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Tuberculin Skin Testing Surveillance of Health Care Personnel

  1. Adelisa L. Panlilio1,
  2. Dale R. Burwen2,a,
  3. Amy B. Curtis2,a,
  4. Pamela U. Srivastava1,a,
  5. John Bernardo3,
  6. Michela T. Catalano4,
  7. Meryl H. Mendelson5,
  8. Peter Nicholas5,b,
  9. William Pagano4,a,
  10. Carol Sulis3,
  11. Ida M. Onorato2,a,
  12. Mary E. Chamberland1,a, and
  13. Tuberculin Skin Testing Surveillance Project
  1. 1Division of Healthcare Quality Promotion, National Center for Infectious Diseases, Atlanta, Georgia
  2. 2Division of Tuberculosis Elimination, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia
  3. 3Tuberculosis Program, Boston Department of Health and Hospitals, Boston City Hospital, Massachusetts
  4. 4Montefiore Medical Center, Bronx
  5. 5Division of Infectious Diseases, Department of Medicine, Mount Sinai Medical Center, New York
  1. Reprints or correspondence: Dr. Adelisa L. Panlilio, Div. of Health Care Quality Promotion, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Mailstop E-68, 1600 Clifton Rd. NE, Atlanta, GA 30333 (Apanlilio{at}cdc.gov).

  • ↵a Present affiliations: US Food and Drug Administration, Rockville, Maryland (D.R.B.); Division of HIV/AIDS Prevention, National Center for HIV, STD, and TB Prevention (A.B.C. and I.M.O.), Division of Viral and Rickettsial Diseases, National Center for Infectious Diseases (M.E.C.), and National Immunization Program (P.U.S.), Centers for Disease Control and Prevention, Atlanta, Georgia; and Concentra Health Services, Secaucus, New Jersey (W.P.).

  • ↵b Deceased.

 
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Abstract

To estimate the incidence of and assess risk factors for occupational Mycobacterium tuberculosis transmission to health care personnel (HCP) in 5 New York City and Boston health care facilities, performance of prospective tuberculin skin tests (TSTs) was conducted from April 1994 through October 1995. Two-step testing was used at the enrollment of 2198 HCP with negative TST results. Follow-up visits were scheduled for every 6 months. Thirty (1.5%) of 1960 HCP with ⩾1 follow-up evaluation had TST conversion (that is, an increase in TST induration of ⩾10 mm). Independent risk factors for TST conversion were entering the United States after 1991 and inclusion in a tuberculosis-contact investigation in the workplace. These findings suggest that occupational transmission of M. tuberculosis occurred, as well as possible nonoccupational transmission or late boosting among foreign-born HCP who recently entered the United States. These results demonstrate the difficulty in interpreting TST results and estimating conversion rates among HCP, especially when large proportions of foreign-born HCP are included in surveillance.

Occupational transmission of Mycobacterium tuberculosis has been recognized as a risk to health care personnel (HCP) since the 1920s [1]. Several outbreaks of tuberculosis in health care settings in the early 1990s heightened concern about transmission to both patients and HCP [2,3,4,5,6,7–8]. Some of these outbreaks involved multidrug-resistant strains of M. tuberculosis [2–6]. The investigations of these outbreaks highlighted the infectiousness of tuberculosis in general, the susceptibility of immunocompromised persons (particularly those with HIV infection) to rapid progression of this condition to life-threatening clinical tuberculosis, and the potential for rapid spread of tuberculosis when HCP and immunocompromised patients are exposed to patients with infectious tuberculosis. At least 20 HCP developed multidrug-resistant tuberculosis in association with these outbreaks [5] (Centers for Disease Control and Prevention [CDC], unpublished data).

