ORIGINAL

Niger J Paed 2013; 40 (3): 248 –253

Sadoh AE

Sadoh WE

Serological markers of hepatitis B

infection in infants presenting for

their first immunization

DOI:http://dx.doi.org/10.4314/njp.v40i3,9

Accepted: 29th December 2012

Abstract Introduction: Hepatitis

B vaccine can prevent perinatal

transmission if administered

within 24 hours of birth. Nigerian

infants are known to present late

for their first immunizations and

may acquire the virus either verti-

cally or horizontally before re-

ceipt of the first dose of hepatitis

B immunization. This study

evaluated serological markers for

hepatitis B virus infection in Ni-

gerian infants prior to receipt of

the first dose of hepatitis B immu-

nization.

Method: Blood samples obtained

prior to the receipt of hepatitis B

vaccine from infants presenting

for their first immunization were

analysed for HBsAg, antiHBc and

antiHBe..

Results: The mean age at presen-

tation of the 153 infants studied

was 14.3±15.6 days while only

two infants presented on the first

day of life. The prevalences of

HBsAg and antiHBc were 16.3%

and 15.7% respectively. Of those

positive for either HBsAg or an-

tiHBc 20(47.6%) were positive

for antiHBe. The presence of

HBsAg was not significantly asso-

ciated with sex, age, circumcision,

ear piercing and blood transfusion.

Conclusion: Majority of the in-

fants did not receive hepatitis B

vaccine within 24 hours of birth.

Institutional delivery should be

encouraged while emphasizing to

mothers and health care workers

that hepatitis B vaccination must

commence within 24 hours of

birth.

(

)

Sadoh AE

Institute of Child Health

University of Benin

Benin City, Nigeria

Email: ayebosadoh@yahoo.com

Tel: +234 803 3435 312

Sadoh WE

Department of Child Health

University of Benin Teaching Hospital

Benin City, Nigeria

Key words: Serological markers,

hepatitis B. first infant immuniza-

tion

Introduction

and horizontal transmission. Most countries in the Afri-

can sub-region utilize the Expanded Programme on Im-

munization (EPI) schedule which recommends Hepatitis

B vaccine to be given at birth.

Universal infant immunization has been recommended

since 1992 by the World Health Organization as the

1

strategy to prevent hepatitis B infection. Th₂ere are dif-

ferent schedules for infant immunization. Schedules

which include a birth dose are able to prevent perinatal

Endemicity of hepatitis B is defined based on the pro-

portion of the population who are HBsAg seropositive.

Areas with ≥ 8% of the population being HBsAg posi-

tive are highly endemic while areas with 2-7% HBsAg

seropisitivity are of intermediate endemicity; <2%

2

transmission. In such schedules, Hepatitis B vaccine

should be administered within 24 hours of birth. When

Hepatitis B vaccine is given alone at birth, it is more₂

than 90% effective in preventing vertical transmission

whereas the concomitant administration of hepatit₃is B

immune globulin improves the protection of infants.

In Africa horizontal transmission through close contact

within households, medical procedures and traditional

scarifications is thought to be the main route of trans-

2

HBsAg seropositivity represents low endemicity. The

prevalence of hepatitis B surface antigen ranges betwe₈e_-₁n₀

9.1 and 12.6% in the general Nigerian population,

indicating that Nigeria is highly endemic for hepatitis B

virus infection. Nigeria operates the EPI schedule of

11

commencing hepatitis B vaccination at birth; two fur-

ther doses at 6 weeks and 14 weeks completes the

schedule. The efficacy of hepatitis B vaccine in prevent-

ing vertical transmission depends on its being given in a

timely fashion, that is the birth dose being administered

4

mission. Even though the major route of transmission is

horizontal some children still acquire the infection verti-

cally. In Senegal 7% of newborns were shown to be

5

HBsAg seropositive at birth. Also in Gha₆na 1.3% of

2

newborns were found to be HBsAg positive. In a study

from the study locale 0.96% of newborns were found to

within 24 hours of birth. Several reports from Nigeria

have₁₂s_,₁h₃own that many infants commence immunization

7

be HBsAg seropositive. Thus commencing immuniza-

late.

