Am. J. Trop. Med. Hyg., 86(4), 2012, pp. 703–710
Copyright © 2012 by The American Society of Tropical Medicine and Hygiene
Anthrax Outbreaks in Bangladesh, 2009–2010
Apurba Chakraborty,* Salah Uddin Khan, Mohammed Abul Hasnat, Shahana Parveen, M. Saiful Islam,
Andrea Mikolon, Ranjit Kumar Chakraborty, Be-Nazir Ahmed, Khorsed Ara, Najmul Haider, Sherif R. Zaki,
Alex R. Hoffmaster, Mahmudur Rahman, Stephen P. Luby, and M. Jahangir Hossain
Centre for Communicable Diseases, International Centre for Diarrheal Disease Research, Bangladesh, Dhaka, Bangladesh;
Institute of Epidemiology Disease Control and Research, Dhaka, Bangladesh; Department of Livestock Services,
Ministry of Fisheries and Livestock, Dhaka, Bangladesh; Centers for Disease Control and Prevention, Atlanta, Georgia
human anthrax in Bangladesh to identify the etiology, pathway of transmission, and social, behavioral, and cultural
factors that led to these outbreaks. The team identified 140 animal cases of anthrax and 273 human cases of cutaneous
anthrax. Ninety one percent of persons in whom cutaneous anthrax developed had history of butchering sick animals,
handling raw meat, contact with animal skin, or were present at slaughtering sites. Each year, Bacillus anthracis of
identical genotypes were isolated from animal and human cases. Inadequate livestock vaccination coverage, lack of
awareness of the risk of anthrax transmission from animal to humans, social norms and poverty contributed to these
outbreaks. Addressing these challenges and adopting a joint animal and human health approach could contribute to
detecting and preventing such outbreaks in the future.
During August 2009–October 2010, a multidisciplinary team investigated 14 outbreaks of animal and
Anthrax is an acute infectious zoonotic disease caused by
the spore-forming, aerobic, gram-positive, non-motile bacte-
rium Bacillus anthracis.1,2Among the three clinical forms of
anthrax in humans, more than 95% of naturally occurring
infections are cutaneous anthrax.3Gastrointestinal anthrax is
usually caused by consumption of insufficiently cooked con-
taminated meat and it is relatively uncommon.4,5Inhalation
anthrax is rare in naturally occurring infections and it is asso-
ciated with processing and handling of hides and wool in
enclosed factory spaces, where aerosolized anthrax spores
may be inhaled.5Cutaneous anthrax occurs worldwide, with
an estimated 20,000–100,000 human cases occurring annu-
ally,5,6generally in low-income countries, where livestock are
not routinely vaccinated. No cutaneous anthrax outbreaks
have been reported from Bangladesh since 1986,7,8but anthrax
infection among livestock in Bangladesh was reported rou-
tinely,9and cutaneous anthrax outbreaks have been reported
from neighboring states in India in recent years.10,11
outbreaks of cutaneous anthrax in Bangladesh (Figure 1). A
collaborative team of epidemiologists, physicians, veterinar-
ians, and anthropologists from the Institute of Epidemiology,
Disease Control and Research (IEDCR), the Department of
Livestock Services of the Government of Bangladesh, and Inter-
national Centre for Diarrheal Disease Research, Bangladesh
conducted the outbreak investigations. The objectives of these
outbreak investigations were to identify the etiology, modes of
transmission, the social, behavioral, and cultural factors that
contributed to these outbreaks, along with suggesting control
and prevention measures.
Outbreak reporting and investigations. The first outbreak
was identified in August 2009 by a researcher from the Inter-
national Centre for Diarrheal Disease Research, Bangladesh,
whose relatives from Pabna District in northwestern Bangladesh
told him that two moribund cattle with high fever and convul-
sions had been slaughtered in his village and skin lesions had
developed in many persons in the following days. Two more
similar outbreaks were detected in the adjacent Sirajganj Dis-
trict during September and October 2009 (Figure 1). None
of these outbreaks were reported through the formal health
system in Bangladesh.
Human health authorities of Tangail District in the central
part of Bangladesh reported four similar outbreaks during
April–June 2010 (Figure 1). After a newspaper report of
another outbreak of cutaneous anthrax in Sirajganj District
in August 2010, health workers and newspapers reported a
series of outbreaks and sporadic cases of cutaneous anthrax
from different parts of the country.
We defined an occurrence of two or more suspected cases
of cutaneous anthrax in a community that were epidemiologi-
cally linked to sick or dead livestock or slaughtering of a
sick animal or handling of meat of a sick slaughtered animal
as an outbreak of cutaneous anthrax. Among the 14 outbreaks
we investigated during August–October 2010, 10 occurred
in two adjacent districts (Pabna and Sirajganj) that had
the highest cattle density in Bangladesh and were known as
the main milk-producing areas.12All outbreak sites were low-
lying areas and usually flooded during and after the annual
For each of these outbreaks, after receiving the initial
report, the investigation team members traveled to the out-
break site and collected animal, human, and anthropologic
information simultaneously. Investigation teams also conducted
follow-up visits in 9 of these 14 outbreak areas four weeks
after initial investigations.
