World Journal of Cardiovascular Diseases, 2013, 3, 512-518 WJCD Published Online November 2013 (
Carrier rate of hepatitis B surface antigen (HBsAg) among
urban pregnant women in a secondary health
facility in Maiduguri, Northeastern Nigeria
David Nadeba Bukbuk1, Maxwell Bayo Samaila2, Akawu Denue Ballah3,
Ibrahim Musa Kida3, Chima Iwuoha2
1Department of Microbiology, Faculty of Science, Essien Udom Court, University of Maiduguri, Maiduguri, Nigeria
2Department of Biological Sciences, Faculty of Science, Essien Udom Court, University of Maiduguri, Maiduguri, Nigeria
3Department of Medicine, College of Medical Sciences, University of Maiduguri, Maiduguri, Nigeria
Received 22 August 2013; revised 29 September 2013; accepted 12 October 2013
Copyright © 2013 David Nadeba Bukbuk et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
A serological survey conducted among 196 pregnant
women resident in and around Maiduguri, an urban
town in north eastern Nigeria showed that 33 (16.8%)
were asymptomatic carriers of hepatitis B virus sur-
face antigen (HBsAg). They are within the age range
of 14 - 40 years with mean (± SD) age of 24.7 (± 6.3).
The women attend antenatal clinic at the State Spe-
cialist Hospital, a secondary health facility in
Maiduguri, Borno state. The women are all hetero-
sexuals. The distribution of HBsAg carrier rate ac-
cording to age of women studied showed a significant
(p = 0.0061) increase of the prevalence of HBsAg from
4 (8.7%) in the lower age group (<20 years) to 1 (50%)
among those in the higher age group (>39 years). Ac-
cording to the number of pregnancies, the prevalence
of HBsAg infection increased significantly from 6
(9.2%) among primiparous to 13 (13.7%) and 14
(38.9%) among multiparous and grand multiparous
respectively. The carrier rate of HBsAg infection
among the pregnant women studied based on their
duration of pregnancies and their social class showed
no significant differences. However, according to the
factors known to be commonly associated with the
highest risk of transmission of HBV such as history of
blood transfusion, Tribal marks/tattooing, use of
sharps, sharing of articles, history of jaundice in the
women and husbands, history of sexually transmitted
infections (STIs) of the women and husban ds and the
type of marriage (monogamous or polygamous), num-
ber of sexual relationships per week, only the history
of blood transfusion was significantly associated with
HBsAg carrier rate (RR = 3.71., 95% Confidence In-
terval (C.I.), 1.89 - 7.30, p = 0.0078). The study con-
firms that pregnant women who attend antenatal
clinic in this secondary health facility are at higher
risk of being infected with the HBV, which could lead
to both prenatal and post natal transmission to their
Keywords: Carrier Rate; HBsAg; Urban; Pregnant
Women; SSH; Borno State; Nigeria
Hepatitis B is one of the commonest and most wide-
spread infections of humans [1]. It is estimated that world-
wide more than two billion people have been infected by
HBV and 350 million people have chronic infection [2].
Worldwide, HBV infections account for 1 million deaths/
year, most of which occur in the developing world [3].
The prevalence of infection with the virus varies
greatly from country to country and even within the same
country or continent. This variation depends upon a com-
plex of behavioural, environmental and host or genetic
factors [1]. The variation in prevalence of the infection is
significant within the different geographic areas of the
world and can be divided into areas of high, intermediate
and low endemicity based on the prevalence of HBV
markers and carriers [4]. The infection appears to be
highly endemic in areas such as Southeast Asia, the
Amazon Basin, sub-Saharan Africa and areas of China,
where an estimated 70% - 90% of the population shows
serologic evidence of previous or current hepatitis B in-
fection and high carrier rates of 8% - 20% [4]. In the
intermediate endemicity areas such as Middle East, Ja-
pan, North Africa, Central and Latin America, Russia and
parts of eastern and southern Europe, 20% - 55% of the
D. N. Bukbuk et al. / World Journal of Cardiovascular Diseases 3 (2013) 512-518 513
populations show markers and 2% - 7% are carriers [5].
