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Johnson KR, Braden CR, Cairns KL, et al. Transmission of Mycobacterium tuberculosis From Medical Waste. JAMA. 2000;284(13):1683–1688. doi:10.1001/jama.284.13.1683
Author Affiliations: Epidemic Intelligence Service, Division of Applied Public Health Training, Epidemiology Program Office (Drs Johnson and Cairns), Division of Tuberculosis Elimination, National Center for HIV, STD, and TB Prevention (Drs Braden, Onorato, and Valway), and Division of AIDS, STD, and TB Laboratory Research, National Center for Infectious Diseases (Dr Woodley and Mr Morlock), Centers for Disease Control and Prevention, Atlanta, Ga; Washington State Department of Health, Olympia and Seattle (Drs Johnson, Stehr-Green, and Cairns, Ms Field, and Mr Colombel); Central Arkansas Veterans Health Care System, Little Rock (Dr Yang); Hazard Evaluation and Technical Assistance Branch, Division of Surveillance Hazard Evaluations and Field Studies, National Institute for Occupational Safety and Health, Atlanta, Ga and Denver, Colo (Ms Weber and Dr Boudreau); and Lewis County Health Officer, Chehalis, Wash (Dr Bell). Dr Johnson is now with the Health Studies Branch, Division of Environmental Hazards and Health Evaluation, National Center for Environmental Health, Centers for Disease Control and Prevention. Dr Bell is deceased.
Context Washington State has a relatively low incidence rate of tuberculosis
(TB) infection. However, from May to September 1997, 3 cases of pulmonary
TB were reported among medical waste treatment workers at 1 facility in Washington.
There is no previous documentation of Mycobacterium tuberculosis transmission as a result of processing medical waste.
Objective To identify the source(s) of these 3 TB infections.
Design, Setting, and Participants Interviews of the 3 infected patient-workers and their contacts, review
of patient-worker medical records and the state TB registry, and collection
of all multidrug-resistant TB (MDR-TB) isolates identified after January 1,
1995, from the facility's catchment area; DNA fingerprinting of all isolates;
polymerase chain reaction and automated DNA sequencing to determine genetic
mutations associated with drug resistance; and occupational safety and environmental
evaluations of the facility.
Main Outcome Measures Previous exposures of patient-workers to TB; verification of patient-worker
tuberculin skin test histories; identification of other cases of TB in the
community and at the facility; drug susceptibility of patient-worker isolates;
and potential for worker exposure to live M tuberculosis cultures.
Results All 3 patient-workers were younger than 55 years, were born in the United
States, and reported no known exposures to TB. We did not identify other TB
cases. The 3 patient-workers' isolates had different DNA fingerprints. One
of 10 MDR-TB catchment-area isolates matched an MDR-TB patient-worker isolate
by DNA fingerprint pattern. DNA sequencing demonstrated the same rare mutation
in these isolates. There was no evidence of personal contact between these
2 individuals. The laboratory that initially processed the matching isolate
sent contaminated waste to the treatment facility. The facility accepted contaminated
medical waste where it was shredded, blown, compacted, and finally deactivated.
Equipment failures, insufficient employee training, and respiratory protective
equipment inadequacies were identified at the facility.
Conclusion Processing contaminated medical waste resulted in transmission of M tuberculosis to at least 1 medical waste treatment facility
Mycobacterium tuberculosis is usually transmitted
when persons with pulmonary tuberculosis (TB) aerosolize bacteria by coughing,
sneezing, speaking, or singing.1 Susceptible
persons inhale the aerosolized bacteria, which then can implant deep within
the lung and establish infection. However, novel methods of transmission have
been reported, for example, nosocomial infections resulting from the use of
poorly cleaned, contaminated bronchoscopes2,3;
infections due to the aerosolization of bacteria during vigorous wound4 irrigation; disposal of peritoneal dialysate5; and autopsy6,7
and embalming procedures.8 To our knowledge,
transmission of M tuberculosis as a result of processing
medical waste has not been documented.