Animal investigation. For each outbreak, veterinarians of
the investigation team developed a list of affected cattle,
goats, and sheep in the outbreak area and gathered epidemi-
ologic and clinical information by interviewing owners of the
animals by using a structured questionnaire. A suspected case
of animal anthrax was defined as sudden death or convul-
sion of a ruminant, with or without fever, 30 days before
the date of onset of first human case of cutaneous anthrax
in the area until the date of investigation. We collected bone
*Address correspondenceto Apurba Chakraborty, Centre for Commu-
nicable Diseases, International Centre for Diarrheal Disease Research,
Bangladesh, 68, Shaheed Tajuddin Ahmed Sarani, Mohakhali, Dhaka
1212, Bangladesh. E-mail: email@example.com
marrow smears of slaughtered sick animals from the meat
stored in household refrigerators. We also collected ocular
fluid from two dead goats, one from the first outbreak in
August 2009 and the other from the outbreak in August 2010.
Microbiologists of the Central Disease Investigation Labo-
ratory (CDIL), Bangladesh prepared bone marrow smears
stained with polychrome methylene blue and performed
microscopic examination from animal specimens collected
from four outbreak areas. We sent animal specimens to the
Centers for Disease Control and Prevention (CDC) for labo-
ratory confirmation and genotyping of isolates. We defined
those suspected animal anthrax cases as confirmed cases that
had laboratory evidence of acute B. anthracis infection shown
by microscopy of bone marrow smears stained with Loeffler’s
polychrome methylene blue and/or isolation of the bacilli.
Human investigation. We visited slaughtering sites and
spoke to owners of the slaughtered animals, local health
workers, and neighbors to obtain identifying, demographic,
and clinical information of suspected cutaneous anthrax cases.
In August–September 2010, we also visited door to door in
the affected communities in three outbreak areas to identify
cases and record exposure status of members of the house-
holds who received meat of a sick slaughtered animal. We
defined a suspected human case of cutaneous anthrax as any
person who had acute onset of a skin lesion with papule or
vesicle or skin ulceration with a raised margin and central
black eschar from three weeks before the date of slaughtering
the first sick animal to three weeks after the slaughtering of
last sick animal in the area. The field team investigated the
epidemiologic, clinical, and exposure history of the identified
cases by using a structured questionnaire.
We collected vesicular fluid for slide smears and vesicular
swabs in nutrient broth for culture. We obtained skin biopsy
specimens from three patients from the first outbreak. In
eight of the 14 outbreaks, we collected paired serum samples
from human cases for antibody testing. Microbiologists from
IEDCR conducted microscopy of field-prepared vesicular
smears by using staining with Loeffler’s polychrome methy-
lene blue. They also cultured material from vesicular swabs
on nutrient agar and blood agar media, followed by colony
morphology study, staining, and microscopy. We sent human
specimens from eight outbreaks to CDC for laboratory con-
firmation and genotyping of the isolates. We categorized
those suspected cutaneous anthrax cases as confirmed cases
that had laboratory evidence of acute B. anthracis infection
shown by either microscopy of vesicular smears stained with
Loeffler’s polychrome methylene blue, and/or isolation of
bacilli, and/or a four-fold increase in anti-protective antigen
(PA) antibody titer.
In the first three of the outbreaks investigated in August–
September 2010, four weeks after the initial investigations, we
searched for suspected cases of gastrointestinal anthrax by
using the list of household members developed in preliminary
investigations. We defined a suspected case of gastrointestinal
anthrax as a person in the affected communities who ate meat
or handled the raw meat of cattle, goats, or sheep and showed
development of a febrile illness associated with either oral
ulcer, sore throat, vomiting, or diarrhea from the date of
slaughtering the first sick animal to three weeks after the
slaughtering of last suspected animal anthrax case in the area.
To interview suspected cases of gastrointestinal anthrax, we
modified the questionnaire used in the preliminary investiga-
tion to include exposure and clinical information related to
gastrointestinal anthrax. From the suspected cases of gastro-
intestinal anthrax without cutaneous lesions, we collected
single serum samples for antibody testing.
Through unstructured discussion with local health officials
and community people we explored death of any suspected
cutaneous or suspected gastrointestinal anthrax case in the
Anthropologic investigation. In four outbreak areas, two
outbreaks in 2009 and two outbreaks in 2010, a team of
anthropologists conducted 13 in-depth interviews and 30 short
interviews with suspected case-patients in the community to
understand their knowledge and perception regarding conta-
giousness, illness, and treatment history. They also conducted
20 informal and formal group discussions with affected per-
sons in the community to explore beliefs, rituals, and usual
Figure 1.Bangladesh map showing 14 anthrax outbreak areas during August 2009–October 2010.
CHAKRABORTY AND OTHERS
practices of sick animal slaughtering, disposal of dead ani-
mals, and their knowledge regarding disease transmission
(animal to animal, animal to human, and human to human).
Building on this in-depth exploration by the anthropologic
team, the epidemiologists continued to explore social, behav-
ioral, and cultural factors in all other outbreaks.
Data analysis. We analyzed quantitative data by using SPSS
version 12.0 for Windows (SPSS, Chicago, IL) and descriptive
statistics to calculate frequencies of variables. We calculated
attack rates and risk ratios for different exposures among
the exposed and unexposed groups in three outbreak areas.
