Tuberculosis and the Health Care Worker: A Historical Perspective

1 January 1994 | Volume 120 Issue 1 | Pages 71-79

Many hospital outbreaks of tuberculosis have occurred in recent years in the United States, resulting in tuberculosis infection and disease among health care workers and patients.Several hospital workers have died of nosocomially acquired multidrug-resistant tuberculosis. Assuring the safety of the health care worker with respect to tuberculosis has become an urgent priority. A review of the medical literature of the past 100 years reveals that our current view of tuberculosis care as an occupational hazard emerged only in the 1950s, after a fierce and extensive debate. Many authorities had felt that care of the tuberculous patient conferred a health advantage to the care provider. This paper reviews this debate and considers steps taken decades ago, before our current environmental interventions were available to ensure the safety of the health care worker.

After decades of fading from public view, tuberculosis is once again a major public health problem [1-3]. The annual number of cases has increased since 1988, reversing a long-established downward trend [4]. Patients co-infected with tuberculosis and human immunodeficiency virus (HIV) progress to active tuberculosis at startlingly high rates [5, 6]; multidrug-resistant tuberculosis has become a pervasive threat in some areas, accounting for 14% to 19% of cases in New York City [7, 8]; and nosocomial outbreaks of tuberculosis affecting both patients and health care workers have occurred at numerous facilities [9-21]. Several health care workers have recently died of tuberculosis and many others have developed active tuberculosis that is identical, by susceptibility profile or restriction-fragment-length polymorphism analysis, or both, to the outbreak strain from their hospital [4, 18, 19].

Much national attention has been focused on the risk of this epidemic to the public and to health care workers. Although drug-susceptible tuberculosis is now readily curable, the demoralizing effect of developing an occupationally acquired illness, as well as the spectre of multidrug-resistant tuberculosis, makes control of this problem an urgent priority. The Centers for Disease Control and Prevention has issued guidelines for the control of tuberculosis [22, 23]. Some recommendations include use of high-efficiency particulate air (HEPA) filtration, germicidal ultraviolet light irradiation, and particulate respirators, as well as placement of patients with suspected tuberculosis into rooms with negative-pressure ventilation [22].

Concern about the threat of tuberculosis to health care workers is long-standing. A review of the medical literature, however, is surprising. Our certainty that care of patients with tuberculosis represents a risk to the health care worker was only established relatively recently. Many articles have refuted the notion, with some even suggesting that caring for patients with tuberculosis conferred an advantage to the health care worker. Tuberculosis sanatoria, in fact, were considered by many experts to be the "safest place one can be" [24] with regard to tuberculosis. In the last major review of the subject, in 1950, Connolly noted that, despite the "extremely high infection rates (that) prevail among medical students and nurses. (i)t is difficult to attribute higher tuberculosis morbidity rates to hospital personnel than to the general population of comparable age" [25].

Our current concept—that a risk does indeed exist—evolved from a fiercely contested debate that lasted more than 50 years. I review the arguments made by both sides and consider the studies used to support the various claims. I also recount some of the steps taken before such devices as particulate respirators, ultraviolet light, and negative-pressure ventilation became available to protect the hospital worker.

Early History

Credit for first recognizing the contagious nature of tuberculosis is usually given to Aristotle. He observed that "in approaching the consumptive one breathes (his) pernicious air. One takes the disease because there is in this air something disease-producing" [26, 27]. Such a suspicion was not unique to the Greeks; Herodotus noted that among the Persians, isolation of persons with leprosy or scrofula was common [26].

The main recorded scourge that dominated the next many centuries was not tuberculosis but the plague. During this time, the rudiments of infection control—wearing protective clothing when around contagious persons and burning corpses—were established. The notion that tuberculosis represented a public health threat emerged slowly. In 1699, the Italian Republic of Lucca issued a decree of "legislative prophylaxis" [26] that required destruction of "objects remaining after the death of a person" with tuberculosis and mandated that doctors notify the authorities whenever they treated a person with consumption. Lists of all patients with tuberculosis were published, and doctors were compelled to perform autopsies on all fatal cases.

The requirement to perform autopsies would not have suited the great Italian pathologist Valsalva (1666-1723), who is said to have avoided doing autopsies on patients with consumption for fear of catching the disease [26]. His pupil, Morgagni, similarly avoided autopsies of those with tuberculosis, although he took a slightly higher ground, claiming it was to protect the health of the young students who worked with him [26].

