Address of Corresponding Author

Respiration 2005;72:431-446 (DOI: 10.1159/000086261)

 Outline

• Key Words
• Abstract
• Introduction
• Methods
• Results of the Evaluation of the Tuberculosis or Tuberculosis Infection Risk in Specific Occupations
• Health Care Workers (General)
• Nurses
• Physicians
• Laboratory Employees
• Funeral Home Employees
• Respiratory Therapists and Physiotherapists
• Non-Medical Hospital Employees
• Prison Employees
• Conclusion and Outlook
• References

• Author Contacts
• Article Information
• Publication Details
• Drug Dosage / Copyright

  Key Words

• Tuberculosis
• Occupational risk
• Epidemiologic studies

  Abstract

This review summarizes the epidemiological evidence for occupationally acquired tuberculosis and considers the implications for the prevention of tuberculosis. The relevant epidemiological studies were identified on the basis of the Medline data bank, starting with the year 1966. The evaluation of occupational groups with an elevated tuberculosis risk is exclusively based on epidemiologic studies of good or acceptable quality, applying clearly defined criteria of methodological quality. In summary, the availableepidemiological evidence suggests that the risk of tuberculosis is elevated in the following occupational groups: hospital employees in wards with tuberculosis patients; nurses in hospitals; nurses attending HIV-positive or drug-addicted patients; pathology and laboratory workers; respiratory therapists and physiotherapists; physicians in internal medicine, anaesthesia, surgery and psychiatry; non-medical hospital personnel in housekeeping and transport work; funeral home employees, and prison employees. However, the epidemiological evidence is limited for all these occupations, with the exception of the nurses, because of the lack of methodologically adequate studies that have got the statistical power to differentiate between specific work tasks. There is a need for large population-based studies with precise definition of exposure, which should include molecular epidemiologic methods in the investigation of occupational risk factors of tuberculosis.

Copyright © 2005 S. Karger AG, Basel

 Introduction

At the beginning of the 20th century, medical occupations were accompanied by a high risk of tuberculosis. The incidence of active tuberculosis was 35- to 50-fold higher in the medical occupations than in the general population [1]. Parallel to the general decrease in the frequency of tuberculosis in industrial countries, there was a tendency to ignore the question of the risk of health care workers. However, in the 1980s and early 1990s several nosocomial outbreaks of tuberculosis were observed, particularly in the eastern United States. These outbreaks often involved HIV-infected individuals, and the high proportion of multidrug-resistant tuberculosis strains was particularly worrying. These outbreaks drew attention to the danger of infection in the medical occupations. Many publications pointed out that employees of affected hospitals were at greatly increased risk of infection. Conversion of the tuberculin test could be documented in 20-50% of the susceptible hospital employees in the context of one of these tuberculosis outbreaks [2,3,4].

Outbreak reports can nevertheless not contribute much to the assessment of the probability of occupationally acquired tuberculosis in medical personnel. Of course, the infectious pathway is quite clear if an employee is involved in a tuberculosis outbreak. However, it is more difficult to clarify the causal relationship between occupation and tuberculosis when the employee in the medical occupation has no obvious contact with tuberculosis patients.

The present analysis of the epidemiological literature was intended to further clarify the occupational risk of tuberculosis in specific medical occupations and to identify tasks that entail a particularly high risk. The analysis includes cross-sectional studies, case-control studies, cohort studies and interventional studies related to tuberculosis morbidity and mortality or to the conversion of the tuberculin test. The identification of high-risk occupational groups has consequences for the prevention of tuberculosis and compensation of tuberculosis as an occupational disease.

 Methods

The relevant epidemiological studies were identified on the basis of the Medline data bank, starting with the year 1966. The key words entered were: 'tuberculosis' and ('nosocomial' or 'occupational' or 'employees' or 'nurses' or 'physicians' or 'technicians'). These key words had already been selected by Menzies et al. [5] in their review article on tuberculosis in health care workers. Additionally, we entered the key words 'tuberculosis' and ('health care workers' or 'HCW').

The methodological quality of the identified epidemiological studies was rated according to standardized criteria. These criteria were a priori derived from the critical methodical points formulated by Markowitz [6] in his review article on epidemiological studies. The following items were considered (table 1): size of the study, participation rate, selection of the comparison group, regularity and completeness of the tuberculin testing of the study participants, differentiation of occupations, quality of the statistical evaluation, adjustment of the study results for potential confounders (namely age, sex, country of origin, BCG vaccination, household contact with tuberculosis, socioeconomic status and - for hospital-based studies - the established protective measures in the hospitals involved). Each item was scored (table 1) and the quality of the study was assessed by the sum of the scores, the maximum being 10 points for studies on the risk of tuberculosis infection. The studies were subdivided into 'poor' studies (0-3.5 points), studies with 'acceptable' methodological quality (4-6.5 points), and 'good' studies (7-10 points).

Table 1. Summary of evaluation criteria

Two-step tuberculin testing has been recommended because a single tuberculin test may elicit little responseyet stimulate an anamnestic immune response so that a secondtest may elicit a muchlarger, or boosted, response. The performance of a two-step test procedure can raise the methodical quality of an epidemiological study [7,8,9]; however, there remains some doubt as to the necessity of a two-phase test procedure [10]. In our study evaluation, the performance of a two-phase test was not included in the overall evaluation, nor did the evaluation specify whether the standard tuberculin test [11] - the Mantoux intracutaneous test - was used or the 'stamp test', which is less sensitive and less specific [12]. Most studies used the intracutaneous test, although some [13, 14] also used the stamp test. It should be pointed out that these evaluation criteria should only be used for information. For example, a study with some minor methodical deficiencies might attain the same formal methodical quality as a study which cannot be reasonably interpreted because of a serious methodical error. It is important, in the final analysis, to consider the overall significance of the methodical advantages and disadvantages of each study. The classification of the methodical quality into 'inadequate', 'acceptable' and 'good' nevertheless makes it possible in most cases to arrive at a tenable assessment. However, one study, although formally classified as methodologically 'acceptable' [15], was excluded from the following review because of the inadequately operationalized comparison group and because of the low numbers of tuberculin test conversions (n = 30). All methodologically 'inadequate' studies [13,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52] were excluded from the following review. In this review, no statistical meta-analyses were performed, as there were large differences among the studies of adequate methodologic quality.

