West Nile Virus Outbreak: Lessons for Public Health Preparedness
Released: 2000-09-11T00:00:00

Letter

Background

The Viruses: West Nile and St. Louis Encephalitis

Identified in 1937 and named after the Ugandan province where its discovery took place, West Nile virus has a widespread distribution in Africa, West Asia, and the Middle East, occasionally causing epidemics also in Europe. Many people infected with the virus do not become ill or show symptoms, and even when they do, symptoms may be limited to a headache, sore throat, backache, or fatigue. Because no effective antiviral drugs have been discovered, treatment for those who do become seriously ill can only attempt to address symptoms such as swelling of the brain (encephalitis) and other complications such as bacterial pneumonia.

Fatality rates—the percentage of people with confirmed infections who have died—have ranged from 3 to 15 percent for West Nile and are highest in the elderly.

The virus that was originally misidentified as the cause of the New York outbreak is called St. Louis virus. Both West Nile and St. Louis encephalitis viruses are in a group called “flaviviruses,” and can be spread when mosquitoes bite birds (often a natural host for the virus), acquire the virus, and then pass it on to humans (see fig. 1). St. Louis encephalitis is found in nature through much of the lower 48 states and is the most common mosquito-borne virus causing outbreaks of human disease in the United States. About 30 confirmed cases occur on average each year during non- outbreak years. St. Louis encephalitis is also similar to West Nile in that most people infected with it show no symptoms, but for those who become seriously ill, no effective antiviral drugs are available. St. Louis encephalitis has a slightly higher fatality rate than West Nile, ranging from 3 to 30 percent of confirmed cases.

Overview of the Public Health Response Network

Rapid and accurate diagnosis of disease outbreaks is essential for many reasons. It can help contain an outbreak quickly by allowing health officials to implement appropriate control or prevention measures and provide the most effective treatment for those who are affected. Rapid and accurate diagnosis is essential not only for the public at large, but also for health care workers and others who work with patients and laboratory samples. Accurate diagnosis is also important in providing information that could help determine whether the outbreak could have been deliberate—an act of bioterrorism. Public health officials use the term “surveillance” to denote the ongoing effort to collect, analyze, and interpret health-related data so that public health actions can be planned, implemented, and evaluated.

Local health personnel are likely to be the front line of response. Local and state health departments might be the first to recognize unusual patterns of illnesses. For example, an epidemiologist (a health official trained to investigate diseases of unknown origin) in a city health department might receive phone calls from nurses, doctors, or emergency room personnel about increasing numbers of patients with similar symptoms. If the problem is thought to be widespread or suspicious in origin, the local health department is likely to involve the state health department, which is responsible for statewide surveillance and investigations involving multiple locations. The local and state response may also involve emergency management personnel. Current protocols recommend that law enforcement officials be notified if a case or series of cases have a suspicious origin.

Local, state, and federal laboratories also play a vital role. Initially, this role may be to determine whether the unusual cases have the same pathogen (the specific causative agent for the disease), and if so, to identify it. Once an outbreak is established, laboratories may be called upon to test samples such as blood or spinal fluid from persons with similar symptoms, to determine who has the illness and the extent of the problem.

At the federal level, CDC, an agency of the Department of Health and Human Services (HHS), is available upon request to help state and local officials investigate the nature and origin of disease outbreaks. For example, CDC maintains several laboratories that identify unusual or exotic viruses and other pathogens when other laboratories are unable to do so. One such laboratory, at the Division of Vector-Borne Infectious Diseases in Fort Collins, Colorado, deals with viral and bacterial diseases transmitted by vectors such as mosquitoes and ticks. It is part of CDC’s National Center for Infectious Diseases. Besides providing laboratory services, this division also develops ways to diagnose vector-borne pathogens more quickly and helps develop and evaluate approaches to preventing and controlling outbreaks.

CDC is also the lead agency in HHS for bioterrorism preparedness. In recent years, the President and Congress have been increasingly concerned about the threat of terrorists using weapons of mass destruction, including biological agents.Part of CDC’s National Center for Infectious Diseases, the Bioterrorism Preparedness and Response Program is responsible for public health preparedness for potential acts of bioterrorism. In fiscal year 2000, HHS received $278 million of the $10.2 billion in counterterrorism monies allocated to federal agencies. Of the HHS funding, CDC received approximately $155 million for bioterrorism preparedness programs in fiscal year 2000, approximately $40 million of which is to be awarded to state and local health departments for surveillance, epidemiology, laboratory, and communications.

West Nile Identified After Separate Investigations Converge

During the first recognized outbreak of West Nile virus in the United States, infection of animals preceded the first human cases by at least 1 to 2 months. Large numbers of dying birds and an unusual cluster of human cases were at first viewed as separate events. Gradually, as an increasing number of laboratories became involved to conduct further testing on human, animal, and mosquito samples, the linkages became clear, resulting in the identification of the West Nile virus (see fig. 2). The scale of these efforts was substantial, involving participants around the country. Since the end of the outbreak, various local, state, and federal agencies have taken actions to address the potential ongoing consequences of the virus’s introduction into North America.

Detecting West Nile: An Overview

The identification of a newly emerging infectious diseasewithin a few months was due to the combined, considerable efforts of scores of individuals and several agencies in the animal and the human public health fields and in academia. Here is an overview of the key events that occurred. Appendix II contains a more detailed chronology.

The Animal Outbreak

No one is sure exactly when or how birds became infected. By late June a veterinarian at an animal health clinic in the New York City borough of Queens had examined and treated several birds that appeared to have nervous system disorders, releasing those that survived. Reports of dead birds increased through July and into August. By mid-August, dead birds were being sent to the wildlife pathologist at the New York State Department of Environmental Conservation. The wildlife pathologist was able to determine that the birds were not dying from any of several common problems, but he could not identify a clear cause. By late August, veterinarians at the Bronx and Queens zoos had joined the effort to identify the disease, after several wild and caged birds died on zoo property.

The Human Outbreak

Meanwhile, near the end of August, a specialist in infectious diseases in a community hospital in Queens noticed that the hospital had an abnormally large number of suspected cases of encephalitis or meningitis (diseases involving inflammation of the brain or spinal cord) and that several of the patients had developed an unusual pattern of muscle weakness. When the hospital’s doctors were unable to find a clear cause or an effective treatment, the specialist called the Bureau of Communicable Disease within the New York City Department of Health.After a quick but careful investigation, city health officials contacted the state health department and CDC for additional help. Blood and spinal fluid specimens from hospital patients were rapidly tested at state and CDC laboratories. On September 3, CDC announced that the test results were positive for St. Louis encephalitis, a virus known in the United States but never before known to occur in New York City. That same day, the city, assisted by the state and CDC, launched a massive campaign to prevent people from being bitten by mosquitoes and to determine the extent of the St. Louis encephalitis outbreak.