We reviewed anthropologic data to identify themes and their
context. Using the identified patterns, we developed and final-
ized a code list. We later summarized coded data according to
the study objectives and themes.
Ethical issues. For all outbreaks, we obtained informed
consent from adult respondents and guardians of children
and assent for children 11–17 years of age. Because these
investigations were outbreak investigations, a study protocol
was not reviewed by a human subjects committee, but the inves-
tigation plan was approved by the Government of Bangladesh.
Animal investigation. We identified 140 sick animals in
the 14 outbreaks. Among these animals, 96 (69%) were cattle,
41 (29%) were goats, and 3 (2%) were sheep. Ninety-six (69%)
animals were female. The median age was 36 months for
cattle, 24 months for goats, and 9 months for sheep. Ninety
eight (70%) of 140 animals died of their illness and 35 (25%)
were slaughtered (Table 1). Twenty four (25%) of the 96 cattle
had a history of anthrax vaccination in the previous year. The
median period from onset of illness to death of an animal
anthrax case was 5 hours (range = 5 minutes–8.5 days). The
median period from onset of illness to slaughtering of an
animal anthrax case was 7 hours (range = 15 minutes–6.2 days).
We collected disposal history for the 59 death cases in the
11 outbreaks in 2010. Of these cases, 29 (49%) were thrown
into flood or river waters, 10 (17%) were abandoned in open
fields, and 20 (34%) were buried. The median duration from
the date of slaughtering of the first sick animal in an outbreak
area to the date of investigation of the outbreak was 17 days
(range = 6–34 days). All 35 slaughtered sick animals were
associated with human cases.
Microbiologists of CDIL identified gram-positive, chain-
forming, spore-containing, capsulated bacilli from smears of
bone marrow of five slaughtered cattle. The CDC isolated
B. anthracis from the ocular fluid of two dead goats, and also
detected B. anthracis from bone marrow smears collected
from a slaughtered cow and a disposed dead goat by
M’Fadyean staining. Based on the laboratory evidence from
CDIL and CDC, we identified seven confirmed animal
anthrax cases, five in cattle and two in goats.
Human investigation. Combining all 14 outbreak investiga-
tions, we interviewed 273 cases of cutaneous anthrax, 39 con-
firmed cases and 234 suspected cases. In the three outbreak
investigations in 2010 in which we inquired about gastrointes-
tinal symptoms, we identified 25 cases of suspected gastro-
intestinal anthrax, 10 of which also had cutaneous anthrax. In
all 14 outbreaks, human cases occurred after slaughtering of
anthrax-infected animals (Figure 2). Of the 273 cutaneous
anthrax cases, 165 (60%) were in male patients. The median
age of cutaneous anthrax case-patients was 26 years (range =
1–90 years) (Table 2). The median duration from exposure to
onset of illness was 2 days (range = 0–22 days). Skin lesions
were characterized by ulcers (86%), papules (85%), vesicles
(84%), central black eschars (75%), erythema (65%), and
surrounding edema (60%) (Table 2 and Figure 3). Lesions
were mostly distributed on the upper limbs (81%), but were
also present on lower limbs (17%), face (5%), chest (4%),
back (3%), neck (2%), abdomen (2%) and scalp (2%). A
significant difference was observed between confirmed and
suspected cutaneous anthrax cases with regard to surrounding
erythema (82% versus 62%; P = 0.02), surrounding edema
(84% versus 56%; P = 0.01), nausea (30% versus 14%; P =
0.01), and oropharyngeal ulceration (5% versus 1%; P = 0.04)
Of 273 cutaneous anthrax case-patients, 225 (82%) handled
raw meat from sick animals, 172 (63%) were present at a
slaughtering site, 89 (33%) handled skin of a sick slaughtered
animal, 86 (32%) were involved in butchering sick animals,
and 71 (26%) had contact with a sick animal. Ninety-one
percent of 273 cutaneous anthrax cases reported a history of
at least one of these exposures. Two hundred thirty-five
(86%) cutaneous anthrax case-patients had a history of con-
suming meat of a sick slaughtered animal. Local health
for at least 10 days. Of 169 cutaneous anthrax case-patients
who received ciprofloxacin before the date of investigation,
10 (6%) reported vomiting, compared with 7 (7%; P = 0.79)
of 104 case-patients who received it on or after the date
Demographic and clinical characteristic of 140 anthrax-infected
animals in outbreaks investigated during 2009–2010 in Bangladesh
Cattle: median (range)
Goats: median (range)
Sheep: median (range)
Females, no. (%)
Clinical presentation, no. (%)
Decease in milk production
Outcome, no. (%)
Death from illness
Sick at the time of interview
Sold during illness
Median (range) onset of illness
Median (range) onset of illness
5 hours (5 minutes–8.5 days)
7 hours (15 minutes–6.2 days)
CUTANEOUS ANTHRAX, BANGLADESH
of investigation. Two (1%) of 169 cutaneous anthrax case-
patients who received ciprofloxacin before the date of
investigation reported diarrhea, compared with 4 (4%; P =
0.15) of 104 case-patients who received it on or after the
date of investigation. Local health workers followed-up
case-patients and ensured that they had medication. No case-
patient required hospitalization, and all case-patients recov-
ered uneventfully. We did not identify any reported deaths
of suspected cutaneous anthrax or suspected gastrointestinal
anthrax cases in the outbreak communities.