No such fear darkened the heart of the great French physician Laennec (1789-1826), at least initially. He bluntly claimed that "phthisis is contagious in the opinion of a few laymen and a few physicians in the South" [26]; yet later, when he himself developed the disease, he was convinced that he had acquired it by doing autopsies [28].

Initial Studies: What Risk?

In 1882, Williams, of the Brompton Hospital for Consumption in London, reported an influential study on health care workers and tuberculosis [29]. He noted that of hundreds of workers at Brompton who had cared for thousands of consumptives, none had developed tuberculosis. The results were so compelling that he questioned whether tuberculosis was even contagious. "The north of Europe" held, as he did, that tuberculosis was noncontagious, whereas "the south (held) its contagiousness" [29]. Clapp, of Boston, Massachusetts, agreed with the views of the south and contagion [30].

Williams updated and reconfirmed his study in 1909 [31]. His findings were persuasive [32, 33] and entered the standard texts of the day: "Although the Brompton Hospital has treated more than 15 000 cases of tuberculosis during the past 20 years, neither a nurse, a physician, nor an attendant has become infected" [34]. "No instance of infection has ever been reported from any modern hospital with even elementary precautions about the expectoration" [35].

Fishberg [36] and Dublin [37] summarized numerous additional European studies of more than 18 000 sanitorium workers [37-40] and further advanced the view that care of tuberculous patients involved no risk. Stories of doctors who contracted tuberculosis from patients were, according to Fishberg, "fairy tales" [41]. The many studies reflected the opinion "widely held in the medical world" at the time that tuberculosis work "involves no special hazards among those who engage in it" [37].

This view did not soon fade. A standard pulmonary text of the 1920s brashly stated: "There is no danger from the expired air of consumptives. For this reason a tuberculosis sanitorium is probably the safest place one can be so far as the danger of infection is concerned" [24]. In 1930, Baldwin, Director of the Trudeau Foundation, called the perceived danger of working among tuberculous patients "phthisiophobia" and dismissed precautions such as wearing masks as "extreme," noting that "no case of pulmonary tuberculosis has been known to develop among hundreds of healthy employees at the Trudeau Sanitorium during 45 years" [42]. Fishberg, in his 1932 text on tuberculosis, even claimed that it was not dangerous for "healthy adults to be coughed at by patients suffering from pulmonary or laryngeal tuberculosis" [43]. In the next years, however, this confident swagger began to falter as several studies, initially of nursing students, then of medical students, began to define the occupational hazard of caring for tuberculous patients.

Perceiving the Risk

Although most large reviews from the early part of the century had concluded that work with tuberculous patients was safe, some voices did dissent [44-52]. In 1889, Cornet studied German Catholic nursing orders and found the death rate due to tuberculosis to be "exceedingly high ... . A (nurse) of seventeen ... died on average twenty-one and a half years sooner than a young girl of the same age moving through the general population" [44, 45]. In 1925, Britton and Bollman [49] determined that 2.2% of all nurses in Chicago had tuberculosis (a rate exceeded only by telephone operators and seamstresses), and Steidl observed in 1930: "Tuberculosis might be called an industrial hazard for the medical profession. It is not unusual to find that ten per cent of a (medical school) class develop clinical tuberculosis within a year or two of their graduation" [52].

Defining the Risk: Nurses

In the 1920s, the results of several studies began to determine objectively the risk to nurses and doctors. It is not surprising that this phenomenon should occur in the 1920s: The prevalence of tuberculosis infection among young adults of the 1920s was distinctly lower than that of previous generations. Set against this large group of young tuberculin-negative nursing and medical students was a population of older patients with cavitary tuberculosis. The ironic result of decades of improved public health, therefore, was the exposure of a new, nonimmune generation of health care workers to patients with tuberculosis. As Stewart wrote [53]: "At the present time young people in good homes and in careful communities can grow up with scarcely enough acquaintance with tuberculosis infection to build up any defence against it. In a gathering place of tagged and untagged infections, such as a general hospital, such unprotected young people are as sheep among wolves". It might be speculated that the failure of many tuberculosis experts to recognize the risk of caring for tuberculous patients derives from their failure to discern the consequences of an influx of tuberculin-negative young adults into the health care workforce.

