Outbreak of cutaneous anthrax in a tribal village: A clinico-epidemiological study

Abstract

Anthrax is a life-threatening infectious disease that normally affects animals, especially ruminants. It is caused by the bacteria Bacillus anthracis. The most common mode of infection is through the skin, which causes a painless sore that usually heals without treatment. If left untreated, cutaneous anthrax may progress in up to 20% of cases to septicaemia with potentially lethal outcome.
We visited a small tribal village of the state of West Bengal, where an outbreak of cutaneous anthrax was suspected following slaughtering a dead bullock. The population at risk were subjected to detailed interrogation, thorough clinical examination and relevant investigations.
The mean age of our study population was 32.1 years, and 100% were male. The mean incubation period was three days. Most cases (81.8%) were exposed to the bacteria during butchering. The predominantly affected sites were fingers (54.5%), followed by forearms (18.2%), around elbows (18.2%) and arm (9.1%). All cases initially had painless papules, ulcers with vesicles; dissemination of the lesion was seen in 27.3% of patients. 9 patients (who were alive) underwent complete blood count, baseline biochemistry and chest X-ray. Smears were made from the cutaneous lesions for gram's stain in 5 patients. Wound swabs were also inoculated in nutrient broth and subcultured in blood agar media. FNAC from the enlarged axillary lymph node was done in 1 patient and blood was sent for aerobic culture in 2 individuals. Both the blood cultures were sterile. Smears made from the culture obtained from cutaneous lesion of one of the affected person revealed gram positive aerobic spore bearing non-motile bacilli in long chain with capsular halo suggesting Bacillus anthracis. In this outbreak, the attack rate was 7% and case fatality rate was 18%.
Cutaneous anthrax should be considered as a differential diagnosis in cases presenting with painless ulcers, vesicles or eschars with a recent history of exposure to animals or animal products. It is important to recognise the clinical aspects of this disease in routine practice since any delay in treatment may have fatal consequences, as observed in this study.

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Abstract
Background : Anthrax is a life-threatening infectious disease that normally affects animals, especially ruminants.
It is caused by the bacteria Bacillus anthracis. The most common mode of infection is through the skin, which
causes a painless sore that usually heals without treatment. If left untreated, cutaneous anthrax may progress in
up to 20% of cases to septicaemia with potentially lethal outcome.
Methodology : We visited a small tribal village of the state of West Bengal, where an outbreak of cutaneous
anthrax was suspected following slaughtering a dead bullock. The population at risk were subjected to detailed
interrogation, thorough clinical examination and relevant investigations.
Results : The mean age of our study population was 32.1years, and 100% were male. The mean incubation period
was three days. Most cases (81.8%) were exposed to the bacteria during butchering. The predominantly affected
sites were fingers (54.5%), followed by forearms (18.2%), around elbows (18.2%) and arm (9.1%). All cases initially
had painless papules, ulcers with vesicles; dissemination of the lesion was seen in 27.3% of patients. 9 patients
(who were alive) underwent complete blood count, baseline biochemistry and chest X-ray. Smears were made
from the cutaneous lesions for gram’s stain in 5 patients. Wound swabs were also inoculated in nutrient broth
and subcultured in blood agar media. FNAC from the enlarged axillary lymph node was done in 1 patient and
blood was sent for aerobic culture in 2 individuals. Both the blood cultures were sterile. Smears made from the
culture obtained from cutaneous lesion of one of the affected person revealed gram positive aerobic spore bearing
non-motile bacilli in long chain with capsular halo suggesting Bacillus anthracis. In this outbreak, the attack rate
was 7% and case fatality rate was 18%.
Conclusion : Cutaneous anthrax should be considered as a differential diagnosis in cases presenting with painless
ulcers, vesicles or eschars with a recent history of exposure to animals or animal products. It is important to
recognise the clinical aspects of this disease in routine practice since any delay in treatment may have fatal
consequences, as observed in this study.
*Assistant Professor, Department of Medicine, **RMO-cum-clinical
tutor, Department of Medicine, ***Assistant Professor, Department of
Microbiology, ****Demonstrator, Department of Community Medicine,
$Demonstrator, Department of Microbiology, #Assistant Professor,
Department of Dermatology and Veneriology, Midnapore Medical
College, Paschim Medinipur 721101, West Bengal, INDIA
Received: 17.05.2010; Revised: 30.07.2010; Accepted: 07.10.2010
Introduction
Anthrax is a potentially fatal zoonotic disease caused by
the gram-positive organism, Bacillus anthracis, which
rarely aects humans under normal conditions. In most of the
developed nations, anthrax has almost disappeared but in many
of the developing countries the disease is still endemic. A good
number of cutaneous anthrax cases have been reported from
Turkey.1,2 However, patients with cutaneous anthrax have been
found in developed countries like United States3 and France.4
Anthrax is a potential agent for use as a biological weapon or
for bioterrorism. In 2001, bioterrorist activities involving the
United States Postal Service infected 22 people with anthrax.
