Introduction

New York City launched two major immunization programs in the twentieth century to control immediate threats to the public health. The first of these was the smallpox immunization program of 1947, which was in response to several cases of the disease [1]. The second, initiated in 1976–1977, was directed at protecting the public against the perceived threat of the swine influenza. Unlike the smallpox grogram, it was not just a local effort, but rather part of a national immunization program. In 1947, 6.35 million people were vaccinated against smallpox in 29 days [1]. However, in 1976–1977, only 639,000 were immunized against swine influenza over a period of 60 days [2]. The population of New York City in those years was relatively stable at 7.5 million in 1940 and 7.8 million in 1970 [3].

The resources deployed in 1976 to achieve the objective of immunizing most of the city’s population against swine influenza were equivalent to those available in 1947. Yet the number of those immunized in 1976 was far fewer, and represented a tenth of those vaccinated against smallpox in 1947. This vast difference in both the absolute number and rates of immunization in 1976 had its roots in several issues including public perceptions of the low threat level of swine flu. Whereas contracting smallpox in 1947 was perceived as a real and frightening possibility within the context of a sudden outbreak, epidemic swine flu was eventually assessed as a remote possibility by an increasingly skeptical public [2].

There were many other issues that influenced the public’s rejection of swine flu vaccination in 1976 as well as unanticipated and unprecedented implementation obstacles. These have all been insightfully and extensively commented on by several writers [2, 4–6].

This review of New York City’s two most important vaccination programs of the twentieth century will hopefully contribute to a better understanding of the issues involved in formulating public health policies and implementing the practical measures that reflect them. These reflections are offered by an author who spent 6 years in West Africa eradicating smallpox, and controlling a number of disease outbreaks and epidemics including cholera, meningococcal meningitis, and yellow fever. In addition, I also served as Chair of the Swine Influenza Immunization Task Force for New York City in 1976 and directed the city’s swine flu vaccination program.

Documentation of the 1947 Smallpox Outbreak in New York City

The most frequently cited source of information about New York City’s 1947 smallpox outbreak is Israel Weinstein’s article published in the American Journal of Public Health [1]. In this article, published soon after the outbreak and the vaccination program to contain it, Weinstein provided summary information about the cases and complications following vaccination [1]. In essence, he minimized vaccination reactions such as post-vaccination encephalitis and generalized vaccinia. A clearer and more accurate account of these complications was provided by Dr. Morris Greenberg, Director of the Bureau of Preventable Diseases of the Department of Health [7, 8]. Greenberg was an eminent epidemiologist and a revered pioneer in the field [9].

Although not as frequently cited, other papers describing the 1947 smallpox outbreak are far more detailed than Weinstein’s general account, and clearly were not fettered by the political considerations that must have impelled him to present as positive a picture as possible [10, 11]. In addition, there have been popular accounts of the 1947 outbreak and the vaccination program [12, 13]. These also provide many interesting details not contained in Weinstein’s account.

Public Health Leadership in a Time of Crisis

At the beginning of the smallpox outbreak in March 1947, Dr. Israel Weinstein had been New York City’s Commissioner of Health for a year. His appointment to the post by Mayor William O’Dwyer had been surrounded by controversy. The mayor, a short time before, eased out Mayor Fiorello LaGuardia’s highly respected Commissioner of Health, Dr. Ernest L. Stebbins. The latter had declared a state of imminent peril during a February tugboat strike that held the significant potential for a fuel shortage. This and other actions on Stebbins’ part in effect shut down some industries in the interests of conserving fuel. O’Dwyer perceived significant political risks in Stebbins’s action and asked him to step down. He left in March 1946 to become Dean of the Johns Hopkins School of Public Health.

Despite the recommendations of a search committee headed by Dr. Thomas Parran, Surgeon General of the US Public Health Service, O’Dwyer appointed Dr. Edward M. Bernecker, who was the Commissioner of the Department of Hospitals. Bernecker was a close friend of Mayor O’Dwyer which probably played a major role in his appointment as Commissioner of Health. However, because he lacked the public health credentials for the position, there was widespread opposition from a variety of groups including the Board of Health and the New York Academy of Medicine [14].

The mayor backed down and appointed Weinstein, who was then the Director of the Bureau of Public Health Education. As Duffy has noted, Weinstein’s appointment “was greeted with a mixture of amusement and mild derision” [14]. He also noted that Weinstein thought that he had been appointed because of the recommendations of newspapermen, and in particular a reporter for The New York Times [14]. Whatever the reasons, Weinstein was not a member of Stebbins’s leadership group. They had a biased, low opinion of him, and did their best to spread their views far and wide. What they may have failed to appreciate is that Weinstein had regular contacts with the press given his role as the Department of Health’s principal spokesperson for routine health education messages. Nonetheless, the general assessment of his health department colleagues was that he had not distinguished himself as a health educator [14]. Added to this was the fact that he had to deal with two formidable women executives in the department, Margaret Barnard, MD, DrPH, who was Director of the Bureau of District Health Administration, and Leona Baumgartner, MD, PhD, who was Director of the Bureau of Maternal and Child Hygiene. Both were highly regarded both within and outside of the department, and Baumgartner later served as Commissioner of Health (1954–1962). However, she so irritated Weinstein with her boundless energy that he moved her office from the floor where he had his in order to put distance between them [14].

Weinstein later irritated Bernecker by suggesting that his hospital physicians should have easily diagnosed the first smallpox case in a more timely manner [14]. In making this criticism, Weinstein was partially correct. Although smallpox had ceased to be a problem in New York City for a generation, there had been one imported case in 1939 that did not give rise to any secondary cases [11]. However, Weinstein was correct in assuming that physicians at the Willard Parker Hospital (1885–1958), where the index case was hospitalized, should have been capable of making the correct initial diagnosis. This hospital was New York City’s premier communicable disease hospital located on East 16th Street and the East River, and its physicians were considered to be experts in infectious diseases. In their defense, however, the index case’s history and clinical presentation proved challenging when it came to making the correct diagnosis.

