Lessons from Select Public Health Events Having Relevance to Bioterrorism Preparedness

Introduction

The intent of this briefing paper is to examine the responses of the public health and health delivery systems of three cities that were challenged by extraordinary disease outbreaks and draw lessons useful to those who are involved in bioterrorism preparedness. We thus analyze the infectious disease outbreaks that occurred in The Dalles, Oregon, in 1984; Surat, India, in 1994; and Toronto, Canada, in 2003. In addition, we give a brief explanation why the so-called "anthrax letters" attacks of September-October 2001, are not addressed here. The brief concludes with a listing of lessons we have drawn from the case studies that could prove useful to bioterrorism preparedness planners in the United States.

FOODBORNE SALMONELLA: THE DALLES, OREGON, UNITED STATES, 1984

Site and Effects of Outbreak

The Dalles is located on the Columbia River in north-central Oregon, about 80 miles east of Portland. Its small population of about 11,000 in 1984, belies the large scale of economic activity in the city resulting from The Dalles being a major transportation hub between eastern and southern Oregon and Washington State.[1] The major east-west thoroughfare, Interstate 84, passes through The Dalles, so, on any given day, the city's population temporarily increases as travelers stop to rest and eat. For this reason, The Dalles is home to a disproportionately large number of restaurants; approximately 38 restaurants in 1984.[2] Such a large number of eating establishments and the transient nature of many of their customers made for a challenging epidemiological investigation when Salmonella typhimurium was discovered to be at the root of an outbreak of gastrointestinal illness in September 1984.

Salmonella bacteria typically are found in and transported by the feces of humans and other animals. In humans, these bacteria can cause gastrointestinal diseases, characterized by diarrhea, fever, and abdominal cramping. Salmonella infection (salmonellosis) does not usually require treatment beyond rest and oral rehydration; however, potentially life-threatening situation may occur when the infection strikes infants, children, and immunocompromised adults. When this occurs, treatment with antibiotics may be appropriate. Approximately 40,000 cases of salmonellosis are reported annually in the United States, with about 600 of the affected dying.[3]

On September 17, 1984, an individual who had gotten sick after eating at a local restaurant called the Wasco-Sherman County Health Department in The Dalles. Two days later, an additional 21 persons reported similar complaints and implicated two other restaurants. Within 48 hours of the first reported case, the clinical laboratory at the Mid-Columbia Medical Center, Wasco-Sherman County's only hospital, identified Salmonella in the patient's stool sample. The Oregon State Public Health Laboratory quickly confirmed this identification, and was able to further ascertain the species as typhimurium.[4]

Two weeks after the first case of salmonellosis, a classic epidemiological investigation carried out by the county health department established a link between salmonellosis victims and restaurants in The Dalles. All 38 restaurants in the city and its vicinity were asked to shut down their salad bars, which they did. Assistance from the U.S. Centers for Disease Control and Prevention (CDC) was sought.[5] Teams comprised of local and federal epidemiologists interviewed hundreds of victims and hundreds of restaurant customers who had not become sick to determine what they had eaten. They tracked down out-of-town visitors who had eaten at the restaurants. They also interviewed restaurant workers, inspected food handling practices at the restaurants, and examined farms, dairies, and water systems that supplied the restaurants.[6] In the end, the epidemiologists concluded that food handlers employing poor sanitary practices had contaminated restaurant salad bars with Salmonella typhimurium.[7] In the final tally, 751 cases, representing about 12% of the town's populations, of salmonellosis were confirmed. Ten of the county's restaurants were implicated as having been contaminated.[8]

In October, 1985, a bit over one year after the salmonellosis outbreak, the Bhagwan, the head of the Rajneesh cult, which had its U.S. headquarters in Wasco-Sherman County, during a television press conference alleged that some cult members had attempted to contaminate the water supply in The Dalles.[9] In response, state police, in collaboration with the FBI, obtained a warrant to search the Rajneeshees' compound, where they discovered a simple clinical laboratory that was equipped with an incubator and had supplies for growing cultures.[10] The searchers also found glass vials containing discs impregnated with Salmonella typhimurium.[11] Under questioning, cult members told the police that two women, Ma Anand Sheela and Ma Anand Puja, had ordered the laboratory technician to secure the Salmonella discs from a commercial supplier and to propagate a large quantity of the pathogen. Cult members then sprinkled the pathogenic "salsa" on lettuce and other fruits and vegetables and put Salmonella bacteria in restaurant coffee creamers and salad dressings.[12] Those who took part in this deliberate contamination were arrested and tried. The Bhagwan was deported to India, while Ma Anand Sheela and Ma Anand Puja were convicted and sentenced to multiple 20-year prison terms. Other cult members who took part in the dispersal of the pathogen were also convicted and received light jail sentences.[13]

