Transactions of the Royal Society of Tropical Medicine and Hygiene (2008) 102, 729—734

available at www.sciencedirect.com

journal homepage: www.elsevierhealth.com/journals/trst

REVIEW

Epidemiology of hepatitis B virus infection among

the tribes of Andaman and Nicobar Islands, India
Manoj V. Murhekar a,∗, Kanchan M. Murhekar b, Subhash C. Sehgal c

a
National Institute of Epidemiology (ICMR), Chennai, Tamilnadu, India
b
Department of Pathology, Cancer Institute (WIA), Adyar, Chennai, Tamilnadu, India
c
Regional Medical Research Centre, Port Blair, Andaman and Nicobar Islands, India

Received 10 December 2007; received in revised form 28 April 2008; accepted 28 April 2008
Available online 18 June 2008

KEYWORDS Summary The Andaman and Nicobar Islands, Union Territory of India, are home to six primitive
tribes, namely the Great Andamanese, Onges, Jarawas and Sentinelese (Negrito race), and the
Hepatitis B;
Shompens and Nicobarese (Mongoloid race). These tribes account for about 8% of the island’s
Hepatitis B surface
population and the Nicobarese constitute >95% of the tribal population. Hepatitis B virus (HBV)
antigen;
infection is highly endemic among them with the prevalence of hepatitis B surface antigen
Disease transmission;
(HBsAg) ranging from 23% among the Nicobarese to 66% among the Jarawas. The high HBsAg
Tribes;
prevalence among pregnant mothers (20.5%), a linear increase in the age-specific rates of HBV
Andaman and Nicobar
exposure and the presence of HBsAg-positive individuals in every family suggested a combination
Islands;
of perinatal and horizontal transmission among the Nicobarese. Molecular studies of HBV isolates
India
from the Onges, Nicobarese and Great Andamanese indicated a predominance of genotype D and
there was a close similarity between these isolates and isolates from mainland India, suggesting
that HBV may have been introduced from mainland India. In contrast, genotype C predominated
among the Jarawas, with isolates similar to strains from Southeast Asian countries. Due to its
high prevalence, hepatitis B vaccine is included in the childhood vaccination programme in these
islands. It might be worth considering a pilot screening programme for chronic HBV patients to
detect hepatocellular carcinoma.
© 2008 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights
reserved.

1. Introduction

In 1963, Blumberg, in a search for polymorphic serum pro-

∗ Corresponding author. Present address: R-127, Tamilnadu Hous-
ing Board, Ayapakkam, Ambattur, Chennai 600 077, Tamilnadu,
India. Tel.: +91 44 2635 7476.
E-mail address: mmurhekar@yahoo.com (M.V. Murhekar).
teins, discovered a previously unknown antigen (Australia
antigen) in the blood of an Australian Aborigine (Blumberg
et al., 1965). Subsequently, the appearance of this antigen
was related to type B hepatitis (Blumberg et al., 1967). After
the discovery of Australia antigen, several studies reported a

0035-9203/$ — see front matter © 2008 Royal Society of Tropical Medicine and Hygiene. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.trstmh.2008.04.044
730 M.V. Murhekar et al.

higher prevalence of hepatitis B virus (HBV) infection among

the Aboriginal populations than in the general population

al., 2002a
al., 2004a
al., 2000

Murhekar et al., 2003

(Coimbra Júnior et al., 1996; Gaxotte et al., 1978; Gust et
al., 1978; Hart, 1993; Lin et al., 2000). In India, the preva-

al.,
lence of hepatitis B surface antigen (HBsAg) among the tribes

et
et
et
et
was estimated to vary from 10.15% (95% CI 10.1—10.2) to
Reference

Murhekar
Murhekar
Murhekar
Murhekar
15.9% (95% CI 11.4—20.4) (Batham et al., 2007; Murhekar
and Zodpey, 2005). This prevalence was several-fold higher

2000
than the estimated carrier rate of 2.4—4.7% in the non-tribal
population (Batham et al., 2007; Thyagarajan et al., 1996).
In the present paper, we review the epidemiology of HBV
infection among different tribes of the Andaman and Nicobar
Islands.
41.7 (38.9—44.6)
73.7 (70.7—76.6)
43.8 (41.3—46.2)
48.2 (35.7—61.1)
40.5 (25.7—56.8)
Overall exposure

18.5 (7.1—36.4)
75 (63.3—84.4) 2. The tribes of the Andaman and Nicobar
(%) (95% CI)

Islands

The Andaman and Nicobar Islands, Union Territory of India,

Prevalence of different markers of hepatitis B infection among the tribes of Andaman and Nicobar islands, India

are an archipelago of over 300 islands in the Bay of Bengal.