Within the next week, however, the State Department of Health obtained what appeared to be conflicting test results for St. Louis encephalitis, raising doubts among some health officials about whether the exact cause of the outbreak in humans had been determined. In addition, CDC officials were questioned by city and state health workers and the public as to whether the deaths of large numbers of birds and the human encephalitis cases might be connected. Because St. Louis encephalitis had not been known to kill its bird hosts, CDC officials said they considered the two outbreaks to be unrelated. The cause of the outbreak in birds remained unidentified, and, to help identify it, the zoo veterinarians and the state wildlife pathologist enlisted the help of federal veterinary laboratories at the U.S. Department of Agriculture (USDA) and the U.S. Geological Survey (USGS). By mid-September, both laboratories concluded that the bird disease was caused by a virus, that it did not appear to be any strain of St. Louis encephalitis or other avian virus they had previously tested, and that they had insufficient laboratory capabilities to identify it more specifically. The USDA veterinary laboratory sent its virus samples to the CDC laboratory for further analysis.

The Two Responses Converge and More Laboratories Become Involved

The test results in birds, along with repeated negative test results in human samples in the state health department laboratory, increased the doubts of some state health officials about whether the human disease agent had been correctly identified as St. Louis encephalitis. On September 15, they invited a visiting academic researcher from California to try out some new testing methods on tissue specimens from human patients. The following week, a Connecticut agricultural laboratory involved in that state’s routine mosquito surveillance reported isolating St. Louis encephalitis virus from both a dead bird and mosquitoes collected near the outbreak area. This finding was significant in implying that, if the virus was St. Louis encephalitis, it was killing birds and possibly could be connected to the human outbreak.

At about the same time, CDC had begun testing and retesting mosquito, bird, and human specimens against a wider variety of flaviviruses in order to rule out the possibility of another closely related virus. Independently, the head pathologist at the Bronx Zoo gained agreement from the U.S. Army Medical Research Institute of Infectious Diseases to attempt to identify the virus in birds.

Beginning on September 23, the academic researcher and CDC came to the same general conclusion: the virus causing the outbreak was not St. Louis encephalitis but, rather, a virus that had never before appeared in the United States. By the week of September 27, CDC had confirmed that a “West Nile-like” virus was responsible for both the animal and the human outbreaks.

Workload Was Significant

The effort involved in addressing these outbreaks and identifying the cause was concentrated and considerable. Hundreds of reported potential human cases were investigated to determine whether West Nile was the infecting virus. By the end of the investigation, health officials confirmed 62 cases of West Nile virus, including 7 people who died. Thousands of bird deaths were similarly investigated by several state and federal laboratories and agencies, to determine how far the virus had spread. In addition to the laboratory investigations, state and local emergency management teams were mobilized to respond to public health concerns. They managed the coordination of conference calls and other communications, the establishment of hotlines to address the general public’s concerns, and the procurement, distribution, and application of pesticides. The New York City and State Departments of Health also developed fact sheets for the public on each of the pesticides in 1999, and in 2000 they implemented a surveillance system for health effects from pesticides.Table 1 shows some specific examples of the case surveillance and laboratory workload experienced by some of the involved agencies during and since the outbreak. Not all of the agencies involved have developed cost estimates for their efforts. As one indication of the cost, however, New York State officials estimated that the state, city, and four counties in the area spent more than $14 million on protective measures such as mosquito control from late August through October.

Many Federal, State, and Local Activities Have Continued Since the Initial Outbreak

While the first frost of the season signaled the end to the initial outbreak in 1999, activities at the national, state, and local levels have continued. In the first week of October 1999 the New York City Department of Health and CDC conducted a random survey of Queens residents to assess the overall infection rate associated with the outbreak. The results of this serosurvey (in which a blood test for West Nile antibodies is performed) revealed that between 1.2 and 4.1 percent of the population in the area surveyed had been infected with West Nile virus.

The change in diagnosis from St. Louis encephalitis to West Nile also caused public health agencies to evaluate whether aspects of their intervention response should be changed. While the West Nile and St. Louis encephalitis viruses are closely related and mosquito-borne, the change in diagnosis had some implications for the intervention approach. For example, past research had shown that different types of mosquitoes might carry the viruses. Both West Nile and St. Louis encephalitis are carried by a certain species of mosquito, Culexpipiens. However, West Nile is also carried by other species, including Aedesvexansand Anopheles. Some of these species have different habitat and activity patterns. For example, Culexpipiensbreeds in polluted water and is active at night, while A. vexanshas been found in natural areas and is active during the day.Once the distinction between the viruses was made, the public health interventions were changed accordingly to reflect the other types of mosquitoes potentially carrying the West Nile. For example, local public health notices stated that the public should also avoid contact with mosquitoes active during the day. While these differences are not considered significant since the public health recommendations for mosquito control are appropriate in either case, they illustrate the potential significance of an accurate diagnosis in that even closely related viruses might require different responses.

Some of the activity since the initial outbreak has involved learning more about where the virus came from and when it arrived. Research into the origins of the virus found that it is most closely related to a strain isolated in a goose found in Israel in 1998. Testing of previously stored bird tissue samples at the Bronx Zoo was negative for West Nile virus, suggesting the virus was introduced in 1999.

Much of the ongoing effort has been applied to determining whether West Nile will be an ongoing threat to animal and human health. The West Nile outbreak represents a potential problem stretching well beyond New York City, because the virus can spread through bird migrations. In fiscal year 2000, HHS and CDC will provide approximately $10 million for West Nile virus activities. This amount includes grants totaling $4.5 million available to 19 state and local health departmentsalong the Atlantic flyway of migratory birds for West Nile virus surveillance in humans, mosquitoes, and birds. An additional $2.7 million of the $10 million has been made available to 31 other state health departments to expand surveillance capabilities. As of August 2000, communities in at least seven eastern stateshad undertaken active mosquito control programs, such as spraying, as well as public education campaigns and surveillance activities.

Surveillance activities have already produced evidence that West Nile has spread to other areas. In October 1999 a dead crow carrying the virus was found in Baltimore, Maryland. In 2000, as of August, West Nile virus had been detected in birds in nearly all New York counties as well as in Massachusetts, Connecticut, Rhode Island, and New Jersey and in mosquito pools in several states. If West Nile is carried further south along bird migratory routes (see fig. 3 for examples), it could become permanently established in the Western Hemisphere.