Weinstein became Commissioner of Health at a time when the Department of Health was considered to be the premier such agency in the United States. His immediate predecessors as commissioner were among the most important public health leaders in the United States. Over the years, they had created a cadre of exceptionally talented professionals in all the domains of public health. Whatever his perceived leadership inadequacies, Weinstein would partially silence his critics by the exceptional leadership he demonstrated in the face of an unexpected outbreak of smallpox. Still, even decades later when this writer occupied the same position, older career employees did not hold Weinstein in high regard. They remembered him more for the chin-up bar he had installed in the doorway to the commissioner’s office for the purpose of performing daily callisthenic exercises. They recalled seeing him dangling in the doorway as he pulled himself up to the bar. Although they remembered the smallpox vaccination campaign of 1947, they did not attribute its success directly to him, but rather to the exceptional leadership of other professionals in the department. It is important to place these recollections in perspective. Long time rank and file employees of the Department of Health tended to remember commissioners more for their unique and sometimes idiosyncratic personality traits than for their achievements. Thus, Weinstein’s successor, Dr. Harry S. Mustard (1947–1948), was remembered for his seemingly inexhaustible repertoire of off-color jokes. His successor, Dr. John Mahoney (1949–1953), was recalled as a pleasant and easygoing man who often whistled or hummed popular music to himself. Leona Baumgartner (1954–1962) was remembered as a powerful and brash presence, while her successor, Dr. George James, was remembered for his informal administrative style and marked limp due to a congenital leg abnormality.

Given all the facts, a poor assessment of Weinstein seems rather harsh. He possessed outstanding educational credentials including an AB from City College, AM, MD, and PhD degrees from Columbia University, and a ScD degree from New York University. During his early years, Weinstein was a high school biology teacher, and then an instructor in physiology at Columbia University’s College of Physicians and Surgeons. He had a long career in the Department of Health beginning in 1914 when he was still a student. A dutiful employee who served in various capacities in the Bureau of Laboratories, he eventually became Director of the Bureau of Health Education. It was while in this position that he was selected to be Commissioner of Health at the age of 53 years. After serving as Commissioner of Health, he returned to his position as Director of the Bureau of Health Education which he eventually left in 1949. He died at the age of 82 years at his home in the Bossert Hotel in Brooklyn, New York on 27 May 1975, and was survived by his brother, Milton Weinstein [15].

The 1947 Smallpox Epidemic

Although the epidemic began with an American businessman who contracted smallpox in Mexico, this fact was only established retrospectively after secondary cases appeared. It was through meticulous epidemiologic investigations directed by Dr. Morris Greenberg that the index case was eventually identified [12]. This proved crucial in terms of tracking down potential contacts and vaccinating them.

The Index Case

The index case was a 47-year-old American merchant who had lived and worked in Mexico for several years. He and his wife embarked on a bus trip from Mexico to New York City on 24 February 1947. Their destination was Maine, where his wife had inherited a farm. En route, he became ill with a headache, rash and a pain in the back of his neck. Because he was feeling ill, they decided to stop in New York City where they arrived on 1 March, after having made several stops en route. In order to relieve his headache, he started on a regimen of several medications [1]. He and his wife stayed at a midtown hotel in Manhattan, did some sightseeing, and shopped in a department store. This history, when it eventually came to light, raised serious concerns about his having transmitted the disease to others, not only in New York City, but also en route from Mexico.

On 5 March, after having been in New York City for 4 days, he felt sufficiently ill to seek medical help at Bellevue Hospital [1, 11]. At Bellevue, he had pustular and hemorrhagic lesions widely distributed over his body [1]. However, a diagnosis of smallpox was not made. On 8 March, he was transferred to the Willard Parker Hospital where the physicians who treated him established a differential diagnosis that included drug eruption, erythema multiforme, Kaposi’s varicellifom eruption, and smallpox [1].

Although smallpox was considered, it was ruled out because of the presence of an old vaccination scar, no known recent history of exposure to smallpox cases, a history of smallpox vaccination the year before (it did not produce a reaction), and the presence of an atypical rash. The rash was partially hemorrhagic, and while this is a known variant of classical smallpox, it is relatively rare. In the end, a diagnosis of toxic drug reaction was made because the patient had taken a number of medications for his headache. This diagnosis seemed to be the most plausible one, especially after a skin biopsy did not demonstrate Guarneri bodies which are found in smallpox cases. The findings on autopsy were non-specific [1].

Despite the fact that smallpox was ruled out as a possible diagnosis, the index case’s wife was given a smallpox vaccination [1]. This would indicate that among the physicians at Willard Parker there must have been some who remained concerned that they were dealing with smallpox.

Secondary Cases

All of the four secondary cases in this outbreak occurred among individuals who had been hospitalized at Willard Parker at the same time as the index case. These included a 27-year-old male who was hospitalized with mumps, and a 22-month-old girl with croup. A 4-year-old male was also in the hospital at the same time as the index case, and was discharged on 10 March to a convalescent home in Millbrook, New York [1, 11].

On 22 March, 10 days after the death of the index case, the 27-year-old male, who had been at Willard Parker at the same time as the index case, developed a rash. He was an employee at Bellevue Hospital, and was admitted to that hospital’s dermatology ward. Five days later, he was transferred to Willard Parker with a diagnosis of chicken pox. On 19 March, the 22-month-old girl, who had also been at Willard Parker when the index case was there, developed a rash and was readmitted with a diagnosis of chicken pox. However, in both cases, the rash was not typical of chicken pox and thus a tentative diagnosis of smallpox was made. This diagnosis was confirmed through laboratory testing at the US Army Medical School Laboratory and at Western Reserve University. Once this diagnosis was made, other sections from the skin biopsy material from the index case were examined and found to be positive for Guarneri bodies [1]. Meanwhile, the 4-year-old boy who had been discharged to a convalescent home came down with a typical smallpox rash [5]. He in turn gave rise to three tertiary cases as listed in Table 1.

