Below are the first 10 and last 10 pages of uncorrected machine-read text (when available) of this chapter, followed by the top 30 algorithmically extracted key phrases from the chapter as a whole.
Intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text on the opening pages of each chapter. Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.
Do not use for reproduction, copying, pasting, or reading; exclusively for search engines.
OCR for page 189
Tuberculosis in the Workplace C The Occupational Tuberculosis Risk of Health Care Workers Thomas M.Daniel, M.D.* SUMMARY AND CONCLUSIONS A review of published literature has been undertaken in response to a commission from the Institute of Medicine Committee on Regulating Occupational Exposure to Tuberculosis. The charge of this commission was to prepare a review paper addressing the question of whether health care workers (and workers at other sites covered by the proposed regulations of the Occupational Safety and Health Administration [OSHA]) are at a greater risk of infection, disease, and mortality due to tuberculosis than the general community within which they reside. This paper focuses principally on the risk of infection, with only limited comments on the risks of disease and mortality. In conducting this review, the author faced limitations imposed by the quality of the published data and by the lack of published information relevant to some of the aspects of the charge. In particular, much of the quantitative data presented here can be taken as no more than approximate. Nevertheless, certain conclusions have been drawn by the author. Health care workers are at risk of contracting tuberculous infection in the workplace. This risk has been declining in recent decades. In those health care facilities where modern infection control measures are in place, it now approaches the level of risk incurred by health care workers in the communities in which they reside. That it has declined and continues to * Professor Emeritus of Medicine and International Health, Case Western Reserve University, Cleveland, Ohio.
OCR for page 190
Tuberculosis in the Workplace decline means that it has been higher than the baseline community risk, and it will not be possible to assume that there is no excess risk until no further decline is observed. A large portion of the current and recent risk to health care workers of tuberculous infection is the result of exposure to unsuspected cases of infectious tuberculosis or to exposure in circumstances of poor ventilation. In some outbreaks from unsuspected sources, exposed employee infection rates have been as high as 50 percent. When effective infection control procedures are in place, unsuspected contagious cases of tuberculosis may provide nearly all of the occupational tuberculosis risk. The risk to health care workers of tuberculous infection varies with job category. In general, health care workers in contact with patients are at higher risk than those with no patient contact. Noncontact employees often have a higher incidence of infection than contact employees, but this is due to community exposure risk. Job situations of exceptionally high risk are those involving the generation of respiratory aerosols from patients, including bronchoscopy, endotracheal suctioning and intubation, cough and sputum induction, and the administration of irritation medications (e.g., pentamidine) by aerosol. The risk to health care workers of tuberculous infection varies in the United States with geographic locale. The incidence of tuberculosis varies greatly with location in the United States. Coastal urban cities bear the greatest tuberculosis burden and rural Midwest and mountain state regions the least. Health care facilities in these various regions care for numbers of patients with tuberculosis that vary substantially in parallel with variations in incidence. The risk to health care workers of tuberculous infection varies in the United States with demography and ethnicity. In general, individuals of African-American, Hispanic, and Asian heritage have a higher incidence of tuberculous infection than do persons of European extraction. Foreign-born Americans bring with them much of the tuberculous infection risk of the countries of their origins. The risk of tuberculous infection varies greatly with socioeconomic status, most of the infection risk being incurred by those who are less affluent. For health care workers, these variations in population tuberculosis incidence have two important consequences. First of all, the tuberculous infection risk in the community in which health care workers reside and in which they usually spend more time than they do in their job setting is correlated with these ethnic and demographic variables. Second, the population served by the health care facility will influence the amount of potential tuberculosis exposure of the employees. The occupational tuberculosis risk to American health care workers can be quantified only in approximate terms. The magnitude of the tuberculosis risk to American health care workers at the current time in those
OCR for page 191
Tuberculosis in the Workplace facilities where recent Centers for Disease Control and Prevention (CDC) guidelines for infection control have been implemented is usually not substantially greater than the risk incurred by these individuals in the communities in which they reside. The risk to infected health care workers of progression to tuberculous disease (tuberculosis) is lower than often stated; the risk of mortality for immunocompetent individuals harboring drug-susceptible organisms is negligible. The risks of tuberculous disease and mortality in Mycobacterium tuberculosis-infected health care workers is probably no higher than that of individuals in the general population. Overall, the risk of tuberculosis in individuals who become infected as adults is probably of the order of 5 percent. Nearly all of the tuberculosis mortality in the United States today is accounted for by individuals who fail to be diagnosed or treated in timely fashion, who are immunocompromised (usually by human immunodeficiency virus [HIV] infection), or who suffer from multidrug-resistant tuberculosis. INTRODUCTION In an era of recently resurgent tuberculosis and accompanying concern about the occupational tuberculosis risk of health care workers, the Institute of Medicine has been asked by the U.S. Congress to study the magnitude of this occupational risk and the potential impact on it of a newly proposed rule regulating the environment in which care of tuberculosis patients is conducted. At the present time, health care workers account for about 3 percent of the cases of tuberculosis reported in the United States (1). Charge to the Reviewer This paper reviews the published medical literature relevant to the occupational tuberculosis risks of American health care workers. It was commissioned by the Institute of Medicine Committee on Regulating Occupational Exposure to Tuberculosis. The charge of this committee was to prepare a state-of-the-art literature review addressing the following questions: Are health care workers (and workers at other sites covered by the proposed OSHA regulations) at a greater risk of infection, disease, and mortality due to tuberculosis than the general community within which they reside? If so, what is the excess risk due to occupational exposure? Can the occupationally acquired risk be quantified for different work environments and different job classifications? Determinants of Tuberculosis Risks Consideration of the occupational tuberculosis risk of health care workers must be done in two parts: the risk of infection and the risk of
OCR for page 192
Tuberculosis in the Workplace disease. The determinants of these risks are multiple. Exposure is a major determinant of infection risk, and it may be related to the work place, although it must be realized that health care workers may also face exposure in the communities in which they reside. Individual factors such as age, immune status, and genetic composition (possibly including race) are also important, especially for the risk of disease. These factors are not per se related to the workplace, but that does not mean they are not operative in the workplace. Published Literature Reviews There have been a number of well-done literature reviews of the occupational tuberculosis risk to health care workers published during the past decade (2–9). In general, these reviews emphasize the risk of tuberculous infection and do not deal with the subsequent risk of disease. Nor do they provide much information permitting one to compare the workplace risk to that incurred in the community in which health care workers reside. These reviews have documented that tuberculin conversion rates for American health care workers in the recent past were as high as 4–5 percent/year in many urban areas and perhaps twice that in some areas of New York City and for certain job situations with high exposures to aerosols of respiratory secretions. In nonurban areas, they were generally lower than 0.2 percent/year. With the implementation of enhanced infection control measures recommended by such advisory groups as CDC during the past decade, these rates have dropped to below 1 percent generally. However, outbreaks continue to occur from unrecognized sources, and with these outbreaks the tuberculin conversion rates among exposed employees may be as high as 50 percent. METHODS Literature Review This paper is based on a review of published literature. Searching was done using PubMed (MedLine) with a variety of topics relevant to tuberculosis and health care workers. Additional publications were selected from the bibliographies of published reports. Identified papers were then retrieved using the resources of the Health Sciences Library and Allen Memorial Library of Case Western Reserve University. Finally, a number of relevant papers were already present in the author’s personal library and reprint collection. Data presented in this paper have been converted, when possible, from the form in which they were originally presented to percent per year. In a few reports, the original data are given as per 100 person-years, and this