Seven survivors had conrmed cases of cutaneous anthrax.
While at least 17 nations are believed to have a biological
weapons program, it is unknown how many nations or groups
are working with anthrax. However, most bioterrorism experts
have concluded that it is technologically dicult to use anthrax
eectively as a weapon on a large scale.
The actual incidence of anthrax in India is largely unknown
perhaps due to under-diagnosis or due to under-reporting of the
cases. Cases of human anthrax have been reported mainly from
southern part of India and thus conrm the endemicity of the
disease. This outbreak of cutaneous anthrax occurred in a small
village named Chandmurha, situated in the south-west part of
the state of West Bengal. The village is inhabited by tribal people
living on farming and cale grazing. It has 65 households with
an estimated total population of 320. Our study incorporates the
epidemiological data and the clinical features of the involved
cases. It is important to recognise the clinical features of this
potentially lethal disease in clinical practice since any delay in
initiating treatment may have fatal consequences, as illustrated
by this study.
Background
A 43 year old gentleman RH (Table 3) was brought to
the emergency on 26/04/2010 with laboured respiration and
unconsciousness. He had frequent aacks of generalised tonic
clonic seizure for last 10 hours. Clinical examination revealed
the following: Glasgow Coma Scale: 4 (E-1, M-2, V-1), BP:
64/40mm of Hg. pulse: 124/mn. (very feeble), respiration rate:54/
mn.,SpO2: 56% (while breathing ambient air). Neck was supple
with non-responding plantars. Pupils were dilated, equal and
non-reacting to light. Coarse crepitations were heard scaered
over both the lung elds. The right arm, right axilla and neck
Original Article
Outbreak of Cutaneous Anthrax in a Tribal Village: A
Clinico-epidemiological Study
Partha Pratim Chakraborty*, Sudeshna Guha Thakurta**, Partha Sarathi Satpathi***,
Shukchand Hansda****, Sudipta Sit$, Arun Achar#, Dibyendu Banerjee***
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meat or were involved during slaughtering or handling the raw
meat. The team visited all the 36 households and all of the 152
individual were evaluated with a detailed history and thorough
clinical examination. We found that only 11 persons (including
those who died) had clinical manifestations of the disease.
Investigations were performed in 9 patients who were
alive and had signs and symptoms of the disease. All of them
underwent complete blood count, baseline biochemistry (blood
sugar, renal function tests, and liver function tests) and chest
X-ray. Smears were made from the cutaneous lesions for gram’s
stain in 5 patients. In all those 5 patients wound swabs were also
taken and inoculated in nutrient broth and subcultured in blood
agar media. Smears and swabs were taken from the cutaneous
vesicles, from the ulcer bases, and from accumulated uids
surrounding the lesions. FNAC from the enlarged axillary lymph
node was done in 1 patient and blood was sent for aerobic culture
in 2 individuals. Cutaneous lesions were almost healed in 3 of the
9 patients and in those individuals only baseline investigations
were done (Table1).
On the basis of suggestive history and characteristic clinical
features a provisional diagnosis of cutaneous anthrax was
considered. All contacts and aected persons were given tab.
Ciprooxacin (500 mg BD) under supervision of BMOH. One
patient with axillary lymphadenopathy received Inj. Benzyl
Penicillin (120 million/day) in addition to ciprooxacin.
Observations and Findings
What came out from the history is that a bullock was sick
for past few days and died on 15/04/2010. It was butchered
at a nearby field in the locality and the cooked meat was
consumed over the next 3 days. The 11 symptomatic individual
were involved during slaughtering, chopping, preparing and
cooking the meat. Persons who were engaged in slaughtering
were not butcher by profession. None of them wore gloves or
any other protective equipment. Two of them (who ultimately
died) sustained deep cut injuries over their hands during that
time. Their helpers chopped and prepared the beef without any
protection. Persons involved in skin trading carried the skin
bare handed. The beef was boiled for 50 minutes before serving.