Table 1 Twelve cases of smallpox by age, gender, ethnicity, vaccination status, approximate date of onset, and role in transmission, New York City, 1947
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Tertiary Cases

The 4-year-old secondary case, as mentioned above, gave rise to three tertiary cases. The 27-year-old secondary case also gave rise to tertiary cases. These included his 26-year-old wife who died from the disease, despite recent vaccination, and three patients with whom he had contact at Bellevue Hospital [1, 15]. In total, there were seven tertiary cases. The chronology of the outbreak is presented in Table 2.

Table 2 Chronology of the 1947 smallpox outbreak in New York City
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General Characteristics of the Cases

Of the twelve cases, eight (66.7 %) were male and four (33.3 %) female. Five (41.7 %) were white, four (33.3 %) African American, and three (25.0 %) Hispanic. Only two (16.7 %) of the twelve had a previous history of smallpox vaccination, and in both cases this was in the remote past. Two patients (16.7 %) died. One was the index case and the other was the wife of the 27-year-old secondary case. At the time of her death, she was 7 months pregnant [11]. It is probable that her pregnant state contributed to her death (Table 3).

Table 3 The twelve cases of smallpox in the 1947 New York City outbreak
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Epidemiologic Investigation

The chain of transmission in this outbreak was established retroactively to the index case from two secondary cases in whom the diagnosis was definitively made on 5 April. The index case had died on 10 March, approximately a month before [11]. In all, there were four secondary cases, all of whom had contracted smallpox while patients at the Willard Parker Hospital. Dr. Morris Greenberg and his epidemiologists quickly determined that transmission had occurred at the hospital. A thorough review of the hospital’s patient records soon revealed the probable index case, and further studies of his preserved pathologic specimens confirmed the diagnosis of smallpox [11]. Greenberg soon discovered that only two of the secondary cases had been on the same floor as the index case, while the others were on separate floors. There appeared to have been no demonstrable contact between the index case and those on separate floors of the hospital [17].

The immediate task was to vaccinate all who had been in contact with smallpox patients, which was quickly extended to all personnel and patients in the hospital. A list of all guests at the midtown hospital where the index case stayed and all hotel employees was quickly drawn up. The former amounted to 3000 people from 29 nine states. They all had to be tracked down and vaccinated [12]. Weinstein called upon the US Public Health for assistance in tracking down possible contacts in the several cities where the bus carrying the index case had stopped.

Under Greenberg’s direction, contact tracing and contact vaccinations were carried out with amazing speed. The same held true for contact tracing and vaccinations outside of New York City [11]. In vaccinating an increasing number of contacts, the Department of Health was implementing “expanding ring” vaccination, a long established procedure for containing smallpox outbreaks [16].

On 12 April, Weinstein was informed of the secondary case in a young boy who was then in the Cardinal Hayes Convalescent Home in Millbrook, New York. This child had been at the Willard Parker Hospital at the same time as the index case. Later, he was told that the wife of a secondary case of smallpox had just died of the disease, and that ring vaccination of contacts had used up almost all of the city’s supply of some 200,000 plus doses of smallpox vaccine. He and Dr. Bernecker, who had by now mended their fences over the delay in diagnosing smallpox, met with Mayor O’Dwyer and briefed him on the situation.

The 1947 Smallpox Vaccination Program

The confirmation of smallpox through laboratory testing in the 27-year-old secondary case on 4 April actually set into motion plans for a mass vaccination program. The fact that this laboratory confirmation was reported by Dr. Joseph Smadel at the US Army Medical School Laboratory and Dr. Robert F. Parker at Western Reserve University left no doubts that New York City was in the midst of a smallpox outbreak [1]. Meanwhile, the US Public Health Service had carefully investigated the bus route taken by the index case and his wife. They were also able to confirm that there were no secondary cases of smallpox in the cities where the bus stopped. These included Laredo, Dallas, St. Louis, Cincinnati, and Pittsburgh. The index case’s wife, who was in Maine at the time, had been vaccinated and was free of the disease [1].

Given the slowly increasing number of smallpox cases, Weinstein and his colleagues in the Department of Health along with Dr. Edward Bernecker, Commissioner of Hospitals, and his staff, drafted a plan for vaccinating the city’s population. On 4 April, the Department issued a statement to the press and broadcast media urging those who had not received a smallpox vaccination since childhood to be vaccinated [17].

In order to meet the anticipated surge of people requesting vaccination, Weinstein and his colleagues established vaccination clinics at the Department of Health’s 125 Worth Street headquarters, at the 21 district health centers, 60 child health clinics, and 13 municipal hospitals. All of these facilities were open to the public on a twenty-four/seven basis. In addition, clinics were established in the city’s 179 police precincts and in non-municipal hospitals and clinics, where vaccinations were given free of charge. They were also established in other facilities. Teams of physicians and nurses made the rounds of the city’s public and parochial schools where they vaccinated several hundred thousand children (Table 4).

Table 4 Locations for smallpox vaccinations, 5 April–3 May 1947
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The Department of Health relied on a number of voluntary organizations to assist in carrying out this vaccination program. These included not only individual physicians and nurses, but also volunteers from the American Red Cross, the American Women’s Voluntary Services, and former Air Raid Warden groups. The program greatly benefited from the fact that World War II had ended just 2 years before. As a result, there was a strong sense of volunteerism among the general public as well as many who had served with a range of voluntary organizations created during the war.

Weinstein did his best to allay public anxieties about the outbreak. However, the appearance of subsequent cases of smallpox after the start of the vaccination program only served to fuel public fear and increase demands for immediate vaccination. While the Department of Health’s slogan, “Be Sure, Be Safe, Get Vaccinated,” was being widely disseminated, Weinstein and his colleagues were facing a shortage of vaccine to satisfy public demand. This demand for vaccination only intensified after 13 April when the death of a second victim was made public [18]. At this point, Mayor William O’Dwyer’s concerns rose, and in a show of personal example, he was publicly vaccinated by Dr. Weinstein. However, 3 days later, the city had to halt vaccinations because the supply of vaccine was exhausted [19].