In one community based study the mean age at

tion at birth is the better option preventing both vertical

commencement of immunization was 32.11 ±49.17 days

2

49

while up to 31.7% of the studied c₂hildren commenced

This gave a sample size of 148.03 which was approxi-

mated to 150. Consecutive infants who were brought for

their first immunization were recruited. Any child

whose birth weight was less than 2kg was excluded

since babies who have not attained a weight of 2kg are

not offered hepatitis B vaccine.

Information on bio data such as date of birth, sex, mater-

nal and paternal educational level and occupation were

obtained using a proforma. Information on place of

birth, receipt of antenatal care, birth weight, any illness

since birth and blood transfusion was also sought.

1

immunization after 28days of life. Also only 35% of

1

4

deliveries in Nigeria take place in health facilities,

therefore the birth dose of hepatitis B may not be given

within 24 to 48 hours except the baby is immediately

taken to a health facility. Previous studies have however

noted that even babies born within health facilities do

`12

not commence immunization within 24 hours of birth.

These delays in commencement of immunization may

place the infant at risk of acquiring the hepatitis B infec-

tion before the commencement of immunization. A pre-

vious study had shown that immunization of those al-

ready₅infected does not reduce the risk of chronic infec-

Two mls of blood was obtained through venepuncture

under sterile conditions prior to the administration of

any vaccine. The blood was spun and serum separated

and then stored at -20°C until the time of testing.

HbsAg and anti Hbc were assayed for in the serum using

DRG Hepatitis B surface antigen Enzyme linked immu-

nosorbent assay kit (EIA-3892) and DRG Anti-Heoatitis

B core antigen Enzyme linked immunosorbent assay kit

(EIA-3894) reapectively both manufactured by DRG

international inc. USA.

1

tion. Thus administration of hepatitis B vaccine to a

child who is already infected may not prevent chronic

HBsAg carriage and would constitute a waste of re-

sources.

The success of an immunization programme in prevent-

ing perinatal transmission may be assessed by the pro-

portion of infants who receive the first dose of hepatitis

2

B vaccine within 48 hours of birth. The World Health

Organization suggests that timely delivery of the birth

dose should be a performance indicator for all immuni-

zation programmes. Delays in commencement of hepa-

Any sample that was positive for either HBsAg or an-

tiHBc was tested for the presence of antiHBe using

DRG Anti-Hepaitis B e Antigen Enzyme linked immu-

nosorbent kit by DRG international inc- USA.. The tests

were carried out by a Laboratory scientist according to

the manufacturer’s specifications

3

titis B immunization may compromise the effectiveness

of the hepatitis B control programme as many cases of

delayed commencement of immunization who become

infected will be erroneously classified as vaccine fail-

ures. The administration of hepatitis B vaccine to infants

who are already infected is also a waste of resources.

This study therefore set out to ascertain prospectively

the age at commencement of hepatitis B immunization

and to determine the HBsAg status prior to the com-

mencement of immunization.

Ethical Issues

Ethical clearance for the study was obtained from the

UBTH ethical review committee. Verbal consent was

obtained from parents of subjects after the objectives

and procedure of the study was explained to them.

Methodology

Results

Sociodemographic characteristics of the study popula-

tion

The study was carried out at the Immunization clinic of

the Institute of Child Health, University of Benin, Benin

City between December 2010 and June 2011. The Insti-

tute of Child Health Immunization clinic offers services

to the inhabitants of Benin City, the capital of Edo state,

Nigeria. The services offered include immunizations,

growth monitoring, nutrition education and general

health education. About 1000 babies receive their immu-

nizations in this facility yearly.

There were 153 infants, 72(47.1%) girls and 81(52.9%)

boys. The median age of the babies was 14.3±15.6 days

with a range of 1 to 90 days. Of the 153 babies, 66

(43.1%) presented in the first week of life.(Table1).