Heimbeck, in a landmark series of articles from Oslo, dramatically showed the risk to a nurse of caring for a patient with tuberculosis [54-58]. Beginning in 1924, he serially tested student nurses on entry into nursing school and then annually in order to establish prospectively the tuberculin skin test conversion rate as well as the rate of development of active tuberculosis.

In an early study, he reported on 420 nursing students [55]. Of these, 220 were tuberculin negative at entry, but tuberculin skin tests had converted in 210 (95%) by graduation. More dramatically, 48 (22%) cases of clinical tuberculosis occurred in this group compared with 3 (1.5%) among 200 initially tuberculin-positive nurses.

In subsequent articles, he continued to describe high rates of tuberculin skin test conversion and development of active tuberculosis. By 1946, 105 (37%) of 284 initially tuberculin-negative nurses had developed active tuberculosis [58]. Despite criticism for his inclusion of certain findings, such as erythema nodosum, as diagnostic of tuberculosis, Heimbeck's work alerted the medical community to the very real and concerning fact that nurses had an excessive risk for developing tuberculosis.

A series of reports similar to those by Heimbeck followed as nursing schools [59-89], sanatoria [90-95], and other medical facilities [96-98] reported the tuberculin conversion rate, incidence of tuberculosis, or both, among nurses and other employees (Table 1). Every study found a rate of tuberculin conversion above that expected in the general population, and many found an increase in cases of tuberculosis. The expected annual incidence of tuberculosis among nonhospital employees varied by decade. In the 1930s, it was established at about 1% for employees of the Metropolitan Life Insurance Company [99] and 2% for food-handlers in New York City [100], much lower than the 2% to 12% encountered in the surveys of nursing schools. One study concluded that nurses were 500 times more likely than the general public to develop tuberculosis [75].

View this table: [in this window] [in a new window]   Table 1. Some Representative Studies Examining Prevalence of Tuberculin Positivity, Frequency of Tuberculin Conversion, and Cases of Tuberculosis among Nurses

 

Israel published the most compelling series reported from the United States [79]. He followed 637 nursing students from 1935 to 1939. Of 277 initially tuberculin-negative nurses, 100% tuberculin converted—half of them within 4 months of entering school. Riley determined that tuberculin conversion occurred, on average, 1.5 years after employment [101].

Unlike Heimbeck, Israel found that the incidence of active tuberculosis in initially tuberculin-negative nurses was roughly the same as that in tuberculin-positive nurses. This particular debate was finally settled by the British Prophit Tuberculosis Survey that reported on 10 000 health care workers, as well as on 20 000 additional cases reported in the literature [85, 86]. The authors found that clinical tuberculosis was three times more likely in initially tuberculin-negative persons compared with initially tuberculin-positive persons. This finding led to a recommendation from many experts that "tuberculin-negative nurses should not work in the tuberculosis wards" [86] and contributed to our understanding of the pathogenesis of adult tuberculosis [102, 103].

For more than 40 years, Myers championed the view that caring for tuberculous patients represented a risk to all health care workers, but particularly to the nurse [104-117]. He staked out his position in a polemic article published in 1930 [104]: "The situation is indeed serious. It is rumored that some of our great life insurance companies are beginning to look upon nurses as poor risks from the standpoint of disability, and ... may refuse to write disability insurance for nurses". In other words, the evidence was sufficient that the great American arbiters of justice—the insurance companies—were beginning to view nursing as hazardous. Hospitals could no longer ignore the problem.

Defining the Risk: Medical Students

The risk to medical students also was acknowledged slowly. Many medical schools reported on their tuberculin conversion rates or rates of active tuberculosis [118-142]. Abruzzi summarized the available surveys and conducted one of his own [140]. He compiled information on more than 42 000 persons who were medical students from 1940 to 1950 and found 557 cases of tuberculosis in 166 959 student-years, a rate of 3.34/1000 per year. This compared with a rate in the general population in the 1940s ranging from 0.32 to 1.0/1000 per year and led to a consideration of "tuberculosis insurance for the medical student" [143].

