D
Effects of CDC Guidelines on Tuberculosis Control in Health Care Facilities

Keith F.Woeltje, M.D., Ph.D.*

SUMMARY

In response to nosocomial outbreaks of tuberculosis among patients and health care workers, the Centers for Disease Control and Prevention (CDC) released tuberculosis control guidelines in 1990. These were later expanded and revised in 1994. The CDC guidelines rely on a series of controls: administrative, engineering, and personal respiratory protection. Administrative controls include the prompt identification and isolation of patients who may have pulmonary tuberculosis. Engineering controls include proper ventilation for isolation rooms and other areas, possibly supplemented by ultraviolet germicidal irradiation or high-efficiency particulate air (HEPA) filtration. Personal respiratory protection consists of some form of mask or respirator worn by a health care worker to minimize the risk of inhaling infectious airborne droplet nuclei.

Implementation of control measures in outbreak settings has been shown repeatedly to stop the outbreak. Although many steps may be started at once, the bulk of the evidence suggests that the CDC controls are hierarchical, in that administrative controls are most important (if tuberculosis is not suspected, the other controls will not be initiated), followed by the engineering controls, and lastly, the type of personal respiratory equipment. In nonoutbreak settings having these measures in place almost certainly reduces the risk for health care workers and patients of nosocomial exposure to tuberculosis. However, studies trying to correlate health care worker infections with adherence to tuberculosis

*  

Assistant Professor of Medicine, Section of Infectious Diseases, Medical College of Georgia, Augusta.



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Tuberculosis in the Workplace D Effects of CDC Guidelines on Tuberculosis Control in Health Care Facilities Keith F.Woeltje, M.D., Ph.D.* SUMMARY In response to nosocomial outbreaks of tuberculosis among patients and health care workers, the Centers for Disease Control and Prevention (CDC) released tuberculosis control guidelines in 1990. These were later expanded and revised in 1994. The CDC guidelines rely on a series of controls: administrative, engineering, and personal respiratory protection. Administrative controls include the prompt identification and isolation of patients who may have pulmonary tuberculosis. Engineering controls include proper ventilation for isolation rooms and other areas, possibly supplemented by ultraviolet germicidal irradiation or high-efficiency particulate air (HEPA) filtration. Personal respiratory protection consists of some form of mask or respirator worn by a health care worker to minimize the risk of inhaling infectious airborne droplet nuclei. Implementation of control measures in outbreak settings has been shown repeatedly to stop the outbreak. Although many steps may be started at once, the bulk of the evidence suggests that the CDC controls are hierarchical, in that administrative controls are most important (if tuberculosis is not suspected, the other controls will not be initiated), followed by the engineering controls, and lastly, the type of personal respiratory equipment. In nonoutbreak settings having these measures in place almost certainly reduces the risk for health care workers and patients of nosocomial exposure to tuberculosis. However, studies trying to correlate health care worker infections with adherence to tuberculosis *   Assistant Professor of Medicine, Section of Infectious Diseases, Medical College of Georgia, Augusta.

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Tuberculosis in the Workplace controls in low- to moderate-risk situations have had mixed results. This may be due to underlying differences in the baseline purified protein derivative (PPD) conversion rates in different hospitals. In addition to the adoption of the whole guidelines, a number of studies have focused on parts of the guidelines. This is particularly true of administrative controls. It is in this area where the most variability in practice will arise, particularly in designing criteria for patient isolation, owing to the wide differences in patient populations seen at different hospitals. Although compliance with the guidelines in the early 1990s was suboptimal, a number of studies show significant improvements in guideline compliance. However, there are many areas that still have considerable room for improvement, particularly in the education of health care workers about tuberculosis. Information on implementation of the guidelines outside of the inpatient setting of acute-care hospitals is scarce. Some evidence exists that many emergency departments are making progress. The cost of implementation of the guidelines can be substantial, but many of these costs are one-time facility improvements. Although the ongoing costs of a tuberculosis control program can be substantial, these programs may be relatively cost-effective compared with the costs incurred in evaluating patients or healthcare workers exposed to a nonisolated tuberculosis patient. INTRODUCTION Summary of 1990 and 1994 CDC Guidelines After decades of declining rates of tuberculosis in the United States, case rates leveled off and then increased in the late 1980s and early 1990s (1, 2). A number of factors led to the reversal of the previous trend: decreased public health infrastructure, the human immunodeficiency virus (HIV) epidemic, and an influx of immigrants from areas where tuberculosis is endemic (3). The problem was compounded by the fact that many physicians and other healthcare workers had very little experience with tuberculosis. They often did not suspect the diagnosis when a patient with the disease first presented and, even if suspected, often had little appreciation for the infection control issues involved. Almost inevitably, a number of nosocomial outbreaks of tuberculosis occurred, including outbreaks involving multidrug-resistant tuberculosis (MDR tuberculosis) (4, 5, 6, 7, 8, 9, 10). In December 1990, CDC published “Guidelines for Preventing the Transmission of Tuberculosis in Health-Care Settings, with Special Focus on HIV-Related Issues” (11) in response to these outbreaks. Subsequently, these guidelines were expanded and refined with the publication in October 1994 of “Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health-Care Facilities, 1994” (12).