In 1997, Washington State had a TB incidence rate of 5.4 cases per 100,000
persons,9 which was less than the national
TB incidence rate of 7.4 cases per 100,000 persons.10
Furthermore, multidrug-resistant TB (isolates resistant to at least isoniazid
and rifampin) is uncommon in Washington State. Five or fewer cases have been
reported annually during 1992-1997.9 This report
summarizes an investigation of 3 TB cases reported from May through September
1997. All 3 patients lived in a county (population approximately 67,000) in
Washington State that had a history of 3 or fewer cases of TB per year for
the past decade,9 and the patients had been
employed as workers in a medical waste treatment facility. Our investigation
sought to identify the source of the infections and to determine if exposure
to medical waste resulted in the transmission of M tuberculosis.
We interviewed each patient-worker and reviewed their medical records
to determine their previous exposures to TB and to verify their histories
of tuberculin skin tests. We reviewed the state TB registry for 1996 and 1997
to identify other cases of TB in the community. We also matched the current
and former (1996-1997) employee rosters of the medical waste treatment facility
to the state TB registry to identify other employees diagnosed with TB.
We submitted M tuberculosis isolates from each
of the patient-workers for susceptibility testing. Laboratory records and
specimen handling methods were reviewed for all laboratories involved in processing
the isolates to identify potential laboratory cross-contamination or mislabeling
of specimens.11 Representative isolates from
each patient-worker underwent DNA fingerprinting using IS6110-based restriction fragment length polymorphism, according to published
standards.12M tuberculosis isolates resistant to isoniazid, rifampin, and streptomycin collected
from patients after January 1, 1995, from the catchment region of the medical
waste facility (medical waste was received from Oregon, Washington, Idaho,
and British Columbia) also underwent DNA fingerprinting. The DNA fingerprints
from the patient-worker isolates were cross-matched with the Centers for Disease
Control and Prevention, National Tuberculosis Genotyping and Surveillance
Network regional laboratory database of M tuberculosis
To identify M tuberculosis drug-resistant mutations,
regions of the RNA polymerase β subunit (rpob)
gene and the entire pyrazinamidase (pncA) gene were
amplified using polymerase chain reaction. The resulting amplicons were sequenced
using an ABI 373XL automated DNA sequencer (Applied Biosystems, Inc, Foster
City, Calif). The pan-susceptible strain M tuberculosis H37Rv was used as a control. The sequences of the patient-worker
isolates and the control strain were compared with the published sequences
of these genes using the Sequence Navigator software (version 1.0.1; Applied
We interviewed the household, social, and coworker contacts of the patient-workers
and reviewed their medical records. All contacts underwent tuberculin skin
test screening with 5 units of purified protein derivative.13
Persons who had recent contact with a patient-worker underwent a second skin
test 3 months after the last exposure. We defined a positive skin test result
as 5 mm or larger induration and a tuberculin skin test conversion as an increase
in induration of 5 mm or more compared with a negative test result within
the previous 2 years.13
The Washington State Department of Labor and Industries Division of
Industrial Safety and Health, Olympia, Wash, performed a safety and health
evaluation of the facility and, subsequently, the National Institute for Occupational
Safety and Health (NIOSH) evaluated the potential for occupational exposure
to M tuberculosis from processing the medical waste.
The investigators conducted walk-through surveys of the facility, interviewed
employees, observed work practices, reviewed the facility's work and safety
policies and procedures, met with local health care providers, reviewed employee
medical records, and photographed and videotaped the plant's methods and procedures.14,15 In addition, in their evaluation,
the NIOSH team used a variety of environmental sampling methods to assess
the potential for aerosolization of medical waste during processing.14
To determine if worker exposure to live M tuberculosis cultures was possible, we conducted a telephone survey of all clinical
laboratories in Washington State approved to perform acid-fast bacilli (AFB)
testing. Personnel at each laboratory were questioned about types of diagnostic
testing performed, current and past laboratory waste decontamination procedures,
and waste disposal methods.16
All 3 patient-workers were white, US born, between the ages of 28 and
52 years old, and seronegative for the human immunodeficiency virus (HIV).
All 3 worked at the medical waste treatment facility, for various amounts
of time between 1992 and 1997. None of them had known exposures to any other
persons with active TB, and none of the 3 had documented results of prior
tuberculin skin tests. The first patient-worker identified (patient-worker
1) worked at the medical waste treatment facility for 4.5 years. Patient-worker
1 reported a productive cough in December 1996 and was evaluated for pneumonia
in April 1997. Infiltrates and cavitary lesions were seen on chest radiograph,
smears of sputum samples contained numerous AFB, and sputum cultures grew
isoniazid-resistant M tuberculosis. Patient-worker
1 did not report other risk factors for TB infection.
