| This is the full text of the JAMA article.
source: http://jama.ama-assn.org/issues/v288n22/rfull/joc21393.html
(requires a subscription)
Secondary Aerosolization of Viable
Bacillus anthracis Spores in a Contaminated US Senate Office
Christopher P. Weis, PhD; Anthony J. Intrepido, MS, CIH; Aubrey K. Miller,
MD, MPH; Patricia G. Cowin, MS,
CIH; Mark A. Durno, BS; Joan S. Gebhardt, PhD; Robert Bull, PhD
Context Bioterrorist attacks involving letters and mail-handling
systems in Washington, DC, resulted in Bacillus anthracis
(anthrax) spore contamination in the Hart Senate Office Building and
other facilities in the US Capitol's vicinity.
Objective To provide information about the nature and extent of
indoor secondary aerosolization of B anthracis spores.
Design Stationary and personal air samples, surface dust, and
swab samples were collected under semiquiescent (minimal
activities) and then simulated active office conditions to estimate
secondary aerosolization of B anthracis spores. Nominal size
characteristics, airborne concentrations, and surface contamination
of B anthracis particles (colony-forming units) were
evaluated.
Results Viable B anthracis spores reaerosolized under semiquiescent
conditions, with a marked increase in reaerosolization
during simulated active office conditions. Increases were observed
for B anthracis collected on open sheep blood agar plates
(P<.001) and personal air monitors (P = .01) during active office
conditions. More than 80% of the B anthracis particles
collected on stationary monitors were within an alveolar respirable
size range of 0.95 to 3.5 µm.
Conclusions Bacillus anthracis spores used in a recent terrorist
incident reaerosolized under common office activities. These
findings have important implications for appropriate respiratory protection,
remediation, and reoccupancy of contaminated
office environments.
JAMA. 2002;288:2853-2858
On October 15, 2001, a letter containing threatening language and a
light tan powdery substance was opened in the mail
handling area of a Senate office suite in the Hart Senate Office Building,
Washington, DC. Federal officials removed the letter
and shut down the local air handling systems. The letter was transported
to the US Army Medical Research Institute of
Infectious Disease and was subsequently confirmed to contain viable
Bacillus anthracis (anthrax) spores that were dispersible
in air.1 Scanning electron microscopy of the spores used in the Senate
office attack showed that they ranged from individual
particles to aggregates of 100 µm or more. Spores were uniform
in size and appearance and the aggregates had a propensity
to pulverize1 (ie, disperse into smaller particles when disturbed).
Following the attack, nasal swabs were collected by other investigators
from more than 7000 building occupants and cultured
for B anthracis. Twenty of 38 individuals in the office suite where
the envelope was opened had positive nasal swab tests
including 13 individuals present in the vicinity of the mail area and
7 workers on an interconnected lower floor. Additionally, 2
workers from an adjacent office suite that entered an adjoining contaminated
hallway and 6 emergency responders who
entered the office or hallway had positive nasal swab tests.
The building was officially closed to the public on October 17, 2001,
with access to the contaminated suite limited to forensic
investigators only. This study was completed after forensic investigation
and prior to remediation of the Hart Senate Office
Building.
Information regarding primary aerosolization of B anthracis spores has
been reported,2-5 but few data are available regarding
secondary aerosolization indoors. The purpose of this investigation
was to evaluate secondary aerosolization of viable B
anthracis spores under both quiescent and active office conditions.
Understanding secondary aerosolization (reaerosolization)
of B anthracis spores in building environments is essential for exposure
assessment and risk evaluation following bioterrorism
attacks. Such understanding will also guide cleanup strategies for
readily dispersible bioaerosols.
METHODS
Environmental samples were collected in the affected Senate office suite
(total area approximately 1200 sq ft) beginning 25
days after the initial incident. Stationary and personal air samples
and surface samples were collected during 3 separate building
entries (Table 1). Initial semiquiescent sampling was followed by second
and third rounds of sampling under simulated active
office conditions. All analyses were conducted such that only viable
spores or spore aggregates were recorded.