North America, western and northern Europe and Austra-
lia are classified as low endemicity areas with a preva-
lence of HBV markers ranging from 4% - 6% and a car-
rier rate of 0.5% - 2%. In high endemicity areas, neo-
nates are most at risk, through infection from carrier
mothers during pregnancy or just after birth [6,7]. Be-
cause of the high carrier rate, those in the general popu-
lation who have not had the infection remain at risk of
being infected throughout their lives from those carriers
in their midst [8]. In areas of intermediate endemicity,
however, young children are mostly at risk through hori-
zontal transmission [9]. While in low endemicity areas,
heterosexual transmission makes adolescent and young
adults the highest risk group [10]. Travellers to areas of
high endemicity are also at increased risk [11].
Nigeria is classified among the group of countries
highly endemic for HBV infection, where about 75% of
the populace is reported likely to have been exposed to
HBV at one time or the other in their life [12]. The clas-
sification of high endemicity for HBV has been defined
as HBsAg greater than 7% in an adult population [13].
In regions where hepatitis B is endemic, high inci-
dence of hepatoma (liver cancer) has also been recorded
and a strong association between HBV infection and
liver cancer established [14]. Worldwide, it has been re-
ported that those who become carriers in adulthood have
a 15-40-fold increased risk of developing chronic liver
disease and primary liver cancer [15]. HBV may be the
cause of up to 8% of all cases of hepatocellular carci-
noma worldwide second only to tobacco among known
human carcinogens. This cancer is very common in the
Maiduguri area [16] where hepatitis B virus in the popu-
lation is also known to be highly prevalent [17-19].
Pregnant women are a very important group to study
with regards to HBV transmission, since infection with
HBV is mainly transmitted through the mother-to-neo-
nate route in endemic countries, where in most cases,
chronic infection results and the transmission will there-
fore occur from generation to generation [20]. Perinatal
and postnatal transmission of the virus had been stated to
be important in some societies in South East Asia [21].
Ghana [22] and Nigeria [23,24]. Many children who ac-
quired the virus in the early years of life may eventually
become carriers with its attendant complications. There-
fore, prevention of early childhood infection will eventu-
ally reduce the prevalence of HBsAg in early childhood
and coupled with the advent of an effective HBV vaccine,
such preventive measures and treatment options with drugs
such as peg-interferon and lamivudine among others are
The present study aims to determine the possible risk
factors associated with HBV transmission among preg-
nant women and the prevalence of one of the markers of
hepatitis B virus infection (HBsAg). And also to suggest
possible preventive and control measures for hepatitis B
virus infection among pregnant women in our commu-
2.1. Study Area and Study Population
The study was carried out at the Antenatal Clinic of the
State Specialist Hospital, Maiduguri, Borno State, Nige-
ria. The clinic has the capacity of attending to over 500
pregnant women monthly. Pregnant women from within
Maiduguri metropolis and from other parts of the state
attend the clinic. A total of 196 pregnant women in the
age range of 14 - 40 years, mean (SD) age of 24.7 (6.3)
years and a median age of 23 years were recruited and
tested for the presence of HBsAg. They were studied be-
cause of the increased risk of either acquiring or spread-
ing hepatitis B virus to their newborns/spouses. The so-
cial class of the women involved in the study was assess-
ed using the scoring method earlier proposed [25]. This
is obtained through a scoring index combining a wo-
man’s level of education with the occupation of her hus-
band, which allocates each woman to a social class I to V,
social class V being at the bottom of the social stratifica-
tion. The suitability and application of this social classi-
fication system for our environment has been well tested
and presented elsewhere [26,27].
2.2. Sample Collection
After explaining the purpose of the study to the women,
from those that expressed verbal or written consent to
participate about 5ml of blood were aseptically drawn by
venepuncture into sterile clean test tube containers. The
blood were allowed to clot at room temperature and sera
separated by centrifugation at 1,500 rpm for 5 min. The
separated sera were aspirated into clean cryogenic vials,
labelled and stored frozen at 20˚C until tested.
