*From the Florida Department of Health, Bureau of Tuberculosis Control and Refugee Health, Gainesville, FL.
Correspondence to: Michael Lauzardo, MD, Florida Department of Health, 730 NE Waldo Rd, Suite 600, Gainesville, FL 32641-3699; e-mail: Michael_Lauzardo@doh.state.fl.us
Several studies have shown that funeral directors have an
increased risk of tuberculosis (TB). Although there is indirect
evidence of transmission of TB from cadavers to mortuary workers, there
is only one recently documented case in the literature. We report here
another case of occupationally acquired TB in a funeral director, which
was confirmed by conventional epidemiology and genotyping. This case
illustrates the risk of TB transmission to mortuary workers from
routine embalming of deceased TB patients with active
tuberculosis (TB) is inversely related to socioeconomic status, those
occupations that have a disproportionate number of impoverished
individuals, such as agricultural workers, will have high rates of
TB.1Recent studies have shown that funeral directors have
an increased risk of TB infection and disease despite their high
socioeconomic status.2The implication of these findings
is that deceased individuals can transmit active TB during routine
embalming. Although the transmission of TB to pathologists during
autopsy has been well-documented,3to our knowledge, the
transmission of active disease during routine embalming has been
described only recently.4 We report here another case of
TB transmitted during routine embalming that was proven by conventional
epidemiology and molecular techniques.
A 34-year-old woman presented to her local physician complaining
of fever and weight loss in June 1995. She was found to be positive for
HIV at that time. During this initial evaluation, she was found to have
retroperitoneal lymphadenopathy, which on biopsy and culture proved to
be caused by Mycobacterium tuberculosis. Blood cultures
taken during this time were also positive for M
tuberculosis. The organism was demonstrated to be susceptible to
all the first-line drugs for TB. Shortly after starting medications in
early July 1995, compliance with the regimen became a problem. The
patient was being managed by a private physician and was receiving her
medications through the health department. The patient’s mother was
providing the presumed directly observed therapy. Although the patient
was receiving four-drug therapy, she was receiving only 300 mg rifampin
daily instead of the usual 600 mg daily. In August 1996, the patient
was found to have cervical adenopathy. A culture of the lymph node was
positive for M tuberculosis, and susceptibility testing
revealed the organism to be resistant to rifampin alone. A subsequent
chest radiograph in October 1996 showed evidence of pulmonary
infiltrates. The patient died of respiratory failure in November 1996.
A 48-year-old woman with no medical problems other than
hypertension developed dyspnea and a dry cough in 1993. She was noted
to have had a chest radiograph suggestive of sarcoidosis and underwent
a bronchoscopy with transbronchial biopsy, which was nondiagnostic. The
results of a purified protein derivative skin test for TB was negative
at that time. The clinical and radiographic picture was most consistent
with sarcoidosis, despite the nondiagnostic bronchoscopy. Therefore,
she began receiving oral systemic steroids in the form of prednisone.
She responded well clinically and was lost to follow-up until December
1996 when she presented once again with marked dyspnea and dry cough.
She began receiving prednisone and oxygen, and her condition improved
somewhat. She had not received prednisone or any other therapy for the
sarcoid for > 2 years. The prednisone was tapered in February 1997;
however, her dyspnea and cough progressed. Oral cyclophosphamide was
added to the prednisone in March 1997. In April 1997, a bronchoscopy
with transbronchial biopsy was performed. Histology results for biopsy
specimens were negative, and the results of stains were negative for
any organisms. The cyclophosphamide was discontinued, and the
patient was treated empirically for causes of atypical pneumonia with
clarithromycin. She was admitted once again in June 1997 and was
referred for lung transplantation. The patient died during that
hospitalization. The cultures from the bronchoscopy in April grew
M tuberculosis 3 days prior to her death. Susceptibility
testing later revealed the organism to be rifampin monoresistant (RMR).