During semiquiescent sampling, movement was minimized in the suite while
air and surface samples were collected from various
locations. During the semiquiescent sampling, the sample team (wearing
sterile gloves, boots, hooded protective suits, and
powered air purifying respirators with P.100 cartridges) placed sampling
devices in the locations indicated in Figure 1 and left
the suite to reduce air turbulence for the duration of the sample collection
period. Following semiquiescent sampling, active
office conditions were simulated to reflect routine behaviors in a
busy office environment (ie, paper handling, active foot traffic,
simulated mail sorting, moving trash containers, patting chairs). There
was no activity in the office suite several days prior to or
between sampling periods.
There are no validated environmental sampling or risk assessment methods
for B anthracis contamination. Questions regarding
collection techniques, laboratory extraction efficiency from environmental
media, and appropriate methods for air monitoring
remain unanswered. Accordingly, in this investigation a variety of
environmental sampling methods were used to assess their
usefulness for estimating environmental exposure and risk from B anthracis
spores. Samples and sample locations were based
on plausible exposure pathways (both inhalation and dermal) and were
selected based on proximity to the original release,
pedestrian traffic patterns within the suite, representative exposures
to the staff in the work area, and areas of interest for spore
transport within the office suite (eg, computer monitors).
Environmental sampling methods included air monitoring with stationary
and personal sampling devices (devices worn by the
sample team to characterize colony-forming unit [CFU] levels in their
breathing zone) that actively collected spores from a
known volume of air as well as open blood agar plates that passively
collected spores deposited from the Hart Senate Office
Building aerosol. Surface samples were collected to help characterize
the presence of B anthracis contamination on a variety
of surface types using both microvacuum devices and sterile swabs.
These environmental samples were collected under both
quiescent and active office conditions to assess the influence of human
movement within the suite on environmental spore
concentrations.
Andersen 6-stage viable (microbial) particle-sizing samplers (Thermo-Andersen,
Smyrna, Ga) were used to collect airborne
spores to evaluate concentrations and size ranges of spores or spore
aggregates. Andersen samplers were operated for 10
minutes at an air flow rate of 28.3 L/min during each sample collection
period. The Andersen sampler collects spores
according to nominal aerodynamic diameters on each of 6 vertically
stacked agar plates. Andersen samplers use petri dishes
filled with 42 mL of agar to control aerodynamics of particle impact
on plates according to manufacturer-specified cutoffs of
7.0, 4.7, 3.3, 2.1, 1.1, and 0.65 µm. For this investigation,
18 mL of 5% sheep blood agar (SBA) plates (Remel Inc, Lenexa,
Kan) were used for collection media. Use of reduced media volume resulted
in an increase in the specified jet-to-plate distance
of 0.3 cm with a corresponding increase of 0.3 µm in the particle
size cutpoints.6 Thus, the smallest particle impacting the
number 6 plate in the cascade would have a nominal diameter of 0.95
µm (ie, 0.65 µm + 0.3 µm).
For the semiquiescent and the first active testing period, 2 viable
Andersen impact samplers (6-stage) were used; 1 was placed
on the floor in the vicinity of the original contamination and 1 was
placed on the floor 20 feet away near the common entrance
to the suite (Figure 1). During the second active sampling period,
the 2 Andersen samplers were placed at the breathing zone
level in the same locations, and a specially configured 2-stage Andersen
sampler was placed at a floor location near the original
source zone. The final stage of this sampler was fitted with a glass
fiber filter to trap any remaining viable spores smaller than
the final impact stage (approximately 0.9 µm). At the end of
each sample collection period, Andersen samplers were
disinfected to avoid cross-contamination.
Direct colony counts on SBA plates in the Anderson samplers were obtained
and the positive hole correction method (Box)
was used to acquire a statistical probability count of CFUs (Table
2).