The spread of the virus by birds and mosquitoes has significant implications for animal health as well. Animal health officials are concerned about the potential effects on wildlife and other animals, particularly those birds that are susceptible to fatal illness from the virus. The USGS, which conducts surveillance of wildlife health, has helped develop and maintain national maps showing the current wildlife surveillance data now submitted by states.Economic concerns also have been raised. While wild birds were the primary carrier of West Nile in last year’s outbreak, the disease was also detected in domestic livestock. Twenty-five cases were identified in horses on Long Island, nine of which died or were euthanized. Although there is no evidence that the virus can spread from infected horses to uninfected horses or other animals, countries from Argentina to the United Arab Emirates placed import restrictions on horses from affected areas.In addition, the role of commercial poultry in maintaining or transmitting the virus is not thoroughly understood. CDC research has found that chickens can develop a short-lived infection without clinical signs.

Several organizations, including CDC, USDA, the Wildlife Conservation Society, and Flushing Hospital, have organized conferences and workshops to review the West Nile virus outbreak. In December 1999, CDC issued guidelines for West Nile virus surveillance, prevention, and control. In the spring of 2000, HHS and USDA appointed West Nile coordinators to oversee efforts against the virus. See appendix III for a list of some key publications about or related to the virus outbreak.

Lessons Learned Center on Infrastructure and Communication

While many officials and experts we contacted believe aspects of the outbreak investigation went quickly and well, nearly all of them also believe there were lessons to be learned. These lessons may be especially relevant for acts of bioterrorism, where the outbreak of cases may be much more rapid and law enforcement agencies may need to be involved to prevent terrorists from releasing additional biological agents. The time available for decision-making and response may be compressed from days or weeks to a matter of hours. The lessons we identified related primarily to addressing possible needs in five areas: local surveillance and response capabilities, communication among public health agencies, coordination between public health and animal health efforts, capabilities of laboratories, and efforts to distinguish between natural and unnatural events.

The Local Disease Surveillance and Response System Is Critical

The West Nile outbreak provided a number of lessons about surveillance. We learned that many aspects of the surveillance network worked well, speeding the response to the outbreak. These positive lessons can serve as models for other communities that may have less substantial surveillance networks. However, while several of the lessons are positive, the outbreak also exposed some weaknesses.

Many Aspects of Surveillance and Response Worked Quickly and Well

The human outbreak of West Nile began with a few unusual cases. The potential that one or two persons’ medical conditions could be an indication of some larger concern, such as an emerging infectious disease, may not be readily apparent to the health professionals involved. In many cases, such events might not be noticed until a number of physicians have reported the cases and the local health department identifies a cluster, or a number of victims seek care for similar conditions at the same location. Alert responses by the doctors and nurses who first see such victims are particularly crucial in alerting the public health community to the possibility of a wider problem.

In the West Nile outbreak, several actions were particularly important in providing this early alert, as well as in providing valuable evidence for the investigation. Among these actions are the following:

The physician who encountered the first human cases at the local hospital in Queens reported the unusual cluster of illnesses to local public health officials. Such occurrences could easily go unreported, if, for example, the physician does not consider the circumstances to be unusual enough to report or does not recognize a rare disease.

Epidemiologists and staff at the New York City Department of Health took a number of actions that were essential to containing the outbreak. They quickly investigated and recognized the potential significance of the initial case reports. Their interviews with patients and families identified common features in how the patients were exposed out of doors, suggesting that a mosquito-borne disease might be involved. They canvassed all New York City area hospitals to identify potential cases, and throughout their investigation, they remained in daily touch with the many local, state, and federal officials who had quickly become involved. These staff members said previous planning for bioterrorism response in place at the city health department was key to the success of the Department’s response.

Autopsies were performed on the victims. The New York City Department of Health and Office of Chief Medical Examiner worked together to ensure that autopsies were performed on any fatal case of encephalitis. Autopsies were performed on over 25 fatal cases who were initially suspected as having viral encephalitis, including all 4 fatal cases of West Nile encephalitis that occurred among city residents. According to one assessment of the response, information obtained from the autopsies pointed to a flavivirus as the cause and helped guide subsequent laboratory testing.Autopsy rates nationally have been decreasing, at a time when public health officials believe they should increase to help detect infectious diseases. The decline has been influenced by such factors as costs and jurisdictional and authorization uncertainties.

Uncertainty Exists About What to Report, When, and to Whom

While the West Nile outbreak was identified more quickly than otherwise might have been expected because an astute physician reported two unusual cases, it still provides evidence that the reporting system could be improved. The virus might have been identified earlier—perhaps by a week according to an involved official—if case reporting had been better and if good baseline data showing past trends of encephalitis and related diseases had been available. Similarly, a physician we interviewed who had treated West Nile patients said clinicians often do not know whom to call when a cluster of patients with a disease of unknown origin is noticed. Wildlife and zoo officials also indicated that within their fields there is a need for better information and guidance about whom to contact in the public health community when an outbreak is suspected.

These problems have been noted in other instances besides the West Nile outbreak. For example, a November 1998 workshop on public health systems and emerging infections sponsored by the Institute of Medicine— an organization chartered by the National Academy of Sciences to examine public health policy matters—reported that physicians are not sure when or where to report suspicious cases of infection. The workshop also reported that physicians are unaware of the need to collect and forward clinical specimens for laboratory analysis and may not be educated regarding the criteria used to launch a public health investigation. Unlike the case in New York City, where the health department had been actively communicating with physicians, the workshop found that there is often a lack of communication between public health agencies and community physicians.

A 1999 assessment by the Institute found that disease surveillance systems in place at local, state, and federal levels rely on systems of disease reporting from health providers that are notorious for their poor sensitivity, lack of timeliness, and minimal coverage.Because an effective medical response to a bioterrorist event would depend in part on the ability of individual clinicians to identify, accurately diagnose, and effectively treat diseases (including many that may be uncommon), the Institute reported that education about the threat posed by bioterrorism and about the diagnosis and treatment of various agents deserves priority.

Some Inadequacies in Resources for Surveillance Were Exposed

Although this outbreak was relatively small in terms of the number of human cases, it taxed the resources of one of the nation’s largest local health departments. The strain on resources is particularly noteworthy because local health departments in the United States have initiated nearly all the investigations that led to the recognition of infectious disease outbreaks. At the time of the West Nile outbreak, the New York City Department of Health had a unit of about eight people responsible for surveillance and case investigations related to over 50 reportable infectious diseases. Officials told us that having even this small number of trained staff available was critical to the quick response to the initial outbreak. Once the outbreak was identified, these and other staff assigned to help from other agencies and departments worked long hours, seven days a week.

We reported in 1999 that surveillance for important emerging infectious diseases is not comprehensive in all states, leaving gaps in the nation’s surveillance network.Many state epidemiologists reported inadequate staffing for generating and using laboratory data—often considered more reliable for case investigation purposes than physician-reported data—for performing infectious disease surveillance. The Institute of Medicine workshop reported that, in general, epidemiological investigations and surveillance efforts are challenged by a variety of factors. These include changes in the health care system and the continuing use of paper-based disease-reporting systems in many locations, where surveillance is consequently sporadic and inadequate.