The exact source of spread in medical schools was determined early. Hetherington inoculated guinea pigs with the dust from various rooms frequented by medical students [122] (Table 2). He found that only the men's tuberculosis ward and the autopsy room contained dust that transmitted fatal tuberculosis to guinea pigs. Hedvall in Sweden [127] and Meade [138] found a high rate of tuberculin conversions associated with cadaver dissection during the general pathology course. Meade tabulated tuberculin conversion rates before and after discontinuation of tuberculosis autopsies and found that conversions decreased dramatically among medical students—from 81% down to 4%.

View this table: [in this window] [in a new window]   Table 2. Results of Inoculation of Guinea Pigs with Dust from Rooms Frequented by Medical Students*

 

In 1953, Mikol determined relative risk according to hospital occupation [94]. Persons with direct patient contact, such as nurses and technical workers, were 8 to 10 times more likely to develop tuberculosis than those working at the same institution who did not have patient exposure (Table 3).

View this table: [in this window] [in a new window]   Table 3. Incidence of Tuberculosis Cases by Occupational Group*

 

Why Was the Recognition of Risk Delayed?

Despite the mounting evidence, by 1950 still no consensus existed that caring for the tuberculous involved risk. There are many possible explanations for the delay. Clark, in 1924, described an obvious concern [144]: "So far has this fear (of contacting tuberculosis) reached that the private hospitals in recent years have not openly received cases of active pulmonary tuberculosis, thinking that if they did they would lose patronage".

Another fear was that acknowledging the risk of contagion would scare young women away from nursing. This particular debate became public in 1930, in an exchange between Myers and Fishberg [145-147]. Myers wrote that, because of the available evidence, he questioned whether the "exposure of students to tuberculous patients should be allowed to continue". Fishberg, denying that a risk existed, responded that he was concerned that "the views expressed in Dr. Myers' paper (that tuberculosis care was a risk) may be accepted by the public and thus make it more difficult to recruit nursing staffs". Myers later went further: He compared the exposure of class after class of student nurses and doctors to a type of ongoing study "rarely equalled by animal experimentation, except that in animal work it is possible to control the dosage and kill an animal at any time" [106].

Liability was also a concern. Childress wrote that development of tuberculosis after known occupational exposure is "not prima facie evidence of causal relationship" [95]. He also noted, however, that by 1940, 23 states gave full workmen's compensation for tuberculosis as an occupational disease. In closing, he made the best of a grim situation by remarking, "it should be stressed that clinical disease did not develop in 98.2% of employees in this study (a review of 3486 employees at Grasslands Hospital), and 28.6% escaped infection sufficient to convert the tuberculin reaction".

Some experts simply did not believe there was an increased risk, stating that the higher incidence defined among health care workers resulted from increased surveillance, not from increased disease [98, 137, 148]. This view held that hospital workers, by virtue of their frequent tuberculin tests and chest radiographs, were more likely to be diagnosed with a skin-test conversion or mild tuberculosis and therefore had inflated annual rates of infection and disease.

A middle ground emerged that accommodated both those who had documented a striking increase in tuberculin conversion and those who saw no increase. This view acknowledged that, indeed, primary infection was occurring at alarming rates but that these primary infections did not translate into active, disabling tuberculosis.

Leading proponents of this concept included Amberson and Riggins of Bellevue Hospital [68]. They noted that on their tuberculosis ward from 1931 through 1936, more than 1000 nurses cared for over 3100 persons with tuberculosis. Of the 43% initially tuberculin-negative nurses, most tuberculin converted. However, only 8 (1.5%) of 539 nurses developed active tuberculosis during the study period, and 6 of these cases were mild. Such an attack rate, the authors concluded, was similar to that expected in the general community. "It is clear," they wrote, "that ... the hazard of serious and advanced tuberculosis for Bellevue student nurses has not exceeded that for young women pursuing other occupation in the City" [68].

This reasoning was further advanced by Brahdy, who summarized information from nursing schools and medical residencies throughout New York City [148]: "The incidence of tuberculosis among hospital personnel is about the same as that in any similar group," he wrote. "Student nurses are an exception, however, despite a high rate of tuberculin conversion, graduate nurses do not have a high tuberculosis morbidity in later life". He also cited studies of death rates due to tuberculosis ranked by occupation [149-151] that showed that relatively few male physicians died of tuberculosis (23.7 deaths/100 000) compared with men in other occupations (Figure 1). Similar findings were reported for British men [152].