OCR for page 193
Tuberculosis in the Workplace more precise form has been retained. In many instances, no time interval was given, and in these cases percent is used. Because many of these conversions to percentages are based on small absolute numbers, the actual numbers are given in those cases to allow the reader to note this fact. Annual Risk of Tuberculous Infection The annual risk of infection (ARI) with M. tuberculosis, the tubercle bacillus, is central to any consideration of the occupational tuberculosis risk of health care workers. Ideally, one would like to know this figure not only for employees but also for the community in which they reside. Data upon which the ARI for American populations can be calculated are generally lacking, however, and many of the reports of infections in health care workers do not provide relevant time intervals. In this review, ARI is expressed as percent per year, the usage of most workers who have dealt with this subject. It is acknowledged that the term “annual risk” as it is used here is imprecise—annual probability or likelihood would be more accurate terms—but its use is widely established in the published literature on this subject, and it is used here for consistency with that literature. It is also true that such calculations on an annual basis ignore the fact that the pool of individuals considered may change during a year. However, data are almost always lacking in the studies reviewed here for estimation of the more accurate use of person-years at risk. Errors thus introduced are small at low levels of risk and do not affect the conclusions drawn in this review. Two types of ARI are reported here: (a) calculated annual risks, when the data permit such direct calculation, and (b) estimated annual risks based on tuberculosis incidence when direct calculation is not possible. Calculated Annual Risk of Infection If one accepts the development of tuberculin hypersensitivity as a reliable index of primary tuberculous infection, then it is a straightforward task to calculate the ARI with M. tuberculosis expressed as percent per year from serial skin testing data. The algebraic formula for this calculation is ARI = [1 − (Qb/Qa)1/(b−a)] * 100, where Q is 1 − P, P is the probability of being infected at a given age or year a or b, a is the initial age or year of observation, and b is the second year or age of observation (10). In the text of the present review paper, ARI thus calculated is referred to as the “calculated ARI.”
OCR for page 194
Tuberculosis in the Workplace Estimated Annual Risk of Infection Styblo has observed that there is an empiric and relatively constant relationship between the incidence of smear-positive tuberculosis and the annual risk of infection (11). He estimated that the ratio between this incidence and the ARI ranged between 50 and 60 in a variety of populations, pricipally those of high tuberculosis prevalence. Daniel and Debanne reasoned that this relationship could be used in reverse to estimate ARI when good case reporting was available but tuberculin skin test data were absent. They tested this hypothesis using data from white male U.S. naval recruits and found that in this population the ratio of incidence of tuberculosis of all forms to ARI was approximately 150 (10). The disparity between this figure and the lower figure of Styblo may result in part from the use of low-incidence populations, but the largest reason for the difference rests with the use by Daniel and Debanne of rates for all forms of tuberculosis, whereas Styblo considered only single-sputum smear-positive, pulmonary tuberculosis. In the current review paper estimation of ARIs is based on a ratio of 150, and ARI thus derived is referred to as the “estimated ARI.” While this method is imprecise, it is often the only means available to judge ARI in American populations. Limitations of This Study In doing this review, three limitations were deliberately imposed. First, papers published prior to 1970 were used only to a limited degree and then only to provide historical context. Second, limited use was made of reports of outbreaks, for these accounts are usually anecdotal in character. Third, most papers describing studies done in other countries were excluded because both health care occupational sites and attitudes toward occupational risks in most other countries differ substantially from those in the United States. A major limitation in this review and in the entire body of knowledge that it approaches rests with the definitions of tuberculous infection and of tuberculous disease. This subject is separately addressed in a paper authored by John B. Bass Jr., and is included in this report as Appendix B. RISK OF TUBERCULOUS INFECTION Risk in the U.S. General Population If one is to examine the occupational risk of tuberculous infection among health care workers in relation to the communities in which they reside, then it is first important to try to determine the annual risk of infection in the general American public. Tuberculin testing data upon
OCR for page 195
Tuberculosis in the Workplace which such a determination can be based are limited. The last systematic attempt to estimate the prevalence of tuberculin reactivity in the United States was that of the National Health Survey of 1971–72, which concluded that in American adults aged 25 to 74 years the prevalence of tuberculin reactivity was 21.5 percent (12). A reasonable estimate for the current date for Americans of all ages might be 5 to 10 percent, and perhaps 10 percent in adults. Tuberculous infection is not uniformly distributed among Americans, and it is important to stratify any assessment of the general population risk so that infection in health care workers can be compared with that in the appropriate reference community. For example, tuberculosis is much more common in urban areas than in rural areas, and even in the cities of middle America it is not as frequent as in this country’s coastal cities. Many demographic factors correlate with tuberculosis incidence in America. Health care workers are employed, while nearly 60 percent of tuberculosis in the United States occurs among the unemployed (1). Importantly for this consideration, a substantial number of health care workers are foreign-born, one-third of them coming from the Philippines; among other employed persons, one-quarter come from Mexico (A. Curtis, personal communication of material presented to a workshop held in December 1999). The importance of this difference rests with the difference in tuberculosis in the countries of origin for these groups. Based on recent World Health Organization estimates, the current incidence of sputum smear-positive tuberculosis in the Philippines is 260/100,000, and that in Mexico is 58/100,000 (13). Calculated ARI with M. tuberculosis in Selected American Populations There are relatively few tuberculin surveys available from which one can calculate the ARI in American populations and none in recent years. Moreover, those surveys that have been conducted have often been flawed by the use of poorly standardized tuberculin testing techniques and by poor characterization of the populations studied, especially with respect to demographic characteristics. The use of tuberculins other than purified protein derivative (PPD) at 5 tuberculin units may lead to an overestimation of the actual prevalence of tuberculin reactivity. Data from 12 selected surveys conducted in the United States during the middle half of the 1990s are presented in Table C-1. These studies rarely involved serial testing or testing of more than one age group. In that situation, the calculation of ARI for Table C-1 was done from birth, assuming a reactor rate of zero at birth, a maneuver admittedly flawed because it assumes the risk to be uniform throughout life. The error thus introduced has the potential for underestimating the adult risk relevant to health care workers.