Better Communication Is Needed Among Public Health Agencies

Experts consider rapid and reliable communication among public health agencies to be essential to bioterrorism preparedness and coordination. Timely dissemination of information allows public health officials to make decisions with the most current information available. During the West Nile outbreak, however, officials indicated that the lack of leadership in the initial stages of the outbreak and the lack of sufficient and secure channels for communication among the large number of agencies involved prevented them from sharing information efficiently.

Many officials interviewed pointed to the lack of clear reporting guidelines as one source of confusion. Knowing who was in charge or could act as an agency spokesperson, and which agency was responsible for what, would have allowed each agency to operate more effectively. Some officials suggested that each agency should have one “point person” overseeing operations and the flow of information.

During the outbreak, local, state, and federal officials held daily conference calls coordinated by the City or State Department of Health, or CDC. During these calls, officials received up-to-date information on such topics as the human and animal surveillance systems, test results from each laboratory, and schedules for mosquito spraying. While these calls were considered necessary to ensure that all parties heard the same information, they sometimes involved over 100 people and lasted 2 hours or more.As a result, key officials had less time to investigate the outbreak in the laboratory and in the field. Additionally, veterinary health officials were concerned because they were not always included in these calls.

While a secure electronic communication network was in place at the time of the initial outbreak, not all involved agencies and officials were using it at the time. For example, because CDC’s laboratory was not linked to the New York State network, the New York State Department of Health had to act as an intermediary in sharing CDC’s laboratory test results with local health departments. CDC and the New York State Department of Health laboratory databases were not linked to the database in New York City, and laboratory results consequently had to be manually entered there. Physicians, local health departments, and laboratory officials indicated that during the outbreak, it was sometimes difficult to determine the status of patients’ samples and of the laboratory results. During and since the outbreak, however, officials indicated that the use and utility of the network have improved for West Nile surveillance and information sharing. Using the network, the state has put together an interactive surveillance system for mosquito, bird, and human disease reports. Since the fall of 1999, access to the network has been provided to more health officials, including animal health agencies, for tracking West Nile in animals and humans. The communication limitations during the outbreak, the resulting changes to the electronic network capabilities, and the increased reliance on the network for sharing information have increased awareness of the need for established electronic data-sharing mechanisms.

New York State officials told us that the state has invested heavily in its communication infrastructure and has created an advanced information system, but at a national level some local health departments still do not have access to modern communication technologies. A 1999 survey by the National Association of County and City Health Officials found that one- third of health departments serving fewer than 25,000 people did not have access to the Internet or electronic mail. Similarly, more than half the agencies surveyed had neither continuous, high-speed access to the Internet nor broadcast facsimile transmission capabilities.

Links Between Public and Animal Health Agencies Are Becoming More Important

The West Nile events illustrate the value of communication between public and animal health communities, the latter including those dealing with domestic animals, wildlife, and other animals such as zoo animals. Many infectious diseases, including West Nile, are zoonotic, that is, capable of infecting both animals and people. According to recent research, approximately three of every four emerging infectious diseases reach humans through animals.Of over 1,700 known pathogens affecting humans, including viruses and bacteria, 49 percent are zoonotic. Of the 156 pathogens associated with emerging diseases, 73 percent are zoonotic. Many of the viruses or other pathogens considered most likely by CDC to be used in a bioterrorist incident are zoonotic, such as anthrax, plague, brucellosis, tularemia, and the equine encephalitic viruses. An official of the USGS National Wildlife Center noted that many zoonotic pathogens become established in wildlife before they are transmitted to humans and domestic animals. The November 1998 Institute of Medicine workshop reported that, because of their familiarity with a number of these biological agents, the veterinary medicine community should not be overlooked in surveillance efforts.Moreover, veterinarians and veterinary laboratory workers are likely to have been vaccinated against many zoonotic diseases and are used to working with zoonotic pathogens.

The West Nile outbreak shows how domestic, wild, and zoo animals can be considered “sentinels,” providing an early warning device for diseases that can harm people. Even for a deliberate biological attack, animals may be the first victims, unintentionally or as part of an effort to avoid discovery, according to the Institute of Medicine and National Research Council.In the case of the West Nile outbreak, USDA and USGS National Wildlife Center laboratories were involved in early or mid-September in testing bird samples prior to the identification of the West Nile virus. However, because these laboratories lacked reagentsfor the virus, they were unable at the time to specifically identify it.

Experience with the West Nile outbreak also illustrates how links between the animal and public health communities were missing. For example,

Some key public health officials, such as the city health department’s Director of the Bureau of Communicable Disease, indicated that they were not aware of the similarities in the clinical symptoms occurring in the birds and humans until many days or weeks after the human outbreak began. Officials said they believe that communication was hindered even further because, even within the animal health community, there is fragmentation at the state and federal level in what agencies are responsible for different types of animals. For example, domestic animals, such as cats and dogs, are usually the responsibility of state and local health departments. Livestock, such as cattle and swine, are often the responsibility of state agricultural agencies. Wildlife, such as birds, are under the state environmental or wildlife agencies.

When wildlife health officials approached the state public health laboratory to test the bird samples, they were told their samples should be tested at another laboratory, because the state laboratory did not have the reagents to perform animal (bird) testing. According to a New York State animal health official, not having adequate capacity within the state laboratory to test animal samples can create administrative and cost barriers to getting samples tested. For example, many veterinary laboratories will test samples only on a fee basis and not for public health purposes. In some areas of the country, such as the Southwest, where zoonotic diseases such as hantavirus are endemic in the animal population, integration of the animal and public health communities is considered to be better.

Several persons involved in the outbreak commented that the zoo community is currently left out of the animal and public health paradigm, even though zoo animals may be useful sentinels. Zoo animals generally receive close attention from veterinarians, and in some cases pathologists track health care and disease causes, creating detailed health records and storing tissue samples for future analysis. Officials indicated that because zoo animals are not considered to be wildlife or domestic animals, they do not fall within the jurisdiction of animal health agencies such as the USGS, which tracks wildlife issues, or the USDA, which tracks concerns related to domestic animals. The Bronx Zoo pathologist tried many different channels in order to find laboratories willing to prioritize performing additional tests on the bird samples and to provide advice on needed safety precautions for zoo laboratory personnel working with the bird samples.

Many officials provided other examples of where communication between public and animal health communities had not worked well and indicated that the West Nile events pointed to a need for better partnership between these communities. This opinion was voiced even by those who at first disregarded animal health officials’ views and questions about the potential links between the animal and the human outbreaks. For example, in its own internal assessment of the West Nile events, CDC concluded that the relationships between public health agencies at the federal, state, and local levels and their counterparts in public and private agencies that monitor veterinary health should be strengthened. There are indications that some of this greater collaboration has begun. Since the outbreak, archived blood samples from zoo animals drawn in past years have been analyzed as part of the ongoing investigation to determine when and how West Nile was introduced.