They noticed the cutaneous lesions appearing within the next
2-4 days after slaughtering. The lesions started as one or more
painless papules, mainly on the hands and ngers transforming
soon into blisters followed by healing with a black central scar.
Some of these cases were initially associated with malaise and
both the deceased had bloody diarrhoea. They were initially
treated by a local quack with Inj. Tetanus Toxoid and some
antibiotics.
Of the 152 exposed individual, 11 had clinical manifestations
in the form of cutaneous features (papules, vesicles or eschars),
regional lymphadenopathy or gastrointestinal symptoms
(vomiting, diarrhoea or bloody dysentery) (Table2). All of the
symptomatic individuals (n=11) were involved in handling the
were swollen. There were multiple vesicles over the right upper
arm and axilla with some purplish discolouration (Figure 1a).
Cardio-pulmonary resuscitation was started but the patient died
within 20 minutes.
Soon after another patient SS (Table 3) aged about 30 years
was admied with almost identical clinical presentation. He had
right axillary lymphadenopathy with some papulo-vesicular
lesions over right ante-cubital fossa (Figure 1b). The patient died
3 hours after admission.
A detailed history from the accompanying persons revealed
that both the deceased resided in the same locality and were
suffering from identical illness for last 9 days and were
admied in the local health care facility. They were involved in
slaughtering of a dead bullock 11 days back. 2 days after that
they noticed cutaneous blisters appearing in their right hands
followed by painful swelling over the right axilla. They had
fever for the last 4 days with progressive clinical deterioration.
We decided to visit the particular village to enquire about the
symptoms, to identify new cases if any and have a conrmed
diagnosis of the disease.
Aims and Objectives
1. To have a denite diagnosis.
2. Estimate the incidence and severity of the disease.
3. To identify the probable risk factors.
4. To provide recommendations to avoid further outbreak.
Materials and Methods
A medical team comprising of faculty members from
department of Medicine, Dermatology, Microbiology,
Community medicine and the Block Medical Ocer of Health
(BMOH) visited the said village. A total of 152 people (of 36
families) were at risk. They either have ingested the cooked
Fig.1 : Cutaneous lesions and axillary swelling of RH (a) and SS (b)
Table 1 : Investigations performed in the symptomatic
individuals
Investigations performed Number of patients (%) (n=9)
Complete blood count 9 (100%)
Blood sugar, Renal function tests 9 (100%)
Liver function tests 9 (100%)
Chest X-ray 9 (100%)
Wound material for gram stain 5 (55.5%)
Wound material for culture 5 (55.5%)
Blood culture 2 (22.2%)
FNAC from axillary lymph node 1 (11.1%)
Table 2 : Clinical manifestations observed in the study
population
Clinical manifestations Number of patients (%)(n=152)
Cutaneous manifestations 11 (7.2%)
Malaise 4 (2.6%)
Vomiting 3 (1.9%)
Diarrhoea and bloody dysentery 2 (1.3%)
Lymphadenopathy 3 (1.9%)
Death 2 (1.3%)
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raw meat (either slaughtering or cooking) whereas persons who
only ingested the cooked meat (n=141) did not report to have
any clinical symptoms.
The mean age of our study population was 32.1years,
and 100% were male. The mean incubation period was three
days. Most cases (81.8%) were exposed to the bacteria during
butchering. Only two patients used an antibiotic prior to the
survey (18.2%). The predominantly aected sites were ngers
(54.5%), followed by forearms (18.2%), around elbows (18.2%)
and arm (9.1%). All cases initially had painless papules, ulcers
with vesicles; dissemination of the lesion was seen in 27.3% of
patients (Table 3). In this outbreak, the aack rate was 7% and
case fatality rate was 18%.
The baseline investigations were essentially normal except for
a minimal elevation of total leucocyte count and sedimentation
rate in the patient having axillary lymphadenopathy. The FNAC
was suggestive of acute suppurative lymphadenitis. Both the
blood cultures did not grow any organism. Gram stained smear
made from the material obtained from cutaneous vesicles
documented plenty of squamous cells with some isolated gram
positive bacilli not fully resembling Bacillus anthracis. Another
striking feature was the absence of neutrophils in the smear.
Smears were also made from nutrient broth and examined
under microscope. Smears made from the culture obtained from
cutaneous lesion of SH1 (Table 3) revealed gram positive aerobic
spore bearing bacilli in long chain with capsular halo (Figure
2). Subculture of the specimen in blood agar produced typical
medusa head colonies. It was catalase positive and non-motile.
Based on these ndings the organism was identied as Bacillus
anthracis (as per CDC guideline) and the diagnosis of cutaneous
anthrax was conrmed.