These islands are the home of six tribes, namely the Great
Andamanese, Onges, Jarawas and Sentinelese of the Negrito
race, and the Nicobarese and Shompens of the Mongoloid
23.9 (21.2—26.9)
26.3 (23.0—29.9)

race. These tribes who number about 30 000 constitute 8.3%

15.4 (5.1—33.1)
25 (13.5—40.1)
4.3 (0.2—19.6)

of the total population of these islands (2001 census). More

(%) (95% CI)

than 98% of the tribal population is constituted by the Nico-

Anti-HBs

barese who reside predominantly in the Nicobar group of

islands. The population of other tribes, especially those
NT

NT

belonging to Negrito race, however, has shown a declining

trend over several decades. The Great Andamanese, who
had a population of 4000—5000 in the 1860s, numbered 37
in the 2001 census, making them the smallest tribal commu-
nity in India (Chakraborty, 1990). They are now rehabilitated
27.5 (25.0—30.0)

68.8 (56.7—79.1)

on Strait Island. The Onges, who inhabit the Dugong creek

54 (49.5—58.4)

and South Bay areas of the Little Andaman Islands number

(%) (95% CI)

100, and the Jarawas who inhabit the west coast of south and
Anti-HBC

middle Andaman have an estimated population of 275. The

Jarawas did not have friendly relations with non-Jarawa peo-
NT

NT
NT
NT

ple and were living in isolation until recently. However, in the

past 4—5 years, they have started to come out of their habi-
23.3 (21.0—25.9)
22.2 (19.5—25.1)
22.5 (20.5—24.6)

37.8 (23.4—54.1)

65.6 (53.4—76.5)

tat, shedding their hostility, and are mixing with outsiders.

3.7 (0.2—16.9)
31 (20.5—44.4)

The Sentinelese, who inhabit North Sentinel Island, are still

hostile to the outside world. The Shompens, a nomadic tribe
HBsAg (%)

who inhabit the Great Nicobar Islands, have an estimated

(95% CI)

population of 157. Besides the tribes, settlers from mainland

HBsAg: hepatitis B surface antigen; NT: not tested.

India reside in these islands. These islands are frequently

visited by tourists from the Indian sub-continent.

3. Prevalence of HBV infection among the

No. tested

Nicobarese
1144
887
1574
58
37
27
64

3.1. Serological markers of HBV infection

A high prevalence of HBV infection among the tribal popula-

tion of the Andaman Islands was first reported by Arankalle
et al. (1999). They observed HBsAg prevalence of 15.5% in
Andamanese