2.3. Screening and Confirmatory Assay on the
Serum Samples for HBsAg
All sera samples were thawed once and thereafter
screened for the presence of hepatitis B surface antigen
using KEMRI HEP CELL II B (HBsAg) a reversed pas-
sive haemagglutination test kit for the detection of hepa-
titis B surface antigen produced by the Kenya Medical
Research Institute (KEMRI) and developed at the centre
for virus Research, Hepatitis Division. In this system, a
serum is considered positive if the coated sheep erythro-
cytes in the microplate wells forms an agglutination with
the test serum and is considered negative if the coated
sheep erythrocytes settle and form a button-like precipi-
tate in the bottom of the well of the microplate. The prin-
ciple of the assay is that when the test serum or plasma
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D. N. Bukbuk et al. / World Journal of Cardiovascular Diseases 3 (2013) 512-518
are mixed with anti-HBs coated sheep erythrocytes in a
microplate and incubated at room temperature, the sam-
ples that contain HBsAg will form an agglutination pat-
tern during the incubation period. On the other hand,
those samples that contain no HBsAg will not form any
agglutination instead the coated sheep erythrocyte will
settle to form a button-like precipitate. The presence of
HBsAg is thereafter determined by the appearance of the
agglutination patterns. All the positive sera samples were
later confirmed as positive by inhibition of agglutination
using confirmation inhibition assay according to instruc-
tions of the kit manufacturers. In this system a positive
result for the presence of HBsAg showed a decrease of
agglutinating titre. Those samples that showed no fall in
agglutinating titre were presumed as negatives for
HBsAg. A positive control and negative control sera are
included in each assay.
2.4. Data Analysis
All data generated from the study were entered analyzed
using Epi Info version 6.04d [Centers for Disease Con-
trol and Prevention, Atlanta, GA, USA
( /) and World Health Organization,
Geneva, Switzerland (] and GraphPad
Prism version 5.00 for Windows (GraphPad Software,
San Diego California USA, Socio-
demographic characteristic or variables of the women
studied were calculated and expressed as means, stan-
dard deviation (SD), median, range, frequencies and per-
centages. Chi-square and linear chi-square for trend were
calculated for categorical variables such as age groups,
parity, duration of pregnancy, duration of marriage, ave-
rage number of sexual relationships per week and social
class and compared with the carrier rate of HBsAg in the
group, while fisher exact test was used as appropriate.
Relative risks (RR) and 95% confidence intervals (95%
C.I.) were also calculated to assess the association be-
tween the different risk factors for HBsAg transmission
and HBV infection in the study group. The data on the
occupation of the women and their spouses studied were
represented as charts. A p-value of less than or equal to
0.05 was considered as significant.
3.1. Socio-demographic Characteristics of the
Pregnant Women S tu died
A total of 196 pregnant women at various stages of ges-
tation were recruited/studied at the State Specialist Hos-
pital Maiduguri, Borno State for the prevalence and risk
factors to HBV infection. Table 1 shows some socio-
demographic characteristics of the pregnant women stu-
died. They fall within the age range of 14 to 40 years
with mean (SD) age of 24.7 (6.3) years and a median age
Table 1. Socio-demographic characteristics of the pregnant
women studied.
Characteristics Mean ± SD MedianRange
Age (years) 24.7 ± 6.3 23 14 - 40
No. of pregnancies 3.4 ± 2.5 3 1 - 12
Duration of pregnancy (months)7.2 ± 1.4 7 3 - 9
Duration of marriage (years) 6.6 ± 5.9 5 0.5 - 30
Mean no. sexual relationships
(week) 2.3 ± 1.0 2 1 - 5
Social class Frequency Percentage
I 8 4.1
II 22 11.2
III 58 29.6
IV 48 24.5
V 60 30.6
SD, Standard deviation, No., Number.