Through door-to-door visits of 437 households in three
outbreak areas in 2010, we collected information about case
status and exposure history of 1,665 persons. Among them,
67 (4%) were identified as case-patients. Persons involved
in butchering a sick animal at the slaughtering site were at
a significantly higher risk of contracting cutaneous anthrax
(relative risk = 21.9, 95% confidence interval = 14.5–32.9)
than those who did not participate in butchering a sick animal
at the slaughtering site. Involvement in handling raw meat of
a sick animal at home or being present at the slaughtering
site without participating in butchering was not significantly
associated with development of cutaneous lesions (Table 3).
Microbiologists of IEDCR identified blue-stained bacilli
with squared ends by microscopy of vesicular smears by
using Loeffler’s polychrome methylene blue stain for 23 of
28 suspected cutaneous anthrax case-patients whose speci-
men they tested. At CDC, B. anthracis was detected in three
skin biopsy specimens by immunohistochemical analysis and
from 10 vesicular swab smears by M’Fadyean staining. Bacillus
anthracis was isolated at CDC from vesicular swabs of three
cases, two from the first outbreak in 2009 and one from the
outbreaks in August 2010.
June 2010. B, Distribution of seven overlapping cutaneous anthrax outbreaks in relation to animal slaughtering over time in Bangladesh during
A, Distribution of cutaneous anthrax outbreaks in relation to animal slaughtering over time in Bangladesh during August 2009–
CHAKRABORTY AND OTHERS
Nineteen of 45 persons in whom a case of suspected cutane-
ous anthrax developed and whose paired serum samples were
tested at CDC showed a four-fold increase in anti-PA titer. The
first serum sample from 31 (69%) suspected cutaneous anthrax
case-patients was collected within eight days of their onset of ill-
ness. Those persons who had their first serum samples collected
within eight days of their onset of illness were more likely to
have a four-fold increase in anti-PA titer than those whose first
serum sample was collected after eight days of their onset of
illness (58% versus 7%; odds ratio = 18, 95% confidence inter-
val = 2–806, P < 0.001). Fifteen of 26 case-patients who did not
have a four-fold increase had a detectable anti-PA titer.
Multiple-locus variable-number tandem repeat analysis
(MLVA) was performed for B. anthracis isolated from human
and animal specimens at CDC. The MLVA-8 genotype of
2009 isolates confirmed that animals and humans were
infected by isolates of the same genotype. The MLVA-8 geno-
type of 2010 isolates that caused infection in animals and
humans in 2010 differed from the 2009 isolate at one locus
(pXO1 locus) (Table 4).
Fifteen (60%) of 25 suspected gastrointestinal anthrax cases
were in female patients. The median age of these case-patients
was 20 years (range = 2–50 years). Suspected gastrointestinal
anthrax case-patients reported fever (100%), abdominal pain
(76%), nausea (56%), vomiting (56%), diarrhea (36%), and
ulceration in oral mucosa (19%). All suspected gastrointesti-
nal anthrax case-patients had a history of consuming meat of
slaughtered sick animals. All case-patients recovered and did
not require hospitalization. Among 15 case-patients with sus-
pected gastrointestinal anthrax who did not have cutaneous
anthrax lesions, two had a detectable anti-PA titer.
Anthropologic investigation. Persons in the affected com-
munity were aware of anthrax in livestock and identified it by
using the local term torka. Persons were not aware that they
could become infected with anthrax because of butchering,
handling or eating the meat of sick animals.
After observing the deteriorating condition of the sick cattle
and realizing that livestock would not survive, neighbors and
relatives of the cattle owners recommended slaughtering
them. In some cases, neighbors and relatives slaughtered
the cattle without even seeking consent from the owner.
Slaughtering sick livestock and selling the meat at a price
below its normal value was a common practice in these out-
break areas because owners were attempting to recover some
of their financial investment. Some sick cattle and goats were
not slaughtered because the owners believed that slaughtering
a pregnant or an animal less than one year of age is against
during 2009 in Bangladesh.
Laboratory-confirmed cutaneous anthrax case identified
Demographic and clinical presentation of 273 suspected and confirmed human cutaneous anthrax cases in outbreaks investigated during 2009–2010
Characteristic Suspected cutaneous anthrax cases (n = 234)*
Confirmed cutaneous anthrax cases (n = 39)†P Total (n = 273)‡
Age group, no. (%)
Sex, no. (%)
Clinical presentation, no. (%)
Central black eschar
Itching around skin lesion
28 (1–90)25 (4–65) 26 (1–90)
140 (60) 25 (64)0.61 165 (60)
*Includes eight cases of suspected cutaneous and suspected gastrointestinal anthrax.
†Includes two cases of suspected cutaneous and suspected gastrointestinal anthrax.
‡Includes 10 cases of suspected cutaneous and suspected gastrointestinal anthrax.