In addition to stationary air samples, personal air samples were collected
from the breathing zone of sample team members
during all 3 rounds of sampling. Sample pumps were calibrated to operate
at a flow rate of 4 L/min. The flow rate was not
intended to simulate respiratory minute ventilation but to provide
efficient deposition of spores on the collection media.
Collection media consisted of gelatin filters placed in 37-mm open-faced
filter cassettes and located in breathing zones of team
members for each sampling period. These cassettes are commonly used
for personal air monitoring applications and were
available with corresponding gelatin inserts conducive to the collection
and direct incubation of microbial samples. Sample
cassettes were placed on the front of the team members' suits just
below the shoulder and connected to a sampling pump worn
at the waist by a length of Tygon tubing (Saint-Gobain Performance
Plastics Corporation, Akron, Ohio).
Open plates were placed in workstations, on the floor, and within the
stairway to estimate spore settling during and following
various levels of human activity in the suite. Seventeen SBA plates
were placed in various locations and at various heights
throughout the office during the semiquiescent and the first active
sampling period. Ten plates were placed on office chairs, 3 at
various floor locations, and 4 on the steps of an internal office stairway
(Figure 1). Plates were opened for 45 minutes to
collect viable spores then closed and wrapped with parafilm.
A total of 17 surface samples were collected on fabric office dividers,
carpets, paper files, and near the source of the original
contamination. A microvacuum sampler was used to quantify the surface
loading of B anthracis on a variety of surface types.
Microvacuum samples were collected using personal air monitoring pumps
operated at a calibrated flow rate of 4 L/min. Filter
cowls containing gelatin filters with a nominal pore size of 3 µm
(having submicron retention efficiencies) were connected to the
pump with tubing to form a microvacuum device. Sampled areas were defined
by a 100-cm2 template, then vacuumed using a
slow back and forth motion first in one direction, and then perpendicular
to the original direction. Microvacuum samples were
collected at workstations in 5 different office areas during the second
active sampling period.
Swab samples were used to assess the presence of B anthracis contamination
on an additional 12 surfaces. Sterile nylon
swabs moistened with sterile water were used to sample both vertical
and horizontal surfaces as defined by 100-cm2
templates. Areas were swabbed in perpendicular directions using a slowly
progressing S-shaped motion and then placed in
sterile 15-mL tubes. Nine swab samples were collected for both the
semiquiescent and first active sampling periods: 3 vertical
semigloss latex painted surfaces (2 doors and 1 wall), 3 computer monitors,
and 3 individual mailboxes.
Aseptic handling techniques were used throughout the sampling and analytical
process. All samples were labeled immediately
following collection using predetermined sample codes. Samples were
placed in individual resealable bags and immediately
shipped to the analytical laboratory with blind identification codes
and under chain-of-custody. Field blank samples
(quality-control samples used to ensure adherence to sterile microbiologic
technique) were included at a frequency of 10%.
Samples were evaluated for the presence of viable B anthracis at the
Naval Medical Research Center in Silver Spring, Md.
Gelatin filters were removed from the filter cassettes and placed directly
on SBA plates. Swabs and glass fiber filters were
macerated in 3.0 and 7.5 mL, respectively, of sterile phosphate-buffered
saline for approximately 1 minute to free viable
spores. Following maceration, a 1.0-mL aliquot of each sample was removed
and heat shocked at 65°C for 15 minutes to
reduce viable vegetative bacteria in the sample. A 200-µL aliquot
of each heated sample was spread on an SBA plate and
plates were incubated at 37°C for 14 hours. Following incubation,
bacterial colonies morphologically consistent with B
anthracis were counted and recorded. Rapid real-time polymerase chain
reaction assays were used to confirm the identity of
suspect B anthracis colonies.8, 9 At least 1 suspect colony from each
plate was tested for the presence of the genetic markers
pag and cyaB, specific to the virulence plasmids pXO1 and pXO2, respectively.