Vaccine supplies had been an issue from the outset of the program. The city had 250,000 doses available for immediate distribution through the Department of Health’s Bureau of Laboratories. In addition, there were another 400,000 doses, but in bulk form that had to be transferred into 50-dose vials. The US Army and Navy provided on loan another 800,000 doses requisitioned from various parts of the country. Yet, these additional doses were clearly inadequate to vaccinate some 7.0 million people. As it was, some 600,000 doses had been distributed during the first week of the vaccination program.

O’Dwyer called an emergency meeting at City Hall with representatives of the manufacturers of smallpox vaccine. Weinstein and Bernecker were also present at the meeting along with their key staff members. At O’Dwyer’s urging, the manufacturers agreed to alleviate the problem by diverting supplies to the city from other parts of the country and by packaging their bulk vaccine. As a result, in a few days, sufficient vaccine was arriving in the city. In fact, a million doses became available on 17 April, and half of it was quickly used [20]. O’Dwyer was not only successful in obtaining the required doses of smallpox vaccine, but also provided $500,000 to support the vaccination program and cover the added costs of the epidemiologic investigations that had preceded it.

In order to more efficiently distribute the vaccine to private physicians, the Department of Health enlisted the assistance of retail pharmacists [1]. While this phase of the program was very successful, the department’s efforts to recruit physicians to administer the vaccine produced poor results. In part, this was due to the very modest stipend that the Department of Health was able to pay volunteer physicians.

The smallpox vaccination effort was officially terminated on 3 May 1947. Weinstein reported that 6,350,000 people had been vaccinated, five million within the 2-week period following the Mayor’s 13 April appeal that everyone get vaccinated [1]. By any measure, the vaccination program was highly successful not only in terms of the number of people vaccinated, but also because the transmission of smallpox was halted.

Complications of Vaccination

In his account of the smallpox outbreak and vaccination program, Weinstein correctly noted that given the scope of the latter, many would assume that a variety of illnesses and even deaths were due to it [1]. He specifically addressed the issues of post-vaccination encephalitis and generalized vaccinia. Concerning post-vaccinal encephalitis, Weinstein reported that a probable diagnosis was entertained in 46 cases. Eight of the 46 died. However, characteristic lesions of post-vaccinal encephalitis were not found in any of them [1]. Rather, two died from tuberculous meningitis, one from a brain tumor, one from coronary sclerosis, and four from cerebral lesions. Weinstein did not elaborate about the last named lesions [1]. In addition, he did not report that an adult male died as a result of septicemia that followed infection of the vaccination site, and that two infants, who had eczema, developed generalized vaccinia as a result of contact with persons who had been recently vaccinated [1].

A year following the vaccination program, Morris Greenberg, who was Director of the Bureau of Preventable Diseases of the Department of Health, and Emanuel Appelbaum, Chief of the Division of Acute Infections of the Central Nervous System, reviewed 49 possible cases of post-vaccinal encephalitis [7]. Four of these cases did not meet the criteria for post-vaccinal encephalitis, and were immediately ruled out. Of the remaining 45, four died, but in no instance was there pathological evidence of post-vaccinal encephalitis. Of the 41 who survived, one could not be located, one was left with a residual hemiparesis, and one had an optic neuritis. The remaining 38 recovered [7]. Greenberg and Applebaum concluded that there was no evidence in the brains of the four who died of post-vaccinal encephalitis. However, among the remaining 41, they left open the possibility that they had post-vaccinal encephalitis giving an attack rate of 1/100,000 vaccinations [7]. The slight difference of one case between their study and Weinstein’s report could be explained on the basis of the time frames examined. Whether these 40 plus patients suffered from post-vaccinal encephalitis or not remains an open question.

While Weinstein reported only two cases of generalized vaccinia, and those in unvaccinated infants with eczema, Greenberg reported a total of 45 cases [1, 8]. Of these, 38 (84 %) had eczema. Among these 38, 10 were vaccinated, 27 were not vaccinated but had contact with someone who was, and one was not vaccinated and had no known contact with a vaccinated person. Seven individuals without eczema developed generalized vaccinia. Most of the 45 cases occurred among children under 5 years of age. However, there was a case in an 82-year-old male [8]. Greenberg reported that two infants who were not vaccinated died from generalized vaccinia [8].

Greenberg’s data for vaccination complications was largely based on a sample of 25,925 vaccinated people who returned to the Department of Health to have their vaccination sites read [8]. Thus, it is possible that his data may have been an underestimation of non-reportable complications. That said, however, Greenberg left no stone unturned and reported no case of tetanus due to vaccination, no increase in congenital defects among women vaccinated in the first 4 months of pregnancy, but a 9 % false-positive test for syphilis among 133 non-syphilitic subjects [8, 21].

Following the 9 November 2001 terrorist attacks, there was increased concern about possible future bioterrorist attacks. This concern focused on agents such as smallpox and anthrax. In 2002, President George W. Bush moved to build up the stores of smallpox vaccine in the US, and routine smallpox vaccinations were administered to military personnel and some civilians as well. At that time, there were fears that archived smallpox virus samples stored in the former Soviet Union could fall into the hands of terrorists.

From December 2002 to April 2003, 29,584 American civilians and 365,000 military personnel were vaccinated against smallpox. By late March, three fatal and four non-fatal acute myocardial infarctions were reported among these groups of vaccinated individuals [22]. Thorpe et al. [23] undertook to study whether or not such deaths occurred during the 1947 smallpox vaccination program in New York City in order to clarify whether or not the 2003 deaths were vaccine-associated or coincidental. In a meticulously designed study, the authors examined death certificates for 1946, 1947, and 1948 (N = 81,529). They then calculated adjusted relational death rates for the post-vaccination period, and found no increases in cardiac deaths. While reassuring, the results of this study also pointed out the value of the 1947 New York City smallpox vaccination program to contemporary and future epidemiologic research.