CDC recommends periodically performing tuberculin skin tests (TSTs) for HCP who have the potential for exposure to M. tuberculosis [9]. TST results are used in the clinical treatment of HCP and assessment of the adequacy of infection-control measures in health care facilities. Many skin testing programs in health care facilities are suboptimal—for example, they are characterized by low compliance rates, lack of initial 2-step testing, use of inappropriate cutoff points in interpreting TST results, and inability to aggregate data for analysis (CDC, unpublished data) [10]. Because of these and other shortcomings, high-quality data to assess the risk of M. tuberculosis transmission to HCP are limited. To address these limitations, we conducted a prospective multicenter surveillance of M. tuberculosis infection among HCP from April 1994 through October 1995. Our objectives were to estimate the incidence of and assess risk factors for occupational transmission of M. tuberculosis to HCP.

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Methods

Participants. Participants in this surveillance project were HCP who worked in New York City and Boston at 5 health care facilities (4 hospitals and 1 correctional facility; table 1). At least 100 patients were treated for tuberculosis and/or had tuberculosis diagnosed at each of these facilities in 1992. From April 1994 to May 1995, a sample of HCP with negative TST results were enrolled from work locations and/or occupations of relatively high or low tuberculosis exposure. For instance, we targeted for enrollment HCP hypothesized a priori to have increased risk of exposure to M. tuberculosis because they worked where patients with tuberculosis were admitted. For comparison, we enrolled demographically similar HCP considered to have decreased risk of exposure to M. tuberculosis (e.g., persons working in the operating room or neonatal intensive care unit and first- and second-year medical students). On the basis of the likelihood of contact with patients with tuberculosis, the health care facilities themselves determined which HCP locations and occupations had high or low potential for exposure to M. tuberculosis.

Figure 1
Figure 1

Distribution of final tuberculin skin test (TST) results with an induration of >0 mm among health care personnel (HCP) enrolled in prospective surveillance project, according to place of birth (US-born subjects [gray bar] vs. foreign-born subjects [black bar]), 1994–1995. Results for 1465 foreign-born HCP and 455 US-born HCP with induration size of 0 are not shown.

Table 1
Table 1

Characteristics of health care facilities that participated in tuberculin skin testing surveillance of health care workers for occupational transmission of tuberculosis.

Personnel who were already known to have a documented positive TST result or previously treated tuberculosis were ineligible to participate in the project. We did not exclude HCP solely on the basis of receipt of BCG vaccine. We performed TSTs (either single or 2-step, as appropriate) for HCP who were not already known to have a positive TST result or to have been treated for tuberculosis. Only those HCP with negative TST results at baseline were recruited to participate in the surveillance project.

Study protocol. Skin testing was done using the Mantoux technique [11] with use of 0.1 mL of purified protein derivative containing 5 TU, which was placed intradermally and read 48–72 h after placement. TST results were measured as the diameter of induration transverse to the axis of the forearm and recorded in millimeters. To help ensure the uniformity of results, only 1 brand of antigen (Tubersol; Connaught) was used throughout the surveillance period at all sites that participated in this surveillance project. A 2-step test (i.e., 2 TSTs performed 1–3 weeks apart) was required for all initial testing to minimize the likelihood of interpreting a boosted reaction as a true conversion due to recent infection. However, employees with written documentation of TST performance (regardless of whether the result was read) within 12 months of enrollment underwent only a single test at enrollment. All new employees enrolled in the surveillance underwent 2-step testing.

Project personnel responsible for placement and reading of TSTs were trained by CDC staff. These trained project personnel placed and read Mantoux skin tests at work sites. Self-reporting of results was not allowed. Follow-up tests and questionnaire administration were scheduled for every 6 months or were done as part of workplace tuberculosis contact investigations. The study protocol was approved by the Institutional Review Board at each participating health care facility.

Definitions. Definitions of negative and positive TST results and TST conversions were based on the 1990 diagnostic standards [11]. For purposes of this surveillance project, an induration of ⩾10 mm was classified as a positive result for all persons, because all participants in this surveillance were HCP. For analysis purposes, a conversion was defined as an increase of ⩾10 mm, regardless of the subject's age; this was considered evidence of new infection with M. tuberculosis. A boosted TST result, which is thought to indicate waned mycobacterial sensitivity that is restored by the antigenic challenge of an initial test, was defined as a positive result of the second test 1–3 weeks after a negative result of the first test [12, 13].