of 23 years. The mean (SD) duration of pregnancies were
7.2 (1.4) months with a range of 3 to 9 months while the
number of pregnancies were of the mean (SD) of 3.4 (2.5)
and range of 1 to 12. The mean (SD) duration of mar-
riage were 6.6 (5.9) years with range of 6 months to 30
years and median of 5 years, while mean (SD) number of
sexual relationships with their husbands are of the risk
factors earlier found to be associated with HBV infection
was 2.3 (1.0), range of 1 to 5. The socio-economic clas-
sification of the women shows that very few of them
belonged to the higher social classes of I and II, with
4.1% and 11.2% respectively. About 30.6% belonged to
class V and 29.6%, 24.5% in classes III and IV respec-
3.2. Distribution of the Occupation of the
Wo men and Their Husbands
Figures 1 and 2 are pie charts showing the distribution of
the occupation of the women and that of their husbands.
Farming appears to be the least occupation engaged by
the two groups with only 1% and 2% among wives and
husbands respectively. Those attending various schools
are higher in the women (6% vs. 2%) than in the hus-
bands, while most husbands are traders/ Business men
and civil servants (40% vs. 37%), most of the women are
full time house wives (FTHW) (64%) and only 17% are
Traders/Business women.
3.3. Distribution of HBsAg According to
Maternal Age
The prevalence of HBsAg according to maternal age is
as shown in Ta b l e 2 . The prevalence rate increases sig-
nificantly with the age of the mothers studied from 8.7%
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D. N. Bukbuk et al. / World Journal of Cardiovascular Diseases 3 (2013) 512-518 515
Farming (1%)
Trading/Buss. (17%)
Civil servant (12%)
Schooling (6%)FTHW (64 %)
Figure 1. Occupation of the Women studied.
Mechanic (5%)
Farming (2%)
Dri ving (9% )
Paramil ./Mil. (5%)
Trading/Buss. (41%)
Civil servant (3 7%)
Schooling (2%)
Figure 2. Occupation of Husbands of the Wome n studie d.
among those under the age of 20 years to 18.4%, 36.4%
and 50% in the age groups of 25 - 29 years, 35 - 39 years
and those above 39 years respectively (X2 linear trend =
7.535, p = 0.0061).
3.4. Prevalence of HBsAg According to Number
and Duration of Pregnancies
Table 3 shows the prevalence of HBsAg according to the
number of pregnancies. There were no nulliparous wo-
men in the study, while the prevalence rates of the
HBsAg increased significantly from 9.2% among primi-
parous women to 13.7% and 38.9% among multiparous
and grand-multiparous women respectively. (X2 = 15.86,
df = 2, p = 0.0004). The prevalence of HBsAg according
to duration of pregnancies is as shown in Table 4. Al-
though, the seroprevalence of HBsAg increased from
10.3% in women who had between 3 to 5 months of
pregnancies to 16.8% and 22.2% in 6 to 8 and more than
8 months of pregnancies respectively. There was no sta-
tistically significant difference between them (X2 = 1.619,
df = 2, p= 0.445).
3.5. Distribution of HBsAg According to the
Social Status of the Women Studied
On the basis of the social status of the women studied
(Table 5), there was no statistically significant difference
Table 2. Distribution of HBsAg according to maternal age.
Age group (Years)No. testedNo. positive (%) (95% CI)
< 20 46 4 (8.7) (1.8284 - 1.9976)
20 - 24 62 9 (14.5) (1.7647 - 1.9450)
25 - 29 38 7 (18.4) (1.6867 - 1.9449)
30 - 34 26 4 (15.4) (1.6975 - 1.9948)
35 - 39 22 8 (36.4) (1.4181 - 1.8547)
40 - 44 2 1 (50.0) -
Total 196 33 (16.8)
X2 linear trend = 7.535, df = 1, p = 0.0061; CI, Confidence Interval.
Table 3. Distribution of HBsAg according to parity.