In response to the identification of a large number of RMR TB
cases in Florida from 1995 to 1996, a detailed chart review was
undertaken in the fall of 1997 of all RMR cases. Cases from 1997 that
appeared to be linked epidemiologically later were included. The
identification of two cases of RMR TB from the same metropolitan area
led to further investigation that established an epidemiologic link
that had not been identified during the initial conventional
investigation. A chart review was performed again as well as a
reinterview of the family members of both patients to determine whether
other epidemiologic links existed. In addition, as part of a separate
unrelated study, those M tuberculosis isolates that were
demonstrated to be RMR were sent to the New York State Department of
Health (Wadsworth Center Laboratory; Albany, NY) for DNA typing. Strain
subtyping of M tuberculosis was performed by standardized
IS6110 restriction fragment length polymorphism (RFLP), as
Briefly, genomic DNA was digested into fragments with the restriction
enzyme PvuII. Restriction fragments were separated by size
on an agarose gel and were transferred to a nylon membrane by Southern
blotting.8 The nylon membrane was hybridized with a
peroxidase-conjugated probe for the insertion sequence
IS6110. Chemiluminescence from the hybridized probe was
detected by exposure of the blot to X-ray film. The resulting pattern
demonstrated the DNA fragments containing the IS6110
Strains possessing less than six copies of the IS6110
element demonstrate a highly conserved site specificity for insertion
into the genome.9 Thus, the fingerprints for strains with
few copies of IS6110 show limited variation. The usefulness
of IS6110 fingerprinting in epidemiologic studies for
low-copy-number strains, therefore, is reduced. For such strains, a
secondary typing method is required in cases in which it is necessary
to differentiate strains that are not related epidemiologically.
Secondary strain typing of M tuberculosis was performed by
spoligotyping (Isogen Bioscience, BV; Maarssen, The Netherlands) as
described by Kamerbeek et al.10 Spacer regions within the
direct repeat locus of the chromosome were amplified by polymerase
chain reaction and hybridized to 43 complementary synthetic
oligonucleotides covalently bound to a nylon membrane. The
detection of the hybridized polymerase chain reaction products was
performed by streptavidin-horseradish peroxidase-enhanced
chemiluminescence according to the manufacturer’s recommendations
(Amersham Pharmacia Biotech; Piscataway, NJ).
After it was determined that the patient in the source case had
been embalmed by the patient in the secondary case 1 month prior to the
patient in the secondary case becoming ill, a site survey was
undertaken of the funeral home where it was suspected that transmission
occurred. This site survey occurred in two parts. The first part
involved a review of the records that were available from the
embalming, including the death certificate, and also a review of
the procedures used for embalming. The second part was performed by a
private indoor air engineering firm (All American Air Cleaning
Equipment, Inc; Clearwater, FL). The number of air changes per hour as
well as the air flow in the embalming room was calculated using a hood
(Alnor Instrument Company; Skokie, IL).
The isolates from both cases were resistant only to rifampin when
tested by an indirect method (BACTEC; BD Biosciences; Franklin Lakes,
NJ). The level of resistance was at 2.0 μg/mL for the isolates
from both patients. The isolates were not thought to be laboratory
contaminants, since the clinical specimens were processed 8 months
apart and were independently sent to New York for DNA typing. In
addition, no other RMR cases have been reported in this area before or
since these two cases were discovered.
RFLP analysis demonstrated identical DNA fingerprints for the two
isolates of M tuberculosis. Each isolate possessed three
copies of the IS6110 transposable element. These were
present on restriction fragment sizes 4.52, 2.30, and 1.37
kilobases. The spoligotyping results also were identical for
both isolates. Hybridization was obtained for spacer oligonucleotides 1
to 17, 19 to 32, 37, 38, and 43. The RFLP and spoligotyping patterns
are shown in Figure 1
Neither the source case nor the secondary case was on the
original contact investigation lists at the time each case was
identified. In addition, the two patients did not share any contacts
between them. The fact that both patients were resistant only to
rifampin was the trigger to cause suspicion about a link between the
two patients, a link that was confirmed when it was discovered that the
patient in the secondary case embalmed the patient in the source case.