Social Consequences of Outbreak

The Dalles salmonellosis outbreak stressed the small town's health infrastructure. The Mid-Columbia Medical Center had around 125 beds at the time. During the outbreak, the hospital surpassed its capacity for the first time in its history, forcing patients to receive care in the building's corridors. Angry about the capacity issue and no doubt worried about the large number of fellow victims suffering the same symptoms, patients grew hostile, allegedly throwing stool and urine samples at health care workers in some cases and making unreasonable demands for laboratory results. As the number of samples sent to the Mid-Columbia Medical Center's clinical laboratory increased 30- to 40-fold during the outbreak, it was overtaxed. At its most trying time, the laboratory actually ran out of culture media. The laboratory was able to increase the shipments of culture medium that it received during the outbreak, but it was still insufficient for the number of samples with which it was presented at the height of the outbreak.[14]
It is important to note that while the outbreak stressed the local public health and health delivery systems, there was no indication that either was anywhere near the point of collapse. Neither city, nor county officials asked the state of federal government for assistance beyond the request for certain types of experts and no mutual assistance agreements between the Wasco-Sherman County and neighboring counties were invoked.

Economic Damages

As far as we are aware, no economic analysis has been done on the consequences of The Dalles outbreak, so they cannot be determined with certainty. We can infer that the costs associated with the substantially increased patient load experienced by the Mid-Columbia Medical Center were borne largely by the inhabitants of the city and county, as were the salaries of health workers putting in overtime. Further, the epidemiological investigation into the origin of the outbreak, which involved public health officials checking the many possible sources of Salmonella, including local water systems, a local dairy, a tomato and cucumber farm, and others, probably incurred costs beyond the county health department's normal budget. As natural sources were found to be clean, it became apparent that restaurants were the origin. Health officials spent much effort on testing restaurant employees to identify possible carriers of Salmonella, which must have been a costly process. Further, once it became known that restaurants were the source of infection, this likely had a substantial adverse economic effect as consumers understandably would have grown leery of eating away from home; also, many employees who handled food in these establishments were sickened and probably were unable to work. The economic consequences of this Salmonella outbreak on the city and county almost certainly were even greater than losses suffered by the restaurant industry alone. These costs, however, cannot be documented.

PLAGUE: SURAT, INDIA, 1994

Site and Effects of Outbreak

Surat is a western Indian city that lies along the Tapti River in the state of Gujarat approximately 250 kilometers north of Mumbai (Bombay). The city has an estimated population of between 1.8 million[15] and 2.2 million[16], about 600,000 of whom are part-time residents[17]. A large number of Surat's inhabitants live in the city's wretched urban slums. Surat is the home to bustling diamond and textile industries. In 1994, Surat was challenged by a large outbreak of pneumonic plague.

The bacterium that causes plague, Yersinia pestis, is known to exist in natural reservoirs in India, including certain wild rodent populations.[18] From there the plague bacterium can be transmitted via insect vectors – most commonly the flea – to urban black rats (Ratus ratus), as well as the fleas that inhabit them. Y. pestis usually is transmitted to humans by the bite of an infected flea, which most often leads to the bubonic form of the disease. If the bubonic form of plague progresses to a systemic form, thus infecting the lungs, human-to-human spread via aerosolized droplets becomes possible.[19]

The origin of the disease outbreak in Surat and, indeed its diagnosis, has been the subject of much disagreement.[20],[21],[22] For our purpose, the retrospective questioning of the accuracy of the diagnosis (i.e., whether the outbreak was pneumonic plague or some other type of infectious disease) matters little since the disease was believed to be "plague" by both those who were directly affected, those who were not affected but took certain actions because they believed it was "plague," and observers who reported on the events as they unfolded in 1994.