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Tuberculosis in the Workplace The 1994 CDC guidelines include recommendations for assignment of responsibility for tuberculosis control. A risk assessment for the facility (and potentially for individual wards and areas within the facility) is suggested. This risk assessment takes into account the number of tuberculosis patients seen at the facility, the number of tuberculosis patients in the surrounding community, and whether or not there is evidence of increased health care worker PPD skin test conversions. The extent to which other control actions are taken would then depend on the risk of the facility. For example, a baseline PPD test for new employees is recommended for essentially all facilities, but the frequency of routine serial testing would be determined by the risk assessment. The guidelines also suggest health care worker education consistent with the duties/training of the employee. Good cooperation with local health departments is also stressed. Although the bulk of the guidelines are targeted to acute-care hospitals, tuberculosis control in other settings such as dental clinics, physicians’ offices, and long-term-care facilities are also briefly discussed. The core of the 1994 CDC guidelines is a series of control measures for handling patients suspected of having tuberculosis. Three categories of controls are described: administrative, engineering, and personal respiratory protection. Administrative controls include prompt recognition of patients who may have tuberculosis with subsequent rapid isolation of these patients, efficient diagnostic evaluation, and criteria for releasing patients from isolation. Other administrative controls include practices such as keeping patients on tuberculosis isolation in their room unless medically necessary. Engineering controls involve primarily ventilation, tuberculosis isolation rooms should have negative pressure, ≥ six air changes per hour (ACH), and exhaust air directly to the outside (or HEPA filter the air before recirculation if this is not possible). Engineering controls also include having good general ventilation, especially in areas where patients may congregate. Ultraviolet germicidal irradiation (UVGI) may be used as an adjunct to both general ventilation and tuberculosis isolation room ventilation. Finally, the guidelines discuss personal respiratory protection for health care workers who are likely to be exposed to tuberculosis aerosols (e.g., while in a tuberculosis isolation room). The respirator should be compliant with Occupational Safety and Health Administration (OSHA) requirements, and used as part of a comprehensive respiratory protection program. Focus of Review The author was directed to “prepare a technical background paper reviewing the literature and data on the effects of the CDC guidelines on tuberculosis control in health care facilities.” This paper is being written as background for an Institute of Medicine report on occupational expo-

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Tuberculosis in the Workplace sure to tuberculosis. Although the 1994 guidelines do include employee tuberculin skin testing programs and personal respiratory equipment, this paper will not address these particular aspects because the topics will be covered in other background papers. One important exception is that employee PPD test conversion rates will be discussed as a marker for the effectiveness of different tuberculosis control plans. Although the 1994 CDC guidelines are the most current, as summarized above, these guidelines are an extension and revision of the 1990 guidelines. Thus, this paper will review the impact of implementation of policies following both sets of guidelines. As with the guidelines, this paper will focus primarily on the inpatient, acute-care setting. This is partly out of necessity, as there is a paucity of data on implementation of the guidelines in other settings. Methods To find papers for review, a MedLine search using Ovid (Ovid Technologies, New York, New York) was performed. The database was searched from the most recent update available in mid-June 2000 back through 1991. Initial search terms were Tuberculosis/pc,ep,tm (Prevention & Control, Epidemiology, Transmission) AND Health facilities. The search was further limited to English-language articles. This yielded 257 references. Abstracts of these references were reviewed to choose appropriate articles. Additional Medline search strategies included Guidelines AND Tuberculosis/pc (which added 5 references not previously obtained), and (Tuberculosis OR Mycobacterium tuberculosis) AND Occupational exposure (which yielded 64 additional references, only 2 of which were useful). The author’s files served as another source of articles. Finally, potentially useful references found while reading the initial papers were also reviewed. Although the guidelines are generally applicable, because the expectation of implementation is primarily in U.S. hospitals, papers regarding health-care facilities outside of the United States were not included. Not all papers reviewed were included in the final document—papers were chosen either for the strength of their data or because they contributed a unique view into the implementation of the CDC standards. IMPACT OF FOLLOWING THE GUIDELINES Studies of Implementation of Entire Guidelines Studies Showing Resolution of Outbreaks The strongest evidence for the beneficial impact of the CDC guidelines comes from institutions where control measures were implemented

