Isolated case of bioterrorism-related inhalational anthrax, New York City, 2001.

Abstract

On October 31, 2001, in New York City, a 61-year-old female hospital employee who had acquired inhalational anthrax died after a 6-day illness. To determine sources of exposure and identify additional persons at risk, the New York City Department of Health, Centers for Disease Control and Prevention, and law enforcement authorities conducted an extensive investigation, which included interviewing contacts, examining personal effects, summarizing patient's use of mass transit, conducting active case finding and surveillance near her residence and at her workplace, and collecting samples from co-workers and the environment. We cultured all specimens for Bacillus anthracis. We found no additional cases of cutaneous or inhalational anthrax. The route of exposure remains unknown. All environmental samples were negative for B. anthracis. This first case of inhalational anthrax during the 2001 outbreak with no apparent direct link to contaminated mail emphasizes the need for close coordination between public health and law enforcement agencies during bioterrorism-related investigations.

Full text

Page 1

On October 31, 2001, in New York City, a 61-year-old
female hospital employee who had acquired inhalational
anthrax died after a 6-day illness. To determine sources of
exposure and identify additional persons at risk, the New
York City Department of Health, Centers for Disease
Control and Prevention, and law enforcement authorities
conducted an extensive investigation, which included inter-
viewing contacts, examining personal effects, summarizing
patient’s use of mass transit, conducting active case finding
and surveillance near her residence and at her workplace,
and collecting samples from co-workers and the environ-
ment. We cultured all specimens for Bacillus anthracis. We
found no additional cases of cutaneous or inhalational
anthrax. The route of exposure remains unknown. All envi-
ronmental samples were negative for B. anthracis. This first
case of inhalational anthrax during the 2001 outbreak with
no apparent direct link to contaminated mail emphasizes
the need for close coordination between public health and
law enforcement agencies during bioterrorism-related
investigations.
A
(NYC) became a preeminent concern at the Department of
Health (DOH). Active syndromic surveillance at emer-
gency department for bioterrorism-related illnesses was
initiated in 15 hospitals, and frequent broadcast alerts were
sent by email and fax to all NYC emergency departments,
commercial and hospital laboratories, infection-control
programs, and selected providers (1).
After the announcement of the inhalational anthrax
index case in Florida on October 4 and the cutaneous
anthrax index case in NYC on October 12, DOH enhanced
its active surveillance activities citywide (2). Detailed
diagnostic and treatment protocols were provided through
fter the World Trade Center attack on September 11,
2001, the possibility of bioterrorism in New York City
a broadcast alert system and the DOH website to the med-
ical and laboratory community, including emergency
departments, intensive-care units, infectious disease and
infection-control specialists, dermatologists, and laborato-
ries. A provider hotline was established for rapid referral
and evaluation of suspect cases. Broadcast fax alerts also
were sent to veterinarians to request reporting of suspect
animal cases. In addition,