Discussion
Anthrax is a life-threatening zoonotic disease. It can be
transmied to humans by contact with infected animals or their
Fig. 2 : Gram positive bacilli in chains with spores (black arrow) and
capsular halo (red arrow)
Table 3 : Summary of the observations of the symptomatic patients
No. Name Sex Age (yr) Mode of contact Cutaneous lesions Lymphadenopathy Culture material Outcome
1 TM Male 15 Slaughtering Middle nger (Rt.) (Fig.3a) No Extract from vesicle Cured
2 DH Male 25 Slaughtering Index nger (Rt.) (Fig.3b) No Extract from vesicle Cured
3 SH (1) Male 37 Slaughtering Lile nger (Rt.) (Fig.3c) No Extract from vesicle Cured
4 SH(2) Male 45 Slaughtering Middle and ring ngers (Lt.) (Fig.4a) No ----- Cured
5 RH Male 26 Handling raw meat only Right thumb (Fig.4b) No Extract from vesicle Cured
6 KS(1) Male 45 Slaughtering Right forearm (Fig.4c) Yes (axillary) FNAC from lymph
node and blood
Cured
7 CS Male 45 Slaughtering Middle nger (Rt.) (Fig.5a) No ----- Cured
8 MS Male 15 Handling raw meat only Left elbow (Fig.5b) No Extract from vesicle and
blood
Cured
9 KS(2) Male 27 Slaughtering Left forearm (Fig.5c) No ----- Cured
10 RH Male 43 Slaughtering Arm, axilla and chest (Rt.) (Fig.1a) Yes (axillary,
cervical)
----- Died
11 SS Male 30 Slaughtering Antecubital fossa (Rt.) (Fig.1b) Yes (axillary) ----- Died
Fig. 3 : Cutaneous lesions of TM (a), DH (b) and SH (1) (c) (Table 3)
Fig. 4 : Cutaneous lesions of SH (2) (a), RH (b) andKS (1) (c)
(Table 3).
Fig. 5 : Cutaneous lesions of CS (a), MS (b) andKS (2) (c) (Table 3)
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products. Anthrax does not spread from person to person. The
agent of anthrax is a gram-positive, encapsulated, spore-forming
rod-shaped bacterium called Bacillus anthracis. Anthrax can
infect humans in three ways and thus there are three forms
of the disease: cutaneous anthrax, inhalation anthrax and
gastrointestinal anthrax. The most common type of human
anthrax infection is cutaneous anthrax which accounts for
nearly 95% of all anthrax cases worldwide. Cutaneous anthrax
occurs when either the spores or the bacteria itself enter the
body through a cut or abrasion. In most cases, symptoms begin
to develop within 48 hours, although a range of 2-7 days has
been found. Cutaneous anthrax begins as a small, red, itchy
papule at the site of infection. Within about 2 days, it develops
into a uid-lled blister that eventually ruptures. The lesion
ultimately dries into a coal-black scab (known as eschar) that
covers an area of dead skin, hence the name anthrax (Greek for
“coal”). Some patients may have painful enlargement of regional
lymph nodes. In some cases, the infection can spread through the
bloodstream and become fatal. However, death is extremely rare
in the majority of individuals who receive prompt, appropriate
treatment. If untreated, cutaneous anthrax is fatal in 20% of
cases due to spread of the bacteria throughout the body and
the release of deadly toxins in the bloodstream. However, with
appropriate treatment, cutaneous anthrax is deadly in only 1%
of cases. The patients in our study group presented late and we
observed a case fatality rate of 18% which is consistent with the
fatality rate mentioned in literature.