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Tuberculosis in the Workplace in response to nosocomial transmission of tuberculosis to patients and/or health care workers. Implementation of these measures then led to decreases in nosocomial cases of tuberculosis infection or disease. Wenger and coworkers (13) reported the experience of Jackson Memorial Hospital, Miami, Florida, following an outbreak of MDR tuberculosis from 1988 to 1990 on an HIV ward (4, 14). Control measures were implemented over time, starting in March 1990. The measures implemented included the following: March Stricter enforcement of isolation policy to include isolation of any HIV-positive patient with an abnormal chest radiograph (CXR) Change in criteria for stopping isolation from discontinuation after 7 days on therapy to discontinuation only after three negative smears for acid-fast bacilli (AFB) (or after reduction in AFB on three smears plus a clinical response) Enforcement of policy to keep tuberculosis patients in their rooms unless medically necessary and having patients wear a surgical mask when out of their rooms Sputum induction done only in isolation rooms Initial therapy for tuberculosis with four drugs April (through April 1991) The 6 tuberculosis isolation rooms (of 23) without negative pressure were repaired, and the ventilation in the other rooms was made more consistent June Aerosolized pentamidine administered only in isolation room September Change from cup-type surgical mask to submicron mask for health care workers A review of admissions of HIV-positive patients with MDR tuberculosis was performed, covering three time periods: initial period (January 1990 to May 1990), early follow-up (June 1990 to February 1991), and late follow-up (March 1991 to June 1992). There was a decrease in MDR tuberculosis patient-days over the three periods (222/100 real days initially, then 119/100, and finally 16/100). Fifteen patients with MDR tuberculosis were admitted during the initial period: 12 (80 percent) had been exposed while on the HIV ward. Eleven patients were admitted during the follow-up periods, only five of whom had been exposed on the ward, all during the initial period. No known patient exposures occurred during the follow-up periods.

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Tuberculosis in the Workplace Health care worker PPD test results were also reviewed over the same time periods. A total of 39 health care workers were previously PPD negative and tested (25 during the initial period, 17 during early follow-up, and 23 during the late follow-up). There was a total of 10 PPD conversions: 7/25 (28 percent) in the initial period, 3/17 (18 percent) in early follow-up, and 0/23 in late follow-up (P < 0.01). Of the three PPD conversions during the early follow-up period, two were linked to exposure to a patient with MDR tuberculosis who was not isolated on admission because of the fact that he was on therapy and had been AFB smear negative at the time of a recent hospital discharge. However, he subsequently proved to be smear positive. This led to an additional policy that any patient with a history of MDR tuberculosis would be isolated regardless of previous smear and treatment status. The authors point out that it is difficult to know what components of the control measures were most important. However, the early implementation of administrative controls linked with beginning improvements in engineering controls led to a reduction in nosocomial transmission of MDR tuberculosis to other patients, as well as a reduction in PPD conversions in health care workers. Similarly, Maloney and colleagues (15) detailed control methods implemented in June through October 1991 after an outbreak of MDR tuberculosis at Cabrini Medical Center in New York City. Control measures included improved isolation criteria (not detailed in the paper, but 90 percent of patients with MDR tuberculosis were isolated on admission, compared with isolation of 40 percent of patients preintervention) and molded surgical masks for employees (June): improved lab services (July); increase from 0/10 tuberculosis isolation rooms with negative pressure to 16/27 with negative pressure (September); and a chamber for sputum induction and pentamidine administration (October). With the adoption of these measures the number of patients with MDR tuberculosis who had previously been admitted to Cabrini fell from 24 in the preintervention period (January 1990 through June 1991) to 6 in the postintervention period (July 1991 through August 1992). Three of the six postintervention patients also had documented nonhospital or preintervention exposures documented. In the postintervention period only 1 patient was found to have had a documented nosocomial exposure during a previous hospitalization, as opposed to 20/24 (83%) in the preintervention period. Implementation of control measures led to no change in the overall rate of PPD conversions (~3 percent). However the rate of conversion on the HIV and medical wards fell from 16.7 percent during the preintervention period to 5.1 percent postintervention (p = 0.02), with no change on wards that did not usually house tuberculosis patients. The postintervention PPD

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Tuberculosis in the Workplace rates on HIV and medicine wards became essentially the same as the rates on other wards (5.1 percent versus 4.0 percent; p = 0.5). Again, the impact of the individual control measures could not be determined, but clearly, the overall impact was significant. The authors note that the overall PPD conversion rate was unchanged. They highlight the importance of determining job-specific rates. Blumberg and colleagues (16) reported the efforts made at Grady Memorial Hospital in Atlanta. These were in response to nosocomial transmissions of drug-sensitive tuberculosis in 1991 and early 1992 (5). Control measures implemented included the following: March 1 Expanded isolation policy—all patients with known or suspected tuberculosis (including all patients for whom AFB smear and culture were ordered), also any patient with HIV infection (or risk for HIV infection with unknown serology) with abnormal CXR. Increased surveillance by infection control to ensure that patients for whom smears ordered were in isolation. Isolation stopped only after three negative AFB smears (previously stopped after 2 weeks of therapy) Increased physician education Window fans added to 90 rooms to provide negative pressure June 1 Submicron masks used for personal respiratory protection July 1 PPD testing done every 6 months now included nonemployee health care workers (e.g., attendings, house staff, medical students) tuberculosis nurse epidemiologist hired To determine the effectiveness of these measures the authors reviewed tuberculosis exposure episodes (from July 1, 1991, to June 30, 1994) and PPD conversions (from January 1, 1992 to June 30, 1994). Over the 3-year period there were 752 admissions (673 patients) with tuberculosis; for 461 admissions (61 percent) the patients had positive AFB smears and were considered infectious. The results for these patients are shown in Table D-1. Employee PPD conversion rates fell steadily from 3.3 percent to 0.4 percent during the postintervention period (for trend, p < 0.001). For the January-June 1994 PPD conversions (23/5,153 [0.4 percent]) no clustering by work area was noted. In fact only 10 health care workers had direct patient contact on wards where tuberculosis patients were housed, 4 had patient contact on low-risk tuberculosis areas (e.g., neonatal intensive care unit [ICU]), and 9 had no patient contact, suggesting that more than half of the conversions may have been community acquired.