Patient-worker 2 worked at the facility for 6 months. Patient-worker
2 described the onset of cough and fever during November and December 1996.
After hearing of patient-worker 1's diagnosis, patient-worker 2 sought a tuberculin
skin test in June 1997 and the results were positive (>15 mm). Chest radiographs
revealed infiltrates, smears of sputum samples were positive for AFB, and
sputum cultures grew M tuberculosis that was sensitive
to all drugs tested. Patient-worker 2 had a history of incarcerations in a
county jail and a psychiatric hospitalization but had not had previous tuberculin
Patient-worker 3 worked at the medical waste facility for 2.5 years
after reporting the onset of a productive cough at the end of July 1997. Patient-worker
3 was screened as an employee contact of patient-workers 1 and 2 and in August
1997, had a positive tuberculin skin test result (17 mm). The chest radiograph
showed bilateral apical densities. Smears of sputum samples did not reveal
AFB, but sputum cultures grew M tuberculosis that
was resistant to isoniazid, rifampin, and streptomycin. Patient-worker 3 did
not recall exposure to patients with active TB other than patient-workers
1 and 2. He had a history of substance abuse and underwent inpatient substance
abuse treatment several years before but was not screened for TB at that time.
All 3 patient-workers were residents of the community for more than
7 years. The only cases of TB reported from the county for 1997 were these
3 patients. None of the former employees of the facility had been reported
as having a case of TB.
After review of laboratory records and procedures of the 5 laboratories
involved in processing the M tuberculosis isolates
from the 3 patient-workers, no evidence of laboratory cross-contamination
or mislabeling of isolates was found. The laboratory characteristics of isolates
from each patient-worker are summarized in Table 1. The isolates from the 3 patient-workers showed different
antimicrobial resistance patterns (Table
1), and their DNA fingerprints were distinct from one another (Figure 1). No isolates with matching fingerprints
were identified from the National Tuberculosis Genotyping and Surveillance
Network regional database.
We identified 10 M tuberculosis isolates from
the medical waste processing facility's catchment region with resistance patterns
that matched the isolates from patient-worker 3 (ie, resistant to isoniazid,
rifampin, and streptomycin. One regional isolate had a DNA fingerprint pattern
that was identical to that from patient-worker 3 (Figure 1). Approximately 96% of rifampin-resistant M tuberculosis isolates possess a mutation within an 81–base
pair region of the rpob gene.17
The isolate from patient-worker 3 and the matching regional isolate both had
the same mutation in codon 516 (GAC → GTC) resulting in the substitution
of valine for aspartic acid. This particular mutation is found in approximately
6% of rifampin-resistant isolates.17 The entire pncA gene was sequenced, and both isolates had the same
silent mutation in codon 38 (GCG → GCC). Silent mutations do not change
the amino acid sequence of the translated protein and are rarely seen in M tuberculosis.18
We performed tuberculin skin tests for all patient-worker contacts (Table 2). No household contacts had positive
tuberculin skin test results. One social contact had a positive skin test
result; this contact had not had previous tuberculin skin tests but had a
history of substance abuse. A follow-up chest radiograph showed no abnormalities.
All 29 employees (7 clerical and 22 waste workers) of the medical treatment
facility were screened as coworker contacts of patient-workers 1 and 2 (Table 2). Ten workers had a positive skin
test result, and an additional 3 had skin test conversions; 4 of these 13
workers had previous risk factors for TB. None of the 10 workers with positive
tuberculin skin test results had had prior skin tests. All contacts with positive
skin test results had normal chest radiographic findings.
The medical waste treatment facility began operating in January 1992.
The facility received waste from hospitals, clinical laboratories, and medical
and dental clinics in Oregon, Washington, Idaho, and British Columbia. The
facility did not require incoming waste to be decontaminated prior to receipt
and processing; the packaging and interstate shipping of the waste met published
guidelines19 and legal requirements.
The treatment facility is a 13,500-square-foot building with an 800-square-foot,
2-story steel-walled containment room located in the center of the plant floor
where the processing equipment is located.14,20
The containment room is designed to operate under negative air pressure relative
to the plant floor. Waste workers perform their duties at various locations
around the plant floor or in the containment room. A second-floor office space
provides a work area for clerical staff.