retrospective testing of sera samples collected during 1989

Nicobarese

Shompens

(Arankalle et al., 1999). During the year 2000, Murhekar

Jarawas
Table 1

Onges

et al. (2000) reported a HBsAg prevalence of 23.3% (95%

Tribe

CI 21.0—25.9) and anti-HBs prevalence of 23.9% (95% CI

21.2—26.9%) among the Nicobarese.
Hepatitis B among tribes of Andaman and Nicobar Islands
Another survey conducted among the Nicobarese aged
45 years or less in a tribal village of Car Nicobar Island
revealed that 73.7% (95% CI 70.7—76.6) of the popula-
tion was exposed to HBV and 22.2% (95% CI 19.5—25.1%)
of them were positive for HBsAg (Murhekar et al., 2002a)
(Table 1). In the same village, all the 27 tuhets (which
denotes an extended family in Car Nicobar) had at least
one individual positive for HBsAg with the mean number of
carriers in the tuhet of 7.3 (SD 4.9, range 1—18). Hepati-
tis B e antigen (HBeAg) positivity among the HBV carriers
was 18.4%. The prevalence observed among the Nicobarese
was higher than the weighted prevalence among the Indian
tribes (Batham et al., 2007; Murhekar and Zodpey, 2005).
Serological tests in these studies were conducted at the
National Institute of Virology, Pune and Regional Medical
Research Centre, Port Blair, using commercially available
ELISAs.
3.2. Prevalence among pregnant women
The HBsAg positivity among pregnant Nicobarese women
was 21%. Thirteen percent of the HBsAg-positive mothers
were positive for HBeAg. The prevalence of HBsAg observed
among the Nicobarese was several-fold higher than the
prevalence reported among non-tribal pregnant women in
India, whereas the HBeAg positivity among carrier mothers
was comparable with non-tribal women. HBsAg prevalence
reported in studies among non-tribal women ranged from
0.6% to 9.5% whereas the HBeAg positivity among HBV
carrier mothers varied between 8% and 47%, with most
of the studies showing positivity towards the lower end
of this range (Biswas et al., 1989; Gupta et al., 1992;
Mittal et al., 1996; Nayak et al., 1987; Prakash et al.,
1998).
3.3. Age-related prevalence
Five percent of the Nicobarese infants were HBsAg positive.
Thereafter, the prevalence of HBsAg and overall expo-
sure to HBV increased linearly with age and by 5 years
of age, 25% of children had been exposed to HBV with
13.5% chronic carriers (Murhekar et al., 2004a). By 15
years of age, 44% of the children had been exposed to
the virus with about 23% HBsAg positive (Murhekar et al.,
2004a). The overall exposure reached 90% among individu-
als aged 25—34 years with 27.4% HBV carriers (Murhekar et
al., 2002a). On the other hand, studies conducted among
non-tribal populations in India showed that the HBsAg
positivity among infants was 2.4% (Kant and Hall, 1995;
Tandon et al., 1991), while pre-school children have an
HBV carrier rate of between 2% and 3%, which is the same
as that recorded among adults in India (Tandon et al.,
1996).
3.4. Perinatal versus horizontal transmission
The high HBsAg prevalence among pregnant mothers, a
linear increase in the age-specific rates of HBV exposure
and the presence of HBsAg-positive individuals in every
tuhet suggested a combination of perinatal and horizontal
731
transmission among the Nicobarese. With HBsAg prevalence
of 21% among pregnant women, HBeAg positivity of 13%
and assuming 80% efficiency of perinatal transmission, the
frequency of HBV carriers among the Nicobarese due to peri-
natal infection would be 2.2%. Thus, the proportion of HBV
carriers due to perinatal transmission among the Nicobarese
is estimated to be 9.6%. With an HBsAg positivity of 23%
among children aged 15 years or less, the ratio of childhood
to perinatal transmission in causing HBV carriage in children
(HBsAg prevalence among children minus HBsAg prevalence
due to perinatal infection divided by HBsAg prevalence due
to perinatal infection) (WHO, 1990) is estimated to be 9.5:1.
This finding suggests the relative importance of horizontal
transmission compared to the perinatal route among the
Nicobarese.
3.5. Role of unsafe injections
Besides horizontal and vertical routes, a case—control study
conducted in Car Nicobar also identified that a history
of hospitalization and intramuscular (i.m.) injections were
important risk factors for HBV infection (Murhekar et al.,
2002a). Malaria is highly endemic in the Nicobar group of
islands (Giri and Das, 1993). The case—control study iden-
tified that fever was the most commonly reported reason
for hospitalization and receiving injections. All the injec-
tions were administered in a hospital setting and 89% of the
individuals who received i.m. injections reported the use of
glass syringes.