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Tuberculosis in the Workplace Tuberculosis isolation rooms were tested with smoke approximately every 3 months. The failure rate ranged from 6.1 percent to 21.7 percent (mean, 16.5 percent). One room tested with sulfur hexafluoride had 4.9 ACH. The author suggest that their data imply that the improvements in PPD conversion rates were primarily the result of improved administrative controls since changes mirrored improved isolation as a result of the new policies. They argue that since room negative pressure was demonstrated to be frequently suboptimal, engineering controls were not the major factor in the improvements. Likewise submicron masks appeared to be adequate. The new policies resulted in only one of eight patients placed on tuberculosis isolation having culture-confirmed tuberculosis. Columbia-Presbyterian Medical Center in New York City had control measures detailed by Bangsberg and colleagues (17). They revised their tuberculosis control guidelines to be consistent with the CDC guidelines. Prior to June, 1992, medical house staff were PPD tested at baseline and were then instructed to be tested annually by their primary physicians. Starting in June 1992, PPD testing was done every 6 months on medical house staff. The overall rate of participation was 92 percent. Revised tuberculosis control measures included stricter isolation policy (implemented in May 1992) so that patients with HIV infection or HIV in fection risk factors or who were homeless and presented with pneumonia or evidence of tuberculosis were placed in tuberculosis isolation until three sputum samples were AFB negative and the patient was judged noninfectious by pulmonary and infectious disease consultants. Tuberculosis isolation rooms were installed in the emergency department (ED) in July 1992. A tuberculosis service was implemented at the end of June 1993. In July 1993 3M respirators (type not stated) were instituted. TABLE D-1. Results of Interventions at Grady Memorial Hospital Measure Pre-intervention (7/91–2/92) Post-intervention (3/92–6/94) p No. of tuberculosis admissions 184 568 No. of tuberculosis admissions/ month (AFB +) 23 (12.9) 20 (12.8) No. of exposure episodes/month 4.4 0.6 No. of exposure days/month 35.4 3.3 < 0.001 No. of patients not appropriately isolated/total no. of patients 35/103 (34%) 18/358 (5%) < 0.001 No. of HIV infected patients admissions associated with exposure episodes/total no. of admissions 22/33 (67%) 7/143 (5%) < 0.001

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Tuberculosis in the Workplace The number of patients with pulmonary tuberculosis appropriately isolated during January through June 1992 (preintervention) was only 29/71 (38 percent). This increased to 29/45 (64 percent) from January to December 1992. Subsequent isolation rates continued to improve slightly: 60/82 (72 percent) from January to June 1993 and 33/44 (75 percent) from July to December 1993 (p < 0.01 for trend). Results considering only HIV infected patients were similar. PPD conversion rates among house staff were as follows: June 1992, 10 percent (5.8/100 person-years); December 1992, 3 percent (5.1/100 person-years); June 1993, 0 percent; December 1993, 1 percent (2.3/100 person-years); June 1994, 0 percent. Conversion rates were calculated per 100 person-years of exposure because of varying exposure times possible at the June 1992 testing (12–36 months, depending on the year of the resident). Because the biggest drop occurred between December 1992 and June 1993, the authors imply that isolation policy and possibly the tuberculosis isolation rooms in the ED were most important in leading to the improvements. Clearly their expanded isolation policy resulted in much better isolation of patients with pulmonary tuberculosis over this time period. Stroud and colleagues (18) reviewed the effects of control measures at Roosevelt during three 15-month periods: period I, January 1989 to March 1990; period II, April 1990 to June 1991; and period III, July 1991 to September 1992. Period I was essentially a preintervention period, during which there was an outbreak of nosocomial tuberculosis (7). Patients with suspected tuberculosis were admitted to private room (only 1 of 16 with negative pressure), doors were often left open, and isolation was discontinued without negative AFB smears. Surgical masks were used for respiratory protection. Most rooms, however, did exhaust to the outside. During period II administrative controls were enforced—a lower threshold for initiating isolation was set, more aggressive evaluation for possible tuberculosis was started, and more aggressive treatment regimens were started if there was no response to initial therapy. An effort was made to keep HIV-infected patients off wards with tuberculosis patients. In period III engineering controls were phased in. From July to December 1991, 11 rooms were fitted with UVGI. From November 1991 through January 1992 seven of these rooms were fitted with exhaust fans for ≥6 ACH and negative pressure. Isolation chambers were used for sputum induction/aerosolized pentamidine administration. Surgical masks (Technol 47080070) were used through all three study periods. With the implementation of administrative controls during periods II and III, patients with pulmonary tuberculosis were more likely to be isolated on admission (44 percent versus 0 percent during period I). The median delay before isolation initiated (2 versus 6 days) also improved.