Social Consequences of Outbreak

In late September 1994, just after the yearly Hindu Ganesh Festival had brought an influx of visitors to Surat and just as the weather in India was becoming mild enough to usher in the annual tourist season, the first pneumonic patients appeared at the Surat Civil Hospital.[23] Local doctors quickly diagnosed them as suffering from plague. Within about one day, word of a mysterious fever spread by way of print and radio media, and panic enveloped Surat. Over the course of a few days, 400,000-600,000 people fled the city.[24] There was chaos at Surat's bus and rail stations, sometimes escalating to mob violence.[25] The Indian army's Rapid Action Force, which is specially trained in riot control, was called in to restore order and, most importantly, to prevent possible carriers of Y. pestis from leaving Surat.[26] Messages from the World Health Organization (WHO) to stay calm,[27] as well as reassurance from Indian Prime Minister Narasimha Rao that the situation was "well under control," went largely unheeded by Surat's inhabitants.[28]

The city's health delivery system was severely damaged as many of the city's health care workers absconded. In fact, a volunteer organization later filed criminal charges against 70 physicians, stating that they had abandoned the population in a time of great need.[29] Some offices of doctors who had left the city were torched.[30] However, it is not known how many health professionals remained and how many fled.[31] In addition to health workers fleeing, the antibiotic tetracycline, which is commonly used to treat plague, disappeared from pharmacies.[32] This drug was unregulated and thus available over the counter. Lacking proper guidance on how to effectively utilize the antibiotic, people—even those who were not presenting with disease symptoms—hoarded the drug. The resulting shortage of tetracycline led to the antibiotic being black-marketed, even among pharmacies.[33]

Economic Damages

Internationally, India's tourism and trade were heavily impacted. The Gulf states (Kuwait, Saudi Arabia, Qatar, Oman, and United Arab Emirates), followed by Pakistan and Sri Lanka, prohibited travel to and from India altogether.[34] Indian exports were also banned from entering these countries.[35] Even when a country did not place explicit travel restrictions on persons arriving from India, officials at many airports delayed travelers from India after they disembarked for inspections and other forms of scrutiny.[36]

On a local level, many workers failed to report to their work sites during late September, so commerce and productivity were negatively affected.[37] The reports of chaos in Surat led to a general trepidation among investors in the Indian stock market.[38] The Mumbai stock market suffered substantial losses after the announcement that trade between India and the Gulf state nations, which amounts to around $3 billion per year, would be suspended. Interestingly, the stock market dipped even further as India's Cabinet members held a meeting on September 29 to discuss the crisis in Surat,[39] perhaps demonstrating that the public interpreted the high-level meeting to be an indicator of a worsening situation in Surat.

Plague's impact on Surat, and India, were remarkable given that only about 100 people died from the disease.[40] Economically, the trade and tourism losses resulting from the plague outbreak have been estimated at about $1.3 billion. If one also factors in direct medical expenses and decline in production, that loss approaches $2 billion.[41] These numbers are staggering, especially when one considers that most of the financial losses came from worries that the stigmatized disease would spread and not from the actual physical harm associated with the outbreak.

It is of interest, and concern, that communications from high national and international leaders and agencies had few if any positive effects on how events unfolded in Surat. Reassurances from government officials that the situation was under control and messages from the WHO instructing residents not to panic were proved to be weak, possibly because they were so poorly communicated to the Surat population.

SEVERE ACUTE RESPIRATORY SYNDROME (SARS): TORONTO, CANADA, 2003

Sites and Effects of Outbreak

The first case of a virulent, atypical pneumonia materialized at a hospital in Foshan, Guangdong Province, in southeastern China on November 16, 2002, and then spread throughout the region. It is not our purpose to describe how this illness, named severe acute respiratory syndrome (SARS) by WHO on February 21, 2003,[42] spread in China and then internationally;[43] rather, we focus on how the causative virus arrived in Toronto, Canada.

SARS is caused by a coronavirus (SARS-CoV) and presents itself as a serious respiratory illness with high fever, bodyaches, headache; and pneumonia. SARS' fatality rate depends to a large extent on the victim's age; thus, under the age of 24 it is less than 1%, for ages 25-44 it is 6%, for ages 45-64 it is 15%, and for over the age of 65 it is higher than 50%.[44] SARS-CoV spreads human-to-human via infectious droplets released by coughs and sneezes or direct contact.[45] The virus is hardy, able to survive after drying on a surface for up to 48 hours and for four days in a stool sample. The average number of secondary infections generated per case (Ro) is estimated to be 2.7;[46] for comparison, the Ro for measles is 10-15, pertussis is 16-18, polio is 8-12, and seasonal influenza is 1.4-2.6 ( can go up as high as 21 in certain settings).[47] SARS-CoV is thus considered a moderately transmissible pathogen. (Under certain circumstances individuals infected with SARS-CoV have been demonstrated to be much more contagious than the average SARS sufferer, with a Ro of up to 90. These individuals are called super-spreaders. There appears to have been at least one super-spreader in Toronto.)