The aim was to arrive at a statement on the risk of occupational tuberculosis in regions of low tuberculosis incidence. For this reason, studies from regions with a tuberculosis incidence of above 50/100,000 and studies in hospitals with more than 50 tuberculosis patients per 10,000 admissions or in hospitals with 200 or more tuberculosis patients per year were excluded. We nonetheless believe that there is also a need for further analytical and interventional studies dealing with the problem of occupationally acquired tuberculosis in high-incidence areas, e.g. in Eastern Europe. Moreover, as the incidence of tuberculosis in immigrants in industrial countries is increased 10- to 20-fold [53,54,55], immigration of workers from high-incidence areas might raise both the occupational and the non-occupational risk of tuberculosis in Western industrialized countries. However, the methodologically adequate Canadian study conducted by Menzies et al. [56] reported no association between the proportion of immigrants at school or at the workplace and a positive tuberculin test.

 Results of the Evaluation of the Tuberculosis or Tuberculosis Infection Risk in Specific Occupations

The results of all methodologically acceptable and good studies are given in detail in table 2 (Studies on the risk of a positive tuberculin test) and table 3 (Studies on tuberculosis morbidity and mortality). The interpretation of tuberculosis infection studies must take into consideration limitations in the accuracy of the tuberculin test procedure itself [57,58,59]. Moreover, false-positive test results in BCG-vaccinated persons might influence the study results [60] even if adjusted for BCG vaccination. However, our analysis does not point to systematic differences between the results of infection studies and those of studies referring to clinically manifest tuberculosis. Therefore studies on infection rates and those on clinically manifest tuberculosis were combined in the following summary of the occupation-specific risks.

Table 2. Epidemiological studies on the frequency of a positive tuberculin test or tuberculin test conversion

Table 3. Epidemiological studies on the risk of clinical tuberculosis disease

 Health Care Workers (General)

Epidemiological studies often do not apply to specific medical occupational groups, but calculate the risk of infection or disease for the overall group of health care workers. The methodologically good prospective conversion study and methodologically acceptable prevalence study of Schwartzman et al. [61] reported a significantly and markedly increased infection risk for health care workers. The relative risk estimate for medical personnel is 13.6 in the cohort study and 2.6 in the cross-sectional study. On the other hand, the study of McKenna et al. [62] found no evidence for an association between health care work in general and clinically manifest tuberculosis. A possible explanation for the lack of epidemiological evidence for an association between health care work in general and tuberculosis infection or disease may be attributed to the highly heterogeneous definition of 'health care work', which includes both occupational groups with a potentially increased risk and groups without any contact with tuberculosis patients.

However, the criterion 'frequency of patient contacts' is of only limited use for the identification of employees at increased risk of disease. Unfortunately, no epidemiological studies of high methodological quality deal with this question. In the very small study of Liss et al. [63] (n = 18 tuberculin conversions), the relationship between the frequency of patient contacts and tuberculosis infection or disease approached statistical significance. In the cross-sectional study conducted by Bailey et al. [64], the tuberculin conversion rate of employees with frequent patient contacts was slightly increased. On the other hand, Raad et al. [65] even found a negative association between the frequency of patient contacts and tuberculosis infection or disease. However, the latter result is likely to be explained by the choice of an inappropriate comparison group and by confounding. All reviewed epidemiological studies detected an association between work on wards with tuberculosis patients and tuberculosis infection and disease [63,66,67,68]. Relative risk estimates range from 2.1 [68] to 10.3 [67]. The study of Menzies et al. [66] detected no increased risk for contact with patients with initially missed diagnosis. This result was qualified by a later evaluation of the same study by Greenaway et al. [69], including the participation of Menzies. According to this publication, the risk of infection for hospital employees is associated with delayed diagnosis and treatment. In the hospitals studied, as the rate of tuberculosis admissions decreased, the likelihood of delayed diagnosis and risk of transmission of tuberculosis infection per hospitalized patient with tuberculosis increased. Despite the apparent (and only partially comprehensible) discrepancies between the published results of this research group, this study indicates that professional experience in the management of tuberculosis might, to a certain extent, protect from occupationally acquired tuberculosis infections.

 Nurses

The methodologically good or acceptable studies on the occupational risk of tuberculosis of nurses give a largely consistent picture. All epidemiologically good [61, 66, 70, 71] and acceptable studies [14, 70,72,73,74,75] on this question reveal an increased risk of tuberculosis for nurses. Relative risk estimates for nurses range from 1.7 [73] to 32.7 [61]. In the study conducted by Hill et al. [70] in England and Wales, the risk of tuberculosis is elevated only for white nurses. According to this study, reactivation of an earlier acquired infection might play a more important role in foreign-born health care workers than occupation; however, this is rather speculative. In the mortality study conducted by the American Centers for Disease Control and Prevention, the proportional mortality rates are significantly increased solely for white male nurses, the corresponding risk estimates for black men, white women and black women are non-significantly decreased [72]. Another study reported no statistically elevated risk of tuberculosis disease for nurses, in contrast to nursing aids, orderlies, and attendants [62]. As the number of relevant studies is low, it is difficult to assess the risk for specific nursing tasks. Only one study deals with the infection risk of nurses in internal medicine; this study reveals a clearly and significantly elevated risk [76]. However, the ward for internal medicine in that study was near the HIV ward, so the increased risk is not unambiguously due to the patients treated in the ward for internal medicine. In the study conducted by Schwartzman et al. [61], the elevated infection risk among surgical nurses was ascribed to inadequate ventilation of the surgical units as well as delayed diagnosis. Two studies [76,77] found an association between the tuberculosis infection risk and the care of HIV-positive patients. The increased risk in the latter study was found to be related to the pentamidine aerosol treatment of HIV patients. In their combined cross-sectional and cohort study on employees attending HIV-positive patients, Zahnow et al. [78] found a statistically significant association between infection rate and work in a drug program. Only a single study relating to work in an emergency ward reported a significant and clearly increased risk of infection before the introduction of adequate protective measures [79].