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Tuberculosis in the Workplace During period I, the likelihood of an HIV-infected patient getting tuberculosis decreased with distance from source patient room (but oddly, not related to the amount of time spent on the ward). Smear negative patients were not a source of nosocomial infection in period I. Crude rates of nosocomial tuberculosis were reduced from 8.8 percent during period I to 2.6 percent during period II and to 0 percent in period III. During period II, there was no association of nosocomial tuberculosis with distance from the source patient’s room. The impact on health care worker PPD conversion rates could not be determined due to insufficient data. However, during period II plus period III, PPD conversion rates were higher on tuberculosis wards than on other wards (5/29 versus 0/15; p = 0.15). The impact of implementing the CDC guidelines on employee PPD conversion rates at St. Clare’s Hospital in New York was reported by Fella and colleagues (19). Beginning in 1991, all health care workers with patient contact had PPD testing every 6 months; others were tested annually. Two-step testing of new employees was implemented in February 1993. Prior to 1991, no negative-pressure isolation rooms were available at St. Clare’s. The implementation of control measures and PPD conversion rates are shown in Table D-2. In an abstract presented at the 1994 Annual Conference of the Society for Occupational and Environmental Health—Tuberculosis Control in the Workplace: Science, Implementation, and Prevention Policy, Koll and colleagues (20) summarized data from Beth Israel Medical Center (BIMC) in New York City. The hospital had large numbers of tuberculosis patients and admissions in the early 1990s. A comprehensive tuberculosis policy (based on the 1990 CDC guidelines) was implemented in mid-1992. tuberculosis isolation rooms with negative pressure, ≥6 ACH, and UVGI were TABLE D-2. PPD Conversions and Interventions at St. Clare’s Hospital Year Interval No. PPD Positive/ No. tested Rate (%) PRP Environmental Interventions 1991 Jan–June 30/145 20.7 Technol shield Negative-pressure rooms July–Dec 11/158 7.0 Technol shield 1992 Jan–June 7/219 3.2 Particulate respirator UVGI July–Dec 14/227 6.2 Particulate respirator 1993 Jan–June 10/249 4.0 Dust-mist-fume respirator July–Dec 9/154 5.8 Dust-mist-fume respirator NOTE: PRP = personal respiratory protection.

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Tuberculosis in the Workplace made available. Automatic door closers were installed. HEPA filters were used for recirculated air. A protocol for rapid identification of patients with possible tuberculosis was instituted. Surgical masks were replaced with submicron masks. Strict adherence to tuberculosis isolation precautions was promoted with patient education and incentives. Booths were used for aerosolized pentamidine administration and sputum induction. An annual PPD program for health care workers was implemented, with testing of high-risk health care workers every six months. The impact of the policies on health care worker PPD conversion is noted in Table D-3. The reason for such small numbers of respiratory therapist conversions was not noted in the abstract. The authors noted that the rate of compliance with PPD testing in 1991 and 1992 was <75 percent; in 1993 it was 95 percent, so the reduction may have been even greater than documented. Unfortunately, rates are not provided, but overall the data are suggestive. Grant (21) presented the results of a review of all tuberculosis cases at Parkland Memorial Hospital, Dallas, in 1994 and 1995. A variety of enhancements to the tuberculosis control policies were made from April to December 1994, including certification of PPD placement, an algorithm for tuberculosis isolation room assignment in times of low availability, standing orders for patients with suspected tuberculosis, increased UV in waiting areas, a fit testing program, increased employee PPD frequency (depending on job category), and notification of infection control by radiology of suspicious CXRs. Previously, an increase in health care worker PPD conversions had led to improvements in engineering controls, with 64 tuberculosis isolation rooms being made available. Over the 2 years, 253 tuberculosis patients were admitted, 85 percent of whom had pulmonary disease. In 1994, all AFB smears were processed within 24 hours. Nontuberculous mycobacteria (NTM) were found in 193/ 407 (47 percent) patients with a positive AFB smear. Further results are presented in Table D-4. The authors report that the data gathered each year were released along with information about the importance of compliance with the tuberculosis control protocols. They suggest that the high rate of NTM made the diagnosis of true tuberculosis more difficult. They also suggest that TABLE D-3. PPD Conversions in Health Care Workers at BIMC   No. of Conversions Year House Staff Nurses RT All Other 1991 9 14 0 7 1992 4 9 0 7 1993 1 7 0 6  