OCR for page 196
Tuberculosis in the Workplace TABLE C-1. Tuberculin Surveys in the United States and ARI with M. tuberculosis Calculated from Them Year of Study Population (Reference) Tuberculin* Calculated ARI (%/year) 1930 New York City, schoolchildren (17) OT, 10 TU 11.14 1957 Pamlico County, GA, general population (18) PPD-S, 5 TU 0.25 1957–60 Chicago nursing students (19) OT, 2 TU 0.75 1958–65 White naval recruits (20) PPD-S, 5 TU 0.14 1963 Pennsylvania high school students (21) PPD, 5 TU 0.19 1964–65 Air force recruits (14) Tine test 0.16 1965–69 First grade children in United States (21) Probably PPD-S 0.08–0.05 1964–67 CDC surveys at selected sites (22) PPD, 5 TU 0.16 1971–72 National health survey (HANES) (12) PPD-S, 5 TU 0.58 1973–74 New York City Board of Education employees (16) PPD, 5 TU 0.23 1975–79 CDC-reported data from selected sites (1) Variable 0.20–0.15 1980–81 New York City school children (23) PPD, 5 TU 0.45 *Tuberculins used for skin testing have included old tuberculin (OT), a crude preparation, and purified protein derivative (PPD), a somewhat purified preparation made from OT. PPD has been made by many manufacturers. PPD-S refers to a single large batch of PPD prepared by Florence Seibert, of which half was deposited as the reference standard against which all other PPDs are standardized and half was given to the U.S. Public Health Service for use in research studies. Tine tests use OT. The dose of tuberculin used for testing is expressed in tuberculin units (TU), which are based upon bioequivalent standardization with PPD-S. The usual dose, for which the largest amount of validation data are available, is 5 TU. It is evident that ARIs are larger in urban populations—specifically, New York City—than elsewhere. Unfortunately, the available data often are not sufficient to make generalizations with respect to geography nor with respect to such demographic factors as ethnicity or socioeconomic status. Two studies of military recruits allow one to examine race and ethnicity (14, 15). The annual risks of infection calculated from these studies are shown in Table C-2. Data from a single study in New York City school board employees allow one to examine race and ethnicity in the urban setting (16). The calculated ARIs from this study are shown in Table C-3. The ARI calculated for African American and Hispanic military recruits for 1990 was approximately six times that for whites. For Asian recruits the calculated ARI was approximately 36 times that for whites. For New York City, calculation from the 1973 data yielded an ARI for African Americans 8.6 times those in whites and for Puerto Ricans 6.5 times those in whites.
OCR for page 197
Tuberculosis in the Workplace TABLE C-2. ARIs Calculated for U.S. Military Recruits in 1965 (14) and 1990 (15) Racial/Ethnic Group as Characterized by Study Author Calculated ARI, 1965 (30) (%/year) Calculated ARI, 1990 (35) (%/year) White 0.16 0.04 Black 0.56 0.25 Puerto Rican 1.12 0.26 American Indian 0.92 Asian 1.45 TABLE C-3. ARIs Calculated for New York City in 1962 (20) and 1973 (16) Racial/Ethnic Group as Characterized by Study Author Calculated ARI, 1962 (20) (%/year) Calculated ARI, 1973 (16) (%/year) White 0.2 0.08 Black 0.69 Puerto Rican 0.52 Estimated ARI with M. Tuberculosis in Selected American Populations As noted previously, it is possible to estimate the ARI from reported case rates. However, one must be cautious about the precision of these estimates. Having expressed this concern about their use, estimated ARIs are presented for various American populations in Tables C-4, C-5, and C-6. TABLE C-4. ARI in 1998 Estimated by Method of Daniel and Debanne (10) for Various Demographic and Racial Segments of the U.S. Population, 25- to 44-Year-Old Age Cohort Population Group Tuberculosis Case Rate per 100,000, 1998* Estimated ARI (%/year) United States total 6.8 0.05 White, not Hispanic, male 3.1 0.02 White, not Hispanic, female 1.5 0.01 Black, not Hispanic, male 23.5 0.16 Black, not Hispanic, female 12.7 0.08 Hispanic male 17.1 0.11 Hispanic female 9.9 0.07 Asian/Pacific Islander, male 42.8 0.29 Asian/Pacific Islander, female 30.9 0.21 *Tuberculosis case rates for 1998 are CDC-reported data (1).
OCR for page 198
Tuberculosis in the Workplace TABLE C-5. ARI in 1998 Estimated by Method of Daniel and Debanne (10) for Selected American Cities, All Ages City Tuberculosis Case Rate per 100,000, 1998* Estimated ARI (%/year) Atlanta, GA 8.9 0.06 Baltimore, MD 7.6 0.05 Greensboro, NC 5.6 0.04 Los Angeles, CA 14.9 0.10 Miami, FL 13.4 0.09 New York, NY 19.1 0.13 Newark, NJ 10.7 0.07 Philadelphia, PA 5.8 0.04 St. Louis, MO 4.3 0.03 Salt Lake City, UT 3.3 0.02 San Francisco, CA 18.2 0.12 Seattle, WA 5.9 0.04 *Tuberculosis case rates for 1998 are CDC-reported data (1). Summary of Risk of Tuberculous Infection in the General U.S. Population In general, the ARI in American populations has been declining during the past century and is now very low, although it may have increased in New York City and certain other urban areas with the recent resurgence of tuberculosis. The risk is much lower in rural areas and cities in the Midwest and mountain states than it is in major coastal cities, where most of the infectious cases of tuberculosis occur. The risk in America’s TABLE C-6. ARI Estimated by Method of Daniel and Debanne (10) for Selected Demographic Groups Ages 16–64 Years as Reported for 1984– 85 by McKenna and Colleagues (24) Demographic Group Tuberculosis Case Rate per 100,000 Estimated ARI (%/year) Total 8.4 0.06 Not Hispanic, white 3.6 0.02 Not Hispanic, black 35.1 0.23 Hispanic 20.2 0.13 Asian 56.1 0.37 Male 11.8 0.08 Female 5.1 0.03 Currently employed 4.9 0.03 Previously employed 11.6 0.08 Unemployed 337.2 2.25 U.S.-born 7.2 0.05 Foreign-born 29.2 0.19
OCR for page 199
Tuberculosis in the Workplace ethnic minority populations is much higher than it is in Americans of European extraction—of the order of 0.1 to 0.2 percent/year as opposed to 0.01 to 0.02 percent/year. For unemployed individuals, the group from which more than half of American tuberculosis cases are reported, the annual risk of infection probably exceeds 2.0 percent/year. Tuberculosis among foreign-born individuals now accounts for about 40 percent of new cases each year in the United States. Foreign-born individuals bring with them their infection histories from the countries in which they originate, many of them high-tuberculosis-incidence countries. The ARI in foreign-born persons in the United States is probably about 0.2 percent/ year. Considering the country as a whole, 0.05 percent is probably a reasonable estimate of the ARI. Risk in Hospital-Based Health Care Workers Until the 1950s, when effective chemotherapy heralded the closing of most tuberculosis sanatoria and categorical tuberculosis hospital services, the occupational risk of tuberculous infection was generally accepted by all health care workers. Indeed, primary tuberculous infection was welcomed by many because of the immunity to subsequent infection that accompanied it. Numerous studies showed student nurses to be at especially high risk, and medical students fared little better. Following the widespread introduction of isoniazid in 1953, tuberculosis sanatoria saw a dramatic fall in their patient censuses, with much shortened hospital stays, and they began