Parity No.
positive (%) (95% CI)
Nulliparae0 0 0 (0) -
Primiparae1 65 6 (9.2) (1.8354 - 1.9800)
Multiparae2 - 5 95 13 (13.7) (1.7928 - 1.9335)
multiparae > 5 36 14 (38.9) (1.4438 - 1.7784)
Total 1 - 12 196 33 (16.8)
Table 4. Prevalence of HBsAg according to duration of
Duration of
pregnancy (months)No. testedNo.
positive (%) (95% CI)
3 - 5 29 3 (10.3) (1.7787 - 2.0144)
6 - 8 131 22 (16.8) (1.7672 - 1.8969)
> 8 36 8 (22.2) (1.6351 - 1.9204)
Total 196 33 (16.8)
X2 = 1.619, df = 2, p = 0.445.
Table 5. Prevalence of HBsAg according to social status.
Social statusNo. testedNo. positive (%) (95% CI)
I 8 0 (0.0) (2.0000 - 2.0000)
II 22 5 (22.7) (1.5825 - 1.9629)
III 58 10 (17.2) (1.7274 - 1.9278)
IV 48 7 (14.6) (1.7506 - 1.9577)
V 60 11 (18.3) (1.7159 - 1.9175)
Total 196 33 (16.8)
in the carrier rates of the HBsAg between women who
belonged to the higher classes compared to those in the
lower social classes and vice versa (X2 = 2.442, df = 4, p =
0.655, X2 for linear trend = 0.191, df = 1, p = 0.662).
Copyright © 2013 SciRes. OPEN ACCESS
D. N. Bukbuk et al. / World Journal of Cardiovascular Diseases 3 (2013) 512-518
3.6. Risk Factors and Their Possible Association
with HBsAg Transmission
The factors that are commonly associated with the high-
est risk of transmission of the HBV are as shown in Ta-
ble 6. About 75% (147 out of 196) of the women are
mostly from monogamous marriages compared to only
25% (49 out of 196) who are polygamous. Few of the
women had a positive history of blood transfusion 4.6%
(9 out of 196), and a history of sexually transmitted in-
fections (STIs) in their husbands, 5.6% (11 out of 196).
Most of the women however, gave a positive history of
tribal makes/tattooing, 62.8% (123 out of 196), use of
sharps, 70.4% (138 out of 196), and self history of jaun-
dice and in their husbands. 20.9% (41 out of 196), 18.4%
(36 out of 196) respectively. Sharing of articles such as
toothbrushes, spoons, cups etc with their spouses showed
96.9% (190 out of 196).
The only risk factor that has been positively and signi-
ficantly associated with HBsAg carrier rate is those with
the history of blood transfusion (RR = 3.71, 95% Confi-
dence Interval C.I., 1.89 to 7.30, p = 0.008).
This study reports an overall high carrier rate of 16.8%
HBsAg among pregnant women attending antenatal cli-
nic at state specialist Hospital Maiduguri, Borno State.
The group studied fairly represents part of the entire po-
pulation and particularly those at an increased risk of
either acquiring or spreading the infection in our commu-
A prevalence rate of 16.8% HBsAg in pregnant wo-
men is high which shows that the virus (HBV) infection
is endemic in our community and in Nigeria generally as
in areas such as south-east Asia, sub-Saharan Africa, etc.
[4,22,28]. It can be suggested that within our community
the infection occurring early in childhood could be
through vertical transmission from mother to child [29].
Pregnant women are very important group to study
with regards to HBV infection or transmission. This is
because both perinatal and postnatal transmission of the
virus had been stated to be important in some societies in
south-east Asia [28]. This higher carrier rate of 16.8% for
the HBsAg among pregnant women agrees with the
study in the same area [17] who reported a rate of 11.6%
for HBsAg among pregnant women. Other reports in
Nigeria among pregnant women had observed a similarly
higher carrier rate. A higher value of 11.2% was reported
in Ibadan [23] and 13.8% among pregnant women at-
tending antenatal clinic in Lagos [30].
