Carrier rate of hepatitis B surface antigen (HBsAg) among urban pregnant women in a secondary health facility in Maiduguri, Northeastern Nigeria

doi:10.4236/wjcd.2013.38081

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World Journal of Cardiovascular Diseases, 2013, 3, 512-518 WJCD

http://dx.doi.org/10.4236/wjcd.2013.38081 Published Online November 2013 (http://www.scirp.org/journal/wjcd/)

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

Email: [email protected], [email protected]

Received 22 August 2013; revised 29 September 2013; accepted 12 October 2013

License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

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

newborns.

Keywords: Carrier Rate; HBsAg; Urban; Pregnant

Women; SSH; Borno State; Nigeria

1. INTRODUCTION

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

OPEN ACCESS

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

possible.

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-

nity.

2. MATERIALS AND METHODS

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

D. N. Bukbuk et al. / World Journal of Cardiovascular Diseases 3 (2013) 512-518

514

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

(www.cdc.gov/epiinfo /) and World Health Organization,

Geneva, Switzerland (www.who.int)] and GraphPad

Prism version 5.00 for Windows (GraphPad Software,

San Diego California USA, www.graphpad.com). 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. RESULTS

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-

tively.

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%

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.

pregnancy

No.

tested

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)

Grand

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

pregnancy.

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).

D. N. Bukbuk et al. / World Journal of Cardiovascular Diseases 3 (2013) 512-518

516

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).

4. DISCUSSION

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-

nity.

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. (%)

Positive

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

transfusion*

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

jaundice/hepatitis

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 =

0.008.

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-

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].

5. CONCLUSIONS

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.

6. ACKNOWLEDGEMENTS

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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