Containers of waste are manually unloaded from delivery trucks onto
a conveyor that delivers them to the in-feed station of the processing equipment.
Containers are manually emptied into the in-feed chute and placed on another
conveyor to be washed with steam or hot chlorinated water. The processing
equipment shreds the waste and blows it through the system with fans, filling
vessels with approximately 225 kg of waste. Shredded waste is compacted in
the vessels by a hand-operated hydraulic press. The vessels are then manually
capped and guided to a conveyor that delivers them to a radiofrequency oven
that decontaminates the waste using a heating process referred to as "electrothermal
deactivation." Processed vessels exit the containment room and are probed
to determine a core temperature. Vessels not reaching a core temperature of
at least 194°F (90°C) are returned to the oven for reheating. Processed
waste is then hauled from the facility by truck to a landfill.
The 3 patient-workers performed different tasks, but they worked in
close proximity to one another in the facility; all workers shared a common
break room. Patient-worker 1 washed containers after they were emptied. Patient-worker
2 emptied containers into the processing equipment at the in-feed station
and also provided assistance to patient-worker 3 numerous times throughout
the day. In accordance with the facility's task-specific personal-protective
equipment policy, respiratory protection was not required for the positions
of patient-workers 1 and 2. Patient-worker 3 operated the hydraulic press
within the sealed containment room while wearing a Tyvek suit, impervious
shoes and gloves, and a supplied-air hooded respirator. All patient-workers
worked with the waste prior to the electrothermal deactivation decontamination
A safety flap within the in-feed chute, which was designed to prevent
waste from being thrown back onto the plant floor, had been missing for 2
to 5 years.14,15 Employees reported
that when the shredding equipment became clogged, waste particles reversed
direction and vented from the in-feed chute onto the plant floor. Employees
referred to this occurrence as "blowback." Employees did not consistently
shower following their shift, nor did they decontaminate themselves when leaving
the enclosed containment room.14
Employees did not fully understand the potential health risks (eg, needle
injuries and waste spills) associated with exposures to medical waste nor
did they report all such occurrences to supervisors.14
Employees also reported uncertainty about the correct way to don and remove
protective clothing, and they did not always wear it appropriately. The airline
respirator system used inside the containment room did not meet the requirements
for NIOSH approval. Workers reported they had responded to spills without
respiratory protection, that they had repackaged contaminated waste, and that
the doors between the contained processing equipment and the plant floor were
left open during waste processing. The NIOSH evaluation documented the "blowback"
phenomenon using smoke tubes and video equipment.14
All 44 laboratories licensed to process AFB specimens in Washington
State were surveyed by telephone. Forty-one laboratories (93%) sent all waste
to an off-site medical waste disposal company, including the facility where
the 3 patient-workers worked. Three laboratories (7%) incinerated all or nearly
all waste on site. Of the 41 laboratories that contracted for off-site waste
disposal, 21 (51%) performed some decontamination on site. However, 20 laboratories
(49%) did not decontaminate laboratory waste, including stocks and cultures,
prior to shipment. Nineteen (95%) of these laboratories shipped waste to processing
facilities and 1 (5%) to a landfill.16
The regional isolate that matched the isolate of patient-worker 3 was
from a patient who was foreign-born, had immigrated to the United States in
1994 and had known exposures to multidrug-resistant TB. This patient underwent
testing for symptoms consistent with TB in early 1996. At that time, an aspirate
specimen collected from a cutaneous lower limb lesion was culture-positive
for M tuberculosis; lung biopsy and bronchoalveolar
wash specimens were AFB smear- and culture-negative. There was no evidence
of infectious pulmonary disease.
The laboratory that handled the matching isolate had contracted exclusively
with the medical waste treatment facility for waste removal since August 1992.
Furthermore, the laboratory did not decontaminate cultures of M tuberculosis with growth on solid media prior to discarding them
as medical waste. A solid media culture with growth of the matching isolate
was discarded in mid-1996 from this laboratory. Specimens from patient-worker
3 were never processed in this laboratory.
Patient-worker 3 and the patient with the matching isolate were interviewed.
Personal contact between the 2 patients was not identified; they lived more
than 60 miles from one another and had lived within their respective communities
for more than 3 years. The patients did not have common workplaces, hobbies,
social groups, or medical care providers.