The high carrier rate among the pregnant women in
the present study could be due to the increased suscepti-
bility of women to infection during pregnancy. They
could hence serve as an important reservoir or potential
Table 6. Risk factors and their possible association with
HBsAg transmission.
Risk factor Tested
No. (%)
No. (%) RR (95% CI)
Type of marriage
Monogamous 147 (75.0) 24 (16.3) 0.89 (0.44 - 1.78)
Polygamous 49 (25.0) 9 (18.4)
History of blood
Yes 9 (4.6) 5 (55.6) 3.71 (1.89 - 7.30)
No 187 (95.4) 28 (15.0)
Tribal marks/Tattooing
Yes 123 (62.8) 21 (17.1) 1.04 (0.54 - 1.99)
No 73 (37.2) 12 (16.4)
Use of sharps
Yes 138 (70.4) 23 (16.7) 0.97 (0.49 - 1.90)
No 58 (29.6) 10 (17.2)
History of
Yes 41 (20.9) 6 (14.6) 0.84 (0.37 - 1.90)
No 155 (79.1) 27 (17.4)
History of jaundice/
hepatitis in husband
36 (18.4) 4 (11.1) 0.61 (0.23 - 1.64)
Yes 160 (81.6) 29 (18.1)
Sharing of articles 190 (96.9) 32 (16.8) 1.01 (0.16 - 6.22)
Yes 6 (3.1) 1 (16.7)
No. of sexual relationships
1 - 3 173 (88.3) 29 (16.8) 0.96 (0.37 - 2.49)
> 3 23 (11.7) 4 (17.4)
History of STIs
Yes 34 (17.3) 4 (11.8) 2.48 (1.11 - 5.53)
No 162 (82.7) 29 (17.9)
History of STIs in husband
Yes 11 (5.6) 2 (18.2) 0.91 (0.25 - 3.31)
No 185 (94.4) 31 (16.8)
RR, Relative risk, STIs, Sexually transmitted Infections; *Fisher exact, p =
pockets of infection to their newborns in utero or through
subsequent exposure to unsterilized and contaminated
materials used during deliveries and breast feeding.
Blood transfusion which was shown to be significantly
associated with a higher carrier rate of HBsAg, is an im-
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D. N. Bukbuk et al. / World Journal of Cardiovascular Diseases 3 (2013) 512-518 517
portant risk factor in Nigeria as pregnancy-related haem-
orrhage among others are known to increase the possibil-
ity of transmission of HBV (and other blood-borne pa-
thogens) through contaminated blood as reported by Uni-
ted Nations System in Nigeria (UNSN) [31].
From the result of this study which showed a higher car-
rier rate 16.8% of HBsAg among pregnant women, who
are said to be representatives of our society, it can be said
that Maiduguri is an endemic area for HBV infection.
Blood transfusion appears to be the only major risk fac-
tor of HBV infection among pregnant women in this
secondary health facility in Maiduguri, Borno state. This
might be a reflection of the situation in other health fa-
cilities across the country (Nigeria), possibly as a result
of increased demand for blood to treat certain pregnancy
related emergencies such as the different gynaecology
bleeding disorders.
There is therefore, the need to know the prevalence of
HBV markers such as HBsAg in pregnancy and the level
of perinatal transmission in the planning of preventive
measures. Hence routine screening for HBV infection in
pregnant women attending antenatal clinics is necessary,
followed by health enlightenment campaigns on the risk
and mode of transmission of the virus which can be
linked to the ongoing campaigns against HIV-AIDS. This
is coupled with the fact that an effective recombinant
vaccine against HBV has been developed, the govern-
ment and employers of labour should therefore supple-
ment the cost and make it available and affordable for
selective vaccination of those associated with high risk
exposures in our society.
We are greatly indebted to Mzee Muli of the Kenya Medical Research
Institute, Nairobi for providing us with the hepatitis test kit (HEP
CELL kit). We also thank the doctors, nurses and all staff of the Ante-
natal Clinic, Obstetrics & Gynaecology department of the State Spe-
cialist Hospital, Maiduguri for allowing us access to the patients.
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