 Physicians

The methodologically good study of Meredith et al. [ 71] reported a significantly 2.7-fold increased tuberculosis risk for physicians. However, the picture is not as consistent as with nurses, as one methodologically good study [70] and a methodologically acceptable study [73] found no association between work as a physician and the risk of tuberculosis infection or disease; one methodologically acceptable study even found a negative association [62]. However, in the latter study, socioeconomic status was not included in the analysis as a confounder. Because of the inadequate data, it is difficult to evaluate the tuberculosis risk in different medical specialties. One study found an increased infection risk for specialists in internal medicine, anaesthesists, surgeons and psychiatrists [80].The study of Christie et al. [81 ] found no increased risk of infection for paediatricians. The study of Berman et al. [82] conducted in a general hospital in Baltimore reported a significantly lower infection risk for radiologists than for maintenance and engineering, housekeeping, or laundry employees. In their cross-sectional study, Plitt et al. [83 ] found a significant association between a positive tuberculin test and work in respiratory medicine, general surgery, or internal medicine.

 Laboratory Employees

The risk of tuberculosis in the dissecting room has been an issue for centuries [84]. In a review on occupationally acquired infections of health care workers, Sepkowitz [85] throws light on tuberculosis infections in pathologists and laboratory workers. An overall examination of the epidemiological studies involving pathologists and laboratory employees gives the following picture: Most of the studies that have been carried out on this subject, none of which are methodologically good, found an elevated risk of tuberculosis for pathological work. Three studies of acceptable quality reveal a statistically significant association between work in pathology and tuberculosis infection: Ussery et al. [86] reported an elevated conversion risk for employees who had participated in autopsies of persons with multidrug-resistant tuberculosis. In the small hospital-based study conducted by Menzies et al. [87], the tuberculin conversion risk was significantly elevated for pathology employees in comparison with non-clinical employees. Kralj et al. [14] found a significantly increased prevalence of infection in the department of pathology, but they did not give any risk estimates. One cross-sectional study found a non-significant relative risk of having a positive tuberculin test [78]. No association between laboratory work and tuberculosis infection was found in the small study of Menzies et al. [87].

Taken together, the epidemiological evidence suggests that the tuberculosis risk is increased for pathologists. There is also some epidemiologic evidence for a relationship between laboratory work and tuberculosis infection. It should however be pointed out that, firstly, there is a lack of methodologically high-quality studies and, secondly, that an overall statement on laboratory work is problematical. It would be preferable to relate the risk of tuberculosis to discrete tasks, in particular to work with infectious material.

 Funeral Home Employees

Two methodologically acceptable epidemiological studies deal with the specific infection risk for funeral home employees: The study of Gershon et al. [ 88] found a positive association between embalming bodies and the infection risk. The study of McKenna et al. [62 ] - which did not include socioeconomic status as a potential confounder - found an increased risk of tuberculosis for funeral directors in spite of their high social status.

 Respiratory Therapists and Physiotherapists

All studies surveyed found that employees working in respiratory or inhalation therapy had an increased tuberculosis risk. This applies to two studies of high methodological quality [61] (conversion study), [ 66] and to two methodologically acceptable studies [61] (cross-sectional study), [ 62]. The relative risk estimates for respiratory therapists range between 2.9 and 14.9. Only the methodologically good study of Menzies et al. [66 ] included physiotherapists; this study reported a significantly increased infection risk of 3.3.

 Non-Medical Hospital Employees

When evaluating the risk of tuberculosis for non-medical hospital employees it is particularly important to bear in mind the methodological quality of the epidemiological studies, as especially methodologically inadequate studies are open to bias introduced by social and cultural confounding factors. The only methodologically adequate study indicated that the risk of infection for housekeeping personnel was significantly and clearly raised [66]. There was also a significant and clear increase in risk in the study of Dooley et al. [76], although the housekeepers are only considered together with the escorts and maintenance workers. One study found an association between transport personnel (in hospital) and tuberculosis infection [64]. Only a single study dealt specifically with the infection risk of employees in the laundry [82]; this study found a significantly and markedly increased conversion rate. Kitchen personnel has also been the subject of a single study [14]; this study found a significantly elevated infection risk.

 Prison Employees

The cross-sectional study conducted by Jochem et al. [89 ] found a positive association between workasaprison employee(however only in men's prisons) and tuberculosis infection.

 Conclusion and Outlook

The results of the present analysis agree to a large extent with the recommendations of the OSHA (US Occupational and Health Administration) dealing with work-related tuberculosis risks in the USA [90]. In summary, the availableepidemiological evidence suggests that the risk of tuberculosis is elevated in the following occupational groups:

hospital employees in wards with tuberculosis patients;

nurses in hospitals;

nurses of HIV-positive or drug-addicted patients;

pathology and laboratory workers;

respiratory therapists and physiotherapists;

physicians in internal medicine, anaesthesia, surgery and psychiatry;

non-medical hospital personnel in housekeeping and transport work;

funeral home employees, and

prison employees.