Assessment of Laboratory Capacity and Improvement of Linkages Among Laboratories Are Needed

Another frequently cited lesson was the need for improved laboratory infrastructure and technologies for responding to outbreaks and newly emerging viruses. While the concerns were wide-ranging, three common themes emerged: broadening laboratory capabilities, ensuring adequate staffing and expertise, and improving ability to deal with work surges in testing needs. Since the extent to which public health and other laboratories across the country are capable of safely testing dangerous pathogens is unknown, a first step in addressing these concerns may be to complete assessments of inventory and core capacity needs. At the same time, lessons from the West Nile outbreak point to the need to improve current linkages among laboratories.

Broadening Laboratory Capabilities

The need for enhanced laboratory capabilities was frequently mentioned by officials involved in the West Nile outbreak, as well as in various assessments. Officials pointed out the need for more laboratory capacity for identifying and handling infectious agents of high concern to human health, particularly emerging or exotic ones. For example, they said that at the time of the outbreak, only two or three laboratories in the country had the reagents necessary to identify the West Nile virus. One of these was CDC’s laboratory in Fort Collins, which did not initially use this reagent since the first test it had performed was consistent with the related St. Louis encephalitis virus.Because New York State’s laboratory was considered less equipped to perform the diagnostic testing on the human samples once the outbreak was identified, CDC performed the bulk of these tests. In this regard, the need to “expect the unexpected,” a phrase frequently quoted in outbreak assessments, expresses the importance of developing a broader awareness within the laboratories of the potential for new agents to appear and, concurrent with such awareness, developing broader testing capacity. One federal laboratory official suggested, for example, that federal policy should consider a broader dissemination of methods for identifying more exotic pathogens—perhaps those pathogens that are more likely to be introduced to the country through international travel or otherwise.

Some bioterrorism and public health officials noted that, while expansion of laboratory capacity is vital to preparedness, efforts to identify more exotic agents may be beyond the scope of all but the largest health departments and therefore should be a regional or state-based activity. Consequently, some experts have suggested research into determining the utility of developing a network of regional laboratories capable of rapid diagnostic testing.Determining current capacity will be a key first step in assessing the need for a regional network. Currently, the number of public health and other laboratories that can handle those viruses considered most harmful (those classified as requiring Biosafety Level-3 or Biosafety Level-4 equipment, trained staff, and safety procedures in place) is unknown.CDC information indicates that most states lack the public health laboratory capacity to handle many of those viruses that CDC has classified as dangerous and identified as high priority because of risk to national security and public health. Specifically, in fiscal year 1999, less than half of the over 40 states and localities receiving funding for laboratory capacity through CDC’s bioterrorism preparedness grant program reported having advanced capacity for rapid testing for at least four critical biologic agents.Within the veterinary community, a USDA official told us that probably fewer than 20 veterinary laboratories across the country have the capacity to test for Biosafety Level-3 pathogens, and no veterinary laboratories have Biosafety Level-4 capacity.

Ensuring Adequate Staffing and Expertise

Several officials commented on the declining capacity and expertise within the federal and state public health laboratory infrastructure, particularly as it relates to zoonotic and vector-borne diseases. At the time of the outbreak the Fort Collins laboratory capacity was considered to be low, and many needed specialist positions had been eliminated or left vacant as experienced staff had left. Similarly, CDC reported that only a few states and even fewer local health departments have trained personnel or the resources to adequately address vector-borne diseases. According to CDC and other officials, the infrastructure of laboratories with the capacity to handle such diseases has deteriorated in recent decades. The number of laboratories and extent of capacity have dropped, and the staffing, physical plant, and financial support of many remaining laboratories have also been affected.

New York State, prior to the outbreak, lacked the capacity to address vector-borne diseases. A New York State laboratory official indicated that at one time the state had 5 or 6 staff to perform mosquito surveillance to track viruses. In recent years the laboratory’s staff had been cut back as funding was diverted to other public health priorities. By contrast, Connecticut officials indicated that they had—after a similar encounter with eastern equine encephalitis, another mosquito-borne virus—instituted mosquito surveillance in 1997, at a cost of about $200,000.Because of its ongoing surveillance program, the state was able to quickly respond to the outbreak, placing mosquito-monitoring devices in potentially infected areas and identifying the appropriate places to spray. According to a program official, having baseline data—for example, data on where most mosquitoes of concern resided in previous years—allowed the state to make informed decisions about where to spray.

Improving Ability to Deal With Surges in Testing Needs

Testing for West Nile taxed those parts of the laboratory system that were dealing with the outbreak—and in some ways, affected what some of these laboratories were normally expected to do. The New York laboratory that was testing samples for St. Louis encephalitis was also dealing with an outbreak of EscherichiacoliO157:H7 at the same time.Both the New York State and CDC Division of Vector-Borne Infectious Disease laboratories were quickly inundated with requests for tests, and because of the limited capacity at the New York laboratories, the CDC laboratory handled the bulk of the testing. CDC officials reported that nearly all the Fort Collins Arbovirus Disease Branch laboratory staff at one point was working on the response to the virus. Normally, the CDC laboratory functions as a reference laboratory for arboviruses, maintaining the technology and capability to accurately diagnose viruses of this type.In this case, it was acting largely as a diagnostic laboratory, testing patient samples to determine who had the virus and who did not. Officials indicated that the CDC laboratory would have been unable to respond to another outbreak, had one occurred at the same time. Some officials also described what were considered to be unfortunate aspects of CDC’s taking on the role of the diagnostic laboratory. Typically, the CDC laboratory’s role would be to confirm test results rather than to perform diagnostic testing. In this case, in assisting the state in performing the diagnostic testing, CDC focused on determining whether individual patients had St. Louis encephalitis (and then West Nile) rather than identifying other possible causes of illness. This was considered by some to be unfortunate from the standpoint of the individual patients, whose diagnoses could therefore be delayed. Testing at the state laboratory from 95 patients with suspect viral infections found 16, or about 17 percent, of the patients positive for viruses other than West Nile.

Improving the laboratory network is key to improving the laboratory capacity to respond to surges in workload and to provide the new technologies, staff, and expertise to respond to outbreaks. Networks or linkages among federal, state, academic, and possibly private sector laboratories may also be needed, in part to clarify responsibilities for involved laboratories for providing surge capacity, diagnostic testing, and other critical roles in emergency situations. CDC’s internal investigation concluded that the agency should enlist help from academic laboratories. The California researcher who conducted some of the diagnostic laboratory work on the West Nile outbreak was brought in by officials at New York State’s Department of Health because they learned of the innovative research his laboratory was developing to quickly and accurately identify the viral causes of unexplained deaths from encephalitis.Some involved officials indicated that the California laboratory’s involvement was fortuitous in allowing a laboratory not consumed with diagnostic testing for the outbreak to focus on performing the types of tests required to eventually identify the virus. On the other hand, some officials also indicated that this laboratory’s unplanned involvement contributed to confusion about which laboratories were performing tests and the types of tests being performed.