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Tuberculosis in the Workplace search are simply reviews of tuberculosis and tuberculosis control with some suggestions at implementing control measures in whatever setting rather than studies of actual practices or outcomes. Emergency Departments Moran and colleagues (62) reported the results of a 1993 CDC survey of tuberculosis control practices in the ED. Written policies for managing patients with suspected tuberculosis in the triage and waiting areas were available at 159/282 (56.4 percent) hospitals. A total of 214/280 (76.4 percent) had written policies for the ED proper. The decision to isolate patients was usually made in triage (235/286 [82.2 percent] hospitals). Written criteria for this decision were available in 105/286 (44.7 percent) hospitals. Patients suspected of having tuberculosis were given a mask in 228/246 (91.9 percent) of institutions. A total of 5/247 (1.7 percent) had tuberculosis isolation rooms in the triage/waiting area, while 56/286 (19.6 percent) had tuberculosis isolation room in the ED proper. UVGI was used in 15/277 (5.4 percent) triage/waiting areas and in 21/264 (8 percent) EDs proper. Air was recirculated in 211/262 (81 percent) of triage areas and 205/258 (79 percent) of EDs proper. An employee PPD program was in place at 283/286 (99 percent). A total of 186 (65.7 percent) were tested annually, 58 (20.5 percent) were tested every six months, and 18 (6.4 percent) were tested only at hire. For 1991, 34/211 (16.1 percent) had >1 PPD conversion; for 1992 this changed to 63/234 (26.9%). The overall rate of PPD conversion in 1991 was 78/ 7,348 (1.1 percent) whereas it was 141/8,698 (1.6 percent) in 1992. This study showed that in the early 1990s, compliance with suggested control measures for EDs was suboptimal, along the lines of general compliance discussed above. Dental Clinics Murphy and Younai (63) report on a study done at the New York University College of Dentistry. This school runs an extremely busy clinic with 288,000 patient visits/contacts per year in New York City. From 1991 it had gradual implementation of annual PPD testing for faculty, staff, and students. For the 1993–1994 testing period, there was a 20.9 percent conversion rate in employees (56 percent of these conversions were in employees with no patient contact) and a 15 percent conversion rate in students. To evaluate for possible tuberculosis exposures in the clinic, the authors conducted a retrospective review of patients referred out for a medical condition from August 1994 through July 1995. A total of 96/ 1,259 (0.4 percent) of the referrals were potentially related to tuberculosis—a review of those who returned to dental care and had records avail-

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Tuberculosis in the Workplace able showed no cases of patients with active tuberculosis at time of their dental visit. These chart review data were also reported separately in greater detail (64). The authors conducted a survey of 54 dental schools and received 24 (44 percent) responses. A total of 14/24 (58 percent) had no PPD data available, and 5 (21 percent) had no data available but were planning to start testing. Of five (21 percent) with data, only three shared their results. At one dental clinic on the West Coast, the PPD conversion rate was approximately 1 percent. At another West Coast school, the conversion rate for faculty was 1.6 percent, for students it was 2 percent, and for staff it was 1.8 percent. At the third school, in the Midwest, the only positive PPD results were in foreign-born students. A 1-year study, completed in July 1995, of student conversions during the 3rd year (the first clinical year) revealed a 10.6 percent conversion rate. It was unclear if students had received two-stage testing for their initial tests. The control plan for the facility involved a risk analysis, after which the facility was designated very low risk (i.e., tuberculosis in the community but not the facility). The paper speculates that a lot of the skin test conversion may have been community acquired. Administrative controls included obtaining a detailed history from every new patient and an abbreviated history on patient return to screen for tuberculosis; patients with suspicious findings were sent to a designated clinic for more detailed evaluation. HEPA masks were made available and were to be used for high-risk patients. Engineering controls are not required at that risk level, and none were specifically planned. Although no cases of tuberculosis were found by their chart review, given the high prevalence of tuberculosis in New York City during that time period and given the high rates of PPD conversions in students and faculty, a higher-level risk assessment would seem more appropriate. An argument could be made for implementing more aggressive control measures, especially engineering controls in common areas, and perhaps better personal protective equipment for the staff. COSTS OF IMPLEMENTING GUIDELINES Entire Guidelines Kellerman and colleagues (65) calculated the costs from 1989 to 1994 of implementing the CDC guidelines at three New York City hospitals (Roosevelt, Cabrini, St. Clare’s) and a Miami hospital (Jackson) that had had nosocomial outbreaks. Also included was one low-risk hospital in Nebraska (Regional West) for comparison. The hospitals provided estimates of nursing time for placing and reading PPD tests, supply costs,

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Tuberculosis in the Workplace and costs of follow-up of those with positive PPD test results. The absolute costs of an employee PPD program ranged from $330 to $58,380 per year. The cost per health care worker tested ranged from $3.53 to $12.94. Additional personnel costs for administering a tuberculosis control program ranged from $10,000 (0.25 full-time equivalents [FTE]) to $137,400 (2 FTE). Capital costs for environmental controls ranged from $54,000 to $554,900. Maintenance costs (including increased utility costs due to increased ventilation) were estimated at $4,000 to $25,000 per year. Kellerman and colleagues (66) also evaluated the costs of tuberculosis control in children’s hospitals in 1994–1995. The Baby and Children’s Hospital-New York Presbyterian Medical Center (BCH-NYPMC) Children’s Hospital and Health Center-San Diego (CHHC-SD), and the pediatric ward at the University of California at San Diego (UCSD) were surveyed. Costs per health care worker for PPD testing ranged from $6.91 to $12.49, with total costs of the program running $2,470 to $26,577 per year. Construction costs for that year ranged from $12,800 to $24,500. Total respirator costs for a year were $1,360 at BCH-NYPMC (with fit testing by manufacturer), $1,680 at CHHC-SD (fit testing was available but was not used), and $480 at UCSD (no fit testing). While the “data” aspects of the implementation of control measures at Roosevelt in New York City were reviewed by Stroud et al. (18), Williams et al. (67) provided a discussion of the “soft” aspects of the control program. A primary barrier early on was a lack of tuberculosis knowledge by health care workers, which required providing significant education efforts. Because much of the tuberculosis at Roosevelt came through the ED, the medical director there played a key role in educating that department. This led to more timely isolation in the ED. They noted that a key priority was enlisting the collaboration of the admitting department so that patients could be moved out of the ED in a timely fashion. They developed a system of bed triage based on estimated risk so that tuberculosis isolation rooms would be used appropriately in times of shortage. Getting health care workers to implement controls was hampered by the perception that prevention of tuberculosis outbreaks was solely the responsibility of infection control, which had “failed” since an outbreak had occurred. Also, the increased numbers of patients on isolation increased the perception that more tuberculosis patients were being admitted, increasing employee fear and anger. However, the concerns of health care workers did spark increased compliance with routine PPD testing. The authors noted that one key difficulty was keeping patients in their rooms. They tried offering incentives (e.g., free television, free incoming phone calls, special food choices) as suggested in the CDC guidelines, but noted that the actual impact was small. Although this paper does not address any dollar costs in implementing control measures, it