CUTANEOUS ANTHRAX, BANGLADESH
Islamic customs. Because of the sudden onset and unpredictable
course of illness, some cattle and goats died before their
owners were able to decide whether to slaughter the animal.
Because residents of affected communities perceived that
river water washes everything away with its current, they
usually discarded dead cattle in the river or in flood waters.
According to the community members, eating meat of
slaughtered sick cattle and goats is a common practice. The
price of this meat is low, and because most persons cannot
afford to buy meat regularly, they were eager to purchase it.
Despite selling meat of a slaughtered sick animal, owners of
these animals had substantial economic losses. In the first
outbreak in 2009, the market price of a healthy cow was
reported as 50,000 Taka (US$ 714), but the owner received
only 20,000 Taka (US$ 285) by selling the meat. In each of
these outbreaks, cattle owners could only recover 10–30% of
the market price of a healthy animal of the same size by
selling its meat.
Epidemiologic, clinical, and laboratory findings suggest that
these outbreaks in animals and humans were caused by
B. anthracis. Participation in butchering anthrax-infected ani-
mals and exposure to infected meat and animal by-products
were responsible for the human outbreaks. There are several
environmental factors in Bangladesh that favor the presence of
anthrax, including high ambient temperature and relative
humidity.13Because persons are not aware of proper disposal
practices, anthrax-infected dead animals were frequently dis-
posed in open fields and rivers, which can contaminate grazing
land with anthrax bacilli that can sporulate rapidly on exposure
to air and high temperatures.14Therefore, unvaccinated animals
mighthave acquired anthraxby ingestionofsporeswhilegrazing.
The three districts where these 14 outbreaks occurred
during August 2009–September 2010 shared similar environ-
mental characteristics. With animal anthrax cases reported in
Bangladesh in previous years9and a low coverage of livestock
anthrax vaccination and disposal of 66% of dead animals in
flood waters or surrounding open fields, these outbreaks were
likely separate outbreaks in which animals were infected from
spores spread in the grazing lands around those outbreak
areas. Difference in genotype of B. anthracis isolates during
2009 and 2010 outbreaks also suggest these were separate
outbreaks, which were unlikely to be the result of a spread of
the organism from one outbreak area to the other.
Up to 2009, no human anthrax cases had been reported in
Bangladesh for more than 25 years, and most of these recent
outbreaks were not detected through the routine reporting
system of the health or livestock departments. This finding
likely indicates substantial under-diagnosis and under-
reporting of human anthrax in Bangladesh, which might be
influenced by the medical education system in the country,
where cutaneous anthrax is not considered a common disease
and so is not emphasized within the medical curriculum.
In the wave of outbreaks during August–October 2010, 607
suspected cases of cutaneous anthrax were reported by the
health authorities from 12 of the 64 districts.15These out-
breaks were much more widespread compared with previous
reported anthrax outbreaks in Bangladesh. This increase in
the number of outbreaks and suspected cases might have been
caused by increased awareness among health workers and the
general population because of the unprecedented media
attention to the outbreaks, but we cannot rule out an under-
lying increase in cases.
Although there were no deaths of human case-patients,
reports of anthrax outbreaks in different parts of the coun-
try during August–September 2010 created fear among the
general population, which reduced meat consumption.
Newspapers reported a 92% decrease in number of cattle
slaughtered in a day in the capital city of Dhaka. Reduction
in sales of animals ahead of Eid-ul-Fitr, a major Muslim
festival, had a major negative impact on the livestock indus-
try of the country.16
A number of social, cultural, and economic factors con-
tributed to these human outbreaks. In all of these outbreaks,
neighbors and relatives of the owners of the sick animals
actively participated in butchering sick animals and process-
ing raw meat. Community participation in such activities is
common in rural Bangladesh where collective, not individual,
Relationship between exposure variables and cutaneous anthrax case status (n = 1,665), Bangladesh
Risk ratio No. missing95% CITotalCasesAttack rate, %Total CasesAttack rate, %
Butchered sick animal at slaughtering site but did not
handle raw meat of sick animal at home
Handled raw meat of sick animal at home but did not
participate in butchering at slaughtering site and was
not present at slaughtering site
Present at slaughtering site but did not participate in
butchering or in handling raw meat of sick animal
63 31 49.211,60036 2.2521.92 14.5–32.9
495 275.45 1,165 413.51 1.65 1–2.5
4524.44 1,618 664.081.12 0.3–4.3
CI = confidence interval.
MLVA-8 genotyping of Bacillus anthracis isolated during 2009 and 2010 in Bangladesh
B. anthracis strainOutbreak year pXO1pXO2 CG3vrrB2
MLVA = multiple-locus variable-number tandem repeat analysis.
CHAKRABORTY AND OTHERS
decision making is the norm. Voluntary participation in
butchering resulted in exposure of more persons to infected
meat and other by-products of the sick slaughtered animal.
Of 60 countries reporting anthrax in 2004, nearly 60% were
low-income countries.17Poor persons are more at risk of
contracting anthrax because of traditional raising practices
involving close contact with animals, even when they are
sick.17In Bangladesh, the average per capita annual income
is US $599 (42,000 Taka),18and 43% of rural persons live
below the poverty line.19With more than one-third of rural
women identified as undernourished,18buying inexpensive
meat is viewed as a favorable opportunity when animals
become sick and must be slaughtered. Moreover, livestock play
a vital component in the economy of these outbreak areas.