Person-time for HCP without TST conversion was calculated as the time from the first negative until the last negative TST result. Person-time for HCP with TST conversion was calculated as the time from the first negative TST result to midway between the last negative and the positive TST result.

Data collection. At enrollment, we collected demographic and occupational data, including age, occupation, country of birth, and work location. We assessed receipt of BCG vaccine by self-report, without confirming the presence of a scar consistent with vaccination. At each follow-up visit, we asked HCP about contact with patients who had tuberculosis, performance of cough-inducing procedures, use of respiratory protection, and other potential tuberculosis contact in settings such as other health care facilities, correctional facilities, and drug treatment centers. We also asked subjects about household contact with active tuberculosis and travel outside of the United States. To provide objective information about potential tuberculosis exposure, each facility tracked the number and location of patients admitted to the hospital with active tuberculosis in a respiratory site and tuberculosis contact investigations conducted during this surveillance project. Data collection ended October 1995.

Data analysis. The SAS software package (SAS Institute) was used for data analysis [14]. Adjusted TST conversion rate ratios were computed by Poisson regression [15].

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Results

During the study period, 60–214 patients with tuberculosis were admitted to the health care facility, and 1–22 tuberculosis contact investigations were conducted at each of the 5 health care facilities (table 1). The 5 facilities identified 5232 HCP in targeted occupations and work locations. Of these HCP, 2117 (40%) were already known to have positive results of TSTs and thus were ineligible for participation in this project. The 917 HCP (18%) who declined to participate in the study had either negative or unknown TST status. We enrolled 2198 HCP with negative TST results in the project. Of this cohort, 504 (23%) had only 1 follow-up TST, 1405 (64%) had 2, and 51 (2%) had 3. Of the 1960 (89%) who underwent ⩾1 follow-up TST during the project period, 30 (2%) had TST conversion (table 2), for a TST conversion rate of 16 conversions per 1000 person-years (table 3).

Table 2
Table 2

Characteristics of health care personnel with tuberculin skin test conversion in surveillance of health care workers for occupational transmission of tuberculosis.

Table 3
Table 3

Number of health care personnel who participated in a study of occupational transmission of tuberculosis, number of tuberculin skin test conversions, and conversion rates, according to selected demographic factors, on univariate analysis.

The distributions of TST results of >0 mm among HCP with ⩾1 follow-up test were similar for US-born and foreign-born HCP (figure 1). Of HCP with TST results of >0 mm, 5 had negative TST results of 5–9 mm, 10 had TST conversions with reaction sizes of 10–14 mm, and 20 had TST conversions with reactions of ⩾15 mm.

TST conversion rates were significantly associated with certain risk factors (table 4). HCP who reported having undergone BCG vaccination and those who reported an unknown BCG vaccination status had higher rates of TST conversion than did those who did not report BCG vaccination (P = .0001 and .003, respectively). HCP who did not work on a single ward for ⩾75% of the time had a TST conversion rate 2.5 times higher than the rate for HCP who worked primarily on a single ward (TST conversion rate, 30.0 vs. 11.9 conversions per 1000 person-years, respectively; P = .01). However, among the 1504 HCP who worked primarily on 1 ward, there was little difference in the TST conversion rate between those who worked on high-exposure wards and those who worked on low-exposure wards (11.2 vs. 12.6 conversions per 1000 person-years, respectively; P = .81). The 122 HCP who underwent TSTs as part of a work-related contact investigation had higher conversion rates than did the 1838 HCP who were tested as part of routine surveillance (42.8 vs. 14.3 conversions per 1000 person-years, respectively; P = .03). HCP with nonoccupational exposure to patients with tuberculosis had a higher TST conversion rate than did HCP with no known nonoccupational exposure to tuberculosis, although the difference was not statistically significant (89.6 vs. 15.7 conversions per 1000 person-years, respectively; P = .09). Other risk factors were not associated with the rate of TST conversion.