to close their doors. The May 1969 issue of the Bulletin of the National Tuberculosis and Respiratory Disease Association announced on its cover and above the first page of every article it contained, “The General Hospital is the logical place” (25). The contents of this publication are largely devoted to reassuring health care workers that there is little risk to them, although it stated that “good ventilation without recirculation of air is essential for rooms or wards used for tuberculous patients.” Unfortunately, such ventilation was not widely available in many hospitals at that time. During the 1970s and 1980s, the decades following these changes in the venue of care of tuberculous patients, a number of outbreaks of tuberculous infection among health care workers were reported and the first attempts at systematic study of nosocomial transmission of tuberculous infection were undertaken. Most of these studies are not relevant to the current situation, but a few are worth noting because their conclusions remain important. In 1975, Ruben, Norden, and Schuster evaluated the tuberculosis screening program for employees of a Pittsburgh hospital (26). This study is of particular note because it was among the first to look at patient contact in relation to infection. Employees considered to work in patient
OCR for page 219
Tuberculosis in the Workplace who reacted only to 100 units, tuberculosis developed in 1.2 percent (406/ 33,518). Follow-up surveillance was conducted at 2.5-year intervals. The incidence in the first interval was nearly double that in ensuing follow-up periods. Comstock reported 18-year follow-up data on a 1946 tuberculin survey and BCG vaccination program in Muscogee County, Georgia (90). Among 1,492 individuals positive for reactivity to 5 tuberculin units of PPD, 24 (1.6 percent) had developed tuberculosis. In a larger trial conducted in Muskogee County about 10 years later, Comstock and colleagues observed more than 22,000 individuals of all ages who reacted to PPD with more than 10 millimeters of induration for 20 years (91; G.W. Comstock, personal communication). Overall, 207 of the reactors (0.94 percent) developed tuberculosis. The average annual rate was 0.73 percent. Thirty-eight pecent of the cases developed during the first 5 years of observation. Perhaps the most useful data on the occurrence of tuberculosis in tuberculin skin test reactors excluded from BCG vaccination trials comes from the report of Comstock, Livesay, and Woolpert that includes data from the Puerto Rican trial (92). Using case registers from both Puerto Rico and New York City, they traced more than 80,000 individuals with a mean follow-up of 18.9 years. They reported data by several demographic characteristics, which are presented in Table C-14. Not surprisingly, tuberculosis occurred much more frequently among urban than rural residents. It occurred more frequently in females than males and substantially more frequently in young children. TABLE C-14. Tuberculosis Occurring in Nonvaccinated Puerto Ricans Identified in a BCG Trial, Initially Reacting to 1 or 10 Tuberculin Units of PPD with ≥6 millimeters of Induration (92) Demographic Category Number of PPD-Positive Persons Number of Tuberculosis Cases Percent Total 82,269 1,400 1.7 Urban residence 47,021 844 1.8 Rural residence 35,248 56 0.2 White 67,184 1,152 1.7 Black 15,085 248 1.6 Male 43,100 674 1.6 Female 39,169 726 1.9 Age 1–6 years 3,906 119 3.0 Age 7–12 years 35,869 520 1.4 Age 13–18 years 42,494 761 1.8
OCR for page 220
Tuberculosis in the Workplace Studies of Control Subjects in Trials of Treatment of Latent Tuberculous Infection The U.S. Public Health Service trials of isoniazid treatment of latent tuberculous infection provide useful 10-year follow-up information for the untreated, control groups (82). A variety of studies were conducted, of which those with household contacts and inmates of mental hospitals are probably the most relevant to health care workers. Overall, tuberculous infection marked by a PPD reaction of ≥10 millimeters occurred in 2.9 percent of infected household contacts and 1.2 percent of infected mental hospital inmates. Approximately one-third of cases developed during the first year of observation. Attack rates were higher in adults (essentially at the overall levels cited above) than children, and at least in the household contact group, the adult rate did not change through age 55. A small study of a shipboard outbreak in the Dutch navy was cited by Ferrebee in her review (82). Tuberculosis developed in 12 of 128 seamen (9.4 percent) not given isoniazid in a trial of the effectiveness of this therapy, a figure much higher than that reported in any other investigation. This study, although small, is of interest because it reflects results in employed individuals. Shipboard exposures have been found to be more intense and have higher attack rates than those in other situations, and the population was probably skewed toward the young-adult age group that has the highest risk. In an editorial dealing with the use of isoniazid for the treatment of latent tuberculous infections in young adults, George Comstock and Phyllis Edwards used published and unpublished data from both BCG trials and isoniazid chemotherapy trials to estimate the lifetime risk of tuberculosis among tuberculin skin test reactors (93). They noted that the risk declined with passing years. Lumping together their estimates of lifetime tuberculosis risks for tuberculin-positive black and white males and females, their estimates were approximately 3.5 to 4.5 percent at age 25, 3.1 to 3.6 percent at age 35, 2.6 to 3.0 percent at age 45, 2.0 to 2.5 percent at age 55, and 1.2 to 1.6 percent at age 65. Impact of HIV Infection HIV infection, even before the onset of frank AIDS, increases the risk of tuberculosis in infected individuals. In fact, tuberculosis is one of the major intercurrent infections of dually infected persons, and tuberculosis often occurs at a time when immune function is relatively well preserved. Setting aside some excellent studies done in Africa as perhaps not applicable to American health care workers, the 2-year prospective study of Selwyn and colleagues conducted in a New York City methadone clinic in 1985–1987 provided what has been widely quoted and generally ac-
OCR for page 221