Toronto, the capital of Ontario Province, is the largest metropolis in Canada and the fifth largest city in North America.[48] According to 2003 data, Toronto's population was 2.5 million people, while the population of the Greater Toronto Area (GTA), which incorporates adjacent cities, was over 5 million.[49] The city is a major stopping point for both immigrants[50] and international travelers. Tens of thousands of travelers from Asia arrive every month at Toronto's Lester Pearson International Airport.[51]

Toronto's SARS index case was Mrs. Kwan Sui-chu (Mrs. K),[52] a 78 year old diabetic who in February 2003 stayed at the Hotel Metropole in Hong Kong. A severely ill physician who had arrived on February 21 from Guangdong Province stayed for just one night in a room adjacent to that of Mrs. K. Mrs. K is believed to have been infected by SARS-CoV on February 21 as she and her husband passed by "…an elderly Chinese man who was coughing severely and struggling to stay upright. He coughed several times in their general direction and when he looked up, they were struck by his angry, blood-shot eyes."[53] On February 23, Mrs. K flew to Toronto, her home city, and began to feel ill on February 25. Her primary care physician treated her with antibiotics on February 28, but she developed breathing problems and died at home on March 2. Retrospective epidemiological studies found that Mrs. K had infected her physician, who in turn started an epidemic among other health workers and their patients, as well as her 43 year old son and 38 year old daughter. The ill son sought help at the nearby Scarborough-Grace hospital on March 7, where he was kept in the emergency department for about 12 hours since no beds were available in the in-patient wards. During this time, he infected many health workers, out-patients, and visitors.[54] He died on March 13 of respiratory failure.

Toronto's SARS outbreak has been described in detail elsewhere;[55] here we review the highlights of the outbreak.[56] The outbreak had two phases, with phase 1 occurring between March 23 and April 19, and phase 2 between April 20 and July 2, when WHO designated Toronto as free of SARS. During this 3.5 month long period, 2,132 persons in Toronto were investigated as possible SARS victims; of these, 225 met WHO's case definition of SARS (it should be noted that an additional 133 persons living in municipalities adjoining Toronto contracted SARS). Of Toronto's SARS victims, 55 (24.4%) required intensive care and 38 (16.8%) died. There were 23,103 persons who had some sort of contact with actual or suspected SARS victims and therefore required quarantine; of these, 13,291 (57.5%) complied while the remainder either could not be reached or was reached after the quarantine period had expired. It therefore appears as if there was no case of outright refusal to comply with what was a voluntary quarantine imposed by city and provincial authorities. It is important to note that the site where by far most of those who were exposed to SARS-CoV (16,149 or 69.9%) was a hospital, while 2,148 (9.3%) was at a school, 2,150 (9.3%) at a doctor's office, 924 (4%) at a social setting, and 554 (2.4%) at the household of a sick person. Of the 19 acute care hospitals in the GTA, 11 became directly involved in the outbreak.

Social Consequences

We begin by noting what did not happen in Toronto; thus, there was no public disorder, no flight of inhabitants or health professionals, no run on drugs in pharmacies, nor any apparent restrictions on Canadian citizens or products by other countries. In fact, the social consequences for public health and health delivery tended to be so subtle as to become known only in retrospect.

In regard to public health, an analyst put it succinctly: Toronto suffered from "…a system under significant duress because of a 20-year erosion of investment in the public health system and because, as a consequence, many building blocks of an effective emergency response were not in place when SARS hit the city."[57] The "building blocks" included a weak and understaffed Toronto Public Health Department (TPH), a software program for reporting infectious diseases in Ontario that proved unworkable, and lack of expertise within TPH on communicable diseases and handling them. Further, when the TPH ordered the institution of a voluntary quarantine program to keep contacts at home (the quarantined persons were contacted by TPH twice per day by phone), there were a few serious break-downs of this system, such as a worker who asked his wife to cover for him when the TPH phoned while he went to work; he contracted a fatal case of SARS and infected a co-worker who also died.[58] On another level, public health officials at the federal, provincial, and city levels became incensed when WHO issued a global advisory against all non-essential travel to Toronto on April 23. However, by this time, the SARS outbreak was largely over and, furthermore, it was clear that by far most persons who had contracted the disease had done so in hospitals and doctors' offices, which meant that a visitor to Toronto stood a very, very small chance of becoming exposed to SARS-CoV. While the largest effect of the advisory was on the Canadian economy, it was demoralizing and embarrassing for the Canadian public health system to seemingly be put on the same level as the poverty-stricken Guangdong province in China.