However, an assessment of injection-related practices
in the Nicobar Islands in 2004 showed increasing use
of new disposable equipment for administering injections
in this population as well as availability of sufficient
stock of such injections in different sub-centres. The
change was attributed to the awareness generated among
health authorities about the higher HBV prevalence
among the tribes by earlier studies (Murhekar et al.,
2005b).
3.6. Hepatitis B disease burden
In spite of high rates of HBsAg, very little information
is available about hepatitis B disease burden among the
Nicobarese. The number of HBV infections and serious dis-
ease outcomes, however, can be estimated using input
data including the results of HBV prevalence studies and
other data based on the mathematical model developed by
Goldstein et al. (2005). With the HBsAg positivity of 21%
among pregnant women, HBeAg positivity of 13% among
women of childbearing age, anti-HBc prevalence of 13%
at 5 years and 78% at the age of 30 years and assum-
ing a surviving birth cohort of 458 (birth rate = 15.7/1000
and infant mortality rate = 27/1000) (Central Bureau of
Health Intelligence, Government of India, 2006), as per
the model, it is expected that HBV infection would result
in 93 acute symptomatic and 47 chronic cases. Assum-
ing no vaccination programme, seven HBV-related deaths
are expected to occur in this birth cohort. Of these, four
would be due to cirrhosis and three to hepatocellular carci-
noma.
732
4. Prevalence of HBV infection among the
non-Nicobarese tribes
HBsAg positivity among the non-Nicobarese tribes of these
islands ranged from 3.7% (95% CI 0.2—16.9) among the Great
Andamanese, 31% (95% CI 20.5—44.4) among the Onges to
37.8% (95% CI 23.4—54.1) among the Shompens. The cor-
responding figures for anti-HBs among these tribes were
15.4% (95% CI 5.1—33.1), 25% (95% CI 13.5—40.1) and 4%
(95% CI 0.2—19.6%), respectively (Murhekar et al., 2000).
The prevalence of HBsAg among the Jarawas was alarmingly
high, with 65.6% of the samples tested being positive for
HBsAg (Murhekar et al., 2003). Overall 75% of the Jarawas
were exposed to HBV. HBV exposure rates were high among
young children with 86.4% children positive for HBsAg and/or
anti-HBc. The closed nature of these communities, inbreed-
ing, small population size, poor hygienic living conditions
and close person-to-person contact might be some of the
factors facilitating extensive horizontal as well as vertical
transmission leading to very high rates of HBV infection.
Besides, certain socio-cultural practices prevalent among
these tribes might also be involved in transmission of the
virus.
5. HBV genotypes among the tribes
HBV genotypes reflect the geographical distribution of HBV
and are often useful in understanding the possible origin of
the infection. Genotyping of the HBV isolates from the tribes
of these islands indicated the predominance of genotype
D among the Nicobarese, Onges and Andamanese whereas
genotype C was prevalent among the Jarawas (Arankalle
et al., 2003; Murhekar et al., 2006). Genotype C is preva-
lent in Southeast Asian countries (Norder et al., 2004)
from where these tribes are believed to have originated
(Bellwood, 1997; Prasad et al., 2001; Thangaraj et al.,
2003). The isolates from the Nicobarese differed from the
mainland Indian isolate of D genotype by 1.6—2.0% while
HBV strains from Jarawas were found to be most closely
related in terms of evolutionary distance to a strain isolated
from Thailand (percent nucleotide identity = 99.44 ± 0.2).
These findings suggest that the Jarawas carried HBV geno-
type C during their migration, possibly several thousand
years ago, and the same genotype is still circulating, in
the absence of contact with outsiders. On the other hand,
the close similarity of HBV strains from Nicobarese with
mainland Indian isolates suggests that the introduction of
HBV among them might have taken place after their migra-
tion to these islands. Genotype C, if carried by them
during migration from Southeast Asia, might have been
replaced by genotype D during contact with settlers from
mainland India (Arankalle et al., 2003; Murhekar et al.,
2006).
6. Delta hepatitis and other blood-borne virus
infections
Screening of HBsAg-positive sera samples from the Nico-
barese and Onges revealed presence of IgG anti-delta
antibodies among 5% of the Nicobarese samples, while none
M.V. Murhekar et al.
of the samples from the Onges was positive (Murhekar et al.,
2005a). The infection was found to be present in eight of the
27 tuhets (29.6%) in one village, suggesting that the infec-
tion is widespread in the community. However, screening of