Tuberculosis in the Workplace cepted as a measure of the risk of tuberculosis in dually infected persons (94). He found a tuberculosis risk of 7.9/100 person-years in PPD-positive, HIV-infected addicts and a risk of 0.3/100 person-years in PPD-negative, HIV-seropositive individuals. Isoniazid treatment of latent tuberculous infection was offered to all tuberculin-positive addicts, but the rate of compliance was low. In a second study in 1987–1990, Selwyn and collaborators documented patient compliance with isoniazid treatment and also used a battery of delayed hypersensitivity antigens to assess skin test anergy (95). Among 25 persons who did not complete isoniazid, the tuberculosis incidence was 9.7/100 person-years. No cases occurred among those who completed treatment of latent infection. Among anergic individuals, the incidence was 6.6/100 person-years. Useful information on the risk of tuberculosis in HIV-infected persons exposed to tuberculosis comes from two outbreak studies. Di Perri and coworkers described an outbreak of tuberculosis among AIDS patients in a hospital in Italy at which no patient with tuberculosis had been hospitalized during the previous 3 years (96). Ventilation included air recirculation. An individual with initially unsuspected tuberculosis was admitted, and an outbreak ensued. Among 18 exposed HIV-infected individuals, tuberculosis developed in eight, seven of them within 60 days. Daley and colleagues described an outbreak in a congregate living facility for AIDS patients in San Francisco (97). A person with unrecognized tuberculosis was admitted to the facility; the diagnosis was made 6 weeks later after 3 weeks of progressive respiratory symptoms. Eleven of 30 exposed residents developed tuberculosis within the next 6 months, and organisms isolated from them were all of the same RFLP type as the organism from the index case. These two outbreaks demonstrate the enormous impact of HIV infection on susceptibility to tuberculosis. In sum, one should probably accept a 10 percent annual risk of disease among tuberculin-positive persons who become HIV infected and a 35 to 45 percent early disease risk among AIDS patients who acquire infection with M. tuberculosis. Appropriate treatment of latent infection in both groups should reduce these risks. Risk of Mortality Among American Health Care Workers with Tuberculosis Clinical trials of antituberculosis therapeutic regimens conducted in the United States and elsewhere beginning the 1950s demonstrated low mortality rates among adequately treated individuals. The only modern American data come from United States Public Health Service trial number 21, a multicentered national trial of modern drug treatment regimens. Nine deaths occurred among 1,451 participants, 0.6 percent (98). HIV
OCR for page 222
Tuberculosis in the Workplace status of the participants in this trial was not determined as part of the study and was generally unknown. One of the nine persons who died was known to be receiving treatment for AIDS at the time of death, however. Of the other eight, at least six were noncompliant or did not complete prescribed therapy because of drug toxicity. Moreover, the causes of death reported in this trial were taken from death certificates, which may not have reflected the true cause (L.Geiter, personal communication, December 2000). A large portion of individuals dying of tuberculosis have the diagnosis made at the time of death and hence do not receive therapy. Rieder and his colleagues examined this aspect of tuberculosis mortality in the United States for the years 1985 through 1988, a time period preceding the major explosion of both AIDS and multidrug-resistant tuberculosis in America (99). Overall, 5.1 percent of tuberculosis diagnosed nationwide in those years was recognized at the time of death. During those years, there were a total of 7,210 tuberculosis deaths in the United States (1). Rieder and coworkers identified 4,373 diagnoses made at death. This represents 60.7 percent of the total deaths due to tuberculosis for those years. Tuberculosis is not evenly distributed among Americans (1). About 23 or 24 percent occurs in individuals over the age of 65; presumably most of them are no longer in the work force. Nearly 60 percent occurs among the unemployed. Six percent of patients are inmates of correctional facilities; 6 percent are homeless; and 3 percent are residents of long-term-care facilities. Reduced access to health care among the homeless and the unemployed can be presumed to increase their risk of being diagnosed and treated late or not at all and, in turn, their risk of death from untreated tuberculosis. HIV infection and drug resistance increase the mortality risk. During the decade prior to the HIV epidemic, Goble and colleagues at a national referral hospital noted a rate of mortality of 20.1 percent (27/134) among patients with tuberculosis due to organisms resistant to both isoniazid and rifampin (100). Data from 466 patients with a culture positive for M. tuberculosis in New York City in April 1991 were assembled by Frieden and collaborators (62). Follow-up of these patients was achieved until death or for 14 months. The case fatality rate for patients with multidrug-resistant organisms who were HIV infected was 80 percent; for HIV-uninfected individuals it was 47 percent. In summary, the risk for immunocompetent individuals in the United States of dying from appropriately treated tuberculosis due to drug-susceptible organisms is vanishingly small. For health care workers it should be smaller than for the general population because they should have the advantages of more rapid diagnosis and institution of appropriate therapy
OCR for page 223
Tuberculosis in the Workplace and should not come from the malnourished, often homeless population that contributes substantially to national tuberculosis mortality. Summary of Risks of Tuberculous Disease and Mortality Among M. tuberculosis-Infected Health Care Workers In the surveillance studies cited above the methods of tuberculin skin testing, the completeness of follow-up, and the definitions of tuberculin positivity and of tuberculosis varied, and the rigor of examination for tuberculosis may also be open to challenge. Yet certain generalizations seem justified. First, the attack rates among tuberculin reactors is substantially lower than the oft-stated 10 percent. Even if risks observed during the first few years after infection are projected forward in linear fashion, it is hard to envision a cumulative risk as high as 10 percent. The lifetime risk estimates by Comstock and Edwards (93) suggest that perhaps 3 percent should be chosen; other studies suggest a rate closer to 5 percent. Next, although the risk cannot be converted to annual risk in any of them, it is apparent from these studies that the risk diminishes with the passage of time. In those studies in which age-specific data are presented, the risk among adults is greatest in the young adult, postpubertal years. This is the age when many individuals enter the health care workforce, but it is not representative of the many older health care workers. The disease risk is dramatically increased in immunocompromised individuals. The risk of tuberculosis in infected persons is substantially reduced by appropriate treatment of latent infection, and health care workers should be ideally situated for the use of such treatment. Tuberculosis mortality risk in immunocompetent health care workers with tuberculosis not due to multidrug-resistant organisms is probably close to zero. ACKNOWLEDGMENTS This review could not have been accomplished without the help of others whom the author wishes to acknowledge. The reference librarians at the Health Sciences and Allen Memorial Libraries of Case Western Reserve University were helpful in finding many of the articles reviewed here, including obtaining a few by interlibrary loan. Marilyn Field, Elizabeth Epstein, and Cara Christie of the Institute of Medicine were helpful in supplying additional background material. Amy Curtis and Eugene McCray at CDC kindly gave me permission to cite some of their unpublished work. Finally, I am grateful to the members and staff of the Institute of Medicine Committee on Regulating Occupational Exposure to Tuberculosis for helpful reviews of successive drafts of this paper.