It should nevertheless be pointed out that the epidemiological evidence is limited for all these occupations, with the exception of the nurses, as only a small number of studies can be regarded as being of adequate methodological quality. Moreover, few studies have got the statistical power to differentiate between specific tasks. Therefore, further epidemiologic research should address specifically defined tasks rather than roughly defined occupational groups as, for example, 'nurses'.

Differences in task-specific risk estimators of health care workers might, on the one hand, reflect methodological shortcomings. However, we have tried to minimize this potential bias by excluding methodologically inadequate studies from our review. On the other hand, the differences in the reported task-specific risk estimators might be partially explained by regional, individual, and workplace-specific factors that are difficult to measure in epidemiologic studies, e.g. regional differences in health-seeking behaviour of tuberculosis patients, professional experience of health care workers, hospital-specific spacious conditions and protective equipment, and hospital-specific case management procedures. Further epidemiologic studies should more specifically address these potentially risk-modifying factors to develop more purposeful and efficient prevention strategies for occupationally acquired tuberculosis.

Our finding of elevated risks in specific occupational groups rather raises the question of enforced protective efforts to prevent health care workers from contracting tuberculosis. Unfortunately only a few epidemiologic studies address the preventive potential of protective measures. In the methodologically high-quality study of Menzies et al. [66], inadequate ventilation in 'general' sick-rooms, defined as less than two exchanges of air per hour, was statistically significantly associated with tuberculin conversions. In the methodologically acceptable study of Behrman and Shofer [79], the conversion rates in the emergency department could be lowered from 12% per year to 0% by the introduction of specific protective measures. These measures include setting up isolation rooms in the emergency department, prevention of recirculation of air, improved ventilation in the whole emergency department, and improved personal protective measures.

In accordance with the recommendations of the OSHA [90,] the authors recommend to perform periodical tuberculin testing for all employees in the mentioned occupational groups even in Western European areas with a low incidence of tuberculosis. This procedure would not only enhance the early detection of infected individuals, but would also improve the data basis for in-depth epidemiologic analyses of task-specific infection risks. However, we cannot conclude from the epidemiologic evidence that it is necessary to conduct this testing annually in low-incidence areas.

A decreased incidence of tuberculosis in the general population may lead to reduced professional experience in health care workers. As a consequence, the likelihood of delayed diagnosis and the risk of transmission of tuberculosis infection per hospitalized patient with tuberculosis might increase. Therefore, we would like to emphasize the importance of regular information and training measures concerning protective measures as well as the diagnosis and treatment of tuberculosis. Early recognition, efficient treatment and isolation of patients with tuberculosis are key issues regarding the prevention of work-related tuberculosis [91,92,93,94,95,96]. A patient with lung tuberculosis should be instructed about coughing hygiene and should wear a surgical mask. Particular emphasis should be laid on the ventilation of the isolation room. Re-circulation of contaminated air should be avoided, the air stream should be redirected into the isolation room or outside. When a ventilation system is used, the air change rate should be at least 4-6 times per hour [94, 95, 97]. The hospital staff should wear masks during the treatment of infectious patients. A surgical mask is considered to be ineffective because of the leakage and the small particle filtration effect [98]. A mask with a filter capacity of 95% for particles with a diameter of 1 µm and a leakage rate of less than 10% is recommended in the US and Canada [94, 99]. These requirements are fulfilled by the FFP 2 (Filtering Face Pieces) mask, recommended in different European countries [95, 100]. The FFP 2 mask has a leakage rate of no more than 11% for particles with a diameter of 0.6 µm [101]. While dealing with multi-drug resistant tuberculosis or in special infectious situations (like bronchoscopy), FFP 3 masks (leakage rate 5%) or even the use of respirators might be considered [102].

Moreover, there is a need for improved strategies for contact tracing that avoids ineffective procedures and allows a better-targeted identification of cases. As several studies have shown that conventional contact tracing is an unreliable procedure [103,104,105], those traditional methods of contact tracing should be complemented by new molecular biology methods. The use of molecular biology 'fingerprint' analyses is expected to enlarge the epidemiologic knowledge concerning occupationally acquired tuberculosis. A promising perspective is offered by the study of Sepkowitz et al. [106], which combines new molecular epidemiologic methods with conventional epidemiologic methods. Molecular biological 'fingerprint' analyses are used to separate tuberculosis patients who belong to a chain of recent transmission from patients with endogenously reactivated tuberculosis (for an overview of the molecular epidemiology of tuberculosis transmission, please see Seidler et al. [107]). The study of Sepkowitz et al. [106] indicates that the risk of recent tuberculosis transmission may possibly be clearly increased in health care workers. It would seem to be a promising approach to improve the precision of occupational risk assessment by performing large population-based studies with differentiated data collection on occupational exposure and combining the methods of conventional epidemiology and molecular epidemiology.

The identification of high-risk occupational groups even in low-incidence areas might have consequences not only for preventive matters, but also for compensation practice. In Germany, until a short while ago, tuberculosis was only recognized as an occupational disease if the source of infection could be definitely identified. Against the backdrop of the reported epidemiologic evidence, an expert group has recommended to drop this general claim of a concrete infection source in specific high-risk occupations [108].

  References

1.

Sepkowitz KA: Tuberculosis and the health care worker: A historical perspective. Ann Intern Med 1994;120:71-79.

2.

Pearson ML, Jereb JA, Frieden TR, Crawford JT, Davis BJ, Dooley SW, Jarvis WR : Nosocomial transmission of multidrug-resistant Mycobacterium tuberculosis. A risk to patients and health care workers. Ann Intern Med 1992;117:191-196.