An Assessment of the 1947 Smallpox Vaccination Program

An enduring question has long been whether or not vaccination of most of the city’s population was really necessary in order to arrest the transmission of smallpox. Although the Department of Health’s official figure for the total number of people vaccinated was 6.35 million, Greenberg, the city’s chief epidemiologist, placed the actual number at 5.0 million [7]. More recently, based on data reported by The New York Times during the 1947 vaccination program, Sepkowitz found that, “The claim of 5 or 6 million vaccinations administered cannot be reconciled against the daily tally reported by the Times” [24]. He makes a cogent observation in noting that if the daily numbers reported by The New York Times were approximately accurate, then 2.5 million people were vaccinated. Sepkowitz accepts that the official number might be accurate, and notes that the discrepancy might “be a case of not adding columns of numbers in a systematic way” [24]. What also may have occurred is that the daily numbers provided to the press may have been undercounts given that the communication of vaccination data to the central office of the Department of Health could have been initially incomplete. The final numbers from so many different vaccination sites could have taken days to arrive at the central office.

Even if far fewer than the claimed 6.35 million vaccinations had been given, the question remains whether or not even a million or 2.5 million vaccinations were really necessary. This issue received greater scrutiny in the post-2001 terrorist attack era because of concerns about possible bioterrorism using archived smallpox viruses stored in the former Soviet Union. One aspect of this issue was a need to estimate national vaccine requirements if there were a bioterrorist attack with smallpox virus.

Glasser et al. published models in 2005 which demonstrate that the key to containing smallpox outbreaks is patient isolation, vaccinating contacts, and monitoring those vaccinated too late to ensure protection [25]. They also conclude that the pre-emptive vaccination of health care personnel in hospitals and varying proportions of the population, and school closures add little to outbreak control. They view surveillance and containment as the cornerstones of outbreak control [25].

From one perspective, part of this strategy is based on “expanding ring vaccination” which was employed for many decades to contain smallpox outbreaks [16]. Based on the models of Glasser et al. and also on empirical experiences combatting smallpox outbreaks, it is clear, as this writer has noted that: “outbreak investigations, increased surveillance, and targeted vaccinations resulted in a quick interruption of transmission that mass immunizations could not have achieved” [26].

New York City initially employed the above methods. However, limiting the containment of a smallpox outbreak to these methods alone would have been politically untenable for both Mayor O’Dwyer and Commissioner Weinstein. Although smallpox had not been present in New York City for 8 years, the collective public image and memory of it were still vivid [27]. It is a certainty that the public as well as the media of that time would have demanded access to vaccination. Thus, O’Dwyer and his administration had no choice but to also implement a mass vaccination program.

The 1976 Swine Flu Vaccination Program

In February 1976, an outbreak of influenza occurred at Fort Dix, then a US Army training center in New Jersey. While most of the isolates proved to be the prevailing influenza virus, A/Victoria/75 (H3N2), several were identified as swine flu, A/New Jersey/76 HswN1, then believed to be similar to the 1918 pandemic virus which is estimated to have killed some twenty million people worldwide [4]. Since none of the affected Army recruits had a history of contact with swine, it was reasonably concluded that human-to-human transmission had occurred [4].

Fear that the cases in New Jersey represented a reappearance of a 1918-like pandemic drove the public health policy to vaccinate the entire population of the US. However, there were other concerns that influenced this decision. Among these was the fact that since persons under 50 years of age possessed no antibodies to this strain, there was sufficient time to produce a vaccine that would be ready for the influenza season in the fall of 1976, and the fact that the influenza vaccine annually used by the military contained an H1N1 component [6]. As it turned out, later evidence was found that demonstrated that this HswN1 had long been circulating in the US population, and that it either produced inapparent or mild clinical illness. It was not until almost 30 years later that the 1918 virus was reconstructed and demonstrated to be a uniquely virulent form of an avian influenza virus [28, 29]. However, this evidence was not available to those public health and scientific leaders who, based on what they then knew, advised the Secretary of Health, Education, and Welfare to launch a national immunization program against the swine flu [4].

This decision was later sharply criticized by Neustadt and Fineberg in a monograph commissioned by Joseph A. Califano, Jr., then Secretary of Health, Education, and Welfare [6]. More recently, Fineberg repeated some of these criticisms when the specter of a pandemic of avian influenza loomed [5]. The lessons pointed out in both publications included “over-confidence in theory spun from meager evidence, conviction fueled by pre-existing agendas, zeal by health officials to make lay superiors ‘do the right things,’ premature commitment, failure to address uncertainties, insufficient questioning of implementation prospects, and insensitivity to media relations and to long-term credibility” [5]. Despite misgivings by many, the program was launched on 24 March 1976 by President Gerald Ford, and funded at a level of $137 million. Its goal was to immunize every man, woman, and child in the US, and thus was the largest and most ambitious national immunization program ever undertaken in the United States [2].

Decision Making Within the New York City Department of Health

State and local health departments were not under a mandate to participate in the program. At the time the national program was announced, there had been no further documented cases of swine flu in the month following the cases at Fort Dix, New Jersey. This fact, plus some thin evidence that swine flu viruses might be regularly circulating in the population, raised reservations about the potential of this virus causing a pandemic. At the time, Lowell E. Bellin, MD, MPH (2 October 1928–14 July 1997) was Commissioner of Health. An eminent public health leader and health care administrator, he had accepted Mayor Abraham D. Beame’s offer of the health commissionership in late 1973, and assumed the office on 1 January 1974. Prior to accepting the position, he had been Professor of Health Care Administration at Columbia University, School of Public Health. However, Bellin had extensive previous public health practice experience as Commissioner of Health of Springfield, Massachusetts, and later as Executive Director of New York City’s Medicaid Program, and First Deputy Commissioner of Health in the New York City Department of Health [30, 31].