OCR for page 224
Tuberculosis in the Workplace REFERENCES 1. Centers for Disease Control and Prevention. Reported Tuberculosis in the United States. Annual Reports. Centers for Disease Control and Prevention. Atlanta: 1999. 2. Sepkowitz KA. Tuberculosis and the health care worker: a historical perspective. Annals of Internal Medicine 1994; 120:71–79. 3. Bowden KM, McDiarmid MA. Occupationally acquired tuberculosis: what’s known. Journal of Occupational Medicine 1994; 36:320–325. 4. Markowitz SB. Epidemiology of tuberculosis among health care workers. Occupational Medicine 1994; 9:589–608. 5. McGowan JE Jr. Nosocomial tuberculosis: new progress in control and prevention. Clinical Infectious Diseases 1995; 212:489–505. 6. Menzies D, Fanning A, Yuan L, Fitzgerald M. Tuberculosis among health care workers. New England Journal of Medicine 1995; 332:92–98. 7. Sepkowitz KA. AIDS, tuberculosis, and the health care worker. Clinical Infectious Diseases 1995; 20:232–242. 8. Pugliese G, Tapper ML. Tuberculosis control in health care. Infections Control and Hospital Epidemiology 1996; 17:819–827. 9. Blumberg HM. Tuberculosis infection control. In Reichman LB, Hershfield ES (editors). Tuberculosis. A Comprehensive International Approach 2nd ed. New York: Marcel Dekker, Inc., 2000; pp.609–643. 10. Daniel TM, Debanne SM. Estimation of the annual risk of tuberculous infection for white men in the United States. Journal of Infectious Diseases 1997; 175:1535–1537. 11. Styblo K. The relationship between the risk of tuberculous infection and the risk of developing infectious tuberculosis. Bulletin of the International Union against Tuberculosis 1985; 60:117–119. 12. Engel A, Roberts J. Tuberculin skin test reaction among adults 25–74 years, 1971–1972. DREW publication no. (HRA) 77–1649. Washington, DC: U.S. Department of Health, Education, and Welfare, 1977. 13. World Health Organization. WHO report on the global tuberculosis epidemic 1998. Geneva, Switzerland: World Health Organization, 1998. 14. Rhoades ER, Alexander CP. Reactions to the tuberculin the test in Air Force recruits. American Review of Respiratory Diseases 1968; 98:837–841. 15. Trump DH, Hyams KC, Cross ER, Struewing JP. Tuberculosis infection among young adults entering the US Navy in 1990. Archives of Internal Medicine 1993; 153:211–216. 16. Reichman LB, O’Day R. Tuberculous infection in a large urban population. American Review of Respiratory Diseases 1978; 117:705–712. 17. Barnard MW, Amberson JB Jr, Loew MF. Tuberculosis in adolescents. A study of 1000 school-children in New York City made under the auspices of the Bellevue-Yorkville Health Demonstration in 1930. American Review of Tuberculosis 1931; 23:593–641. 18. Edwards LB, Smith DT. Community-wide tuberculin testing study in Pamlico County, North Carolina. American Review of Respiratory Diseases 1965; 92:43–54. 19. Rosenthal SR, Afremow ML, Nikurs L, Loewinsohn E, Leppmann M, Katele E, Live-right D, Thorne M. BCG vaccination and tuberculosis in students of nursing. American Journal of Nursing 1963; 63:88–93. 20. Edwards LB, Acquaviva FA, Livesay VT, Cross FW, Palmer CE. An atlas of sensitivity to tuberculin, PPD-B, and histoplasmin in the United States. American Review of Respiratory Diseases 1969; 99(suppl.):1–132. 21. Hanzel GD, Rogers KD. Multiple-puncture and Mantoux tuberculin tests in high school students. A comparative study. Journal of the American Medical Association 1964; 190:1038–1042. 22. Tuberculosis Program, National Communicable Disease Center, US DHEW PHS. Tuberculin testing in special tuberculosis projects 1966, 1967. Summary tables. Atlanta: Public Health Service, U.S. Department of Health, Education, and Welfare, 1968.
OCR for page 225
Tuberculosis in the Workplace 23. Vennema A, Ruggiero D. Tuberculin-sensitivity and risk of infection in New York City school children in 1980–81. Bulletin of the International Union against Tuberculosis 1984; 59:138–140. 24. McKenna MT, Hutton M, Cauthen G, Onorato IM. The association between occupation and tuberculosis. A population-based study. American Journal of Respiratory and Critical Care Medicine 1996; 154:587–593. 25. Bulletin of the National Tuberculosis and Respiratory Disease Association. 1969; 55:1–16. 26. Ruben FL, Norden CW, Schuster N. Analysis of a community hospital employee tuberculosis screening program 31 months after its inception. American Review of Respiratory Diseases 1977; 115:23–28. 27. Vogeler DM, Burke JP. Tuberculosis screening for hospital employees. A five-year experience in a large community hospital. American Review of Respiratory Diseases 1978; 117:227–232. 28. Berman J, Levin ML, Orr ST, Desi L. Tuberculosis risk for hospital employees: analysis of a five-year tuberculin skin testing program. American Journal of Public Health 1981; 71:1217–1222. 29. Aitken ML, Anderson KM, Albert RK. Is the tuberculosis screening program of hospital employees still required? American Review of Respiratory Diseases 1987; 136:805–807. 30. Louther J, Rivera P, Feldman J, Villa N, DeHovitz J, Sepkowitz KA. Risk of tuberculin conversion according to occupation among health care workers at a New York City hospital. American Journal of Respiratory and Critical Care Medicine 1997; 156:201–205. 31. Fella P, Rivera P, Hale M, Squires K, Sepkowitz K. Dramatic decrease in tuberculin skin test conversion rate among employees at a hospital in New York City. American Journal of Infection Control 1995; 23:352–356. 32. Maloney SA, Pearson ML, Gordon MT, Del Castillo R, Boyle JF, Jarvis WR. Efficacy of control measures in preventing nosocomial transmission of multidrug-resistant tuberculosis to patients and health care workers. Annals of Internal Medicine 1995; 122:90–95. 33. Blumberg HM, Watkins DL, Berschling JD, Antle A, Moore P, White N, Hunter M, Green B, Ray SM, McGowan JE. Preventing the nosocomial transmission of tuberculosis. Annals of Internal Medicine 1995; 122:658–663. 34. Sotir MJ, Khan A, Bock NN, Blumberg HM. Risk factors for tuberculin skin test (TST) positivity and conversion among employees at a public inner-city hospital in a high incidence area (abstract). Journal of Investigative Medicine 1997; 45:64A. 35. Blumberg HM, Sotir M, Erwin M, Bachman R, Shulman JA. Risk of house staff tuberculin skin test conversion in an area with a high incidence of tuberculosis. Clinical Infectious Diseases 1998; 27:826–833. 36. Sepkowitz KA, Friedman CR, Hafner A, Kwok D, Manoach S, Floris M. Martinez D, Sathianathan K, Brown E, Berger JJ, Segal-Maurer S, Kreiswirth B, Riley LW, Stoeckle MY. Tuberculosis among urban health care workers: a study using restriction fragment length polymorphism typing. Clinical Infectious Diseases 1995; 21:1098–1101. 37. Rattner SL, Fleischer JA, Davidson BL. Tuberculin positivity and patient contact in healthcare workers in the urban United States. Infection Control and Hospital Epidemiology 1996; 17:369–371. 38. Ball R, Van Wey M. Tuberculosis skin test conversion among health care workers at a military medical center. Military Medicine 1997; 162:338–343. 39. Boudreau AY, Baron SL, Steenland NK, Van Gilder TJ, Decker JA, Galson SK, Seitz T. Occupational risk of Mycobacterium tuberculosis infection in hospital workers. American Journal of Industrial Medicine 1997; 32:528–534. 40. Bailey TC, Fraser VJ, Spitznagel EL, Dunagan WC. Risk factors for a positive tuberculin skin test among employees of an urban, midwestern teaching hospital. Annals of Internal Medicine 1995; 122:580–585. 41. Fraser VJ, Kilo CM, Bailey TC, Medoff G, Dunagan WC. Screening of physicians for tuberculosis. Infection Control and Hospital Epidemiology 1994; 15:95–110.