Therefore, the fear of impending financial loss can influence
the cattle owners to slaughter the sick animal and sell the meat.
Although we did not systematically search for gastrointes-
tinal anthrax cases during initial investigations, we identified
25 suspected gastrointestinal anthrax cases during a follow-up
visit in three outbreak areas in 2010. Anti-PA titer of col-
lected single serum samples failed to confirm any of those
cases as anthrax. The absence of reports of hospitalization or
deaths in these outbreak areas suggests that these cases were
unlikely to be cases of gastrointestinal anthrax, especially if
one considers the usually reported high case-fatality rate of
this illness.3,13,20The local practice of overcooking meat also
significantly reduces the risk of gastrointestinal anthrax,
which usually results from consuming undercooked meat.1,5
Suspected cutaneous anthrax cases in these outbreaks had
characteristic skin lesions of cutaneous anthrax, starting with
a papule, which gradually progressed to formation of a vesi-
cle, ulcer, and eschar. Although the absence of surrounding
edema in 44% of suspected cases might be related to the time
gap between the onset of illness of cases and date of investi-
gation, there is also evidence of similar characteristic in other
settings.21Enteric symptoms such as nausea, abdominal pain,
vomiting, and diarrhea are unlikely with cutaneous anthrax,
and cutaneous anthrax cases who also met the case definition
of suspected gastrointestinal anthrax in these outbreaks could
not be confirmed as gastrointestinal anthrax. Because 86% of
the cutaneous anthrax case-patients had a history of consum-
ing meat of sick slaughtered animals, reported symptoms such
as nausea and abdominal pain might have been influenced by
subjective feelings of the respondents after consuming meat
from a sick animal.
Delayed collection of the first serum sample might explain
the absence of a four-fold increase in anti-PA titer in 26 of the
45 suspected cutaneous anthrax case-patients whose paired
serum samples were tested. Cutaneous anthrax patients have
a lower anti-PA response than inhalation anthrax patients,22
which might be the reason for a detectable anti-PA titer in
15 cases without a four-fold increase. In another study, anti-
PA IgG was detected only in a subset of cutaneous anthrax
patients.23Therefore, absence of a four-fold increase in anti-PA
titer does not exclude the possibility that a suspected cutane-
ous anthrax case was infected by anthrax bacilli.
Poor coverage of livestock anthrax vaccination and ineffec-
tive vaccination in some animals contributed to the animal
outbreaks. The Livestock Research Institute of the Govern-
ment of Bangladesh is the only supplier of livestock anthrax
vaccine in Bangladesh. There are approximately 23 million
cattle, 1 million buffalo, 21 million goats, and 3 million sheep
in Bangladesh.19However, the total annual vaccine production
is only 3.8 million doses,24which the Department of Livestock
Services distributes at a subsidized rate of US $ 0.74 (50 Taka)
per 100 doses. In comparison, a vial of 50 doses of livestock
anthrax vaccine costs approximately $49 in the United States.25
If one considers the economic impact of animal and human
anthrax, if this vaccine was available in the local market, even
at a higher price, it might be feasible for individual cattle
raisers to purchase it. Increasing the availability of anthrax
vaccine in the market, either through increasing domestic
production or through importation, and increasing the demand
through raising awareness among the cattle owners, would be
one strategy to increase coverage.
A history of anthrax vaccination within the previous year
among 25% of the suspected cattle cases of anthrax suggests
either over-reporting of vaccination or vaccination failure.
Successful development of protective immunity against anthrax
in animals requires effective vaccine and proper vaccination
technique. Also, a single dose of Sterne vaccine may not be
sufficient to ensure protective immunity in the animal to last
for a year, and more than one initial dose of the Sterne vaccine
may be necessary.13,26,27The Department of Livestock Ser-
vices, should assess vaccine efficacy and develop a strategy to
improve coverage. If one considers the scarcity of resources,
the vaccination strategy should identify target areas for vacci-
nation based on the understanding of the spatial ecology and
the geographic distribution of B. anthracis in Bangladesh, as
has been done in other settings.28,29
Because some human cases were reported more than
one month after the onset of illness, imperfect recall by the
case-patients might be a reason that 24 (9%) of the 273 cuta-
neous anthrax case-patients did not report a history of any of
the exposures related to contact with a sick animal, meat of a
sick slaughtered animal, or animal by-products. There might
also have been some unknown exposure because the sur-
rounding environment was contaminated by disposed animal
carcasses, and stable flies and mosquitoes may play a role in
transmission of animal and human anthrax.5,30–32
Lack of awareness of the cattle owners and the community
regarding transmission of this disease from animals to humans,
scarcity of the livestock vaccine, social norms, and poverty all
contributed to these cutaneous anthrax outbreaks. The anthrax
outbreaks affected households through livestock deaths and
morbidity of humans. Improved treatment of human cases of
anthrax can be achieved through short-term training for prac-
ticing physicians and by modifying the undergraduate medical
curriculum to include information on detecting and managing
cutaneous anthrax cases. Although anthrax affects human and
animal health, there is no legal, policy or institutional frame-
work in Bangladesh to ensure joint action of the Directorate
General of Health Services and Department of Livestock Ser-
vices to control anthrax. A joint human and animal health
approach, or the one health concept, can be beneficial in
controlling zoonotic diseases such as anthrax because they
can be better surveyed, diagnosed, and controlled.17This one
health approach could improve coordination between human
and animal health departments and thereby facilitate early
detection, control, and prevention of anthrax outbreaks.