Table 4
Table 4

Number of health care personnel who participated in a study of occupational transmission of tuberculosis, number of tuberculin skin test (TST) conversions, and conversion rates, according to selected risk factors or markers, on univariate analysis.

On multivariate analyses, the only factors that independently predicted TST conversion were (1) being foreign born and arriving in the United States ⩽2 years before the study started, and (2) having TSTs performed as part of a work-related contact investigation (table 5). Because of multicolinearity between foreign birth and history of BCG vaccination, history of BCG vaccination was not included in the final multivariate model. After adjustment for other variables, foreign-born HCP who recently arrived in the United States had a TST conversion rate 16.7 times greater than that of US-born HCP (95% CI, 5.6–49.5), whereas foreign-born HCP arriving in the United States >2 years before the study period had a TST conversion rate double that of US-born HCP (95% CI, 0.9–5.0). HCP who underwent TST as part of a workplace contact investigation had a TST conversion rate >3 times that of HCP who were tested routinely (95% CI, 1.2–8.4).

Table 5
Table 5

Factors associated with tuberculin skin test (TST) conversion for health care personnel in a study of occupational transmission of tuberculosis, on multivariate analysis.

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Discussion

There are 3 possible explanations for an increase of ⩾10 mm of induration found on serial TSTs performed among our cohort of HCP. The first is that occupational M. tuberculosis transmission occurred. Multivariate analysis identified inclusion in a contact investigation as an important risk factor. Twelve conversions occurred in HCP who reported having both patient contact of >30 h per week and contact with patients known to have active tuberculosis. The observed conversion rates are similar to some reported elsewhere in studies of HCP [16, 17]. Although the health care facilities in this surveillance project provided care to many patients with tuberculosis during the study period, the number of patients with tuberculosis at 4 of these 5 health care facilities was less than one-half of the number in the years immediately preceding the study. Therefore, our study likely occurred after the period of peak transmission of M. tuberculosis. Furthermore, infection-control measures in the participating health care facilities may have been largely responsible for limiting occupational M. tuberculosis transmission to HCP. (An outbreak of multidrug-resistant tuberculosis occurred at 1 of the participating health care facilities before this project was conducted.) However, none of the other work-related factors that we assessed (e.g., high-exposure work location, more hours at work or of patient contact, entrance of rooms of patients who had been isolated or who were undergoing respiratory precautions for tuberculosis, or performance of cough-inducing procedures) were associated with TST conversion. Perhaps the inability to detect other significant occupational risk factors resulted from a lack of power or from selection of a cohort of workers that included a large number of foreign-born persons. This study did not assess the role of ventilation as a factor contributing to transmission of M. tuberculosis in these health care facilities [18]. However, if the level of ventilation were a factor in such transmission, then clustering of conversions by location might have been expected; this was not observed.

Second, we found that foreign birth and, especially, recent entry into the United States were most strongly associated with TST conversion, which suggests that possible nonoccupational M. tuberculosis exposure was the source of infection. That the strongest risk factor identified was nonoccupational suggests that many of the conversions could have been community acquired or explained by other reasons, as has been found in other studies [19, 20]. Studies of TST conversion among HCP suggesting community acquisition of infection as more likely than occupational acquisition lend support to this explanation [21,22,23–24]. The majority of foreign-born HCP with TST conversion were from countries with a high prevalence of tuberculosis (i.e., Pakistan and The Philippines). These findings are similar to those for patients with clinically active tuberculosis in the United States [25]. Social networks of foreign-born HCP may be more likely to include other foreign-born persons, including networks with a higher rate of active tuberculosis. This may be especially true for persons who have recently arrived in the United States. However, only 1 of the 30 HCP with TST conversion reported known contact with active tuberculosis outside of work. Thus, if infections were acquired in the community during the study period, HCP were unaware of the source. It is possible that additional questions might have elicited information about potential nonoccupational tuberculosis exposure with greater sensitivity.