other HBsAg-positive individuals in the tuhet showed than
none of them was positive for anti-delta antibodies thereby
indicating that intrafamilial spread of HDV infection among
the Nicobarese is infrequent (Murhekar et al., 2005a).
Serological testing of 710 samples from the Nicobarese,
Onges, Andamanese and Shompens revealed a very low
prevalence of hepatitis C virus (HCV). Only two samples
from Nicobarese were positive for antibodies against HCV
with an overall prevalence of 0.34% (Murhekar et al., 2004c).
HIV infection has also been reported among the Nicobarese
(Sarkar et al., 1994).
7. Hepatitis B vaccination
Considering the high prevalence of HBV infection, a pilot
project of HBV vaccination using an indigenously devel-
oped vaccine (Shanvac-B, Shantha Biotechnics, Medchal, AP,
India) was initiated among the Nicobarese. The vaccine was
administered to all the HBsAg negative individuals aged 45
years or less in two tribal villages in Car Nicobar Islands.
The seroprotection rates after the completion of a course of
three doses of vaccine, and two and three years later, were
97%, 89% and 85.5%, respectively (Murhekar et al., 2002b,
2004b). The vaccination project was subsequently extended
to cover all the students studying in 13 primary schools of
the island (ICMR, 2007).
8. Conclusions and implications
Hepatitis B virus infection is hyperendemic among the tribal
populations of Andaman and Nicobar Islands. The infection
is transmitted both by perinatal and horizontal routes. Delta
virus infection was detected among the HBV carriers in Nico-
barese. Genotype D was found to be predominant among the
Nicobarese, Onges and Andamanese, and genotype C was
prevalent among the Jarawas.
Considering the high endemicity of HBV infection, the
Government of India recently introduced hepatitis B vaccine
in the universal immunization programme in these islands
with three doses of the vaccine starting at the age of 6
weeks. In adding hepatitis B vaccine to the childhood immu-
nization programme, an important consideration is the use
of a birth dose of vaccine for prevention of perinatal trans-
mission. In several Asian countries, HBeAg positivity among
HBV carrier pregnant women is high (Evans and London,
1998; Gregorio, 1998). In such situations, an additional birth
dose of the vaccine is often recommended (WHO, 2002).
On the other hand, among the tribes of these islands,
horizontal transmission contributed more to the overall hep-
atitis B disease burden than the perinatal mode. Besides,
many of the deliveries in Nicobarese are conducted in their
traditional birth-houses. Considering these factors, a birth
dose of the vaccine might not be beneficial in this commu-
nity.
As the majority of chronic infections are acquired in early
years of life, the impact of hepatitis B vaccination is the
maximum when it is done at birth. However, in regions with
Hepatitis B among tribes of Andaman and Nicobar Islands
high endemicity, it may be useful to immunize, in addi-
tion to newborns, pre-school children since the latter may
also be at a significant risk of acquiring chronic hepatitis B.
The cost-effectiveness of immunization of all the children
below the age of 5 years, in addition to newborns, revealed
that this strategy would provide additional advantages with
gain in life years and quality-adjusted life years as com-
pared to the strategy of vaccinating newborns alone (M.V.
Murhekar and R. Aggarwal, unpublished document). A strat-
egy of immunization of older age groups has been used in
the past in hyperendemic regions like Taiwan with excellent
results (Medley et al., 2001).
Besides vaccination of newborns and young children,
screening a large pool of chronic HBV patients for hepatocel-
lular carcinoma (HCC) could be an important issue among the
tribal population of these islands. Population-based screen-
ing of HBsAg-positive carriers for HCC using an inexpensive
test of alpha-fetoprotein determination among the Alaskan
natives showed that in most HBsAg-positive carriers, HCC
can be detected at an early, potentially resectable stage and
had significant survival benefits at 5 and 10 years in screened
carriers compared with historical controls (Mcmahon et
al., 2000). Similar programmes were also implemented in
Taiwan (Chen et al., 1995). Though cost-effectiveness of
the population-based screening programmes remains to be
elucidated, it might be worthwhile to consider such pro-
grammes on a pilot basis among the tribes of the Andaman
and Nicobarese Islands.
Funding: None.
Conflicts of interest: None declared.
Ethical approval: Not required.
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