Discussions among the department’s leadership in early April 1976 made clear doubts about the necessity for the vaccination program based on the weak scientific facts. This writer, then the First Deputy Commissioner and former Director of the Bureau of Infectious Disease Control, was especially skeptical. This skepticism was based on 2 years’ experience establishing a sophisticated influenza surveillance system in New York City. In discussions with Mayor Beame, it was clear that he was not enthusiastic about the swine flu vaccination program. However, Bellin concluded that the New York City Department of Health, whatever the misgivings of its scientific and public health leaders, had no choice but to participate in it. He said, “There are about half a million people in this city out of the eight million who will demand access to swine flu vaccination. Denying them access will place us in an untenable situation.” Bellin’s projection was accurate given that only 639,144 people in the city were eventually vaccinated [2].

Organizing the Swine Flu Vaccination Program for New York City

Unlike the smallpox vaccination program of 1947, the 1976 swine flu vaccination program of 1976 was part of a national effort. Consequently, it was vulnerable to a number of external forces and events. Given its size and scope, it is not surprising that a range of problems soon arose including delays in vaccine production to malpractice insurance challenges. Added to its magnitude and complexity, was its controversial nature. Critics and supporters eventually emerged on the basis of the validity of the scientific evidence [32–34].

The federal government defined broad guidelines for the program, but left the organization, planning, and administration of the program to individual state and local health departments. Federal guidelines required a coordinating committee, participation by the private medical sector, utilization of volunteers, public health education and public awareness programs, training of personnel in cardiopulmonary resuscitation and the use of automatic jet injectors, assessment of vaccine utilization, obtaining a signed informed consent for all those to be immunized, and surveillance for the disease and for reactions to the vaccine.

The organization of this program for New York City was discussed intensively within the executive level of the Department of Health in early April. As a result, the Commissioner of Health made the following recommendations to Mayor Abraham D. Beame: Establish a New York City Swine Influenza Immunization Task Force to include representatives from industry and commerce, the voluntary, proprietary, and municipal hospital systems, the private medical sector, academic medicine, the American Red Cross, and other volunteer groups and specialists from within the Department of Health. The Commissioner also established a special swine influenza immunization unit within the Department of Health to administer the program.

On 4 April 1976, the mayor announced formation of the task force, and appointed this writer, then the First Deputy Health Commissioner, as chair. The task force had 25 members, about half of whom were professional staff of the Department of Health. The directors of bureaus whose staffs would be involved in the program were appointed to the task force, including the directors of public health nursing, child health, school health, laboratories, preventable diseases, district health services, the immunization program, and public health education.

The task force met a week after its formation to formulate general policies and directions for the program. At that time, there were still many ambiguities at the national level concerning the starting date, vaccine availability, target population, and malpractice insurance. The task force decided on a policy of immediate and detailed planning and organization of a program for the entire population so that, being fully prepared to do the maximum, the city could do less if necessary. Health Department members of the task force formed an internal committee to implement the program, and approved of the following general guidelines: The full participation in the program by private physicians and other health care providers, the utilization of volunteers and other community resources, coordination of the influenza program with ongoing immunization activities, professional education and public awareness activities, a training program for staff and volunteers, the establishment of a vaccine storage, supply and delivery system, programs for high-risk groups and the rest of the population, the continuous assessment of vaccine utilization, surveillance for disease and vaccine reactions, and the use of signed informed consent forms.

Progress of Program Planning and Organization

The national program was initially scheduled to begin in July, but in mid-June, the four pharmaceutical firms producing the vaccine announced that they were losing malpractice liability insurance, and stopped making the vaccine. The Department of Health, Education and Welfare then asked Congress to indemnify the vaccine producers, a request later denied by the House Subcommittee on Health. The malpractice issue was not resolved until late August, when Congress finally passed legislation indemnifying all the vaccine producers and program participants from malpractice suits. Irresolution of this issue for 2 months, and the production of six million doses of vaccine by one manufacturer from the wrong virus strain, further delayed the program’s beginning until 12 October 1976.

It was in this atmosphere of uncertainty that the program had to be planned between April and August. On 21 June 1976, the Public Health Service announced the results of vaccine field trials. Recommendations were made for vaccine use in the high-risk population and in the remainder of the population older than 18 years. Essentially, the recommendations were as follows: Bivalent vaccine containing killed A/Victoria/75 and A/New Jersey/Swine/76 was to be given to all individuals above 65 years of age and all individuals of any age suffering from any of the following chronic medical conditions: diabetes mellitus, chronic broncho-pulmonary disease, congenital, rheumatic, coronary or hypertensive heart disease, chronic renal disease, and other chronic metabolic diseases; and the monovalent vaccine containing A/New Jersey/Swine/76 was to be given to all individuals 18 years and older not at high risk.

The New York City program included several essential elements. Ninety new personnel, all university graduates, were hired and trained to use automatic jet injectors and to give cardiopulmonary resuscitation. Seventy-five sanitary inspectors and 150 public health nursing assistants were given similar training. Five hundred to 600 volunteers each day were recruited through the New York chapter of the American Red Cross. Forty-five swine influenza immunization clinics were established throughout the city, 20 in Department of Health facilities, and 25 in the outpatient departments of hospitals. All these clinics were staffed by Department of Health personnel, using automatic jet injectors. Fifteen mobile teams, using automatic jet injectors were established to inoculate 47,000 people in more than 200 nursing homes and about 100,000 people in 150 senior citizen centers. Vaccine was made available to private physicians in quantities of 100 doses of both types at a time and a cumulative total of 600 doses. Vaccine was made available to large group medical practices in quantities of 1000 doses per request, with a cumulative total of 5000 doses. Requests above these quantities had to receive special approval.