department–based syndromic surveillance system was
expanded to 29 hospitals to augment DOH’s ability to
detect a large, covert bioterrorist event. The medical exam-
iner’s office was asked to notify DOH of any suspicious
deaths from unexplained sepsis or respiratory causes.
During October, four simultaneous investigations were
conducted at news media outlets where cutaneous anthrax
cases were detected among employees (M. Phillips, et al.,
unpub. data). All interviews were performed by teams of
the emergency
Emerging Infectious Diseases • Vol. 9, No. 6, June 2003689
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Isolated Case of Bioterrorism-
related Inhalational Anthrax,
New York City, 2001
Timothy H. Holtz,*† Joel Ackelsberg,† Jacob L. Kool,‡ Richard Rosselli,† Anthony Marfin,‡
Thomas Matte,*§ Sara T. Beatrice,† Michael B. Heller,† Dan Hewett,* Linda C. Moskin,†
Michel L. Bunning,‡¶ Marcelle Layton,† and the New York City Anthrax Investigation Working Group1
*Centers for Disease Control and Prevention, Atlanta, Georgia,
USA; †New York City Department of Health, New York, New York,
USA; ‡Centers for Disease Control and Prevention, Fort Collins,
Colorado, USA; §New York Academy of Medicine, New York, New
York, USA; and ¶Office of the Surgeon General, Bolling Air Force
Base, Washington, D.C., USA
1New York City Anthrax Investigation Working Group: New York City
Department of Health: Sharon Balter, Katie Bornschlegel, Darcy Carr, Neal
Cohen, Debjani Das, Annie Fine, Jane Greenko, Laura Mascuch, Benjamin
Mojica, Farzad Mostashari, Denis Nash, Beth Nivin, Sheila Palevsky, Sarah
Perl, Michael Phillips, Jeanine Prud’homme, Barbara N. Samuels, Karen
Schlanger, Polly Thomas, Isaac Weisfuse, Don Weiss; New York City Public
Health Laboratory: Alice Agasan, Joselito Amurao, Josephine Atamian,
Debra Cook, Erica DeBernardo, Philomena Fleckenstein, Anne Marie
Incalicchio, Ed Lee, William Oleszko, Lynn Paynter, Chiminyan
Sathyakumar, George Williams, Marie T. Wong, Ben Yang Zhao; Lenox Hill
Hospital: Dilcia Ortega, Sarah Petrello, Michael Tapper; Centers for Disease
Control and Prevention/Division of Vector-Borne Diseases: May Chu, David
Dennis, Kathleen Julian, Lyle R. Petersen; National Institute of Safety and
Health: Josh Harney, Robert McCleery, Ken Martinez; Centers for Disease
Control and Prevention: McKenzie Andre, Mick Ballesteros, Mary Brandt,
Shadi Chamany, Daniel Feikin, Collette Fitzgerald, Jessica Gardom, Alex
Hoffmaster, Kristy Kubota, Richard Leman, Naile Malakmadze, Els Mathieu,
Leonard Mayer, Shawn McMahon, Juliette Morgan, Tim Naimi, Steve
Ostroff, John Painter, Harald Pietz, Tanya Popovic, Joe Posid, Efrain Ribot,
Dejana Selenic, Tanya Sharpe, Montserrat Soriano-Gabarro, Allison Stock,
Phil Talboy, Sara Whitehead, William Wong, Weigong Zhou; University of
North Carolina Medical School: Manoj Menon; U.S. Department of Defense:
Francis S. Baluyot, Marcelo V. Bayquen, Monicka J. Boyd, Lisa A. De Los
Santos, Martin E. France, Lora L. Galloway, Theron J. Hudson, Angel
Lorenzo, Ludwig Mantay, Patrick H. Murray, Debra M. Niemeyer, Len
Peruski, Christopher M. Sekula; New York City Police Department: Michael
T. Corr, Kevin G. Frazer, John Galasso, Evelyn M. Harris, Joseph M.
Herbert, Kevin J. Kehoe, Patrick E. Pogan, Phil T. Pulaski, Joseph J.
Reznick; Port Authority of New York and New Jersey Police Department:
Michael J. Podolak; Federal Bureau of Investigation: William P. Hyland,
Gregory Jones, Howard Leadbetter II, Anthony Willett, and William A.
Zinnikas.