View larger version (56K): [in this window] [in a new window]   Figure 1. Tuberculosis mortality among men in 1930. Physicians and surgeons have very low risk, prompting the author to suggest the occupational hazard of caring for the tuberculous was minimal. Adapted with permission from Brahdy [148].

 

The compromise view had been suggested decades earlier by Osler: "All who mix with tuberculous patients got infected, but remained well so long as they ... kept the soil in a condition unfavourable for the growth of the seed" [47]. Finally, in the 1950s, when, as Myers wrote, the "rapid decline of tuberculosis in the general population (made) the disease among physicians more conspicuous" [101], did the medical community finally agree that a significant occupational risk existed.

Control Interventions

Even though a consensus was not achieved until the 1950s, in 1930, Myers had recommended how best to control the problem [104]. He suggested five steps: 1) Perform tuberculin testing and chest radiographs on all new employees. 2) Do follow-up tuberculin testing and chest radiographs every 6 to 12 months. 3) Exclude tuberculosis in all new patients admitted to the hospital, including initiating routine admission chest radiography. 4) Establish a tuberculosis service in all hospitals. 5) Practice aseptic technique as was routine for other infections such as diphtheria and scarlet fever.

In addition to the above steps, several other ideas were put forward. Dufault [28] recommended easing the work schedule: "The work should not be too hard nor the hours too long. A month's vacation a year is desirable". Jennings [153] suggested that, to cover the mouth, two layers of paper were superior to ten pieces of gauze. Gordon and Cashman [60] proudly proclaimed that their hospital diet, "essentially high in carbohydrate and ... augmented further by the addition of pastry, ice cream, candy and fruit between meals" was the secret to the relatively low rate of infection among their employees. Proper diet, specifically free beer, was also mentioned by Goldman [154].

Immunization against tuberculosis with bacille Calmette–Guérin (BCG) vaccination was considered by several investigators, although no large prospective study of BCG in health care workers was done. Among smaller studies, Heimbeck followed a group of tuberculin-negative nurses [58]. Tuberculosis was diagnosed in 42 (8%) of 501 nurses who received BCG vaccine compared with 105 (37%) of 284 who were not vaccinated. This dramatic finding, however, was not duplicated in other series. Rosenthal found no cases of tuberculosis in 142 BCG-vaccinated nurses compared with 3 cases in 199 unvaccinated nurses [155]. Abruzzi found only 3 cases of tuberculosis among 4400 vaccinated medical students and ascribed the downward trend in rates of tuberculosis among medical students to use of the vaccine [140]. A similar decrease from a medical school that did not offer BCG vaccination was reported by Karns, who suggested that the decrease described by Abruzzi was caused by factors other than BCG vaccination [141]. Myers felt there was "no premise for attempting to produce immunity artificially" [115] and did not recommend BCG vaccination for health care workers. Although BCG vaccination of health care workers has recently again been suggested [156], no consensus currently exists regarding its use.

A crucial step to control the problem taken by American hospitals was the institution of chest radiographs for all patients admitted to the hospital (Myers' third suggestion). Undiagnosed tuberculosis, then as now, was viewed as the cause of most nosocomial spread. Riggins wrote that, in the early 1950s, approximately 40 000 patients with unknown cases of tuberculosis were hospitalized in the United States annually [98]. Cavitary tuberculosis is was found in 0.5% to 5% of nontuberculosis autopsies [157, 158]. Calls for routine admission chest radiographs were sounded as early as 1936 [159] but were unheeded for many years. In 1948, only 247 (5%) of 4539 hospitals surveyed reported doing chest radiographs on all patients admitted [160]. The use of routine admission chest radiographs was shown by Jacobson to reduce dramatically the number of tuberculosis cases among hospital employees Figure 2 [161].

View larger version (13K): [in this window] [in a new window]   Figure 2. Cases of tuberculosis among employees in Los Angeles County hospitals. Decrease began in 1951 with the institution of a mandatory admission chest radiograph for all patients. Adapted with permission from Jacobson and colleagues [161].

 

The benefits of the various interventions were later reported [114, 162]. The advent of effective chemotherapy and routine prophylaxis also contributed greatly to the decline in cases of tuberculosis seen among health care workers.