The department’s 60 teams consisted of six people including two vaccinators, a clinic supervisor, and three clerical and support personnel. Malpractice coverage was provided for all participants. A participant was defined in the federal legislation as any person, clinic or facility, public or private, who administered the vaccine free of charge. The vaccine in all instances had to be given free. Private physicians could charge an administrative fee if they so wished, but by doing so lost medical malpractice coverage. All participants had to sign an informed consent to be retained for 3 years. All vaccine recipients received an information sheet informing them of the advantages and risks of vaccination and possible side reactions. Telephone numbers were provided in each of the five boroughs for people to call in the event of severe reactions. All participants had to send in a tally by age of immunizations given to be forwarded daily and weekly to the Centers for Disease Control (CDC). Because the vaccine was free at facilities operated by the Department of Health, Medicaid and Medicare providers could not charge for it, but were eligible to give the vaccine to their patients if they did so free of charge. All forms were printed in Chinese, Japanese, Italian, Yiddish, French, Spanish, and Greek. An extensive public health education program was undertaken using radio, television, and local newspapers.

Cost of the Program

The federal government allocated New York City 10 million doses of vaccine to immunize the entire population, but only those who were 18 years and older were immunized. In New York City, this population, projected from the 1970 census, was 5,926,059. However, the city received about 4 million doses of vaccine, enough to reach less than 70 % of this population. The vaccine cost was 52 cents per dose, amounting to $2,080,000. Eighty jet injectors cost $78, 800, supplies cost $150, 000, and personnel costs (90 people) were $890,167. Table 5 shows that federal funds came to $3,446,984 for immunizing the population over 18 years. Had the entire population been immunized, additional vaccine costs would have brought the total to $6,606,984.

Table 5 Resources allocated to the 1976 swine influenza immunization program
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Table 5 also shows the direct costs to the Department of Health, most of it personnel costs. Ongoing programs had to be curtailed or suspended to conduct the program, and 225 people were assigned to it full time. Some 500 more gave varying periods of time to the program, at a cost of $300,000 included in the last item under other indirect costs.

The department’s steering committee included three individuals who had worked in West Africa directing a mass immunization campaign against smallpox, measles, cholera, and yellow fever. They were a great asset. The American Red Cross recruited thousands of volunteers, and maintained a Swine Flu Hotline telephone service for the general public, which contributed enormously to the success of the program. Without their assistance, the Department of Health could not have delivered the program. The presence of 20 individuals in the department’s immunization program, who were knowledgeable in the use and repair of automatic jet injectors, was an important asset because they trained many others to use jet injectors capable of delivering 1000 immunizations per hour.

The necessity of having each person vaccinated read a detailed informed consent form greatly curtailed the speed with which vaccinations could be delivered, but the greatest problems confronting the program were those that shaped public attitudes and made people refuse to be immunized. The program was plagued by problems from its inception in March 1976. Table 6 lists the chronology of major events affecting the program prior to its operational phase, which began in October 1976.

Table 6 Events affecting the swine influenza immunization program in New York City prior to its commencement
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Program Operations

The New York City program began on 12 October 1976. The ceremonial opening of the program was held at 9:00 a.m. that morning at one of the department’s 60 immunization stations. Mayor Beame, who had always been skeptical of the pandemic threat of swine flu and the necessity for the immunization program, declined to be publicly vaccinated. Instead, this writer, as Chair of the Swine Influenza Immunization Task Force, was immunized before the press and media. Turnout at all 60 stations was excellent that morning, but during the opening ceremonies, at which most of the New York City radio and television stations and newspapers were represented, the Associated Press and United Press International reported that three people were said to have died in Pittsburgh, PA following swine influenza immunizations.

Because New York City is a world media center, the local swine influenza program received intense scrutiny. By midday, several state health departments had suspended their immunization programs. However, the decision of the New York City Department of Health was to continue the program. After an emergency meeting at midday, the staff of the Department of Health recommended continuing the program, even though the lot of bivalent vaccine being used was that alleged to have caused deaths in Pennsylvania. The department’s staff could see no causal relation between three cardiac deaths in Pennsylvania and the swine influenza vaccine.

Rubin summarized press coverage of the swine flu program, and said the following of the October crisis, “Many reporters complained about the CDC’s level of cooperation during the October crisis. They realized that phones were ringing off the hook, but, when calls did get through, reporters said they were treated in a haughty manner” [35]. No comments were made by the Center on the issue until late in the day. By this time, the hysteria which began at midday had mushroomed. Television, radio, and newspapers were reporting on the alleged mounting death toll. By the time the CDC came out with a statement, radio and television had been broadcasting the story for close to 5 h, and copy had been set for the next day’s newspapers. Headlines in New York City newspapers the following day included: “The Scene at The Death Clinic” and “Death Toll Mounting.”

Other adverse events during October lessened public confidence in the vaccine. On 23 October 1976, recommendations were made to immunize the 3–18-year-old age group. The recommendation of two inoculations 4 weeks apart was impractical, given the already complex bureaucratic processes and paperwork surrounding each inoculation. National advisory bodies making this decision decided that split virus monovalent vaccine was to be used in healthy youngsters three to 18 years of age, and whole virus monovalent vaccine in those 18–24 years. Whole virus bivalent vaccine was used in those over 65 years and high-risk individuals 25–65, but split virus bivalent vaccine was recommended for high-risk individuals 3–18 years. In effect, then, the program was being asked to administer four vaccines to different age groups, two of which required a booster after 4 weeks. Logistically, it was virtually impossible to implement so complex a protocol in a mass immunization program designed for millions within 8 weeks, and already weighted down by inordinate bureaucratic red tape.

In November 1976, the New York City Department of Health convened an Ad Hoc Expert Advisory Committee to advise the task force on swine influenza immunizations for children three to 18 years. This committee of ten consisted of the directors of pediatric services at the city’s leading university hospitals. In view of the poor antibody responses, the significant level of side reactions, and the fact that the flu season was already well underway with no swine flu in sight, this committee recommended that healthy children in this age group not be immunized unless an epidemic occurred. This became the policy of the New York City Department of Health. It sharply diverged from that recommended by the CDC (Table 7).