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Tuberculosis in the Workplace provides an excellent review of the social costs of an outbreak and associated controls. Isolation/Administrative Controls A significant fraction of the ongoing cost of a tuberculosis program may be in evaluating patients who do not have tuberculosis but who meet criteria to be evaluated. Scott and colleagues (68) evaluated the experience at the University of Iowa Hospital and Clinics. All patients with a positive sputum culture for tuberculosis between January 1, 1987, and September 24, 1992, were considered a case. Forty-four patients were identified, and charts were available for review for 43. Control patients were chosen randomly from patients who had had sputum submitted for AFB but who had negative cultures. Since bronchoscopy specimens were routinely sent for AFB smear and culture regardless of clinical suspicion of tuberculosis, patients who had specimens only from bronchoalveolar lavage were excluded. Of 92 potential controls for every case, 43 random controls chosen matched by location (inpatient/outpatient) and service. Of the case patients, 39 (91 percent) were smear positive; 25 (58 percent) were positive on the first smear. Only one test for AFB was sent from 48 percent of the control subjects. Of 24 inpatients with pulmonary tuberculosis, only 10 (42 percent) were isolated upon admission. A total of 37/ 43 (86 percent) case patients had a CXR consistent with tuberculosis, as did 7/43 (16 percent) controls. If same rate held for all patients, ~670 patients would have had abnormal CXRs. The six other case patients had abnormal CXRs, but not “typical” for tuberculosis. From July 1, 1991, through June 30, 1992, there were 12 “exposure” workups for an AFB+ smear, with 363 contacts. Only 4 of the 12 had tuberculosis; the others had infection with non-tuberculous mycobacteria (NTM). Scott and colleagues (68) calculated the cost of diagnosing a case of tuberculosis: $18.30 was spent for an AFB smear and culture. Control patients had an average of 2 sputum specimens sent, while case patients had an average of 3.2 specimens sent. With 92 control patients for every tuberculosis patient, this led to a cost of $3,426 per case of tuberculosis diagnosed. The authors also estimated that 15 minutes/person of nurse epidemiologist time was spent tracing and contacting health care workers exposed to a case of tuberculosis, with an additional $6.00 to $11.00 per employee for PPD testing. The authors state that a policy of isolating everyone for whom an AFB smear was sent would be unreasonable, causing a 92-fold overuse of isolation rooms. However, this is within the range reported in the Veterans Affairs hospital study by Roy et al. (30). Although not discussed, if only the estimated 670 patients with “typical” CXRs were isolated, the overisolation ratio would be ~18:1, which does not seem unreasonable.

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Tuberculosis in the Workplace It would seem that the ordering of testing of sputum for AFB at Iowa at that time period was excessive, especially given that almost half of the control patients had only one sputum specimen sent. Despite this apparent interest in diagnosing tuberculosis, only 42 percent of tuberculosis patients were isolated on admission. One wonders if physicians are lulled into complacency about tuberculosis since so many of the positive AFB smears proved to be NTM. This increase in NTM compared with tuberculosis has been reported elsewhere (21, 69) as well. Although the authors did not calculate this, using their estimate of 30 contacts per case, the 14 nonisolated tuberculosis patients would have exposed 420 health care workers at a cost of 105 nurse epidemiologist hours ($2,100 at the $20/hour they estimated), plus an additional $2,520 to $4,620 for PPD testing. Kerr and Savage (70) calculated the potential cost of exposure to a single nonisolated patient in a postanesthesia care unit (PACU). Based on traffic in the PACU and typical recovery times, they estimated that a patient with tuberculosis would expose 24 other patients, 10 PACU staff, 38 operating room staff, and 9 ancillary staff (total 81). Cost and time estimates were from Brown et al. (70) and Scott et al. (67). Their results follow: Cost per contact identification   $17.00 PPD testing cost   $8.21 Total contact tracing/testing $25.21 * 81 = $2,042.01 Legal/risk management   $550.00 Infectious disease consult   $200.00 Total initial costs   $2,792.01 Follow-up 65 with negative initial     PPD test $8.21 * 65 = $533.65 Follow-up for 16 PPD conversions     Physician visit, smear, CXR $88.30 * 16 = $1,412.80 Follow-up for 3 with active disease     Hospital costs $12,369.00 * 3 = $37,107.00 Physician visits $1,785.00 * 3 = $5,355.00 Follow-up for 13 with latent tuberculosis     6 months of INH @ $7.20/month   $562.38 Monthly nurse visits @ $20.00/month   $1,560.00 Follow-up physician exam @ $45.00   $585.00 Follow-up CXR @ $25.00   $325.00 Grand Total   $57,477.84