Third, boosting is a possible explanation for some of the increased reaction sizes. Although we expected use of 2-step testing at enrollment to minimize interpretation of boosting as conversion, boosting may help explain our finding of recent US entry and foreign birth as risk factors for conversion. Because boosting can occur with past M. tuberculosis infection, nontuberculous mycobacterial infection, or BCG receipt, recent US entry and BCG receipt may be markers for immigration from countries with a high prevalence of tuberculosis and/or nontuberculous mycobacteria [26,27,28–29]. Four of those HCP who had conversion were foreign born, received BCG, entered the United States during or after 1992, and had 2–3 TSTs performed in the year before their TST induration increased. Because the increase in induration to a positive result occurred on the third or fourth test rather than the second, boosting, if it occurred, was noted later than usual. This has been described elsewhere [27–30], but not among HCP. More recent studies of HCP have found similar risk factors for TST conversion [31, 32].

Several limitations should be considered in interpreting these data. First, individual reactivity to tuberculin antigen varies [33]. Second, even experienced readers vary in their measurements of induration [33]. Furthermore, the Mantoux test is neither 100% specific nor 100% sensitive, and its positive predictive value decreases with decreasing prevalence of infection [34]. Most data used to assess risk factors for M. tuberculosis transmission in this project were self reported and not objectively verified. For instance, project personnel did not verify BCG receipt by documenting the presence of a scar, although the reliability of relying on the presence of a scar versus history is unclear [35, 36]. To what extent BCG receipt was over- or underreported is unknown. HCP estimated their hours of patient contact and number of contacts with patients who had active tuberculosis. Some workers (none of whom were physicians) who were tested because of contact with patients who had infectious tuberculosis denied having contact with patients who had active tuberculosis. HCP also self-reported nonoccupational tuberculosis contact but were not asked to report occupational tuberculosis contact at other facilities. Our data collection instruments were limited in their sensitivity to assess occupational and nonoccupational tuberculosis contact. Further, because 27% of the persons who had conversion reported having worked in another health care setting, occupational tuberculosis exposure could have occurred at locations other than the study site. Finally, we excluded from our risk factor analysis 3 workers with boosts or conversions at 4 weeks, 6 weeks, and 5 months after their first tests, because improper 2-step testing made it difficult to distinguish between boosting and conversion.

The trend of decreasing admissions of patients with tuberculosis to US hospitals has continued since this surveillance project was conducted, so the potential for occupational contact with tuberculosis in the hospital is decreasing. Nevertheless, as shown in our study, there continues to be a risk of occupational M. tuberculosis transmission. This study highlights the importance of continued adherence to measures for prevention of M. tuberculosis infection and appropriate targeted tuberculin skin testing, including 2-step baseline testing. This is particularly crucial because of the potential for increased vulnerability of health care facilities and HCP to outbreaks of health care—associated M. tuberculosis transmission as infection-control and occupational health resources shrink. Our data also highlight some of the challenges in interpreting serial TST results and the lack of correlation between risk of occupational M. tuberculosis transmission and work location; finally, they reinforce the importance of the epidemiological context in interpreting whether a TST conversion is due to occupational or nonoccupational transmission.

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Acknowledgments

We thank Penny S. McKibben (Hospital Infections Program, currently known as the Division of Healthcare Quality Promotion, CDC, Atlanta), for help with data management; Kim Laurich, Lynn Mancini, Karen Minerva, Denise O'Connor, Maria Serrano, Jill Solomon, Robin Solomon, and Linda van der Beek, for help with data collection; and all of the HCP, without whose cooperation this project would not have been possible.

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Footnotes

  • The findings, views, and recommendations contained herein are those of the authors and should not be construed as official Centers for Disease Control and Prevention or US Department of Health and Human Services positions. The use of trade names and commercial sources is for identification only and does not imply endorsement by the US Public Health Service or the US Department of Health and Human Services.

  • Received August 13, 2001.
  • Revision received December 14, 2001.
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  1. Clin Infect Dis. (2002) 35 (3): 219-227. doi: 10.1086/341303
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