios. The involvement of state and local public health and emergency response staff, many federal agencies, and the private sector in planning for an influenza pandemic also helped create a shared sense of expectations for what was important in the response. The Ebola and Zika responses benefited from the experience gained during the H1N1 response.
The second observation is that public health systems used routinely—everyday systems—form the basis for emergency response; these systems are easier to scale than systems not in everyday use. CDC adapted the Vaccines for Children system, the system that ships more than half of all childhood vaccines in the United States to providers, to distribute monovalent H1N1 vaccine in the H1N1 pandemic. CDC also scaled up routine vaccine coverage surveys to measure vaccine uptake weekly. 34 In contrast, CDC shipped antiviral drugs to state health departments, where distribution plans differed widely. It remains unclear how many patients with influenza received antiviral drugs from the Strategic National Stockpile, but treatment of more patients could have led to improved outcomes.
The third observation is that naturally occurring emergencies are more frequent than bioterror attacks. 35 This has implications for ensuring that these more frequent responses, especially aspects of the response that need to be improved, are used to plan for scenarios that require near instantaneous response—such as low-likelihood, high-consequence terrorist attacks. Large-scale natural disasters, such as hurricanes, earthquakes, and tornadoes, will continue to occur, and these events require dedicated plans and exercises. However, of the 3 major emergency responses in the past 10 years, only the H1N1 influenza pandemic was anticipated. Plans and the experience from exercises and real-life events have to be adapted to respond to unpredicted and unexpected emergencies.
The fourth major observation, evident in all large emergency responses, is that the best responses adapt quickly to changing circumstances. Unlike responses to natural disasters, in which the course of events is somewhat predictable based on the magnitude and location of the event, an effective response to a public health emergency depends on rapid collection and analysis of complex information and adaptive response based on both epidemiologic trends and the documented impact of program interventions. The ability to receive new, sometimes unexpected, information and to change the objectives and operations of the response is critical. Effective emergency response is similar to effective public health action generally—using data to improve performance rapidly. In both emergency responses and in public health programs, policymakers need to use all available facts and base decisions on scientifically valid principles in order to optimally protect the public. As the full extent of the Ebola epidemic in Liberia became apparent in the summer of 2014, it became clear that resources were insufficient to implement all control measures widely. Efforts to establish clinical care for Ebola patients that met established minimal standards and assuring safe and dignified burial for people who died of Ebola took priority. Later, when action to reduce transmission from burials and ill patients led to a decrease in cases, the emphasis shifted to rapid laboratory confirmation of cases, case isolation, and contract tracing.
Another example of this adaptation occurred during the Ebola response following the domestic diagnosis of the first case of Ebola virus disease and the subsequent confirmation of the disease in 2 nurses who had cared for the initial patient. Within days, CDC and DHS's Customs and Border Protection established procedures for screening at 5 airports where almost all travelers from the highly affected countries entered the United States; CDC revised and released more specific guidance for personal protective equipment and established a system to track travelers from highly affected countries through their potential incubation period. 36 This tracking system used data collected during airport screening and relied on state and local health departments to make contact with travelers on a daily basis.
The fifth observation is that public communication is a crucial response function. The need for a massive communication response—the need to respond to media and public inquiries orders of magnitude greater than baseline—might serve as the definition of a public health emergency. Effective risk communication cannot change bad outcomes or decisions, but poor communication can lead to confusion or lack of confidence and erosion of trust. Basic risk commination principles include explaining what is known and not known, what is being done to better understand the situation and to intervene, and what individuals can do to reduce their health risks. 37 Setting realistic expectations is key but may be difficult, depending on the situation. For large emergencies, the media act as an amplifier of public opinion, but also offer a platform to assure that people have the most up-to-date information and are sufficiently informed so that they can take action. This spotlight of attention is linked with the next finding.
Sixth, large emergency responses require the ability to coordinate response actions with many groups external to CDC. CDC has a close relationship with state and local health departments, but events frequently require a broader set of partners. Providing timely and essential information, not only to the public, but also to political leaders, is important in order to avoid misunderstanding and unproductive work and to identify areas where higher level intervention and assistance is necessary. For example, during the Ebola response, the disposition of medical waste in the United States became a major challenge. The Pipeline and Hazardous Materials Safety Administration with the Department of Transportation has the responsibility to regulate the transportation of medical waste. 38 Within 48 hours of becoming involved, that office had issued guidance to hospitals for contracts with medical waste transporters on how to package and transport medical waste.
The final observation, perhaps also implicit in the definition of an emergency, is that a sense of urgency is inherent in the event. Unlike public health programs that address diseases in which the disease burden changes slowly, in an emergency, events can and do change quickly. Response leaders need to remember that every decision and implementation action has to be accomplished within a timeframe—often a very short timeframe. Understanding that timeframe, when a decision or action has to be initiated or completed, means that some decisions have to be made with incomplete information or analysis.
Recurrent Issues and Next Steps
Since 2001, CDC and the nation's public health system have continued to improve capabilities to respond to emergencies. We have accomplished this improvement through ongoing adjustments and refinements to internal procedures and guidance to state and local health departments. Despite this progress, more work remains. The current preparedness and response program represents efforts to develop, improve, and sustain response capabilities. Without sustained funding and leadership support, these gains would quickly erode.
Resources are always scarce at the beginning of a large-scale public health response, and at the outset the ultimate scale of an emergency and response cannot be known. An emergency public health response fund, set up along the same lines as FEMA's Disaster Relief Fund, could alleviate much of this challenge. Such a response fund would include established triggers, authorities, and reporting requirements. Because the scale of public health emergencies varies by orders of magnitude, the resources needed to respond also vary. Even with a response fund, large responses would require a supplemental appropriation or replenishment to a response fund to assure the best response, as is done to fund response and recovery efforts to large-scale natural disasters. Congress appropriated $2.1 billion to CDC for the 2009 H1N1 response and $1.8 billion for the Ebola response. Even when funds are available, public health programs (federal, state, and local) need to have expedited means of contracting, hiring, and otherwise bringing available resources to bear quickly. For CDC, emergency authorities to distribute funds to states quickly would alleviate delays associated with usual grant procedures.
Assuring that trained and experienced staff are available is a further challenge. At CDC, a system of identifying personnel needs and requesting staff with specific skills and training has been established. Being able to recruit retired staff and staff from other agencies and rapidly hire are additional means of shoring up the workforce.
Every emergency CDC has responded to since 2001 has been a natural event—either an emerging infectious disease or natural disaster. 39 Although the strategies and structures put in place after the attacks of September 2001 have shown their value in responding to these natural events, the original motivation for these systems was to be better prepared for bioterror attacks. By their nature, bioterror attacks will be unannounced and will require responders to mobilize countermeasures quickly; resources have to be in place before the attack. A difficult policy decision for the future requires balancing the resources devoted to everyday, naturally occurring emergencies with resources to procure countermeasures and plan and train for their distribution and dispensing in a bioterror attack.
Emergency response—protecting the public from health emergencies—has always been a bedrock function of public health. The planning, training, staffing, and experience of the past 15 years to prepare for and respond to public health emergencies has expanded the scope of emergency preparedness and response as a discipline in public health.
Footnotes
Acknowledgments
The authors thank the following people for their review, editorial assistance, and advice: Dan M. Sosin, Jeffery Bryant, Christine A. Kosmos, Samuel S. Edwin, Roberto Henry, and Cara Rivera.