Only one child presented within a day of life while 6

(3.9%) presented within 2 days of life and 13(8.5%)

presented within the first 3 days of life. Sixteen (10.5%)

1

6

th

The sample size was determined using the formula:

babies presented after the 4 week of life.

2

n = z p₂q

The age range of the mothers was 18-42years with a

mean of 29.6±5.6years. The mean parity of the mothers

was 2.7±1.7 with a range of 1 to 10. Most 141 (92.2%)

of the mothers had antenatal care but only 124(81.1%)

were delivered in orthodox health care settings. Of those

who were delivered in orthodox health care settings, 51

(41.1%) were in government owned facilities while 73

(58.9%) were in private facilities. Of the 29 who were

delivered outside orthodox health care setting 14 were

delivered at home, 8 in churches, 4 with traditional birth

attendants and one each with a midwife and nurse. Of

the 153 mothers only 9(5.9%) were screened for hepati-

d

where

n = the desired sample size

z = the standard normal deviate set at 1.96 which corre-

sponds to 95% confidence interval

p = the proportion in the target population estimated to

be positive for the hepatitis B surface antigen (estimated

to be 10.8% using₁t₇he prevalence found in an earlier

study in Benin City)

q = 1.0 – p

d = degree of accuracy desired which is 0.05

2

50

tis B antenatally while 91(59.5%) were not screened.

The remaining 53(34.6%) did not know if they had been

screened as they had been asked to do tests whose

names nor results were unknown to them. All 9 mothers

who were screened tested negative and did not require

any intervention. The mean number of persons in the

household of the infants was 5.2±1.8 with a range of

markers were present in 5(3.2%) babies. Some 14

(9.2%) babies were positive for antiHBc and antiHBe.

HBsAg alone was present in 18(11.8%) babies while

antiHBc alone was present in 17(11.4%).

Of the 66 babies who presented in the first week of life

11(16.7%) were positive for HBsAg (Table 3) whereas 7

(16.7%) of 42, 4(17.4%) of 23, none of 6 and3(18.8%)

of 16 babies presenting in the second, third, fourth and

beyond the fourth weeks of life respectively were posi-

tive for HBsAg. Age was not significantly associated

with being positive for HBsAg. AntiHBc was positive in

2

-11

Table 1: Sociodemographic characteristics of the study

population

Characteristic

n

%

1

6

0(15.2%) of 66,7(16.7%) of 42,4(17.4%) of 23, none of

and 3(18.8%) of 16 babies presenting in the first, sec-

Gender

Male

Female

81

72

52.9

47.1

ond, third, fourth and beyond the fourth weeks of life

respectively.

Age at presentation(in days)

1

8

-7

-14

66

42

23

6

48.1

27.5

15.0

3.9

Determinants of presence of serological markers

1

2

5-21

2-28

Of the 81 males 11(13.6%) were HBsAg positive and

this was not significantly different from 14(19.4%) of 72

females p=0.38. The number of persons in the household

of the infant, ear piercing and circumcision were not

significantly associated with the presence of HBsAg in

the infant. (Table 4) All the ear piercings were done

≥

Place of Delivery

Within Health facility

Outside Health facility

Number of persons in household

29

19

10.5

124

29

81.1

18.9

≤4

60

91

39.7

60.3

≥

Table 2: Relationship between age at presentation for immunization and presence of serological markers of hepatitis