Received April 15, 2011. Accepted for publication December 4, 2011.
Acknowledgments: We thank Dr. Labib Imran Faruque, Dr. Abu
Mohammed. Naser Titu, Dr. Hossain Mohammed, Shahed Sazzad,
CUTANEOUS ANTHRAX, BANGLADESH
Dr. Kazi Mohammed, Hassan Ameen, and Dr. Selina Khatun for
contributions during field investigations; Robyn A. Stoddard, Chung
K. Marston, Wun-Ju Shieh, and Cari A. Beesley for contributions
during laboratory investigations at CDC; all study participants for
their contributions; civil surgeons and district livestock officers of
Pabna, Sirajganj, and Tangail Districts and sub-district health and
family planning officers and livestock officers of Santhia, Shahjadpur,
Kamarkhand, Faridpur, Belkuchi, Ghatail, and Bhuapur sub-districts
for assistance; and Dorothy Southern for reviewing the manuscript.
Financial support: This study was supported by CDC and the Gov-
ernment of Bangladesh. The International Center for Diarrheal
Disease Research, Bangladesh acknowledges with gratitude the
commitment of the Government of Bangladesh and CDC to research
efforts of the Centre.
Authors’ addresses: Apurba Chakraborty, Salah Uddin Khan,
Mohammed Abul Hasnat, Shahana Parveen, M. Saiful Islam,
Andrea Mikolon, Najmul Haider, Stephen P. Luby, and M. Jahangir
Hossain, Centre for Communicable Diseases, International Centre
for Diarrheal Disease Research, Bangladesh, 68, Shaheed Tajuddin
Ahmed Sarani, Mohakhali, Dhaka 1212, Bangladesh, E-mails:
firstname.lastname@example.org, email@example.com, firstname.lastname@example.org,
icddrb.org, email@example.com, and firstname.lastname@example.org. Ranjit Kumar
Chakraborty, Department of Livestock Services, Ministry of Fisheries
and Livestock, Dhaka, Bangladesh, E-mail: chakraborty.ranjit@yahoo
.com. Be-Nazir Ahmed, Khorsed Ara, and Mahmudur Rahman,Institute
Bangladesh, E-mails: email@example.com, khorsedara1957@yahoo
1. Woods CW, Ospanov K, Myrzabekov A, Favorov M, Plikaytis B,
Ashford DA, 2004. Risk factors for human anthrax among
contacts of anthrax-infected livestock in Kazakhstan. Am J
Trop Med Hyg 71: 48–52.
2. Demirdag K, Ozden M, Saral Y, Kalkan A, Kilic SS, Ozdarendeli A,
2003. Cutaneous anthrax in adults: a review of 25 cases in the
eastern Anatolian region of Turkey. Infection 31: 327–330.
3. Centers for Disease Control and Prevention, 2009. Anthrax.
Atkinson W, Wolfe S, Hamborsky J, McIntyre L, eds. Epi-
demiology and Prevention of Vaccine-Preventable Diseases.
Washington, DC: Public Health Foundation, 308.
4. Sirisanthana T, Brown AE, 2002. Anthrax of the gastrointestinal
tract. Emerg Infect Dis 8: 649–651.
5. Swartz MN, 2001. Recognition and management of anthrax: an
update. N Engl J Med 345: 1621–1626.
6. Freedberg IM, Eisen AZ, Wolff K, Austen K, Goldsmith LA,
Katz SI, 2003. Fitzpatrick’s Dermatology in General Medicine.
6th edition. New York: McGraw-Hill, 1918–1921.
7. International Centre for Diarrhoeal Diseases Research, Bangladesh,
2009. Cutaneous anthrax outbeak in two districts of North-
Western Bangladesh. Health and Science Bulletin 7: 1–8.
8. Samad MA, Hoque ME, 1986. Anthrax in man and cattle in
Bangladesh. J Trop Med Hyg 89: 43–45.
9. World Organization for Animal Health, 2010. World Animal
Health Information Database. Available at: http://www.oie.int/
858ff84f59f. Accessed August 12, 2010.
10. Ray TK, Hutin YJ, Murhekar MV, 2009. Cutaneous anthrax,
West Bengal, India, 2007. Emerg Infect Dis 15: 497–499.
11. Datta KK, Singh J, 2002. Anthrax. Indian J Pediatr 69: 49–56.
12. Jabbar MA, Islam SMF, Delgado C, Ehui S, Akanda MAI, Khan
MI, Kamruzzaman M, 2005. Policy and Scale Factors Influenc-
ing Efficiency in Dairy and Poultry Production in Bangladesh.