Following polymerase chain reaction
confirmation of selected suspect colonies, the number of B anthracis
colonies on each plate was reported. Analyse-It
Software version 1.64 (Analyse-It Software Ltd, Leeds, England) was
used for statistical analyses and P<.05 was considered
significant. All sample team members were specially trained in response
to extremely hazardous environments and all
participation was voluntary. The US Federal Incident Command System
reviewed and approved the study. Incident Command
System is a system used to organize and manage participating groups
during emergency response situations.
RESULTS
Results for the 6-stage Andersen air samples are presented in Table
2. Positive hole correction results are presented below
where applicable. Comparison of floor samples between semiquiescent
and active conditions showed an increase in viable
spore collection across all sampler stages at both the mail area (48
vs >3006 total CFUs) and entrance area (71 vs 204 total
CFUs) locations. In the mail area, stationary Andersen breathing zone
samples showed an increase compared with
semiquiescent sampling taken previously at floor level (200 vs 48 total
CFUs). Estimated airborne spore concentrations
collected near the floor over a 10-minute period ranged from 171 to
251 CFUs/m3 during the semiquiescent period. For the
active period, airborne CFU concentrations ranged from 721 to more
than 11 000 and 106 to 707 CFUs/m3 for floor and
breathing zone samples, respectively. This represents as much as a
65-fold increase in CFUs under active conditions
compared with semiquiescent conditions. Approximately half of the CFUs
had corrected nominal diameters ranging from 1.4
to 2.4 µm, with more than 80% ranging from 0.95 to 3.5 µm.
Results from the 2-stage Andersen sampler indicated no viable
spores less than a corrected nominal diameter of 0.95 µm.
Locations and results of viable colony counts on the 17 open SBA plates
(10 on chairs; 7 on the floor) collected during
semiquiescent and active periods are shown in Figure 1. During the
semiquiescent period, 5 of the 17 plates were positive for
B anthracis (median, 0 CFU; range, 1-3 CFUs; 95% confidence interval
[CI], 0-1). In comparison, 14 of 15 plates (1 plate
was left in the suite and was desiccated beyond use) during the first
active sampling period were positive for B anthracis
(median, 15 CFUs; range, 4-80 CFUs; 95% CI, 11-28) illustrating a significant
increase in colony counts (P<.001; using a
2-tailed nonparametric Wilcoxon signed rank test).
Results of personal air monitor samples collected from team members
during each of the sampling periods are presented in
Table 3. Filters from all 10 of the samples were positive for B anthracis.
Results were positive for B anthracis during
semiquiescent office conditions (mean, 4 CFUs; range, 1-7 CFUs) and
increased during active office conditions (mean, 14
CFUs; range, 1-36 CFUs). There was a significant increase in the number
of CFUs collected on personal air samples during
the second active test period (P = .01; 1-tailed paired t test with
2 df) but not the first active test period (P = .17) when
compared with the semiquiescent sampling period. A 1-tailed statistical
test was used with the expectation that the number of
airborne viable CFUs would increase (rather than decrease) when activity
increased in the suite.
Six of the 9 surface swab samples taken during the semiquiescent and
first active period were positive; 3 vertical mailbox
surfaces (range, 3-43 CFUs) and 3 computer screens (range, 2-150 CFUs),
with little change in viable spore counts in
response to increased activity. Three swab samples collected from vertical
wall surfaces during each sampling period were
negative. During the second active sampling period, sequential swab
samples of a computer monitor screen sampled in the off,
then on position, resulted in a 25-fold increase in viable colony counts
on the charged screen. Deposition of spores on the
charged monitor may indicate influence of electrostatic effects on
spore behavior.