India, where people depend largely on livestock for their
livelihood has many regions which are still enzootic for animal
anthrax.5 A significant number of cutaneous anthrax cases
in India have been reported from Christian Medical College,
Vellore6 and JIPMER hospital, Puducherry.7,8,9 A review of
Indian literature done way back in 1996 has also found 71 cases
of cutaneous anthrax (112 cases in total) in southern India.10
Cutaneous anthrax was reported from a tribal area in Araku
Valley of Visakhapatnam district of the state of Andhra Pradesh
where people got infected after slaughtering, cooking and eating
meat of dead goats, similar to what we observed in our study.11
Four cases of cutaneous anthrax were encountered in a mini
outbreak in Vizianagaram district, of Andhra Pradesh, India
where one of the patients had axillary lymphadenopathy. Those
cases were diagnosed by conventional methods like what we did
in our patient population.12
In the background of a suggestive history some features are
strongly suggestive of cutaneous anthrax. These are oedema out
of proportion to the size of the lesion, lack of pain during the early
phases of infection and the rare presence of polymorphonuclear
leucocytes in the gram‘s stained smear made from vesicular
uid.13 We had almost similar observations in our patients. As
culture of the organism from typical skin lesions yields positive
results in approximately 60 to 65 per cent of cases, the presence of
the bacilli in the gram’s stained smear from the cutaneous lesions
and a robust epidemiological proof may be the only evidence
in favour of the diagnosis of cutaneous anthrax.14 Several other
methods, such as specic enzyme-linked immunosorbent assays,
enzyme-linked immunoelectrotransfer bloing and indirect
microhemagglutination, have been used for the serologic
diagnosis of anthrax.15 However, because of lack of availability
of the above tests in our set up we had to resort on conventional
methods like examination of gram’s stained smear and culture of
the material obtained from cutaneous lesions and blood culture
in cases of suspected septicaemia. We had only one positive
culture (20%) and this may be aributable to the late presentation
of the cases and prior antibiotic use by the local quack.
To the best of our knowledge till date there is only one study
that has reported cutaneous anthrax from eastern India.16 We
observed a number of similarities between the present study and
this study from Murshidabad district of West Bengal. In both the
studies the aack rate was highest among the age group 15-45
years. It was also found that persons who were not involved in
slaughtering or handling meat or skin and whose sole exposure
was eating the cooked beef did not have any manifestations of the
disease. The isolation rate of the causative bacterium in our study
is identical to that in the second outbreak observed by Ray et.al.
Cutaneous anthrax, like the more deadly inhalational
anthrax, is treated with antibiotics. The CDC recommends
rst-line treatment with ciprooxacin or doxycycline. Other
recommended antibiotics are erythromycin and penicillin. Cases
of naturally occurring cutaneous anthrax are treated with a
10-14 day course of antibiotics. However, a full 60-day course
of antibiotics is recommended for cases of cutaneous anthrax
associated with bioterrorism. We have used ciprooxacin and
penicillin in our cohort.
Our study had some limitations. We could not ascertain the
cause of death in those two individuals though septicaemia
with multi-organ dysfunction was considered. One noticeable
thing was that both of them sustained deep cut injuries during
slaughtering which may have contributed to a higher bacterial
inoculation and sepsis. Causes of death in anthrax include
asphyxiation from oedema of the neck with tracheal compression
and concurrent gastrointestinal anthrax.17 Both of the deceased
had bloody diarrhoea and one of them had swelling of neck.
However, we are not sure whether the gastrointestinal symptoms
were the manifestations of gastrointestinal anthrax. Moreover,
because of lack of infrastructure we could not perform autopsies
on those patients.
Conclusions
To summarise our ndings, the disease was limited to the
tribal population engaged in butchering the dead animal bare
handed. The symptoms appeared 2-3 days after butchering
and the lesions were painless and healed with central black
scar. Because this anthrax outbreak was associated with a very
high case fatality rate, probably due to the late presentation,
we suggest that the healthcare providers in anthrax-endemic
areas should be educated about the signs and symptoms of
the disease, so that early initiation of appropriate antibiotic is
possible. Dierent medical and government agencies should
arrange medical education programmes to sensitize the primary
care givers about the possible signs and symptoms of anthrax
and should provide adequate supply of antibiotics for early use
in such outbreaks. More importantly perhaps, the community
must be educated about using personal protective gears during
butchering of ruminant animals and handling of raw meat and
skins.
To prevent such outbreak some simple precautions may be
adopted by the local population.
1. Protective, impermeable clothing and equipment such as
rubber gloves, rubber apron, and rubber boots with no
perforations should be used when handling the body of an
anthrax infected animal or person. No skin, especially if it
has any wounds or scratches, should be exposed.
2. Eective decontamination of possible anthrax-contaminated
sites can be accomplished by a thorough wash down with
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antimicrobial soap and water. Waste water should be
treated with bleach or other anti-microbial agent. Eective
decontamination of articles can be accomplished by
boiling contaminated articles in water for 30 minutes or
longer. Chlorine bleach is ineective in destroying spores
and vegetative cells on surfaces, though formaldehyde is
eective. Burning clothing is very eective in destroying
spores.
3. Cremating victims is the preferred way of body disposal.
Delays of only a few days may make the disease untreatable
and treatment should be started even without symptoms if
possible contamination or exposure is suspected.
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