Recent Studies

In later years, as the incidence of tuberculosis dwindled, so too did the concern about tuberculosis as an occupational hazard for nurses and physicians [154, 163-167]. Employee tuberculin conversion rates were reported rarely [163], although scattered reports of hospital outbreaks appeared [168-177]. Almost all such articles, interestingly, begin with the statement that "tuberculosis has long been an occupational hazard for persons working in hospitals" [178]. The exact moment that the debate and uncertainty of the preceding decades was resolved is untraceable. Yet by the 1960s, the risk was acknowledged as simple, self-evident truth.

Several recent outbreaks are particularly instructive. At Jackson Memorial Hospital in Miami, 21 (35%) of 60 employees had documented tuberculin conversions after working on a ward where a patient with an index case had been present for 57 hours [170]. A malfunctioning air conditioning system may have allowed recirculation of contaminated air, spreading the infection. In an outbreak in San Diego, 14 (31%) of 45 exposed staff tuberculin converted, with the rate highest among those present at bronchoscopy [172]. The risk presented by bronchoscopy was further suggested by Malasky, who found that the tuberculin conversion rate of pulmonary fellows-in-training was significantly higher than that of infectious disease fellows-in-training [179]. A 1983 outbreak occurred when a patient with an index case spent only 4 hours in an emergency department [175]. He was felt to account for 11 tuberculin conversions (five of whom developed active tuberculosis) among 112 emergency department employees.

Tuberculous skin abscess has also been associated with nosocomial spread, emphasizing that nonpulmonary cases of tuberculosis may be contagious [176, 177]. In one outbreak, 59 (13%) of 442 exposed employees tuberculin converted, and nine cases of active tuberculosis occurred [176].

The emergence of the HIV epidemic rapidly made nosocomial spread of tuberculosis to hospital workers and patients an urgent concern. Worker safety issues are being actively addressed [22, 23, 180-184]. The Centers for Disease Control and Prevention has investigated many hospital outbreaks and found tuberculosis infection and disease among workers [9-21]. Tuberculin conversion rates have ranged from 33% to 50% and several deaths due to occupationally acquired multidrug-resistant tuberculosis have occurred in HIV-positive health care workers [4, 18, 19].

Conclusion

Top Conclusion Author & Article Info References

After several decades of debate, it became clear that the health care worker was at increased risk for development of tuberculosis infection and disease. Surprisingly, this simple conclusion, so obvious now as to seem self-evident, took many decades to establish. A combination of genuine confusion, ignorance, and willful neglect conspired to keep the debate active and unsettled as late as the 1950s. Our current unanimity on the issue appears to have been achieved somewhat passively, because no definitive article appeared nor was any consensus paper issued that served to settle the matter.

As the incidence of tuberculosis decreased nationally, so too did the concern about health care worker safety. But with the current marked increase in cases of tuberculosis being treated in hospitals, ensuring hospital worker safety is once again of highest importance. The perceived threat is so great that many workers are reconsidering their decision to enter the health care field. Such a decision would have profound consequences for all patients, not only those with tuberculosis.

A review of the literature of the last 100 years emphasizes that health care workers do indeed face a real occupational risk in caring for persons with tuberculosis. Although this risk may be reduced with consistent use of respiratory isolation beds, environmental interventions, and immediate treatment of all suspected cases, the risk is, finally, never reducible to zero. The threat, however, can be minimized if highest priority is given to identifying and isolating persons with suspected tuberculosis. Modern technologic advances, such as particulate respirators, germicidal ultraviolet light irradiation, and rooms with negative-pressure ventilation, can, after all, afford no protection against the unsuspected case.

Author and Article Information

Top Conclusion Author & Article Info References

From Memorial Sloan-Kettering Cancer Center and New York Hospital-Cornell Medical Center, New York, New York.
Requests for Reprints: Kent Sepkowitz, MD, Infectious Disease Service, Memorial Sloan-Kettering Cancer Center, New York Hospital-Cornell Medical Center, 1275 York Avenue, Box 288, New York, NY 10021.
Acknowledgment: The author thanks the staffs of the medical libraries of Memorial Sloan-Kettering Cancer Center and of Cornell Medical Center for their assistance.
Grant Support: In part by National Institute of Allergy and Infectious Disease AIDS Clinical Trials Group grant 5 U01 AI27669-04.

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Top Conclusion Author & Article Info References

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