Those involved in responding to the West Nile outbreak have concluded that with a more formal network and clearer roles, necessary tests to accurately identify the virus could have been started the resulting confusion about which federal and other laboratories were involved in the process and the tests each laboratory was performing could have been avoided or minimized.

However, while many agree that more should be done to develop the laboratory network, the plans for such a network are still being developed. CDC’s planned laboratory response network for bioterrorism—linking public health laboratories at the local, state, and federal levels—is still under development.Private, veterinary, and USDA laboratories are not yet part of the network.

Assessment of the public health infrastructure by public health experts, and CDC’s strategic plan for preventing emerging infectious diseases, also point out the need for defining and building the laboratory network. The Institute of Medicine workshop that assessed the capabilities of the public and private sectors for identifying emerging infections reported that surge capacity in response to an outbreak is an area in which the public health laboratory should define its core capability and standards, including the unique and complementary roles of the public and private sector laboratories.CDC’s strategic plan has a goal to strengthen the public health infrastructure in part by strengthening CDC’s capacity to serve as the national and international reference laboratory for the diagnosis of infectious diseases.

Challenges in Distinguishing Between Natural and Unnatural Events Show Common Elements of Preparedness

Finally, the outbreak and surrounding events illustrate the challenges inherent in recognizing a bioterrorist event versus a natural outbreak. In October 1999 a media report suggested that the outbreak could have had an unnatural origin.The Central Intelligence Agency examined the allegations and concluded that there was no evidence indicating that the outbreak was caused intentionally.

The report of the possibility of a bioterrorist event, and the difficulties in correctly identifying the virus and its source, highlight how hard it can be to determine whether an outbreak has an unnatural origin. While the actual response to the West Nile virus outbreak might not have been significantly different had it been considered a potential bioterrorist act, such an event would require the involvement of additional organizations to carry out a criminal investigation. CDC’s current recommended protocols are to notify the Federal Bureau of Investigation and law enforcement officials, who would also seek to determine whether terrorists had targeted additional locations for release of the pathogen. The need to involve these agencies may not be evident at the start. An HHS Office of Emergency Preparedness official indicated that an investigation of a real bioterrorism attack may start as an emerging infectious disease outbreak investigation that finds that the cause was terrorism. It is difficult to establish specific criteria for reporting an outbreak as suspicious, but officials indicated that improved reporting criteria may be needed.

The West Nile investigation is not the only incident that has illustrated the difficulties of determining whether an outbreak was intentionally caused. According to the Federal Bureau of Investigation, there has been only one act of terrorism in the United States in which a biological agent was used, and in this case the deliberate cause was not known until long after the outbreak had passed. The event occurred in September 1984, when 751 persons in Oregon became ill with gastroenteritis, an inflammation of the stomach and intestines. The local health department, with assistance from CDC, discovered that food at salad bars had been contaminated with Salmonellatyphimurium. More than a year later, the Federal Bureau of Investigation learned through a former member of a religious cult that the cult had used the Salmonellato contaminate the food.

The West Nile outbreak may also illustrate the importance of improving our understanding of the causes of unexplained deaths of previously healthy people. Currently, much is unknown about the specific pathogens that cause the deaths of Americans from suspected infectious diseases. Most of the specific causes of encephalitis are undiagnosed. From the point of view of improving surveillance for acts of bioterrorism, a key may be in improving the ability to identify the causative agent in any case where the disease is serious and unusual. One effort toward this end is CDC’s unexplained death project. The project—the focus of the Albany conference at which the academic laboratory at the University of California at Irvine was asked to use innovative techniques to test the human samples—aims to improve CDC’s capacity to rapidly identify the cause of unexplained deaths or critical illness, and to improve understanding of the causes of specific infectious disease syndromes for which a cause is often not found.

Finally, the outbreak and surrounding events support public health officials’ views that bioterrorism preparedness rests in large part on the soundness and preparedness of the public health infrastructure for detecting any disease and the causes of disease outbreaks. An important public health responsibility in any disease outbreak is to identify the agent and source of the disease as part of the process to determine how to prevent it from spreading further. From the public health standpoint, whether an outbreak is natural or artificial may be of little significance, although the political or legal ramifications may be large.Bioterrorism preparedness officials aware of the West Nile outbreak and investigation indicated that because the local public health officials were taking appropriate steps to identify the spread and source of the disease, the proper steps were under way for determining whether the source or origin should be considered suspicious.

Appendix III contains a bibliography of selected assessments and reports that relate to the public health infrastructure and bioterrorism preparedness.

Conclusions

The sudden appearance of West Nile virus in this hemisphere is a clear illustration of the often-repeated need to “expect the unexpected.” Much of the initial response was based on typical steps for identifying and responding to diseases that occasionally break out in the United States. From that standpoint, the correct public health agencies were involved and the response was timely and appropriate. But in this case, critical information and clues pointing to a newly emerging virus were discounted early on, but reemerged later. Persistence, coupled with the significant contributions of additional laboratories, investigators, and researchers, produced the additional evidence leading to the final identification of West Nile as the cause of the outbreak. However, as more agencies became involved, coordination with those already involved in the investigation was not always effective, and communication became more difficult.

How can this incident be translated into increasing the likelihood that the public health network can detect similar threats and then identify and contain them more effectively in the future? The public health community is doing a great deal to respond—both to this particular outbreak, which continues to unfold, and to the larger set of concerns it raised. The lessons we identified are, to some extent, already part of that ongoing effort.

These lessons support the view of many that “an outbreak is an outbreak is an outbreak”—that is, whether an outbreak is intentional or natural, the public health response of determining the causes and containing its spread will be the same. Thus, policies and actions that improve the capabilities of the public health infrastructure—including those that improve the animal health infrastructure—do more than help the nation better prepare for a potential bioterrorist event. These same improvements will also increase our ability to detect and contain the more likely sort of outbreak that starts with a global traveler, a wayward mosquito, or a migrating bird.

We provided a copy of the draft report to CDC, USDA, and New York City and State Department of Health officials for comment. CDC and the New York City Department of Health provided written comments, which are provided in Appendices IV and V. USDA and the New York State Department of Health also provided comments, which are summarized below.