Additionally, 5 microvacuum samples were taken in different office areas
during the second period of activity to evaluate
contamination of different types of surfaces (Table 4). Although microvacuum
samples showed substantial viable spore
contamination of carpeted and smooth horizontal surfaces, very little
contamination of vertical fabric workstation dividers or the
tops of paper files was found. No CFUs were found on the field blanks
collected from any of the sample types during the
course of the investigation.
COMMENT
The importance of secondary aerosolization of B anthracis spores associated
with a bioterrorism attack has been discussed
by a number of researchers.10-14 However, few empirical data existed
to allow for scientifically based public health conclusions
or recommendations. Although research conducted by the military has
shown that Bacillus subtilis spores, used as a surrogate
for B anthracis, can reaerosolize with varying activities in outdoor
environments,13, 15 until now, no published data have been
available concerning secondary aerosolization of B anthracis spores
indoors. Prior to the attacks in the fall of 2001, consensus
recommendations from the Working Group on Civilian Biodefense11 suggested
only a slight risk of acquiring inhalational
anthrax by secondary reaerosolization from heavily contaminated surfaces.
These recommendations were based on an incident
involving accidental release of B anthracis in Sverdlovsk, Russia,5
occupational studies of workers in goat hair processing
mills,16 and modeling analyses by the US Army.12 The Working Group
on Civilian Biodefense recognized that its
recommendations were based on interpretation and extrapolation from
an incomplete knowledge base and needed to be
regularly reassessed as new information becomes available.11 A recent
reassessment by the consensus group includes a
precautionary note regarding reaerosolization of B anthracis spores
based, in part, on work presented here.17
This investigation presents empirical findings concerning secondary
aerosolization of viable B anthracis spores following a
bioterrorism incident indoors. Among the limitations of the work are
the severe schedule constraints, limited availability of
equipment, and the extreme conditions under which the investigation
was planned and implemented. Both empirically observed
and substantially increased spore concentrations were recorded on open
SBA plates during active conditions in the office suite.
Elevations of CFUs recorded on personal air monitoring devices during
active vs semiquiescent office conditions are consistent
with military investigations showing activity-related increases in
airborne spore exposures outdoors.13 However, the personal
air monitor data reported in this study are limited due to high variability
and small sample size.
During simulated activities, airborne concentrations of viable B anthracis
spores within the office ranged from 2 to 86
CFUs/m3 for personal air monitors and 100 to more than 11 000 CFUs/m3
for stationary Andersen samples, with more than
80% of the spores falling into the respirable range (<5 µm).
Relatively higher collection efficiencies on stationary monitors may
be due to sample locations within the contaminated suite, higher air
flow rates through the stationary sampling devices, or the
sample team personal monitors integrating exposure over both contaminated
and noncontaminated areas of the Hart Senate
Office Building (personal monitors were activated on entry to the building
6 floors below the contaminated suite).
Using a mean (SD) respiratory rate of 1.38 m3/h (0.66) reported for
office workers,18 estimated inhalation exposures to B
anthracis in the breathing zone were 119 and 250 CFUs/h for personal
air monitors and breathing zone Andersen samplers,
respectively. Based on CFU concentrations recorded by floor level Andersen
samplers, estimated exposures were as high as
15 000 CFUs/h. Additionally, findings of airborne B anthracis spores
during the initial semiquiescent sampling period suggest
that even minimal movements may result in resuspension of viable spores.
These findings were recorded almost a month
following the original incident, despite the removal of the contaminated
letter from the suite.
Determining the magnitude of inhalational risks from reaerosolized B
anthracis spores is uncertain. Reliable human data on the
minimum infective dose for inhalational B anthracis is lacking. Individual
susceptibility, virulence of the strain, and spore
physical characteristics may all have profound impacts on the dose
necessary to cause inhalational anthrax.3, 4 Primate model
extrapolations suggest an estimated human median lethal dose between
2500 and 55 000 spores,10 with the highest infectivity
associated with clouds of single spores, vs multispore aggregates.4
Recent primate studies have demonstrated inhalational
infectivity of B anthracis following exposure to only a few spores.19
Human cases of inhalational anthrax have also been
reported involving minimal exposures.16 Risk predictions indicate that
infective doses may be as low as 1 to 3 spores14 and
these predictions may be reflected in the 2 cases of inhalational anthrax
in New York and Connecticut still under
investigation.20
This work clearly demonstrates a potential for secondary aerosolization
of viable B anthracis spores originating from
contaminated surfaces in an indoor environment. As a result, precautions
to protect exposed decontamination workers and
area occupants are indicated.