Table 7 Events affecting the outcome of the swine influenza immunization program in New York City after its commencement
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The threat of swine flu was increasingly seen as being very remote. By mid-November, less than 5 % of the New York City target population had been immunized. Widespread availability of the vaccine and the convenient location of the department’s 60 clinics, many of which saw few people each day, indicated that most did not wish to be immunized.

To obtain more precise data on public attitudes toward the program, a 1-week interview survey was conducted in two distinct areas of the city to assess the attitudes of middle-class commuters and those living in disadvantaged urban communities. In order to ascertain attitudes among the former, interviews were conducted on Wall Street and in Grand Central Station. To solicit attitudes among African American and Hispanic populations, interviews were conducted in the Bedford-Stuyvesant area of Brooklyn. Of the 436 people interviewed, only 70 (16.1 %) said they had received swine flu shots; 233 (53.4 %) had not and did not intend to. Of these, 51.5 % thought the inoculation was unnecessary, 33.5 % were afraid to get it, 12.8 % had been advised by their physicians not to get it, and 2.2 % had no reason (Table 8).

Table 8 Attitudes toward swine influenza immunizations, New York City, November, 1976
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Table 8 shows that most middle-class commuters did not consider swine influenza immunizations necessary. Only a minority were afraid to get it. Among those in Bedford-Stuyvesant, fears of the vaccine were considerably greater, but most thought immunization unnecessary.

On 27 November 1976, the CDC, concerned by poor turnout across the nation, especially in the larger cities, stated that programs in large cities were failing to reach African American and other minority populations. This statement erroneously presumed that African American and other minority populations wanted immunization. The New York City Department of Health swiftly cited the results of its surveys, and pointed out that of all the populations in the city, the disadvantaged had the best access to the swine flu clinics because the department’s health centers were all built in the 1930s and 1940s in areas which had subsequently become disadvantaged. Most of the department’s swine flu clinics were located in these centers.

Shortly after the department’s surveys, one was undertaken by The New York News, one of the city’s two leading newspapers. Among 504 people interviewed, results were similar to those obtained by the Department of Health survey. Clearly most people did not intend to be immunized.

On 14 December 1976, the CDC reported a number of cases of Guillain-Barré paralysis among individuals after receiving swine influenza immunizations. On 16 December 1976, the program was suspended throughout the United States. The Guillain-Barré syndrome is known to occur after immunizations and a certain incidence was expected after swine influenza immunizations. Because of intense surveillance of vaccines for all kinds of side reactions and the litigious atmosphere surrounding the swine flu program, these cases surfaced very quickly. At the time the program was suspended, 40 million (17 %) of the national target population had been immunized.

On 15 January 1977, the Public Health Service Expert Advisory Committee on Immunization Practices recommended partial resumption of the program for the high risk population. In New York City, the Department of Health again made the vaccine available to private physicians, clinics, and hospitals, and opened an immunization clinic in each of the city’s five boroughs. No other elements of the program were reinstated. Less than half a dozen people showed up daily at each of the five clinics.

Table 9 presents the results of the swine influenza immunization program in New York City. A total of 639,144 doses were actually administered. There were 2357 untoward reactions, making for a rate of 3.7 per 1000. A total of 2,197,130 doses of vaccine were distributed to the three principal groups of providers, but only slightly more than a quarter of these were actually administered. These results were far below the targets established at the inception of the program, but reflected the public’s perception of little need for immunization. Table 9 presents the immunizations by age group and type of vaccine administered. Most immunizations were given in the 25–44 and 45–64-year age groups.

Table 9 Swine influenza immunizations by age group, New York City, 1976
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Discussion

This article discusses the two largest immunization programs undertaken in New York City in the twentieth century. The first of these was the smallpox vaccination program of 1947, and the second the swine flu immunization program of 1976. The different issues that challenged these programs are presented in Table 10.

Table 10 Comparisons between the 1947 smallpox and the 1976 swine influenza immunization programs in New York City
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The 1947 smallpox vaccination program was a local one that was launched to control an outbreak in which two deaths occurred. By contrast, the 1976 program was national in nature and directed to protect people from a disease that few saw as a threat, and no cases of which were ever documented in the city. Despite the adjusted equivalent expenditures, the 1976 program resulted in the vaccination of only a tenth of those who were vaccinated in 1947.

It is clear from the 1976 experience that public compliance with mass immunization efforts are strongly determined by threat perceptions and the risks associated with the vaccines administered. While in 1947 New Yorkers were very fearful of smallpox and comfortable being vaccinated, in 1976, they were fearful of the risks associated with the vaccine and confident that swine flu posed no threat.

Although the press and media extensively covered both programs, that for the swine flu was more intense and extensive. This was a result of vastly changed communication networks during the previous three decades, the national scope of the 1976 vaccination program, and the numerous challenges that arose both before and after it began. Rubin and Hendy extensively studied the media coverage of the swine flu vaccination program [36]. Their study of 19 daily newspapers, the three television networks, and wire services found that the best reporting was done by science and medical writers associated with leading metropolitan newspapers. They euphemistically state that, “Television newsmen and wire reporters were unprepared for a story of such complexity” [36]. In other words, these news outlets were far less competent in reporting events, and often engaged in disseminating inaccurate information. They also conclude that press coverage of the swine flu program was often superficial and characterized by a “body count” mentality [36]. They state that the coverage was rarely inaccurate or sensational, and that the press relations effort by the CDC and other public health agencies “contributed to the public’s confusion and upset professionals in the press” [36].

The issues confronting New York City in both 1947 and 1976 required the rapid planning, organizing, and implementation of enormous and complex immunization efforts. In both cases, the New York City Department of Health demonstrated that it was capable of such efforts in a very complex urban environment.