3.

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. JAMA 1992;268:1280-1286.

4.

Sepkowitz KA: Occupationally acquired infections in health care workers. Part I. Ann Intern Med 1996a;125:826-834.

5.

Menzies D, Fanning A, Yuan L, Fitzgerald M: Tuberculosis among health care workers. N Engl J Med 1995;332:92-98.

6.

Markowitz SB: Epidemiology of tuberculosis among health care workers. Occup Med 1994;9:589-608.

7.

Sepkowitz KA, Feldman J, Louther J, Rivera P, Villa N, DeHovitz J: Benefit of two-step PPD testing of new employees at a New York City hospital. Am J Infect Control 1997;25:283-286.

8.

Sherman RA, Shimoda KJ: Tuberculosis tracking: Determining the frequency of the booster effect in patients and staff. Am J Infect Control 2001;29:7-12.

9.

Horowitz HW, Luciano BB, Kadel JR, Wormser GP: Tuberculin skin test conversion in hospital employees vaccinated with bacille Calmette-Guérin: Recent Mycobacterium tuberculosis infection or booster effect? Am J Infect Control 1995;23:181-187.

10.

Hallak KM, Schenk M, Neale AV: Evaluation of the two-step tuberculin skin test in health care workers at an inner-city medical center. J Occup Environ Med 1999;41:393-396.

11.

Ferlinz R: Tuberkulindiagnostik. Gesundheitswesen 1996;58:657-665.

12.

Hofmann F, Grundmann HJ, Walcher J: Zur Aussagefähigkeit von Tuberkulinstempeltests. Öff Geswes 1989;51:359-351.

13.

Kralj N, Hofmann F, Michaelis M: Zur Bedeutung der Tuberkulose und der Tuberkulinkonversion bei Beschäftigten im Gesundheitsdienst. Immun Infekt 1997:60-64.

14.

Kralj N, Hofmann F, Michaelis M: Zur Methodik der Tuberkulosefrüherkennung bei arbeitsmedizinischen Vorsorgeuntersuchungen im Gesundheitsdienst. Arbmed Sozmed Umweltmed 1997;32:50-54.

15.

Panlilio AL, Burwen DR, Curtis AB, Srivastava PU, Bernardo J, Catalano MT, Mendelson MH, Nicholas P, Pagano W, Sulis C, Onorato IM, Chamberland ME: Tuberculin skin testing surveillance of health care personnel. Clin Infect Dis 2002;35:219-227.

16.

Arbelaez MP, Ocampo MC, Montoya J, Jaramillo LM, Giraldo PM, Maldonado A, Cano E, Mejia OA, Garcia LF, Garcia LF: Evaluación de la repuesta a la tuberculina en estudiantes del área de la salud. Rev Panam Salud Publica 2000;8:272-279.

17.

Ball R, Van Wey M: Tuberculosis skin test conversion among health care workers at a military medical center. Mil Med 1997;162:338-343.

18.

Barrett-Connor E: The epidemiology of tuberculosis in physicians. JAMA 1979;241:33-38.

19.

Capewell S, Leaker AR, Leitch AG: Pulmonary tuberculosis in health service staff - is it still a problem? Tubercle 1988;69:113-118.

20.

Cooper-Arnold K, Morse T, Hodgson M, Pettigrew C, Wallace R, Clive J, Gasecki J: Occupational tuberculosis among deputy sheriffs in Connecticut: A risk model of transmission. Appl Occup Environ Hyg 1999;14:768-776.

21.

Cuhadaroglu C, Erelel M, Tabak L, Kilicaslan Z: Increased risk of tuberculosis in health care workers: A retrospective survey at a teaching hospital in Istanbul, Turkey. BMC Infect Dis 2002;2:14.

22.

DiPerri G, Cadeo GP, Castelli F, Miccioli R, Bassetti S, Rubini F, Cazzadori A, Marocco S, Carlotto A, Adami T, Vento S, Malena M, Carosi G, Concia E, Bassetti D: Transmission of HIV-associated tuberculosis to healthcare workers. Infect Control Hosp Epidemiol 1993;14:67-72.

23.

Doody MM, Mandel JS, Linet MS, Ron E, Lubin JH, Boice JD Jr, Fraumeni JF Jr: Mortality among Catholic nuns certified as radiologic technologists. Am J Ind Med 2000;37:339-348.

24.

Fridkin SK, Manangaan E, Bolyard E, Jarvis WR: SHEA-CDC TB survey. I. Status of TB infection control programs at member hospitals, 1989-1992. Infect Control Hosp Epidemiol 1995a;16:129-134.

25.

Fridkin SK, Manangaan E, Bolyard E, Jarvis WR: SHEA-CDC TB survey. II. Efficacy of TB infection control programs at member hospitals, 1989-1992. Infect Control Hosp Epidemiol 1995b;16:135-140.

26.

Geiseler PJ, Nelson KE, Crispen RG, Moses VK: Tuberculosis in physicians: A continuing problem. Am Rev Respir Dis 1986;133:773-778.

27.

Harrington JM, Shannon HS: Incidence of tuberculosis, hepatitis, brucellosis, and shigellosis in British medical laboratory workers. Br Med J 1976;i:759-762.

28.

Hofmann F, Schrenk C, Kleimeier B: Zum Tuberkuloserisiko von Beschäftigten im Gesundheitsdienst. Öff GesundhWes 1990;52:177-180.

29.

Holzman RS: A comprehensive control program reduces transmission of tuberculosis (TB) to hospital staff. Clin Infect Dis 1995;21:733.

30.

Ktsanes VK, Williams WL, Boudreaux VV: The cumulative risk of tuberculin skin test conversion for five years of hospital employment. Am J Public Health 1986;76:65-67.