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Tuberculosis in the Workplace Although one can take exception to some of the estimates, the values chosen for baseline PPD test positivity, PPD conversion, and development of active disease are all within reasonable ranges. The conversion rates were cited from Griffith and colleagues (72). The rate of developing active tuberculosis seems high (albeit possible), and the need for inpatient therapy seems unlikely. For outpatient therapy of tuberculosis, Brown et al. (71) list $2,300/case for drug-susceptible tuberculosis (health department data). Nevertheless it is clear that one tuberculosis exposure can be quite expensive if one figures in all the costs involved and not just contact tracing and a single round of PPD testing. A study submitted for publication by Topal and colleagues (73) and associates at Yale University reviewed their experience with isolation protocols. Because their case finding included all patients for whom a sample for testing for AFB was sent, even if only from a bronchoscopy specimen, it is difficult to compare their results with those of others. Their initial protocol required tuberculosis isolation if a patient had cough for ≥2 weeks AND infiltrate on CXR AND a risk factor (tuberculosis exposure/history of tuberculosis or positive PPD/HIV infection/homelessness/IV drug use/alcohol use OR [fever + weight loss + night sweats]). Patients were evaluated from October 1996 through June 1997. In the initial group, 48/141 (34 percent) of isolated patients (19 percent of total patients for whom cultures for AFB testing were sent) did not meet isolation criteria and were considered over-isolated. Twenty-one of these were HIV-infected patients. At least one patient who was over-isolated by their criteria had tuberculosis. This patient had a cough and an abnormal CXR, but no clinical symptoms or risk factors on their list. He was from India and had been isolated anyway. A total of 13/115 patients for whom AFB tests were ordered and who were not placed on isolation actually met the criteria, and should have been isolated. One such patient with tuberculosis exposed 200 health care workers (no PPD conversions were found on follow-up). The protocol was revised to allow for clinical concern in HIV-infected patients. The revised protocol also included foreign birth in an area with high prevalence of tuberculosis as a risk factor. A postintervention study was done from January through June 1998, after educating health care workers about the new guidelines. Only 12.6 percent of the group were over-isolated, and only 2 (1.5 percent) patients were under-isolated. Thus, their educational intervention was successful, and apparently, with the new criteria, no patient with tuberculosis was not isolated. Overall, the new criteria had increased sensitivity (80 versus 100 percent) with a loss of specificity (50 to 40 percent). Although it is not clear from the data in the results, the authors state in the discussion that their over-isolation ratio was 25:1 in the post-intervention period. Their cost estimate for smears for AFB and culture was $50.00 (it is implied that this is for three sputum samples). Thus, labora-

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Tuberculosis in the Workplace tory costs for a 25:1 over-isolation are $1,250 spent for every case of tuberculosis diagnosed. They also estimate respirator costs at $5.00 to $6.50 per day ($0.50/mask with 10–13 used/day), and with a mean duration in tuberculosis isolation of 4.2 days, respirator cost would be about $700 for 25 patients. This leads to a total laboratory and isolation cost of under $2,000 for every patient actually diagnosed with tuberculosis (the authors actually calculate a cost of approximately $3,000 per case, but their calculation assumes that every patient isolated stays on isolation for the duration of their stay, about 10 days). If one patient exposed 400 health care workers (as had happened at Yale in 1993), labor costs alone were estimated at $11,000. Thus, even if there were no PPD converters, they suggest that their 25:1 over-isolation ratio may be cost-effective. Education Trovillion and colleagues (37) reported on the costs of implementing an educational program. A tuberculosis protocol was introduced at BarnesJewish Hospital in St. Louis in the summer of 1995. An estimated 3,000 employees with patient contact (35 percent of total) needed training. Because this was beyond the means of the infection control practitioners, 146 volunteer trainers were instructed and provided with training materials. These trainers then provided training sessions at their respective locations. Only 924 employees (31 percent) received training within 6 weeks as was requested. By the end of 5 months, 1,909 (64 percent) of targeted employees had been trained. The sessions tended to last ~20 minutes because of time constraints, not the 40 minutes envisioned during the training of the trainers. The estimated costs were infection control program development time (40 hours) ($1,386) + training packets ($812) + employee time away from workplace to provide/attend training ($23,855), for a total of $26,053. Excluding the cost for the employees to attend, which would be incurred by any training method, this format was thought to be a cost-effective way of providing efficient training. No hard evidence of the effectiveness of the training was obtained, but the discussion mentions that staff seemed to be more knowledgeable. REFERENCES 1. American Thoracic Society. Control of tuberculosis in the United States. American Review of Respiratory Diseases 1992; 146:1623–1633. 2. Centers for Disease Control and Prevention. Tuberculosis morbidity-United States, 1997. Morbidity and Mortality Weekly Report 1998; 47:253–257. 3. 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.

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