Page 2

investigators from DOH, Centers for Disease Control and
Prevention (CDC), and law enforcement on the basis of
pre-established agreements between DOH and the New
York field office of the Federal Bureau of Investigation
(FBI), and its associated Joint Terrorism Task Force (a task
force between the NYC Police Department and FBI). By
the end of October 2001, seven laboratory-confirmed or
suspected cutaneous anthrax cases had been reported in
NYC. All case-patients were thought to have been exposed
through direct contact with contaminated mail addressed
to media outlets and postmarked on September 18 (3). The
last known contaminated letters were postmarked on
October 9 from Trenton, New Jersey, to Senators Thomas
Daschle and Patrick Leahy in Washington, D.C.
Case Confirmation
On October 28, 2001, a local hospital reported a sus-
pected case of inhalational anthrax to DOH. The case-
patient was a 61-year-old female with a 3-day history of
progressive weakness, chest heaviness, myalgia, cough,
and shortness of breath. She was admitted to intensive care
with respiratory failure, emergently intubated before being
interviewed, and treated with multiple antibiotics and
diuretics for a presumptive diagnosis of community-
acquired pneumonia, congestive heart failure, or inhala-
tional anthrax (4). On October 29, nonmotile, gram-posi-
tive rods in long chains were isolated from routine blood
cultures, and her antibiotic therapy was adjusted to provide
for enhanced coverage of inhalational anthrax. That
evening, Bacillus anthracis was preliminarily identified
from her blood culture isolate and from pleural, fluid, and
bronchial washings by polymerase chain reaction (PCR) at
the DOH Public Health Laboratory and CDC. The follow-
ing day, pleural and blood isolates were confirmed as B.
anthracis by gamma phage lysis and direct fluorescent
antibody testing. The case-patient died on October 31. B.
anthracis isolates were subtyped at CDC by multiple-locus
variable-number tandem repeat analysis (MLVA) and
sequencing of the pagA gene. All isolates were MLVA
genotype 62 and pagA genotype I, the same genotype as
all other isolates from the 2001 anthrax outbreak in
Florida, New Jersey, Washington, D.C., and Connecticut
(5).
We report the results of the epidemiologic and environ-
mental investigation by DOH, CDC, and local and federal
law enforcement agencies in response to this isolated case
of inhalational anthrax. The objectives of our investigation
were to determine the time, location, and route of expo-
sure; to identify any additional cases of cutaneous or
inhalational anthrax; to determine whether this case was an
isolated case or sentinel case of a larger outbreak; and to
guide our public health response.
Methods
Case Investigation
Immediately after confirming the case-patient’s diagno-
sis, epidemiologists from DOH and CDC and a detective
and special agents from the Joint Terrorism Task Force
formed joint investigative teams to ensure the rapid and
efficient sharing of relevant information between the epi-
demiologic and criminal investigations. To identify the
time and location where the case-patient might have been
exposed to anthrax during the 60 days before illness onset,
detectives from the NYC Police Department and FBI along
with local and federal epidemiologists performed joint
interviews of the patient’s social, work, and neighborhood
contacts. We chose a 60-day period on the basis of the
range of the inhalational anthrax incubation period during
the Sverdlovsk anthrax outbreak in 1979 (6). We conduct-
ed regular interagency meetings to analyze new informa-
tion collaboratively and strategize about the next steps of
the investigations.
We collected information about the case-patient’s
habits and activities through interviews with co-workers,
neighbors, acquaintances, and a mail carrier to uncover
any potentially relevant personal details, including places
she frequented, and her social contacts. Investigators
searched the case-patient’s apartment, examined personal
effects, reviewed telephone and financial records, and vis-
ited four post offices that she was known or thought to
have used. To locate persons who might have information
regarding activities during the incubation period, we dis-
played the case-patient’s photograph in churches that she
reportedly attended and in Chinatown, which she frequent-
ed. Employees from 15 businesses near the case-patient’s
apartment complex and work were interviewed. Members
of the NYC Anthrax Investigation Team also met with
investigators of the other unexplained inhalational case in
Connecticut (7).
Using the identification number from a subway transit
card issued to the case-patient by the New York City
Metropolitan Transportation Authority (MTA), we
obtained data about her transit activity from October 22 to