B infection

Age at presentation

In days

Serological Markers

Positive

a

b

c

HBsAg

AntiHBc

AntiHBe

Positive Negative

Negative

n

%

n

%

n

%

n

%

n

%

n

%

1

8

-7

-14

11 16.7 55 83.8

7 16.6 35 83.3

4 17.4 19 82.6

10 15.2

7 16.6

4 17.4

56 84.8

35 83.4

19 82.6

6 100.0

13 81.2

9

16.1 57 86.4

14.3 36 85.7

17.4 19 82.6

0.0 6 100.0

25.0 12 75.0

6

4

0

4

1

2

5-21

2-28

0

0.0 6 100.0

0

3

0.0

18.8

≥

29

3 18.8 13 81,2

a

2

b

2

c 2

χ 0.029 p=0.99

χ 0.045 p=0.98

χ 0.39 p=0.83

The age groups 15-21,22-28 and ≥29 were merged for the Chi square analysis

Table 3: Serological profiles of studied children

using sterile pin ear rings. Of the 25 infants who had

been circumcised, 12(48%) were done in health facili-

ties. Of the 13(52%) that were done at home 5(38.5%)

were carried out by health care personnel. The place of

delivery was also not associated with the presence of

serological markers. Jaundice was not significantly asso-

ciated with the presence of HBsAg. (Table 4).

Serological Profile

n

%

HBsAg only

AntiHBc only

18

17

7

11

14

5

11.8

11.1

4.6

7.2

9.2

HBsAg +AntiHBc

HBsAg +AntiHBe

AntiHBc+AntiHBe

All three markers

Any marker

3.3

29.4

42

Age at presentation for immunization and presence of

serological markers for hepatitis B

Serological markers (HBsAg and antiHBc) were present

in 42 (29.4%) babies. HBsAg was present in 25(16.3%)

babies while antiHBc was present in 24(15.7%) babies.

Of the 42 babies with HBsAg and antiHBc 20(47.6%)

had antiHBe. There were 7(4.6%) babies who were posi-

tive for both HBsAg and antiHBc while 11(7.2%) were

positive for HBsAg and antiHBe.(Table 2) All three

2

51

studied infants receiving the hepatitis B vaccine within

8 hours of birth it is possible that many of these infants

Table 4: Relationship between presence of HBsAg and some

parameters

4

Parameter

test

HBsAg

Fisher’s Exact

pvalue

would remain seropositive. Follow up of these sero-

positve infants is imperative to determine those who

become chronic carriers so that appropriate follow up

and care can be given to them.

Positive

N

Negative

n

%

Gender

Male

Female

11

14

13.6 20

19.4 58

86.4

80.6

0.38

1.00

0.75

0.78

0.79

0.83

0.47

One of the strategies for the prevention of perinatal

transmission of hepatitis B is screening of pregnant

women for hepatitis B surface antigen and then offering

the hepatitis B vaccine and immune globulin to infants

Number of persons in HH

≤

≥

4

5

10 16.7

15 16.5

50

76

83.3

83.5

Ear Piercing

Yes

No

Circumcision

Yes

No

Place of Delivery

Within health facility

Outside health facility

Jaundice

Yes

No

Parity

1

2

4

20.0 16

80.0

of positive mothers within 24 hours of delivery. In this

21

15.8 112 84.2

study almost 60% of the mothers were not screened for

hepatitis B while only 5.9% were screened. With such

low screening rates this strategy is unlikely to be effec-

tive in preventing perinatal transmission. Educating

health care workers on the importance of screening for

HBsAg in pregnant women is a strategy that may im-

prove the uptake of this intervention especially in popu-

lations where coverage of antenatal care is high as in the

mothers in this study.

5

18.5 22 81.5

20 15.9 106 84.1

21 17.1 102 82.9

4

13.8 25

86.2

7

18

18.0 32

15.9 95

82.0

84.1

9

16

20.5 35

15.1 90

79.5

84.9

22

AntiHBc has been known to cross the placenta, and it

≥2

has been shown that up to 80% of Nigerian adults have

one or more markers of hepatitis B exposure by the age

8

of 40 years. Thus the presence of antiHBc in 15.7% of

the studied infants may be due to transfer of maternal

antibodies. In one study it was found that all infants

born to mothers who we₂re antiHBc positive were also

Discussion

Almost a third of the studied infants had one or more

hepatitis B serological markers. This is a reflection of

maternal exposure to the virus indicating the high level

of hepatitis B endemicity in the study locale. The pres-

ence of HBsAg in 16.3% of the newborns is much

higher than the 0.96% documented in a study on paired

2

positive for this marker. The marker was however no

longer positive by the age of two years in infants who

were free of the infection. But those who became

HBsAg positive w₂ere persistently positive for the an-

2

tiHBc from birth. The test in this study did not distin-

guish between IgM and IgG anti HBc. IgM antiHBc will

suggest infection of the baby. Some studies have how-

ever suggested that in hepatiti₅s B infection in infancy

IgM anti HBc is not elaborated.