Generally, officials agreed with the lessons and conclusions drawn from experience that are presented in the report. The commenting agencies also offered several observations on various aspects of the report draft. CDC said that its strategic plans for emerging infectious diseases and bioterrorism should be mentioned in the report, and we have done so. CDC expressed a concern with the emphasis in the draft on those aspects that did not go as well as others. Because this report was designed to analyze the events of the fall of 1999 and identify lessons learned for the nation’s preparedness, it necessarily focused on those things that were perceived as problems at that time. CDC also expressed a concern that the report overemphasized the role of the convergence of the human and animal investigations, because laboratory tests conducted by the California researcher and others on the human side were also showing that the virus was not the one initially identified as the cause at the same time as the animal tests. We agree that these contributions were significant, and we made clarifications to the text to recognize them. Nonetheless, we continue to believe that the information from the animal investigations was critical to the timing of the final accurate diagnosis.

New York City Department of Health officials highlighted as important the points in the draft discussing the importance of effective disease surveillance, the need for better communication among public health agencies, and particularly the need for better communication within and among public and animal health communities.

USDA officials indicated that increased emphasis is warranted on the importance not only of public health preparedness, but also of animal health preparedness. Several New York State Department of Health officials and all of the agencies mentioned above provided technical comments, which were incorporated where appropriate.

We also provided relevant excerpts of the draft report to officials from the Bronx Zoo, State of Connecticut, New York State Department of Environmental Conservation, USGS, and University of California at Irvine for technical review, and their comments were incorporated in the draft where appropriate.

We are sending copies of this letter to Donna E. Shalala, Secretary of Health and Human Services; Daniel R. Glickman, Secretary of Agriculture; Jeffrey Koplan, M.D., Director of CDC; and other interested officials.

This work was performed under the direction of Marcia Crosse, Assistant Director. Other major contributors are Rob Ball, Katherine Iritani, Anita Kay, Deborah Miller, and Stan Stenerson. Please contact me at (202) 512- 7119 if you or your staff have any questions.

Methodology

We interviewed officials in the public and private sectors at the national, state, and local levels, and, to the extent it was made available to us, we obtained relevant documentation from them. With this information, we developed a chronology and compiled a list of lessons learned from the West Nile virus outbreak. To some extent, the chronology was based on officials’ recollections of the specific events occurring on particular dates. When information provided by agencies or officials was inconsistent, we assessed its relevance to our reporting objectives, sought any needed corroboration from other involved officials, and incorporated the information accordingly. Officials and agencies contacted included the following:

U.S. Department of Health and Human Services, Office of Emergency

Centers for Disease Control and Prevention, National Center for Infectious Diseases, Division of Vector-Borne Infectious Diseases, Division of Viral and Rickettsial Diseases, Division of Bacterial and Mycotic Diseases

Central Intelligence Agency

U.S. Department of Agriculture, Animal and Plant Health Inspection

U.S. Geological Survey, National Wildlife Health Center

U.S. Army Medical Research Institute of Infectious Diseases

New York State Department of Health

New York State Department of Environmental Conservation

New York City Department of Health

New York City Commissioner’s Office of Emergency Management

Wildlife Conservation Society/Bronx Zoo

Flushing Hospital Medical Center

Connecticut Agricultural Experiment Station

University of California at Irvine

Association of Public Health Laboratories

National Association of County and City Health Officials a ProMED moderator active during the initial outbreak To gather background information and relevant literature on the West Nile outbreak, West Nile virus, and surveillance activities put in place since the outbreak, we searched academic journals and news media and performed an extensive review of publications related to the virus. We performed a similar review to identify reports and literature related to the preparedness of the public health infrastructure for a bioterrorist event.

We also reviewed assessments of the response to the West Nile outbreak prepared by various agencies. These assessments both describe the views of these agencies on lessons learned and outline the steps they have taken and policies they have implemented since the initial outbreak.

Timeline of Key Dates and Events in the West Nile Virus Outbreak, 1999

Time is of the essence in responding to an outbreak of an infectious disease. When the cause of an outbreak is unknown, it is much more difficult to respond quickly and effectively. As can be seen in the following chronological table of events, the key to rapidly identifying and responding to the West Nile virus outbreak lay in merging efforts and information from separate investigations of outbreaks in animals and humans. At the same time, as the number of participants increased, so did the complexity and difficulty of communication and coordination. Looking back on the outbreak of the fall of 1999 provides an opportunity not only to review the significant investigative and laboratory work of a myriad of participants and the contributions of each toward the final diagnosis of the virus, but also to analyze the communications and actions of the responding government agencies in order to improve the nation’s preparedness for future outbreaks, including ones not due to natural causes. Table 2 provides a detailed chronology of significant actions and events.

Related Publications

West Nile Response Summaries and Plans

Centers for Disease Control and Prevention. ExpectingtheUnexpected: Lessonsfromthe1999WestNileEncephalitisOutbreak.Atlanta, Ga.: Centers for Disease Control and Prevention, July 2000. -----. Epidemic/EpizooticWestNileVirusintheUnitedStates:Guidelinesfor Surveillance,Prevention,andControl.Atlanta, Ga.: Centers for Disease Control and Prevention, March 2000.

New York State Department of Health. NewYorkStateWestNileVirus ResponsePlan. Albany, N.Y.: New York State Department of Health, May 2000.

Wildlife Conservation Society. ProceedingsoftheWestNileVirusAction Workshop. New York, N.Y.: Wildlife Conservation Society, Jan. 19-21, 2000.

West Nile Virus

Veterinary/Animal Health

Anderson, J.F., T.G. Andreadis, C.R. Vossbrinck, and others. “Isolation of West Nile Virus From Mosquitoes, Crows, and a Cooper’s Hawk in Connecticut.” Science, Vol. 286, No. 5448 (Dec. 17, 1999), p. 2331.

Nolen, R.S. “Veterinarians Key to Discovering Outbreak of Exotic Encephalitis.” JournaloftheAmericanVeterinaryMedicalAssociation, http://www.avma.org/onlnews/javma/nov99/s111599a.asp (cited Nov. 15, 1999).

Steele, K.E., M.J. Linn, R.J. Schoepp, N. Komar, T.W. Geisbert, R.M. Manduca, P.P. Calle, B.L. Raphael, T.L Clippinger, T. Larsen, J. Smith, R.S. Lanciotti, N.A. Panella, and T.S. McNamara. “Pathology of Fatal West Nile Virus Infections in Native and Exotic Birds During the 1999 Outbreak in New York City, New York.” VeterinaryPathology, Vol. 37 (May 3, 2000), pp. 208-24.

Medical/Public Health

Asnis, D., R. Conetta, A. Teixeira, and others. “The West Nile Virus Outbreak of 1999 in New York: The Flushing Hospital Experience.” Clinical InfectiousDiseases, Vol. 2000, No. 30 (Feb. 29, 2000), pp. 413-18.