The social impacts on the health delivery system were significant. One stemmed from an existing problem; Toronto's health delivery system had no surge capacity. This situation stemmed from the fact that many hospitals had been closed down during the 1990s for financial reasons, so the Toronto's hospitals were filled to 95% capacity when Mrs. K's son presented arrived at the Scarborough-Grace Hospital and therefore could not be accommodated in a closed ward.[59] As the outbreak grew, and as emergency departments, and even hospitals, were closed, a big problem arose regarding what to do with SARS victims. Eventually, a closed tuberculosis ward in one hospital was reactivated, and wards in other hospitals were converted overnight to contagious wards. The problem then became how to staff them (below), which remained an issue to the outbreak's end. Thus the problems created by the surge of severely sick SARS victims was largely solved, but it must be kept in mind that their number in GTA was just 358, and those cases arose over a 3.5 month period.[60]

However, one of the main impacts stemmed from the fact that so many doctors, nurses, and other health workers contracted SARS from patients; in all 46.3% of Toronto's SARS victims were health workers,[61] including many who everyone thought had taken careful precautions such as wearing gowns and masks, and practicing frequent hand washing. Many health workers came to fear working in environs where SARS patients were kept, so there developed a shortage of care-givers at temporary emergency facilities set up at various Toronto hospitals for the specific purpose of treating SARS victims. So, while health workers did not flee from Toronto, many of them declined to work with SARS patients, which resulted in those who did so becoming overworked and overstressed.

Further, all supplies of special equipment needed to treat SARS victims, such as assisted breathing devices, intubation kits, negative pressure rooms, etc., were quickly depleted in Toronto, causing shortages that negatively affected patient care.[62] Although shortages were soon rectified by bringing in supplies from stores elsewhere in Canada, it again must be kept in mind that "only" 358 SARS victims in GTA had such a profound affect on depleting the supply of all this type of special equipment in a major city and its environs in a highly industrialized country.

Economic Damages

There were three types of economic damages suffered by public and private sectors of Canada, Ontario, and GTA: (1) direct costs related to containing the outbreak and treating its victims; (2) indirect costs related to lost productivity, wages, health insurance premiums, and others; and (3) tourism revenue losses.

We do not have figures for the first two types, but believe it must have been at least one billion Canadian dollars. The estimated revenue loss for such spending categories as accommodation, food and beverage, transportation, recreation, and entertainment was 260.6 million Canadian dollars for the period March 2, 2003 through June 21, 2003.[63] Unemployment in the city rose to 7.7%, a full half-percent higher than the preceding month, with over 40% of job losses occurring in the hotel and restaurant sectors.[64] WHO's advisory likely contributed to these figures; however, tourism remained depressed even after the warnings were rescinded.[65] Because Toronto's economy contributes 20% of Canada's total economic activity, financial consequences of SARS had a national impact.[66] Even relatively early in the outbreak economists were predicting reductions in the national annualized growth figures,[67] but we have not been able to find a good estimate as to the total loss. Putting the economic impact of SARS on Toronto and Canada into perspective, some likened the consequences of this outbreak to the financial fallout that resulted from the events of September 11, 2001, in New York City and Washington, D.C.,[68] which certainly was more than a few billion dollars.

ANTHRAX ATTACKS IN SEPTEMBER/OCTOBER 2001

The terrorist attacks in 2001 that utilized envelopes filled with Bacillus anthracis spores and sent through the U.S. Postal Service probably is one of the most prominent health events of that year, and one that undoubtedly remains in the minds of most adult Americans to this day. These attacks caused 22 cases of cutaneous and pneumonic anthrax in New York, New Jersey, Florida, Connecticut, and Washington, D.C.; of these, five died.[69] As of this writing, those responsible for these attacks have not been brought to justice. These attacks, and the casualties they caused, without a doubt shook public confidence in the government's ability to protect its constituents from a bioterror attack and respond effectively to accomplished attacks. However, the relatively small number of casualties they caused, as well as their wide geographic reach, makes them individually or collectively poorly suited for the purposes of this brief.