31.

Langille DB, Sweet LE: Tuberculin skin testing in a hospital and two chronic care facilities in Prince Edward Island. Can J Infect Control 1995;10:41-44.

32.

Lunn JA, Mayho V: Incidence of pulmonary tuberculosis by occupation of hospital employees in the National Health Service in England and Wales 1980-84. J Soc Occup Med 1989;39:30-32.

33.

Malasky C, Jordan T, Potulski F, Reichman LB: Occupational tuberculous infections among pulmonary physicians in training. Am Rev Respir Dis 1990;142:505-507.

34.

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. Ann Intern Med 1995;122:90-95.

35.

Manangan LP, Bennett CL, Tablan N, Simonds DN, Pugliese G, Collazo E, Jarvis WR: Nosocomial tuberculosis prevention measures among two groups of US hospitals, 1992 to 1996. Chest 2000;117:380-384.

36.

Marena C, Marone P, Gervino D, Azzaretti S, La Nave M, Togni CL: Tuberculosis among health care workers at San Matteo Hospital, 1985-1994 (abstract). Infect Contr Hosp Epidemiol 1996;17:P17.

37.

Marena C, Mangiarotti P, Manara G, Gervino D, Lodi R, Barone A, La Nave M, Maganuco S, Azzaretti S, Marone P (abstract): Occupational tuberculosis infections among health care personnel. Eleven years experience in a large university hospital. Eur Respir J 1996b;9(suppl 23):176S.

38.

Mendelson MH, Finkelstein L, Szulc T, Solomon R, Mancini L, Solomon J, Meyers B, Adler J, Hirschman S: Prospective surveillance of tuberculosis (TB) infection in high risk (HR) health care workers (HCWs) at a New York City medical center (1992-1995). Infect Control Hosp Epidemiol 1996;17:P17.

39.

Mikitka D, Mills SE, Dazey SE, Gabriel ME: Tuberculosis infection in US Air Force dentists. Am J Dent 1995;8:33-36.

40.

Müller HE: Risikofaktoren und Risikoabschätzungen in Tuberkuloselaboratorien. Laboratoriumsmedizin 1988;12:284-289.

41.

Pleszewski B, FitzGerald JM: Tuberculosis among health care workers in British Columbia. Int J Tuberc Lung Dis 1998;2:898-903.

42.

Raitio M, Tala E: Tuberculosis among health care workers during three recent decades. Eur Respir J 2000;15:304-307.

43.

Vogeler DM, Burke JP: Tuberculosis screening for hospital employees. A five-year experience in a large community hospital. Am Rev Respir Dis 1978;117:227-232.

44.

Ramphal-Naley L, Kirkhorn S, Lohman WH, Zelterman D: Tuberculosis in physicians: Compliance with surveillance and treatment. Am J Infect Control 1996;24:243-253.

45.

Riley M, Loughrey CM, Wilkinson P, Patterson CC, Varghese G: Tuberculosis in health service employees in Northern Ireland. Respir Med 1997;91:546-550.

46.

Rosenman KD, Hall N: Occupational risk factors for developing tuberculosis. Am J Ind Med 1996;30:148-154.

47.

Ruben FL, Norden CW, Schuster N: Analysis of a community hospital employee tuberculosis screening program 31 months after its inception. Am Rev Respir Dis 1977;115:23-28.

48.

Snider DE Jr, Cauthen GM: Tuberculin skin testing of hospital employees: Infection, 'boosting', and two-step testing. Am J Infect Control 1984;12:305-311.

49.

Wagner M: Tuberkulinkonversionsrate bei längerbeschäftigtem Personal eines Universitätsklinikums im Zeitraum von 1975 bis 1985. Zbl Bakt Hyg B 1987;184:87-94.

50.

Casas X, Ruiz-Manzano J, Casa I: Tuberculosis en personal sanitario de un hospital general (in Spanish). Med Clin (Barc) 2004;122:741-743.

51.

Cook S, Maw KL, Munsiff SS, Fujiwara PI, Frieden TR: Prevalence of tuberculin skin test positivity and conversions among healthcare workers in New York City during 1994 to 2001. Infect Control Hosp Epidemiol 2003;24:807-813.

52.

Garber E, San Gabriel P, Lambert L, Saiman L: A survey of latent tuberculosis infection among laboratory healthcare workers in New York City. Infect Control Hosp Epidemiol 2003;24:801-806.

53.

McKenna MT, McCray E, Onorato I: The epidemiology of tuberculosis among foreign-born persons in the United States. 1986-1993. N Engl J Med 1995;332:1071-1076.

54.

Gaudette L, Ellis E: Tuberculosis in Canada: A focal disease requiring distinct control strategies for different risk groups. Tuberc Lung Dis 1993;74:244-253.

55.

Thomas RE, Gushulak B: Screening and treatment of immigrants and refugees to Canada for tuberculosis: Implications of the experience of Canada and other industrialized countries. Can J Infect Dis 1995;6:246-255.

56.

Menzies D, Chan CH, Vissandjee B: Impact of immigration on tuberculosis infection among Canadian-born schoolchildren and young adults in Montreal. Am J Respir Crit Care Med 1997;156:1915-1921.

57.

Kendig EL, Kirkpatrick BV, Carter WH, Hill FA, Caldwell K, Entwistle M: Underreading of the tuberculin skin test reaction. Chest 1998;113:1175-1177.

58.

Rieder HL: Methodological issues in the estimation of the tuberculosis problem from tuberculin surveys. Tuberc Lung Dis 1995;76:114-121.

59.

Bass JB: How good is the tuberculin skin test (editorial)? Infect Control Hosp Epidemiol 2003;24:797-798.

60.