October 26, indicating which buses and subway stations
she entered in the week before onset of illness. The MTA
also identified a previous transit card number with board-
ing times that matched the pattern of subway use linked to
her card. Using this information, we were able to approxi-
mate her bus and subway travel during the previous month
(September 21–October 20).
Case Finding
Our investigation included active case finding and sur-
veillance for additional anthrax cases at the case-patient’s
workplace and in her apartment complex. We asked all co-
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workers, patients, and visitors who had spent >1 hour at her
workplace during the preceding 2 weeks to report for an
interview; at the interview, they were offered antibiotic pro-
phylaxis. We also used the following information to identi-
fy additional suspect cases: 1) the hospital’s employee
health department list of all employees who had been eval-
uated for fever during the previous 2 weeks; 2) the human
resources department list of employees who had missed >1
day of work during this period; 3) interviews regarding
symptoms in occupants from 27 of 28 of the neighboring
apartments in her complex; and 4) a community meeting in
the case-patient’s Bronx neighborhood in which the case
was discussed and neighbors were encouraged to report ill-
nesses or skin lesions suggestive of anthrax.
In addition, active surveillance for suspect cases was
established with the U.S. Postal Service and MTA in NYC
because of concern regarding potential exposures in post
offices, from mail, or in the subway system. Any ill
employee was contacted by DOH staff by telephone and
asked about symptoms. Any suspect cases were referred
for immediate evaluation and follow-up.
Environmental and Laboratory Investigation
To search for evidence of a recent exposure to
aerosolized anthrax-containing particles, we collected both
nasal swabs and environmental samples. On October 29,
we collected nasal swabs from 28 co-workers who worked
near the case-patient. We used four sampling techniques
for environmental surface samples: dry Bacti-swab (Remel
Inc., Lenexa, KS) sampling, wet swabs, composite dry
swabs, and HEPA vacuum samples (8).
From October 29 through December 12, sampling was
performed in and around the case-patient’s apartment and
from selected personal effects: from the hospital where she
worked, with an emphasis on the mail bins, mailroom, and
stockrooms she frequented; in an acquaintance’s apartment
where she had slept during the incubation period; from a
neighborhood post office where she had purchased a postal
money order 2 days before illness onset; from three mail-
processing facilities and two post offices that served her
home and workplace; and from two businesses near her
apartment complex (Table). Subway stations were selected
for sampling on the basis of the pattern of her subway use
gleaned from her MTA transit card (Figure). Nasal swabs,
bulk specimens, dry surface swabs, composite swabs, and
vacuum sock samples were analyzed by the DOH Public
Health Laboratory and the U.S. Department of Defense by
using standard culture techniques and PCR analysis (9).
Mail Investigation
We obtained data from the U.S. Postal Service on the
final destinations for first-class mail sorted from October 9
to October 16 on the same digital bar code–sorting
machine in the Trenton, N.J., processing and distribution
center that sorted the letters addressed to Senators Daschle
and Leahy. Bulk mail is presorted and not labeled with
codes. We focused on first-class mail that was then deliv-
ered to the same zip codes as our case-patient’s home and
work addresses.
Public Health and Prevention Activities
On October 30, in conjunction with the hospital, DOH
established an antibiotic prophylaxis clinic for persons
who were considered at potential risk for inhalational
anthrax; at this time, we expanded the initial prophylaxis
given to include the 28 staff persons who worked in the
hospital basement near the stockroom and mailroom (10).
All co-workers, patients, and visitors who had spent >1
hour at the case-patient’s workplace in the preceding 2
weeks were recommended for antibiotic prophylaxis eval-
uation. Initially, persons were offered 10 days of doxycy-
cline or ciprofloxacin (11), pending results from the epi-
demiologic and environmental investigations to determine
whether the hospital was the site of exposure. We offered
amoxicillin to children on the basis of the susceptibility
pattern of the other B. anthracis isolates associated with
this outbreak (following CDC guidelines) (12).
Results
Case Investigation
The case-patient was a resident of an apartment in a
predominately Hispanic section of the Bronx; she lived
alone. She had no known family members in NYC and a