Centers for Disease Control and Prevention. “Outbreak of West Nile-Like Viral Encephalitis—New York, 1999.” MorbidityandMortalityWeekly Report, Vol. 48, No. 38 (Oct. 1, 1999), pp. 845-49. -----. “Update: West Nile-like Viral Encephalitis—New York, 1999.” Morbidity andMortalityWeeklyReport, Vol. 48, No. 39 (Oct. 8, 1999), pp. 890-92.

Cheng, G.S. “West Nile Virus: Physician Reports Will Be Crucial.” Family PracticeNews, Vol. 30, No. 1 (Jan. 1, 2000), p. 12. “Exotic Diseases Close to Home.” Editorial, TheLancet, Vol. 354, No. 9186 (Oct. 9, 1999), p. 1221.

Research

Briese, T., J. Xi-Yu, C. Huang, L.J. Grady, and I.W. Lipkin. “Identification of a Kunjin/West Nile-like Flavivirus in Brains of Patients With New York Encephalitis” (Letter). TheLancet, Vol. 354, No. 9186 (Oct. 9, 1999), pp. 1261-62.

Enserink, M. “Groups Race to Sequence and Identify New York Virus.” Science, Vol. 286, No. 5438 (Oct. 8, 1999), p. 206. -----. “New York’s Lethal Virus Comes From Middle East, DNA Suggests.” Science, Vol. 286, No. 5444 (Nov. 19, 1999), p. 1450.

Lanciotti, R.S., J.T. Roehrig, V. Deubel, and others. “Origin of the West Nile Virus Responsible for an Outbreak of Encephalitis in the Northeastern United States.” Science, Vol. 286, No. 5448 (Dec. 17, 1999), p. 2333.

Shieh, W.J., J. Guarner, M. Layton, A. Fine, J. Miller, D. Nash, G.L. Campbell, J.T. Roehrig, D. J. Gubler, and S.R. Zaki. “The Role of Pathology in an Investigation of an Outbreak of West Nile Encephalitis in New York, 1999.” EmergingInfectiousDiseases, Vol. 6, No. 4 (May-June 2000), pp. 370-72.

Smithburn, K.C., T.P. Hughes, A.W. Burke, and J.H. Paul. “A Neurotropic Virus Isolated From the Blood of a Native of Uganda.” AmericanJournalof TropicalMedicineandHygiene, Vol. 20 (1940), p. 471.

Tsai, T.F., F. Popovici, G.L. Cernescu, and N.I. Nedelcu. “West Nile Encephalitis Epidemic in Southeastern Romania.” TheLancet, Vol. 352 (Sep. 5, 1998), pp. 767-71. “West Nile Virus Similar to Israel ’98 Virus.” FamilyPracticeNews, Vol. 30, No. 1 (Jan. 1, 2000), p. 12.

Reemergence

Holloway, M. “Outbreak Not Contained.” ScientificAmerican, Vol. 282 (April 2000), pp. 20-22.

Moran, M. “West Nile Outbreak Sends Wake-up Call for Surveillance.” AmericanMedicalNews, Vol. 43, No. 3 (Jan. 24, 2000), p. 1.

General

Centers for Disease Control and Prevention. PreventingEmerging InfectiousDiseases:AStrategyforthe21stCentury. Atlanta, Ga.: U.S. Department of Health and Human Services, 1998.

Centers for Disease Control and Prevention, National Center for Infectious Diseases, Division of Vector-Borne Infectious Diseases. Guidelinesfor ArbovirusSurveillanceProgramsintheUnitedStates. Atlanta, Ga.: Centers for Disease Control and Prevention, April 1993.

Public Health Service. AddressingEmergingInfectiousDiseaseThreats:A PreventionStrategyfortheUnitedStates. Atlanta, Ga.: U.S. Department of Health and Human Services, 1994.

Bioterrorism and Public Health

West Nile Specific

Schoch-Spana, M. “A West Nile Virus Post-Mortem.” BiodefenseQuarterly, Vol. 1, No. 3, www.hopkins-biodefense.org/pages/news/quarter1_3.html (cited Dec. 1999).

General

Advisory Panel to Assess Domestic Response Capabilities for Terrorism Involving Weapons of Mass Destruction. “Excerpts, First Annual Report to the President and the Congress.” ww.rand.org/organization/nsrd/terrpanel/ terror.pdf (cited Dec. 15, 1999).

Centers for Disease Control and Prevention. “Biological and Chemical Terrorism: Strategic Plan for Preparedness and Response: Recommendations of the CDC Strategic Planning Workgroup.” Morbidity andMortalityWeeklyReport, Vol. 49, No. RR-4 (April 21, 2000).

Ember, L. “News Focus/Bioterrorism: Combating the Threat.” Chemical andEngineeringNews, Vol. 77, No. 27 (July 5, 1999), pp. 8-17.

Institute of Medicine. ChemicalandBiologicalTerrorism:Researchand DevelopmenttoImproveCivilianandMedicalResponse. Washington, D.C.: National Academy Press, 1999.

Lasker Charitable Trust. “Bioterrorism/Domestic Preparedness Suffers From Neglect of Public Health Infrastructure.” www.laskerfoundation.org/ fundingfirst (cited Sept. 16, 1999).

McDade, J.E. “Addressing the Potential Threat of Bioterrorism—Value Added to an Improved Public Health Infrastructure.” EmergingInfectious Diseases, Vol. 5, No. 4, (July-Aug. 2000), pp. 591-92.

National Intelligence Council. “The Global Infectious Disease Threat and Its Implications for the United States.” NationalIntelligenceEstimate99- 17D(Jan. 2000).

Novick, L. (ed.). JournalofPublicHealthandManagementPractice(July 2000).

Comments From the Centers for Disease Control and Prevention

Comments From the New York City Department of Health

Ordering Information

The first copy of each GAO report is free. Additional copies of reports are $2 each. A check or money order should be made out to the Superintendent of Documents. VISA and MasterCard credit cards are accepted, also.

Orders for 100 or more copies to be mailed to a single address are discounted 25 percent.

Ordersbymail: U.S. General Accounting Office P.O. Box 37050 Washington, DC 20013 Ordersbyvisiting: Room 1100 700 4th St. NW (corner of 4th and G Sts. NW) U.S. General Accounting Office Washington, DC Ordersbyphone: (202) 512-6000 fax: (202) 512-6061 TDD (202) 512-2537 Each day, GAO issues a list of newly available reports and testimony. To receive facsimile copies of the daily list or any list from the past 30 days, please call (202) 512-6000 using a touchtone phone. A recorded menu will provide information on how to obtain these lists.

To Report Fraud, Waste, or Abuse in Federal Programs

Web site: http://www.gao.gov/fraudnet/fraudnet.htm e-mail: fraudnet@gao.gov

1-800-424-5454 (automated answering system)