After the DNA analysis provided further evidence of a causal link
between the two patients, the family members were interviewed again,
this time with more specific questions regarding any outside social
contact between the two patients. No outside links could be
established. The patients lived in different parts of the city, did not
attend the same church, did not have mutual friends, were not
hospitalized at the same time, and did not go to the same physician.
Routine embalming procedures were followed. A large trocar attached to
a siphon suction device was employed to remove body fluids from the
abdominal cavity. The siphoned body fluids would splash in the waste
sink and then were discarded. The location of the sink was immediately
below an exhaust fan housed in an 18 × 18-inch opening. No
deviations from the usual embalming protocol were noted or
recorded according to the daughter of the patient in the secondary
case, who was also the codirector of the funeral home. By report,
universal precautions are used routinely, including use of the
exhaust fan during the embalming. The fan, however, is turned off
immediately after the embalming is complete and is not used routinely
when preparing the deceased for viewing.
The air in the embalming room was supplied by four 8 × 12-inch
vents. There was no air return in the room; however, a 24 × 24-inch
air return capable of moving 367 cu ft/min was positioned in the
adjacent room. The embalming room measured
15.3 × 15.5 × 8.2 feet or 1,944.63 cu ft. The exhaust fan was
able to produce between 25.57 and 26.56 air changes per hour.
There are three possible explanations for the transmission of TB
between these individuals. The first is that there was some contact
between these individuals outside of the embalming room that eluded the
contact investigation. This is not considered to be likely because of
the numerous interviews conducted by different personnel both at the
time of the initial contact investigations and retrospectively after it
was determined that the two cases were related. The other two possible
explanations for these cases focus on the embalming room. During the
handling of the cadaver, the moving of the body may have caused the
expulsion of air from the chest cavity and resulted in the release of
M tuberculosis organisms in aerosol form. Although this is
possible, the volume of air that would be expelled does not seem
sufficient to achieve a threshold number of droplet nuclei that could
have led to the infection of the patient in the secondary case. A more
likely explanation seems to stem from the embalming procedure itself.
As the body cavity is pierced and the body fluids are siphoned out of
the abdomen and thorax, it is conceivable that large numbers of
tubercle bacilli may be included in the suction material. When the
suction material is discarded, tubercle bacilli can theoretically
become aerosolized after mixing with water and splashing in the waste
sink. This is especially possible in the case of patients with
disseminated disease such as the patient in the source case in this
investigation. It is interesting to note that the patient in the source
case in the only other published case of transmission from a cadaver to
an embalmer also was coinfected with HIV and may have had disseminated
What can be learned from this investigation to prevent further
transmission of TB to funeral directors during embalming? On the
surface, it appears that proper precautions were adhered to with the
use of masks, universal precautions, and a ventilation system that was
more than adequate. On closer investigation, however, it was discovered
that the masks routinely employed in this particular funeral home are
surgical masks, which provide no documented protection against the
spread of M tuberculosis. Furthermore, even though the
ventilation rate exceeded 25 air changes per hour, a rate that would
result in a removal efficiency of 99% of airborne contaminants after
only 11 min of use,11 turning off the exhaust fan
immediately after completing the embalming conceivably could leave
infectious particles in the air.
This case adds to a small, but growing, body of literature
pointing out the risk to funeral directors from TB. We
recommend that funeral directors be educated with regard to the
risks posed to them by TB and that further efforts be made to reduce
the risks of transmission to all mortuary workers.
Abbreviations: RFLP = restriction fragment length
polymorphism; RMR = rifampin monoresistant; TB = tuberculosis
Presented at the International Conference of the American Thoracic
Society, May 2000, Toronto, Ontario, Canada.
Special thanks to Michael A. McGarry, BA, Jeffrey
Driscoll, PhD, Linda Parsons, PhD, of the Wadsworth Center Laboratory
of the New York State Department of Health for their assistance in
providing the DNA data.
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