Conclusion

The three infectious disease outbreaks described and discussed here were caused by one non-communicable bacterial pathogen (Salmonella typhimurium), one communicable bacterial pathogen – Yersinia pestis (its communicability appeared to be of low order), and one moderately communicable virus (SARS-CoV). Many, many lessons can be learned from these outbreaks useful to both public health and health delivery professionals, but here we draw three.

First, without doubt the communicable pathogens caused many more problems to both the public health and health delivery communities. Thus, for public health the immediate issue had to do with containing the spread of disease, which entails the immediate imposing of public health measures ranging from frequent hand washing to the quarantine of entire communities. The longer it takes to impose these measures, the wider the scope of the outbreak and the more serious its intensity. Thus, communicating information to the public and its leaders about the causative pathogen, its mechanism of spread, and what the community needs to do to stop the spread becomes of the utmost importance. Conversely, if the outbreak is caused by a non-communicable pathogen, once public health professionals have identified from whence it originated, it usually is not so difficult to isolate and neutralize that pathogen's reservoir or source and thus stop the outbreak.

For health providers, communicable diseases also create difficult problems, in the first place having to do with protecting themselves and the public from contracting the contagious pathogen from infected individuals. As was demonstrated by SARS, if protection is not affected, the health providers and their institutions can act as amplifiers of the disease, thus becoming an important part of the problem rather than the solution. Therefore, although the quick identification of the pathogen is of high importance, it is paramount that health providers coming into contact for the first time with sick individuals displaying the usual signs of infection (e.g., elevated temperature, wheezing, coughing, high white blood cell count) immediately assume that they are dealing with a communicable disease and take appropriate personal and community protective actions.

The Surat and Toronto outbreaks both demonstrated that a dreaded contagious disease is likely to severely affect the availability of health workers willing to work with its victims. It is not hard to visualize that regardless of its site, were an outbreak to occur in the future that is caused by a highly contagious pathogen (SARS-CoV is moderately contagious and Y. pestis was probably even less contagious) and would last for some months or longer, the situation regarding availability of health workers to work with victims would deteriorate markedly and more or less rapidly, possibly leading to a deadly vicious circle where more and more inhabitants become sick and fewer and fewer health providers are available to provide help to them.

Second, it has become almost a truism among preparedness professionals that catastrophic health events are, first of all, local events, which means the response to them must in the first instance depend on locally made preparedness plans and resources available to local leaders and health professionals. As for preparedness planning, probably none had yet been made in either The Dalles or Surat (at least we have not found any sign of any plans at these cities being activated to deal with the exigencies of the outbreaks they faced). Of course, these events took place before September 11, 2001, which appears to be a turning point in regards to how community leaders view the need for preparedness planning; before 9/11, preparedness planning usually was limited to making ready for natural events, such as earthquakes, hurricanes, and others; after 9/11 there grew an awareness that communities also needed to plan for the possibility of catastrophes brought about by human actions.[70] Further, after the SARS pandemic in 2003, with additional stimuli provided by the ravages of avian influenza, community leaders have become better aware of the need for preparing for the occurrence of infectious diseases. However, such awareness seems not to have been present in The Dalles or Surat, and barely in Toronto, at the time of the outbreaks discussed here.
Returning to this issue of outbreaks being local events, each of the cases considered here occurred as isolated events; i.e., each outbreak affected a particular city and did not have wider spread.[71] Even so, each city had to quickly marshal its resources and address immediate challenges posed by the outbreak it faced. In particular, quick action was required in the cases of communicable diseases so they would not disperse and thus come to affect many persons. Eventually assistance did arrive to each city from higher levels of governance, but it took some days. The point we would like to make is that if a disease outbreak were to occur in the future that affected several or many communities in a country nearly simultaneously, the ability of higher authorities at the state/provincial and federal levels to assist each one of them would be limited and this limited assistance probably would take some time to arrive.

Third, in none of the cities we consider did officials immediately communicate information about the outbreaks they were experiences in an adequate manner. This did not matter so much in The Dalles, where the outbreak was localized and of relative short duration, and in Toronto the event communication situation improved markedly within a few days, but it could have made a large difference in Surat by preventing panic and the dislocation of the populace. This tells us that preparedness plans should included provisions for communicating event information accurately and in a timely fashion to the populace; in particular, political leaders must be in tune with leaders in the public health and health delivery systems so to make certain that they are all communicating the same messages. This would also help prepare the local health delivery community so its members maintain social responsibility and allow the public health system to institute public health measures, such as quarantine, vaccine campaigns, social distancing, and others without unduly alarming the public.