To our knowledge, this report is the first to document transmission
of M tuberculosis from occupational exposure to infectious
medical waste. Five lines of evidence from this investigation support this
First, no evidence indicated that transmission to the 3 medical waste
workers occurred as a result of exposure to cases occurring in the community.
DNA fingerprinting data also excluded the possibility that transmission occurred
from one patient-worker to another.
Second, an unusually high percentage (45%) of the coworker contacts
of the 3 patient-workers had positive tuberculin skin test results, especially
considering there was no evidence that patients transmitted TB to their household
Third, in Washington State, 49% of laboratories routinely shipped viable M tuberculosis cultures to medical waste disposal facilities,
including this facility, despite Centers for Disease Control and Prevention
recommendations to decontaminate such material prior to disposal.19
Fourth, the environmental investigations of the facility support the
plausibility of workers being exposed to contaminated waste in ways that put
them at risk for infection. One study reported that bacteria (eg, Bacillus subtilis var niger), particularly
dry spores, added to the waste prior to processing were released from equipment
during the compaction process.21 Therefore,
all workers in the processing area of the plant may have been exposed to aerosols
released from the shredding process.
Finally, an isolate from patient-worker 3 had a DNA fingerprint pattern
that was identical to the pattern for an isolate from a patient whose only
relationship to this outbreak was exposure to the medical waste stream. That
these 2 isolates also share rare mutations increases the likelihood that both
patients were infected with the same organism. The patient whose isolate matched
patient-worker 3's isolate did not have infectious pulmonary TB, and there
was no evidence of contact between them.
A substantial percentage (45%) of the coworker contacts had positive
(11-40 mm) tuberculin skin test results. The level of TB infection in this
study is 3 to 4 times greater than the prevalence for funeral service industry
employees (11.7%),22 an occupational group
previously identified to be high risk for clinically active TB.23
However, it is unknown to what extent exposure to infectious medical waste
played a role in this finding. The 3 persons with documented tuberculin skin
test conversions may have been infected by patient-worker 1, who worked for
several months while infectious. The coworkers with skin test conversions
also had brief contact with patient-worker 2 while potentially infectious.
Four of the persons with positive skin test results acknowledged risk factors
prior to the outbreak that increased their potential for exposure to TB.
This investigation revealed that infectious laboratory waste (eg, stocks
and cultures) are frequently discarded into the solid medical waste stream
in Washington State. Our survey was limited to Washington State; this finding
may not be true for other states. Medical waste was identified as the source
for patient-worker 3's infection only because he was infected with an organism
with a rare pattern of drug resistance that limited the number of possible
sources. Because multidrug-resistant TB rarely occurred in the treatment facility's
catchment region, cultures had been banked since January 1995, permitting
comparison of DNA fingerprints from these isolates with the one from patient-worker
3. This approach was not possible for the more common isolates from the other
Documented results of previous tuberculin skin tests were not available
for patient-workers 1 and 2 or for their coworker contacts. These results
would have allowed estimation of when their exposures occurred. The possibility
that these patient-workers developed TB from previous infections cannot be
excluded. However, based on the annual incidence of TB in Washington State
(5.4 cases/100,000 persons), we would expect 0.0017 cases of TB annually among
32 workers.9 Therefore, the probability of
observing 3 cases in 1 year by chance is less than 0.000001.24
The findings of this investigation lead to several recommendations.
First, laboratories should review their policies and procedures for disposal
of viable M tuberculosis stocks and cultures. To
minimize the risk of infection for medical waste workers, stocks and cultures
should be decontaminated by autoclaving or other approved methods prior to
disposal, preferably within the laboratory where they are generated.19 Ideally, medical waste treatment facilities should
not accept contaminated laboratory waste. Facilities that do accept contaminated
waste should consider deactivation of contaminated stocks and cultures as
the first step in processing waste. Engineering controls that prevent employee
exposure to potentially infectious waste need to be adopted by medical waste
treatment facilities. In addition, medical waste workers need extensive and
ongoing safety training. Such training should include general infection control
principles, personal protective equipment use, and techniques for responding
to waste spills. This training will help employees recognize situations that
put them at risk for exposure to potentially viable pathogens. Medical waste
workers who are employed at facilities that accept contaminated waste should
be considered for routine screening for TB.
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