limited number of close acquaintances. A refugee from
Vietnam, she had lived in the United States for 26 years.
Her acquaintances at work and in her neighborhood report-
ed her daily routine and usual activities to be habitual, with
a regular work schedule, visits to Chinatown in Manhattan
to shop, and trips to post offices and department stores near
her workplace and home. Although reportedly friendly and
generous, she lived a solitary life. Her apartment was clean
and tidy. We collected no information suggesting that she
had traveled outside NYC during the 60-day period before
onset of illness. Neighbors did not recall any recent visi-
tors to her home. From information received from MTA,
we ascertained that she rode the No. 6 Lexington Avenue
subway almost daily, traveling from her home in the Bronx
to her workplace in Manhattan (Figure).
She had worked full time in an East Side Manhattan
hospital for 12 years, delivering supplies from basement
stockroom to clinics and wards within the hospital. She
had not missed any work in the several weeks before onset
of illness. She did not directly work with or sort mail. The
hospital’s mail was sorted in a section of one of these
stockrooms, where it was placed into wooden mail slots.
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692Emerging Infectious Diseases • Vol. 9, No. 6, June 2003
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Table. Summary of environmental test sampling in inhalational anthrax investigation, New York City, 2001
Date in
2001
Location
Case-patient’s hospital workplace: old
and new mail room keyboard, and air-conditioning air-intake filters
Case-patient’s workplace: workroom,
basement rooms, and elevator and ceilings
Admitting hospital
Case-patient’s clothing and personal property from
admission
Case-patient’s workplace Nasal swabs of hospital coworkers
10/30 Case-patient’s apartment
Appliance tops, mail bins, table tops, post office receipts,
window sills, light fixtures, trash cans, and bank cards
10/31
Case-patient’s workplace locker and
workspace belongings), elevator exhaust blades and cages, air-
intake grills, door jambs, and computer cooling fans
Manhattan post office A
Computer fan intakes, light fixtures, teller computer
monitors, air-intake grills, counter surfaces, and vacuum
sample of multiple mail-sorting cubbies
Case-patient’s apartment
Mailbox, adjacent mailboxes, elevator fans, refrigerator,
baseboards, personal items, clothes hampers, television
screen, boxes containing recent mail, light fixtures,
vacuum cleaner dust, and cooling fans
Case-patient’s apartment
Closet, hanging garments, bedroom clothes, and hallway
bureau
Personal items from case-patient’s
apartment pictures, and stuffed animal
Office of the Chief Medical Examiner Autopsy room, sink, table, cutting floor, and floor
Bronx post office A
Multiple mail slots, sorting areas, and intake grills of
ventilation systems
Manhattan post office B
Mail-sorting areas and ventilation system, fluorescent
light fixtures
11/3
Case-patient’s workplace (basement
storage) filters, pipes
Bronx mail sorting and distribution
center system, manual sorting stations, dead-letter repository,
digital bar code sorters (including the machine that sorts
mail to case-patient’s home), overhead air filters
Bronx parcel post office B Sorting stations, registered mail cage and delivery trucks
Case-patient’s apartment Powder samples
Bronx post office box A Case-patient’s post office box
Friend’s home Dining room and bedroom surfaces
Case-patient’s workplace (basement
storage)
Case-patient’s workplace work station Fan, light, and pipe
11/6
Case-patient’s personal effects from
apartment
Subway line, #6 Lexington Ave line
(including Grand Central Station) and 1
N/R station used by case-patient conditioner system in Grand Central Station
Four subway stations not known to be
used by case-patient (control stations)
11/30
Two businesses near to case-patient’s
apartment that received mail from
Trenton postmarked October 9
12/12
Case-patient’s personal effects from
apartment associated with hypothesized
exposure locations or pathways mid-October including mail, money orders, bank
withdrawal slips, receipts, phone, and perfume bottles
Total
aLeft column indicates the date samples were taken. Aggressive sampling was performed by intensively and individually vacuuming each item by using a HEPA filter
vacuum sock. Collected material was processed through a membrane to selectively remove extraneous material (e.g. hairs, which can be saved for later forensic
examination) and concentrate spores in the filtrate. Filtrate was then analyzed by polymerase chain reaction and cultured for Bacilllus anthracis. Material in perfume bottles
was cultured directly. Tests on samples were completed on 12/12/2001.
Items
Wet
swabs