International Livestock Research Institute, Nairobi, Kenya,
Systemwide Livestock Programme, Addis Ababa, Ethiopia,
and Bangabandhu Sheikh Mujibur Rahman Agricultural Uni-
versity, Salana, Gazipur, Bangladesh. 76 pp.
13. World Health Organization, 2008. Anthrax in Animals and
Humans. Available at: http://www.who.int/csr/resources/
publications/anthrax_webs.pdf. Accessed November 25, 2011.
14. Christie AB, 1987. Anthrax. Infectious Diseases: Epidemiology and
Clinical Practice. 4th edition. Edinburgh: Churchill Livingstone,
15. Institute of Epidemiology, Disease Control and Research, 2010.
Anthrax Update. Available at: http://www.iedcr.org. Accessed
January 11, 2010.
16. Akter S, 2010. Anthrax scare hurts leather industry. The Daily Star.
Dhaka. Available at: http://www.thedailystar.net/newDesign/
news-details.php?nid=155128. Accessed July 21, 2011.
17. World Health Organization, 2005. The Control of Neglected
Zoonotic Diseases—A Route to Poverty Alleviation. Geneva:
World Health Organization.
18. National Institute of Population Research and Training, 2009.
Bangladesh Demographic and Health Survey 2007. Dhaka,
Bangladesh and Calverton, MD: Mitra and Associates and
19. Bangladesh Bureau of Statistics, 2008. Bangladesh Data Sheet.
Available at: http://www.bbs.gov.bd/. Accessed May 20, 2010.
20. Beatty ME, Ashford DA, Griffin PM, Tauxe RV, Sobel J, 2003.
Gastrointestinal anthrax: review of the literature. Arch Intern
Med 163: 2527–2531.
21. Maguina C, Flores Del Pozo J, Terashima A, Gotuzzo E,
Guerra H, Vidal JE, Legua P, Solari L, 2005. Cutaneous
anthrax in Lima, Peru: retrospective analysis of 71 cases,
including four with a meningoencephalic complication. Rev
Inst Med Trop Sao Paulo 47: 25–30.
22. Quinn CP, Dull PM, Semenova V, Li H, Crotty S, Taylor
TH, Steward-Clark E, Stamey KL, Schmidt DS, Stinson KW,
Freeman AE, Elie CM, Martin SK, Greene C, Aubert RD,
Glidewell J, Perkins BA, Ahmed R, Stephens DS, 2004.
Immune responses to Bacillus anthracis protective antigen
in patients with bioterrorism-related cutaneous or inhalation
anthrax. J Infect Dis 190: 1228–1236.
23. Brenneman KE, Doganay M, Akmal A, Goldman S, Galloway
DR, Mateczun AJ, Cross AS, Baillie LW, 2011. The early
humoral immune response to Bacillus anthracis toxins in
patients infected with cutaneous anthrax. FEMS Immunol
Med Microbiol 62: 164–172.
24. Livestock Research Institute, 2010. Annual Report on Produc-
tion, Distribution and Balance of Vaccines in the Financial Year
2009–2010, Bangladesh. Dhaka: Livestock Research Institute.
25. Colorado Serum Company, 2008. Anthrax Spore Vaccine. Avail-
able at: https://ssl1001.qwestoffice.com/colorado-serum.com/
Anthrax&x=0&y=0. Accessed January 8, 2010.
26. Ndiva Mongoh M, Dyer NW, Stoltenow CL, Hearne R, Khaitsa
ML, 2008. A review of management practices for the control of
anthrax in animals: the 2005 anthrax epizootic in North Dakota–
case study. Zoonoses Public Health 55: 279–290.
27. Turnbull PC, Tindall BW, Coetzee JD, Conradie CM, Bull RL,
Lindeque PM, Huebschle OJ, 2004. Vaccine-induced protec-
tion against anthrax in cheetah (Acinonyx jubatus) and black
rhinoceros (Diceros bicornis). Vaccine 22: 3340–3347.
28. Joyner TA, Lukhnova L, Pazilov Y, Temiralyeva G, Hugh-Jones
ME, Aikimbayev A, Blackburn JK, 2010. Modeling the poten-
tial distribution of Bacillus anthracis under multiple climate
change scenarios for Kazakhstan. PLoS ONE 5: e9596.
29. Blackburn JK, McNyset KM, Curtis A, Hugh-Jones ME, 2007.
Modeling the geographic distribution of Bacillus anthracis, the
causative agent of anthrax disease, for the contiguous United
States using predictive ecological [corrected] niche modeling.
Am J Trop Med Hyg 77: 1103–1110.
30. Turell MJ, Knudson GB, 1987. Mechanical transmission of
Bacillus anthracis by stable flies (Stomoxys calcitrans) and
mosquitoes (Aedes aegypti and Aedes taeniorhynchus). Infect
Immun 55: 1859–1861.
31. Fasanella A, Scasciamacchia S, Garofolo G, Giangaspero A,
Tarsitano E, Adone R, 2010. Evaluation of the house fly
Musca domestica as a mechanical vector for an anthrax. PLoS
ONE 5: e12219.
32. Hugh-Jones M, Blackburn J, 2009. The ecology of Bacillus
anthracis. Mol Aspects Med 30: 356–367.
CHAKRABORTY AND OTHERS