Wang L, Turner MO, Elwood RK, Schulzer M, FitzGerald JM: A meta-analysis of the effect of bacille Calmette-Guérin vaccination on tuberculin skin test measurements. Thorax 2002;57:804-809.

61.

Schwartzman K, Loo V, Pasztor J, Menzies D: Tuberculosis infection among health care workers in Montreal. Am J Respir Crit Care Med 1996;154:1006-1012.

62.

McKenna MT, Hutton M, Cauthen G, Onorato IM: The association between occupation and tuberculosis. A population-based survey. Am J Respir Crit Care Med 1996;154:587-593.

63.

Liss GM, Khan R, Koven E, Simor AE: Tuberculosis infection among staff at a Canadian community hospital. Infect Control Hosp Epidemiol 1996;17:29-35.

64.

Bailey TC, Fraser VJ, Spitznagel EL, Dunagan WC: Risk factors for a positive tuberculin skin test among employees of an urban, midwestern teaching hospital. Ann Intern Med 1995;122:580-585.

65.

Raad I, Cusick J, Sherertz RJ, Sabbagh M, Howell N: Annual tuberculin skin testing of employees at a university hospital: A cost-benefit analysis. Infect Control Hosp Epidemiol 1989;10:465-469.

66.

Menzies D, Fanning A, Yuan L, FitzGerald JM: Hospital ventilation and risk for tuberculous infection in Canadian health care workers. Canadian Collaborative Group in Nosocomial Transmission of TB. Ann Intern Med 2000;133:779-789.

67.

Boudreau AY, Baron SL, Steenland NK, Van Gilder TJ, Decker JA, Galson SK, Seitz T: Occupational risk of Mycobacterium tuberculosis infection in hospital workers. Am J Ind Med 1997;32:528-534.

68.

Zarzuela Ramirez M, Dona CJA, Milla EP, Benitez E, Pujolar AE, Fernandez FJL: Influencia del criterio de análisis sobre la incidencia y los factores de riesgo de conversión tuberculínica en personal sanitario. Med Clin (Barc) 2000;114:493-495.

69.

Greenaway C, Menzies D, Fanning A, Grewal R, Yuan L, FitzGerald JM, The Canadian Collaborative Group in Nosocomial Transmission of Tuberculosis: Delay in diagnosis among hospitalized patients with active tuberculosis - predictors and outcomes. Am J Respir Crit Care Med 2002;165:927-933.

70.

Hill A, Burge A, Skinner C: Tuberculosis in National Health Service hospital staff in the west Midlands region of England, 1992-5. Thorax 1997;52:994-997.

71.

Meredith S, Watson JM, Citron KM, Cockcroft A, Darbyshire JH: Are healthcare workers in England and Wales at increased risk of tuberculosis? BMJ 1996;313:522-525.

72.

Centers for Disease Control and Prevention CDC: Proportionate mortality from pulmonary tuberculosis associated with occupations - 28 states, 1979-1990. MMWR Morb Mortal Wkly Rep 1995;44:14-19.

73.

Stuart RL, Bennett NJ, Forbes AB, Grayson ML: Assessing the risk of tuberculosis infection among healthcare workers: the Melbourne Mantoux Study. Melbourne Mantoux Study Group. Med J Aust 2001;174:569-573.

74.

Lainez RM, Consul M, Olona M, Martinez-Ballarin JI, Miravitlles M, Vidal R : Infección tuberculosa en estudiantes de enfermería. Prevalencia y virajes durante 3 anos de seguimiento. Med Clin (Barc) 1999;113:685-689.

75.

Burrill D, Enarson DA, Allen EA, Grzybowski S: Tuberculosis in female nurses in British Columbia: Implications for control programs. Can Med Assoc J 1985;132:137-140.

76.

Dooley SW, Villarino ME, Lawrence M, Salinas L, Amil S, Rullan JV, Jarvis WR, Bloch AB, Cauthen GM: Nosocomial transmission of tuberculosis in a hospital unit for HIV-infected patients. JAMA 1992;267:2632-2634.

77.

Calder RA, Duclos P, Wilder MH, Pryor VL, Scheel WJ: Mycobacterium tuberculosis transmission in a health clinic. Bull Int Union Tuberc Lung Dis 1991;66:103-106.

78.

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. Terry Beirn Community Programs for Clinical Research on AIDS. Infect Control Hosp Epidemiol 1998;19:829-835.

79.

Behrman AJ, Shofer FS: Tuberculosis exposure and control in an urban emergency department. Ann Emerg Med 1998;31:370-375.

80.

Warren DK, Foley KM, Polish LB, Seiler SM, Fraser VJ: Tuberculin skin testing of physicians at a midwestern teaching hospital: A 6-year prospective study. Clin Infect Dis 2001;32:1331-1337.

81.

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. Infect Control Hosp Epidemiol 1998;19:168-174.

82.

Berman J, Levin ML, Orr ST, Desi L: Tuberculosis risk for hospital employees: Analysis of a five-year tuberculin skin testing program. Am J Public Health 1981;71:1217-1222.

83.

Plitt SS, Soskolne CL, Fanning A, Newman SC: Prevalence and determinants of tuberculin reactivity among physicians in Edmonton, Canada: 1996-1997. Int J Epidemiol 2001;30:1022-1028.

84.

Collins CH, Grange JM: Tuberculosis acquired in laboratories and necropsy rooms. Commun Dis Public Health 1999;2:161-167.

85.

Sepkowitz KA: Tuberculin skin testing and the health care worker: Lessons of the Prophit Survey. Tuberc Lung Dis 1996b;77:81-85.

86.

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. Infect Control Hosp Epidemiol 1995;16:160-165.

87.