Dry
swabs
10
Vacuum
filters

Mail cubby spaces, air intake, lights, desk top, computer
Desk tops, floor, lighting and vents, door casings, walls,
24
7
10/29


28
40


Locker contents (clothing, shoes, lab coat, personal
52 4
12 1
29
8
Slippers, shoes, hats, pieces of recent mail, address book,
9
11/1


31
15

3 11/2
9
Door jams, light fixtures, conduits, air-conditioner intake
8
Optical character readers, air intake of ventilation
25






8
9
1
2
7





11/4
Storage lockers, urinal, plumbing, switches, and bulbs
11/5


5
1

Unspecified substance in case-patient’s wallet
Multiple dust-collecting areas along platform and
multiple air-intake filters of recently installed air-
120 19 11/11
Multiple dust-collecting areas along platform 76
Mail bins, scissors, letter openers, desk, phone, window,
computer, air-conditioner, and copier
40
Coat, shoes, tennis shoes, slippers, hats, scarf and lab
coat, hospital identification card, documents dated in
18
196 372 53
a

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The mailroom and stockroom staff reported no suspicious
packages or letters.
We constructed a timeline of her activities in the sever-
al weeks preceding her illness. Although her subway tran-
sit card, work records, financial records, and sales receipts
allowed us to account for some of her activities, approxi-
mately 40% of the nonwork-related hours before her death
remained unaccounted for. The criminal investigation
found no suspicious letters or activity to connect the case-
patient to any of the known anthrax-laden postmarked let-
ters, and no evidence existed that she had visited any of the
media sites in NYC affected by this outbreak. Shared
information with the investigators in Connecticut indicat-
ed that she and the case-patient in that state had little in
common.
Case Finding
A total of 232 coworkers, occupants from 27 of 28
neighboring apartment units, 35 acquaintances, and 1,675
hospital patients and visitors were screened for symptoms
of cutaneous or inhalational anthrax in connection with
this single case. A total of 69 persons with respiratory
symptoms and 21 with suspicious skin lesions were fol-
lowed up by medical evaluation or telephone call. None of
these persons were diagnosed with inhalational or cuta-
neous anthrax.
We contacted all hospital employees listed as ill on
absentee (n=60) and employee health (n=88) lists and
found them to have recovered from minor illnesses or
injuries. Enhanced surveillance in NYC hospitals, the U.S.
Postal Service, and emergency departments in NYC have
continued since 2001 to 2003. No further cases of anthrax
have been identified in NYC.
Environmental Investigation
All 621 environmental samples tested negative for B.
anthracis by culture and PCR: workplace (n=138), apart-
ment (n=86), personal effects (n=35), an acquaintance’s
apartment (n=2), businesses near her apartment (n=40),
post offices (n=74), the Office of the Chief Medical
Examiner (n=31), and subway (n=215) (Table).
Mail Investigation
The U.S. Postal Service identified letters delivered to
the case-patient’s work address, but not to her home
address, that were postmarked on October 9 in Trenton and
sorted by the same digital bar code–sorting machine as the
letters sent to Senators Daschle and Leahy. However, all
other hospitals with the same zip code as her workplace
and many other places in the city also received mail post-
marked on October 9 by this same machine. The closest
location to her home where an October 9–postmarked let-
ter from the Trenton facility was delivered was a commer-
cial property two blocks from her apartment complex. No
letters postmarked October 9 were identified at the two
businesses located at this property, no persons at either
business had been ill with symptoms suggestive of anthrax
infection, and all environmental samples were negative.
Five digital bar code–sorting machines at the main
Manhattan postal distribution center tested positive for B.
anthracis in late October during the initial investigation of
the media-related cutaneous cases. None of these five con-
taminated machines routinely performed final sorting of
mail for the 5-digit zip codes that included the case-
patient’s home and workplace. The sorting machines that
routinely sorted mail sent to the case-patient’s workplace
and home zip codes tested negative.
Public Health Intervention
On the recommendation of DOH, the local hospital
where the case-patient worked closed voluntarily for 10
days after her diagnosis. DOH and local hospital screened
and offered prophylaxis for anthrax to 232 coworkers and
1,675 hospital patients and visitors beginning on October
29. After all of the initial environmental samples at the
case-patient’s workplace tested negative and no addition-
al suspect cases were identified, DOH recommended that
Emerging Infectious Diseases • Vol. 9, No. 6, June 2003693
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Figure. Key Manhattan and Bronx locations during investigation of
inhalational anthrax, New York City, 2001.