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[1] City of The Dalles, "City of The Dalles: City History and Geographical Area," City of The Dalles, www.ci.the-dalles.or.us.
[2] Judith Miller, Stephen Engelberg, and William Broad, Germs: Biological Weapons and America's Secret War (New York: Simon & Schuster, 2001), p. 19.
[3] Centers for Disease Control and Prevention Division of Bacterial and Mycotic Diseases: Salmonellosis, Centers for Disease Control and Prevention, www.cdc.gov.
[4] Seth Carus, "The Rajneeshees (1984)," in Jonathan B. Tucker, ed.,Toxic Terror: Assessing Terrorist Use of Chemical and Biological Weapons, (Cambridge, MA: MIT Press, 2000), pp. 130-131.
[5] Judith Miller, Stephen Engelberg, and William Broad, Germs: Biological Weapons and America's Secret War, (New York: Simon & Schuster Ltd., 2001), pp. 19-20.
[6] Ibid., pp. 20-21.
[7] Florida Department of Health, "Case Study: The Dalles Bioterror Event and Response," 2004, Florida's Health, www.doh.state.fl.us.
[8] Carus, p. 131.
[9] Miller, Engelberg, and Broad, pp. 23-24.
[10] Ibid, p. 34.
[11] Ibid.
[12] Ibid, pp. 20-21.
[13] Carus, p. 136.
[14] Miller, Engelberg, and Broad, p. 19.
[15] K.S. Jayaraman, "Indian plague poses enigma to investigators," Nature 371 (October 13, 1994), p. 547.
[16] Laurie Garrett, Betrayal of Trust: The Collapse of Global Public Health (New York: Hyperion, 2000), p. 16.
[17] Ibid.
[18] Robert D. Perry and Jacqueline D. Fetherston, "Yersinia pestis—Etiologic Agent of Plague," Clinical Microbiology Reviews 10(1) (January 1997), pp. 35-66.
[19] Centers for Disease Control and Prevention, "Information on Plague," CDC, www.cdc.gov.
[20] N. S. Deodhar, Vishwanath L. Yemul, and Kalyan Banerjee, "Plague That Never Was: A Review of the Alleged Plague Outbreaks in India in 1994," Journal of Public Health Policy 19 (Issue 2, 1998), pp. 184-199.
[21] K.S. Jayaraman, "Indian plague poses enigma to investigators," Nature 371 (October 1994), p. 547.
[22] K.S. Jayaraman and Declan Butler, "…as doubts over outbreak rumble on," Nature 372 (November 1994), p. 119.
[23] Ibid, p. 26.
[24] Judith B. Tysmans, "Plague in India—1994 Conditions, Containment, Goals," University of North Carolina at Chapel Hill School of Public Health Carolina Papers in International Health and Development Fall 1995, Number 3.
[25] G.C. Cook, "Plague: Past and Future Implications for India," Public Health 109 (January 1995), p. 9.
[26] Garrett, p. 31.
[27] Ibid, p. 33.
[28] Ibid, pp. 30-31.
[29] G. Nandan, "Plague spreads in India but is 'under control,'" British Medical Journal 309 (October 8, 1994), p. 897.
[30] Ibid.
[31] Garrett.
[32] N.S. Deodhar, Vishwanath L. Yemul, and Kalyan Banerjee, "Plague That Never Was: A Review of the Alleged Plague Outbreaks in India in 1994," Journal of Public Health Policy 19 (1998, Issue 2), pp. 185-186.
[33] Krishnan Guruswamy, "Renowned Doctor Flees Hospital With Plague Symptoms," Associated Press, September 28, 1994.
[34] Pratap Chakravarty, "Indian exporters hope to bounce back from plague epidemic," Agence France Presse, October 10, 1994.
[35] Chakravarty.
[36] Garrett, p. 33.
[37] Dileep V. Mavalankar, "Plague in India," Lancet 344 (November 5, 1994), p. 1298.
[38] "Indian stock markets hit by plague threat," Xinhua News Agency, October 3, 1994.
[39] Garrett, p. 33.
[40] Tysmans.
[41] Garrett, p. 43. Figures are in U.S. dollars.
[42] World Health Organization, "Severe acute respiratory syndrome (SARS)," Weekly Epidemiological Record 78(12):81-83 (March 21, 2003).
[43] For a detailed account of the emergence and spread of SARS, see Karl Taro Greenfeld, China Syndrome: The True Story of the 21st Century's First Great Epidemic, (New York: HarperCollins Publishers, 2006).