Author/Article Information
Author Affiliations: US Environmental Protection Agency National Enforcement
Investigations Center, Denver Federal
Center, Denver, Colo (Dr Weis); US Army Center for Health Promotion
and Preventive Medicine, Aberdeen Proving
Ground, Md (Mr Intrepido and Ms Cowin); US Public Health Service, Denver,
Colo (Dr Miller); US Environmental
Protection Agency Region 5, Cleveland Office, Westlake, Ohio (Mr Durno);
and Naval Medical Research Center, Biological
Defense Directorate, Silver Spring, Md (Drs Gebhardt and Bull).
Corresponding Author and Reprints: Christopher P. Weis, PhD, US Environmental
Protection Agency National
Enforcement Investigations Center, Denver Federal Center, Bldg 53,
PO Box 25227, Denver, CO 80225 (e-mail:
weis.chris@epa.gov).
Author Contributions: Study concept and design: Weis, Miller, Durno.
Acquisition of data: Weis, Intrepido, Miller, Cowin, Durno, Gebhardt,
Bull.
Analysis and interpretation of data: Weis, Intrepido, Miller, Cowin,
Durno, Gebhardt, Bull.
Drafting of the manuscript: Weis, Intrepido, Miller, Cowin.
Critical revision of the manuscript for important intellectual content:
Weis, Miller, Durno, Gebhardt, Bull.
Statistical expertise: Weis, Miller.
Obtained funding: Weis.
Administrative, technical, or material support: Weis, Intrepido, Miller,
Cowin, Durno, Gebhardt, Bull.
Study supervision: Weis, Durno, Gebhardt, Bull.
Funding/Support: Funding and/or resources for this investigation were
provided by the participating federal agencies.
Disclaimer: The views, opinions, assertions, and findings contained
herein are those of the authors and should not be
construed as official US agency policies or decisions unless so designated
by other documentation. Any reference to products
or methods does not constitute an endorsement of those products or
methods by the authors or by the US federal government.
Acknowledgment: In support of this work, we graciously acknowledge the
US Capitol Police for their hospitality, sample
transport, and site security during the incident; the Capitol Hill
Incident Commander for spirited leadership and endless
encouragement; US Architect of the Capitol for providing tireless engineering
and architectural advice; US Environmental
Protection Agency management and especially the EPA On-Scene Coordinators;
Bill Daniels, MS, CIH, CSP, of the US
Public Health Service for invaluable advice on sampling, study design,
and detailed editorial recommendations; Chris Ansell,
MS, of Center for Health Promotion and Preventive Medicine for assisting
with project logistics; and the laboratory technicians
at Naval Medical Research Center for many hours of analysis.
Box. Positive Hole Correction Method
The positive hole correction method determines a statistical probablility
count of colony-forming units. It represents a count of
the jets that delivered the spores to the agar plates and the conversion
of the jet number to a particle count by using the
"positive hole" conversion formula7:
where Pr is the expected number of viable particulates to produce r
positive holes and N is the total number of holes per stage
(400). This formula is based on the principle that as the number of
viable particles being impinged on a given plate increases,
the probability of the next particle going into an unpenetrated hole
decreases. Thus, when 9 of 10 of the holes have each
received 1 or more particles, the next particle has but 1 chance in
10 of going into an unpenetrated hole. Therefore, on
average, 10 additional particles would be required to increase the
number of positive holes by 1.
(Return to text.)
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