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all persons discontinue antibiotic prophylaxis on
November 7.
Discussion
This investigation focused on the first and only case of
inhalational anthrax in NYC during the 2001 anthrax out-
break. This case was the first of two that occurred during
this outbreak that did not have an apparent direct link to
contaminated mail (13). No other confirmed cutaneous or
inhalational anthrax infections associated with this case
were identified during the 2001 outbreak. The timing,
location, and route of the case-patient’s exposure remain
unknown. Our epidemiologic and environmental investi-
gations yielded no firm indications regarding when, where,
how, or why this case-patient was infected. Despite con-
cern that she might represent the sentinel case of a much
larger outbreak, subsequent surveillance showed that this
case was probably an isolated case of inhalational anthrax
and not part of a larger local outbreak.
During this investigation, we considered multiple hypo-
thetical scenarios to explain how the case-patient could
have been exposed to B. anthracis. Natural exposure was
thought to be unlikely because the last case of naturally
acquired anthrax in NYC occurred in 1947, the case-
patient had no known risk factors for natural infection, and
her isolate was genotypically indistinguishable from other
isolates from the 2001 anthrax outbreak. Although expo-
sure to an intentionally contaminated letter was considered
the most likely hypothesis from the onset, our case-patient
had none of the risk factors for anthrax infection identified
among earlier cases (e.g., working for the news media or
government, handling mail) (14). Other less likely expla-
nations for her death—that she was associated with the ter-
rorists or targeted purposely, that she was present when a
small-scale attack intentionally occurred, or that she hap-
pened to pass by when a small amount of anthrax spores
were accidentally released by the perpetrator—were con-
sidered, but no evidence supporting these hypotheses was
discovered. In the absence of any data to support alterna-
tive hypotheses, and consistent with the hypothesis raised
in the Connecticut case that contact with cross-contaminat-
ed bulk mail accounted for exposure (7), we think that this
hypothesis is also reasonable for our NYC case. However
we found no direct evidence to support or to refute it.
We cannot definitively conclude, however, that con-
taminated or cross-contaminated mail was the mechanism
of exposure in this isolated case. First, the case-patient was
not linked to a known contaminated or threat letter, and
environmental testing did not provide any evidence of
anthrax spores in her home or workplace. Second,
although some potentially cross-contaminated mail from
the contaminated digital bar code–sorting machine in
Trenton was delivered to her workplace and to an address
two blocks from her apartment, similar mail was sent to
thousands of other locations in NYC, the metropolitan
area, and nationwide. Only one other additional inhalation-
al case was identified in the United States after this case
(13). More cases of cutaneous or inhalational anthrax
might be expected if cross-contaminated mail were the
mechanism of transmission for our case-patient.
We also found no evidence of inhalational anthrax
cases in the areas where the most heavily contaminated
postal distributional centers were located in Washington,
D.C., and New Jersey. Moreover, the two unexplained
cases in NYC and Connecticut occurred several weeks
after the last known contaminated letters were postmarked.
Why cases that might have been caused by cross-contami-
nated mail did not occur closer to the time that cross-con-
tamination likely occurred remains unclear. Although our
surveillance may have missed a nonhospitalized person ill
with anthrax, no other inhalational cases were identified
nationwide. Therefore, if cross-contaminated mail was the
source for these two last inhalational cases, the risk for ill-
ness after exposure to low levels of spores on secondarily
contaminated mail is low, given that potentially millions of
letters might have had low-level contamination (15) based
on the positive environmental findings in numerous postal
facilities during the 2001 anthrax outbreak.
We decided to close the case-patient’s workplace sever-
al hours after her definitive diagnosis. Four factors were
involved in this early decision: 1) whether the hospital was
the site of recent aerosolized anthrax was unclear, 2) our
case had no obvious link to exposure through the mail, 3)
environmental testing was facilitated by a closed facility,
and 4) closure put the fewest possible people at risk for
further exposure. We benefited from decisions made in
other states during other anthrax investigations in the pre-
ceding weeks. After the final results of the environmental
sampling were available, the hospital was reopened on
November 6.
Our entire investigation lasted 6 weeks and involved
>100 local, state, and federal investigators. The bulk of the
environmental sampling was completed within 7 days,
although subway sampling began 2 weeks after the case-
patient went to the hospital (Table). The case-patient’s hos-
pital workplace was not forced to close permanently, and
employees were back at work 10 days after she was diag-
nosed.
Some limitations exist in our investigation of this case.
The case-patient’s rapid death prevented investigators
from interviewing her directly to assess potential sources