[44] Philip W.H. Peng, et al., "Infection control and anesthesia: lessons learned from the Toronto SARS outbreak," Canadian Journal of Anesthesia 50(10):989-997 (2003).
[45] Centers for Disease Control and Prevention, "Fact Sheet: Basic Information About SARS," CDC, www.cdc.gov.
[46] Steven Riley, et al., "Transmission Dynamics of the Etiological Agent of SARS in Hong Kong: Impact of Public Health Interventions," Science 300:1961-1966 (June 20, 2003).
[47] GlobalSecurity.org, "Flu transmission," www.globalsecurity.org.
[48] "Toronto International," City of Toronto, www.toronto.ca.
[49] Toronto Urban Development Services: Policy & Research, "Profile Toronto: Population Growth and Aging," January1, 2003, City of Toronto, www.toronto.ca.
[50] Ibid.
[51] Pamela Varley, "Emergency Response System Under Duress: The Public Health Fight to Contain SARS in Toronto (A)," report C16-05-1792.0 of the Case Program, Kennedy School of Government, Harvard University, 2005.
[52] National Advisory Committee on SARS and Public Health, Learning from SARS: Renewal of Public Health in Canada, (Ottawa: Health Canada, October 2003).
[53] Greenfeld, p. 161.
[54] Suburban Emergency Management Project, "SEMP Biot #302: Emergency Departments and Epidemics: The 2003 Toronto SARS Experience," November 27, 2005: www.semp.us.
[55] Tomislav Svoboda, et al., "Public Health Measures to Control the Spread of the Severe Acute Respiratory Syndrome during the Outbreak in Toronto," New England Journal of Medicine 350(23):2352-2361 (June 3, 2004); Philip W.H. Peng, et al., 2003; National Advisory Committee on SARS and Public Health, 2003; and Suburban Emergency Management Project, 2005.
[56] Svoboda, et al., 2003.
[57] Pamela Varley, "Emergency Response System Under Duress: The Public Health Fight to Contain SARS in Toronto. Epilogue," report C16-05-1793.1 of the Case Program, Kennedy School of Government, Harvard University, 2005.
[58] Pamela Varley, "Emergency Response System Under Duress: The Public Health Fight to Contain SARS in Toronto (B)," report C16-05-1793.0 of the Case Program, Kennedy School of Government, Harvard University, 2005.
[59] Learning from SARS: Renewal of Public Health in Canada, National Advisory Committee on SARS and Public Health, October 2003, p. 25.
[60] Tomislav Svoboda, et al., "Public Health Measures to Control the Spread of the Severe Acute Respiratory Syndrome during the Outbreak in Toronto," New England Journal of Medicine, 350 (2004), p. 2355.
[61] Svoboda, et al., 2004.
[62] Learning from SARS: Renewal of Public Health in Canada, p. 27.
[63] KPMG, "Toronto Tourism Revenue Loss Exceeds Quarter of a Billion," July 2, 2003; www.kpmg.ca.
[64] Steven Theobald, "SARS fallout hammers economy," Toronto Star, May 10, 2003, p. A1.
[65] Ibid.
[66] Stefanie Batcho, "Toronto businesses try to address SARS outbreak's economic fallout," Agence France Presse, April 24, 2003.
[67] Jacqueline Thorpe, "SARS to take a bite out of Canadian growth: J.P. Morgan forecast: Economist cuts his second-quarter target in half to 1%," Financial Post, April 23, 2003.
[68] Colin Perkel, "Economic fallout of SARS said worse than Sept. 11; politicians plan recovery," Canadian Press Newswire, April 24, 2003.
[69] Centers for Disease Control and Prevention, "Anthrax," www.cdc.gov.
[70] Surat officials probably were aware of the chemical disaster that befell the city of Bhopal (located about 500 kilometers north-east of Surat) in December 1984, but we have detected no evidence that such an awareness, if any, guided the city's response in 1994.
[71] There were additional cases of SARS in Canada at the time of the Toronto outbreak, particularly in British Columbia, but these were small and thus hardly impacted Canada as a whole.