maternal infant samples in the study locale published in

7

2

001. In that study maternal HBsAg seroprevalence

was 2.19%. In a more recent study( carried out in 2010)

from the study locale a seroprevalence of 12.8% was

found in pregnant women indicating a higher prevalence

than the earlier study. A higher prevalence as docu-

mented by the latter study is likely to be associated with

higher transmission as observed in the current study

which was carried out at about the same period.

1

8

In another study on the significance of antiHBc it was

noted that majority of infants who were IgG₃ antiHBc

2

positive became negative after six months. In that

same study however significantly more infants (24.6%)

who were IgG antiHBc positive became HBsAg positive

comp₃ared to 10.9% of those who were antiHBc nega-

Compared to the 7% documented in Senegalese infants

at birth the finding in this study is also higher. The age

range in this study is wider than for the birth cohort in

both the Senegalese study and the study on paired sam-

ples from the study locale. This may explain the higher

HBsAg seroprevalence observed in this study. However,

2

5

tive. Thus the presence of antiHBc may be a risk factor

in the infants in the current study.

The presence of antiHBe may also be an indication of

transfer of maternal anti₂b₂odies as it has been shown to

also cross the placenta. In a study which evaluated

children serially from birth till 24 months antiHBe was

found in all infants born to mo₂thers who were HBeAg

5

0% of the Senegalese infants who were HBsAg posi-

tive at birth had become negative at age 6-7months. In

that study it is not stated if Hepatitis B vaccine was

given to the babies postnatally. In other studies in which

hepatitis B vaccine wa₁s₉_,₂g₀iven most of the babies were

2

negative but antiHBc positive. AntiHBe was not found

in any of the infants born to HBeAg positive mothers.

The finding in this study may thus suggest a high level

of antiHBe and low level of HBeAg in the mothers. It

has been suggested that HBeAg which indicates high

infectivity is not as common in Africa compared to

South East Asia; hence the relatively smaller role of

perina₄tal transmission in Africa compared to South East

Asia.

negative subsequently.

There were however, some

posit₁iv₉_,e₂₀cases which were considered vaccine fail-

ures. In these studies hepatitis B vaccine was admin-

istered within 24 hours of birth and in some Hepatitis B

immu₁n₉_-o₂g₁lobulin was also given within 12-24 hours of

birth.

In this study none of the HBsAg positive in-

fants had received the hepatitis B vaccine within 24

hours of delivery. With less than five percent of the

We note the increasing proportion of infants with

2

52

1

2

serological markers with age although this was not sta-

tistically significant it may suggest increasing exposure

to the virus postnatally emphasizing the need for infants

to receive the hepatitis B vaccine on time (that is at

birth).

Sex was not significantly associated with being positive

for serological markers. Although i₂n₄trafamilial spread of

hepatitis B has been documented, in this study there

was no significant association between being seroposi-

tive and the number of persons in the infants’ household.

This may suggest that horizontal exposure may be less

significant in early infancy

health facilities. The authors suggested that perhaps

women irrespective of where they were delivered can be

1

2

motivated to bring their children for immunization.

This is relevant since administering a birth dose may

pose challenges for babies born outside of health facili-

ties. Thus emphasizing to mothers that immunization

should be commenced within 24 hours may be all that is

required.