of exposure, including contact with suspicious mail or per-
sons. Given the absence of additional inhalational cases in
NYC for comparison, we could only speculate about the
activities that represented risk factors for her infection.
Unlike the subsequent Connecticut inhalational anthrax
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case, we could not account for a large proportion of our
case-patient’s time when exposure could have occurred.
Low-level contamination from mail in her home, work-
place, or NYC postal facilities may also have been cleaned
up before environmental testing during the 16-day period
after these letters were processed. Finally, our environmen-
tal sampling strategy was based on the assumption that an
aerosol release of B. anthracis at any of the locations
would have resulted in evidence of environmental contam-
ination detectable by the methods used.
All aspects of the epidemiologic and environmental
investigation (e.g., interviewing, collecting samples, inter-
preting results, developing strategy) occurred through
active collaboration with multiple local and federal part-
ners, including public health and law enforcement agencies
and the involved healthcare facilities. Our investigation
underscores how pre-existing relationships and preplanning
among local response agencies fosters the coordination and
collaboration needed between the parallel epidemiologic
and criminal investigations during an acute crisis (16).
This case also emphasizes the important roles that epi-
demiologic and environmental investigations play in shap-
ing decisions regarding appropriate antibiotic prophylaxis
during suspected bioterrorist events. Co-workers, patients,
and hospital visitors were initially offered antibiotic pro-
phylaxis when we were uncertain whether an aerosolized
release had occurred in her workplace. Given the short
incubation period for inhalational disease and the high
death rate if treatment is not started early, we decided to
initially offer antibiotic prophylaxis to potentially exposed
persons. After the initial investigation failed to identify
additional suspected cases or any evidence of anthrax
spores in the case-patient’s work environment, we recom-
mended discontinuing antibiotics. If any of the environ-
mental samples collected from her workplace had yielded
B. anthracis isolates, we would have extended the duration
of prophylaxis to >60 days to those persons deemed to be
at risk for inhalational disease on the basis of the location
of the positive results. The liberal use of broad antibiotic
prophylaxis earlier in the 2001 anthrax outbreak is thought
to have prevented many cases of inhalational anthrax (17).
Our investigation provided a number of lessons for
future such investigations. We learned that a rapid and
adaptive decision-making process regarding scientific
issues is necessary and that this process must use both gov-
ernmental and academic advisors. Laboratory surge capac-
ity is required to continue vital public health activities and
respond to a crisis, and surveillance systems for bioterror-
ism incidents are needed that can be used routinely with
familiarity by staff. Health department staff must be famil-
iar with environmental testing and decontamination;
proactive information management with early media pres-
ence and key officials who are informed is essential.
DOH, in cooperation with multiple local and federal
agencies, investigated a single, fatal case of inhalational
anthrax whose genotypic similarity to other cases of inten-
tional anthrax in the 2001 anthrax outbreak indicates it was
bioterrorism-related. The place and route of exposure to B.
anthracis in this isolated case remain unknown. Unless the
criminal investigation yields further answers, we will like-
ly never know the source of infection or method of expo-
sure in this case. This case highlights the challenges in
explaining single bioterrorism-related illnesses with stan-
dard epidemiologic and environmental methods and
underscores the need for coordination between public
health officials and law enforcement agencies during
bioterrorism-related investigations.
Acknowledgments
We thank the public health workers from local, state, and
federal agencies who responded to the anthrax outbreak in New
York City during 2001. We specifically thank Brad Perkins,
David Ashford, Marc Fischer, Julie Gerberding, James Hughes,
and Jeffrey Koplan for their leadership and guidance. We also
thank E.E. Peterson for laboratory support, Susan Resnick for her
assistance in mapping, and Daniel O’Connell for his support and
insight.
Dr. Holtz is a medical epidemiologist in the Division of
Tuberculosis Elimination at the Centers for Disease Control and
Prevention (CDC). From 1999 to 2001, he served as an Epidemic
Intelligence Service officer for the Malaria Epidemiology
Branch, CDC, after which he completed a preventive medicine
residency through the CDC at the NYC Department of Health.
He was an active participant in the public health response to the
World Trade Center disaster and served as one of many epidemi-
ologists investigating the anthrax outbreak in New York City in
2001.
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Address for correspondence: Timothy H. Holtz, Division of Tuberculosis
Elimination, NCHSTP Centers for Disease Control and Prevention, 1600
Clifton Road, Mailstop E10, Atlanta, GA 30333, USA; fax: 404-639-
1566; email: tkh3@cdc.gov
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