OCR for page 226
Tuberculosis in the Workplace 42. Christie CD, Constantinou P, Marx ML, Willke MJ, Marot K, Mendez FL, Donovan J, Thole J. Low risk for tuberculosis in a regional pediatric hospital: nine-year study of community rates and the mandatory employee tuberculin skin-test program. Infection Control and Hospital Epidemiology 1998; 19:168–174. 43. Van Drunen N, Bonnicksen G, Pfeiffer AJ. A survey of tuberculosis control programs in seventeen Minnesota hospitals: implications for policy development. American Journal of Infection Control 1996; 24:235–242. 44. Managan LP, Bennett CL, Tablan N, Simonds DN, Pugilese G, Collazo E, Jarvis WR. Nosocomial tuberculosis prevention measures among two groups of US hospitals, 1992 to 1996. Chest 2000; 117:380–384. 45. U.S. Department of Labor. Occupational Safety and Health Administration. Occupational exposure to tuberculosis; proposed rule. Federal Register 1997; 62:54160–54308. 46. National Center for Health Statistics, Centers for Disease Control and Prevention, U.S. Department of Health and Human Services. An Overview of Nursing Homes and their Current Residents: Data from the 1995 National Nursing Home Survey. Atlanta: Centers for Disease Control and Prevention, 1997: pp.97–250. 47. Centers for Disease Control. Prevention and control of tuberculosis in facilities providing long-term care to the elderly. Recommendations of the Advisory Committee for Elimination of Tuberculosis. Morbidity and Mortality Weekly Report 1990; 39(RR-10):7– 13. 48. Hutton MD, Cauthen GM, Bloch AB. Results of a 29-state survey of tuberculosis in nursing homes and correctional facilities . Public Health Reports 1993; 108:305–314. 49. Stead WW. Tuberculosis among elderly persons: an outbreak in a nursing home. Annals of Internal Medicine 1981; 94:606–610. 50. Munger R, Anderson K, Leahy R, Allard J, Kobayashi JM. Tuberculosis in a nursing care facility—Washington. Morbidity and Mortality Weekly Report 1983; 32:121–128. 51. Price LE, Rutala WA. Tuberculosis screening in the long-term care setting. Infection Control 1987; 8:353–356. 52. Pelletier AR, DiFerdinando GT Jr, Greenberg AJ, Sosin DM, Jones WD Jr, Bloch AB, Woodley CL. Tuberculosis in a correctional facility. Archives of Internal Medicine 1993; 153:2692–2695. 53. Steenland K, Levine AJ, Sieber K, Schulte P, Aziz D. Incidence of tuberculous infection among New York State prison employees. American Journal of Public Health 1997; 87: 2012–2014. 54. Campbell R, Sneller V-P, Khoury N, Hinton B, DeSouza L, Smith S, Howard J, Ciofalo F, Welsh AL, Krycia W, Mycroft F, Hooper K, Goldman L, Royce S, Dorfman B, Morita S, Coulter S, Rutherford GW. Probable transmission of multidrug-resistant tuberculosis in a correctional facility—California. Morbidity and Mortality Weekly Report 1993; 42:48–51. 55. Prendergast T, Hwang B, Alexander R, Charron T, Lopez E, Culton J, Bick J, Shalaby M, Dewsnup D, Meyer H, Horowitz E, Khoury N, Mohle-Boetani J, Royce S, Chin D, Petrillo S, Miguelino V, Desmond E, Harrison R, Cone J, Greene C, Joseph M, Waterman S. Tuberculosis outbreaks in prison housing units for HIV-infected inmates— California, 1995–1996. Morbidity and Mortality Weekly Report 1999; 48:79–82. 56. Koo DT, Baron RC, Rutherford GW. Transmission of Mycobacterium tuberculosis in a California state prison, 1991. American Journal of Public Health 1997; 87:279–282. 57. Bergmire-Sweat D, Barnett BJ, Harris SL, Taylor JP, Mazurek GH, Reddy V. Tuberculosis outbreak in a Texas prison, 1994. Epidemiology and Infection 1996; 117:485–492. 58. Jones TF, Craig AS, Valway SE, Woodley CL, Schaffner W. Transmission of tuberculosis in a jail. Annals of Internal Medicine 1999; 131:557–563. 59. Johnsen C. Tuberculosis contact investigation: two years of experience in New York City correctional facilities. American Journal of Infection Control 1993; 21:1–4.
OCR for page 227
Tuberculosis in the Workplace 60. Erdil M, Stahl K. Prevalence of tuberculosis skin test reactivity in preplacement applicants to the Connecticut Department of Corrections from 1991 to 1992. Journal of Occupational Medicine 1993; 35:1178–1179. 61. Brudney K, Dobkin J. Resurgent tuberculosis in New York City. Human immunodeficiency virus, homelessness, and the decline of tuberculosis control programs. American Review of Respiratory Diseases 1991; 144:745–749. 62. Frieden TR, Sterling T, Pablos-Mendez A, Kilburn JO, Cauthen GM, Dooley SW. The emergence of drug-resistant tuberculosis in New York City. New England Journal of Medicine 1993; 328:521–526. 63. Nardell E, McInnis B, Thomas B, Weidhaas S. Exogenous reinfection with tuberculosis in a shelter for the homeless. New England Journal of Medicine 1986; 315:1570–1575. 64. Nolan CM, Elarth AM, Barr H, Saeed AM, Risser DR. An outbreak of tuberculosis in a shelter for homeless men. A description of its evolution and control. American Review of Respiratory Disease 143(2):257–261, 1991. 65. Barnes PF, El-Hajj H, Preston-Martin S, Cave MD, Jones BE, Otaya M, Pogoda J, Eisenach KD. Transmission of tuberculosis among the urban homeless. Journal of the American Medical Association 1996; 275:305–307. 66. Curtis AB, Ridzon R, Novick LF, Driscoll J, Blair D, Oxtoby M, McGarry M, Hiscox B, Faulkner C, Taber H, Valway S, Onorato IM. Analysis of Mycobacterium tuberculosis transmission patterns in a homeless shelter outbreak. International Journal of Tuberculosis and Lung Disease 2000; 4:308–313. 67. Layton MC, Cantwell MF, Dorsinville GJ, Valway SE, Onorato IM, Frieden TR. Tuberculosis screening among homeless persons with AIDS living in single-room-occupancy hotels. American Journal of Public Health 1995; 85:1556–1559. 68. Pierce JR, Sims SL, Holman GH. Transmission of tuberculosis to hospital workers by a patient with AIDS. Chest 1992; 101:581–582. 69. Hoch DE, Wilcox KR Jr. Transmission of multidrug-resistant tuberculosis from an HIV-positive client in a residential substance-abuse treatment facility—Michigan. Morbidity and Mortality Weekly Report 1991; 40:129–131. 70. Howell JT, Scheel WJ, Pryor VL, Tavris DR, Calder RA, Wilder MH. Mycobacterium tuberculosis transmission in a health clinic—Florida, 1988. Morbidity and Mortality Weekly Report 1989; 38:256–264. 71. Zahnow K, Matts JP, Hillman D, Finley E, Brown LS Jr, Torres RA, Ernst J, El-Sadr W, Perez G, Webster C, Barber B, Gordin FM. Rates of tuberculosis infection in healthcare workers providing services to HIV-infected populations. Infection Control and Hospital Epidemiology 1998; 19:829–835. 72. Prezant DJ, Kelly KJ, Mineo FP, Janus D, Karwa ML, Futterman N, Nolte C. Tuberculin skin test conversion rates in New York City Emergency Medical Service health care workers. Annals of Emergency Medicine 1998; 32:208–213. 73. Kao AS, Ashford DA, McNeil MM, Warren NG, Good RC. Descriptive profile of tuberculin skin testing programs and laboratory-acquired tuberculous infections in public health laboratories. Journal of Clinical Microbiology 1997; 35:1847–1851. 74. Ussery XT, Bierman JA, Valway SE, Seitz TA, DiFerdinando GT Jr, Ostroff SM. Transmission of multidrug-resistant Mycobacterium tuberculosis among persons exposed in a medical examiner’s office, New York. Infection Control and Hospital Epidemiology 1995; 16:160–165. 75. Gershon RRM, Vlahov D, Escamilla-Cejudo JA, Badawi M, McDiarmid M, Karkashian C, Grimes, M, Comstock GW. Tuberculosis risk in funeral home employees. Journal of Occupational Environmental Medicine 1998; 40:497–503. 76. Sterling TR, Pope DS, Bishai WR, Harrington S, Gershon RR, Chaisson RE. Transmission of Mycobacterium tuberculosis from a cadaver to an embalmer. New England Journal of Medicine 2000; 342:246–248.