Other strategies such as the use of single dose vials dur-

ing home visits by health care workers may be explored

while making every attempt to increase institutional

deliveries. Single dose vials (such a_Ts_M pre-filled single-

use injection devices like UNIJECT ) used outside of

the cold chain have been reported to simplify logistics,

minimize vaccine wastage and facilitate the speed and

Invasive procedures have the potential for transmission

of hepatitis B if unsterile instruments are used. In this

study circumcision and ear piercing were not associated

with being seropositive for markers of hepatitis₂₅B_-₂₇infec-

2

tion. This is in keeping with previous findings.

This

efficiency of immunization during home visits. A fur-

is probably due to the use of sterile earrings for ear

piercing both for ear piercing that was done in hospitals

and those that were done at home. Almost half (48%) of

the circumcisions were done in health care facility. For

those done at home 38.5%% were done by health care

workers who are also unlikely to use contaminated in-

struments.

ther challenge to achieving timely administration of the

birth dose of hepatitis B vaccine is that some health fa-

cilities do not vaccinate every day. Single dose vials

may also find utility in such settings as it will obviate

the need to open multi dose vials for the single baby

who presents for the birth dose of the hepatitis B vac-

cine. Also identifying women who are carriers through

prenatal screening and then offering the vaccine and

HBIG within 24hours of delivery may be a useful strat-

egy. This may be a worthwhile strategy for the popula-

tion of women studied but may not be effective at na-

tional leve₁l₄ since antenatal care attendance in Nigeria is

only 58%.

The place of delivery was also not associated with sero-

positivity. A history of neonatal jaundice or the presence

of jaundice on examination were not significantly asso-

ciated with serop₅ositivity. This is also in keeping with

previous studies.

The presence of serological markers in up to a third of

infants studied may be a reflection of maternal exposure

to hepatitis B infection which suggests a high level of

prior maternal exposure to the virus. This is in keeping

with the level of endemicity of hepatitis B in Nigeria.

However the presence of HBsAg may be indicative of

infection. Early immunization within 24 hours of birth is

recommended as this can prevent the development of

chronic carrier state. Since all the children who were

HBsAg positive did not receive the vaccine within 24

hours of birth follow up with testing will be mandatory

to determine those who have become infected.

Conclusion

This study has shown that a high proportion of infants

have serological markers for Hepatitis B infection prior

to commencing immunization. Majority of these infants

did not present within the first 48 hours of life for im-

munization a practice that may compromise the effec-

tiveness of the hepatitis B prevention programme. Fol-

low up of these infants is required to determine those

who are persistently infected and also to determine the

effectiveness of hepatitis B vaccine administered at dif-

ferent ages in preventing perinatal transmission.

Using the proportion of infants receiving the birth dose

of hepatitis B within twenty four hours as performance

indicator shows that the immunization programme in the

study locale is performing sub optimally with less than

five percent of the studied infants receiving hepatitis B

in the first 48 hours. This immunization programme may

thus not be effective in preventing perinatal transmission

of hepatitis B.

Author contribution

AES conceptualized the work, was involved in sample

collection, data analysis and interpretation, wrote

the initial draft and approved the final draft for

submission

WES contributed to the concept, was involved in data

analysis and interpretation, reviewed the initial draft

and approved the final draft for submission

Conflict of interest: None declared

Funding: This work was supported by a grant given by

Dr Chinyere Ofure Aneziokoro Research foundation on

infectious diseases and breast cancer. The foundation

had no role in the design of the study, collection, analy-

sis and interpretation of data, writing of manuscript and

decision to submit the manuscript

The need for timely administration of the hepatitis B

vaccine within 24 hours of birth should be emphasized

to both parents and health care workers so that babies

born within health care facilities will be offered hepatitis

B vaccine within 24 hours of birth. In a previous study it

was found that among children who completed the im-

munization schedule there was no significant difference

in the age at commencement of immunization between

babies born in health facilities and those born outside

2

53

Acknowledgments

sions to allow for data and sample collection. We thank

Drs J Uduebor, P Ekpebe and O Iguodala for their help

in sample collection.

We acknowledge with thanks the nurses of the Institute

of Child Health for organizing the immunization ses-

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