Menzies D, Fanning A, Yuan L, FitzGerald JM, Canadian Collaborative Group in Nosocomial Transmission of Tuberculosis: Am J Respir Crit Care Med 2003;167:599-602.

88.

Gershon RR, Vlahov D, Escamilla-Cejudo JA, Badawi M, McDiarmid M, Karkashian C, Grimes M, Comstock GW: Tuberculosis risk in funeral home employees. J Occup Environ Med 1998;40:497-503.

89.

Jochem K, Tannenbaum TN, Menzies D: Prevalence of tuberculin skin test reactions among prison workers. Can J Public Health 1997;88:202-206.

90.

Evenson W: Occupational exposure to Mycobacterium tuberculosis. Legal issues in workers' compensation. AAOHN J 1999;47:373-380.

91.

British Thoracic Society. Control and prevention of tuberculosis in the United Kingdom: Code of Practice 2000. Thorax 2000;55:887-901.

92.

American Thoracic Society. Treatment of tuberculosis and tuberculosis infection in adults and children. Am J Respir Crit Care Med 1994;149:1359-1374.

93.

Canadian Tuberculosis Standards, ed 5. A joint production of the Canadian Lung Association/Canadian Thoracic Society and Tuberculosis Prevention and Control, Centre of Infectious Disease Prevention and Control, Health Canada, 2000.

94.

Centers for Disease Control and Prevention. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care facilities. MMWR Morb Mortal Wkly Rep 1994;43:1-132.

95.

Jost M, Rüegger M, Zellweger JP, et al: Tuberkulose am Arbeitsplatz. Gefährdung und Prävention. Luzern, Schweizerische Unfallversicherungsanstalt (Suva), Abteilung Arbeitsmedizin, 1999.

96.

International Union against Tuberculosis and Lung Disease (IUATLD) and the Tuberculosis Programme of the World Health Organization (WHO): Control of tuberculosis in health care settings. Tuberc Lung Dis 1994;75:94-95.

97.

Deutsche Gesellschaft für Krankenhaushygiene (Gemeinsame Empfehlung der deutschen, belgischen und schweizerischen Gesellschaft für Krankenhaus- und Spitalhygiene der Arbeitsgruppe konventionelle Nachweisverfahren des AKM bei DIN sowie Mitgliedern der Deutschen Gesellschaft für Pädiatrische Infektiologie). Infektionsverhütung bei Tuberkulose in Gesundheits- und Sozialeinrichtungen. Hyg Med 1997;22:523-534.

98.

Centers for Disease Control: Guidelines for preventing the transmission of tuberculosis in health-care settings, with special focus on HIV-related issues. MMWR Morb Mortal Wkly Rep Recomm Rep 1990;39:1-29.

99.

US Department of Health and Human Services. NIOSH guide to the selection and use of particulate respirators certified under 42 CFR 84. 1996. DHHS Publication No. 96-101; www.cdc.gov/niosh.

100.

BGR 250/TRBA 250: Biologische Arbeitsstoffe im Gesundheitswesen und in der Wohlfahrtspflege, Stand 11. August 2003.

101.

Deutsche Norm: Atemschutzgeräte. Filtrierende Halbmasken zum Schutz gegen Partikel. Anforderungen, Prüfung, Kennzeichnung. Deutsche Fassung EN 149:1991.

102.

American Thoracic Society. Respiratory protection guidelines. Am J Respir Crit Care Med 1996;154:1153-1165.

103.

Diel R, Schneider S, Meywald-Walter K, Ruf CM, Rusch-Gerdes S, Niemann S: Epidemiology of tuberculosis in Hamburg, Germany: Long-term population-based analysis applying classical and molecular epidemiological techniques. J Clin Microbiol 2002;40:532-539.

104.

Small PM, Hopewell PC, Singh SP, Paz A, Parsonnet J, Ruston DC, Scecter GF, Daley CL, Schoolnik GK: The epidemiology of tuberculosis in San Francisco: A population-based study using conventional and molecular methods. N Engl J Med 1994;330:1703-1709.

105.

Bennett DE, Onorato IM, Ellis BA, Crawford JT, Schable B, Byers R, Kammerer JS, Braden CR: DNA fingerprinting of Mycobacterium tuberculosis isolates from epidemiologically linked case pairs. Emerg Infect Dis 2002;8:1224-1229.

106.

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. Clin Infect Dis 1995;21:1098-1101.

107.

Seidler A, Nienhaus A, Diel R: The transmission of tuberculosis in the light of new molecular biological approaches. Occup Environ Med 2004;61:96-102.

108.

Nienhaus A: Berufliches Infektionsrisiko für Tuberkulose - Zusammenfassung und Ergebnisse des Expertengesprächs am 12. Mai 2003 (in German); in Nienhaus A, Brandenburg S, Teschler I (eds): Tuberkulose als Berufskrankheit. Ein Leitfaden zur Begutachtung. Ecomed, Landsberg 2003.

  Author Contacts

Dr. Andreas Seidler, MPH
Institute of Occupational Medicine, Johann Wolfgang Goethe University
Theodor-Stern-Kai 7
DE-60590 Frankfurt/Main (Germany)
Tel. +49 69 6301 7607, Fax +49 69 6301 7053, E-Mail a.seidler@em.uni-frankfurt.de

  Article Information

Received: April 19, 2004
Accepted after revision: September 9, 2004
Number of Print Pages : 16
Number of Figures : 0, Number of Tables : 3, Number of References : 108

  Publication Details

Respiration (International Journal of Thoracic Medicine)

Vol. 72, No. 4, Year 2005 (Cover Date: July-August 2005)

Journal Editor: Bolliger, C.T. (Cape Town)
ISSN: 0025-7931 (print), 1423-0356 (Online)

For additional information: http://www.karger.com/res

  Drug Dosage / Copyright

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