OCR for page 228
Tuberculosis in the Workplace 77. Lauzardo M, Duncan H, Hale Y, Lee P. Transmission of Mycobacterium tuberculosis to a funeral director during routine embalming (abstract). American Journal of Respiratory and Critical Care Medicine 2000; 161:A299. 78. Price LE, Rutala WA, Samsa GP. Tuberculosis in hospital personnel. Infection Control 1987; 8:97–101. 79. Beck-Sague C, Dooley SW, Hutton MD, Otten J, Breeden A, Crawford JT, Pitchenik AE, Woodley C, Cauthen G, Jarvis WR. Hospital outbreak of multidrug-resistant Mycobacterium tuberculosis infections. Factors in transmission to staff and HIV-infected patients. Journal of the American Medical Association 1992; 268:1280–1286. 80. Panlilio AL, Burwen DR. Tuberculin skin testing surveillance of health-care workers (HCWS) (abstract). American Journal of Respiratory and Critical Care Medicine 1996; 153 (suppl):A133. 81. Sinkowitz RL, Fridkin SK, Managan L, Wenger PN, Jarvis WR. Status of tuberculosis infection control programs at United States Hospitals, 1989 to 1992. American Journal of Infection Control 1996; 24:226–234. 82. Ferebee SH. Controlled chemoprophylaxis trials in tuberculosis. A general review. Advances in Tuberculosis Research 1970; 17:28–106. 83. Myers JA, Bearman JE, Botkins AC. Natural history of tuberculosis in the human body. IX. Prognosis among students with tuberculin reaction conversion before, during and after medical school. Diseases of the Chest 1966; 50:120–132. 84. Myers JA, Bearman JE, Botkins AC. Natural history of tuberculosis in the human body. IX. Prognosis among students with tuberculin reaction conversion before, during and after school of nursing. Diseases of the Chest 1968; 53:687–698. 85. Sepkowitz KA. Tuberculin skin testing and the health care worker: lessons of the Prophit survey. Tuberculosis and Lung Disease 1996; 77:81–85. 86. Barrett-Connor E. The epidemiology of tuberculosis in physicians. Journal of the American Medical Association 1979; 241:33–38. 87. Edwards LB, Livesay VT, Acquaviva FA, Palmer CE. Height, weight, tuberculous infection, and tuberculous disease. Archives of Environmental Health 1971; 22:106–112. 88. Horwitz O, Wilbek E, Erickson PA. Epidemiologic basis of tuberculosis eradication. Bulletin of the World Health Organization 1969; 41:95–113. 89. Medical Research Council. BCG and vole bacillus vaccines in the prevention of tuberculosis in adolescence and early adult life. Bulletin World Health Organization 1972; 46:371–385. 90. Comstock GW. Community research in tuberculosis. Muscogee County, Georgia. Public Health Reports 1964; 79:1045–1056. 91. Comstock GW, Woolpert SH, Livesay VT. Tuberculosis studies in Muscogee County, Georgia. Twenty-year evaluation of a community trial of BCG vaccination. Public Health Reports 1976; 91:276–280. 92. Comstock GW, Livesay VT, Woolpert SF. The prognosis of a positive tuberculin reaction in childhood and adolescence. American Journal of Epidemiology 1974; 99:131–138. 93. Comstock GW, Edwards PQ. The competing risks of tuberculosis and hepatitis for adult tuberculin reactors. American Review of Respiratory Diseases 1975; 111:573–577. 94. Selwyn PA, Hartel D, Lewis VA, Schoenbaum EE, Vermund SH, Klein RS, Walker AT, Friedland GH. A prospective study of the risk of tuberculosis among intravenous drug users with human immunodeficiency virus infection. New England Journal of Medicine 1989; 320:545–550. 95. Selwyn PA, Sckell BM, Alcabes P, Friedland GH, Klein RS, Schoenbaum EE. High risk of active tuberculosis in HIV-infected drug users with cutaneous anergy. Journal of the American Medical Association 1992; 268:504–509. 96. Di Perri G, Cruciani M, Danzi MC, Luzatti R, De Checchi G, Malena M, Pizzighella S, Mazzi R, Solbiati M, Concia E, Bassetti D. Nosocomial epidemic of active tuberculosis among HIV-infected patients. Lancet 1989; 2:1502–1504.
OCR for page 229
Tuberculosis in the Workplace 97. Daley CL, Small PM, Schecter GF, Schoolnik GK, McAdam RA, Jacobs WR Jr, Hopewell PC. An outbreak of tuberculosis with accelerated progression among persons infected with the human immunodeficiency virus. New England Journal of Medicine 1992; 326: 231–235. 98. Combs DL, O’Brien RJ, Geiter LJ. USPHS tuberculosis short-course chemotherapy trial 21: effectiveness, toxicity, and acceptability. The report of final results. Annals of Internal Medicine 1990; 112:397–406. 99. Rieder HL, Kelly GD, Bloch AB, Cauthen GM, Snider DE Jr. Tuberculosis diagnosed at death in the United States. Chest 1991; 100:678–681. 100. Goble M, Iseman MD, Madsen RN-C, Waite D, Ackerson L, Horsburgh CR Jr. Treatment of 171 patients with pulmonary tuberculosis resistant to isoniazid and rifampin. New England Journal of Medicine 1993; 328:527–532.
Representative terms from entire chapter: